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Common genetic variants (rs4779584 and rs10318) at 15q13.3 contributes to colorectal adenoma and colorectal cancer susceptibility: evidence based on 22 studies

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Abstract

Several genome-wide association studies on colorectal cancer (CRC) have reported similar findings of a new susceptibility locus, 15q13.3. After that, a number of studies have reported that the rs4779584 and rs10318 polymorphisms at chromosome 15q13.3 have been implicated in CRC and colorectal adenoma (CRA) risk; however, these studies have yielded inconsistent results. To investigate this inconsistency, we performed a meta-analysis of 22 studies involving a total of 48,468 CRC cases, 4,189 CRA cases, and 85,105 controls for the two polymorphisms to evaluate its effect on genetic susceptibility for CRC/CRA. Potential sources of heterogeneity and publication bias were also systematically explored. Overall, the summary odds ratio (OR) of rs4779584-T variant for CRC was 1.13 (95 % CI 1.09–1.16, P < 10−5) and 1.15 (95 % CI 1.04–1.28, P = 0.006) for CRA. After stratified by ethnicity, significantly increased CRC risks were found for rs4779584 polymorphism among East Asians and Caucasians, while no significant associations were detected among African American and other ethnic populations. A meta-analysis of studies on the rs10318 polymorphism also showed significant overall association with CRC, yielding a per-allele OR of 1.13 (95 % CI 1.02–1.24, P = 0.02). In the subgroup analysis by ethnicity, significantly increased CRC risks were found in Caucasians; whereas no significant associations were found among East Asians and African Americans. This meta-analysis demonstrated that the rs4779584 and rs10318 polymorphism at 15q13.3 is a risk factor associated with increased CRC/CRA susceptibility, but these associations vary in different ethnic populations.

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References

  • Aaltonen LA, Salovaara R, Kristo P, Canzian F, Hemminki A, Peltomäki P, Chadwick RB, Kääriäinen H, Eskelinen M, Järvinen H, Mecklin JP, de la Chapelle A (1998) Incidence of hereditary non-polyposis colorectal cancer and the feasibility of molecular screening for the disease. N Engl J Med 338:1481–1487

    Article  CAS  PubMed  Google Scholar 

  • Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101

    Article  CAS  PubMed  Google Scholar 

  • Broderick P, Carvajal-Carmona L, Pittman AM, Webb E, Howarth K, Rowan A, Lubbe S, Spain S, Sullivan K, Fielding S, Jaeger E, Vijayakrishnan J, Kemp Z, Gorman M, Chandler I, Papaemmanuil E, Penegar S, Wood W, Sellick G, Qureshi M, Teixeira A, Domingo E, Barclay E, Martin L, Sieber O, Consortium CORGI, Kerr D, Gray R, Peto J, Cazier JB, Tomlinson I, Houlston RS (2007) A genome-wide association study shows that common alleles of SMAD7 influence colorectal cancer risk. Nat Genet 39:1315–1317

    Article  CAS  PubMed  Google Scholar 

  • Carvajal-Carmona LG (2010) Challenges in the identification and use of rare disease-associated predisposition variants. Curr Opin Genet Dev 20:277–281

    Article  CAS  PubMed  Google Scholar 

  • Carvajal-Carmona LG, Zauber AG, Jones AM, Howarth K, Wang J, Cheng T, APC Trial Collaborators; APPROVe Trial Collaborators; CORGI Study Collaborators; Colon Cancer Family Registry Collaborators; CGEMS Collaborators, Riddell R, Lanas A, Morton D, Bertagnolli MM, Tomlinson I (2013) Much of the genetic risk of colorectal cancer is likely to be mediated through susceptibility to adenomas. Gastroenterology 144:53–55

    Article  PubMed Central  PubMed  Google Scholar 

  • Cochran WG (1954) The combination of estimates from different experiments. Biometrics 10:101–129

    Article  Google Scholar 

  • Daley D, Lewis S, Platzer P, MacMillen M, Willis J, Elston RC, Markowitz SD, Wiesner GL (2008) Identification of susceptibility genes for cancer in a genome-wide scan: results from the colon neoplasia sibling study. Am J Hum Genet 82:723–736

