Molecular dissection of premalignant colorectal lesions reveals early onset of the CpG island methylator phenotype

American Journal of Pathology

Volumn 181, Issue 5, 2012, Pages 1847-1861

  Yamamoto, Eiichiro ^a   Suzuki, Hiromu ^a   Yamano, Hiro O ^b   Maruyama, Reo ^a   Nojima, Masanori ^a   Kamimae, Seiko ^a   Sawada, Takeshi ^a   Ashida, Masami ^a   Yoshikawa, Kenjiro ^b   Kimura, Tomoaki ^b   Takagi, Ryo ^b   Harada, Taku ^b   Suzuki, Ryo ^a   Sato, Akiko ^a   Kai, Masahiro ^a   Sasaki, Yasushi ^a   Tokino, Takashi ^a   Sugai, Tamotsu ^c   Imai, Kohzoh ^d   Shinomura, Yasuhisa ^a   Toyota, Minoru ^a   more..

^a SAPPORO MEDICAL UNIVERSITY   (Japan)

^b AKITA RED CROSS HOSPITAL   (Japan)

^c IWATE MEDICAL UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; K RAS PROTEIN;

AGED; ARTICLE; CHROMOSOME 19; CHROMOSOME 7; COLORECTAL CANCER; COPY NUMBER VARIATION; CPG ISLAND; DNA METHYLATION; EPIGENETICS; FEMALE; GENETIC DISORDER; GENOME ANALYSIS; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; PHENOTYPE; PRIORITY JOURNAL;

AGED; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; CPG ISLANDS; DISEASE PROGRESSION; DNA COPY NUMBER VARIATIONS; DNA METHYLATION; ENDOSCOPY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, HUMAN; HUMANS; MALE; MUTATION; PHENOTYPE; PRECANCEROUS CONDITIONS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; RAS PROTEINS;

EID: 84868128686     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.08.007     Document Type: Article

References (50)

