Identification and characterization of functional risk variants for colorectal cancer mapping to chromosome 11q23.1

Human Molecular Genetics

Volumn 23, Issue 8, 2014, Pages 2198-2209

  Biancolella, Michela ^a   Fortini, Barbara K ^a   Tring, Stephanie ^a   Plummer, Sarah J ^a   Mendoza Fandino, Gustavo A ^a   Hartiala, Jaana ^a   Hitchler, Michael J ^a,e   Yan, Chunli ^a   Schumacher, Fredrick R ^a   Conti, David V ^a   Edlund, Christopher K ^a   Noushmehr, Houtan ^a,f   Coetzee, Simon G ^a,f   Bresalier, Robert S ^b   Ahnen, Dennis J ^c   Barry, Elizabeth L ^d   Berman, Benjamin P ^a   Rice, Judd C ^a   Coetzee, Gerhard A ^a   Casey, Graham ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d DARTMOUTH MEDICAL SCHOOL   (United States)

^e KAISER PERMANENTE   (United States)

^f UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; DNA FRAGMENT; TRANSCRIPTION FACTOR;

ALLELE; ARTICLE; BINDING AFFINITY; CHROMATIN; CHROMOSOME 11Q; CHROMOSOME 11Q23.1; CHROMOSOME IDENTIFICATION; CHROMOSOME MAP; COLORECTAL CANCER; CONTROLLED STUDY; ENHANCER REGION; EXON; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; HAPLOTYPE; HISTONE MODIFICATION; HUMAN; HUMAN TISSUE; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; QUANTITATIVE TRAIT LOCUS; REPORTER GENE; SINGLE NUCLEOTIDE POLYMORPHISM; SITE DIRECTED MUTAGENESIS; TRANSIENT TRANSFECTION;

CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, PAIR 11; COLORECTAL NEOPLASMS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENHANCER ELEMENTS, GENETIC; HUMANS; LUCIFERASES; MICROSATELLITE REPEATS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; QUANTITATIVE TRAIT LOCI; RISK FACTORS; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 84897888973     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt584     Document Type: Article

References (56)

