A prospective study of duration of smoking cessation and colorectal cancer risk by epigenetics-related tumor classification

American Journal of Epidemiology

Volumn 178, Issue 1, 2013, Pages 84-100

  Nishihara, Reiko ^a,b   Morikawa, Teppei ^a   Kuchiba, Aya ^a   Lochhead, Paul ^a   Yamauchi, Mai ^a   Liao, Xiaoyun ^a   Imamura, Yu ^a   Nosho, Katsuhiko ^a   Shima, Kaori ^a   Kawachi, Ichiro ^a   Qian, Zhi Rong ^a   Fuchs, Charles S ^a   Chan, Andrew T ^c,d   Giovannucci, Edward ^a,c   Ogino, Shuji ^a,c  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

carcinogen; carcinoma; epigenomics; hypermethylation; molecular epidemiology; public health; tobacco; translational epidemiology

Indexed keywords

B RAF KINASE; DNA HOMOLOG; DNA METHYLTRANSFERASE 3B; ONCOPROTEIN;

CANCER; EPIDEMIOLOGY; METHYLATION; MOLECULAR ANALYSIS; PATHOLOGY; PUBLIC HEALTH; RISK FACTOR; SMOKING; TUMOR;

ADULT; AGED; ARTICLE; CANCER EPIDEMIOLOGY; CANCER RISK; COHORT ANALYSIS; COLORECTAL CANCER; CPG ISLAND; DISEASE ASSOCIATION; DNA METHYLATION; EPIGENETICS; FEMALE; FOLLOW UP; GENE DUPLICATION; GENE EXPRESSION; GENE MUTATION; HEALTH PRACTITIONER; HUMAN; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; PHENOTYPE; PROSPECTIVE STUDY; SARCOMA; SMOKING; SMOKING CESSATION; TUMOR CLASSIFICATION; VIRUS ONCOGENE;

CARCINOGEN; CARCINOMA; EPIGENOMICS; HYPERMETHYLATION; MOLECULAR EPIDEMIOLOGY; PUBLIC HEALTH; TOBACCO; TRANSLATIONAL EPIDEMIOLOGY;

AGED; COLORECTAL NEOPLASMS; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; EPIGENESIS, GENETIC; FEMALE; HUMANS; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; PHENOTYPE; PROPORTIONAL HAZARDS MODELS; PROSPECTIVE STUDIES; PROTO-ONCOGENE PROTEINS B-RAF; RISK FACTORS; SEX FACTORS; SMOKING; SMOKING CESSATION; TIME FACTORS;

MURINAE; NICOTIANA TABACUM;

EID: 84876484863     PISSN: 00029262     EISSN: 14766256     Source Type: Journal    
DOI: 10.1093/aje/kws431     Document Type: Article

References (83)

