Whole-Exome Sequencing Analyses of Inflammatory Bowel Disease-Associated Colorectal Cancers

Gastroenterology

Volumn 150, Issue 4, 2016, Pages 931-943

  Robles, Ana I ^a   Traverso, Giovanni ^b,c   Zhang, Ming ^d   Roberts, Nicholas J ^d,e   Khan, Mohammed A ^a   Joseph, Christine ^d   Lauwers, Gregory Y ^b   Selaru, Florin M ^e   Popoli, Maria ^d   Pittman, Meredith E ^e   Ke, Xiquan ^e   Hruban, Ralph H ^e   Meltzer, Stephen J ^e   Kinzler, Kenneth W ^d,g   Vogelstein, Bert ^d,f,g   Harris, Curtis C ^a   Papadopoulos, Nickolas ^d,g  

^a NATIONAL CANCER INSTITUTE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Crohn's Disease; Exome; Sequencing; Ulcerative Colitis

Indexed keywords

APC PROTEIN; DNA; E1A ASSOCIATED P300 PROTEIN; INTERLEUKIN 16; K RAS PROTEIN; NRG1 PROTEIN; POLE PROTEIN; PROTEIN; PROTEIN MLH1; PROTEIN MSH6; PROTEIN P53; RAC PROTEIN; RHO FACTOR; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; TUMOR MARKER;

ARTICLE; CLINICAL ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; COPY NUMBER VARIATION; CROHN DISEASE; DNA SEQUENCE; EXOME; FRAMESHIFT MUTATION; GENE AMPLIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MISMATCH REPAIR; MISSENSE MUTATION; MOLECULAR PATHOLOGY; MUTATION RATE; PREVALENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SOMATIC MUTATION; ULCERATIVE COLITIS; WNT SIGNALING PATHWAY; CELL TRANSFORMATION; COLITIS, ULCERATIVE; COLORECTAL NEOPLASMS; COMPLICATION; DNA MUTATIONAL ANALYSIS; GENE DOSAGE; GENE FREQUENCY; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MUTATION; PHENOTYPE;

BIOMARKERS, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; COLITIS, ULCERATIVE; COLORECTAL NEOPLASMS; CROHN DISEASE; DNA COPY NUMBER VARIATIONS; DNA MUTATIONAL ANALYSIS; EXOME; GENE DOSAGE; GENE FREQUENCY; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MUTATION; PHENOTYPE;

EID: 84962921222     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2015.12.036     Document Type: Article

References (98)

