Identification of subgroup-specific mirna patterns by epigenetic profiling of sporadic and lynch syndrome-associated colorectal and endometrial carcinoma

Clinical Epigenetics

Volumn 7, Issue 1, 2015, Pages

  Kaur, Sippy ^a   Lotsari, Johanna E ^a   Al Sohaily, Sam ^b   Warusavitarne, Janindra ^b   Kohonen Corish, Maija Rj ^b,c,d   Peltomäki, Päivi ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c ST VINCENT S HOSPITAL   (Australia)

^d UNIVERSITY OF WESTERN SYDNEY   (Australia)

Author keywords

Colorectal cancer; Endometrial cancer; Lynch syndrome; Methylation; Microsatellite instability; MiRNA

Indexed keywords

MICRORNA; MICRORNA 129 2; MICRORNA 132; MICRORNA 345; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER GROWTH; CONTROLLED STUDY; CPG ISLAND; DISEASE ASSOCIATION; DNA METHYLATION; ENDOMETRIUM CARCINOMA; ENDOMETRIUM HYPERPLASIA; EPIGENETICS; FEMALE; GEOGRAPHIC ORIGIN; HEREDITARY NONPOLYPOSIS COLORECTAL CANCER; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MISMATCH REPAIR; PRIORITY JOURNAL; RNA ANALYSIS; RNA METHYLATION; UPREGULATION;

EID: 84927154459     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-015-0059-3     Document Type: Article

References (63)

1. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet. 2011;12:99–110.
2. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011;39:D152–7.
3. Chang TC, Mendell JT. microRNAs in vertebrate physiology and human disease. Annu Rev Genomics Hum Genet. 2007;8:215–39.
4. Saini HK, Enright AJ, Griffiths-Jones S. Annotation of mammalian primary microRNAs. BMC Genomics. 2008;9:564. 2164-9-564.
5. Shenouda SK, Alahari SK. MicroRNA function in cancer: oncogene or a tumor suppressor? Cancer Metastasis Rev. 2009;28:369–78.
6. Ozsolak F, Poling LL, Wang Z, Liu H, Liu XS, Roeder RG, et al. Chromatin structure analyses identify miRNA promoters. Genes Dev. 2008;22:3172–83.
7. Suzuki H, Takatsuka S, Akashi H, Yamamoto E, Nojima M, Maruyama R, et al. Genome-wide profiling of chromatin signatures reveals epigenetic regulation of MicroRNA genes in colorectal cancer. Cancer Res. 2011;71:5646–58.
8. Baer C, Claus R, Frenzel LP, Zucknick M, Park YJ, Gu L, et al. Extensive promoter DNA hypermethylation and hypomethylation is associated with aberrant microRNA expression in chronic lymphocytic leukemia. Cancer Res. 2012;72:3775–85.
9. Popovic R, Licht JD. Emerging epigenetic targets and therapies in cancer medicine. Canc Discov. 2012;2:405–13.
10. Vilar E, Gruber SB. Microsatellite instability in colorectal cancer-the stable evidence. Nat Rev Clin Oncol. 2010;7:153–62.
11. Joensuu EI, Abdel-Rahman WM, Ollikainen M, Ruosaari S, Knuutila S, Peltomaki P. Epigenetic signatures of familial cancer are characteristic of tumor type and family category. Cancer Res. 2008;68:4597–605.
12. Gylling AH, Nieminen TT, Abdel-Rahman WM, Nuorva K, Juhola M, Joensuu EI, et al. Differential cancer predisposition in Lynch syndrome: insights from molecular analysis of brain and urinary tract tumors. Carcinogenesis. 2008;29:1351–9.
13. Whitcomb BP, Mutch DG, Herzog TJ, Rader JS, Gibb RK, Goodfellow PJ. Frequent HOXA11 and THBS2 promoter methylation, and a methylator phenotype in endometrial adenocarcinoma. Clin Cancer Res. 2003;9:2277–87.
14. Ahmed D, Eide PW, Eilertsen IA, Danielsen SA, Eknaes M, Hektoen M, et al. Epigenetic and genetic features of 24 colon cancer cell lines. Oncogenesis. 2013;2:e71.
15. Mouradov D, Sloggett C, Jorissen RN, Love CG, Li S, Burgess AW, et al. Colorectal cancer cell lines are representative models of the main molecular subtypes of primary cancer. Cancer Res. 2014;74:3238–47.
16. Pavicic W, Perkio E, Kaur S, Peltomaki P. Altered methylation at microRNA-associated CpG islands in hereditary and sporadic carcinomas: a methylation-specific multiplex ligation-dependent probe amplification (MS-MLPA)-based approach. Mol Med. 2011;17:726–35.
17. Kohonen-Corish MR, Sigglekow ND, Susanto J, Chapuis PH, Bokey EL, Dent OF, et al. Promoter methylation of the mutated in colorectal cancer gene is a frequent early event in colorectal cancer. Oncogene. 2007;26:4435–41.
18. Zhang S, Hao J, Xie F, Hu X, Liu C, Tong J, et al. Downregulation of miR-132 by promoter methylation contributes to pancreatic cancer development. Carcinogenesis. 2011;32:1183–9.
19. Formosa A, Lena AM, Markert EK, Cortelli S, Miano R, Mauriello A, et al. DNA methylation silences miR-132 in prostate cancer. Oncogene. 2013;32:127–34.
20. Zheng YB, Luo HP, Shi Q, Hao ZN, Ding Y, Wang QS, et al. miR-132 inhibits colorectal cancer invasion and metastasis via directly targeting ZEB2. World J Gastroenterol. 2014;20:6515–22.
21. Jover R, Nguyen TP, Perez-Carbonell L, Zapater P, Paya A, Alenda C, et al. 5-Fluorouracil adjuvant chemotherapy does not increase survival in patients with CpG island methylator phenotype colorectal cancer. Gastroenterology. 2011;140:1174–81.
22. Tang JT, Wang JL, Du W, Hong J, Zhao SL, Wang YC, et al. MicroRNA 345, a methylation-sensitive microRNA is involved in cell proliferation and invasion in human colorectal cancer. Carcinogenesis. 2011;32:1207–15.