1. Botteri E, Iodice S, Bagnardi V, et al. Smoking and colorectal cancer: A meta-Analysis. JAMA. 2008;300(23): 2765-2778
2. Liang PS, Chen TY, Giovannucci E. Cigarette smoking and colorectal cancer incidence and mortality: Systematic review and meta-Analysis. Int J Cancer. 2009;124(10): 2406-2415
3. Verla-Tebit E, Lilla C, Hoffmeister M, et al. Cigarette smoking and colorectal cancer risk in Germany: A population-based case-control study. Int J Cancer. 2006;119(3):630-635
4. Leufkens AM, Van Duijnhoven FJ, Siersema PD, et al. Cigarette smoking and colorectal cancer risk in the European prospective investigation into cancer and nutrition study. Clin Gastroenterol Hepatol. 2011;9(2):137-144
5. Slattery ML, Potter JD, Friedman GD, et al. Tobacco use and colon cancer. Int J Cancer. 1997;70(3):259-264
6. Newcomb PA, Storer BE, Marcus PM. Cigarette smoking in relation to risk of large bowel cancer in women. Cancer Res. 1995;55(21):4906-4909
7. Weijenberg MP, Aardening PW, de Kok TM, et al. Cigarette smoking and KRAS oncogene mutations in sporadic colorectal cancer: Results from the Netherlands Cohort Study. Mutat Res. 2008;652(1):54-64
8. Ogino S, Goel A. Molecular classification and correlates in colorectal cancer. J Mol Diagn. 2008;10(1):13-27
9. Lao VV, Grady WM. Epigenetics and colorectal cancer. Nat Rev Gastroenterol Hepatol. 2011;8(12):686-700
10. Ogino S, Stampfer M. Lifestyle factors and microsatellite instability in colorectal cancer: The evolving field of molecular pathological epidemiology. J Natl Cancer Inst. 2010;102(6): 365-367
11. Ogino S, Chan AT, Fuchs CS, et al. Molecular pathological epidemiology of colorectal neoplasia: An emerging transdisciplinary and interdisciplinary field. Gut. 2011; 60(3):397-411
12. Toyota M, Ahuja N, Ohe-Toyota M, et al. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci U S A. 1999;96(15):8681-8686
13. Samowitz WS, Albertsen H, Herrick J, et al. Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer. Gastroenterology. 2005;129(3):837-845
14. Curtin K, Slattery ML, Samowitz WS. CpG island methylation in colorectal cancer: Past, present and future. Patholog Res Int. 2011;2011:902674
15. Teodoridis JM, Hardie C, Brown R. CpG island methylator phenotype (CIMP) in cancer: Causes and implications. Cancer Lett. 2008;268(2):177-186
16. Hughes LA, Khalid-De Bakker CA, Smits KM, et al. The CpG island methylator phenotype in colorectal cancer: Progress and problems. Biochim Biophys Acta. 2012;1825(1):77-85
17. The Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487(7407):330-337
18. Weisenberger DJ, Siegmund KD, Campan M, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet. 2006;38(7):787-793
19. Barault L, Charon-Barra C, Jooste V, et al. Hypermethylator phenotype in sporadic colon cancer: Study on a populationbased series of 582 cases. Cancer Res. 2008;68(20):8541-8546
20. Nosho K, Irahara N, Shima K, et al. Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample. PLoS One. 2008;3(11):e3698
21. Linhart HG, Lin H, Yamada Y, et al. Dnmt3b promotes tumorigenesis in vivo by gene-specific de novo methylation and transcriptional silencing. Genes Dev. 2007;21(23): 3110-3122
22. Nosho K, Shima K, Irahara N, et al. DNMT3B expression might contribute to CpG island methylator phenotype in colorectal cancer. Clin Cancer Res. 2009;15(11):3663-3671
23. Ibrahim AE, Arends MJ, Silva AL, et al. Sequential DNA methylation changes are associated with DNMT3B overexpression in colorectal neoplastic progression. Gut. 2011;60(4):499-508
24. Steine EJ, Ehrich M, Bell GW, et al. Genes methylated by DNA methyltransferase 3b are similar in mouse intestine and human colon cancer. J Clin Invest. 2011;121(5):1748-1752
25. Palakurthy RK,Wajapeyee N, Santra MK, et al. Epigenetic silencing of the RASSF1A tumor suppressor gene through HOXB3-mediated induction of DNMT3B expression. Mol Cell. 2009;36(2):219-230
26. Curtin K, Samowitz WS,Wolff RK, et al. Somatic alterations, metabolizing genes and smoking in rectal cancer. Int J Cancer. 2009;125(1):158-164
27. Samowitz WS, Albertsen H, Sweeney C, et al. Association of smoking, CpG island methylator phenotype, and V600E BRAF mutations in colon cancer. J Natl Cancer Inst. 2006; 98(23):1731-1738
28. Limsui D, Vierkant RA, Tillmans LS, et al. Cigarette smoking and colorectal cancer risk by molecularly defined subtypes. J Natl Cancer Inst. 2010;102(14):1012-1022
29. Poynter JN, Haile RW, Siegmund KD, et al. Associations between smoking, alcohol consumption, and colorectal cancer, overall and by tumor microsatellite instability status. Cancer Epidemiol Biomarkers Prev. 2009;18(10):2745-2750
30. Lindor NM, Yang P, Evans I, et al. Alpha-1-Antitrypsin deficiency and smoking as risk factors for mismatch repair deficient colorectal cancer: A study from the colon cancer family registry. Mol Genet Metab. 2010;99(2):157-159
