Multiple functional risk variants in a SMAD7 enhancer implicate a colorectal cancer risk haplotype

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Fortini, Barbara K ^a   Tring, Stephanie ^a   Plummer, Sarah J ^a   Edlund, Christopher K ^a   Moreno, Victor ^b   Bresalier, Robert S ^c   Barry, Elizabeth L ^d   Church, Timothy R ^e   Figueiredo, Jane C ^a   Casey, Graham ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

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

^d DARTMOUTH MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; TRANSFORMING GROWTH FACTOR BETA; BONE MORPHOGENETIC PROTEIN; SMAD7 PROTEIN; SMAD7 PROTEIN, HUMAN;

ALLELE; ARTICLE; CANCER RISK; CHROMOSOME 18Q; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; ENHANCER REGION; GENE; GENE EXPRESSION REGULATION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC RISK; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; HUMAN TISSUE; NEGATIVE FEEDBACK; PROTEIN BINDING; RISK ASSESSMENT; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SMAD7 GENE; CHROMOSOME 18; COLORECTAL TUMOR; GENETICS; HCT116 CELL LINE; HEK293 CELL LINE; METABOLISM; TUMOR CELL LINE;

BONE MORPHOGENETIC PROTEINS; CELL LINE, TUMOR; CHROMOSOMES, HUMAN, PAIR 18; COLORECTAL NEOPLASMS; ENHANCER ELEMENTS, GENETIC; GENETIC VARIATION; HCT116 CELLS; HEK293 CELLS; HUMANS; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, SINGLE NUCLEOTIDE; SIGNAL TRANSDUCTION; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84910126795     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0111914     Document Type: Article

References (40)