1. Houlston, R.S., Cheadle, J., Dobbins, S.E., Tenesa, A., Jones, A.M., Howarth, K., Spain, S.L., Broderick, P., Domingo, E., Farrington, S. et al. (2010) Meta-analysis of three genome-wide association studies identifies susceptibility loci for colorectal cancer at 1q41, 3q26.2, 12q13.13 and 20q13.33. Nat. Genet., 42, 973-977.
2. Houlston, R.S., Webb, E., Broderick, P., Pittman, A.M., Di Bernardo, M.C., Lubbe, S., Chandler, I., Vijayakrishnan, J., Sullivan, K., Penegar, S. et al. (2008) Meta-analysis of genome-wide association data identifies four new susceptibility loci for colorectal cancer. Nat. Genet., 40, 1426-1435.
3. Tomlinson, I.P., Webb, E., Carvajal-Carmona, L., Broderick, P., Howarth, K., Pittman, A.M., Spain, S., Lubbe, S., Walther, A., Sullivan, K. et al. (2008) A genome-wide association study identifies colorectal cancer susceptibility loci on chromosomes 10p14 and 8q23.3. Nat. Genet., 40, 623-630.
4. Tenesa, A., Farrington, S.M., Prendergast, J.G., Porteous, M.E., Walker, M., Haq, N., Barnetson, R.A., Theodoratou, E., Cetnarskyj, R., Cartwright, N. et al. (2008) Genome-wide association scan identifies a colorectal cancer susceptibility locus on 11q23 and replicates risk loci at 8q24 and 18q21. Nat. Genet., 40, 631-637.
5. Tomlinson, I., Webb, E., Carvajal-Carmona, L., Broderick, P., Kemp, Z., Spain, S., Penegar, S., Chandler, I., Gorman, M., Wood, W. et al. (2007) A genome-wide association scan of tag SNPs identifies a susceptibility variant for colorectal cancer at 8q24.21. Nat. Genet., 39, 984-988.
6. Broderick, P., Carvajal-Carmona, L., Pittman, A.M., Webb, E., Howarth, K., Rowan, A., Lubbe, S., Spain, S., Sullivan, K., Fielding, S. et al. (2007) A genome-wide association study shows that common alleles of SMAD7 influence colorectal cancer risk. Nat. Genet., 39, 1315-1317.
7. Zanke, B.W., Greenwood, C.M., Rangrej, J., Kustra, R., Tenesa, A., Farrington, S.M., Prendergast, J., Olschwang, S., Chiang, T., Crowdy, E. et al. (2007) Genome-wide association scan identifies a colorectal cancer susceptibility locus on chromosome 8q24. Nat. Genet., 39, 989-994.
8. Dunlop, M.G., Dobbins, S.E., Farrington, S.M., Jones, A.M., Palles, C., Whiffin, N., Tenesa, A., Spain, S., Broderick, P., Ooi, L.Y. et al. (2012) Common variation near CDKN1A, POLD3 and SHROOM2 influences colorectal cancer risk. Nat. Genet., 44, 770-776.
9. Peters, U., Hutter, C.M., Hsu, L., Schumacher, F.R., Conti, D.V., Carlson, C.S., Edlund, C.K., Haile, R.W., Gallinger, S., Zanke, B.W. et al. (2012) Meta-analysis of new genome-wide association studies of colorectal cancer risk. Hum. Genet., 131, 217-234.
10. Peters, U., Jiao, S., Schumacher, F.R., Hutter, C.M., Aragaki, A.K., Baron, J.A., Berndt, S.I., Bezieau, S., Brenner, H., Butterbach, K. et al. (2012) Identification of genetic susceptibility loci for colorectal tumors in a genome-wide meta-analysis. Gastroenterology, 144, 799-807.
11. Jiao, S., Hsu, L., Berndt, S., Bezieau, S., Brenner, H., Buchanan, D., Caan, B.J., Campbell, P.T., Carlson, C.S., Casey, G. et al. (2012) Genome-wide search for gene-gene interactions in colorectal cancer. PLoSONE, 7, e52535.
12. Fernandez-Rozadilla, C., Cazier, J.B., Tomlinson, I.P., Carvajal-Carmona, L.G., Palles, C., Lamas, M.J., Baiget, M., Lopez-Fernandez, L.A., Brea-Fernandez, A., Abuli, A. et al. (2013) A colorectal cancer genome-wide association study in a Spanish cohort identifies two variants associated with colorectal cancer risk at 1p33 and 8p12. BMC Genomics, 14, 55.
13. Jia, L., Landan, G., Pomerantz, M., Jaschek, R., Herman, P., Reich, D., Yan, C., Khalid, O., Kantoff, P., Oh, W. et al. (2009) Functional enhancers at the gene-poor 8q24 cancer-linked locus. PLoS Genet., 5, e1000597.
14. Pomerantz, M.M., Ahmadiyeh, N., Jia, L., Herman, P., Verzi, M.P., Doddapaneni, H., Beckwith, C.A., Chan, J.A., Hills, A., Davis, M. et al. (2009) The 8q24 cancer risk variant rs6983267 shows long-range interaction with MYC in colorectal cancer. Nat. Genet., 41, 882-884.
15. Pomerantz, M.M., Beckwith, C.A., Regan, M.M., Wyman, S.K., Petrovics, G., Chen, Y., Hawksworth, D.J., Schumacher, F.R., Mucci, L., Penney, K.L. et al. (2009) Evaluation of the 8q24 prostate cancer risk locus and MYC expression. Cancer Res., 69, 5568-5574.