31. Slattery ML, Curtin K, Anderson K, et al. Associations between cigarette smoking, lifestyle factors, and microsatellite instability in colon tumors. J Natl Cancer Inst. 2000;92(22): 1831-1836
32. Phipps AI, Baron J, Newcomb PA. Prediagnostic smoking history, alcohol consumption, and colorectal cancer survival: The Seattle Colon Cancer Family Registry. Cancer. 2011; 117(21):4948-4957
33. Eaton AM, Sandler R, Carethers JM, et al. 5,10- Methylenetetrahydrofolate reductase 677 and 1298 polymorphisms, folate intake, and microsatellite instability in colon cancer. Cancer Epidemiol Biomarkers Prev. 2005; 14(8):2023-2029
34. Chia VM, Newcomb PA, Bigler J, et al. Risk of microsatelliteunstable colorectal cancer is associated jointly with smoking and nonsteroidal anti-inflammatory drug use. Cancer Res. 2006;66(13):6877-6883
35. Rozek LS, Herron CM, Greenson JK, et al. Smoking, gender, and ethnicity predict somatic BRAF mutations in colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2010;19(3):838-843
36. Wang T, Chen M, Liu L, et al. Nicotine induced CpG methylation of Pax6 binding motif in StAR promoter reduces the gene expression and cortisol production. Toxicol Appl Pharmacol. 2011;257(3):328-337
37. Liu F, Killian JK, Yang M, et al. Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene. 2010;29(25): 3650-3664
38. Du H, Sun J, Chen Z, et al. Cigarette smoke-induced failure of apoptosis resulting in enhanced neoplastic transformation in human bronchial epithelial cells. J Toxicol Environ Health A. 2012;75(12):707-720
39. Chan AT, Ogino S, Fuchs CS. Aspirin and the risk of colorectal cancer in relation to the expression of COX-2. N Engl J Med. 2007;356(21):2131-2142
40. Liao X, Lochhead P, Nishihara R, et al. Aspirin use, tumor PIK3CA mutation status, and colorectal cancer survival. N Engl J Med. 2012;367(17):1596-1606
41. Giovannucci E, Colditz GA, Stampfer MJ, et al. A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. women. J Natl Cancer Inst. 1994; 86(3):192-199
42. Giovannucci E, Rimm EB, Stampfer MJ, et al. A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. men. J Natl Cancer Inst. 1994; 86(3):183-191
43. Yamauchi M, Morikawa T, Kuchiba A, et al. Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum. Gut. 2012;61(6):847-854
44. Yamauchi M, Lochhead P, Morikawa T, et al. Colorectal cancer: A tale of two sides or a continuum? Gut. 2012; 61(6):794-797
45. Morikawa T, Kuchiba A, Yamauchi M, et al. Association of CTNNB1 (beta-catenin) alterations, body mass index, and physical activity with survival in patients with colorectal cancer. JAMA. 2011;305(16):1685-1694
46. Ogino S, Kawasaki T, Kirkner GJ, et al. CpG island methylator phenotype-low (CIMP-low) in colorectal cancer: Possible associations with male sex and KRAS mutations. J Mol Diagn. 2006;8(5):582-588
47. Ogino S, Nosho K, Kirkner GJ, et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut. 2009; 58(1):90-96
48. Ogino S, Kawasaki T, Brahmandam M, et al. Precision and performance characteristics of bisulfite conversion and real-Time PCR (MethyLight) for quantitative DNA methylation analysis. J Mol Diagn. 2006;8(2):209-217
49. Durrleman S, Simon R. Flexible regression models with cubic splines. Stat Med. 1989;8(5):551-561
50. Lunn M, McNeil D. Applying Cox regression to competing risks. Biometrics. 1995;51(2):524-532
51. Ogino S, Giovannucci E. Commentary: Lifestyle factors and colorectal cancer microsatellite instability-molecular pathological epidemiology science, based on unique tumour principle. Int J Epidemiol. 2012;41(4):1072-1074
52. Canales L, Chen J, Kelty E, et al. Developmental cigarette smoke exposure: Liver proteome profile alterations in low birth weight pups. Toxicology. 2012;300(1-2):1-11
53. Breitling LP, Yang R, Korn B, et al. Tobacco-smoking-related differential DNA methylation: 27K discovery and replication. Am J Hum Genet. 2011;88(4):450-457
54. Wan ES, QiuW, Baccarelli A, et al. Cigarette smoking behaviors and time since quitting are associated with differential DNA methylation across the human genome. Hum Mol Genet. 2012;21(13):3073-3082
55. Ogino S, Galon J, Fuchs CS, et al. Cancer immunology- analysis of host and tumor factors for personalized medicine. Nat Rev Clin Oncol. 2011;8(12):711-719
56. Ogino S, Fuchs CS, Giovannucci E. How many molecular subtypes? Implications of the unique tumor principle in personalized medicine. Expert Rev Mol Diagn. 2012; 12(6):621-628
57. Ogino S, King EE, Beck AH, et al. Interdisciplinary education to integrate pathology and epidemiology: Towards molecular and population-level health science. Am J Epidemiol. 2012;176(8):659-667
58. Kuller LH. Invited commentary: The 21st century epidemiologist-A need for different training? Am J Epidemiol. 2012;176(8):668-671
