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CCR9 (chemokine (C-C motif) receptor 9)

Written2009-03Hisayuki Nomiyama, Osamu Yoshie
Department of Biochemistry, Kumamoto University Medical School, Honjo, Kumamoto 860-0811, Japan (HN); Department of Microbiology, Kinki University School of Medicine, Osaka-Sayama, Osaka 589-8511, Japan (OY)

(Note : for Links provided by Atlas : click)

Identity

Alias_namesGPR28
chemokine (C-C motif) receptor 9
Alias_symbol (synonym)GPR-9-6
CDw199
Other aliasC-C CKR-9
CC-CKR-9
CCR-9
Ckbeta-15
CMKBR9
HGNC (Hugo) CCR9
LocusID (NCBI) 10803
Atlas_Id 44380
Location 3p21.31  [Link to chromosome band 3p21]
Location_base_pair Starts at 45886504 and ends at 45903175 bp from pter ( according to hg19-Feb_2009)  [Mapping CCR9.png]
Note CCR9 is a G protein-coupled receptor with specificity for a CC chemokine CCL25 (originally described as thymus-expressed chemokine or TECK) and is one of the key molecules in leukocyte homing to gut mucosa.

DNA/RNA

Note The gene and mRNA for CCR9 are 16.6 and 2.7 kb in length, respectively.
 
  The CCR9 gene generates two distinct mRNAs.
Description The CCR9 gene consists of three exons, the second and third exons being the coding-exons. Alternative splicing of the gene generates two distinct mRNAs, CCR9-A and CCR9-B. The CCR9-A cDNA was the first to be cloned.
Transcription The CCR9-A mRNA is encoded by the three exons, while the CCR9-B lacks the sequence derived from the second exon of 49 bp. The CCR9 mRNAs are expressed predominantly in the thymus. Among the cell lines tested, T cell leukemia line MOLT-4 and HTLV-1+ T cells express CCR9 mRNA. The CCR9-A mRNA is expressed at ~10-fold higher levels than CCR9-B mRNA in the cells and cell lines investigated.
Pseudogene None.

Protein

Note CCR9-A: 369 amino acids, 42015 Da.
CCR9-B: 357 amino acids, 40712 Da.
Description CCR9 is a member of the seven transmembrane G protein-coupled receptor superfamily, and is the single receptor for chemokine CCL25.
Expression CCR9 is present on thymocytes as well as on intraepithelial and lamina propria lymphocytes of the small intestine. A small subset of lymphocytes in the colon is also expressing CCR9.
Localisation Cell membrane; Multi-pass membrane protein.
Function CCR9 mediates chemotaxis to CCL25, which is selectively expressed in the thymus and small intestine, and plays an important role in the recruitment of T cells into gut mucosa. Dendritic cells derived from gut-associated lymphoid tissues as well as retinoic acid have been shown to induce the expression of alpha4beta7 integrin and CCR9 on T cells, resulting in their preferential homing to the gut. Although CCR9 deletion in mice has no major effects on the intrathymic T-cell development, down-regulation of CCR9 on activated CD4+CD8+ double positive thymocytes has been shown to allow the migration of maturing thymocytes from the cortex to the medulla.
The EC50 of CCL25 for CCR9-A is somewhat lower than that for CCR9-B. CCR9-A-expressing cells are therefore more responsive to CCL25 than the cells expressing CCR9-B in chemotaxis and calcium influx experiments.
Homology CCR9 is closely related to the chemokine receptors CCR6, CCR7, and CXCR6.

Implicated in

Note
  
Entity T-cell acute lymphocytic leukemia (T-ALL)
Oncogenesis Qiuping et al. (2003) assessed the expression of CCR9 in 21 T-ALL and 17 "T-cell chronic lymphocytic leukemia" (T-CLL) cases, and found that functionally active CCR9 was selectively and frequently expressed on T-ALL CD4+ T cells and was moderately expressed on T-CLL CD4+ T cells.
Annels et al. (2004) investigated homing receptor expression on the blast cells of 11 pediatric T-ALL patients. They found that CCR9 and CD103 (alphaE integrin) were expressed at high levels on T-ALL cells of one patient. This patient later switched to a clonally related acute myeloid leukemia during treatment, and the relapse of leukemia was confined to the gut. This study suggests a role of CCR9 in infiltration of leukemic cells into the gut.
  
