The role of epigenetics in colorectal cancer

Expert Review of Gastroenterology and Hepatology

Volumn 8, Issue 8, 2014, Pages 935-948

  Coppedè, Fabio ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

Colorectal cancer; DNA methylation; Epigenetics; Epigenotype; Histone acetylation; Histone methylation; Histone tail modification; MiRNA; Non coding RNA

Indexed keywords

4 PHENYLBUTYRIC ACID; BIOLOGICAL MARKER; CETUXIMAB; DACARBAZINE; FLUOROPYRIMIDINE; FLUOROURACIL; FOLINIC ACID; HISTONE; IRINOTECAN; MICRORNA; OXALIPLATIN; PANITUMUMAB; UNTRANSLATED RNA; VALPROIC ACID; VORINOSTAT;

CANCER DIAGNOSIS; CANCER PROGNOSIS; CARCINOGENESIS; COLON MUCOSA; COLORECTAL CANCER; CPG ISLAND METHYLATOR PHENOTYPE; DNA METHYLATION; DRUG RESPONSE; ENVIRONMENTAL FACTOR; EPIGENETICS; GENE EXPRESSION; GENE MUTATION; GENOTYPE; HEREDITARY COLORECTAL CANCER; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; INTESTINE CRYPT; OVERALL SURVIVAL; REVIEW; COLORECTAL TUMOR; GENETIC EPIGENESIS; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

COLORECTAL NEOPLASMS; DNA METHYLATION; EPIGENESIS, GENETIC; HISTONES; HUMANS;

EID: 84905594502     PISSN: 17474124     EISSN: 17474132     Source Type: Journal    
DOI: 10.1586/17474124.2014.924397     Document Type: Review

References (111)