59. Ogino S, Beck AH, King EE, et al. Ogino et al. Respond to 'The 21st Century Epidemiologist'. Am J Epidemiol. 2012;176(8):672-674
60. Hughes LA, Simons CC, Van Den Brandt PA, et al. Body size, physical activity and risk of colorectal cancer with or without the CpG Island Methylator Phenotype (CIMP). PLoS One. 2011;6(4):e18571
61. Limsui D, Vierkant RA, Tillmans LS, et al. Postmenopausal hormone therapy and colorectal cancer risk by molecularly defined subtypes among older women. Gut. 2012;61(9): 1299-1305
62. Limburg PJ, Limsui D, Vierkant RA, et al. Postmenopausal hormone therapy and colorectal cancer risk in relation to somatic KRAS mutation status among older women. Cancer Epidemiol Biomarkers Prev. 2012;21(4):681-684
63. Gay LJ, Mitrou PN, Keen J, et al. Dietary, lifestyle and clinico-pathological factors associated with APC mutations and promoter methylation in colorectal cancers from the EPICNorfolk Study. J Pathol. 2012;228(3):405-415
64. Schernhammer ES, Giovannucci E, Kawasaki T, et al. Dietary folate, alcohol and B vitamins in relation to LINE-1 hypomethylation in colon cancer. Gut. 2010;59(6):794-799
65. Kuchiba A, Morikawa T, Yamauchi M, et al. Body mass index and risk of colorectal cancer according to fatty acid synthase expression in the Nurses' Health Study. J Natl Cancer Inst. 2012;104(5):415-420
66. Yamaji T, Iwasaki M, Sasazuki S, et al. Association between plasma 25-hydroxyvitamin D and colorectal adenoma according to dietary calcium intake and vitamin D receptor polymorphism. Am J Epidemiol. 2012;175(3):236-244
67. Lubbe SJ, Di Bernardo MC, Broderick P, et al. Comprehensive evaluation of the impact of 14 genetic variants on colorectal cancer phenotype and risk. Am J Epidemiol. 2012; 175(1):1-10
68. Shin A, Hong CW, Sohn DK, et al. Associations of cigarette smoking and alcohol consumption with advanced or multiple colorectal adenoma risks: A colonoscopy-based case-control study in Korea. Am J Epidemiol. 2011;174(5):552-562
69. Chia WK, Ali R, Toh HC. Aspirin as adjuvant therapy for colorectal cancer-reinterpreting paradigms. Nat Rev Clin Oncol. 2012;9(10):561-570
70. Diergaarde B, Vrieling A, van Kraats AA, et al. Cigarette smoking and genetic alterations in sporadic colon carcinomas. Carcinogenesis. 2003;24(3):565-571
71. Satia JA, Keku T, Galanko JA, et al. Diet, lifestyle, and genomic instability in the North Carolina Colon Cancer Study. Cancer Epidemiol Biomarkers Prev. 2005;14(2): 429-436
72. Gay LJ, Arends MJ, Mitrou PN, et al. MLH1 promoter methylation, diet, and lifestyle factors in mismatch repair deficient colorectal cancer patients from EPIC-Norfolk. Nutr Cancer. 2011;63(7):1000-1010
73. Ang PW, Loh M, Liem N, et al. Comprehensive profiling of DNA methylation in colorectal cancer reveals subgroups with distinct clinicopathological and molecular features. BMC Cancer. 2010;10:227
74. Dahlin AM, Palmqvist R, Henriksson ML, et al. The role of the CpG island methylator phenotype in colorectal cancer prognosis depends on microsatellite instability screening status. Clin Cancer Res. 2010;16(6):1845-1855
75. Jover R, Nguyen TP, Perez-Carbonell L, et al. 5-Fluorouracil adjuvant chemotherapy does not increase survival in patients with CpG island methylator phenotype colorectal cancer. Gastroenterology. 2011;140(4):1174-1181
76. Hinoue T,Weisenberger DJ, Lange CP, et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. 2012;22(2):271-282
77. Wong JJ, Hawkins NJ,Ward RL, et al. Methylation of the 3p22 region encompassing MLH1 is representative of the CpG island methylator phenotype in colorectal cancer. Mod Pathol. 2011;24(3):396-411
78. Zlobec I, Bihl M, Foerster A, et al. Comprehensive analysis of CpG Island Methylator Phenotype (CIMP)-high, -low, and -negative colorectal cancers based on protein marker expression and molecular features. J Pathol. 2011;225(3):336-343
79. Yamamoto E, Suzuki H, Yamano HO, et al. Molecular dissection of premalignant colorectal lesions reveals early onset of the CpG Island Methylator Phenotype. Am J Pathol. 2012;181(5):1847-1861
80. Yagi K, Takahashi H, Akagi K, et al. Intermediate methylation epigenotype and its correlation to KRAS mutation in conventional colorectal adenoma. Am J Pathol. 2012; 180(2):616-625
81. Sproul D, Kitchen RR, Nestor CE, et al. Tissue of origin determines cancer-Associated CpG island promoter hypermethylation patterns. Genome Biol. 2012;13(10):R84
82. Xia D, Wang D, Kim SH, et al. Prostaglandin E(2) promotes intestinal tumor growth via DNA methylation. Nat Med. 2012;18(2):224-226
83. Wu C, Bekaii-Saab T. CpG island methylation, microsatellite instability, and BRAF mutations and their clinical application in the treatment of colon cancer. Chemother Res Pract. 2012;2012:359041