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • de Jong MM, Nolte IM, te Meerman GJ, van der Graaf WT, de Vries EG, Sijmons RH, Hofstra RM, Kleibeuker JH (2002) Low-penetrance genes and their involvement in colorectal cancer susceptibility. Cancer Epidemiol Biomark Prev 11:1332–1352

    Google Scholar 

  • de la Chapelle A (2004) Genetic predisposition to colorectal cancer. Nat Rev Cancer 4:769–780

    Article  PubMed  Google Scholar 

  • Dunlop MG, Dobbins SE, Farrington SM, Jones AM, Palles C, Whiffin N, Tenesa A, Spain S, Broderick P, Ooi LY, Domingo E, Smillie C, Henrion M, Frampton M, Martin L, Grimes G, Gorman M, Semple C, Ma YP, Barclay E, Prendergast J, Cazier JB, Olver B, Penegar S, Lubbe S, Chander I, Carvajal-Carmona LG, Ballereau S, Lloyd A, Vijayakrishnan J, Zgaga L, Rudan I, Theodoratou E, Colorectal Tumour Gene Identification (CORGI) Consortium, Starr JM, Deary I, Kirac I, Kovacević D, Aaltonen LA, Renkonen-Sinisalo L, Mecklin JP, Matsuda K, Nakamura Y, Okada Y, Gallinger S, Duggan DJ, Conti D, Newcomb P, Hopper J, Jenkins MA, Schumacher F, Casey G, Easton D, Shah M, Pharoah P, Lindblom A, Liu T, Swedish Low-Risk Colorectal Cancer Study Group, Smith CG, West H, Cheadle JP, Midgley R, Kerr DJ, Campbell H, Tomlinson IP, Houlston RS (2012) Common variation near CDKN1A, POLD3 and SHROOM2 influences colorectal cancer risk. Nat Genet 44:770–776

    Article  CAS  PubMed  Google Scholar 

  • Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • He J, Wilkens LR, Stram DO, Kolonel LN, Henderson BE, Wu AH, Le Marchand L, Haiman CA (2011) Generalizability and epidemiologic characterization of eleven colorectal cancer GWAS hits in multiple populations. Cancer Epidemiol Biomark Prev 20:70–81

    Article  CAS  Google Scholar 

  • Hemminki K, Lorenzo Bermejo J, Försti A (2006) The balance between heritable and environmental aetiology of human disease. Nat Rev Genet 7:958–965

    Article  CAS  PubMed  Google Scholar 

  • Hes FJ, Ruano D, Nieuwenhuis M, Tops CM, Schrumpf M, Nielsen M, Huijts PE, Wijnen JT, Wagner A, Gómez García EB, Sijmons RH, Menko FH, Letteboer TG, Hoogerbrugge N, Harryvan J, Kampman E, Morreau H, Vasen HF, van Wezel T (2014) Colorectal cancer risk variants on 11q23 and 15q13 are associated with unexplained adenomatous polyposis. J Med Genet 51:55–60

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hiripi E, Bermejo JL, Sundquist J, Hemminki K (2008) Association of colorectal adenoma with other malignancies in Swedish families. Br J Cancer 98:997–1000

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ho JW, Choi SC, Lee YF, Hui TC, Cherny SS, Garcia-Barceló MM, Carvajal-Carmona L, Liu R, To SH, Yau TK, Chung CC, Yau CC, Hui SM, Lau PY, Yuen CH, Wong YW, Ho S, Fung SS, Tomlinson IP, Houlston RS, Cheng KK, Sham PC (2011) Replication study of SNP associations for colorectal cancer in Hong Kong Chinese. Br J Cancer 104:369–375

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hong SN, Park CH, Kim JI, Kim DH, Kim HC, Chang DK, Rhee PL, Kim JJ, Rhee JC, Son HJ, Kim YH (2014) Colorectal Cancer-Susceptibility Single Nucleotide Polymorphisms in Korean Population. J Gastroenterol Hepatol. doi:10.1111/jgh.12231