1. Butler EN, Chawla N, Lund J, et al. Patterns of colorectal cancer care in the United States and Canada: a systematic review. J Natl Cancer Inst Monogr 2013; 2013(46):13-35
2. Altobelli E, Lattanzi A, Paduano R, et al. Colorectal cancer prevention in Europe: Burden of disease and status of screening programs. Prev Med 2014;62C:132-41
3. Chawla N, Butler EN, Lund J, et al. Patterns of colorectal cancer care in Europe, Australia, and New Zealand. J Natl Cancer Inst Monogr 2013;2013(46):36-61
4. Wilkes G, Hartshorn K. Clinical update: colon, rectal, and anal cancers. Semin Oncol Nurs 2012;28(4):e1-e22
5. Migliore L, Migheli F, Spisni R, Coppedè F. Genetics, cytogenetics, and epigenetics of colorectal cancer. J Biomed Biotechnol 2011;2011:792362
6. Bardhan K, Liu K. Epigenetics and colorectal cancer pathogenesis. Cancers 2013;5(2):676-713
7. Zoratto F, Rossi L, Verrico M, et al. Focus on genetic and epigenetic events of colorectal cancer pathogenesis: implications for molecular diagnosis. Tumor Biol 2014; In press
8. Coppedè F. Epigenetic biomarkers of colorectal cancer: focus on DNA methylation. Cancer Lett 2014;342(2): 238-47
9. Laird PW. The power and the promise of DNA methylation markers. Nat Rev Cancer 2003;3(4):253-66
10. Curtin K, Slattery ML, Samowitz WS. CpG island methylation in colorectal cancer: past, present and future. Patholog Res Int 2011;2011:902674
11. Shen L, Toyota M, Kondo Y, et al. Integrated genetic and epigenetic analysis identifies three different subclasses of colon cancer. Proc Natl Acad Sci USA 2007; 104(47):18654-9 • The study allowed the identification of three methylation subgroups in colorectal cancer (CRC).
12. Yagi K, Akagi K, Hayashi H, et al. Three DNA methylation epigenotypes in human colorectal cancer. Clin Cancer Res 2010; 16(1):21-33 • Large-scale study that defined three methylation epigenotypes in CRC.
13. Hinoue T, Weisenberger DJ, Lange CP, et al. Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res 2012;22(2):271-82 • Large-scale study that defined three methylation epigenotypes in CRC.
14. Al-Sohaily S, Biankin A, Leong R, et al. Molecular pathways in colorectal cancer. J Gastroenterol Hepatol 2012;27(9): 1423-31
15. Sakai E, Ohata K, Chiba H, et al. Methylation epigenotypes and genetic features in colorectal laterally spreading tumours. Int J Cancer 2014; In press • The study analyzed the methylation epigenotypes in laterally spreading CRC.
16. Coppedè F, Lopomo A, Spisni R, Migliore L. Genetic and epigenetic biomarkers for diagnosis, prognosis and treatment of colorectal cancer. World J Gastroenterol 2014;20(4):943-56
17. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012;13(7):484-92
18. Ballestar E, Wolffe AP. Methyl-CpG-binding proteins. Targeting specific gene repression. Eur J Biochem 2001;268(1):1-6
19. Luger K, Mäder AW, Richmond RK, et al. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997; 389(6648):251-60
20. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007;447(7143):407-12
21. Martin C, Zhang Y. The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 2005;6(11):838-49
22. Sato F, Tsuchiya S, Meltzer SJ, Shimizu K. MicroRNAs and epigenetics. FEBS J 2011; 278(10):1598-609
23. Moazed D. Small RNAs in transcriptional gene silencing and genome defence. Nature 2009;457(7228):413-20
24. Saxena A, Carninci P. Long non-coding RNA modifies chromatin: epigenetic silencing by long non-coding RNAs. Bioessays 2011;33(11):830-9
25. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983;301(5895):89-92 •• One of the first evidence of impaired DNA methylation in CRC.
26. Lao VV, Grady WM. Epigenetics and colorectal cancer. Nat Rev Gastroenterol Hepatol 2011;8(12):686-700 •• A comprehensive review of the genes showing impaired DNA methylation in the various steps of CRC.
27. Toyota M, Ahuja N, Ohe-Toyota M, et al. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 1999;96(15):8681-6 •• Definition of the CpG island methylator phenotype in CRC.
28. Karpinski P, Walter M, Szmida E, et al. Intermediate- and low-methylation epigenotypes do not correspond to CpG island methylator phenotype (low and -zero) in colorectal cancer. Cancer Epidemiol Biomarkers Prev 2013;22(2):201-8
29. Sakai E, Nakajima A, Kaneda A. Accumulation of aberrant DNA methylation during colorectal cancer development. World J Gastroenterol 2014;20(4):978-87
30. Issa JP. Colon cancer: it's CIN or CIMP. Clin Cancer Res 2008;14(19):5939-40
31. Rex DK, Ahnen DJ, Baron JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012;107(9):1315-29