1. B. Vogelstein, E.R. Fearon, S.R. Hamilton, S.E. Kern, A.C. Preisinger, M. Leppert, Y. Nakamura, R. White, A.M. Smits, J.L. Bos Genetic alterations during colorectal-tumor development N Engl J Med 319 1988 525 532
2. W. Grady, J. Carethers Genomic and epigenetic instability in colorectal cancer pathogenesis Gastroenterology 135 2008 1079 1099
3. P.A. Jones, S.B. Baylin The epigenomics of cancer Cell 128 2007 683 692 (Pubitemid 46273572)
4. H. Suzuki, T. Tokino, Y. Shinomura, K. Imai, M. Toyota DNA methylation and cancer pathways in gastrointestinal tumors Pharmacogenomics 9 2008 1917 1928
5. V.V. Lao, W.M. Grady Epigenetics and colorectal cancer Nat Rev Gastroenterol Hepatol 8 2011 686 700
6. K. Curtin, M.L. Slattery, W.S. Samowitz CpG island methylation in colorectal cancer: past, present and future Patholog Res Int 2011 2011 902674
7. M. Toyota, N. Ahuja, M. Ohe-Toyota, J.G. Herman, S.B. Baylin, J.P. Issa CpG island methylator phenotype in colorectal cancer Proc Natl Acad Sci U S A 96 1999 8681 8686 (Pubitemid 29354851)
8. M. Toyota, M. Ohe-Toyota, N. Ahuja, J.P. Issa Distinct genetic profiles in colorectal tumors with or without the CpG island methylator phenotype Proc Natl Acad Sci U S A 97 2000 710 715 (Pubitemid 30070374)
9. D. Weisenberger, K. Siegmund, M. Campan, J. Young, T. Long, M. Faasse, G. Kang, M. Widschwendter, D. Weener, D. Buchanan, H. Koh, L. Simms, M. Barker, B. Leggett, J. Levine, M. Kim, A. French, S. Thibodeau, J. Jass, R. Haile, P. Laird CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer Nat Genet 38 2006 787
10. L. Shen, M. Toyota, Y. Kondo, E. Lin, L. Zhang, Y. Guo, N. Hernandez, X. Chen, S. Ahmed, K. Konishi, S. Hamilton, J. Issa Integrated genetic and epigenetic analysis identifies three different subclasses of colon cancer Proc Natl Acad Sci U S A 104 2007 18654
11. W. Samowitz, H. Albertsen, J. Herrick, T. Levin, C. Sweeney, M. Murtaugh, R. Wolff, M. Slattery Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer Gastroenterology 129 2005 837 845 (Pubitemid 41242676)
12. S. Ogino, T. Kawasaki, G.J. Kirkner, M. Loda, C.S. Fuchs CpG island methylator phenotype-low (CIMP-low) in colorectal cancer: possible associations with male sex and KRAS mutations J Mol Diagn 8 2006 582 588 (Pubitemid 44774157)
13. T. Hinoue, D.J. Weisenberger, C.P. Lange, H. Shen, H.M. Byun, D. Van Den Berg, S. Malik, F. Pan, H. Noushmehr, C.M. van Dijk, R.A. Tollenaar, P.W. Laird Genome-scale analysis of aberrant DNA methylation in colorectal cancer Genome Res 22 2012 271 282
14. K. Spring, Z. Zhao, R. Karamatic, M. Walsh, V.L.J. Whitehall, T. Pike, L. Simms, J. Young, M. James, G. Montgomery, M. Appleyard, D. Hewett, K. Togashi, J. Jass, B. Leggett High prevalence of sessile serrated adenomas with BRAF mutations: a prospective study of patients undergoing colonoscopy Gastroenterology 131 2006 1400
15. B. Leggett, V. Whitehall Role of the serrated pathway in colorectal cancer pathogenesis Gastroenterology 138 2010 2088 2100
16. T. Nagasaka, M. Koi, M. Kloor, J. Gebert, A. Vilkin, N. Nishida, S. Shin, H. Sasamoto, N. Tanaka, N. Matsubara, C.R. Boland, A. Goel Mutations in both KRAS and BRAF may contribute to the methylator phenotype in colon cancer Gastroenterology 134 2008 1950
17. A. Goel, T. Nagasaka, C. Arnold, T. Inoue, C. Hamilton, D. Niedzwiecki, C. Compton, R. Mayer, R. Goldberg, M. Bertagnolli, C.R. Boland The CpG island methylator phenotype and chromosomal instability are inversely correlated in sporadic colorectal cancer Gastroenterology 132 2007 127
18. S. Kudo, S. Tamura, T. Nakajima, H. Yamano, H. Kusaka, H. Watanabe Diagnosis of colorectal tumorous lesions by magnifying endoscopy Gastrointest Endosc 44 1996 8 14 (Pubitemid 26268652)
19. S. Kudo, R. Lambert, J. Allen, H. Fujii, T. Fujii, H. Kashida, T. Matsuda, M. Mori, H. Saito, T. Shimoda, S. Tanaka, H. Watanabe, J. Sung, A. Feld, J. Inadomi, M. O'Brien, D. Lieberman, D. Ransohoff, R. Soetikno, G. Triadafilopoulos, A. Zauber, C. Teixeira, J. Rey, E. Jaramillo, C. Rubio, A. Van Gossum, M. Jung, M. Vieth, J. Jass, P. Hurlstone Nonpolypoid neoplastic lesions of the colorectal mucosa Gastrointest Endosc 68 2008 S3 S47