    Google Scholar 

  • Houlston RS, Webb E, Broderick P, Pittman AM, Di Bernardo MC, Lubbe S, Chandler I, Vijayakrishnan J, Sullivan K, Penegar S, Colorectal Cancer Association Study Consortium, Carvajal-Carmona L, Howarth K, Jaeger E, Spain SL, Walther A, Barclay E, Martin L, Gorman M, Domingo E, Teixeira AS, CoRGI Consortium, Kerr D, Cazier JB, Niittymäki I, Tuupanen S, Karhu A, Aaltonen LA, Tomlinson IP, Farrington SM, Tenesa A, Prendergast JG, Barnetson RA, Cetnarskyj R, Porteous ME, Pharoah PD, Koessler T, Hampe J, Buch S, Schafmayer C, Tepel J, Schreiber S, Völzke H, Chang-Claude J, Hoffmeister M, Brenner H, Zanke BW, Montpetit A, Hudson TJ, Gallinger S, International Colorectal Cancer Genetic Association Consortium, Campbell H, Dunlop MG (2008) Meta-analysis of genome-wide association data identifies four new susceptibility loci for colorectal cancer. Nat Genet 40:1426–1435

    Article  CAS  PubMed  Google Scholar 

  • Houlston RS, Cheadle J, Dobbins SE, Tenesa A, Jones AM, Howarth K, Spain SL, Broderick P, Domingo E, Farrington S, Prendergast JG, Pittman AM, Theodoratou E, Smith CG, Olver B, Walther A, Barnetson RA, Churchman M, Jaeger EE, Penegar S, Barclay E, Martin L, Gorman M, Mager R, Johnstone E, Midgley R, Niittymäki I, Tuupanen S, Colley J, Idziaszczyk S, COGENT Consortium, Thomas HJ, Lucassen AM, Evans DG, Maher ER, CORGI Consortium; COIN Collaborative Group; COINB Collaborative Group, Maughan T, Dimas A, Dermitzakis E, Cazier JB, Aaltonen LA, Pharoah P, Kerr DJ, Carvajal-Carmona LG, Campbell H, Dunlop MG, Tomlinson IP (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

    Article  CAS  PubMed  Google Scholar 

  • Huxley RR, Ansary-Moghaddam A, Clifton P, Czernichow S, Parr CL, Woodward M (2009) The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer 125:171–180

    Article  CAS  PubMed  Google Scholar 

  • Ioannidis JP, Boffetta P, Little J, O’Brien TR, Uitterlinden AG, Vineis P, Balding DJ, Chokkalingam A, Dolan SM, Flanders WD, Higgins JP, McCarthy MI, McDermott DH, Page GP, Rebbeck TR, Seminara D, Khoury MJ (2008) Assessment of cumulative evidence on genetic associations: interim guidelines. Int J Epidemiol 37:120–132

    Article  PubMed  Google Scholar 

  • Jaeger E, Webb E, Howarth K, Carvajal-Carmona L, Rowan A, Broderick P, Walther A, Spain S, Pittman A, Kemp Z, Sullivan K, Heinimann K, Lubbe S, Domingo E, Barclay E, Martin L, Gorman M, Chandler I, Vijayakrishnan J, Wood W, Papaemmanuil E, Penegar S, Qureshi M, CORGI Consortium, Farrington S, Tenesa A, Cazier JB, Kerr D, Gray R, Peto J, Dunlop M, Campbell H, Thomas H, Houlston R, Tomlinson I (2008) Common genetic variants at the CRAC1 (HMPS) locus on chromosome 15q13.3 influence colorectal cancer risk. Nat Genet 40:26–28

    Article  CAS  PubMed  Google Scholar 

  • Jaeger E, Leedham S, Lewis A, Segditsas S, Becker M, Cuadrado PR, Davis H, Kaur K, Heinimann K, Howarth K, East J, Taylor J, Thomas H, Tomlinson I (2012) 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 44:699–703

    Article  CAS  PubMed  Google Scholar 

  • Jarvinen HJ (1992) Epidemiology of familial adenomatous polyposis in Finland: impact of family screening on the colorectal cancer rate and survival. Gut 33:357–360