32. Thiel A, Ristimäki A. Toward a molecular classification of colorectal cancer: the role of BRAF. Front Oncol 2013;3:281
33. Coppedè F, Migheli F, Lopomo A, et al. Gene promoter methylation in colorectal cancer and healthy adjacent mucosa specimens: correlation with physiological and pathological characteristics, and with biomarkers of one-carbon metabolism. Epigenetics 2014;9(4):621-33
34. Colussi D, Brandi G, Bazzoli F, Ricciardiello L. Molecular pathways involved in colorectal cancer: implications for disease behavior and prevention. Int J Mol Sci 2013;14(8):16365-85
35. Guerrero S, Casanova I, Farré L, et al. K-ras codon 12 mutation induces higher level of resistance to apoptosis and predisposition to anchorage-independent growth than codon 13 mutation or proto-oncogene overexpression. Cancer Res 2000;60(23): 6750-6
36. Minoo P. Toward a Molecular Classification of Colorectal Cancer: the Role of MGMT. Front Oncol 2013;3:266
37. Jass JR, Baker K, Zlobec I, et al. Advanced colorectal polyps with the molecular and morphological features of serrated polyps and adenomas: concept of a 'fusion' pathway to colorectal cancer. Histopathology 2006;49(2):121-31
38. Iacopetta B, Russo A, Bazan V, et al. Functional categories of TP53 mutation in colorectal cancer: results of an International Collaborative Study. Ann Oncol 2006; 17(5):842-7
39. Lambert R, Tanaka S. Laterally spreading tumors in the colon and rectum. Eur J Gastroenterol Hepatol 2012;24(10): 1123-11234
40. Moon BS, Jeong WJ, Park J, et al. Role of oncogenic K-Ras in cancer stem cell activation by aberrant Wnt/β-catenin signaling. J Natl Cancer Inst 2014;106(2): djt373
41. Gazzoli I, Loda M, Garber J, et al. A hereditary nonpolyposis colorectal carcinoma case associated with hypermethylation of the MLH1 gene in normal tissue and loss of heterozygosity of the unmethylated allele in the resulting microsatellite instability-high tumor. Cancer Res 2002;62(14):3925-8
42. Venkatachalam R, Ligtenberg MJ, Hoogerbrugge N, et al. The epigenetics of (hereditary) colorectal cancer. Cancer Genet Cytogenet 2010;203(1):1-6 •• An authoritative review of the epigenetics of hereditary CRC.
43. Hitchins MP. The role of epigenetics in Lynch syndrome. Fam Cancer 2013;12(2): 189-205
44. Ligtenberg MJ, Kuiper RP, Chan TL, et al. Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3' exons of TACSTD1. Nat Genet 2009; 41(1):112-17
45. Kaz AM, Wong CJ, Dzieciatkowski S, et al. Patterns of DNA methylation in the normal colon vary by anatomical location, gender, and age. Epigenetics 2014;9(4):492-502
46. Ramírez N, Bandrés E, Navarro A, et al. Epigenetic events in normal colonic mucosa surrounding colorectal cancer lesions. Eur J Cancer 2008;44(17):2689-95
47. Krakowczyk L, Strzelczyk JK, Adamek B, et al. Methylation of the MGMT and p16 genes in sporadic colorectal carcinoma and corresponding normal colonic mucosa. Med Sci Monit 2008;14(10):BR219-25
48. Rawson JB, Sun Z, Dicks E, et al. Vitamin D intake is negatively associated with promoter methylation of the Wnt antagonist gene DKK1 in a large group of colorectal cancer patients. Nutr Cancer 2012;64(7):919-28
49. 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):1012-22
50. 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):1731-8
51. Nishihara R, Morikawa T, Kuchiba A, et al. A prospective study of duration of smoking cessation and colorectal cancer risk by epigenetics-related tumor classification. Am J Epidemiol 2013;178(1):84-100
52. 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):1000-10
53. 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
54. Wu AH, Siegmund KD, Long TI, et al. Hormone therapy, DNA methylation and colon cancer. Carcinogenesis 2010;31(6): 1060-7
55. Ogino S, Lochhead P, Chan AT, et al. Molecular pathological epidemiology of epigenetics: emerging integrative science to analyze environment, host, and disease. Mod Pathol 2013;26(4):465-84
56. Reimers MS, Zeestraten EC, Kuppen PJ, et al. Biomarkers in precision therapy in colorectal cancer. Gastroenterol Rep (Oxf) 2013;1(3):166-83
57. Febbo PG, Ladanyi M, Aldape KD, et al. NCCN Task Force report: Evaluating the clinical utility of tumor markers in oncology. J Natl Compr Canc Netw 2011; 9(Suppl 5):S1-S32
58. Grützmann R, Molnar B, Pilarsky C, et al. Sensitive detection of colorectal cancer in peripheral blood by septin 9 DNA methylation assay. PLoS One 2008; 3(11):e3759
59. Gyparaki MT, Basdra EK, Papavassiliou AG. DNA methylation biomarkers as diagnostic and prognostic tools in colorectal cancer. J Mol Med (Berl) 2013;91(11):1249-56
