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NME1 (NME/NM23 nucleoside diphosphate kinase 1)

Written2013-02Marie-Lise Lacombe, Mathieu Boissan
INSERM UMRS_938, UPMC Univ Paris 06, 27 rue Chaligny, 75012 Paris, France

(Note : for Links provided by Atlas : click)

Identity

Alias_namesnon-metastatic cells 1
Alias_symbol (synonym)NM23
NM23-H1
NDPKA
Other aliasAWD
GAAD
NB
NBS
NDKA
NDPK-A
HGNC (Hugo) NME1
LocusID (NCBI) 4830
Atlas_Id 445
Location 17q21.33  [Link to chromosome band 17q21]
Location_base_pair Starts at 51153559 and ends at 51162089 bp from pter ( according to hg19-Feb_2009)  [Mapping NME1.png]
Fusion genes
(updated 2017)		Data from Atlas, Mitelman, Cosmic Fusion, Fusion Cancer, TCGA fusion databases with official HUGO symbols (see references in chromosomal bands)
NME1 (17q21.33) / LRP5 (11q13.2)NME1 (17q21.33) / NME2 (17q21.33)NME1 (17q21.33) / THRA (17q21.1)

DNA/RNA

Note The NME1 gene was identified in 1988 as the first metastasis suppressor, due to its reduced expression in metastatic murine melanoma cell line (Steeg et al., 1988; reviewed in: Lee et al., 2009). The human gene, also named NM23-H1, was shown to be homologous to the Drosophila AWD gene, involved in larvae development, and to exhibit an expression inversely correlated to the metastatic spread in primary breast tumors (Rosengard et al., 1989). It is the first described member of a family of ten genes in human (Desvignes et al., 2009; reviewed in: Boissan et al., 2009).
 
  The NME1 gene viewed at three different levels of detail (highlighted between two red vertical boundary lines). 1) Overview within chromosome 17. 2) Partial regional view within chromosome 17q21.3. 3) Detailed view within chromosome 17q21.33 showing two of the transcription variants of NME1, which include NME1 (NM_000269.2) and NME1B (NM_198175.1). Abbreviations: M and K: mega- and kilobase pairs from pter; Kbp: kilobase pairs; Chr: chromosome; CDS: coding sequence.
Description The gene is composed of 6 exons of which five are coding exons. Exon 2 skipping results in a shorter transcript.
Transcription Two transcripts have been reported for this gene (Rosengard et al., 1989; Ni et al., 2003). A read-through variant, resulting of the co-transcription of NME1 and the neighboring NME2, generates a transcript, which encodes a fusion protein sharing identity with each individual gene products (Valentijn et al., 2006).
Pseudogene A pseudogene of NME1 (NME1P1) is located on chromosome 13q12.11 (NC_000013.10, Gene ID: 100874501).

Protein

Note The NME1 gene encodes a nucleoside diphosphate kinase (NDPK) (Wallet et al., 1990). The two most abundantly expressed and the most studied genes are NM23-H1 and NM23-H2 (NME1 and NME2). They encode, respectively the A and B subunits of NDPK, 88% identical in their amino acid sequences (Gilles et al., 1991).
NME1 was demonstrated to be a metastasis suppressor 1) by its enforced expression in various metastatic cell lines which decreased motility and invasion (Lee et al., 2009), 2) in double transgenic mice invalidated for Nme1 and prone to develop hepatocarcinoma in which lack of Nme1 increased incidence of pulmonary metastases (Boissan et al., 2005) and 3) by its invalidation (SiRNA) in non-aggressive hepatoma and colon cancer cell lines which induced a "metastatic phenotype" (Boissan et al., 2010). The role of the homologous gene, NME2, in cancer progression is less documented (reviewed in: Thakur et al., 2011).
The mechanisms involved in the metastatic potential control are largely unknown. They could involve several known NM23 enzymatic activities (nucleoside diphosphate kinase, histidine kinase, and 3'-5' exonuclease), protein-protein interactions and downstream gene regulation properties (for reviews: Marino et al., 2011; Marino et al., 2012). A Granzyme A activated DNAse (GAAD) activity involved in caspase-independent apoptosis was also reported for this gene (reviewed in: Lieberman, 2010).
Description The main transcript encodes a protein of 152 amino acids with a Mr of 17 kDa (Rosengard et al., 1989). The longer transcript encodes a protein of 177 amino acids (Ni et al., 2003).
Expression Ubiquitous.
Localisation Mostly cytoplasmic but also reported in nucleus (Bosnar et al., 2009).
Function Nucleoside diphosphate kinase activity responsible for the synthesis of most cellular (oxy- and deoxy-) nucleoside triphosphates (Parks and Agarwal, 1973). Other functions have been proposed, histidine protein kinase activity, 3'-5' exonuclease activity (for review: Marino et al., 2011) and Granzyme A activated DNAse (GAAD) activity (Lieberman, 2010).
Homology The human NME1 gene is conserved in amniota with a high percentage of identity in the pairwise alignment of protein vs. chimpanzee (99%), rat (95%), mouse (94%), dog (93%), cow (93%), opossum (89%) and chicken (84%). The paralogs of human NME1 include NME2, NME3, NME4, NME5, NME6, NME7, NME8 (TXNDC3), NME9 (TXL2) and RP2 (NME10) (Desvignes et al., 2009; Desvignes et al., 2010). These genes encode one (NME1 to NME6 and NME9) or several (NME7 and NME8) conserved NDPK domains, either full length or truncated. The NDPK domain occurs individually or associated with extra-domains (NME5, NME7, NME8, NME9 and RP2) (Boissan et al., 2009).

Mutations

Note A S120G mutation was reported in aggressive neuroblastoma (Chang et al., 1994).

Implicated in

Note
  
Entity Cancers
Note NME1 plays a crucial role in cancer metastasis. Numerous clinical studies reported an inverse association between NME1 expression and the metastatic potential for human solid tumors of epithelial origin such as breast, liver, colorectal, ovarian and lung carcinomas and for melanoma (for review: Marino et al., 2012). A dual expression was reported with an increased expression of NME1 and often NME2 in the primary tumor as compared to the adjacent non-tumoral tissue (Lacombe et al., 1991; Flørenes et al., 1992; Martinez et al., 1995) and with a decreased expression of NME1 in the primary tumor correlated with metastatic spread. If, for liver, breast and lung carcinomas and for melanoma, the vast majority of studies reported an inverse correlation with metastasis and/or poor overall survival, this is less marked in colorectal, gastric and ovarian carcinomas for which more discrepant results are found. The conflicting data reported in the literature, might be due to the presence of the two closely related isoforms (NME1 and NME2) which are most often not discriminated by antibodies and probes, the heterogeneous expression in the primary tumors and the criteria to evaluate and grade NME1 expression in the clinical samples.
Remarkably, enforced NME1 expression induced by transfection in epithelial cancer derived cell lines and melanoma reverses their motility and invasive potential. This was observed with cell lines derived from melanoma (Leone et al., 1991) and from breast (Leone et al., 1993a), colon (Suzuki et al., 2004), lung (Nie et al., 2008), liver (She et al., 2010), ovarian (Li et al., 2006), prostate (Andolfo et al., 2011) and oral (Wang YF et al., 2008) carcinomas.
In other types of cancers such as neuroblastoma (Leone et al., 1993b; Garcia et al., 2012), hematopoietic malignancies (Yokoyama et al., 1998) and osteosarcoma (Liao et al., 2000), a high tumoral expression was noted which was most often correlated with poor clinical outcome.
  
  
Entity Breast cancer
Note Most clinical studies reported an inverse correlation between NME1 expression in breast primary tumors and the metastatic dissemination and/or shorter patient survival (Bevilacqua et al., 1989; Hennessy et al., 1991; Tokunaga et al., 1993; Toulas et al., 1996; Charpin et al., 1997; Caligo et al., 1997; Yamaguchi et al., 1998; Yoshida et al., 1998; Bertheau et al., 1998; Heimann et al., 2000; Mao et al., 2001; Terasaki-Fukuzawa et al., 2002; Niu et al., 2002; Ding and Wu, 2004; Bal et al., 2008; Dong et al., 2011). In some cases, an increased NME1 expression in tumoral cells as compared to normal tissue was observed (Lacombe et al., 1991; Goodall et al., 1994; Caligo et al., 1997). However, some studies showed that NME1 expression was of no prognostic relevance (Russo et al., 1996; Russell et al., 1997; Belev et al., 2002; Göhring et al., 2002) or even positively associated with a poor overall survival (Galani et al., 2002). Yoshida et al. (Yoshida et al., 1998) noted a low NME1 expression at the invasive front. Forced expression of NME1 by transfection in breast cancer cell lines reduced cell motility in vitro and metastasis formation in xenograft mouse models (Kantor et al., 1993; Leone et al., 1993a; Russell et al., 1998; Bhujwalla et al., 1999).
  
  
Entity Hepatobiliary carcinoma
Note Hepatobiliary carcinoma are among of the most aggressive cancers with a five year survival of less than 15%. Most studies reported an inverse association between NME1 expression and metastatic dissemination in hepatocellular carcinoma (reviews: Boissan and Lacombe, 2006 and An et al., 2010) and gallbladder carcinoma (Lee and Pirdas-Zivcic, 1994; Yang et al., 2008) but this is not always the case (Lin et al., 1998). Boissan et al. (2010) noted a low NME1 expression at the invasive front of hepatocellular carcinoma. Also, highly aggressive hepatocarcinoma cell lines exhibited a decrease level of NME1 as compared to less aggressive counterpart (Lin et al., 1995; Qin et al., 2007). NME1 overexpression, induced by transfection in the H7721 hepatocarcinoma cell line, inhibited cell migration and invasion (She et al., 2010). Conversely, NME1 silencing in non-aggressive hepatoma cell lines, HepG2 and PLC/PRF5 (Boissan et al., 2010), induced several parameters of a "metastatic phenotype" (loss of cell-cell contacts, increased motility and invasion).
  
  
Entity Lung carcinoma
Note In lung carcinoma, an inverse association with metastatic spread was reported by several studies (Huwer et al., 1994; Lai et al., 1996; Kawakubo et al., 1997; Ohta et al., 2001; Graham et al., 2002; Katakura et al., 2002; Goncharuk et al., 2004; Tang et al., 2005; Chen et al., 2005; Liu et al., 2011) but was not found by others (Higashiyama et al., 1992; Gazzeri et al., 1996; MacKinnon et al., 1997; Tomita et al., 1999; Wang et al., 2010). Some studies noted an increased level of NME1 in tumors as compared to non-tumoral tissue (Huwer et al., 1994; Gazzeri et al., 1996). Few studies reported a positive association between NME1 expression and metastatic dissemination to lymph nodes (Tomita et al., 2001). NME1 determination in bronchial lavages was proposed as a diagnostic tool for lung cancer (Huwer et al., 1997). In lung carcinoma cell lines, increased NME1 expression (Nie et al., 2008) and NME1 silencing (Zhao et al., 2013) decreased invasion and increased TGFβ-induced epithelial mesenchymal transition, respectively.
  
  
Entity Melanoma
Note An inverse correlation between NME1 mRNA levels and malignant potential of melanoma was reported in several studies (Flørenes et al., 1992; Xerri et al., 1994). This correlation was also found by immunohistochemical studies (Lee et al., 1996; Sarris et al., 2004; Ferrari et al., 2007), one including more than 100 patients (McDermott et al., 2000). However, other studies, including fewer cases, concluded to a lack of correlation (Easty et al., 1996; Saitoh et al., 1996; van den Oord et al., 1997).
In uveal melanoma, high NME1 expression was related to better survival rate (Bakalian et al., 2007) and, inversely, with prognostic factors of metastasis (Greco et al., 1997). Moreover, the high expression of NME1 mRNA and NME1 protein in derived-cell lines from human uveal melanomas is closely correlated with a reduced metastatic behavior in experimental animals (Ma et al., 1996). In accordance with its role as a metastasis suppressor, NME1 deficiency promotes metastasis in a UV radiation-induced mouse model of human melanoma (Jarrett et al., 2013). Enforced expression of NME1 in aggressive melanoma cell lines inhibited their metastatic potential (Leone et al., 1991; Zabrenetzky et al., 1994).
  