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jemal A, Siegel R, Xu J, Ward E (2010) Cancer statistics, 2010. CA Cancer J Clin 60:277–300

    Article  PubMed  Google Scholar 

  • Kupfer SS, Anderson JR, Hooker S, Skol A, Kittles RA, Keku TO, Sandler RS, Ellis NA (2010) Genetic heterogeneity in colorectal cancer associations between African and European americans. Gastroenterology 139:1677–1685 1685.e1-8

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kurlapska A, Serrano-Fernández P, Baszuk P, Gupta S, Starzyńska T, Małecka-Panas E, Dabrowski A, Dębniak T, Kurzawski G, Suchy J, Rogoza-Mateja W, Scott RJ, Lubiński J (2014) Cumulative effects of genetic markers and the detection of advanced colorectal neoplasias by population screening. Clin Genet. doi:10.1111/cge.12481

    PubMed  Google Scholar 

  • Larsson SC, Wolk A (2006) Meat consumption and risk of colorectal cancer: a meta-analysis of prospective studies. Int J Cancer 119:2657–2664

    Article  CAS  PubMed  Google Scholar 

  • Li M, Gu Y (2014) Quantitative assessment of the influence of common variation rs16892766 at 8q23.3 with colorectal adenoma and cancer susceptibility. Mol Genet Genomics doi:10.1007/s00438-014-0928-z

  • Lichtenstein P, Holm NV, Verkasalo PK, Iliadou A, Kaprio J, Koskenvuo M, Pukkala E, Skytthe A, Hemminki K (2000) Environmental and heritable factors in the causation of cancer—analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med 343:78–85

    Article  CAS  PubMed  Google Scholar 

  • Middeldorp A, Jagmohan-Changur S, van Eijk R, Tops C, Devilee P, Vasen HF, Hes FJ, Houlston R, Tomlinson I, Houwing-Duistermaat JJ, Wijnen JT, Morreau H, van Wezel T (2009) Enrichment of low penetrance susceptibility loci in a Dutch familial colorectal cancer cohort. Cancer Epidemiol Biomark Prev 18:3062–3067

    Article  CAS  Google Scholar 

  • Mulder JW, Offerhaus GJ, de Feyter EP, Floyd JJ, Kern SE, Vogelstein B, Hamilton SR (1992) The relationship of quantitative nuclear morphology to molecular genetic alterations in the adenoma-carcinoma sequence of the large bowel. Am J Pathol 141:797–804

    PubMed Central  CAS  PubMed  Google Scholar 

  • Peters U, Hutter CM, Hsu L, Schumacher FR, Conti DV, Carlson CS, Edlund CK, Haile RW, Gallinger S, Zanke BW, Lemire M, Rangrej J, Vijayaraghavan R, Chan AT, Hazra A, Hunter DJ, Ma J, Fuchs CS, Giovannucci EL, Kraft P, Liu Y, Chen L, Jiao S, Makar KW, Taverna D, Gruber SB, Rennert G, Moreno V, Ulrich CM, Woods MO, Green RC, Parfrey PS, Prentice RL, Kooperberg C, Jackson RD, Lacroix AZ, Caan BJ, Hayes RB, Berndt SI, Chanock SJ, Schoen RE, Chang-Claude J, Hoffmeister M, Brenner H, Frank B, Bézieau S, Küry S, Slattery ML, Hopper JL, Jenkins MA, Le Marchand L, Lindor NM, Newcomb PA, Seminara D, Hudson TJ, Duggan DJ, Potter JD, Casey G (2012) Meta-analysis of new genome-wide association studies of colorectal cancer risk. Hum Genet 131:217–234

    Article  PubMed Central  PubMed  Google Scholar 

  • Risch N, Merikangas K (1996) The future of genetic studies of complex human diseases. Science 73:1516–1517