60. Itzkowitz S, Brand R, Jandorf L, et al. A simplified, noninvasive stool DNA test for colorectal cancer detection. Am J Gastroenterol 2008;103(11):2862-70 • A study that opened the way for the development of non-invasive epigenetic diagnostic tools of CRC.
61. Yang H, Xia BQ, Jiang B, et al. Diagnostic value of stool DNA testing for multiple markers of colorectal cancer and advanced adenoma: a meta-analysis. Can J Gastroenterol 2013;27(8):467-75
62. Guo Q, Song Y, Zhang H, et al. Detection of hypermethylated fibrillin-1 in the stool samples of colorectal cancer patients. Med Oncol 2013;30(4):695
63. Imperiale TF, Ransohoff DF, Itzkowitz SH, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med 2014; In press
64. Nilsson TK, Löf-Öhlin ZM, Sun XF. DNA methylation of the p14ARF, RASSF1A and APC1A genes as an independent prognostic factor in colorectal cancer patients. Int J Oncol 2013;42:127-33
65. Xing X, Cai W, Shi H, et al. The prognostic value of CDKN2A hypermethylation in colorectal cancer: a meta-analysis. Br J Cancer 2013;108:2542-8
66. Kohonen-Corish MR, Tseung J, Chan C, et al. K-RAS mutations and CDKN2A promoter methylation show an interactive adverse effect on survival and predict recurrence of rectal cancer. Int J Cancer 2014;134(12):2820-8
67. Jensen LH, Rasmussen AA, Byriel L, et al. Regulation of MLH1 mRNA and protein expression by promoter methylation in primary colorectal cancer: a descriptive and prognostic cancer marker study. Cell Oncol (Dordr) 2013;36(5):411-19
68. Bae JM, Kim JH, Cho NY, et al. Prognostic implication of the CpG island methylator phenotype in colorectal cancers depends on tumour location. Br J Cancer 2013;109(4):1004-12
69. Katoh H, Yamashita K, Waraya M, et al. Epigenetic silencing of HOPX promotes cancer progression in colorectal cancer. Neoplasia 2012;14(7):559-71
70. Yi JM, Dhir M, Van Neste L, et al. Genomic and epigenomic integration identifies a prognostic signature in colon cancer. Clin Cancer Res 2011;17(6): 1535-45
71. Baba Y, Nosho K, Shima K, et al. Hypomethylation of the IGF2 DMR in colorectal tumors, detected by bisulfite pyrosequencing, is associated with poor prognosis. Gastroenterology 2010;139(6): 1855-64
72. Draht MX, Smits KM, Tournier B, et al. Promoter CpG island methylation of RET predicts poor prognosis in stage II colorectal cancer patients. Mol Oncol 2014; in press
73. Dallol A, Al-Maghrabi J, Buhmeida A, et al. Methylation of the polycomb group target genes is a possible biomarker for favorable prognosis in colorectal cancer. Cancer Epidemiol Biomarkers Prev 2012;21(11): 2069-75
74. Amatu A, Sartore-Bianchi A, Moutinho C, et al. Promoter CpG island hypermethylation of the DNA repair enzyme MGMT predicts clinical response to dacarbazine in a phase II study for metastatic colorectal cancer. Clin Cancer Res 2013;19(8):2265-72
75. Ebert MP, Tänzer M, Balluff B, et al. TFAP2E-DKK4 and chemoresistance in colorectal cancer. N Engl J Med 2012; 366(1):44-53
76. Goel A, Boland CR. Epigenetics of colorectal cancer. Gastroenterology 2012; 143(6):1442-60
77. Gargalionis AN, Piperi C, Adamopoulos C, Papavassiliou AG. Histone modifications as a pathogenic mechanism of colorectal tumorigenesis. Int J Biochem Cell Biol 2012;44(8):1276-89 •• An authoritative review of the role of histone tail modifications in CRC.
78. Zhou J, Zhan S, Tan W, et al. P300 binds to and acetylates MTA2 to promote colorectal cancer cells growth. Biochem Biophys Res Commun 2014;444(3):387-90
79. Rönsch K, Jäger M, Schöpflin A, et al. Class I and III HDACs and loss of active chromatin features contribute to epigenetic silencing of CDX1 and EPHB tumor suppressor genes in colorectal cancer. Epigenetics 2011;6(5):610-22
80. Stypula-Cyrus Y, Damania D, Kunte DP, et al. HDAC up-regulation in early colon field carcinogenesis is involved in cell tumorigenicity through regulation of chromatin structure. PLoS One 2013;8(5): e64600
81. Nosho K, Shima K, Irahara N, et al. SIRT1 histone deacetylase expression is associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Mod Pathol 2009;22(7): 922-32
82. Nakazawa T, Kondo T, Ma D, et al. Global histone modification of histone H3 in colorectal cancer and its precursor lesions. Hum Pathol 2012;43(6):834-42
83. Tamagawa H, Oshima T, Numata M, et al. Global histone modification of H3K27 correlates with the outcomes in patients with metachronous liver metastasis of colorectal cancer. Eur J Surg Oncol 2013; 39(6):655-61
84. Simon JA, Kingston RE. Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 2009; 10(10):697-708
85. Ohm JE, McGarvey KM, Yu X, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007;39(2):237-42
