Tumor LINE-1 methylation level and colorectal cancer location in relation to patient survival

Oncotarget

Volumn 7, Issue 34, 2016, Pages 55098-55109

  Mima, Kosuke ^a   Nowak, Jonathan A ^b   Qian, Zhi Rong ^a   Cao, Yin ^c,d   Song, Mingyang ^c,d   Masugi, Yohei ^a   Shi, Yan ^a   da Silva, Annacarolina ^a   Gu, Mancang ^a   Li, Wanwan ^a   Hamada, Tsuyoshi ^a   Zhang, Xuehong ^b   Wu, Kana ^b,d   Meyerhardt, Jeffrey A ^a   Baba, Hideo ^e   Giovannucci, Edward L ^b,d   Chan, Andrew T ^b,c   Fuchs, Charles S ^a,b   Ogino, Shuji ^a,b,d   Nishihara, Reiko ^a,d  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Epigenetics; Left sided; Molecular pathological epidemiology; Prognosis; Right sided

Indexed keywords

B RAF KINASE; K RAS PROTEIN; PROTEIN PIK3CA; TUMOR PROTEIN; UNCLASSIFIED DRUG; KRAS PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PIK3CA PROTEIN, HUMAN; PROTEIN P21;

AGED; ARTICLE; CANCER LOCALIZATION; CANCER MORTALITY; CANCER SURVIVAL; COLON CANCER; COLORECTAL CANCER; CPG ISLAND; DESCENDING COLON; FEMALE; HUMAN; LONG INTERSPERSED REPEAT; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; MUTATION; PHENOTYPE; PROTEIN METHYLATION; COLON TUMOR; DNA METHYLATION; GENETICS; KAPLAN MEIER METHOD; MIDDLE AGED; MULTIVARIATE ANALYSIS; PATHOLOGY; PROGNOSIS; PROSPECTIVE STUDY; RECTUM TUMOR;

AGED; CLASS I PHOSPHATIDYLINOSITOL 3-KINASES; COLONIC NEOPLASMS; DNA METHYLATION; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; MULTIVARIATE ANALYSIS; MUTATION; PROGNOSIS; PROSPECTIVE STUDIES; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS P21(RAS); RECTAL NEOPLASMS;

EID: 84983479239     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.10398     Document Type: Article

References (66)