    Article  Google Scholar 

  • Salovaara R, Loukola A, Kristo P, Kääriäinen H, Ahtola H, Eskelinen M, Härkönen N, Julkunen R, Kangas E, Ojala S, Tulikoura J, Valkamo E, Järvinen H, Mecklin JP, Aaltonen LA, de la Chapelle A (2000) Population-based molecular detection of hereditary nonpolyposis colorectal cancer. J Clin Oncol 18:2193–2200

    CAS  PubMed  Google Scholar 

  • Sneddon JB, Zhen HH, Montgomery K, van de Rijn M, Tward AD, West R, Gladstone H, Chang HY, Morganroth GS, Oro AE, Brown PO (2006) Bone morphogenetic protein antagonist gremlin 1 is widely expressed by cancer-associated stromal cells and can promote tumor cell proliferation. Proc Natl Acad Sci USA 103:14842–14847

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stryker SJ, Wolff BG, Culp CE, Libbe SD, Ilstrup DM, MacCarty RL (1987) Natural history of untreated colonic polyps. Gastroenterology 93:1009–1013

    CAS  PubMed  Google Scholar 

  • Talseth-Palmer BA, Brenne IS, Ashton KA, Evans TJ, McPhillips M, Groombridge C, Suchy J, Kurzawski G, Spigelman A, Lubinski J, Scott RJ (2011) Colorectal cancer susceptibility loci on chromosome 8q23.3 and 11q23.1 as modifiers for disease expression in lynch syndrome. J Med Genet 48:279–284

    Article  CAS  PubMed  Google Scholar 

  • Talseth-Palmer BA, Wijnen JT, Brenne IS, Jagmohan-Changur S, Barker D, Ashton KA, Tops CM, Evans TJ, McPhillips M, Groombridge C, Suchy J, Kurzawski G, Dutch Cancer Genetics Group, Spigelman A, Møller P, Morreau HM, Van Wezel T, Lubinski J, Vasen HF, Scott RJ (2013) Combined analysis of three Lynch syndrome cohorts confirms the modifying effects of 8q23.3 and 11q23.1 in MLH1 mutation carriers. Int J Cancer 132:1556–1564

    Article  CAS  PubMed  Google Scholar 

  • Tenesa A, Farrington SM, Prendergast JG, Porteous ME, Walker M, Haq N, Barnetson RA, Theodoratou E, Cetnarskyj R, Cartwright N, Semple C, Clark AJ, Reid FJ, Smith LA, Kavoussanakis K, Koessler T, Pharoah PD, Buch S, Schafmayer C, Tepel J, Schreiber S, Völzke H, Schmidt CO, Hampe J, Chang-Claude J, Hoffmeister M, Brenner H, Wilkening S, Canzian F, Capella G, Moreno V, Deary IJ, Starr JM, Tomlinson IP, Kemp Z, Howarth K, Carvajal-Carmona L, Webb E, Broderick P, Vijayakrishnan J, Houlston RS, Rennert G, Ballinger D, Rozek L, Gruber SB, Matsuda K, Kidokoro T, Nakamura Y, Zanke BW, Greenwood CM, Rangrej J, Kustra R, Montpetit A, Hudson TJ, Gallinger S, Campbell H, Dunlop MG (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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thean LF, Li HH, Teo YY, Koh WP, Yuan JM, Teoh ML, Koh PK, Tang CL, Cheah PY (2012) Association of Caucasian-identified variants with colorectal cancer risk in Singapore Chinese. PLoS ONE 7:e42407

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tomlinson I, Rahman N, Frayling I, Mangion J, Barfoot R, Hamoudi R, Seal S, Northover J, Thomas HJ, Neale K, Hodgson S, Talbot I, Houlston R, Stratton MR (1999) Inherited susceptibility to colorectal adenomas and carcinomas: evidence for a new predisposition gene on 15q14-q22. Gastroenterology 116:789–795

    Article  CAS  PubMed  Google Scholar 

  • Tomlinson I, Webb E, Carvajal-Carmona L, Broderick P, Kemp Z, Spain S, Penegar S, Chandler I, Gorman M, Wood W, Barclay E, Lubbe S, Martin L, Sellick G, Jaeger E, Hubner R, Wild R, Rowan A, Fielding S, Howarth K, CORGI Consortium, Silver A, Atkin W, Muir K, Logan R, Kerr D, Johnstone E, Sieber O, Gray R, Thomas H, Peto J, Cazier JB, Houlston R (2007) A genome-wide association scan of tag SNPs identifies a susceptibility variant for colorectal cancer at 8q24.21. Nat Genet 39:984–988