16. Meyer, K.B., Maia, A.T., O'Reilly, M., Ghoussaini, M., Prathalingam, R., Porter-Gill, P., Ambs, S., Prokunina-Olsson, L., Carroll, J. and Ponder, B.A. (2011) A functional variant at a prostate cancer predisposition locus at 8q24 is associated with PVT1 expression. PLoS Genet., 7, e1002165.
17. Tuupanen, S., Yan, J., Turunen, M., Gylfe, A.E., Kaasinen, E., Li, L., Eng, C., Culver, D.A., Kalady, M.F., Pennison, M.J. et al. (2012) Characterization of the colorectal cancer-associated enhancer MYC-335 at 8q24: the role of rs67491583. Cancer Genet., 205, 25-33.
18. Visser, M., Kayser, M. and Palstra, R.J. (2012) HERC2 rs12913832 modulates human pigmentation by attenuating chromatin-loop formation between a long-range enhancer and the OCA2 promoter. Genome Res., 22, 446-455.
19. Visel, A., Blow, M.J., Li, Z., Zhang, T., Akiyama, J.A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F. et al. (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature, 457, 854-858.
20. Rahimov, F., Marazita, M.L., Visel, A., Cooper, M.E., Hitchler, M.J., Rubini, M., Domann, F.E., Govil, M., Christensen, K., Bille, C. et al. (2008) Disruption of an AP-2alpha binding site in an IRF6 enhancer is associated with cleft lip. Nat. Genet., 40, 1341-1347.
21. Coetzee, S.G., Rhie, S.K., Berman, B.P., Coetzee, G.A. and Noushmehr, H. (2012) FunciSNP: an R/bioconductor tool integrating functional non-coding data sets with genetic association studies to identify candidate regulatory SNPs. Nucleic Acids Res., 40, e139.
22. ENCODE (2004) The ENCODE (ENCyclopedia Of DNA Elements) Project. Science, 306, 636-640.
23. Barrett, J.C. (2009) Haploview: Visualization and Analysis of SNP Genotype Data. Cold Spring Harbor Protocols, CSHL Press 2009, pdb ip71.
24. Barrett, J.C., Fry, B., Maller, J. and Daly, M.J. (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics, 21, 263-265.
25. Wang, E.T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S.F., Schroth, G.P. and Burge, C.B. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature, 456, 470-476.
26. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J. and Pachter, L. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol., 28, 511-515.
27. Cabili, M.N., Trapnell, C., Goff, L., Koziol, M., Tazon-Vega, B., Regev, A. and Rinn, J.L. (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev., 25, 1915-1927.
28. ENCODE (2009) Post-transcriptional processing generates a diversity of 5'-modified long and short RNAs. Nature, 457, 1028-1032.
29. Sabo, P.J., Hawrylycz, M., Wallace, J.C., Humbert, R., Yu, M., Shafer, A., Kawamoto, J., Hall, R., Mack, J., Dorschner, M.O. et al. (2004) Discovery of functional noncoding elements by digital analysis of chromatin structure. Proc. Natl. Acad Sci. USA, 101, 16837-16842.
30. Sabo, P.J., Kuehn, M.S., Thurman, R., Johnson, B.E., Johnson, E.M., Cao, H., Yu, M., Rosenzweig, E., Goldy, J., Haydock, A. et al. (2006) Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat. Methods, 3, 511-518.
31. Baron, J.A., Cole, B.F., Sandler, R.S., Haile, R.W., Ahnen, D., Bresalier, R., McKeown-Eyssen, G., Summers, R.W., Rothstein, R., Burke, C.A. et al. (2003) A randomized trial of aspirin to prevent colorectal adenomas. New England J. Med., 348, 891-899.
32. Figueiredo, J.C., Grau, M.V., Wallace, K., Levine, A.J., Shen, L., Hamdan, R., Chen, X., Bresalier, R.S., McKeown-Eyssen, G., Haile, R.W. et al. (2009) Global DNA hypomethylation (LINE-1) in the normal colon and lifestyle characteristics and dietary and genetic factors. Cancer Epidemiol. Biomarkers Prevent., 18, 1041-1049.
33. Wallace, K., Grau, M.V., Levine, A.J., Shen, L., Hamdan, R., Chen, X., Gui, J., Haile, R.W., Barry, E.L., Ahnen, D. et al. (2010) Association between folate levels and CpG Island hypermethylation in normal colorectal mucosa. Cancer Prevent. Res., 3, 1552-1564.
34. Matys, V., Kel-Margoulis, O.V., Fricke, E., Liebich, I., Land, S., Barre-Dirrie, A., Reuter, I., Chekmenev, D., Krull, M., Hornischer, K. et al. (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res., 34, D108-D110.
35. Kel, A.E., Gossling, E., Reuter, I., Cheremushkin, E., Kel-Margoulis, O.V. and Wingender, E. (2003) MATCH: A tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res., 31, 3576-3579.
36. Freedman, M.L., Monteiro, A.N., Gayther, S.A., Coetzee, G.A., Risch, A., Plass, C., Casey, G., De Biasi, M., Carlson, C., Duggan, D. et al. (2011) Principles for the post-GWASfunctional characterization of cancer risk loci. Nat. Genet., 43, 513-518.