  
Entity Adult T-cell leukemia (ATL)
Oncogenesis ATL frequently invades the gastrointestinal tract. Nagakubo et al. (2007) examined CCR9 expression in five ATL-derived cell lines and 10 blood samples from ATL patients containing leukemic cells at high levels. Although all ATL cell lines were CCR9-positive, fresh ATL cells derived from patients were mostly negative. However, ATL cells became readily positive for CCR9 mRNA after one-day culture in parallel with the expression of Tax mRNA. This study suggests that CCR9 is inducible in ATL cells and may play a role in the high incidence of ATL cell invasion into the gastrointestinal tract.
  
  
Entity Melanoma metastasis to the small intestine
Oncogenesis Letsch et al. (2004) assessed CCR9 expression in 20 melanoma cell lines. The CCR9-positive cell lines were established from metastases to small intestine (n = 3), lymph node (n = 4), and skin (n = 1). Only melanoma cell lines derived from small intestinal metastases, however, were responsive to CCL25. This study correlated functional expression of CCR9 with melanoma metastasis to the small intestine.
Amersi et al. (2008) assessed CCR9 expression in primary (n = 23) and metastatic (n = 198) melanomas, and melanoma lines derived from small intestinal metastases (n = 8). CCR9 expression was observed in 88 of 102 metastatic melanomas from the small intestine, 8 of 8 melanoma lines derived from small intestine metastasis, but none of 96 metastatic melanomas from other sites. In addition, 11 of 23 primary melanomas were CCR9-positive and 7 of these later developed small intestinal metastases. This study suggests that CCR9 has a role in melanoma metastasis to the small intestine.
  
  
Entity Melanoma metastasis
Oncogenesis Seidl et al. (2007) investigated expression of eight chemokine receptors including CCR9 in 51 tissue samples of melanocytic origin. CCR9 mRNA was observed in more than half of the melanocytic lesions including lymph node metastases and visceral metastases. The authors concluded that there is no clear trend toward an association between the CCR9 expression levels and melanoma progression.
  
  
Entity Prostate cancer metastasis
Oncogenesis Singh et al. (2004) investigated CCR9 expression in two prostate cancer cell lines. Both cell lines expressed CCR9. This study suggests that expression and activation of CCR9 affect prostate cancer metastasis.
  
  
Entity Small intestinal Crohn's disease
Oncogenesis Papadakis et al. (2001) found that CCR9+ T cells were markedly elevated in the peripheral blood of patients with Crohn's disease but not those with purely colonic Crohn's disease. This study suggests selective involvement of CCR9 in the pathogenesis of small bowel Crohn's disease.
  

Bibliography

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Activation of CCR9/CCL25 in cutaneous melanoma mediates preferential metastasis to the small intestine.
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PMID 15086589
 
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Generation of gut-homing T cells and their localization to the small intestinal mucosa.
Johansson-Lindbom B, Agace WW.
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PMID 17291292
 
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Immunity. 2002 Jan;16(1):1-4. (REVIEW)
PMID 11825560
 
Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: Epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity.
Kunkel EJ, Campbell JJ, Haraldsen G, Pan J, Boisvert J, Roberts AI, Ebert EC, Vierra MA, Goodman SB, Genovese MC, Wardlaw AJ, Greenberg HB, Parker CM, Butcher EC, Andrew DP, Agace WW.
J Exp Med. 2000 Sep 4;192(5):761-8.
PMID 10974041
 
Functional CCR9 expression is associated with small intestinal metastasis.
Letsch A, Keilholz U, Schadendorf D, Assfalg G, Asemissen AM, Thiel E, Scheibenbogen C.
J Invest Dermatol. 2004 Mar;122(3):685-90.
PMID 15086554
 
Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells.
Mora JR, Bono MR, Manjunath N, Weninger W, Cavanagh LL, Rosemblatt M, Von Andrian UH.
Nature. 2003 Jul 3;424(6944):88-93.
PMID 12840763
 