1. Kuipers EJ, Grady WM, Lieberman D, Seufferlein T, Sung JJ, Boelens PG, van de Velde CJH and Watanabe T. Colorectal cancer. Nature Reviews Disease Primers. 2015; 1:15065.
2. Sears CL and Garrett WS. Microbes, microbiota, and colon cancer. Cell Host Microbe. 2014; 15:317-328.
3. Keku TO, Dulal S, Deveaux A, Jovov B and Han X. The gastrointestinal microbiota and colorectal cancer. Am J Physiol Gastrointest Liver Physiol. 2015; 308:G351-363.
4. Tahara T, Yamamoto E, Suzuki H, Maruyama R, Chung W, Garriga J, Jelinek J, Yamano HO, Sugai T, An B, Shureiqi I, Toyota M, Kondo Y, et al. Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer Res. 2014; 74:1311-1318.
5. Dejea CM, Wick EC, Hechenbleikner EM, White JR, Mark Welch JL, Rossetti BJ, Peterson SN, Snesrud EC, Borisy GG, Lazarev M, Stein E, Vadivelu J, Roslani AC, et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A. 2014; 111:18321-18326.
6. Mima K, Sukawa Y, Nishihara R, Qian ZR, Yamauchi M, Inamura K, Kim SA, Masuda A, Nowak JA, Nosho K, Kostic AD, Giannakis M, Watanabe H, et al. Fusobacterium nucleatum and T Cells in Colorectal Carcinoma. JAMA Oncol. 2015; 1:653-661.
7. Yamauchi M, Morikawa T, Kuchiba A, Imamura Y, Qian ZR, Nishihara R, Liao X, Waldron L, Hoshida Y, Huttenhower C, Chan AT, Giovannucci E, Fuchs C, et al. Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum. Gut. 2012; 61:847-854.
8. Phipps AI, Limburg PJ, Baron JA, Burnett-Hartman AN, Weisenberger DJ, Laird PW, Sinicrope FA, Rosty C, Buchanan DD, Potter JD and Newcomb PA. Association between molecular subtypes of colorectal cancer and patient survival. Gastroenterology. 2015; 148:77-87 e72.
9. Rosty C, Young JP, Walsh MD, Clendenning M, Sanderson K, Walters RJ, Parry S, Jenkins MA, Win AK, Southey MC, Hopper JL, Giles GG, Williamson EJ, et al. PIK3CA activating mutation in colorectal carcinoma: associations with molecular features and survival. PLoS One. 2013; 8:e65479.
10. Ogino S, Nosho K, Irahara N, Meyerhardt JA, Baba Y, Shima K, Glickman JN, Ferrone CR, Mino-Kenudson M, Tanaka N, DranoffG, Giovannucci EL and Fuchs CS. Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype. Clin Cancer Res. 2009; 15:6412-6420.
11. Ghazi S, Lindforss U, Lindberg G, Berg E, Lindblom A and Papadogiannakis N. Analysis of colorectal cancer morphology in relation to sex, age, location, and family history. J Gastroenterol. 2012; 47:619-634.
12. Kirby JA, Bone M, Robertson H, Hudson M and Jones DE. The number of intraepithelial T cells decreases from ascending colon to rectum. J Clin Pathol. 2003; 56:158.
13. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH and Issa JP. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res. 2004; 32:e38.
14. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, Ehrlich M and Laird PW. Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res. 2005; 33:6823-6836.
15. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leonhardt H and Jaenisch R. Induction of tumors in mice by genomic hypomethylation. Science. 2003; 300:489-492.
16. Holm TM, Jackson-Grusby L, Brambrink T, Yamada Y, Rideout WM, 3rd and Jaenisch R. Global loss of imprinting leads to widespread tumorigenesis in adult mice. Cancer Cell. 2005; 8:275-285.
17. Suzuki K, Suzuki I, Leodolter A, Alonso S, Horiuchi S, Yamashita K and Perucho M. Global DNA demethylation in gastrointestinal cancer is age dependent and precedes genomic damage. Cancer Cell. 2006; 9:199-207.
18. Rodriguez J, Frigola J, Vendrell E, Risques RA, Fraga MF, Morales C, Moreno V, Esteller M, Capella G, Ribas M and Peinado MA. Chromosomal instability correlates with genome-wide DNA demethylation in human primary colorectal cancers. Cancer Res. 2006; 66:8462-9468.