1. J.A. Eaden, K.R. Abrams, and J.F. Mayberry The risk of colorectal cancer in ulcerative colitis: a meta-analysis Gut 48 2001 526 535
2. T. Jess, E.V. Loftus Jr., F.S. Velayos, and et al. Incidence and prognosis of colorectal dysplasia in inflammatory bowel disease: a population-based study from Olmsted County, Minnesota Inflamm Bowel Dis 12 2006 669 676
3. V. Andersen, J. Halfvarson, and U. Vogel Colorectal cancer in patients with inflammatory bowel disease: can we predict risk? World J Gastroenterol 18 2012 4091 4094
4. L.J. Herrinton, L. Liu, T.R. Levin, and et al. Incidence and mortality of colorectal adenocarcinoma in persons with inflammatory bowel disease from 1998 to 2010 Gastroenterology 143 2012 382 389
5. B. Levin, D.A. Lieberman, B. McFarland, and et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology Gastroenterology 134 2008 1570 1595
6. F.A. Farraye, R.D. Odze, J. Eaden, and et al. AGA technical review on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease Gastroenterology 138 2010 746 774
7. A.N. Ananthakrishnan, A. Cagan, T. Cai, and et al. Colonoscopy is associated with a reduced risk for colon cancer and mortality in patients with inflammatory bowel diseases Clin Gastroenterol Hepatol 13 2015 322 329
8. C.E. Rubin, R.C. Haggitt, G.C. Burmer, and et al. DNA aneuploidy in colonic biopsies predicts future development of dysplasia in ulcerative colitis Gastroenterology 103 1992 1611 1620
9. S. Soderlund, B. Tribukait, A. Ost, and et al. Colitis-associated DNA aneuploidy and dysplasia in Crohn's disease and risk of colorectal cancer Inflamm Bowel Dis 17 2011 1101 1107
10. D.A. Ahlquist, J.E. Skoletsky, K.A. Boynton, and et al. Colorectal cancer screening by detection of altered human DNA in stool: feasibility of a multitarget assay panel Gastroenterology 119 2000 1219 1227
11. G. Traverso, A. Shuber, B. Levin, and et al. Detection of APC mutations in fecal DNA from patients with colorectal tumors N Engl J Med 346 2002 311 320
12. D.A. Ahlquist, H. Zou, M. Domanico, and et al. Next-generation stool DNA test accurately detects colorectal cancer and large adenomas Gastroenterology 142 2012 248 256
13. C. Bettegowda, M. Sausen, R.J. Leary, and et al. Detection of circulating tumor DNA in early- and late-stage human malignancies Sci Transl Med 6 2014 224ra224
14. B.J. Druker, C.L. Sawyers, H. Kantarjian, and et al. Activity of a specific inhibitor of the BCR-ABL tyrosine kinase in the blast crisis of chronic myeloid leukemia and acute lymphoblastic leukemia with the Philadelphia chromosome N Engl J Med 344 2001 1038 1042
15. S.E. Kern, M. Redston, A.B. Seymour, and et al. Molecular genetic profiles of colitis-associated neoplasms Gastroenterology 107 1994 420 428
16. L. Tarmin, J. Yin, N. Harpaz, and et al. Adenomatous polyposis coli gene mutations in ulcerative colitis-associated dysplasias and cancers versus sporadic colon neoplasms Cancer Res 55 1995 2035 2038
17. N. Umetani, S. Sasaki, T. Watanabe, and et al. Genetic alterations in ulcerative colitis-associated neoplasia focusing on APC, K-ras gene and microsatellite instability Jpn J Cancer Res 90 1999 1081 1087
18. S.J. Meltzer, S.M. Mane, P.K. Wood, and et al. Activation of c-Ki-ras in human gastrointestinal dysplasias determined by direct sequencing of polymerase chain reaction products Cancer Res 50 1990 3627 3630
19. G.C. Burmer, D.S. Levine, B.G. Kulander, and et al. c-Ki-ras mutations in chronic ulcerative colitis and sporadic colon carcinoma Gastroenterology 99 1990 416 420
20. G.C. Burmer, P.S. Rabinovitch, and L.A. Loeb Frequency and spectrum of c-Ki-ras mutations in human sporadic colon carcinoma, carcinomas arising in ulcerative colitis, and pancreatic adenocarcinoma Environ Health Perspect 93 1991 27 31
21. S.M. Bell, S.A. Kelly, J.A. Hoyle, and et al. c-Ki-ras gene mutations in dysplasia and carcinomas complicating ulcerative colitis Br J Cancer 64 1991 174 178
22. H. van Dekken, J.C. Wink, K.J. Vissers, and et al. Wnt pathway-related gene expression during malignant progression in ulcerative colitis Acta Histochem 109 2007 266 272
23. M.M. Claessen, M.E. Schipper, B. Oldenburg, and et al. WNT-pathway activation in IBD-associated colorectal carcinogenesis: potential biomarkers for colonic surveillance Cell Oncol 32 2010 303 310
