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TBX3 (T-box 3)

Identity

Other namesTBX3-ISO
UMS
XHL
HGNC (Hugo) TBX3
LocusID (NCBI) 6926
Location 12q24.1
Location_base_pair Starts at 115108059 and ends at 115121969 bp from pter ( according to hg19-Feb_2009)  [Mapping]
Note TBX3 is a member of the T-box transcription factor family, characterised by a conserved DNA-binding domain known as the T-box (Kispert and Herrmann, 1993; Bollag et al., 1994; Agulnik et al., 1996; reviewed in Papaioannou 2001). TBX3 belongs to the Tbx2 (also known as the Tbx2/3/4/5) subfamily, which includes the closely related genes Tbx2, Tbx3, Tbx4 and Tbx5 (Showell et al., 2004; Naiche et al., 2005). Tbx3 plays critical roles in the development of several organs such as the heart, limb and mammary gland (Davenport et al., 2003; Hoogaars et al., 2007). TBX3 is overexpressed in a range of cancers including breast, pancreatic and melanoma and has been directly implicated in tumourigenesis (Mahlamaki et al., 2002; Fan et al., 2004; Hoek et al., 2004). It has been reported to promote evasion of apoptosis, migration, invasion and tumour forming ability (Brummelkamp et al., 2002; Ito et al., 2005; Renard et al., 2007; Peres et al., 2010).

DNA/RNA

Note Tbx2 and Tbx3 both belong to the Tbx2 subfamily of T-box factors (Agulnik et al., 1996). Phylogenetic analysis suggests that this subfamily originated from a single ancestral gene which was duplicated by unequal crossing over to form a two-gene cluster (Tbx2/3 and Tbx4/5) and at some point in the vertebrate lineage, duplicated again to form four separate genes with Tbx2 and Tbx4 linked on chromosome 11, and Tbx3 and Tbx5 on chromosome 5 (chromosomes 17q23 and 12q24 respectively in humans; Figure 1A) (Campbell et al., 1995; Agulnik et al., 1996; Bamshad et al., 1997). Due to the original duplication event, Tbx2 and Tbx3 form a closely related gene pair while Tbx4 and Tbx5 are more closely related to each other (Agulnik et al., 1996).
 
  Figure 1: A) Drawing of gene duplication. B) Drawing of TBX3 mRNA. (A) Model describing evolution of Tbx 2/3/4/5 gene family (based on Agulnick et al, 1996). (B) Schematic representation of human TBX3 mRNA depicting relative size and position of exons. In the TBX3 + 2a isoform, exon +2a is included in the mRNA through alternative splicing of the second intron.
Description The human TBX3 gene is found on the reverse strand of chromosome 12 and spans 13.9 kb.
Transcription Four TBX3 transcripts have been identified but only two encode for full length functional proteins viz TBX3 and TBX3 + 2a (Figure 1B). The TBX3 mRNA is 4.7 kb and contains 7 exons encoding a protein of 723 amino acids. Alternative splicing of the intronic region between exons 2 and 3 gives rise to the TBX3 + 2a transcript which contains an extra 60 bp sequence designated exon 2a leading to the production of a 743 amino acid protein (Bamshad et al., 1999). TBX3 and TBX3 + 2a isoforms are widely expressed in mouse and human tissues with TBX3 generally observed to be the dominant isoform and the ratio between the two being both tissue and species dependent (Fan et al., 2004).
Pseudogene No pseudogenes have been identified for TBX3 to date.

Protein

Note The TBX3 + 2a transcript yields a protein with an extra 20 amino acids in the middle of the T-box DNA binding domain, giving rise to speculation that it may affect the DNA-binding ability of the protein (Bamshad et al., 1999). While the work of Fan et al. (2004) has provided evidence supporting this hypothesis, subsequent studies have shown no functional difference between the TBX3 and TBX3 + 2a proteins (Hoogaars et al., 2008; Rodriguez et al., 2008).
 