  
Entity Colorectal cancer
Note Concerning colorectal cancers (CRC), data about NME1 expression are highly conflicting. An enhanced NME1 expression was noted in CRC as compared to normal adjacent tissues at the mRNA (Ayhan et al., 1993; Myeroff and Markowitz, 1993; Yamaguchi et al., 1993; Zeng et al., 1994; Martinez et al., 1995; Okuno et al., 2001) as well as at the protein (Haut et al., 1991; Ayhan et al., 1993; Martinez et al., 1995; Sarris and Lee, 2001; Kapitanovic et al., 2004; Lin et al., 2011; Alvarez-Chaver et al., 2011) levels. Several studies reported 1) an inverse correlation with tumor stages (Cheah et al., 1998) and metastatic spread (Ayhan et al., 1993; Yamaguchi et al., 1993; Royds et al., 1994a; Martinez et al., 1995; Tannapfel et al., 1997; Dursun et al., 2002; Bertucci et al., 2004; Su and Li, 2004; Kapitanovic et al., 2004; Liu et al., 2005; Elagoz et al., 2006; Chen et al., 2007; Lin et al., 2011) or 2) no correlation (Haut et al., 1991; Myeroff and Markowitz, 1993; Ichikawa, 1994; Heide et al., 1994; Lindmark, 1996; Heys et al., 1998; Tabuchi et al., 1999; Lee et al., 2001; Dusonchet et al., 2003; Soliani et al., 2004; Qian et al., 2012) and 3) even a positive correlation with aggressiveness (Berney et al., 1999; Brenner et al., 2003). Boissan et al. (2010) observed a low NME1 expression at the invasive front of CRC.
In contrast to other cancers, for which NME1 LOH was rarely reported, several studies reported LOH for NME1 gene in CRC (Lamb et al., 1996; Lenehan et al., 1997; Sugai et al., 2000; Tsai et al., 2002; Kapitanovic et al., 2004). Allelic loss was correlated with advanced stage of the disease (Kapitanovic et al., 2004), shorter disease free and overall patient survival (Campo et al., 1994) and with formation of distant metastases (Wang et al., 1993; Cohn et al., 1997; Yang et al., 2008) or not correlated (Lamb et al., 1996). In addition, few studies reported no allellic loss of NME1 in CRC (Heide et al., 1994; Cawkwell et al., 1994).
Enhanced expression of NME1 by transfection in colon cancer cell lines reduced their migratory ability and their metastatic potential to the liver (Suzuki et al., 2004). Conversely, silencing NME1 expression by SiRNA in the colon cancer cell line, HCT8/S11, induced a "metastatic phenotype" (Boissan et al., 2010).
  
  
Entity Gastric carcinoma
Note In gastric carcinoma, many studies reported a negative correlation between NME1 expression in the primary tumors and advanced stage of the disease (Yang et al., 2008), metastatic dissemination (Kodera et al., 1994; Kim et al., 1995; Ura et al., 1996; Wang et al., 1999; Terada et al., 2002; Li et al., 2003; Chen et al., 2004; Liu et al., 2005; Guan-Zhen et al., 2007) and overall poor survival (Ura et al., 1996; Terada et al., 2002; Li et al., 2003). However, in some studies, NME1 expression was not correlated (Müller et al., 1998; Yoo et al., 1999; Lee et al., 2003; Mönig et al., 2007; Wang LB et al., 2008) or positively correlated (Wang et al., 1998; Nesi et al., 2001) with metastasis and poor survival.
  
  
Entity Ovarian carcinoma
Note In ovarian cancers, conflicting results were obtained. If several studies observed an inverse correlation with metastatic dissemination and/or poor patient survival (Mandai et al., 1994; Kapitanovic et al., 1995; Okubo et al., 1995; Scambia et al., 1996; Ferrandina et al., 1996; Qian et al., 1997; Galani et al., 2002; Hua et al., 2008), other studies did not observed any correlation (Baekelandt et al., 1999) and others reported a positive correlation with advanced stages, lymph node invasion or shorter overall survival (Leary et al., 1995; Harlozinska et al., 1996; Schneider et al., 2000; Arik and Kulacoglu, 2011). NME1 overexpression induced by transfection inhibited the metastatic potential of aggressive ovarian cancer cells (Li et al., 2006).
  
  
Entity Neuroblastoma
Note In neuroblastoma, all studies reported an enhanced expression of NME1 in tumors, correlated, when evaluated, with a poor prognosis (Hailat et al., 1991; Leone et al., 1993b; Chang et al., 1994; Hiyama et al., 2004; Garcia et al., 2012). In accordance with a metastatic promoting role, enhanced NME1 expression in the NB69 neuroblastoma cell line increased cell migration and metastatic potential (Almgren et al., 2004). A S120G mutation of Nme1 was found in aggressive cases (Chang et al., 1994).
  
  
Entity Leukemia
Note In several hematopoietic malignancies, NME1 was overexpressed and this high expression was positively correlated with poor prognosis. This was the case for acute myeloid leukemia (Yokoyama et al., 1996; Okabe-Kado et al., 1998; Wakimoto et al., 1998; Yokoyama et al., 1998; Cui et al., 2004), for Hodgkin and non Hodgkin lymphoma (Aryee et al., 1996; Lee et al., 2006), for acute lymphoid leukemia (Koomägi et al., 1998; Ning et al., 2009), for peripheral T-cell lymphoma (Niitsu et al., 2003a; Huang et al., 2006; Niitsu et al., 2011) and for diffuse large B-cell lymphoma (Niitsu et al., 2004). Interestingly, the poor prognosis can be evaluated by ELISA test of the NME1 level in patient sera for Hodgkin lymphoma (Niitsu et al., 2008) and non-Hodgkin lymphoma (Niitsu et al., 2001a; Niitsu et al., 2001b), for acute myeloid leukemia (Niitsu et al., 2000), for myelodysplastic syndrome (Ito et al., 2002), for diffuse large B-cell lymphoma (Niitsu et al., 2004; Niitsu et al., 2006) and for extranodal NK/T-cell lymphoma (Niitsu et al., 2003b). However, Bircan et al. (Bircan et al., 2008) reported that the increased NME1 expression was of no prognostic value in a series of Hodgkin and non Hodgkin lymphoma. Pointing to a role of extracellular NME1, recombinant NME1 protein was shown to promote the survival of acute myeloid leukemia blast cells (Okabe-Kado et al., 2009a; Lilly et al., 2011) but to decrease the survival of primary cultured normal peripheral blood mononuclear cells (Okabe-Kado et al., 2009b).
  
  
Entity Other cancers
Note NME1 has been evaluated as a prognostic marker in other types of cancer with various results, against pointing to a potential interest of NME1 as a metastasis suppressor specifically in carcinoma.
Controversial data have been obtained for prostate cancers (reviewed in: Myers and Grizzle, 1997). Several studies reported NME1 overexpression in tumor cells as compared to normal prostatic tissue (Myers et al., 1996; Jensen et al., 1996; Igawa et al., 1996; Luo et al., 2001; Prowatke et al., 2007). NME1 expression was shown to be inversely correlated with metastatic dissemination (Konishi et al., 1993; Stravodimos et al., 2000; Ding et al., 2006), of no prognostic interest (Borchers et al., 1996; Prowatke et al., 2007) or even related to advanced stage of the disease (Igawa et al., 1994) and poor prognosis (Andolfo et al., 2011). Interestingly, NME1 overexpression induced by transfection in PC3 prostate cancer cells, inhibited cell motility (Andolfo et al., 2011).
Few reports exist for pancreas cancers. Friess et al. (Friess et al., 2001) reported that early pancreatic cancer stages exhibited higher NME1 immunostaining than advanced tumor stages, while Nakamori et al. (Nakamori et al., 1993) observed that NME1 expression was positively associated with lymph node metastasis.
In thyroid cancers, several studies reported an increased expression in primary tumors (Zou et al., 1993; Ferenc et al., 2004; Al-Maghrabi and Asa, 2005) and a reduced expression in the metastatic lymph nodes (Arai et al., 1995; Shirahige et al., 1997), most often not correlated with patient survival (Luo et al., 1993; Farley et al., 1993; Zou et al., 1993; Royds et al., 1994b; Okubo et al., 1995; Al-Maghrabi and Asa, 2005; Tabriz et al., 2009). Zafon et al. (2001) observed a decreased expression in metastatic lymph nodes from papillary and follicular carcinomas, correlated with a decreased overall patient survival in follicular carcinoma. Bertheau et al. (1994) noted a nuclear NME1 labeling associated with a longer disease free survival.
For head and neck squamous cell carcinoma, several studies pointed to the absence of prognostic interest for NME1 (Takes et al., 2001; Tsuzuki et al., 2005; Sheikh et al., 2006; Mhawech-Fauceglia et al., 2007). However, some authors reported a lower NME1 level in lymph nodes as compared to the primary tumor (Takes et al., 2001; Wang YF et al., 2008) or an inverse correlation with lymph node invasion but not associated with better survival (Song et al., 2000). McDonald et al. (1996) have shown that a high NME1 expression in the primary tumor predicts a favorable outcome although the reverse was found by another study (Pavelic et al., 2000). Wang YF et al. (2008) have observed a low NME1 level in lymph node metastases of patient with oral squamous cell carcinoma and that induced NME1 overexpression in these cancer derived cell lines decreased their invasive potential.
In osteosarcoma, a positive immunoreactivity was detected in tumoral cells (Oda et al., 1995; Liao et al., 2000), but no correlation (Liao et al., 2000; Ozger et al., 2009) or a positive correlation (Oda et al., 2000) between NME1 expression and metastatic spread was observed.
In mesothelioma, high NME1 expression levels were observed by cDNA array (Røe et al., 2009) and by immunohistochemical analysis of tumors (Lumb and Suvarna, 2004) and of serous effusion samples (Zimmerman and Fogt, 2006) but were not related to prognosis.
Two studies reported that NME1 expression could possess a diagnostic interest by discriminating between benign and malignant pheochromocytoma (Ohta et al., 2005; Saffar et al., 2011) with a lower expression in malignant tumors. This observation should be confirmed by larger studies.
  

Bibliography

Expression of nm23 antimetastatic gene product in parathyroid hyperplasia, adenoma and carcinoma. An immunohistological assessment.
Al-Maghrabi JA, Asa SL.
Saudi Med J. 2005 May;26(5):728-31.
PMID 15951858
 
Nucleoside diphosphate kinase A/nm23-H1 promotes metastasis of NB69-derived human neuroblastoma.
Almgren MA, Henriksson KC, Fujimoto J, Chang CL.
Mol Cancer Res. 2004 Jul;2(7):387-94.
PMID 15280446
 
Selection of putative colorectal cancer markers by applying PCA on the soluble proteome of tumors: NDK A as a promising candidate.
Alvarez-Chaver P, Rodriguez-Pineiro AM, Rodriguez-Berrocal FJ, Garcia-Lorenzo A, Paez de la Cadena M, Martinez-Zorzano VS.
J Proteomics. 2011 May 16;74(6):874-86. doi: 10.1016/j.jprot.2011.02.031. Epub 2011 Mar 6.
PMID 21385632
 
Expressions of nucleoside diphosphate kinase (nm23) in tumor tissues are related with metastasis and length of survival of patients with hepatocellular carcinoma.
An R, Meng J, Shi Q, Dai XX, Chen JH, Lei YJ, Shan B, Gao C, Chu YL, Dong XP.
Biomed Environ Sci. 2010 Aug;23(4):267-72. doi: 10.1016/S0895-3988(10)60062-1.
PMID 20934113
 
Correlation of NM23-H1 cytoplasmic expression with metastatic stage in human prostate cancer tissue.
Andolfo I, De Martino D, Liguori L, Petrosino G, Troncone G, Tata N, Galasso A, Roma C, Chiancone F, Zarrilli S, Arrigoni G, Staibano S, Imbimbo C, Zollo M.
Naunyn Schmiedebergs Arch Pharmacol. 2011 Oct;384(4-5):489-98. doi: 10.1007/s00210-011-0645-7. Epub 2011 May 7.
PMID 21553004
 
Preferential reduction of nm23-H1 gene product in metastatic tissues from papillary and follicular carcinomas of the thyroid.
Arai T, Yamashita T, Urano T, Masunaga A, Itoyama S, Itoh K, Shiku H, Sugawara I.
Mod Pathol. 1995 Apr;8(3):252-6.
PMID 7617649
 
P53, bcl-2, and nm23 expressions in serous ovarian tumors: correlation with the clinical and histopathological parameters.
Arik D, Kulacoglu S.
Turk Patoloji Derg. 2011 Jan;27(1):38-45.
PMID 21469425
 