T-cell homing specificity and plasticity: new concepts and future challenges.
Mora JR, von Andrian UH.
Trends Immunol. 2006 May;27(5):235-43. Epub 2006 Mar 31. (REVIEW)
PMID 16580261
 
Expression of CCR9 in HTLV-1+ T cells and ATL cells expressing Tax.
Nagakubo D, Jin Z, Hieshima K, Nakayama T, Shirakawa AK, Tanaka Y, Hasegawa H, Hayashi T, Tsukasaki K, Yamada Y, Yoshie O.
Int J Cancer. 2007 Apr 1;120(7):1591-7.
PMID 17205512
 
Pivotal role of CCL25 (TECK)-CCR9 in the formation of gut cryptopatches and consequent appearance of intestinal intraepithelial T lymphocytes.
Onai N, Kitabatake M, Zhang YY, Ishikawa H, Ishikawa S, Matsushima K.
Int Immunol. 2002 Jul;14(7):687-94.
PMID 12096027
 
CCR9-positive lymphocytes and thymus-expressed chemokine distinguish small bowel from colonic Crohn's disease.
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PMID 11487533
 
Selectively increased expression and functions of chemokine receptor CCR9 on CD4+ T cells from patients with T-cell lineage acute lymphocytic leukemia.
Qiuping Z, Qun L, Chunsong H, Xiaolian Z, Baojun H, Mingzhen Y, Chengming L, Jinshen H, Qingping G, Kejian Z, Zhimin S, Xuejun Z, Junyan L, Jinquan T.
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PMID 14559839
 
CCR9 homes metastatic melanoma cells to the small bowel.
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Clin Cancer Res. 2008 Feb 1;14(3):621-3.
PMID 18245518
 
Profiles of chemokine receptors in melanocytic lesions: de novo expression of CXCR6 in melanoma.
Seidl H, Richtig E, Tilz H, Stefan M, Schmidbauer U, Asslaber M, Zatloukal K, Herlyn M, Schaider H.
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PMID 17306330
 
Expression and functional role of CCR9 in prostate cancer cell migration and invasion.
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Clin Cancer Res. 2004 Dec 15;10(24):8743-50.
PMID 15623660
 
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PMID 17551016
 
CCL25 mediates the localization of recently activated CD8alphabeta(+) lymphocytes to the small-intestinal mucosa.
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A role for CCR9 in T lymphocyte development and migration.
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J Immunol. 2002 Mar 15;168(6):2811-9.
PMID 11884450
 
Chemokine receptors and leukocyte trafficking in the mucosal immune system.
Williams IR.
Immunol Res. 2004;29(1-3):283-92. (REVIEW)
PMID 15181289
 
Mice lacking the CCR9 CC-chemokine receptor show a mild impairment of early T- and B-cell development and a reduction in T-cell receptor gammadelta(+) gut intraepithelial lymphocytes.
Wurbel MA, Malissen M, Guy-Grand D, Meffre E, Nussenzweig MC, Richelme M, Carrier A, Malissen B.
Blood. 2001 Nov 1;98(9):2626-32.
PMID 11675330
 
The chemokine TECK is expressed by thymic and intestinal epithelial cells and attracts double- and single-positive thymocytes expressing the TECK receptor CCR9.
Wurbel MA, Philippe JM, Nguyen C, Victorero G, Freeman T, Wooding P, Miazek A, Mattei MG, Malissen M, Jordan BR, Malissen B, Carrier A, Naquet P.
Eur J Immunol. 2000 Jan;30(1):262-71.
PMID 10602049
 
CCR9A and CCR9B: two receptors for the chemokine CCL25/TECK/Ck beta-15 that differ in their sensitivities to ligand.
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PMID 10640743
 
Cutting edge: identification of the orphan chemokine receptor GPR-9-6 as CCR9, the receptor for the chemokine TECK.
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Citation

This paper should be referenced as such :
Nomiyama, H ; Yoshie, O
CCR9 (chemokine (C-C motif) receptor 9)
Atlas Genet Cytogenet Oncol Haematol. 2010;14(2):91-94.
Free journal version : [ pdf ]   [ DOI ]
On line version : http://AtlasGeneticsOncology.org/Genes/CCR9ID44380ch3p21.html