1. Principe DR, Doll JA, Bauer J, Jung B, Munshi HG, et al. (2014) TGF-beta: duality of function between tumor prevention and carcinogenesis. J Natl Cancer Inst 106: djt369.
2. Lampropoulos P, Zizi-Sermpetzoglou A, Rizos S, Kostakis A, Nikiteas N, et al. (2012) TGF-beta signalling in colon carcinogenesis. Cancer Lett 314: 1-7.
3. Derynck R, Miyazono KH (2007) The TGF-[beta] family: Cold Spring Harbor, N.YCold Spring Harbor Laboratory Press p p.
4. Bitzer M, von Gersdorff G, Liang D, Dominguez-Rosales A, Beg AA, et al. (2000) A mechanism of suppression of TGF-beta/SMAD signaling by NF-kappa B/RelA. Genes Dev 14: 187-197.
5. Ulloa L, Doody J, Massague J (1999) Inhibition of transforming growth factor-beta/SMAD signalling by the interferon-gamma/STAT pathway. Nature 397: 710-713.
6. Yan X, Liu Z, Chen Y (2009) Regulation of TGF-beta signaling by Smad7. Acta Biochim Biophys Sin (Shanghai) 41: 263-272.
7. Stolfi C, De Simone V, Colantoni A, Franze E, Ribichini E, et al. (2014) A functional role for Smad7 in sustaining colon cancer cell growth and survival. Cell Death Dis 5: e1073.
8. Broderick P, Carvajal-Carmona L, Pittman AM, Webb E, Howarth K, et al. (2007) A genome-wide association study shows that common alleles of SMAD7 influence colorectal cancer risk. Nat Genet 39: 1315-1317.
9. Tomlinson IP, Webb E, Carvajal-Carmona L, Broderick P, Howarth 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.
10. Tomlinson IP, Carvajal-Carmona LG, Dobbins SE, Tenesa A, Jones AM, et al. (2011) Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer. PLoS Genet 7: e1002105.
11. Tenesa A, Farrington SM, Prendergast JG, Porteous ME, Walker M, 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.
12. Peters U, Hutter CM, Hsu L, Schumacher FR, Conti DV, et al. (2012) Meta-analysis of new genome-wide association studies of colorectal cancer risk. Hum Genet 131: 217-234.
13. Peters U, Jiao S, Schumacher FR, Hutter CM, Aragaki AK, et al. (2013) Identification of Genetic Susceptibility Loci for Colorectal Tumors in a Genome-Wide Meta-analysis. Gastroenterology 144:799-807e724.
14. Houlston RS, Webb E, Broderick P, Pittman AM, Di Bernardo MC, et al. (2008) Meta-analysis of genome-wide association data identifies four new susceptibility loci for colorectal cancer. Nat Genet 40: 1426-1435.
15. Pittman AM, Naranjo S, Webb E, Broderick P, Lips EH, et al. (2009) The colorectal cancer risk at 18q21 is caused by a novel variant altering SMAD7 expression. Genome Res 19: 987-993.
16. Biancolella M, Fortini BK, Tring S, Plummer SJ, Mendoza-Fandino GA, et al. (2014) Identification and characterization of functional risk variants for colorectal cancer mapping to chromosome 11q23.1. Hum Mol Genet 23: 2198-2209.
17. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, et al. (2010) The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol 28: 1045-1048.
18. O'Geen H, Echipare L, Farnham PJ (2011) Using ChIP-seq technology to generate high-resolution profiles of histone modifications. Methods Mol Biol 791: 265-286.
19. ENCODE (2004) The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306: 636-640.
20. Sabo PJ, Kuehn MS, Thurman R, Johnson BE, Johnson EM, et al. (2006) Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat Methods 3: 511-518.
21. Sabo PJ, Hawrylycz M, Wallace JC, Humbert R, Yu M, et al. (2004) Discovery of functional noncoding elements by digital analysis of chromatin structure. Proc Natl Acad Sci U S A 101: 16837-16842.
22. Barrett JC (2009) Haploview: Visualization and analysis of SNP genotype data. Cold Spring Harb Protoc 2009:pdb ip71.
23. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263-265.
24. Kel AE, Gossling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, et al. (2003) MATCH: A tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res 31: 3576-3579.
25. Baron JA, Cole BF, Sandler RS, Haile RW, Ahnen D, et al. (2003) A randomized trial of aspirin to prevent colorectal adenomas. N Engl J Med 348: 891-899.
26. Figueiredo JC, Grau MV, Wallace K, Levine AJ, Shen L, et al. (2009) Global DNA hypomethylation (LINE-1) in the normal colon and lifestyle characteristics and dietary and genetic factors. Cancer Epidemiol Biomarkers Prev 18: 1041-1049.
27. Wallace K, Grau MV, Levine AJ, Shen L, Hamdan R, et al. (2010) Association between folate levels and CpG Island hypermethylation in normal colorectal mucosa. Cancer Prev Res (Phila) 3: 1552-1564.
28. Corradin O, Saiakhova A, Akhtar-Zaidi B, Myeroff L, Willis J, et al. (2014) Combinatorial effects of multiple enhancer variants in linkage disequilibrium dictate levels of gene expression to confer susceptibility to common traits. Genome Res 24: 1-13.
29. Hnisz D, Abraham BJ, Lee TI, Lau A, Saint-Andre V, et al. (2013) Super-enhancers in the control of cell identity and disease. Cell 155: 934-947.
30. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, et al. (2013) Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153: 307-319.
31. Parker SC, Stitzel ML, Taylor DL, Orozco JM, Erdos MR, et al. (2013) Chromatin stretch enhancer states drive cell-specific gene regulation and harbor human disease risk variants. Proc Natl Acad Sci U S A 110: 17921-17926.
32. Brodin G, Ahgren A, ten Dijke P, Heldin CH, Heuchel R (2000) Efficient TGF-beta induction of the Smad7 gene requires cooperation between AP-1, Sp1, and Smad proteins on the mouse Smad7 promoter. J Biol Chem 275: 29023-29030.
33. Benchabane H, Wrana JL (2003) GATA- and Smad1-dependent enhancers in the Smad7 gene differentially interpret bone morphogenetic protein concentrations. Mol Cell Biol 23: 6646-6661.
34. Rizzo A, Waldner MJ, Stolfi C, Sarra M, Fina D, et al. (2011) Smad7 expression in T cells prevents colitis-associated cancer. Cancer Res 71: 7423-7432.
35. Rizzo A, De Mare V, Rocchi C, Stolfi C, Colantoni A, et al. (2014) Smad7 induces plasticity in tumor-infiltrating Th17 cells and enables TNF-alpha-mediated killing of colorectal cancer cells. Carcinogenesis.
36. Gulubova M, Manolova I, Ananiev J, Julianov A, Yovchev Y, et al. (2010) Role of TGF-beta1, its receptor TGFbetaRII, and Smad proteins in the progression of colorectal cancer. Int J Colorectal Dis 25: 591-599.
37. Whiffin N, Dobbins SE, Hosking FJ, Palles C, Tenesa A, et al. (2013) Deciphering the genetic architecture of low-penetrance susceptibility to colorectal cancer. Hum Mol Genet 22: 5075-5082.
38. Jia L, Landan G, Pomerantz M, Jaschek R, Herman P, et al. (2009) Functional enhancers at the gene-poor 8q24 cancer-linked locus. PLoS Genet 5: e1000597.
39. Andersen CL, Jensen JL, Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64: 5245-5250.
40. LaVange LM, Koch GG (2006) Rank score tests. Circulation 114: 2528-2533.