24. M. Suzui, T. Ushijima, N. Yoshimi, and et al. No involvement of APC gene mutations in ulcerative colitis-associated rat colon carcinogenesis induced by 1-hydroxyanthraquinone and methylazoxymethanol acetate Molecular Carcinogenesis 20 1997 389 393
25. J. Yin, N. Harpaz, Y. Tong, and et al. p53 point mutations in dysplastic and cancerous ulcerative colitis lesions Gastroenterology 104 1993 1633 1639
26. T.A. Brentnall, D.A. Crispin, P.S. Rabinovitch, and et al. Mutations in the p53 gene: an early marker of neoplastic progression in ulcerative colitis Gastroenterology 107 1994 369 378
27. N. Harpaz, A.L. Peck, J. Yin, and et al. p53 protein expression in ulcerative colitis-associated colorectal dysplasia and carcinoma Hum Pathol 25 1994 1069 1074
28. H.J. Kim, and S.K. Chang p53 mutation in patients with ulcerative colitis in rectal biopsy Korean J Intern Med 13 1998 110 116
29. K. Holzmann, B. Klump, F. Borchard, and et al. Comparative analysis of histology, DNA content, p53 and Ki-ras mutations in colectomy specimens with long-standing ulcerative colitis Int J Cancer 76 1998 1 6
30. S.P. Hussain, P. Amstad, K. Raja, and et al. Increased p53 mutation load in noncancerous colon tissue from ulcerative colitis: a cancer-prone chronic inflammatory disease Cancer Res 60 2000 3333 3337
31. H. Suzuki, N. Harpaz, L. Tarmin, and et al. Microsatellite instability in ulcerative colitis-associated colorectal dysplasias and cancers Cancer Res 54 1994 4841 4844
32. R.F. Souza, J. Lei, J. Yin, and et al. A transforming growth factor beta 1 receptor type II mutation in ulcerative colitis-associated neoplasms Gastroenterology 112 1997 40 45
33. A.S. Fleisher, M. Esteller, N. Harpaz, and et al. Microsatellite instability in inflammatory bowel disease-associated neoplastic lesions is associated with hypermethylation and diminished expression of the DNA mismatch repair gene, hMLH1 Cancer Res 60 2000 4864 4868
34. K. Schulmann, Y. Mori, V. Croog, and et al. Molecular phenotype of inflammatory bowel disease-associated neoplasms with microsatellite instability Gastroenterology 129 2005 74 85
35. L. Cawkwell, F. Sutherland, H. Murgatroyd, and et al. Defective hMSH2/hMLH1 protein expression is seen infrequently in ulcerative colitis associated colorectal cancers Gut 46 2000 367 369
36. F. Fogt, R.L. Zimmerman, C. Poremba, and et al. Immunohistochemical screening of mismatch repair genes hMLH1, hMSH2, and hMSH6 in dysplastic lesions of the colon Appl Immunohistochem Mol Morphol 10 2002 57 61
37. K. Konishi, L. Shen, S. Wang, and et al. Rare CpG island methylator phenotype in ulcerative colitis-associated neoplasias Gastroenterology 132 2007 1254 1260
38. T.T. Zou, F.M. Selaru, Y. Xu, and et al. Application of cDNA microarrays to generate a molecular taxonomy capable of distinguishing between colon cancer and normal colon Oncogene 21 2002 4855 4862
39. F.M. Selaru, Y. Xu, J. Yin, and et al. Artificial neural networks distinguish among subtypes of neoplastic colorectal lesions Gastroenterology 122 2002 606 613
40. D.W. Colliver, N.P. Crawford, M.R. Eichenberger, and et al. Molecular profiling of ulcerative colitis-associated neoplastic progression Exp Mol Pathol 80 2006 1 10
41. A.V. Olaru, F.M. Selaru, Y. Mori, and et al. Dynamic changes in the expression of MicroRNA-31 during inflammatory bowel disease-associated neoplastic transformation Inflamm Bowel Dis 17 2011 221 231
42. Z. Kanaan, S.N. Rai, M.R. Eichenberger, and et al. Differential microRNA expression tracks neoplastic progression in inflammatory bowel disease-associated colorectal cancer Hum Mutat 33 2012 551 560
43. J.J. Sohn, A.J. Schetter, H.G. Yfantis, and et al. Macrophages, nitric oxide and microRNAs are associated with DNA damage response pathway and senescence in inflammatory bowel disease PLoS One 7 2012 e44156
44. A.V. Olaru, S. Yamanaka, C. Vazquez, and et al. MicroRNA-224 negatively regulates p21 expression during late neoplastic progression in inflammatory bowel disease Inflamm Bowel Dis 19 2013 471 480
45. C.W. Wu, S.C. Ng, Y. Dong, and et al. Identification of microRNA-135b in stool as a potential noninvasive biomarker for colorectal cancer and adenoma Clin Cancer Res 20 2014 2994 3002
46. C.J. Hsieh, B. Klump, K. Holzmann, and et al. Hypermethylation of the p16INK4a promoter in colectomy specimens of patients with long-standing and extensive ulcerative colitis Cancer Res 58 1998 3942 3945