External links

Nomenclature
HGNC (Hugo)CCR9   1610
Cards
AtlasCCR9ID44380ch3p21
Entrez_Gene (NCBI)CCR9  10803  C-C motif chemokine receptor 9
AliasesCC-CKR-9; CDw199; GPR-9-6; GPR28
GeneCards (Weizmann)CCR9
Ensembl hg19 (Hinxton)ENSG00000173585 [Gene_View]
Ensembl hg38 (Hinxton)ENSG00000173585 [Gene_View]  chr3:45886504-45903175 [Contig_View]  CCR9 [Vega]
ICGC DataPortalENSG00000173585
TCGA cBioPortalCCR9
AceView (NCBI)CCR9
Genatlas (Paris)CCR9
WikiGenes10803
SOURCE (Princeton)CCR9
Genetics Home Reference (NIH)CCR9
Genomic and cartography
GoldenPath hg38 (UCSC)CCR9  -     chr3:45886504-45903175 +  3p21.31   [Description]    (hg38-Dec_2013)
GoldenPath hg19 (UCSC)CCR9  -     3p21.31   [Description]    (hg19-Feb_2009)
EnsemblCCR9 - 3p21.31 [CytoView hg19]  CCR9 - 3p21.31 [CytoView hg38]
Mapping of homologs : NCBICCR9 [Mapview hg19]  CCR9 [Mapview hg38]
OMIM604738   
Gene and transcription
Genbank (Entrez)AF145207 AF145439 AF145440 AJ132337 AK312824
RefSeq transcript (Entrez)NM_001256369 NM_006641 NM_031200
RefSeq genomic (Entrez)
Consensus coding sequences : CCDS (NCBI)CCR9
Cluster EST : UnigeneHs.225946 [ NCBI ]
CGAP (NCI)Hs.225946
Alternative Splicing GalleryENSG00000173585
Gene ExpressionCCR9 [ NCBI-GEO ]   CCR9 [ EBI - ARRAY_EXPRESS ]   CCR9 [ SEEK ]   CCR9 [ MEM ]
Gene Expression Viewer (FireBrowse)CCR9 [ Firebrowse - Broad ]
SOURCE (Princeton)Expression in : [Datasets]   [Normal Tissue Atlas]  [carcinoma Classsification]  [NCI60]
GenevisibleExpression in : [tissues]  [cell-lines]  [cancer]  [perturbations]  
BioGPS (Tissue expression)10803
GTEX Portal (Tissue expression)CCR9
Protein : pattern, domain, 3D structure
UniProt/SwissProtP51686   [function]  [subcellular_location]  [family_and_domains]  [pathology_and_biotech]  [ptm_processing]  [expression]  [interaction]
NextProtP51686  [Sequence]  [Exons]  [Medical]  [Publications]
With graphics : InterProP51686
Splice isoforms : SwissVarP51686
PhosPhoSitePlusP51686
Domaine pattern : Prosite (Expaxy)G_PROTEIN_RECEP_F1_1 (PS00237)    G_PROTEIN_RECEP_F1_2 (PS50262)   
Domains : Interpro (EBI)Chemokine_CCR9    Chemokine_rcpt    GPCR_Rhodpsn    GPCR_Rhodpsn_7TM   
Domain families : Pfam (Sanger)7tm_1 (PF00001)   
Domain families : Pfam (NCBI)pfam00001   
Conserved Domain (NCBI)CCR9
DMDM Disease mutations10803
Blocks (Seattle)CCR9
PDB (SRS)5LWE   
PDB (PDBSum)5LWE   
PDB (IMB)5LWE   
PDB (RSDB)5LWE   
Structural Biology KnowledgeBase5LWE   
SCOP (Structural Classification of Proteins)5LWE   
CATH (Classification of proteins structures)5LWE   
SuperfamilyP51686
Human Protein AtlasENSG00000173585
Peptide AtlasP51686
HPRD09200
IPIIPI00009902   IPI00019986   IPI00926082   
Protein Interaction databases
DIP (DOE-UCLA)P51686
IntAct (EBI)P51686
FunCoupENSG00000173585
BioGRIDCCR9
STRING (EMBL)CCR9
ZODIACCCR9
Ontologies - Pathways
QuickGOP51686
Ontology : AmiGOCD8-positive, gamma-delta intraepithelial T cell differentiation  chemokine receptor activity  plasma membrane  integral component of plasma membrane  chemotaxis  immune response  cellular defense response  G-protein coupled receptor signaling pathway  positive regulation of cytosolic calcium ion concentration  cell surface  C-C chemokine receptor activity  chemokine-mediated signaling pathway  