19. Rajagopalan H, Nowak MA, Vogelstein B and Lengauer C. The significance of unstable chromosomes in colorectal cancer. Nat Rev Cancer. 2003; 3:695-701.
20. Mlecnik B, Bindea G, Angell HK, Sasso MS, Obenauf AC, Fredriksen T, Lafontaine L, Bilocq AM, Kirilovsky A, Tosolini M, Waldner M, Berger A, Fridman WH, et al. Functional network pipeline reveals genetic determinants associated with in situ lymphocyte proliferation and survival of cancer patients. Sci Transl Med. 2014; 6:228ra237.
21. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Chan AT, Schernhammer ES, Giovannucci EL and Fuchs CS. A cohort study of tumoral LINE-1 hypomethylation and prognosis in colon cancer. J Natl Cancer Inst. 2008; 100:1734-1738.
22. Nosho K, Baba Y, Tanaka N, Shima K, Hayashi M, Meyerhardt JA, Giovannucci E, DranoffG, Fuchs CS and Ogino S. Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review. J Pathol. 2010; 222:350-366.
23. Ahn JB, Chung WB, Maeda O, Shin SJ, Kim HS, Chung HC, Kim NK and Issa JP. DNA methylation predicts recurrence from resected stage III proximal colon cancer. Cancer. 2011; 117:1847-1854.
24. Rhee YY, Kim MJ, Bae JM, Koh JM, Cho NY, Juhnn YS, Kim D and Kang GH. Clinical outcomes of patients with microsatellite-unstable colorectal carcinomas depend on L1 methylation level. Ann Surg Oncol. 2012; 19:3441-3448.
25. Inamura K, Yamauchi M, Nishihara R, Lochhead P, Qian ZR, Kuchiba A, Kim SA, Mima K, Sukawa Y, Jung S, Zhang X, Wu K, Cho E, et al. Tumor LINE-1 methylation level and microsatellite instability in relation to colorectal cancer prognosis. J Natl Cancer Inst. 2014; 106.
26. Bartley AN, Parikh N, Hsu CH, Roe DJ, Buckmeier JA, Corley L, Phipps RA, Gallick G, Lance P, Thompson PA and Hamilton SR. Colorectal adenoma stem-like cell populations: associations with adenoma characteristics and metachronous colorectal neoplasia. Cancer Prev Res (Phila). 2013; 6:1162-1170.
27. Sinicrope FA, Shi Q, Smyrk TC, Thibodeau SN, Dienstmann R, Guinney J, Bot BM, Tejpar S, Delorenzi M, Goldberg RM, Mahoney M, Sargent DJ and Alberts SR. Molecular markers identify subtypes of stage III colon cancer associated with patient outcomes. Gastroenterology. 2015; 148:88-99.
28. Campbell PT, Newton CC, Newcomb PA, Phipps AI, Ahnen DJ, Baron JA, Buchanan DD, Casey G, Cleary SP, Cotterchio M, Farris AB, Figueiredo JC, Gallinger S, et al. Association between body mass index and mortality for colorectal cancer survivors: overall and by tumor molecular phenotype. Cancer Epidemiol Biomarkers Prev. 2015; 24:1229-1238.
29. Colussi D, Brandi G, Bazzoli F and Ricciardiello L. Molecular pathways involved in colorectal cancer: implications for disease behavior and prevention. Int J Mol Sci. 2013; 14:16365-16385.
30. Kocarnik JM, Shiovitz S and Phipps AI. Molecular phenotypes of colorectal cancer and potential clinical applications. Gastroenterol Rep (Oxf). 2015; 3:269-276.
31. Bardhan K and Liu K. Epigenetics and colorectal cancer pathogenesis. Cancers (Basel). 2013; 5:676-713.
32. Suzuki H, Yamamoto E, Maruyama R, Niinuma T and Kai M. Biological significance of the CpG island methylator phenotype. Biochem Biophys Res Commun. 2014; 455:35-42.
33. Benard A, van de Velde CJ, Lessard L, Putter H, Takeshima L, Kuppen PJ and Hoon DS. Epigenetic status of LINE-1 predicts clinical outcome in early-stage rectal cancer. Br J Cancer. 2013; 109:3073-3083.