47. J.M. Wheeler, H.C. Kim, J.A. Efstathiou, and et al. Hypermethylation of the promoter region of the E-cadherin gene (CDH1) in sporadic and ulcerative colitis associated colorectal cancer Gut 48 2001 367 371
48. F. Sato, D. Shibata, N. Harpaz, and et al. Aberrant methylation of the HPP1 gene in ulcerative colitis-associated colorectal carcinoma Cancer Res 62 2002 6820 6822
49. F. Sato, N. Harpaz, D. Shibata, and et al. Hypermethylation of the p14(ARF) gene in ulcerative colitis-associated colorectal carcinogenesis Cancer Res 62 2002 1148 1151
50. N.K. Osborn, H. Zou, J.R. Molina, and et al. Aberrant methylation of the eyes absent 4 gene in ulcerative colitis-associated dysplasia Clin Gastroenterol Hepatol 4 2006 212 218
51. M. Dhir, E.A. Montgomery, S.C. Glockner, and et al. Epigenetic regulation of WNT signaling pathway genes in inflammatory bowel disease (IBD) associated neoplasia J Gastrointest Surg 12 2008 1745 1753
52. S. Matsumura, N. Oue, R. Ito, and et al. The promoter methylation status of the DNA repair gene O6-methylguanine-DNA methyltransferase in ulcerative colitis Virchows Arch 443 2003 518 523
53. T. Mikami, T. Yoshida, Y. Numata, and et al. Low frequency of promoter methylation of O6-methylguanine DNA methyltransferase and hMLH1 in ulcerative colitis-associated tumors: comparison with sporadic colonic tumors Am J Clin Pathol 127 2007 366 373
54. A.V. Olaru, Y. Cheng, R. Agarwal, and et al. Unique patterns of CpG island methylation in inflammatory bowel disease-associated colorectal cancers Inflamm Bowel Dis 18 2012 641 648
55. P.M. O'Connor, T.K. Lapointe, P.L. Beck, and et al. Mechanisms by which inflammation may increase intestinal cancer risk in inflammatory bowel disease Inflamm Bowel Dis 16 2010 1411 1420
56. M.T. Gansauge, and M. Meyer Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA Nat Protoc 8 2013 737 748
57. Y. Jiao, C. Shi, B.H. Edil, and et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors Science 331 2011 1199 1203
58. S. Jones, X. Zhang, D.W. Parsons, and et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses Science 321 2008 1801 1806
59. I. Kinde, J. Wu, N. Papadopoulos, and et al. Detection and quantification of rare mutations with massively parallel sequencing Proc Natl Acad Sci U S A 108 2011 9530 9535
60. Comprehensive molecular characterization of human colon and rectal cancer Nature 487 2012 330 337
61. K. Wang, J. Kan, S.T. Yuen, and et al. Exome sequencing identifies frequent mutation of ARID1A in molecular subtypes of gastric cancer Nat Genet 43 2011 1219 1223
62. Comprehensive molecular characterization of gastric adenocarcinoma Nature 513 2014 202 209
63. L.D. Wood, D.W. Parsons, S. Jones, and et al. The genomic landscapes of human breast and colorectal cancers Science 318 2007 1108 1113
64. Y. Totoki, K. Tatsuno, K.R. Covington, and et al. Trans-ancestry mutational landscape of hepatocellular carcinoma genomes Nat Genet 46 2014 1267 1273
65. L.B. Alexandrov, S. Nik-Zainal, D.C. Wedge, and et al. Signatures of mutational processes in human cancer Nature 500 2013 415 421
66. T. Helleday, S. Eshtad, and S. Nik-Zainal Mechanisms underlying mutational signatures in human cancers Nat Rev Genet 15 2014 585 598
67. A.M. Dulak, P. Stojanov, S. Peng, and et al. Exome and whole-genome sequencing of esophageal adenocarcinoma identifies recurrent driver events and mutational complexity Nat Genet 45 2013 478 486
68. J.M. Weaver, C.S. Ross-Innes, N. Shannon, and et al. Ordering of mutations in preinvasive disease stages of esophageal carcinogenesis Nat Genet 46 2014 837 843
69. T. Sjoblom, S. Jones, L.D. Wood, and et al. The consensus coding sequences of human breast and colorectal cancers Science 314 2006 268 274
70. N.L. Mathy, W. Scheuer, M. Lanzendorfer, and et al. Interleukin-16 stimulates the expression and production of pro-inflammatory cytokines by human monocytes Immunology 100 2000 63 69
71. K.L. Carraway 3rd, and L.C. Cantley A neu acquaintance for erbB3 and erbB4: a role for receptor heterodimerization in growth signaling Cell 78 1994 5 8
72. N. Agrawal, Y. Jiao, C. Bettegowda, and et al. Comparative genomic analysis of esophageal adenocarcinoma and squamous cell carcinoma Cancer Discov 2 2012 899 905
73. J. Yu, W.K. Wu, X. Li, and et al. Novel recurrently mutated genes and a prognostic mutation signature in colorectal cancer Gut 64 2015 636 645