Ontology : EGO-EBICD8-positive, gamma-delta intraepithelial T cell differentiation  chemokine receptor activity  plasma membrane  integral component of plasma membrane  chemotaxis  immune response  cellular defense response  G-protein coupled receptor signaling pathway  positive regulation of cytosolic calcium ion concentration  cell surface  C-C chemokine receptor activity  chemokine-mediated signaling pathway  
Pathways : KEGGCytokine-cytokine receptor interaction    Chemokine signaling pathway    Intestinal immune network for IgA production   
REACTOMEP51686 [protein]
REACTOME PathwaysR-HSA-418594 [pathway]   
NDEx NetworkCCR9
Atlas of Cancer Signalling NetworkCCR9
Wikipedia pathwaysCCR9
Orthology - Evolution
OrthoDB10803
GeneTree (enSembl)ENSG00000173585
Phylogenetic Trees/Animal Genes : TreeFamCCR9
HOVERGENP51686
HOGENOMP51686
Homologs : HomoloGeneCCR9
Homology/Alignments : Family Browser (UCSC)CCR9
Gene fusions - Rearrangements
Polymorphisms : SNP and Copy number variants
NCBI Variation ViewerCCR9 [hg38]
dbSNP Single Nucleotide Polymorphism (NCBI)CCR9
dbVarCCR9
ClinVarCCR9
1000_GenomesCCR9 
Exome Variant ServerCCR9
ExAC (Exome Aggregation Consortium)CCR9 (select the gene name)
Genetic variants : HAPMAP10803
Genomic Variants (DGV)CCR9 [DGVbeta]
DECIPHERCCR9 [patients]   [syndromes]   [variants]   [genes]  
CONAN: Copy Number AnalysisCCR9 
Mutations
ICGC Data PortalCCR9 
TCGA Data PortalCCR9 
Broad Tumor PortalCCR9
OASIS PortalCCR9 [ Somatic mutations - Copy number]
Somatic Mutations in Cancer : COSMICCCR9  [overview]  [genome browser]  [tissue]  [distribution]  
Mutations and Diseases : HGMDCCR9
LOVD (Leiden Open Variation Database)Whole genome datasets
LOVD (Leiden Open Variation Database)LOVD 3.0 shared installation
BioMutasearch CCR9
DgiDB (Drug Gene Interaction Database)CCR9
DoCM (Curated mutations)CCR9 (select the gene name)
CIViC (Clinical Interpretations of Variants in Cancer)CCR9 (select a term)
intoGenCCR9
NCG5 (London)CCR9
Cancer3DCCR9(select the gene name)
Impact of mutations[PolyPhen2] [SIFT Human Coding SNP] [Buck Institute : MutDB] [Mutation Assessor] [Mutanalyser]
Diseases
OMIM604738   
Orphanet
MedgenCCR9
Genetic Testing Registry CCR9
NextProtP51686 [Medical]
TSGene10803
GENETestsCCR9
Target ValidationCCR9
Huge Navigator CCR9 [HugePedia]
snp3D : Map Gene to Disease10803
BioCentury BCIQCCR9
ClinGenCCR9
Clinical trials, drugs, therapy
Chemical/Protein Interactions : CTD10803
Chemical/Pharm GKB GenePA26174
Clinical trialCCR9
Miscellaneous
canSAR (ICR)CCR9 (select the gene name)
Probes
Litterature
PubMed58 Pubmed reference(s) in Entrez
GeneRIFsGene References Into Functions (Entrez)
CoreMineCCR9
EVEXCCR9
GoPubMedCCR9
iHOPCCR9
REVIEW articlesautomatic search in PubMed
Last year publicationsautomatic search in PubMed

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