86. Berry WL, Janknecht R. KDM4/JMJD2 histone demethylases: epigenetic regulators in cancer cells. Cancer Res 2013; 73(10):2936-42
87. Jie D, Zhongmin Z, Guoqing L, et al. Positive expression of LSD1 and negative expression of E-cadherin correlate with metastasis and poor prognosis of colon cancer. Dig Dis Sci 2013;58(6):1581-9
88. Gezer U, Ustek D, Yörüker EE, et al. Characterization of H3K9me3- and H4K20me3-associated circulating nucleosomal DNA by high-throughput sequencing in colorectal cancer. Tumour Biol 2013;34(1):329-36
89. Tamagawa H, Oshima T, Shiozawa M, et al. The global histone modification pattern correlates with overall survival in metachronous liver metastasis of colorectal cancer. Oncol Rep 2012;27(3):637-42
90. Vaiopoulos AG, Athanasoula KC, Papavassiliou AG. Epigenetic modifications in colorectal cancer: Molecular insights and therapeutic challenges. Biochim Biophys Acta 2014;1842(7):971-80
91. Michael MZ, O' Connor SM, van Holst Pellekaan NG, et al. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 2003; 1(12):882-91 • Early evidence of deregulated expression of microRNAs in CRC.
92. Bonfrate L, Altomare DF, Di Lena M, et al. MicroRNA in colorectal cancer: new perspectives for diagnosis, prognosis and treatment. J Gastrointestin Liver Dis 2013; 22(3):311-20 •• An authoritative review of microRNAs in CRC.
93. PubMed database. Available from: www.ncbi.nlm.nih.gov/pubmed
94. Aslam MI, Patel M, Singh B, et al. MicroRNA manipulation in colorectal cancer cells: from laboratory to clinical application. J Transl Med 2013;10:128 •• Links specific microRNAs to the different steps of CRC.
95. Asangani IA, Rasheed SA, Nikolova DA, et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 2008;27(15):2128-36
96. Lou X, Qi X, Zhang Y, et al. Decreased expression of microRNA-625 is associated with tumor metastasis and poor prognosis in patients with colorectal cancer. J Surg Oncol 2013;108(4):230-5
97. Bojmar L, Karlsson E, Ellega˚rd S, et al. The role of microRNA-200 in progression of human colorectal and breast cancer. PLoS One 2013;8(12):e84815
98. Liu Y, Zhou Y, Feng X, et al. Low expression of microRNA-126 is associated with poor prognosis in colorectal cancer. Genes Chromosomes Cancer 2014;53(4): 358-65
99. Slattery ML, Wolff E, Hoffman MD, et al. MicroRNAs and colon and rectal cancer: differential expression by tumor location and subtype. Genes Chromosomes Cancer 2011;50(3):196-206
100. Mosakhani N, Sarhadi VK, Borze I, et al. MicroRNA profiling differentiates colorectal cancer according to K-RAS status. Genes Chromosomes Cancer 2012;51(1):1-9
101. Nosho K, Igarashi H, Nojima M, et al. Association of microRNA-31 with BRAF mutation, colorectal cancer survival and serrated pathway. Carcinogenesis 2014; 35(4):776-83
102. Svoboda M, Slyskova J, Schneiderova M, et al. HOTAIR long non-coding RNA is a negative prognostic factor not only in primary tumors, but also in the blood of colorectal cancer patients. Carcinogenesis 2014; In press
103. Qi P, Xu MD, Ni SJ, et al. Down-regulation of ncRAN, a long non-coding RNA, contributes to colorectal cancer cell migration and invasion and predicts poor overall survival for colorectal cancer patients. Mol Carcinog 2014; In press
104. Xiang JF, Yin QF, Chen T, et al. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res 2014; In press
105. Wang G, Li Z, Zhao Q, et al. LincRNA-p21 enhances the sensitivity of radiotherapy for human colorectal cancer by targeting the Wnt/β-catenin signaling pathway. Oncol Rep 2014;31(4):1839-45
106. Xu MD, Qi P, Du X. Long non-coding RNAs in colorectal cancer: implications for pathogenesis and clinical application. Mod Pathol 2014; In press
107. Zhou XJ, Dong ZG, Yang YM, et al. Limited diagnostic value of microRNAs for detecting colorectal cancer: a meta-analysis. Asian Pac J Cancer Prev 2013;14(8): 4699-704
108. Diaz T, Tejero R, Moreno I, et al. Role of miR-200 family members in survival of colorectal cancer patients treated with fluoropyrimidines. J Surg Oncol 2014; In press
109. Pichler M, Ress AL, Winter E, et al. MiR-200a regulates epithelial to mesenchymal transition-related gene expression and determines prognosis in colorectal cancer patients. Br J Cancer 2014; 110(6):1614-421
110. Xia X, Yang B, Zhai X, et al. Prognostic role of microRNA-21 in colorectal cancer: a meta-analysis. PLoS One 2013;8(11): e80426
111. Chen Q, Xia HW, Ge XJ, et al. Serum miR-19a predicts resistance to FOLFOX chemotherapy in advanced colorectal cancer cases. Asian Pac J Cancer Prev 2013;14(12): 7421-6