Variability of nm23-H1/NDPK-A expression in human lymphomas and its relation to tumour aggressiveness.
Aryee DN, Simonitsch I, Mosberger I, Kos K, Mann G, Schlogl E, Potschger U, Gadner H, Radaszkiewicz T, Kovar H.
Br J Cancer. 1996 Dec;74(11):1693-8.
PMID 8956779
 
Reduced expression of nm23 protein is associated with advanced tumor stage and distant metastases in human colorectal carcinomas.
Ayhan A, Yasui W, Yokozaki H, Kitadai Y, Tahara E.
Virchows Arch B Cell Pathol Incl Mol Pathol. 1993;63(4):213-8.
PMID 8099459
 
The significance of metastasis-related factors cathepsin-D and nm23 in advanced ovarian cancer.
Baekelandt M, Holm R, Trope CG, Nesland JM, Kristensen GB.
Ann Oncol. 1999 Nov;10(11):1335-41.
PMID 10631462
 
Expression of nm23-H1 in uveal melanoma.
Bakalian S, Marshall JC, Faingold D, Logan P, Antecka E, Burnier MN Jr.
Melanoma Res. 2007 Oct;17(5):284-90.
PMID 17885583
 
Expression of nm23 in the spectrum of pre-invasive, invasive and metastatic breast lesions.
Bal A, Joshi K, Logasundaram R, Radotra BD, Singh R.
Diagn Pathol. 2008 May 30;3:23. doi: 10.1186/1746-1596-3-23.
PMID 18510781
 
Nm23 gene product expression in invasive breast cancer--immunohistochemical analysis and clinicopathological correlation.
Belev B, Aleric I, Vrbanec D, Petrovecki M, Unusic J, Jakic-Razumovic J.
Acta Oncol. 2002;41(4):355-61.
PMID 12234027
 
Protein markers in colorectal cancer: predictors of liver metastasis.
Berney CR, Fisher RJ, Yang J, Russell PJ, Crowe PJ.
Ann Surg. 1999 Aug;230(2):179-84.
PMID 10450731
 
C-erbB-2, p53, and nm23 gene product expression in breast cancer in young women: immunohistochemical analysis and clinicopathologic correlation.
Bertheau P, Steinberg SM, Merino MJ.
Hum Pathol. 1998 Apr;29(4):323-9.
PMID 9563780
 
Gene expression profiling of colon cancer by DNA microarrays and correlation with histoclinical parameters.
Bertucci F, Salas S, Eysteries S, Nasser V, Finetti P, Ginestier C, Charafe-Jauffret E, Loriod B, Bachelart L, Montfort J, Victorero G, Viret F, Ollendorff V, Fert V, Giovaninni M, Delpero JR, Nguyen C, Viens P, Monges G, Birnbaum D, Houlgatte R.
Oncogene. 2004 Feb 19;23(7):1377-91.
PMID 14973550
 
Association of low nm23 RNA levels in human primary infiltrating ductal breast carcinomas with lymph node involvement and other histopathological indicators of high metastatic potential.
Bevilacqua G, Sobel ME, Liotta LA, Steeg PS.
Cancer Res. 1989 Sep 15;49(18):5185-90.
PMID 2475243
 
Nm23-transfected MDA-MB-435 human breast carcinoma cells form tumors with altered phospholipid metabolism and pH: a 31P nuclear magnetic resonance study in vivo and in vitro.
Bhujwalla ZM, Aboagye EO, Gillies RJ, Chacko VP, Mendola CE, Backer JM.
Magn Reson Med. 1999 May;41(5):897-903.
PMID 10332871
 
nm23-H1 expression in non-Hodgkin and Hodgkin lymphomas.
Bircan S, Inamdar KV, Rassidakis GZ, Medeiros LJ.
Appl Immunohistochem Mol Morphol. 2008 May;16(3):207-14. doi: 10.1097/PAI.0b013e318156f1ab.
PMID 18301251
 
Implication of metastasis suppressor NM23-H1 in maintaining adherens junctions and limiting the invasive potential of human cancer cells.
Boissan M, De Wever O, Lizarraga F, Wendum D, Poincloux R, Chignard N, Desbois-Mouthon C, Dufour S, Nawrocki-Raby B, Birembaut P, Bracke M, Chavrier P, Gespach C, Lacombe ML.
Cancer Res. 2010 Oct 1;70(19):7710-22. doi: 10.1158/0008-5472.CAN-10-1887. Epub 2010 Sep 14.
PMID 20841469
 
Nm23/NDP kinases in hepatocellular carcinoma.
Boissan M, Lacombe ML.
J Bioenerg Biomembr. 2006 Aug;38(3-4):169-75. (REVIEW)
PMID 16944304
 
Increased lung metastasis in transgenic NM23-Null/SV40 mice with hepatocellular carcinoma.
Boissan M, Wendum D, Arnaud-Dabernat S, Munier A, Debray M, Lascu I, Daniel JY, Lacombe ML.
J Natl Cancer Inst. 2005 Jun 1;97(11):836-45.
PMID 15928304
 
NM23 gene expression in human prostatic carcinomas and benign prostatic hyperplasias: altered expression in combined androgen blockaded carcinomas.
Borchers H, Meyers FJ, Gumerlock PH, Stewart SL, deVere White RW.
J Urol. 1996 Jun;155(6):2080-4.
PMID 8618340
 
Subcellular localization of Nm23/NDPK A and B isoforms: a reflection of their biological function?
Bosnar MH, Bago R, Cetkovic H.
Mol Cell Biochem. 2009 Sep;329(1-2):63-71. doi: 10.1007/s11010-009-0107-4. Epub 2009 Apr 17. (REVIEW)
PMID 19373546
 
Analysis of both NM23-h1 and NM23-H2 expression identifies "at-risk" patients with colorectal cancer.
Brenner AS, Thebo JS, Senagore AJ, Duepree HJ, Gramlich T, Ormsby A, Lavery IC, Fazio VW.
Am Surg. 2003 Mar;69(3):203-8; discussion 208.
PMID 12678475
 
NM23 gene expression in human breast carcinomas: loss of correlation with cell proliferation in the advanced phase of tumor progression.
Caligo MA, Cipollini G, Berti A, Viacava P, Collecchi P, Bevilacqua G.
Int J Cancer. 1997 Feb 20;74(1):102-11.
PMID 9036878
 
Prognostic significance of the loss of heterozygosity of Nm23-H1 and p53 genes in human colorectal carcinomas.
Campo E, Miquel R, Jares P, Bosch F, Juan M, Leone A, Vives J, Cardesa A, Yague J.
Cancer. 1994 Jun 15;73(12):2913-21.
PMID 8199988
 
Frequency of allele loss of DCC, p53, RBI, WT1, NF1, NM23 and APC/MCC in colorectal cancer assayed by fluorescent multiplex polymerase chain reaction.
Cawkwell L, Lewis FA, Quirke P.
Br J Cancer. 1994 Nov;70(5):813-8.
PMID 7947085
 
Nm23-H1 mutation in neuroblastoma.
Chang CL, Zhu XX, Thoraval DH, Ungar D, Rawwas J, Hora N, Strahler JR, Hanash SM, Radany E.
Nature. 1994 Aug 4;370(6488):335-6.
PMID 8047138
 
Automated and quantitative immunocytochemical assays of Nm23/NDPK protein in breast carcinomas.
Charpin C, Bouvier C, Garcia S, Martini F, Andrac L, Lavaut MN, Allasia C.
Int J Cancer. 1997 Aug 22;74(4):416-20.
PMID 9291431
 
Expression of heparanase gene, CD44v6, MMP-7 and nm23 protein and their relationship with the invasion and metastasis of gastric carcinomas.
Chen JQ, Zhan WH, He YL, Peng JS, Wang JP, Cai SR, Ma JP.
World J Gastroenterol. 2004 Mar 15;10(6):776-82.
PMID 15040016
 
Survey of molecular profiling during human colon cancer development and progression by immunohistochemical staining on tissue microarray.
Chen WC, Lin MS, Zhang BF, Fang J, Zhou Q, Hu Y, Gao HJ.
World J Gastroenterol. 2007 Feb 7;13(5):699-708.
PMID 17278192
 
Expression of E-cadherin and nm23 is associated with the clinicopathological factors of human non-small cell lung cancer in China.
Chen XF, Zhang HT, Qi QY, Sun MM, Tao LY.
Lung Cancer. 2005 Apr;48(1):69-76. Epub 2004 Nov 5.
PMID 15777972
 
The significance of allelic deletions and aneuploidy in colorectal carcinoma. Results of a 5-year follow-up study.
Cohn KH, Ornstein DL, Wang F, LaPaix FD, Phipps K, Edelsberg C, Zuna R, Mott LA, Dunn JL.
Cancer. 1997 Jan 15;79(2):233-44.
PMID 9010096
 
Proteomic analysis of human acute leukemia cells: insight into their classification.
Cui JW, Wang J, He K, Jin BF, Wang HX, Li W, Kang LH, Hu MR, Li HY, Yu M, Shen BF, Wang GJ, Zhang XM.
Clin Cancer Res. 2004 Oct 15;10(20):6887-96.
PMID 15501966
 
Nme gene family evolutionary history reveals pre-metazoan origins and high conservation between humans and the sea anemone, Nematostella vectensis.
Desvignes T, Pontarotti P, Bobe J.
PLoS One. 2010 Nov 11;5(11):e15506. doi: 10.1371/journal.pone.0015506.
PMID 21085602
 
[Study on the correlationship between the expression of nm23H1mRNA, TGF-beta1mRNA and tumor metastases, survival rate with prostate cancer].
Ding GF, Li JC, Xu YF.
Fen Zi Xi Bao Sheng Wu Xue Bao. 2006 Dec;39(6):544-52.
PMID 17348207
 
[Expression of sialylated carbohydrate antigens and nm23-H1 gene in prognosis of breast cancer].
Ding KF, Wu JM.
Zhejiang Da Xue Xue Bao Yi Xue Ban. 2004 Jul;33(4):326-30, 339.
PMID 15269984
 
Expression patterns of ER, HER2, and NM23-H1 in breast cancer patients with different menopausal status: correlations with metastasis.
Dong SW, Wang L, Sui J, Deng XY, Chen XD, Zhang ZW, Liu X, Liu ZM, Zhang JH, Yang QS, Jia YF, Song X.
Mol Diagn Ther. 2011 Aug 1;15(4):211-9. doi: 10.2165/11590360-000000000-00000.
PMID 21913743
 
Prognostic implication of nm23-H1 expression in colorectal carcinomas.
Dursun A, Akyurek N, Gunel N, Yamac D.
Pathology. 2002 Oct;34(5):427-32.
PMID 12408341
 
Nm23-H1 expression does not predict clinical survival in colorectal cancer patients.
Dusonchet L, Corsale S, Migliavacca M, Calo V, Bazan V, Amato A, Cammareri P, Totaro MS, Agnese V, Cascio S, La Rocca G, Sisto PS, Dardanoni G, Valerio MR, Grassi N, Latteri S, Cajozzo M, Buscemi M, Castorina S, Morello V, Tomasino RM, Gebbia N, Russo A.
Oncol Rep. 2003 Sep-Oct;10(5):1257-63.
PMID 12883690
 
Expression of NM23 in human melanoma progression and metastasis.
Easty DJ, Maung K, Lascu I, Veron M, Fallowfield ME, Hart IR, Bennett DC.
Br J Cancer. 1996 Jul;74(1):109-14.
PMID 8679442
 
The intratumoral microvessel density and expression of bFGF and nm23-H1 in colorectal cancer.
Elagoz S, Egilmez R, Koyuncu A, Muslehiddinoglu A, Arici S.
Pathol Oncol Res. 2006;12(1):21-7. Epub 2006 Mar 23.
PMID 16554912
 
Expression of a potential metastasis suppressor gene (nm23) in thyroid neoplasms.
Farley DR, Eberhardt NL, Grant CS, Schaid DJ, van Heerden JA, Hay ID, Khosla S.
World J Surg. 1993 Sep-Oct;17(5):615-20; discussion 620-1.
PMID 8273382
 
Analysis of nm23-H1 protein immunoreactivity in follicular thyroid tumors.
Ferenc T, Lewinski A, Lange D, Niewiadomska H, Sygut J, Sporny S, Wloch J, Salacinska-Los E, Kulig A, Jarzab B.
Pol J Pathol. 2004;55(4):149-53.
PMID 15757202
 