34. Ogino S, Galon J, Fuchs CS and DranoffG. Cancer immunology-analysis of host and tumor factors for personalized medicine. Nat Rev Clin Oncol. 2011; 8:711-719.
35. Bishehsari F, Mahdavinia M, Vacca M, Malekzadeh R and Mariani-Costantini R. Epidemiological transition of colorectal cancer in developing countries: environmental factors, molecular pathways, and opportunities for prevention. World J Gastroenterol. 2014; 20:6055-6072.
36. Chia WK, Ali R and Toh HC. Aspirin as adjuvant therapy for colorectal cancer-reinterpreting paradigms. Nat Rev Clin Oncol. 2012; 9:561-570.
37. Ng JM and Yu J. Promoter hypermethylation of tumour suppressor genes as potential biomarkers in colorectal cancer. Int J Mol Sci. 2015; 16:2472-2496.
38. Martinez-Useros J and Garcia-Foncillas J. Obesity and colorectal cancer: molecular features of adipose tissue. J Transl Med. 2016; 14:21.
39. Nosho K, Sukawa Y, Adachi Y, Ito M, Mitsuhashi K, Kurihara H, Kanno S, Yamamoto I, Ishigami K, Igarashi H, Maruyama R, Imai K, Yamamoto H, et al. Association of Fusobacterium nucleatum with immunity and molecular alterations in colorectal cancer. World J Gastroenterol. 2016; 22:557-566.
40. Yamauchi M, Lochhead P, Morikawa T, Huttenhower C, Chan AT, Giovannucci E, Fuchs C and Ogino S. Colorectal cancer: a tale of two sides or a continuum? Gut. 2012; 61:794-797.
41. Kohoutova D, Smajs D, Moravkova P, Cyrany J, Moravkova M, Forstlova M, Cihak M, Rejchrt S and Bures J. Escherichia coli strains of phylogenetic group B2 and D and bacteriocin production are associated with advanced colorectal neoplasia. BMC Infect Dis. 2014; 14:733.
42. Li X, LeBlanc J, Truong A, Vuthoori R, Chen SS, Lustgarten JL, Roth B, Allard J, Ippoliti A, Presley LL, Borneman J, Bigbee WL, Gopalakrishnan V, et al. A metaproteomic approach to study human-microbial ecosystems at the mucosal luminal interface. PLoS One. 2011; 6:e26542.
43. Hayashi H, Takahashi R, Nishi T, Sakamoto M and Benno Y. Molecular analysis of jejunal, ileal, caecal and rectosigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. J Med Microbiol. 2005; 54:1093-1101.
44. Mowat AM and Agace WW. Regional specialization within the intestinal immune system. Nat Rev Immunol. 2014; 14:667-685.
45. Estecio MR, Gharibyan V, Shen L, Ibrahim AE, Doshi K, He R, Jelinek J, Yang AS, Yan PS, Huang TH, Tajara EH and Issa JP. LINE-1 hypomethylation in cancer is highly variable and inversely correlated with microsatellite instability. PLoS One. 2007; 2:e399.
46. Ogino S, Kawasaki T, Nosho K, Ohnishi M, Suemoto Y, Kirkner GJ and Fuchs CS. LINE-1 hypomethylation is inversely associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Int J Cancer. 2008; 122:2767-2773.
47. Baba Y, Huttenhower C, Nosho K, Tanaka N, Shima K, Hazra A, Schernhammer ES, Hunter DJ, Giovannucci EL, Fuchs CS and Ogino S. Epigenomic diversity of colorectal cancer indicated by LINE-1 methylation in a database of 869 tumors. Mol Cancer. 2010; 9:125.
48. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012; 487:330-337.
49. Tamas K, Walenkamp AM, de Vries EG, van Vugt MA, Beets-Tan RG, van Etten B, de Groot DJ and Hospers GA. Rectal and colon cancer: Not just a different anatomic site. Cancer Treat Rev. 2015; 41:671-679.
50. Ogino S, Nishihara R, Lochhead P, Imamura Y, Kuchiba A, Morikawa T, Yamauchi M, Liao X, Qian ZR, Sun R, Sato K, Kirkner GJ, Wang M, et al. Prospective study of family history and colorectal cancer risk by tumor LINE-1 methylation level. J Natl Cancer Inst. 2013; 105:130-140.
51. Meyerhardt JA and Mayer RJ. Systemic therapy for colorectal cancer. N Engl J Med. 2005; 352:476-487.
