A polymorphic enhancer near GREM1 influences bowel cancer risk through differential CDX2 and TCF7L2 binding

Cell Reports

Volumn 8, Issue 4, 2014, Pages 983-990

  Lewis, Annabelle ^a   Freeman Mills, Luke ^a   delaCalle Mustienes, Elisa ^b   Giráldez Pérez, RosaMaría ^b   Davis, Hayley ^a   Jaeger, Emma ^a   Becker, Martin ^c   Hubner, Nina C ^d   Nguyen, Luan N ^d   Zeron Medina, Jorge ^e   Bond, Gareth ^e   Stunnenberg, Hendrik G ^d   Carvajal, Jaime J ^b   Gomez Skarmeta, Jose Luis ^b   Leedham, Simon ^a   Tomlinson, Ian ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Departamento de Biología Molecular e Ingeniería Bioquímica   (Spain)

^c MAX PLANCK INSTITUTE FOR PSYCHOLINGUISTICS   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR 7 LIKE 2; TRANSCRIPTION FACTOR CDX2; CDX2 PROTEIN, HUMAN; GREM1 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; SIGNAL PEPTIDE; TCF7L2 PROTEIN, HUMAN; MESSENGER RNA;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER RISK; CANCER SUSCEPTIBILITY; CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; EMBRYO; ENHANCER REGION; GENE; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENOTYPE; GREM1 GENE; HUMAN; HUMAN TISSUE; INTESTINE CANCER; MOUSE; NONHUMAN; POLYMORPHIC ENHANCER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; STEM CELL; TUMOR GROWTH; TUMOR VOLUME; WNT SIGNALING PATHWAY; ANIMAL; ANTIBODY SPECIFICITY; COLON TUMOR; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETIC PREDISPOSITION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; RISK; TRANSGENIC MOUSE; TUMOR CELL LINE; CHROMATIN STRUCTURE; GENE FREQUENCY; GENETIC DIFFERENCE; GENETIC SUSCEPTIBILITY; HUMAN CELL;

MUS;

ANIMALS; BASE SEQUENCE; CELL LINE, TUMOR; COLONIC NEOPLASMS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HOMEODOMAIN PROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE, TRANSGENIC; ORGAN SPECIFICITY; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN;

EID: 84908356322     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.07.020     Document Type: Article

References (22)