NM23 in Ovarian Cancer. Correlation with clinicopathological and biochemical parameters.
Ferrandina G, Scambia G, Marone M, Benedetti Panici P, Giannitelli C, Pernisco S, Coronetta F, Mancuso S.
Ann N Y Acad Sci. 1996 Apr 30;784:509-12.
PMID 8651607
 
Dermatopathological indicators of poor melanoma prognosis are significantly inversely correlated with the expression of NM23 protein in primary cutaneous melanoma.
Ferrari D, Lombardi M, Ricci R, Michiara M, Santini M, De Panfilis G.
J Cutan Pathol. 2007 Sep;34(9):705-12.
PMID 17696918
 
Levels of nm23 messenger RNA in metastatic malignant melanomas: inverse correlation to disease progression.
Florenes VA, Aamdal S, Myklebost O, Maelandsmo GM, Bruland OS, Fodstad O.
Cancer Res. 1992 Nov 1;52(21):6088-91.
PMID 1356624
 
Differential expression of metastasis-associated genes in papilla of vater and pancreatic cancer correlates with disease stage.
Friess H, Guo XZ, Tempia-Caliera AA, Fukuda A, Martignoni ME, Zimmermann A, Korc M, Buchler MW.
J Clin Oncol. 2001 May 1;19(9):2422-32.
PMID 11331321
 
Correlation of MDR-1, nm23-H1 and H Sema E gene expression with histopathological findings and clinical outcome in ovarian and breast cancer patients.
Galani E, Sgouros J, Petropoulou C, Janinis J, Aravantinos G, Dionysiou-Asteriou D, Skarlos D, Gonos E.
Anticancer Res. 2002 Jul-Aug;22(4):2275-80.
PMID 12174914
 
A three-gene expression signature model for risk stratification of patients with neuroblastoma.
Garcia I, Mayol G, Rios J, Domenech G, Cheung NK, Oberthuer A, Fischer M, Maris JM, Brodeur GM, Hero B, Rodriguez E, Sunol M, Galvan P, de Torres C, Mora J, Lavarino C.
Clin Cancer Res. 2012 Apr 1;18(7):2012-23. doi: 10.1158/1078-0432.CCR-11-2483. Epub 2012 Feb 10.
PMID 22328561
 
Overexpression of nucleoside diphosphate/kinase A/nm23-H1 protein in human lung tumors: association with tumor progression in squamous carcinoma.
Gazzeri S, Brambilla E, Negoescu A, Thoraval D, Veron M, Moro D, Brambilla C.
Lab Invest. 1996 Jan;74(1):158-67.
PMID 8569178
 
Nucleoside diphosphate kinase from human erythrocytes. Structural characterization of the two polypeptide chains responsible for heterogeneity of the hexameric enzyme.
Gilles AM, Presecan E, Vonica A, Lascu I.
J Biol Chem. 1991 May 15;266(14):8784-9.
PMID 1851158
 
Lack of prognostic significance of nm23 expression in human primary breast cancer.
Gohring UJ, Eustermann I, Becker M, Neuhaus W, Rein DT, Schondorf T.
Oncol Rep. 2002 Nov-Dec;9(6):1205-8.
PMID 12375020
 
Co-downregulation of PTEN, KAI-1, and nm23-H1 tumor/metastasis suppressor proteins in non-small cell lung cancer.
Goncharuk VN, del-Rosario A, Kren L, Anwar S, Sheehan CE, Carlson JA, Ross JS.
Ann Diagn Pathol. 2004 Feb;8(1):6-16.
PMID 15129904
 
Evaluation of the expression levels of nm23-H1 mRNA in primary breast cancer, benign breast disease, axillary lymph nodes and normal breast tissue.
Goodall RJ, Dawkins HJ, Robbins PD, Hahnel E, Sarna M, Hahnel R, Papadimitriou JM, Harvey JM, Sterrett GF.
Pathology. 1994 Oct;26(4):423-8.
PMID 7892043
 
Increased nm23 immunoreactivity is associated with selective inhibition of systemic tumour cell dissemination.
Graham AN, Maxwell P, Mulholland K, Patterson AH, Anderson N, McManus KG, Bharucha H, McGuigan JA.
J Clin Pathol. 2002 Mar;55(3):184-9.
PMID 11896068
 
An immunohistochemical analysis of nm23 gene product expression in uveal melanoma.
Greco IM, Calvisi G, Ventura L, Cerrito F.
Melanoma Res. 1997 Jun;7(3):231-6.
PMID 9195562
 
Reduced protein expression of metastasis-related genes (nm23, KISS1, KAI1 and p53) in lymph node and liver metastases of gastric cancer.
Guan-Zhen Y, Ying C, Can-Rong N, Guo-Dong W, Jian-Xin Q, Jie-Jun W.
Int J Exp Pathol. 2007 Jun;88(3):175-83.
PMID 17504447
 
High levels of p19/nm23 protein in neuroblastoma are associated with advanced stage disease and with N-myc gene amplification.
Hailat N, Keim DR, Melhem RF, Zhu XX, Eckerskorn C, Brodeur GM, Reynolds CP, Seeger RC, Lottspeich F, Strahler JR, et al.
J Clin Invest. 1991 Jul;88(1):341-5.
PMID 2056128
 
nm23 expression in tissue sections and tumor effusion cells of ovarian neoplasms.
Harlozinska A, Bar JK, Gerber J.
Int J Cancer. 1996 Oct 21;69(5):415-9.
PMID 8900377
 
Induction of nm23 gene expression in human colonic neoplasms and equal expression in colon tumors of high and low metastatic potential.
Haut M, Steeg PS, Willson JK, Markowitz SD.
J Natl Cancer Inst. 1991 May 15;83(10):712-6.
PMID 2023273
 
Expression and mutational analysis of Nm23-H1 in liver metastases of colorectal cancer.
Heide I, Thiede C, Poppe K, de Kant E, Huhn D, Rochlitz C.
Br J Cancer. 1994 Dec;70(6):1267-71.
PMID 7981087
 
Separating favorable from unfavorable prognostic markers in breast cancer: the role of E-cadherin.
Heimann R, Lan F, McBride R, Hellman S.
Cancer Res. 2000 Jan 15;60(2):298-304.
PMID 10667580
 
Expression of the antimetastatic gene nm23 in human breast cancer: an association with good prognosis.
Hennessy C, Henry JA, May FE, Westley BR, Angus B, Lennard TW.
J Natl Cancer Inst. 1991 Feb 20;83(4):281-5.
PMID 1994057
 
NM23 gene product expression does not predict lymph node metastases or survival in young patients with colorectal cancer.
Heys SD, Langlois N, Smith IC, Walker LG, Eremin O.
Oncol Rep. 1998 May-Jun;5(3):735-9.
PMID 9538187
 
Immunohistochemical analysis of nm23 gene product/NDP kinase expression in pulmonary adenocarcinoma: lack of prognostic value.
Higashiyama M, Doi O, Yokouchi H, Kodama K, Nakamori S, Tateishi R, Kimura N.
Br J Cancer. 1992 Sep;66(3):533-6.
PMID 1325827
 
Expression profiling of favorable and unfavorable neuroblastomas.
Hiyama E, Hiyama K, Yamaoka H, Sueda T, Reynolds CP, Yokoyama T.
Pediatr Surg Int. 2004 Jan;20(1):33-8. Epub 2003 Dec 23.
PMID 14691637
 
Estrogen and progestin regulate metastasis through the PI3K/AKT pathway in human ovarian cancer.
Hua K, Feng W, Cao Q, Zhou X, Lu X, Feng Y.
Int J Oncol. 2008 Nov;33(5):959-67.
PMID 18949358
 
[Expression and clinical significance of nm23-H1 and MUC-1 in peripheral T-cell lymphoma].
Huang HQ, Pan ZH, Lin XB, Wang BF, Hou JH, Zhang Y, Wu QL.
Ai Zheng. 2006 Dec;25(12):1517-23.
PMID 17166378
 
Squamous cell carcinoma of the lung: does the nm23 gene expression correlate to the tumor stage?
Huwer H, Engel M, Welter C, Dooley S, Kalweit G, Feindt P, Gams E.
Thorac Cardiovasc Surg. 1994 Oct;42(5):298-301.
PMID 7863493
 
Expression of the candidate tumor suppressor gene nm23 in the bronchial system of patients with squamous cell lung cancer.
Huwer H, Kalweit G, Engel M, Welter C, Dooley S, Gams E.
Eur J Cardiothorac Surg. 1997 Feb;11(2):206-9.
PMID 9080143
 
Positive relationship between expression of CD44 and hepatic metastases in colorectal cancer.
Ichikawa W.
Pathobiology. 1994;62(4):172-9.
PMID 7537507
 
High levels of nm23 expression are related to cell proliferation in human prostate cancer.
Igawa M, Rukstalis DB, Tanabe T, Chodak GW.
Cancer Res. 1994 Mar 1;54(5):1313-8.
PMID 8118821
 
Association of nm23 protein levels in human prostates with proliferating cell nuclear antigen expression at autopsy.
Igawa M, Urakami S, Shiina H, Ishibe T, Usui T, Chodak GW.
Eur Urol. 1996;30(3):383-7.
PMID 8931974
 
Elevated plasma level of differentiation inhibitory factor nm23-H1 protein correlates with risk factors for myelodysplastic syndrome.
Ito Y, Okabe-Kado J, Honma Y, Iwase O, Shimamoto T, Ohyashiki JH, Ohyashiki K.
Leukemia. 2002 Feb;16(2):165-9.
PMID 11840281
 
NM23 deficiency promotes metastasis in a UV radiation-induced mouse model of human melanoma.
Jarrett SG, Novak M, Harris N, Merlino G, Slominski A, Kaetzel DM.
Clin Exp Metastasis. 2013 Jan;30(1):25-36. doi: 10.1007/s10585-012-9495-z. Epub 2012 Jun 15.
PMID 22699362
 
Increased levels of nm23 H1/nucleoside diphosphate kinase A mRNA associated with adenocarcinoma of the prostate.
Jensen SL, Wood DP Jr, Banks ER, Veron M, Lascu I, McRoberts JW, Rangnekar VM.
World J Urol. 1996;14 Suppl 1:S21-5.
PMID 8738406
 
Inhibition of cell motility after nm23 transfection of human and murine tumor cells.
Kantor JD, McCormick B, Steeg PS, Zetter BR.
Cancer Res. 1993 May 1;53(9):1971-3.
PMID 8481897
 
nm23-H1 expression and loss of heterozygosity in colon adenocarcinoma.
Kapitanovic S, Cacev T, Berkovic M, Popovic-Hadzija M, Radosevic S, Seiwerth S, Spaventi S, Pavelic K, Spaventi R.
J Clin Pathol. 2004 Dec;57(12):1312-8.
PMID 15563674
 
Clinical significance of nm23 expression in resected pathologic-stage I, non-small cell lung cancer.
Katakura H, Tanaka F, Oyanagi H, Miyahara R, Yanagihara K, Otake Y, Wada H.
Ann Thorac Surg. 2002 Apr;73(4):1060-4.
PMID 11996241
 
Expression of nm23 protein in pulmonary adenocarcinomas: inverse 1orrelation to tumor progression.
Kawakubo Y, Sato Y, Koh T, Kono H, Kameya T.
Lung Cancer. 1997 May;17(1):103-13.
PMID 9194030
 
Expression of p53 and NDP-K/nm23 in gastric carcinomas--association with metastasis and clinicopathologic parameters.
Kim KM, Lee A, Chae HS, Shim SI.
J Korean Med Sci. 1995 Dec;10(6):406-13.
PMID 8924224
 
Expression of nm23 H-1 RNA levels in human gastric cancer tissues. A negative correlation with nodal metastasis.
Kodera Y, Isobe K, Yamauchi M, Kondoh K, Kimura N, Akiyama S, Itoh K, Nakashima I, Takagi H.
Cancer. 1994 Jan 15;73(2):259-65.
PMID 8293386
 
Expression of nm23-H1 and nm23-H2 proteins in prostate carcinoma.
Konishi N, Nakaoka S, Tsuzuki T, Matsumoto K, Kitahori Y, Hiasa Y, Urano T, Shiku H.
Jpn J Cancer Res. 1993 Oct;84(10):1050-4.
PMID 7693635
 
nm23-H1 protein expression in newly diagnosed and relapsed childhood acute lymphoblastic leukemia.
Koomagi R, Sauerbrey A, Zintl F, Volm M.
Anticancer Res. 1998 Nov-Dec;18(6A):4307-9.
PMID 9891483
 