23. Bandres E, Agirre X, Bitarte N, Ramirez N, Zarate R, Roman-Gomez J, et al. Epigenetic regulation of microRNA expression in colorectal cancer. Int J Cancer. 2009;125:2737–43.
24. Tsai KW, Wu CW, Hu LY, Li SC, Liao YL, Lai CH, et al. Epigenetic regulation of miR-34b and miR-129 expression in gastric cancer. Int J Cancer. 2011;129:2600–10.
25. Huang YW, Liu JC, Deatherage DE, Luo J, Mutch DG, Goodfellow PJ, et al. Epigenetic repression of microRNA-129-2 leads to overexpression of SOX4 oncogene in endometrial cancer. Cancer Res. 2009;69:9038–46.
26. Anwar SL, Albat C, Krech T, Hasemeier B, Schipper E, Schweitzer N, et al. Concordant hypermethylation of intergenic microRNA genes in human hepatocellular carcinoma as new diagnostic and prognostic marker. Int J Cancer. 2013;133:660–70.
27. Nieminen TT, Gylling A, Abdel-Rahman WM, Nuorva K, Aarnio M, Renkonen-Sinisalo L, et al. Molecular analysis of endometrial tumorigenesis: importance of complex hyperplasia regardless of atypia. Clin Cancer Res. 2009;15:5772–83.
28. Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL, et al. Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet. 2009;5:e1000602.
29. Fraser HB, Lam LL, Neumann SM, Kobor MS. Population-specificity of human DNA methylation. Genome Biol. 2012;13:R8. 2012-13-2-r8.
30. Nieminen TT, Shoman S, Eissa S, Peltomaki P, Abdel-Rahman WM. Distinct genetic and epigenetic signatures of colorectal cancers according to ethnic origin. Cancer Epidemiol Biomarkers Prev. 2012;21:202–11.
31. McCabe MT, Brandes JC, Vertino PM. Cancer DNA methylation: molecular mechanisms and clinical implications. Clin Cancer Res. 2009;15:3927–37.
32. Samowitz WS, Curtin K, Wolff RK, Albertsen H, Sweeney C, Caan BJ, et al. The MLH1–93 G > A promoter polymorphism and genetic and epigenetic alterations in colon cancer. Genes Chromosomes Canc. 2008;47:835–44.
33. Gal-Yam EN, Saito Y, Egger G, Jones PA. Cancer epigenetics: modifications, screening, and therapy. Annu Rev Med. 2008;59:267–80.
34. How Kit A, Nielsen HM, Tost J. DNA methylation based biomarkers: practical considerations and applications. Biochimie. 2012;94:2314–37.
35. Tournier B, Chapusot C, Courcet E, Martin L, Lepage C, Faivre J, et al. Why do results conflict regarding the prognostic value of the methylation status in colon cancers? The role of the preservation method. BMC Cancer. 2012;12:12. 2407-12-12.
36. Nygren AO, Ameziane N, Duarte HM, Vijzelaar RN, Waisfisz Q, Hess CJ, et al. Methylation-specific MLPA (MS-MLPA): simultaneous detection of CpGmethylation and copy number changes of up to 40 sequences. Nucleic Acids Res. 2005;33:e128.
37. Homig-Holzel C, Savola S. Multiplex ligation-dependent probe amplification (MLPA) in tumor diagnostics and prognostics. Diagn Mol Pathol. 2012;21:189–206.
38. Reed K, Poulin ML, Yan L, Parissenti AM. Comparison of bisulfite sequencing PCR with pyrosequencing for measuring differences in DNA methylation. Anal Biochem. 2010;397:96–106.
39. Paliwal A, Vaissiere T, Herceg Z. Quantitative detection of DNA methylation states in minute amounts of DNA from body fluids. Methods. 2010;52:242–7.
40. Leong KJ, Wei W, Tannahill LA, Caldwell GM, Jones CE, Morton DG, et al. Methylation profiling of rectal cancer identifies novel markers of early-stage disease. Br J Surg. 2011;98:724–34.
41. Niskakoski A, Kaur S, Staff S, Renkonen-Sinisalo L, Lassus H, Järvinen HJ, et al. Epigenetic analysis of sporadic and Lynch-associated ovarian cancers reveals histology-specific patterns of DNA methylation. Epigenetics. 2014;9:1577–87.
42. Gao W, Kondo Y, Shen L, Shimizu Y, Sano T, Yamao K, et al. Variable DNA methylation patterns associated with progression of disease in hepatocellular carcinomas. Carcinogenesis. 2008;29:1901–10.
43. Wu J, Qian J, Li C, Kwok L, Cheng F, Liu P, et al. miR-129 regulates cell proliferation by downregulating Cdk6 expression. Cell Cycle. 2010;9:1809–18.
44. Liao R, Sun J, Zhang L, Lou G, Chen M, Zhou D, et al. MicroRNAs play a role in the development of human hematopoietic stem cells. J Cell Biochem. 2008;104:805–17.