20. T. Kimura, E. Yamamoto, H.O. Yamano, H. Suzuki, S. Kamimae, M. Nojima, T. Sawada, M. Ashida, K. Yoshikawa, R. Takagi, R. Kato, T. Harada, R. Suzuki, R. Maruyama, M. Kai, K. Imai, Y. Shinomura, T. Sugai, M. Toyota A novel pit pattern identifies the precursor of colorectal cancer derived from sessile serrated adenoma Am J Gastroenterol 107 2012 460 469
21. K. Akino, M. Toyota, H. Suzuki, H. Mita, Y. Sasaki, M. Ohe-Toyota, J.P. Issa, Y. Hinoda, K. Imai, T. Tokino The Ras effector RASSF2 is a novel tumor-suppressor gene in human colorectal cancer Gastroenterology 129 2005 156 169 (Pubitemid 41002052)
22. E. Torlakovic, E. Skovlund, D. Snover, G. Torlakovic, J. Nesland Morphologic reappraisal of serrated colorectal polyps Am J Surg Pathol 27 2003 65 81 (Pubitemid 36014900)
23. Y. Goto, K. Shinjo, Y. Kondo, L. Shen, M. Toyota, H. Suzuki, W. Gao, B. An, M. Fujii, H. Murakami, H. Osada, T. Taniguchi, N. Usami, M. Kondo, Y. Hasegawa, K. Shimokata, K. Matsuo, T. Hida, N. Fujimoto, T. Kishimoto, J.P. Issa, Y. Sekido Epigenetic profiles distinguish malignant pleural mesothelioma from lung adenocarcinoma Cancer Res 69 2009 9073 9082
24. M. Toyota, H. Suzuki, Y. Sasaki, R. Maruyama, K. Imai, Y. Shinomura, T. Tokino Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer Cancer Res 68 2008 4123 4132
25. D.W. Parsons, T.L. Wang, Y. Samuels, A. Bardelli, J.M. Cummins, L. DeLong, N. Silliman, J. Ptak, S. Szabo, J.K. Willson, S. Markowitz, K.W. Kinzler, B. Vogelstein, C. Lengauer, V.E. Velculescu Colorectal cancer: mutations in a signalling pathway Nature 436 2005 792 (Pubitemid 41160630)
26. T. Sugai, W. Habano, S. Nakamura, N. Uesugi, S. Sasou, C. Itoh A unique method for mutation analysis of tumor suppressor genes in colorectal carcinomas using a crypt isolation technique Arch Pathol Lab Med 124 2000 382 386 (Pubitemid 30152139)
27. T. Sugai, W. Habano, M. Endoh, Y. Konishi, R. Akasaka, M. Toyota, H. Yamano, K. Koeda, G. Wakabayashi, K. Suzuki Molecular analysis of gastric differentiated-type intramucosal and submucosal cancers Int J Cancer 127 2010 2500 2509
28. C.R. Boland, S.N. Thibodeau, S.R. Hamilton, D. Sidransky, J.R. Eshleman, R.W. Burt, S.J. Meltzer, M.A. Rodriguez Bigas, R. Fodde, G.N. Ranzani, S. Srivastava A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer Cancer Res 58 1998 5248 5257 (Pubitemid 28521189)
29. S. Igarashi, H. Suzuki, T. Niinuma, H. Shimizu, M. Nojima, H. Iwaki, T. Nobuoka, T. Nishida, Y. Miyazaki, H. Takamaru, E. Yamamoto, H. Yamamoto, T. Tokino, T. Hasegawa, K. Hirata, K. Imai, M. Toyota, Y. Shinomura A novel correlation between LINE-1 hypomethylation and the malignancy of gastrointestinal stromal tumors Clin Cancer Res 16 2010 5114 5123
30. H. Suzuki, S. Igarashi, M. Nojima, R. Maruyama, E. Yamamoto, M. Kai, H. Akashi, Y. Watanabe, H. Yamamoto, Y. Sasaki, F. Itoh, K. Imai, T. Sugai, L. Shen, J.P. Issa, Y. Shinomura, T. Tokino, M. Toyota IGFBP7 is a p53-responsive gene specifically silenced in colorectal cancer with CpG island methylator phenotype Carcinogenesis 31 2010 342 349
31. H. Suzuki, D.N. Watkins, K.W. Jair, K.E. Schuebel, S.D. Markowitz, W.D. Chen, T.P. Pretlow, B. Yang, Y. Akiyama, M. Van Engeland, M. Toyota, T. Tokino, Y. Hinoda, K. Imai, J.G. Herman, S.B. Baylin Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer Nat Genet 36 2004 417 422 (Pubitemid 38437267)
32. T. Hinoue, D.J. Weisenberger, F. Pan, M. Campan, M. Kim, J. Young, V.L. Whitehall, B.A. Leggett, P.W. Laird Analysis of the association between CIMP and BRAF in colorectal cancer by DNA methylation profiling PLoS One 4 2009 e8357
33. S. Ogino, T. Kawasaki, G.J. Kirkner, M. Ohnishi, C.S. Fuchs 18q Loss of heterozygosity in microsatellite stable colorectal cancer is correlated with CpG island methylator phenotype-negative (CIMP-0) and inversely with CIMP-low and CIMP-high BMC Cancer 7 2007 72
34. Y.W. Cheng, H. Pincas, M.D. Bacolod, G. Schemmann, S.F. Giardina, J. Huang, S. Barral, K. Idrees, S.A. Khan, Z. Zeng, S. Rosenberg, D.A. Notterman, J. Ott, P. Paty, F. Barany CpG island methylator phenotype associates with low-degree chromosomal abnormalities in colorectal cancer Clin Cancer Res 14 2008 6005 6013
35. F. Fang, S. Turcan, A. Rimner, A. Kaufman, D. Giri, L.G. Morris, R. Shen, V. Seshan, Q. Mo, A. Heguy, S.B. Baylin, N. Ahuja, A. Viale, J. Massague, L. Norton, L.T. Vahdat, M.E. Moynahan, T.A. Chan Breast cancer methylomes establish an epigenomic foundation for metastasis Sci Transl Med 3 2011 75ra25