Overexpression of nucleoside diphosphate kinase (Nm23) in solid tumours.
Lacombe ML, Sastre-Garau X, Lascu I, Vonica A, Wallet V, Thiery JP, Veron M.
Eur J Cancer. 1991;27(10):1302-7.
PMID 1659843
 
Immunohistochemical analysis of nm23-H1 in stage I non-small cell lung cancer: a useful marker in prediction of metastases.
Lai WW, Wu MH, Yan JJ, Chen FF.
Ann Thorac Surg. 1996 Nov;62(5):1500-4.
PMID 8893591
 
Allelic imbalance at NME1 in microdissected primary and metastatic human colorectal carcinomas is frequent but not associated with metastasis to lymph nodes or liver.
Lamb RF, Going JJ, Pickford I, Birnie GD.
Cancer Res. 1996 Feb 15;56(4):916-20.
PMID 8631033
 
Increased expression of the NME1 gene is associated with metastasis in epithelial ovarian cancer.
Leary JA, Kerr J, Chenevix-Trench G, Doris CP, Hurst T, Houghton CR, Friedlander ML.
Int J Cancer. 1995 Jun 22;64(3):189-95.
PMID 7622307
 
Immunohistochemical demonstration of the nm23-H1 gene product in human malignant melanoma and Spitz nevi.
Lee CS, Pirdas A, Lee MW.
Pathology. 1996 Aug;28(3):220-4.
PMID 8912348
 
Reappraisal of the role of NM23-H1 in colorectal cancers.
Lee JC, Lin YJ, Chow NH, Wang ST.
J Surg Oncol. 2001 Jan;76(1):58-62.
PMID 11223826
 
nm23-H1 protein expression and gene mutation in 150 patients with non-Hodgkin's lymphomas.
Lee JH, Cho SJ, Zhang X, Zheng Z, Lee ES, Kim A, Kim YS, Chae YS, Kim I.
J Korean Med Sci. 2006 Aug;21(4):645-51.
PMID 16891807
 
Altered gene and protein expression by Nm23-H1 in metastasis suppression.
Lee JH, Marshall JC, Steeg PS, Horak CE.
Mol Cell Biochem. 2009 Sep;329(1-2):141-8. doi: 10.1007/s11010-009-0124-3. Epub 2009 May 5. (REVIEW)
PMID 19415462
 
Prognostic significance of p53, nm23, PCNA and c-erbB-2 in gastric cancer.
Lee KE, Lee HJ, Kim YH, Yu HJ, Yang HK, Kim WH, Lee KU, Choe KJ, Kim JP.
Jpn J Clin Oncol. 2003 Apr;33(4):173-9.
PMID 12810831
 
Loss of heterozygosity and microsatellite instability at the DCC and nm23 loci in Duke's B colorectal carcinoma.
Lenehan K, Mulcahy H, Curran B, Bennett MA, Kay E, O'Donoghue DP, Leader M, Croke DT.
Biochem Soc Trans. 1997 Feb;25(1):140S.
PMID 9057038
 
Transfection of human nm23-H1 into the human MDA-MB-435 breast carcinoma cell line: effects on tumor metastatic potential, colonization and enzymatic activity.
Leone A, Flatow U, VanHoutte K, Steeg PS.
Oncogene. 1993a Sep;8(9):2325-33.
PMID 8395676
 
Evidence for nm23 RNA overexpression, DNA amplification and mutation in aggressive childhood neuroblastomas.
Leone A, Seeger RC, Hong CM, Hu YY, Arboleda MJ, Brodeur GM, Stram D, Slamon DJ, Steeg PS.
Oncogene. 1993b Apr;8(4):855-65.
PMID 8384356
 
Inhibition of ovarian cancer metastasis by adeno-associated virus-mediated gene transfer of nm23H1 in an orthotopic implantation model.
Li J, Zhou J, Chen G, Wang H, Wang S, Xing H, Gao Q, Lu Y, He Y, Ma D.
Cancer Gene Ther. 2006 Mar;13(3):266-72.
PMID 16179930
 
[Expression of MUC1, CD44v6, nm23 in gastric carcinomas and regional lymph node tissues and their association with invasion, metastasis, and prognosis of the tumor].
Li Y, Zhang JH, Kuang G, Yang JQ, Zhao Q, Wang XL, Jiao ZK, Zhang ZD, Wang LL.
Ai Zheng. 2003 Sep;22(9):985-9.
PMID 12969535
 
Expression of nm23 protein in human osteosarcoma in relationship with early metastasis.
Liao WM, Chiu KY, Li FB, Qiu JS, Han SY, Chow SP.
Orthopedics. 2000 Nov;23(11):1175-8.
PMID 11103961
 
Granzyme A activates another way to die.
Lieberman J.
Immunol Rev. 2010 May;235(1):93-104. doi: 10.1111/j.0105-2896.2010.00902.x. (REVIEW)
PMID 20536557
 
Nm23-h1 indirectly promotes the survival of acute myeloid leukemia blast cells by binding to more mature components of the leukemic clone.
Lilly AJ, Khanim FL, Hayden RE, Luong QT, Drayson MT, Bunce CM.
Cancer Res. 2011 Feb 1;71(3):1177-86. doi: 10.1158/0008-5472.CAN-10-1704. Epub 2010 Dec 17.
PMID 21169412
 
Increased invasive activity of human hepatocellular carcinoma cells is associated with an overexpression of thyroid hormone beta 1 nuclear receptor and low expression of the anti-metastatic nm23 gene.
Lin KH, Lin YW, Lee HF, Liu WL, Chen ST, Chang KS, Cheng SY.
Cancer Lett. 1995 Nov 27;98(1):89-95.
PMID 8529211
 
Significance of nm23 mRNA expression in human hepatocellular carcinoma.
Lin LI, Lee PH, Wu CM, Lin JK.
Anticancer Res. 1998 Jan-Feb;18(1B):541-6.
PMID 9568175
 
Tissue microarrays in Chinese human rectal cancer: study of expressions of the tumor-associated genes.
Lin MS, Chen WC, Huang JX, Gao HJ, Zhang BF, Fang J, Zhou Q, Hu Y.
Hepatogastroenterology. 2011 Nov-Dec;58(112):1937-42. doi: 10.5754/hge11262.
PMID 22024062
 
NM-23 H1 immunohistochemistry is not useful as predictor of metastatic potential of colorectal cancer.
Lindmark G.
Br J Cancer. 1996 Nov;74(9):1413-8.
PMID 8912537
 
Prognostic impact of nm23-H1 and PCNA expression in pathologic stage I non-small cell lung cancer.
Liu C, Liu J, Wang X, Mao W, Jiang L, Ni H, Mo M, Wang W.
J Surg Oncol. 2011 Aug 1;104(2):181-6. doi: 10.1002/jso.21944. Epub 2011 Apr 14.
PMID 21495034
 
Expression and significance of CD44s, CD44v6, and nm23 mRNA in human cancer.
Liu YJ, Yan PS, Li J, Jia JF.
World J Gastroenterol. 2005 Nov 14;11(42):6601-6.
PMID 16425351
 
Metastasis in pleural mesothelioma. Immunohistochemical markers for disseminated disease.
Lumb PD, Suvarna SK.
Histopathology. 2004 Apr;44(4):345-52.
PMID 15049900
 
Human prostate cancer and benign prostatic hyperplasia: molecular dissection by gene expression profiling.
Luo J, Duggan DJ, Chen Y, Sauvageot J, Ewing CM, Bittner ML, Trent JM, Isaacs WB.
Cancer Res. 2001 Jun 15;61(12):4683-8.
PMID 11406537
 
Immunohistochemical analysis of expression of nm23-H1/nucleoside diphosphate kinase in human thyroid carcinomas: lack of correlation between its expression and lymph node metastasis.
Luo W, Matsuo K, Nagayama Y, Urano T, Furukawa K, Takeshita A, Nakayama T, Yokoyama N, Yamashita S, Izumi M, et al.
Thyroid. 1993 Summer;3(2):105-9.
PMID 8396479
 
Association between NM23-H1 gene expression and metastasis of human uveal melanoma in an animal model.
Ma D, Luyten GP, Luider TM, Jager MJ, Niederkorn JY.
Invest Ophthalmol Vis Sci. 1996 Oct;37(11):2293-301.
PMID 8843913
 
p53, c-erbB-2 and nm23 expression have no prognostic significance in primary pulmonary adenocarcinoma.
MacKinnon M, Kerr KM, King G, Kennedy MM, Cockburn JS, Jeffrey RR.
Eur J Cardiothorac Surg. 1997 May;11(5):838-42.
PMID 9196297
 
Expression of metastasis-related nm23-H1 and nm23-H2 genes in ovarian carcinomas: correlation with clinicopathology, EGFR, c-erbB-2, and c-erbB-3 genes, and sex steroid receptor expression.
Mandai M, Konishi I, Koshiyama M, Mori T, Arao S, Tashiro H, Okamura H, Nomura H, Hiai H, Fukumoto M.
Cancer Res. 1994 Apr 1;54(7):1825-30.
PMID 7907945
 
Loss of nm23 expression predicts distal metastases and poorer survival for breast cancer.
Mao H, Liu H, Fu X, Fang Z, Abrams J, Worsham MJ.
Int J Oncol. 2001 Mar;18(3):587-91.
PMID 11179491
 
Protein-protein interactions: a mechanism regulating the anti-metastatic properties of Nm23-H1.
Marino N, Marshall JC, Steeg PS.
Naunyn Schmiedebergs Arch Pharmacol. 2011 Oct;384(4-5):351-62. doi: 10.1007/s00210-011-0646-6. Epub 2011 Jun 29. (REVIEW)
PMID 21713383
 
Insights into the biology and prevention of tumor metastasis provided by the Nm23 metastasis suppressor gene.
Marino N, Nakayama J, Collins JW, Steeg PS.
Cancer Metastasis Rev. 2012 Dec;31(3-4):593-603. doi: 10.1007/s10555-012-9374-8.
PMID 22706779
 
Overexpression of nm23-H1 and nm23-H2 genes in colorectal carcinomas and loss of nm23-H1 expression in advanced tumour stages.
Martinez JA, Prevot S, Nordlinger B, Nguyen TM, Lacarriere Y, Munier A, Lascu I, Vaillant JC, Capeau J, Lacombe ML.
Gut. 1995 Nov;37(5):712-20.
PMID 8549951
 
Immunohistochemical expression of nm23 in primary invasive malignant melanoma is predictive of survival outcome.
McDermott NC, Milburn C, Curran B, Kay EW, Barry Walsh C, Leader MB.
J Pathol. 2000 Feb;190(2):157-62.
PMID 10657013
 
nm23-H1 Expression in Squamous Cell Carcinoma of the Head and Neck.
McDonald JS, Gartside PS, Pavelic LJ, Gluckman JL, Pavelic ZP.
Pathol Oncol Res. 1996;2(1-2):34-36.
PMID 11173580
 
Value of ezrin, maspin and nm23-H1 protein expressions in predicting outcome of patients with head and neck squamous-cell carcinoma treated with radical radiotherapy.
Mhawech-Fauceglia P, Dulguerov P, Beck A, Bonet M, Allal AS.
J Clin Pathol. 2007 Feb;60(2):185-9. Epub 2006 May 12.
PMID 16698950
 
Clinical significance of nm23 gene expression in gastric cancer.
Monig SP, Nolden B, Lubke T, Pohl A, Grass G, Schneider PM, Dienes HP, Holscher AH, Baldus SE.
Anticancer Res. 2007 Jul-Aug;27(4C):3029-33.
PMID 17695492
 
Expression of nm23 in gastric carcinoma: association with tumor progression and poor prognosis.
Muller W, Schneiders A, Hommel G, Gabbert HE.
Cancer. 1998 Dec 15;83(12):2481-7.
PMID 9874452
 
Increased nm23-H1 and nm23-H2 messenger RNA expression and absence of mutations in colon carcinomas of low and high metastatic potential.
Myeroff LL, Markowitz SD.
J Natl Cancer Inst. 1993 Jan 20;85(2):147-52.
PMID 8418304
 
Changes in biomarker expression in the development of prostatic adenocarcinoma.
Myers RB, Grizzle WE.
Biotech Histochem. 1997 Mar;72(2):86-95. (REVIEW)
PMID 9152521
 