    Article  CAS  PubMed  Google Scholar 

  • Tomlinson IP, Carvajal-Carmona LG, Dobbins SE, Tenesa A, Jones AM, Howarth K, Palles C, Broderick P, Jaeger EE, Farrington S, Lewis A, Prendergast JG, Pittman AM, Theodoratou E, Olver B, Walker M, Penegar S, Barclay E, Whiffin N, Martin L, Ballereau S, Lloyd A, Gorman M, Lubbe S, COGENT Consortium; CORGI Collaborators; EPICOLON Consortium, Howie B, Marchini J, Ruiz-Ponte C, Fernandez-Rozadilla C, Castells A, Carracedo A, Castellvi-Bel S, Duggan D, Conti D, Cazier JB, Campbell H, Sieber O, Lipton L, Gibbs P, Martin NG, Montgomery GW, Young J, Baird PN, Gallinger S, Newcomb P, Hopper J, Jenkins MA, Aaltonen LA, Kerr DJ, Cheadle J, Pharoah P, Casey G, Houlston RS, Dunlop MG (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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • von Holst S, Picelli S, Edler D, Lenander C, Dalén J, Hjern F, Lundqvist N, Lindforss U, Påhlman L, Smedh K, Törnqvist A, Holm J, Janson M, Andersson M, Ekelund S, Olsson L, Ghazi S, Papadogiannakis N, Tenesa A, Farrington SM, Campbell H, Dunlop MG, Lindblom A (2010) Association studies on 11 published colorectal cancer risk loci. Br J Cancer 103:575–580

    Article  Google Scholar 

  • Wakefield JA (2007) Bayesian measure of the probability of false discovery in genetic epidemiology studies. Am J Hum Genet 81:208–227

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang H, Haiman CA, Burnett T, Fortini BK, Kolonel LN, Henderson BE, Signorello LB, Blot WJ, Keku TO, Berndt SI, Newcomb PA, Pande M, Amos CI, West DW, Casey G, Sandler RS, Haile R, Stram DO, Le Marchand L (2013) Fine-mapping of genome-wide association study-identified risk loci for colorectal cancer in African Americans. Hum Mol Genet 22:5048–5055

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang H, Burnett T, Kono S, Haiman CA, Iwasaki M, Wilkens LR, Loo LW, Van Den Berg D, Kolonel LN, Henderson BE, Keku TO, Sandler RS, Signorello LB, Blot WJ, Newcomb PA, Pande M, Amos CI, West DW, Bézieau S, Berndt SI, Zanke BW, Hsu L, Genetics and Epidemiology of Colorectal Cancer Consortium (GECCO), Lindor NM, Haile RW, Hopper JL, Jenkins MA, Gallinger S, Casey G, Colon Cancer Family Registry (CCFR), Stenzel SL, Schumacher FR, Peters U, Gruber SB, Colorectal Transdisciplinary Study (CORECT), Tsugane S, Stram DO, Le Marchand L (2014) Trans-ethnic genome-wide association study of colorectal cancer identifies a new susceptibility locus in VTI1A. Nat Commun 8(5):461

    Google Scholar 

  • Winawer SJ, Zauber AG, Ho MN, O’Brien MJ, Gottlieb LS, Sternberg SS, Waye JD, Schapiro M, Bond JH, Panish JF, Ackroyd F, Shike M, Kurtz RC, Hornsby-Lewis L, Gerdes H, Stewart ET, The National Polyp Study Workgroup (1993) Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. N Engl J Med 329:1977–1981

    Article  CAS  PubMed  Google Scholar 

  • Woolf B (1955) On estimating the relation between blood group and disease. Ann Hum Genet 19:251–253

    Article  CAS  PubMed  Google Scholar 

  • Wordinger RJ, Zode G, Clark AF (2008) Focus on molecules: gremlin. Exp Eye Res 87:78–79