52. Hinoue T, Weisenberger DJ, Lange CP, Shen H, Byun HM, Van Den Berg D, Malik S, Pan F, Noushmehr H, van Dijk CM, Tollenaar RA and Laird PW. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res. 2012; 22:271-282.
53. Ogino S, Chan AT, Fuchs CS and Giovannucci E. Molecular pathological epidemiology of colorectal neoplasia: an emerging transdisciplinary and interdisciplinary field. Gut. 2011; 60:397-411.
54. Ogino S, Nishihara R, VanderWeele TJ, Wang M, Nishi A, Lochhead P, Qian ZR, Zhang X, Wu K, Nan H, Yoshida K, Milner DA, Jr., Chan AT, et al. Review Article: The Role of Molecular Pathological Epidemiology in the Study of Neoplastic and Non-neoplastic Diseases in the Era of Precision Medicine. Epidemiology. 2016; 27:602-611.
55. Nishihara R, VanderWeele TJ, Shibuya K, Mittleman MA, Wang M, Field AE, Giovannucci E, Lochhead P and Ogino S. Molecular pathological epidemiology gives clues to paradoxical findings. Eur J Epidemiol. 2015; 30:1129-1135.
56. Ikram MA. Molecular pathological epidemiology: the role of epidemiology in the omics-era. Eur J Epidemiol. 2015; 30:1077-1078.
57. Liao X, Lochhead P, Nishihara R, Morikawa T, Kuchiba A, Yamauchi M, Imamura Y, Qian ZR, Baba Y, Shima K, Sun R, Nosho K, Meyerhardt JA, et al. Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N Engl J Med. 2012; 367:1596-1606.
58. Nishihara R, Wu K, Lochhead P, Morikawa T, Liao X, Qian ZR, Inamura K, Kim SA, Kuchiba A, Yamauchi M, Imamura Y, Willett WC, Rosner BA, et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med. 2013; 369:1095-1105.
59. Irahara N, Nosho K, Baba Y, Shima K, Lindeman NI, Hazra A, Schernhammer ES, Hunter DJ, Fuchs CS and Ogino S. Precision of pyrosequencing assay to measure LINE-1 methylation in colon cancer, normal colonic mucosa, and peripheral blood cells. J Mol Diagn. 2010; 12:177-183.
60. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Meyerhardt JA, Loda M, Giovannucci EL and Fuchs CS. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut. 2009; 58:90-96.
61. Ogino S, Kawasaki T, Brahmandam M, Cantor M, Kirkner GJ, Spiegelman D, Makrigiorgos GM, Weisenberger DJ, Laird PW, Loda M and Fuchs CS. Precision and performance characteristics of bisulfite conversion and realtime PCR (MethyLight) for quantitative DNA methylation analysis. J Mol Diagn. 2006; 8:209-217.
62. Ogino S, Kawasaki T, Kirkner GJ, Kraft P, Loda M and Fuchs CS. Evaluation of markers for CpG island methylator phenotype (CIMP) in colorectal cancer by a large population-based sample. J Mol Diagn. 2007; 9:305-314.
63. Ogino S, Kawasaki T, Brahmandam M, Yan L, Cantor M, Namgyal C, Mino-Kenudson M, Lauwers GY, Loda M and Fuchs CS. Sensitive sequencing method for KRAS mutation detection by Pyrosequencing. J Mol Diagn. 2005; 7:413-421.
64. Imamura Y, Lochhead P, Yamauchi M, Kuchiba A, Qian ZR, Liao X, Nishihara R, Jung S, Wu K, Nosho K, Wang YE, Peng S, Bass AJ, et al. Analyses of clinicopathological, molecular, and prognostic associations of KRAS codon 61 and codon 146 mutations in colorectal cancer: cohort study and literature review. Mol Cancer. 2014; 13:135.
65. Nosho K, Kawasaki T, Ohnishi M, Suemoto Y, Kirkner GJ, Zepf D, Yan L, Longtine JA, Fuchs CS and Ogino S. PIK3CA mutation in colorectal cancer: relationship with genetic and epigenetic alterations. Neoplasia. 2008; 10:534-541.
66. Liao X, Morikawa T, Lochhead P, Imamura Y, Kuchiba A, Yamauchi M, Nosho K, Qian ZR, Nishihara R, Meyerhardt JA, Fuchs CS and Ogino S. Prognostic role of PIK3CA mutation in colorectal cancer: cohort study and literature review. Clin Cancer Res. 2012; 18:2257-2268.