Expression of nm23-H1 in prostatic intraepithelial neoplasia and adenocarcinoma.
Myers RB, Srivastava S, Oelschlager DK, Brown D, Grizzle WE.
Hum Pathol. 1996 Oct;27(10):1021-4.
PMID 8892585
 
Expression of nucleoside diphosphate kinase/nm23 gene product in human pancreatic cancer: an association with lymph node metastasis and tumor invasion.
Nakamori S, Ishikawa O, Ohhigashi H, Kameyama M, Furukawa H, Sasaki Y, Inaji H, Higashiyama M, Imaoka S, Iwanaga T, et al.
Clin Exp Metastasis. 1993 Mar;11(2):151-8.
PMID 8383029
 
Expression of nm23 gene in gastric cancer is associated with a poor 5-year survival.
Nesi G, Palli D, Pernice LM, Saieva C, Paglierani M, Kroning KC, Catarzi S, Rubio CA, Amorosi A.
Anticancer Res. 2001 Sep-Oct;21(5):3643-9.
PMID 11848537
 
Isolation and characterization of a novel human NM23-H1B gene, a different transcript of NM23-H1.
Ni X, Gu S, Dai J, Cheng H, Guo L, Li L, Ji C, Xie Y, Ying K, Mao Y.
J Hum Genet. 2003;48(2):96-100.
PMID 12601555
 
[The mechanism and influence on the biological behavior of human high-metastatic large cell lung cancer cell lines with transfection of nm23-H1 gene.].
Nie Q, Zhu W, Liu L, Fu J, Li D, Li Y, Chen J, Liu H, Zhou Q.
Zhongguo Fei Ai Za Zhi. 2008 Jun 20;11(3):349-53. doi: 10.3779/j.issn.1009-3419.2008.03.035.
PMID 20731932
 
Phase II study of the CPT-11, mitoxantrone and dexamethasone regimen in combination with rituximab in elderly patients with relapsed diffuse large B-cell lymphoma.
Niitsu N, Kohuri M, Higashihara M, Bessho M.
Cancer Sci. 2006 Sep;97(9):933-7. Epub 2006 Jun 29.
PMID 16805825
 
Expression of nm23-H1 is associated with poor prognosis in peripheral T-cell lymphoma, not otherwise specified.
Niitsu N, Nakamine H, Okamoto M.
Clin Cancer Res. 2011 May 1;17(9):2893-9. doi: 10.1158/1078-0432.CCR-10-2999. Epub 2011 Apr 8.
PMID 21478336
 
Serum levels of the nm23-H1 protein and their clinical implication in extranodal NK/T-cell lymphoma.
Niitsu N, Okamoto M, Honma Y, Nakamine H, Tamaru JI, Nakamura S, Yoshino T, Higashihara M, Hirano M, Okabe-Kado J; Adult Lymphoma Treatment Study Group.
Leukemia. 2003b May;17(5):987-90.
PMID 12750720
 
[Expression of nm23 H(1) gene in childhood acute lymphoblastic leukemia and the relationship between nm23 H(1) expression and immunophenotype].
Ning F, Cai SJ, Zhang TJ, Liu XX, Zhang YM.
Zhongguo Dang Dai Er Ke Za Zhi. 2009 Nov;11(11):881-4.
PMID 20113651
 
Potential markers predicting distant metastasis in axillary node-negative breast carcinoma.
Niu Y, Fu X, Lv A, Fan Y, Wang Y.
Int J Cancer. 2002 Apr 10;98(5):754-60.
PMID 11920647
 
Comparison of histological changes and changes in nm23 and c-MET expression between primary and metastatic sites in osteosarcoma: a clinicopathologic and immunohistochemical study.
Oda Y, Naka T, Takeshita M, Iwamoto Y, Tsuneyoshi M.
Hum Pathol. 2000 Jun;31(6):709-16.
PMID 10872665
 
Immunohistochemical analysis of nm23 protein expression in malignant bone tumors.
Oda Y, Walter H, Radig K, Rose I, Neumann W, Roessner A.
J Cancer Res Clin Oncol. 1995;121(11):667-73.
PMID 7593131
 
Downregulation of metastasis suppressor genes in malignant pheochromocytoma.
Ohta S, Lai EW, Pang AL, Brouwers FM, Chan WY, Eisenhofer G, de Krijger R, Ksinantova L, Breza J, Blazicek P, Kvetnansky R, Wesley RA, Pacak K.
Int J Cancer. 2005 Mar 10;114(1):139-43.
PMID 15523699
 
The predictive value of vascular endothelial growth factor and nm23 for the diagnosis of occult metastasis in non-small cell lung cancer.
Ohta Y, Nozaki Z, Nozawa H, Kamesui T, Tsunezuka Y, Oda M, Watanabe G.
Jpn J Cancer Res. 2001 Mar;92(3):361-6.
PMID 11267948
 
Extracellular NM23-H1 protein inhibits the survival of primary cultured normal human peripheral blood mononuclear cells and activates the cytokine production.
Okabe-Kado J, Kasukabe T, Honma Y, Kobayashi H, Maseki N, Kaneko Y.
Int J Hematol. 2009b Sep;90(2):143-52. doi: 10.1007/s12185-009-0384-4. Epub 2009 Aug 5.
PMID 19655221
 
Expression of nm23-H1 gene product in thyroid, ovary, and breast cancers.
Okubo T, Inokuma S, Takeda S, Itoyama S, Kinoshita K, Sugawara I.
Cell Biophys. 1995 Jun;26(3):205-13.
PMID 8521452
 
Gene expression analysis in colorectal cancer using practical DNA array filter.
Okuno K, Yasutomi M, Nishimura N, Arakawa T, Shiomi M, Hida J, Ueda K, Minami K.
Dis Colon Rectum. 2001 Feb;44(2):295-9.
PMID 11227951
 
[The effect of resistance-related proteins on the prognosis and survival of patients with osteosarcoma: an immunohistochemical analysis].
Ozger H, Eralp L, Atalar AC, Toker B, Esberk Ates, L, Sungur M, Bilgic B, Ayan I.
Acta Orthop Traumatol Turc. 2009 Jan-Feb;43(1):28-34. doi: 10.3944/AOTT.2009.028.
PMID 19293613
 
Nucleoside diphosphate kinases.
Parks RE, Agarwal RP.
In: The Enzymes. 1973. Boyer PD. New York, Academic Press. 8: pp307-34.
 
Increased activity of nm23-H1 gene in squamous cell carcinoma of the head and neck is associated with advanced disease and poor prognosis.
Pavelic K, Kapitanovic S, Radosevic S, Bura M, Seiwerth S, Pavelic LJ, Unusic J, Spaventi R.
J Mol Med (Berl). 2000;78(2):111-8.
PMID 10794547
 
Expression analysis of imbalanced genes in prostate carcinoma using tissue microarrays.
Prowatke I, Devens F, Benner A, Grone EF, Mertens D, Grone HJ, Lichter P, Joos S.
Br J Cancer. 2007 Jan 15;96(1):82-8. Epub 2006 Dec 5.
PMID 17146477
 
Multivariate analysis of molecular indicators for postoperative liver metastasis in colorectal cancer cases.
Qian LY, Li P, Li XR, Chen DJ, Zhu SH.
Asian Pac J Cancer Prev. 2012;13(8):3967-71.
PMID 23098501
 
Expression of antimetastatic gene nm23-H1 in epithelial ovarian cancer.
Qian M, Feng Y, Xu L, Zheng S, Zhou X.
Chin Med J (Engl). 1997 Feb;110(2):142-4.
PMID 9594287
 
Proliferation and migration mediated by Dkk-1/Wnt/beta-catenin cascade in a model of hepatocellular carcinoma cells.
Qin X, Zhang H, Zhou X, Wang C, Zhang H, Zhang X, Ye L.
Transl Res. 2007 Nov;150(5):281-94. Epub 2007 Jul 18.
PMID 17964517
 
Genome-wide profile of pleural mesothelioma versus parietal and visceral pleura: the emerging gene portrait of the mesothelioma phenotype.
Roe OD, Anderssen E, Helge E, Pettersen CH, Olsen KS, Sandeck H, Haaverstad R, Lundgren S, Larsson E.
PLoS One. 2009 Aug 7;4(8):e6554. doi: 10.1371/journal.pone.0006554.
PMID 19662092
 
Reduced Nm23/Awd protein in tumour metastasis and aberrant Drosophila development.
Rosengard AM, Krutzsch HC, Shearn A, Biggs JR, Barker E, Margulies IM, King CR, Liotta LA, Steeg PS.
Nature. 1989 Nov 9;342(6246):177-80.
PMID 2509941
 
Nm23 'anti-metastatic' gene product expression in colorectal carcinoma.
Royds JA, Cross SS, Silcocks PB, Scholefield JH, Rees RC, Stephenson TJ.
J Pathol. 1994a Mar;172(3):261-6.
PMID 8195929
 
Nm23 protein expression in thyroid neoplasms.
Royds JA, Silcocks PB, Rees RC, Stephenson TJ.
Pathologica. 1994b Jun;86(3):240-3.
PMID 7808792
 
Relationship of nm23 to proteolytic factors, proliferation and motility in breast cancer tissues and cell lines.
Russell RL, Pedersen AN, Kantor J, Geisinger K, Long R, Zbieranski N, Townsend A, Shelton B, Brunner N, Kute TE.
Br J Cancer. 1998 Sep;78(6):710-7.
PMID 9743288
 
nm23-H1 protein immunohistochemical expression in human breast cancer.
Russo A, Bazan V, Morello V, Valli C, Giarnieri E, Dardanoni G, Cucciarre S, Carreca I, Bazan P, Tomasino R, Vecchione A.
Oncol Rep. 1996 Jan;3(1):183-9.
PMID 21594341
 
Expression of galectin-3, nm-23, and cyclooxygenase-2 could potentially discriminate between benign and malignant pheochromocytoma.
Saffar H, Sanii S, Heshmat R, Haghpanah V, Larijani B, Rajabiani A, Azimi S, Tavangar SM.
Am J Clin Pathol. 2011 Mar;135(3):454-60. doi: 10.1309/AJCPI8AJLUZ3CZLN.
PMID 21350102
 
Expression of metastasis suppressor gene product, nm23 protein, is not inversely correlated with the tumour progression in human malignant melanomas.
Saitoh K, Takahashi H, Yamamoto M, Kishi H, Parsons PG.
Histopathology. 1996 Dec;29(6):497-505.
PMID 8971556
 
nm23 protein expression in colorectal carcinoma metastasis in regional lymph nodes and the liver.
Sarris M, Lee CS.
Eur J Surg Oncol. 2001 Mar;27(2):170-4.
PMID 11289754
 
Cytoplasmic expression of nm23 predicts the potential for cerebral metastasis in patients with primary cutaneous melanoma.
Sarris M, Scolyer RA, Konopka M, Thompson JF, Harper CG, Lee CS.
Melanoma Res. 2004 Feb;14(1):23-7.
PMID 15091190
 
nm23 in ovarian cancer: correlation with clinical outcome and other clinicopathologic and biochemical prognostic parameters.
Scambia G, Ferrandina G, Marone M, Benedetti Panici P, Giannitelli C, Piantelli M, Leone A, Mancuso S.
J Clin Oncol. 1996 Feb;14(2):334-42.
PMID 8636741
 
nm23-H1 expression defines a high-risk subpopulation of patients with early-stage epithelial ovarian carcinoma.
Schneider J, Pollan M, Jimenez E, Marenbach K, Martinez N, Volm M, Marx D, Meden H.
Br J Cancer. 2000 May;82(10):1662-70.
PMID 10817501
 
Nm23-H1 suppresses hepatocarcinoma cell adhesion and migration on fibronectin by modulating glycosylation of integrin beta1.
She S, Xu B, He M, Lan X, Wang Q.
J Exp Clin Cancer Res. 2010 Jul 11;29:93. doi: 10.1186/1756-9966-29-93.
PMID 20618991
 
NM-23 gene loss of heterozygosity and protein expression in high-stage laryngeal squamous cell carcinomas.
Sheikh H, Murphy J, Hunt JL.
Diagn Mol Pathol. 2006 Mar;15(1):1-6.
PMID 16531762
 