45. Bartley AN, Yao H, Barkoh BA, Ivan C, Mishra BM, Rashid A, et al. Complex patterns of altered MicroRNA expression during the adenoma-adenocarcinoma sequence for microsatellite-stable colorectal cancer. Clin Cancer Res. 2011;17:7283–93.
46. Oberg AL, French AJ, Sarver AL, Subramanian S, Morlan BW, Riska SM, et al. miRNA expression in colon polyps provides evidence for a multihit model of colon cancer. PLoS One. 2011;6:e20465.
47. Boren T, Xiong Y, Hakam A, Wenham R, Apte S, Wei Z, et al. MicroRNAs and their target messenger RNAs associated with endometrial carcinogenesis. Gynecol Oncol. 2008;110:206–15.
48. Lee H, Choi HJ, Kang CS, Lee HJ, Lee WS, Park CS. Expression of miRNAs and PTEN in endometrial specimens ranging from histologically normal to hyperplasia and endometrial adenocarcinoma. Mod Pathol. 2012;25:1508–15.
49. Horn LC, Meinel A, Handzel R, Einenkel J. Histopathology of endometrial hyperplasia and endometrial carcinoma: an update. Ann Diagn Pathol. 2007;11:297–311.
50. Ahnen DJ. The American College of Gastroenterology Emily Couric Lecture–the adenoma-carcinoma sequence revisited: has the era of genetic tailoring finally arrived? Am J Gastroenterol. 2011;106:190–8.
51. Balaguer F, Moreira L, Lozano JJ, Link A, Ramirez G, Shen Y, et al. Colorectal cancers with microsatellite instability display unique miRNA profiles. Clin Cancer Res. 2011;17:6239–49.
52. Earle JS, Luthra R, Romans A, Abraham R, Ensor J, Yao H, et al. Association of microRNA expression with microsatellite instability status in colorectal adenocarcinoma. J Mol Diagn. 2010;12:433–40.
53. Sarver AL, French AJ, Borralho PM, Thayanithy V, Oberg AL, Silverstein KA, et al. Human colon cancer profiles show differential microRNA expression depending on mismatch repair status and are characteristic of undifferentiated proliferative states. BMC Cancer. 2009;9:401. 2407-9-401.
54. Kuismanen SA, Holmberg MT, Salovaara R, de la Chapelle A, Peltomaki P. Genetic and epigenetic modification of MLH1 accounts for a major share of microsatellite-unstable colorectal cancers. Am J Pathol. 2000;156:1773–9.
55. Al-Sohaily S, Henderson C, Selinger C, Pangon L, Segelov E, Kohonen-Corish M, et al. Loss of special AT-rich sequence-binding protein 1 (SATB1) predicts poor survival in patients with colorectal cancer. Histopathology. 2014;65:155–63.
56. Boland CR, Thibodeau SN, Hamilton SR, Sidransky D, Eshleman JR, Burt RW, et al. 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. 1998;58:5248–57.
57. Loukola A, Eklin K, Laiho P, Salovaara R, Kristo P, Jarvinen H, et al. Microsatellite marker analysis in screening for hereditary nonpolyposis colorectal cancer (HNPCC). Cancer Res. 2001;61:4545–9.
58. Esemuede I, Forslund A, Khan SA, Qin LX, Gimbel MI, Nash GM, et al. Improved testing for microsatellite instability in colorectal cancer using a simplified 3-marker assay. Ann Surg Oncol. 2010;17:3370–8.
59. Kohonen-Corish MR, Tseung J, Chan C, Currey N, Dent OF, Clarke S, et al. KRAS mutations and CDKN2A promoter methylation show an interactive adverse effect on survival and predict recurrence of rectal cancer. Int J Cancer. 2014;134:2820–8.
60. Isola J, DeVries S, Chu L, Ghazvini S, Waldman F. Analysis of changes in DNA sequence copy number by comparative genomic hybridization in archival paraffin-embedded tumor samples. Am J Pathol. 1994;145:1301–8.
61. Derks S, Bosch LJ, Niessen HE, Moerkerk PT, van den Bosch SM, Carvalho B, et al. Promoter CpG island hypermethylation- and H3K9me3 and H3K27me3-mediated epigenetic silencing targets the deleted in colon cancer (DCC) gene in colorectal carcinogenesis without affecting neighboring genes on chromosomal region 18q21. Carcinogenesis. 2009;30:1041–8.
62. Saini HK, Griffiths-Jones S, Enright AJ. Genomic analysis of human microRNA transcripts. Proc Natl Acad Sci U S A. 2007;104:17719–24.
63. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet. 2006;38:787–93.