37. Sur, I., Tuupanen, S., Whitington, T., Aaltonen, L.A. and Taipale, J. (2013) Lessons from functional analysis of genome-wide association studies. Cancer Res., 73, 4180-4184.
38. Sur, I.K., Hallikas, O., Vaharautio, A., Yan, J., Turunen, M., Enge, M., Taipale, M., Karhu, A., Aaltonen, L.A. and Taipale, J. (2012) Mice lacking a Myc enhancer that includes human SNP rs6983267 are resistant to intestinal tumors. Science, 338, 1360-1363.
39. Bordon, A., Bosco, N., DuRoure, C., Bartholdy, B., Kohler, H., Matthias, G., Rolink, A.G. and Matthias, P. (2008) Enforced expression of the transcriptional coactivator OBF1 impairsB cell differentiation at the earliest stage of development. PloS ONE, 3, e4007.
40. Lee, C.C., Chen, W.S., Chen, C.C., Chen, L.L., Lin, Y.S., Fan, C.S. and Huang, T.S. (2012) TCF12 protein functions as transcriptional repressor of E-cadherin, and its overexpression is correlated with metastasis of colorectal cancer. J. Biol. Chem., 287, 2798-2809.
41. Peltekova, V.D., Lemire, M., Qazi, A.M., Zaidi, S.H., Trinh, Q.M., Bielecki, R., Rogers, M., Hodgson, L., Wang, M., D'Souza, D.J. et al. (2013) Identification of genes expressed by immune cells of the colon that are regulated by colorectal cancer-associated variants. Int. J. Cancer, doi: 10.1002/ijc.28557. [Epub ahead of print].
42. Ong, D.C., Ho, Y.M., Rudduck, C., Chin, K., Kuo, W.L., Lie, D.K., Chua, C.L., Tan, P.H., Eu, K.W., Seow-Choen, F. et al. (2009) LARG at chromosome 11q23 has functional characteristics of a tumor suppressor in human breast and colorectal cancer. Oncogene, 28, 4189-4200.
43. Niittymaki, I., Tuupanen, S., Li, Y., Jarvinen, H., Mecklin, J.P., Tomlinson, I.P., Houlston, R.S., Karhu, A. and Aaltonen, L.A. (2011) Systematic search for enhancer elements and somatic allelic imbalance at seven low-penetrance colorectal cancer predisposition loci. BMC Med. Genet., 12, 23.
44. Wijnen, J.T., Brohet, R.M., van Eijk, R., Jagmohan-Changur, S., Middeldorp, A., Tops, C.M., van Puijenbroek, M., Ausems, M.G., Gomez Garcia, E., Hes, F.J. et al. (2009) Chromosome 8q23.3 and 11q23.1 variants modify colorectal cancer risk in Lynch syndrome. Gastroenterology, 136, 131-137.
45. Talseth-Palmer, B.A., Brenne, I.S., Ashton, K.A., Evans, T.J., McPhillips, M., Groombridge, C., Suchy, J., Kurzawski, G., Spigelman, A., Lubinski, J. et al. (2012) Colorectal cancer susceptibility loci on chromosome8q23.3 and 11q23.1 as modifiers for disease expression in Lynch syndrome. J. Med. Genet., 48, 279-284.
46. Giraldez, M.D., Lopez-Doriga, A., Bujanda, L., Abuli, A., Bessa, X., Fernandez-Rozadilla, C., Munoz, J., Cuatrecasas, M., Jover, R., Xicola, R.M. et al. (2012) Susceptibility genetic variants associated with early-onset colorectal cancer. Carcinogenesis, 33, 613-619.
47. Yang, J., Zhang, W., Evans, P.M., Chen, X., He, X. and Liu, C. (2006) Adenomatous polyposis coli (APC) differentially regulates beta-catenin phosphorylation and ubiquitination in colon cancer cells. J. Biol. Chem., 281, 17751-17757.
48. Fields, S. (2007) Molecular biology. Site-seeing by sequencing. Science, 316, 1441-1442.
49. Johnson, D.S., Mortazavi, A., Myers, R.M. and Wold, B. (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science, 316, 1497-1502.
50. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
51. Li, Q.B., Brown, J.B., Huang, H. and Bickel, P.J. (2011) Measuring reproducibility of high-throughput experiments. Ann. Appl. Stat., 5, 1752-1779.
52. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W. et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol., 9, R137.
53. Holwerda, S.J.B. and de Laat, W. (2013) CTCF: the protein, the binding partners, the binding sites and their chromatin loops. Phil. Trans. R. Soc. B Biol. Sci., 368, 20120369.
54. Rubio, E.D., Reiss, D.J., Welcsh, P.L., Disteche, C.M., Filippova, G.N., Baliga, N.S., Aebersold, R., Ranish, J.A. and Krumm, A. (2008) CTCF physically links cohesin to chromatin. Proc. Natl. Acad. Sci. USA, 105, 8309-8314.
55. Hitchler, M.J. and Rice, J.C. (2011) Genome-wide epigenetic analysis of human pluripotent stem cells by ChIP and ChIP-Seq. Methods Mol. Biol., 767, 253-267.
56. Gonzalez, J.R., Armengol, L., Sole, X., Guino, E., Mercader, J.M., Estivill, X. and Moreno, V. (2007) SNPassoc: an R package to perform wholegenome association studies. Bioinformatics, 23, 644-645.