Immunohistochemical detection of nm23-H1/NDP kinase in childhood thyroid carcinoma.
Shirahige Y, Irie J, Ashizawa K, Yokoyama N, Ishikawa N, Mimura T, Ito K, Nagataki S.
Oncol Rep. 1997 Mar-Apr;4(2):285-8.
PMID 21590044
 
Prognostic significance of nm23 gene product expression in patients with colorectal carcinoma treated with radical intent.
Soliani P, Ziegler S, Romani A, Corcione L, Campanini N, Dell'Abate P, Del Rio P, Sianesi M.
Oncol Rep. 2004 Jun;11(6):1193-200.
PMID 15138555
 
Expression of nm23 antimetastatic gene product in head and neck squamous cell carcinoma.
Song AU, Mais DD, Groo S, Wright JR, Yoshida GY.
Otolaryngol Head Neck Surg. 2000 Jan;122(1):96-9.
PMID 10629490
 
Evidence for a novel gene associated with low tumor metastatic potential.
Steeg PS, Bevilacqua G, Kopper L, Thorgeirsson UP, Talmadge JE, Liotta LA, Sobel ME.
J Natl Cancer Inst. 1988 Apr 6;80(3):200-4.
PMID 3346912
 
Immunohistochemical expression of transforming growth factor beta 1 and nm-23 H1 antioncogene in prostate cancer: divergent correlation with clinicopathological parameters.
Stravodimos K, Constantinides C, Manousakas T, Pavlaki C, Pantazopoulos D, Giannopoulos A, Dimopoulos C.
Anticancer Res. 2000 Sep-Oct;20(5C):3823-8.
PMID 11268461
 
Lymphatic metastasis and nm23H1 genetic instability in Chinese colon cancer patients.
Su ZH, Li JC.
World J Gastroenterol. 2004 Oct 1;10(19):2800-4.
PMID 15334673
 
Use of crypt isolation to determine loss of heterozygosity of multiple tumor suppressor genes in colorectal carcinoma.
Sugai T, Habano W, Nakamura S, Yoshida T, Uesugi N, Sasou S, Itoh C, Katoh R.
Pathol Res Pract. 2000;196(3):145-50.
PMID 10729918
 
nm23-H1 reduces in vitro cell migration and the liver metastatic potential of colon cancer cells by regulating myosin light chain phosphorylation.
Suzuki E, Ota T, Tsukuda K, Okita A, Matsuoka K, Murakami M, Doihara H, Shimizu N.
Int J Cancer. 2004 Jan 10;108(2):207-11.
PMID 14639604
 
Immunohistochemical analysis of nm23 protein expression in thyroid papillary carcinoma and follicular neoplasm.
Tabriz HM, Adabi Kh, Lashkari A, Heshmat R, Haghpanah V, Larijani B, Tavangar SM.
Pathol Res Pract. 2009;205(2):83-7. doi: 10.1016/j.prp.2008.08.007. Epub 2008 Nov 8.
PMID 18996649
 
Expression of nm23-H1 in colorectal cancer: no association with metastases, histological stage, or survival.
Tabuchi Y, Nakamura T, Kuniyasu T, Ohno M, Nakae S.
Surg Today. 1999;29(2):116-20.
PMID 10030735
 
Expression of genetic markers in lymph node metastases compared with their primary tumours in head and neck cancer.
Takes RP, Baatenburg de Jong RJ, Wijffels K, Schuuring E, Litvinov SV, Hermans J, van Krieken JH.
J Pathol. 2001 Jul;194(3):298-302.
PMID 11439361
 
[Expressions of Nm23, E-cadherin, and beta-catenin in non-small cell lung cancer and their correlations with metastasis and prognosis].
Tang XJ, Zhou QH, Zhang SF, Liu LX.
Ai Zheng. 2005 May;24(5):616-21.
PMID 15890109
 
The prediction of lymph node metastases in colorectal cancer by expression of the nucleoside diphosphate kinase/nm23-H1 and histopathological variables.
Tannapfel A, Katalinic A, Kockerling F, Wittekind C.
Am J Gastroenterol. 1997 Jul;92(7):1182-6.
PMID 9219795
 
Clinical significance of nm23 expression and chromosome 17 numerical aberrations in primary gastric cancer.
Terada R, Yasutake T, Nakamura S, Hisamatsu T, Sawai T, Yamaguchi H, Nakagoe T, Ayabe H, Tagawa Y.
Med Oncol. 2002;19(4):239-48.
PMID 12512918
 
Decreased nm23 expression, but not Ki-67 labeling index, is significantly correlated with lymph node metastasis of breast invasive ductal carcinoma.
Terasaki-Fukuzawa Y, Kijima H, Suto A, Takeshita T, Iezumi K, Sato S, Yoshida H, Sato T, Shimbori M, Shiina Y.
Int J Mol Med. 2002 Jan;9(1):25-9.
PMID 11744991
 
Mechanisms of non-metastatic 2 (NME2)-mediated control of metastasis across tumor types.
Thakur RK, Yadav VK, Kumar P, Chowdhury S.
Naunyn Schmiedebergs Arch Pharmacol. 2011 Oct;384(4-5):397-406. doi: 10.1007/s00210-011-0631-0. Epub 2011 May 10.
PMID 21556888
 
Reduced expression of nm23-H1, but not of nm23-H2, is concordant with the frequency of lymph-node metastasis of human breast cancer.
Tokunaga Y, Urano T, Furukawa K, Kondo H, Kanematsu T, Shiku H.
Int J Cancer. 1993 Aug 19;55(1):66-71.
PMID 8102131
 
Expression of nm23-H1 gene product in mediastinal lymph nodes from lung cancer patients.
Tomita M, Ayabe T, Matsuzaki Y, Onitsuka T.
Eur J Cardiothorac Surg. 2001 Jun;19(6):904-7.
PMID 11404150
 
Potential prognostic value in human breast cancer of cytosolic Nme1 protein detection using an original hen specific antibody.
Toulas C, Mihura J, de Balincourt C, Marques B, Marek E, Soula G, Roche H, Favre G.
Br J Cancer. 1996 Mar;73(5):630-5.
PMID 8605098
 
RER and LOH association with sporadic colorectal cancer in Taiwanese patients.
Tsai MH, Yang YC, Chen KH, Jiang JK, Chou SJ, Chiang TC, Jan HS, Lou MA.
Hepatogastroenterology. 2002 May-Jun;49(45):672-7.
PMID 12063967
 
Reliability of platelet-derived endothelial cell growth factor as a prognostic factor for oral and oropharyngeal carcinomas.
Tsuzuki H, Sunaga H, Ito T, Narita N, Sugimoto C, Fujieda S.
Arch Otolaryngol Head Neck Surg. 2005 Dec;131(12):1071-8.
PMID 16365220
 
The significance of nm23 protein expression in human gastric carcinomas.
Ura H, Denno R, Hirata K.
Surg Today. 1996;26(12):957-65.
PMID 9017955
 
Read-through transcript from NM23-H1 into the neighboring NM23-H2 gene encodes a novel protein, NM23-LV.
Valentijn LJ, Koster J, Versteeg R.
Genomics. 2006 Apr;87(4):483-9. Epub 2006 Jan 25.
PMID 16442775
 
Combined analysis of differentiation inhibitory factor nm23-H1 and nm23-H2 as prognostic factors in acute myeloid leukaemia.
Wakimoto N, Yokoyama A, Okabe-Kado J, Nagata N, Motoyoshi K, Honma Y.
Br J Cancer. 1998 Jun;77(12):2298-303.
PMID 9649149
 
Dictyostelium nucleoside diphosphate kinase highly homologous to Nm23 and Awd proteins involved in mammalian tumor metastasis and Drosophila development.
Wallet V, Mutzel R, Troll H, Barzu O, Wurster B, Veron M, Lacombe ML.
J Natl Cancer Inst. 1990 Jul 18;82(14):1199-202.
PMID 2163458
 
Distant metastasis of gastric cancer is associated with elevated expression of the antimetastatic nm23 gene.
Wang CS, Lin KH, Hsu YC, Hsueh S.
Cancer Lett. 1998 Jun 5;128(1):23-9.
PMID 9652789
 
Mutation in the nm23 gene is associated with metastasis in colorectal cancer.
Wang L, Patel U, Ghosh L, Chen HC, Banerjee S.
Cancer Res. 1993 Feb 15;53(4):717-20.
PMID 7916650
 
Changes of histology and expression of MMP-2 and nm23-H1 in primary and metastatic gastric cancer.
Wang LB, Jiang ZN, Fan MY, Xu CY, Chen WJ, Shen JG.
World J Gastroenterol. 2008 Mar 14;14(10):1612-6.
PMID 18330957
 
Nm23-H1 expression of metastatic tumors in the lymph nodes is a prognostic indicator of oral squamous cell carcinoma.
Wang YF, Chen JY, Chang SY, Chiu JH, Li WY, Chu PY, Tai SK, Wang LS.
Int J Cancer. 2008 Jan 15;122(2):377-86.
PMID 17918157
 
nm23 expression in gastric carcinoma and its relationship with lymphoproliferation.
Wang YK, Ji XL, Ma NX.
World J Gastroenterol. 1999 Feb;5(1):87-89.
PMID 11819397
 
Gene expression levels of CSNK1A1 and AAC-11, but not NME1, in tumor tissues as prognostic factors in NSCLC patients.
Wang Z, Liu H, Liu B, Ma W, Xue X, Chen J, Zhou Q.
Med Sci Monit. 2010 Aug;16(8):CR357-64.
PMID 20671611
 
NM23 expression in metastasis of malignant melanoma is a predictive prognostic parameter correlated with survival.
Xerri L, Grob JJ, Battyani Z, Gouvernet J, Hassoun J, Bonerandi JJ.
Br J Cancer. 1994 Dec;70(6):1224-8.
PMID 7981081
 
Expression of nm23-H1 gene and Sialyl Lewis X antigen in breast cancer.
Yamaguchi A, Ding K, Maehara M, Goi T, Nakagawara G.
Oncology. 1998 Jul-Aug;55(4):357-62.
PMID 9663428
 
Relationship between nm23H1 genetic instability and clinical pathological characteristics in Chinese digestive system cancer patients.
Yang YQ, Wu L, Chen JX, Sun JZ, Li M, Li DM, Lu HY, Su ZH, Lin XQ, Li JC.
World J Gastroenterol. 2008 Sep 28;14(36):5549-56; discussion 5555.
PMID 18810774
 
Evaluation by multivariate analysis of the differentiation inhibitory factor nm23 as a prognostic factor in acute myelogenous leukemia and application to other hematologic malignancies.
Yokoyama A, Okabe-Kado J, Wakimoto N, Kobayashi H, Sakashita A, Maseki N, Nakamaki T, Hino Ki, Tomoyasu S, Tsuruoka N, Motoyoshi K, Nagata N, Honma Y.
Blood. 1998 Mar 15;91(6):1845-51.
PMID 9490665
 
Prognostic significance of CD44 and nm23 expression in patients with stage II and stage IIIA gastric carcinoma.
Yoo CH, Noh SH, Kim H, Lee HY, Min JS.
J Surg Oncol. 1999 May;71(1):22-8.
PMID 10362087
 
Heterogeneous expression of nm23 gene product as a predictor of lymph nodal status in human breast cancer.
Yoshida H, Kijima H, Terasaki Y, Suto A, Takeshita T, Omiya H, Shimojima K, Shimbori M, Sato T, Sato S, Onoda N, Yamazaki H, Tamaoki N, Ueyama Y, Nakamura M.
Int J Oncol. 1998 Dec;13(6):1141-6.
PMID 9824622
 
Expression of the extracellular matrix molecule thrombospondin inversely correlates with malignant progression in melanoma, lung and breast carcinoma cell lines.
Zabrenetzky V, Harris CC, Steeg PS, Roberts DD.
Int J Cancer. 1994 Oct 15;59(2):191-5.
PMID 7927918
 
nm23-H1 immunoreactivity as a prognostic factor in differentiated thyroid carcinoma.
Zafon C, Obiols G, Castellvi J, Tallada N, Galofre P, Gemar E, Mesa J, Simo R.
J Clin Endocrinol Metab. 2001 Aug;86(8):3975-80.
PMID 11502841
 