74. M.F. Berger, E. Hodis, T.P. Heffernan, and et al. Melanoma genome sequencing reveals frequent PREX2 mutations Nature 485 2012 502 506
75. A. Post, W.J. Pannekoek, S.H. Ross, and et al. Rasip1 mediates Rap1 regulation of Rho in endothelial barrier function through ArhGAP29 Proc Natl Acad Sci U S A 110 2013 11427 11432
76. N.A. Barlev, L. Liu, N.H. Chehab, and et al. Acetylation of p53 activates transcription through recruitment of coactivators/histone acetyltransferases Mol Cell 8 2001 1243 1254
77. T. Soussi Advances in carcinogenesis: a historical perspective from observational studies to tumor genome sequencing and TP53 mutation spectrum analysis Biochim Biophys Acta 1816 2011 199 208
78. S. Ambs, W.P. Bennett, W.G. Merriam, and et al. Relationship between p53 mutations and inducible nitric oxide synthase expression in human colorectal cancer J Natl Cancer Inst 91 1999 86 88
79. S.K. Gupta, J.F. Fitzgerald, S.K. Chong, and et al. Expression of inducible nitric oxide synthase (iNOS) mRNA in inflamed esophageal and colonic mucosa in a pediatric population Am J Gastroenterol 93 1998 795 798
80. G. Kolios, V. Valatas, and S.G. Ward Nitric oxide in inflammatory bowel disease: a universal messenger in an unsolved puzzle Immunology 113 2004 427 437
81. S.J. Meltzer, D.J. Ahnen, H. Battifora, and et al. Protooncogene abnormalities in colon cancers and adenomatous polyps Gastroenterology 92 1987 1174 1180
82. M. Coskun, J.T. Troelsen, and O.H. Nielsen The role of CDX2 in intestinal homeostasis and inflammation Biochim Biophys Acta 1812 2011 283 289
83. E. Day, G. Poulogiannis, F. McCaughan, and et al. IRS2 is a candidate driver oncogene on 13q34 in colorectal cancer Int J Exp Pathol 94 2013 203 211
84. M.S. Silverberg, J.H. Cho, J.D. Rioux, and et al. Ulcerative colitis-risk loci on chromosomes 1p36 and 12q15 found by genome-wide association study Nat Genet 41 2009 216 220
85. J. Lei, T.T. Zou, Y.Q. Shi, and et al. Infrequent DPC4 gene mutation in esophageal cancer, gastric cancer and ulcerative colitis-associated neoplasms Oncogene 13 1996 2459 2462
86. D. Vigil, J. Cherfils, K.L. Rossman, and et al. Ras superfamily GEFs and GAPs: validated and tractable targets for cancer therapy? Nat Rev Cancer 10 2010 842 857
87. M.F. Neurath Cytokines in inflammatory bowel disease Nat Rev Immunol 14 2014 329 342
88. L. Beaugerie, M. Svrcek, P. Seksik, and et al. Risk of colorectal high-grade dysplasia and cancer in a prospective observational cohort of patients with inflammatory bowel disease Gastroenterology 145 2013 166 175
89. A.D. Gracz, S. Ramalingam, and S.T. Magness Sox9 expression marks a subset of CD24-expressing small intestine epithelial stem cells that form organoids in vitro Am J Physiol Gastrointest Liver Physiol 298 2010 G590 G600
90. L. Topol, W. Chen, H. Song, and et al. Sox9 inhibits Wnt signaling by promoting beta-catenin phosphorylation in the nucleus J Biol Chem 284 2009 3323 3333
91. K.B. Myant, P. Cammareri, E.J. McGhee, and et al. ROS production and NF-kappaB activation triggered by RAC1 facilitate WNT-driven intestinal stem cell proliferation and colorectal cancer initiation Cell Stem Cell 12 2013 761 773
92. C.Y. Ock, E.H. Kim, H. Hong, and et al. Prevention of colitis-associated colorectal cancer with 8-hydroxydeoxyguanosine Cancer Prev Res (Phila) 4 2011 1507 1521
93. J.M. Rhodes, and B.J. Campbell Inflammation and colorectal cancer: IBD-associated and sporadic cancer compared Trends Mol Med 8 2002 10 16
94. S. Galandiuk, M. Rodriguez-Justo, R. Jeffery, and et al. Field cancerization in the intestinal epithelium of patients with Crohn's ileocolitis Gastroenterology 142 2012 855 864 e858
95. W.G. Glass, R.T. Sarisky, and A.M. Vecchio Not-so-sweet sixteen: the role of IL-16 in infectious and immune-mediated inflammatory diseases J Interferon Cytokine Res 26 2006 511 520
96. L.B. Gao, L. Rao, Y.Y. Wang, and et al. The association of interleukin-16 polymorphisms with IL-16 serum levels and risk of colorectal and gastric cancer Carcinogenesis 30 2009 295 299
97. A.C. Keates, I. Castagliuolo, W.W. Cruickshank, and et al. Interleukin 16 is up-regulated in Crohn's disease and participates in TNBS colitis in mice Gastroenterology 119 2000 972 982
98. D. Seegert, P. Rosenstiel, H. Pfahler, and et al. Increased expression of IL-16 in inflammatory bowel disease Gut 48 2001 326 332