36. R. Jover, T. Nguyen, L. Prez-Carbonell, P. Zapater, A. Pay, C. Alenda, E. Rojas, J. Cubiella, F. Balaguer, J. Morillas, J. Clofent, L. Bujanda, J. Re, X. Bessa, R. Xicola, D. Nicols-Prez, A. Castells, M. Andreu, X. Llor, C.R. Boland, A. Goel 5-Fluorouracil adjuvant chemotherapy does not increase survival in patients with CpG island methylator phenotype colorectal cancer Gastroenterology 140 2011 1174 1181
37. H. Noushmehr, D.J. Weisenberger, K. Diefes, H.S. Phillips, K. Pujara, B.P. Berman, F. Pan, C.E. Pelloski, E.P. Sulman, K.P. Bhat, R.G. Verhaak, K.A. Hoadley, D.N. Hayes, C.M. Perou, H.K. Schmidt, L. Ding, R.K. Wilson, D. Van Den Berg, H. Shen, H. Bengtsson, P. Neuvial, L.M. Cope, J. Buckley, J.G. Herman, S.B. Baylin, P.W. Laird, K. Aldape Cancer Genome Atlas Research Network: Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma Cancer Cell 17 2010 510 522
38. S. Jones, W. Chen, G. Parmigiani, F. Diehl, N. Beerenwinkel, T. Antal, A. Traulsen, M. Nowak, C. Siegel, V. Velculescu, K. Kinzler, B. Vogelstein, J. Willis, S. Markowitz Comparative lesion sequencing provides insights into tumor evolution Proc Natl Acad Sci U S A 105 2008 4283 4288 (Pubitemid 351754372)
39. K. Yagi, H. Takahashi, K. Akagi, K. Matsusaka, Y. Seto, H. Aburatani, A. Nakajima, A. Kaneda Intermediate methylation epigenotype and its correlation to KRAS mutation in conventional colorectal adenoma Am J Pathol 180 2012 616 625
40. J.R. Jass, K. Baker, I. Zlobec, T. Higuchi, M. Barker, D. Buchanan, J. Young Advanced colorectal polyps with the molecular and morphological features of serrated polyps and adenomas: concept of a "fusion" pathway to colorectal cancer Histopathology 49 2006 121 131 (Pubitemid 44079695)
41. M. Pino, D. Chung The chromosomal instability pathway in colon cancer Gastroenterology 138 2010 2059 2072
42. S. Ogino, T. Kawasaki, G. Kirkner, Y. Suemoto, J. Meyerhardt, C. Fuchs Molecular correlates with MGMT promoter methylation and silencing support CpG island methylator phenotype-low (CIMP-low) in colorectal cancer Gut 56 2007 1564 1571 (Pubitemid 350033195)
43. S. Ogino, K. Nosho, N. Irahara, K. Shima, Y. Baba, G. Kirkner, J. Meyerhardt, C. Fuchs Prognostic significance and molecular associations of 18q loss of heterozygosity: a cohort study of microsatellite stable colorectal cancers J Clin Oncol 27 2009 4591 4598
44. Y. He, L.J. Van't Veer, I. Mikolajewska-Hanclich, M.L. van Velthuysen, E.C. Zeestraten, I.D. Nagtegaal, C.J. van de Velde, C.A. Marijnen PIK3CA mutations predict local recurrences in rectal cancer patients Clin Cancer Res 15 2009 6956 6962
45. Y. Baba, K. Nosho, K. Shima, M. Hayashi, J.A. Meyerhardt, A.T. Chan, E. Giovannucci, C.S. Fuchs, S. Ogino Phosphorylated AKT expression is associated with PIK3CA mutation, low stage, and favorable outcome in 717 colorectal cancers Cancer 117 2011 1399 1408
46. V.L.J. Whitehall, C. Rickman, C. Bond, I. Ramsnes, S. Greco, A. Umapathy, D. McKeone, R. Faleiro, R. Buttenshaw, D. Worthley, S. Nayler, Z. Zhao, G. Montgomery, K. Mallitt, J. Jass, N. Matsubara, K. Notohara, T. Ishii, B. Leggett Oncogenic PIK3CA mutations in colorectal cancers and polyps Int J Cancer 131 2012 813 820
47. R.B. Corcoran, D. Dias Santagata, K. Bergethon, A.J. Iafrate, J. Settleman, J.A. Engelman BRAF gene amplification can promote acquired resistance to MEK inhibitors in cancer cells harboring the BRAF V600E mutation Sci Signal 3 2010 ra84
48. A.S. Little, K. Balmanno, M.J. Sale, S. Newman, J.R. Dry, M. Hampson, P.A. Edwards, P.D. Smith, S.J. Cook Amplification of the driving oncogene, KRAS or BRAF, underpins acquired resistance to MEK1/2 inhibitors in colorectal cancer cells [Erratum appears in Sci Signal 2011, 4: er2] Sci Signal 4 2011 ra17
49. M. Yamauchi, T. Morikawa, A. Kuchiba, Y. Imamura, Z. Qian, R. Nishihara, X. Liao, L. Waldron, Y. Hoshida, C. Huttenhower, A. Chan, E. Giovannucci, C. Fuchs, S. Ogino Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum Gut 61 2012 847 854
50. M. Yamauchi, P. Lochhead, T. Morikawa, C. Huttenhower, A. Chan, E. Giovannucci, C. Fuchs, S. Ogino Colorectal cancer: a tale of two sides or a continuum? Gut 61 2012 794 797