High level of Nm23-H1 gene expression is associated with local colorectal cancer progression not with metastases.
Zeng ZS, Hsu S, Zhang ZF, Cohen AM, Enker WE, Turnbull AA, Guillem JG.
Br J Cancer. 1994 Nov;70(5):1025-30.
PMID 7947079
 
nm23-H1 is a negative regulator of TGF-b1-dependent induction of epithelial-mesenchymal transition.
Zhao R, Gong L, Li L, Guo L, Zhu D, Wu Z, Zhou Q.
Exp Cell Res. 2013 Mar 10;319(5):740-9. doi: 10.1016/j.yexcr.2012.10.013. Epub 2012 Nov 5.
PMID 23137649
 
nm23 is expressed in reactive mesothelium and is not useful for detection of malignant cells in serous effusions.
Zimmerman RL, Fogt F.
Oncol Rep. 2006 Jan;15(1):85-8.
PMID 16328038
 
High levels of Nm23 gene expression in advanced stage of thyroid carcinomas.
Zou M, Shi Y, al-Sedairy S, Farid NR.
Br J Cancer. 1993 Aug;68(2):385-8.
PMID 8394105
 
Prognostic significance of nm23 protein expression in malignant melanoma. An immunohistochemical study.
van den Oord JJ, Maes A, Stas M, Nuyts J, De Wever I, De Wolf-Peeters C.
Melanoma Res. 1997 Apr;7(2):121-8.
PMID 9167178
 

Citation

This paper should be referenced as such :
Lacombe, ML ; Boissan, M
NME1 (NME/NM23 nucleoside diphosphate kinase 1)
Atlas Genet Cytogenet Oncol Haematol. 2013;17(8):526-538.
Free journal version : [ pdf ]   [ DOI ]
On line version : http://AtlasGeneticsOncology.org/Genes/NME1ID445ch17q21.html

Other Solid tumors implicated (Data extracted from papers in the Atlas) [ 1 ]
  Ovary: Epithelial tumors

External links

Nomenclature
HGNC (Hugo)NME1   7849
Cards
AtlasNME1ID445ch17q21
Entrez_Gene (NCBI)NME1  4830  NME/NM23 nucleoside diphosphate kinase 1
AliasesAWD; GAAD; NB; NBS; 
NDKA; NDPK-A; NDPKA; NM23; NM23-H1
GeneCards (Weizmann)NME1
Ensembl hg19 (Hinxton)ENSG00000239672 [Gene_View]
Ensembl hg38 (Hinxton)ENSG00000239672 [Gene_View]  ENSG00000239672 [Sequence]  chr17:51153559-51162089 [Contig_View]  NME1 [Vega]
ICGC DataPortalENSG00000239672
TCGA cBioPortalNME1
AceView (NCBI)NME1
Genatlas (Paris)NME1
WikiGenes4830
SOURCE (Princeton)NME1
Genetics Home Reference (NIH)NME1
Genomic and cartography
GoldenPath hg38 (UCSC)NME1  -     chr17:51153559-51162089 +  17q21.33   [Description]    (hg38-Dec_2013)
GoldenPath hg19 (UCSC)NME1  -     17q21.33   [Description]    (hg19-Feb_2009)
EnsemblNME1 - 17q21.33 [CytoView hg19]  NME1 - 17q21.33 [CytoView hg38]
Mapping of homologs : NCBINME1 [Mapview hg19]  NME1 [Mapview hg38]
OMIM156490   256700   
Gene and transcription
Genbank (Entrez)AF487339 AK291105 AK309160 AL360166 AL360191
RefSeq transcript (Entrez)NM_000269 NM_198175
RefSeq genomic (Entrez)
Consensus coding sequences : CCDS (NCBI)NME1
Cluster EST : UnigeneHs.463456 [ NCBI ]
CGAP (NCI)Hs.463456
Alternative Splicing GalleryENSG00000239672
Gene ExpressionNME1 [ NCBI-GEO ]   NME1 [ EBI - ARRAY_EXPRESS ]   NME1 [ SEEK ]   NME1 [ MEM ]
Gene Expression Viewer (FireBrowse)NME1 [ Firebrowse - Broad ]
SOURCE (Princeton)Expression in : [Datasets]   [Normal Tissue Atlas]  [carcinoma Classsification]  [NCI60]
GenevestigatorExpression in : [tissues]  [cell-lines]  [cancer]  [perturbations]  
BioGPS (Tissue expression)4830
GTEX Portal (Tissue expression)NME1
Human Protein AtlasENSG00000239672-NME1 [pathology]   [cell]   [tissue]
Protein : pattern, domain, 3D structure
UniProt/SwissProtP15531   [function]  [subcellular_location]  [family_and_domains]  [pathology_and_biotech]  [ptm_processing]  [expression]  [interaction]
NextProtP15531  [Sequence]  [Exons]  [Medical]  [Publications]
With graphics : InterProP15531
Splice isoforms : SwissVarP15531
Catalytic activity : Enzyme2.7.4.6 [ Enzyme-Expasy ]   2.7.4.62.7.4.6 [ IntEnz-EBI ]   2.7.4.6 [ BRENDA ]   2.7.4.6 [ KEGG ]   
PhosPhoSitePlusP15531
Domaine pattern : Prosite (Expaxy)NDP_KINASES (PS00469)   
Domains : Interpro (EBI)Nucleoside_diP_kinase    Nucleoside_diP_kinase_AS   
Domain families : Pfam (Sanger)NDK (PF00334)   
Domain families : Pfam (NCBI)pfam00334   
Domain families : Smart (EMBL)NDK (SM00562)  
Conserved Domain (NCBI)NME1
DMDM Disease mutations4830
Blocks (Seattle)NME1
PDB (SRS)1JXV    1UCN    2HVD    2HVE    3L7U    4ENO   
PDB (PDBSum)1JXV    1UCN    2HVD    2HVE    3L7U    4ENO   
PDB (IMB)1JXV    1UCN    2HVD    2HVE    3L7U    4ENO   
PDB (RSDB)1JXV    1UCN    2HVD    2HVE    3L7U    4ENO   
Structural Biology KnowledgeBase1JXV    1UCN    2HVD    2HVE    3L7U    4ENO   
SCOP (Structural Classification of Proteins)1JXV    1UCN    2HVD    2HVE    3L7U    4ENO   
CATH (Classification of proteins structures)1JXV    1UCN    2HVD    2HVE    3L7U    4ENO   
SuperfamilyP15531
Human Protein Atlas [tissue]ENSG00000239672-NME1 [tissue]
Peptide AtlasP15531
HPRD01131
IPIIPI00012048   IPI00375531   IPI00026260   IPI00795292   IPI00790856   IPI00797082   IPI00604590   IPI00794728   IPI01014620   IPI00790982   
Protein Interaction databases
DIP (DOE-UCLA)P15531
IntAct (EBI)P15531
FunCoupENSG00000239672
BioGRIDNME1
STRING (EMBL)NME1
ZODIACNME1
Ontologies - Pathways
QuickGOP15531
Ontology : AmiGOmagnesium ion binding  RNA polymerase II regulatory region sequence-specific DNA binding  negative regulation of myeloid leukocyte differentiation  single-stranded DNA binding  RNA binding  deoxyribonuclease activity  nucleoside diphosphate kinase activity  nucleoside diphosphate kinase activity  protein binding  ATP binding  GTP binding  nucleus  nucleus  nucleus  cytoplasm  mitochondrial outer membrane  centrosome  cytosol  cytosol  intermediate filament  nucleoside diphosphate phosphorylation  GTP biosynthetic process  UTP biosynthetic process  CTP biosynthetic process  DNA metabolic process  endocytosis  lactation  negative regulation of cell proliferation  negative regulation of gene expression  positive regulation of neuron projection development  response to amine  nucleobase-containing small molecule interconversion  membrane  intermediate filament binding  enzyme binding  hippocampus development  ruffle membrane  response to testosterone  cellular response to drug  identical protein binding  regulation of apoptotic process  gamma-tubulin binding  ribosomal small subunit binding  myelin sheath  positive regulation of DNA binding  perinuclear region of cytoplasm  positive regulation of epithelial cell proliferation  response to cAMP  extracellular exosome  cellular response to glucose stimulus  cellular response to fatty acid  
Ontology : EGO-EBImagnesium ion binding  RNA polymerase II regulatory region sequence-specific DNA binding  negative regulation of myeloid leukocyte differentiation  single-stranded DNA binding  RNA binding  deoxyribonuclease activity  nucleoside diphosphate kinase activity  nucleoside diphosphate kinase activity  protein binding  ATP binding  GTP binding  nucleus  nucleus  nucleus  cytoplasm  mitochondrial outer membrane  centrosome  cytosol  cytosol  intermediate filament  nucleoside diphosphate phosphorylation  GTP biosynthetic process  UTP biosynthetic process  CTP biosynthetic process  DNA metabolic process  endocytosis  lactation  negative regulation of cell proliferation  negative regulation of gene expression  positive regulation of neuron projection development  response to amine  nucleobase-containing small molecule interconversion  membrane  intermediate filament binding  enzyme binding  hippocampus development  ruffle membrane  response to testosterone  cellular response to drug  identical protein binding  regulation of apoptotic process  gamma-tubulin binding  ribosomal small subunit binding  myelin sheath  positive regulation of DNA binding  perinuclear region of cytoplasm  positive regulation of epithelial cell proliferation  response to cAMP  extracellular exosome  cellular response to glucose stimulus  cellular response to fatty acid  
REACTOMEP15531 [protein]
REACTOME PathwaysR-HSA-499943 [pathway]   
NDEx NetworkNME1
Atlas of Cancer Signalling NetworkNME1
Wikipedia pathwaysNME1
Orthology - Evolution
OrthoDB4830
GeneTree (enSembl)ENSG00000239672
Phylogenetic Trees/Animal Genes : TreeFamNME1
HOVERGENP15531
HOGENOMP15531
Homologs : HomoloGeneNME1
Homology/Alignments : Family Browser (UCSC)NME1
Gene fusions - Rearrangements
Fusion : QuiverNME1
Polymorphisms : SNP and Copy number variants
NCBI Variation ViewerNME1 [hg38]
dbSNP Single Nucleotide Polymorphism (NCBI)NME1
dbVarNME1
ClinVarNME1
1000_GenomesNME1 
Exome Variant ServerNME1
ExAC (Exome Aggregation Consortium)ENSG00000239672
GNOMAD BrowserENSG00000239672
Genetic variants : HAPMAP4830
Genomic Variants (DGV)NME1 [DGVbeta]
DECIPHERNME1 [patients]   [syndromes]   [variants]   [genes]  
CONAN: Copy Number AnalysisNME1 
Mutations
ICGC Data PortalNME1 
TCGA Data PortalNME1 
Broad Tumor PortalNME1
OASIS PortalNME1 [ Somatic mutations - Copy number]
Somatic Mutations in Cancer : COSMICNME1  [overview]  [genome browser]  [tissue]  [distribution]  
Mutations and Diseases : HGMDNME1
LOVD (Leiden Open Variation Database)Whole genome datasets
LOVD (Leiden Open Variation Database)LOVD 3.0 shared installation
LOVD (Leiden Open Variation Database)MSeqDR-LSDB Mitochondrial Disease Locus Specific Database
BioMutasearch NME1
DgiDB (Drug Gene Interaction Database)NME1
DoCM (Curated mutations)NME1 (select the gene name)
CIViC (Clinical Interpretations of Variants in Cancer)NME1 (select a term)
intoGenNME1
NCG5 (London)NME1
Cancer3DNME1(select the gene name)
Impact of mutations[PolyPhen2] [SIFT Human Coding SNP] [Buck Institute : MutDB] [Mutation Assessor] [Mutanalyser]
Diseases
OMIM156490    256700   
Orphanet
DisGeNETNME1
MedgenNME1
Genetic Testing Registry NME1
NextProtP15531 [Medical]
TSGene4830
GENETestsNME1
Target ValidationNME1
Huge Navigator NME1 [HugePedia]
snp3D : Map Gene to Disease4830
BioCentury BCIQNME1
ClinGenNME1
Clinical trials, drugs, therapy
Chemical/Protein Interactions : CTD4830
Chemical/Pharm GKB GenePA249
Clinical trialNME1
Miscellaneous
canSAR (ICR)NME1 (select the gene name)
Probes
Litterature
PubMed293 Pubmed reference(s) in Entrez
GeneRIFsGene References Into Functions (Entrez)
CoreMineNME1
EVEXNME1
GoPubMedNME1
iHOPNME1
REVIEW articlesautomatic search in PubMed
Last year publicationsautomatic search in PubMed

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indexed on : Fri Jun 22 17:14:29 CEST 2018
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