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong F, Wu C, Bi X, Yu D, Huang L, Xu J, Zhang T, Zhai K, Chang J, Tan W, Cai J, Lin D (2010) Risk of genome-wide association study-identified genetic variants for colorectal cancer in a Chinese population. Cancer Epidemiol Biomark Prev 19:1855–1861

    Article  CAS  Google Scholar 

  • Yang CY, Lu RH, Lin CH, Jen CH, Tung CY, Yang SH, Lin JK, Jiang JK, Lin CH (2014) Single nucleotide polymorphisms associated with colorectal cancer susceptibility and loss of heterozygosity in a taiwanese population. PLoS ONE 9:e100060

    Article  PubMed Central  PubMed  Google Scholar 

  • Zanke BW, Greenwood CM, Rangrej J, Kustra R, Tenesa A, Farrington SM, Prendergast J, Olschwang S, Chiang T, Crowdy E, Ferretti V, Laflamme P, Sundararajan S, Roumy S, Olivier JF, Robidoux F, Sladek R, Montpetit A, Campbell P, Bezieau S, O’Shea AM, Zogopoulos G, Cotterchio M, Newcomb P, McLaughlin J, Younghusband B, Green R, Green J, Porteous ME, Campbell H, Blanche H, Sahbatou M, Tubacher E, Bonaiti-Pellié C, Buecher B, Riboli E, Kury S, Chanock SJ, Potter J, Thomas G, Gallinger S, Hudson TJ, Dunlop MG (2007) Genome-wide association scan identifies a colorectal cancer susceptibility locus on chromosome 8q24. Nat Genet 39:989–994

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Shrubsole MJ, Li G, Cai Q, Edwards T, Smalley WE, Ness RM, Zheng W (2012) Association of genetic variants for colorectal cancer differs by subtypes of polyps in the colorectum. Carcinogenesis 33:2417–2423

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang B, Jia WH, Matsuda K, Kweon SS, Matsuo K, Xiang YB, Shin A, Jee SH, Kim DH, Cai Q, Long J, Shi J, Wen W, Yang G, Zhang Y, Li C, Li B, Guo Y, Ren Z, Ji BT, Pan ZZ, Takahashi A, Shin MH, Matsuda F, Gao YT, Oh JH, Kim S, Ahn YO, Genetics and Epidemiology of Colorectal Cancer Consortium (GECCO), Chan AT, Chang-Claude J, Slattery ML, Colorectal Transdisciplinary (CORECT) Study, Gruber SB, Schumacher FR, Stenzel SL, Colon Cancer Family Registry (CCFR), Casey G, Kim HR, Jeong JY, Park JW, Li HL, Hosono S, Cho SH, Kubo M, Shu XO, Zeng YX, Zheng W (2014) Large-scale genetic study in East Asians identifies six new loci associated with colorectal cancer risk. Nat Genet 46:533–542

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao DP, Yang CL, Zhou X, Ding JA, Jiang GN (2014) Association between CLPTM1L polymorphisms (rs402710 and rs401681) and lung cancer susceptibility: evidence from 27 case-control studies. Mol Genet Genomics 289:1001–1012

    Article  CAS  PubMed  Google Scholar 

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  1. Department of General Surgery Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, 1630 Dongfang Road, Shanghai, 200127, People’s Republic of China

    Lin Tu

  2. Department of General Surgery, Qingpu Branch of Zhongshan Hospital, Fudan University, 1158 East Gongyuan Road, Shanghai, 201700, People’s Republic of China

    Bin Yan & Zhiyong Peng

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Correspondence to Zhiyong Peng.

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Communicated by S. Hohmann.

L. Tu and B. Yan contributed equally to this work.

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Tu, L., Yan, B. & Peng, Z. Common genetic variants (rs4779584 and rs10318) at 15q13.3 contributes to colorectal adenoma and colorectal cancer susceptibility: evidence based on 22 studies. Mol Genet Genomics 290, 901–912 (2015). https://doi.org/10.1007/s00438-014-0970-x

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