  Figure 2. Schematic representation of the human TBX3 protein. The domains depicted above are: T-box, DNA binding domain (pink); R, repression domain; A, putative activation domain. The amino and carboxy termini of the protein are labelled N and C respectively.
Description The T-box DNA binding domain is found in the N-terminal half of the TBX3 protein extending from amino acids 104 - 285 and in the TBX3 + 2a isoform, the additional 20 amino acids are inserted into the middle of the T-box at position 219 (Figure 2). TBX3 has two repression domains, one in the N-terminus and one in the C-terminus of the protein, as well as a putative activation domain located in the C-terminal end of the protein (Figure 2) (Carlson et al., 2001).
Expression In humans, TBX3 is expressed in a number of organs, including foetal heart, liver, spleen, lung and kidney, and in adult prostate, lung, placenta, ovary, spleen, heart, kidney, testis, small intestine, adrenal gland, thyroid, breast, bladder, uterus, liver and salivary gland (Bamshad et al., 1999).
Localisation The TBX3 protein is predominantly nuclear.
Function TBX3 has been described to function as a transcriptional repressor and to date was shown to directly repress p14, p21, E-cadherin and phosphatase and TENsin homolog (PTEN) (Lingbeek et al., 2002; Hoogaars et al., 2008; Rodriguez et al., 2008; Burgucu et al., 2012). While in vitro assays have suggested that TBX3 is capable of transcriptional activation, it has not yet been shown to activate any physiologically relevant target genes.
Homology Human TBX3 shares 98% amino acid identity with mouse Tbx3 and homologs have been identified in mammals, reptiles, fish and amphibians, as well as invertebrates such as tunicates (Bamshad et al., 1997).

Mutations

Germinal Mutations in human TBX3 have been linked with ulnar-mammary syndrome and those described to date include frame shift, premature termination and missense mutations (Bamshad et al., 1997; Bamshad et al.,1999).

Implicated in

Entity Ulnar-mammary syndrome
Note Results from congenital mutations in a single copy of the human TBX3 gene.
Disease Characterised by posterior limb abnormalities, such as malformed ulna and posterior digits, hypoplasia and/or dysfunction of the mammary and apocrine glands, absent axillary hair, abnormal dentition, delayed puberty in males and genital anomalies (Bamshad et al., 1996; Bamshad et al., 1997).
  
Entity Breast cancer
Note Breast cancer lines screened by real time PCR analysis displayed increased expression of TBX3 in 15 of 28 cell lines tested (Fan et al., 2004). When TBX3 expression was examined by immunohistochemistry in breast tumour tissues, the results showed that levels of TBX3 protein were higher in tumour tissue compared to adjacent normal tissue, with increased cytoplasmic localisation.
  
Entity Pancreatic cancer
Note Microarray analyses comparing non-metastatic and metastatic pancreatic endocrine neoplasms revealed that TBX3 expression is upregulated in the latter tumour type (Hansel et al., 2004).
  
Entity Ovarian cancer
Note Using 2D gel electrophoresis and matrix-assisted laser desorption/ionization (MALDI) time of flight (TOF) mass spectrometry, a truncated form of TBX3 was detected in blood plasma from ovarian cancer patients (Lomnytska et al., 2006).
  
Entity Liver cancer
Note Increased TBX3 expression was shown to correlate with a mutant active form of β-catenin in both human and mouse hepatocellular carcinomas (HCCs) and human hepatoblastomas. Renard et al. (2007) demonstrated TBX3 to be involved in β-catenin's activation of cell proliferation in the human hepatoma cell line HepG2. Using in vitro assays they showed that expression of mutant β-catenin upregulated TBX3 expression and that this was due to direct binding of active β-catenin together with its co-activator T-cell factor (Tcf) to a Tcf-binding element in the TBX3 promoter (Renard et al., 2007).
  
Entity Glioblastoma
Note Genome-wide DNA methylation profiling of 55 glioblastoma tissue samples compared to non-neoplastic brains revealed that methylation of TBX3 correlated with decreased overall survival, identifying it as a potential independent prognostic marker (Etcheverry et al., 2010).
  
Entity Gastric cancer
Note Genome-wide screening identified TBX3 to be epigenetically silenced in the gastric cancer cell line AGS and the TBX3 gene was shown to be methylated in 7 out of 10 primary gastric cancers (Yamashita et al., 2006).
  
Entity Uterine cervical cancer
Note TBX3 expression was shown to be downregulated in microarray analyses comparing lymph node positive to lymph node negative cervical tumours. A significant correlation was observed between low TBX3 expression and the metastatic phenotype. In addition, multivariate analysis identified TBX3 as a potential independent prognostic marker for this cancer (Lyng et al., 2006).
  
Entity Melanoma
Note In 2004, Hoek et al. showed that compared to normal melanocytes TBX3 expression was upregulated in at least 4 of 6 melanoma cell lines tested and Rodriguez et al. (2008) later demonstrated increased TBX3 protein levels in 6 out of 12 melanoma cell lines. Furthermore, TBX3 was shown to contribute to melanoma formation, migration and invasion by a process involving its ability to repress the cell adhesion molecule E-cadherin (Rodriguez et al., 2008; Peres et al., 2010).
  