1. Barros R., da Costa L.T., Pinto-de-Sousa J., Duluc I., Freund J.N., David L., Almeida R. CDX2 autoregulation in human intestinal metaplasia of the stomach: impact on the stability of the phenotype. Gut 2011, 60:290-298.
2. Butter F., Davison L., Viturawong T., Scheibe M., Vermeulen M., Todd J.A., Mann M. Proteome-wide analysis of disease-associated SNPs that show allele-specific transcription factor binding. PLoS Genet. 2012, 8:e1002982.
3. Carvajal-Carmona L.G., Zauber A.G., Jones A.M., Howarth K., Wang J., Cheng T., Riddell R., Lanas A., Morton D., Bertagnolli M.M., Tomlinson I. Much of the genetic risk of colorectal cancer is likely to be mediated through susceptibility to adenomas. Gastroenterology 2013, 144:53-55. APC Trial Collaborators, APPROVe Trial CollaboratorsAPPROVe Trial Collaborators, CORGI Study CollaboratorsCORGI Study Collaborators, Colon Cancer Family Registry CollaboratorsColon Cancer Family Registry Collaborators, CGEMS CollaboratorsCGEMS Collaborators.
4. Cavallo R.A., Cox R.T., Moline M.M., Roose J., Polevoy G.A., Clevers H., Peifer M., Bejsovec A. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 1998, 395:604-608.
5. Gao N., White P., Kaestner K.H. Establishment of intestinal identity and epithelial-mesenchymal signaling by Cdx2. Dev. Cell 2009, 16:588-599.
6. Gazzerro E., Smerdel-Ramoya A., Zanotti S., Stadmeyer L., Durant D., Economides A.N., Canalis E. Conditional deletion of gremlin causes a transient increase in bone formation and bone mass. J.Biol. Chem. 2007, 282:31549-31557.
7. Giresi P.G., Kim J., McDaniell R.M., Iyer V.R., Lieb J.D. FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin. Genome Res. 2007, 17:877-885.
8. Hardwick J.C., Kodach L.L., Offerhaus G.J., van den Brink G.R. Bone morphogenetic protein signalling in colorectal cancer. Nat. Rev. Cancer 2008, 8:806-812.
9. He X.C., Zhang J., Tong W.G., Tawfik O., Ross J., Scoville D.H., Tian Q., Zeng X., He X., Wiedemann L.M., et al. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat. Genet. 2004, 36:1117-1121.
10. Jaeger E., Webb E., Howarth K., Carvajal-Carmona L., Rowan A., Broderick P., Walther A., Spain S., Pittman A., Kemp Z., et al. Common genetic variants at the CRAC1 (HMPS) locus on chromosome 15q13.3 influence colorectal cancer risk. Nat. Genet. 2008, 40:26-28. CORGI Consortium.
11. Jaeger E., Leedham S., Lewis A., Segditsas S., Becker M., Cuadrado P.R., Davis H., Kaur K., Heinimann K., Howarth K., et al. Hereditary mixed polyposis syndrome is caused by a 40-kb upstream duplication that leads to increased and ectopic expression of the BMP antagonist GREM1. Nat. Genet. 2012, 44:699-703.
12. Mokry M., Hatzis P., de Bruijn E., Koster J., Versteeg R., Schuijers J., van de Wetering M., Guryev V., Clevers H., Cuppen E. Efficient double fragmentation ChIP-seq provides nucleotide resolution protein-DNA binding profiles. PLoS ONE 2010, 5:e15092.
13. Qualtrough D., Hinoi T., Fearon E., Paraskeva C. Expression of CDX2 in normal and neoplastic human colon tissue and during differentiation of an invitro model system. Gut 2002, 51:184-190.
14. Roose J., Molenaar M., Peterson J., Hurenkamp J., Brantjes H., Moerer P., van de Wetering M., Destrée O., Clevers H. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 1998, 395:608-612.
15. Scoville D.H., Sato T., He X.C., Li L. Current view: intestinal stem cells and signaling. Gastroenterology 2008, 134:849-864.
16. Su L.K., Kinzler K.W., Vogelstein B., Preisinger A.C., Moser A.R., Luongo C., Gould K.A., Dove W.F. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 1992, 256:668-670.
17. Tomlinson I.P., Carvajal-Carmona L.G., Dobbins S.E., Tenesa A., Jones A.M., Howarth K., Palles C., Broderick P., Jaeger E.E., Farrington S., et al. Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer. PLoS Genet. 2011, 7:e1002105. COGENT Consortium, CORGI CollaboratorsCORGI Collaborators, EPICOLON ConsortiumEPICOLON Consortium.
18. Umlauf D., Goto Y., Feil R. Site-specific analysis of histone methylation and acetylation. Methods Mol. Biol. 2004, 287:99-120.
19. Verzi M.P., Hatzis P., Sulahian R., Philips J., Schuijers J., Shin H., Freed E., Lynch J.P., Dang D.T., Brown M., et al. TCF4 and CDX2, major transcription factors for intestinal function, converge on the same cis-regulatory regions. Proc. Natl. Acad. Sci. USA 2010, 107:15157-15162.
20. Verzi M.P., Shin H., San Roman A.K., Liu X.S., Shivdasani R.A. Intestinal master transcription factor CDX2 controls chromatin access for partner transcription factor binding. Mol. Cell. Biol. 2013, 33:281-292.
21. Whiffin N., Dobbins S.E., Hosking F.J., Palles C., Tenesa A., Wang Y., Farrington S.M., Jones A.M., Broderick P., Campbell H., et al. Deciphering the genetic architecture of low-penetrance susceptibility to colorectal cancer. Hum. Mol. Genet. 2013, 22:5075-5082.
22. Zuniga A., Laurent F., Lopez-Rios J., Klasen C., Matt N., Zeller R. Conserved cis-regulatory regions in a large genomic landscape control SHH and BMP-regulated Gremlin1 expression in mouse limb buds. BMC Dev. Biol. 2012, 12:23.