Entity Head and neck squamous cell cancer
Note TBX3 is upregulated in head and neck squamous cell carcinoma (HNSCC) cell lines and tissues (Humtsoe et al., 2011; Burgucu et al., 2012). The study by Humtsoe et al. shows that TBX3 expression is specifically upregulated in HNSCC cells which display characteristics of epithelial to mesenchymal transition (EMT). Interestingly, however they show that TBX3 promotes cell survival and to a lesser extent, cell invasion in these cells (Humtsoe et al., 2011). This is consistent with the results of Burgucu et al. (2012) which demonstrate that TBX3 represses the tumour suppressor, phosphatase and TENsin homolog (PTEN).
  

External links

Nomenclature
HGNC (Hugo)TBX3   11602
Cards
AtlasTBX3ID42486ch12q24
Entrez_Gene (NCBI)TBX3  6926  T-box 3
GeneCards (Weizmann)TBX3
Ensembl (Hinxton)ENSG00000135111 [Gene_View]  chr12:115108059-115121969 [Contig_View]  TBX3 [Vega]
ICGC DataPortalENSG00000135111
cBioPortalTBX3
AceView (NCBI)TBX3
Genatlas (Paris)TBX3
WikiGenes6926
SOURCE (Princeton)NM_005996 NM_016569
Genomic and cartography
GoldenPath (UCSC)TBX3  -  12q24.1   chr12:115108059-115121969 -  12q24.1   [Description]    (hg19-Feb_2009)
EnsemblTBX3 - 12q24.1 [CytoView]
Mapping of homologs : NCBITBX3 [Mapview]
OMIM181450   601621   
Gene and transcription
Genbank (Entrez)AF002228 AF074999 AF140240 AF170708 AF216750
RefSeq transcript (Entrez)NM_005996 NM_016569
RefSeq genomic (Entrez)AC_000144 NC_000012 NC_018923 NG_008315 NT_029419 NW_001838063 NW_004929385
Consensus coding sequences : CCDS (NCBI)TBX3
Cluster EST : UnigeneHs.744016 [ NCBI ]
CGAP (NCI)Hs.744016
Alternative Splicing : Fast-db (Paris)GSHG0007806
Alternative Splicing GalleryENSG00000135111
Gene ExpressionTBX3 [ NCBI-GEO ]     TBX3 [ SEEK ]   TBX3 [ MEM ]
Protein : pattern, domain, 3D structure
UniProt/SwissProtO15119 (Uniprot)
NextProtO15119  [Medical]
With graphics : InterProO15119
Splice isoforms : SwissVarO15119 (Swissvar)
Domaine pattern : Prosite (Expaxy)TBOX_1 (PS01283)    TBOX_2 (PS01264)    TBOX_3 (PS50252)   
Domains : Interpro (EBI)p53-like_TF_DNA-bd [organisation]   TBX [organisation]   TF_T-box [organisation]   TF_T-box_CS [organisation]  
Related proteins : CluSTrO15119
Domain families : Pfam (Sanger)T-box (PF00907)    TBX (PF12598)   
Domain families : Pfam (NCBI)pfam00907    pfam12598   
Domain families : Smart (EMBL)TBOX (SM00425)  
DMDM Disease mutations6926
Blocks (Seattle)O15119
PDB (SRS)1H6F   
PDB (PDBSum)1H6F   
PDB (IMB)1H6F   
PDB (RSDB)1H6F   
Human Protein AtlasENSG00000135111 [gene] [tissue] [antibody] [cell] [cancer]
Peptide AtlasO15119
HPRD03373
IPIIPI00005110   IPI00298944   IPI00219356   IPI00791862   IPI01013680   
Protein Interaction databases
DIP (DOE-UCLA)O15119
IntAct (EBI)O15119
FunCoupENSG00000135111
BioGRIDTBX3
InParanoidO15119
Interologous Interaction database O15119
IntegromeDBTBX3
STRING (EMBL)TBX3
Ontologies - Pathways
Ontology : AmiGOnegative regulation of transcription from RNA polymerase II promoter  RNA polymerase II transcription factor binding  RNA polymerase II activating transcription factor binding  skeletal system development  blood vessel development  in utero embryonic development  heart looping  outflow tract morphogenesis  atrioventricular bundle cell differentiation  sequence-specific DNA binding transcription factor activity  protein binding  nucleus  transcription, DNA-templated  regulation of transcription from RNA polymerase II promoter  cell aging  positive regulation of cell proliferation  anterior/posterior axis specification, embryo  organ morphogenesis  specification of organ position  stem cell maintenance  limbic system development  male genitalia development  female genitalia development  negative regulation of epithelial cell differentiation  mammary gland development  luteinizing hormone secretion  embryonic forelimb morphogenesis  forelimb morphogenesis  embryonic digit morphogenesis  negative regulation of apoptotic process  sequence-specific DNA binding  negative regulation of myoblast differentiation  positive regulation of cell cycle  negative regulation of transcription, DNA-templated  positive regulation of transcription, DNA-templated  follicle-stimulating hormone secretion  mesoderm morphogenesis  palate development  ventricular septum morphogenesis  branching involved in mammary gland duct morphogenesis  mammary placode formation  cardiac muscle cell fate commitment  sinoatrial node cell development  cellular senescence  positive regulation of stem cell proliferation  
Ontology : EGO-EBInegative regulation of transcription from RNA polymerase II promoter  RNA polymerase II transcription factor binding  RNA polymerase II activating transcription factor binding  skeletal system development  blood vessel development  in utero embryonic development  heart looping  outflow tract morphogenesis  atrioventricular bundle cell differentiation  sequence-specific DNA binding transcription factor activity  protein binding  nucleus  transcription, DNA-templated  regulation of transcription from RNA polymerase II promoter  cell aging  positive regulation of cell proliferation  anterior/posterior axis specification, embryo  organ morphogenesis  specification of organ position  stem cell maintenance  limbic system development  male genitalia development  female genitalia development  negative regulation of epithelial cell differentiation  mammary gland development  luteinizing hormone secretion  embryonic forelimb morphogenesis  forelimb morphogenesis  embryonic digit morphogenesis  negative regulation of apoptotic process  sequence-specific DNA binding  negative regulation of myoblast differentiation  positive regulation of cell cycle  negative regulation of transcription, DNA-templated  positive regulation of transcription, DNA-templated  follicle-stimulating hormone secretion  mesoderm morphogenesis  palate development  ventricular septum morphogenesis  branching involved in mammary gland duct morphogenesis  mammary placode formation  cardiac muscle cell fate commitment  sinoatrial node cell development  cellular senescence  positive regulation of stem cell proliferation  
Protein Interaction DatabaseTBX3
Wikipedia pathwaysTBX3
Gene fusion - rearrangments
Polymorphisms : SNP, mutations, diseases
SNP Single Nucleotide Polymorphism (NCBI)TBX3
snp3D : Map Gene to Disease6926
SNP (GeneSNP Utah)TBX3
SNP : HGBaseTBX3
Genetic variants : HAPMAPTBX3
Exome VariantTBX3
1000_GenomesTBX3 
ICGC programENSG00000135111 
Somatic Mutations in Cancer : COSMICTBX3 
CONAN: Copy Number AnalysisTBX3 
Mutations and Diseases : HGMDTBX3
Mutations and Diseases : intOGenTBX3
Genomic VariantsTBX3  TBX3 [DGVbeta]
dbVarTBX3
ClinVarTBX3
Pred. of missensesPolyPhen-2  SIFT(SG)  SIFT(JCVI)  Align-GVGD  MutAssessor  Mutanalyser  
Pred. splicesGeneSplicer  Human Splicing Finder  MaxEntScan  
Diseases
OMIM181450    601621   
MedgenTBX3
GENETestsTBX3
Disease Genetic AssociationTBX3
Huge Navigator TBX3 [HugePedia]  TBX3 [HugeCancerGEM]
General knowledge
Homologs : HomoloGeneTBX3
Homology/Alignments : Family Browser (UCSC)TBX3
Phylogenetic Trees/Animal Genes : TreeFamTBX3
Chemical/Protein Interactions : CTD6926
Chemical/Pharm GKB GenePA36365
Clinical trialTBX3
Cancer Resource (Charite)ENSG00000135111
Other databases
Other databasehttp://cancergenome.broadinstitute.org/index.php?tgene=TBX3
Probes
Litterature
PubMed61 Pubmed reference(s) in Entrez
CoreMineTBX3
iHOPTBX3
OncoSearchTBX3

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Contributor(s)

Written01-2013Reyna Deeya Ballim, Sharon Prince
Department of Human Biology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa, 7925

Citation

This paper should be referenced as such :
Ballim, RD ; Prince, S
TBX3 (T-box 3)
Atlas Genet Cytogenet Oncol Haematol. 2013;17(7):473-477.
Free online version   Free pdf version   [Bibliographic record ]
URL : http://AtlasGeneticsOncology.org/Genes/TBX3ID42486ch12q24.html

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indexed on : Tue Aug 26 15:24:45 CEST 2014

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