Overexpression of cancer-associated genes via epigenetic derepression mechanisms in gynecologic cancer

Frontiers in Oncology

Volumn 4 FEB, Issue , 2014, Pages

  Jeong, Hae Min ^a   Kwon, Mi Jeong ^b   Shin, Young Kee ^a,c  

^a Seoul National University   (South Korea)

^b Kyungpook National University   (South Korea)

^c Seoul National University   (South Korea)

Author keywords

DNA methylation; Epigenetic derepression; Epigenetic therapy; Gynecologic cancer; Histone modification; MicroRNA

Indexed keywords

BETA CATENIN; BRCA1 PROTEIN; BRCA2 PROTEIN; GAMMA SYNUCLEIN; K RAS PROTEIN; METHYLCYTOSINE DIOXYGENASE; MICRORNA; MICRORNA 143; MICRORNA 145; MICRORNA 149; MICRORNA 17 92; MICRORNA 203; MICRORNA 21; MICRORNA 26A; MICRORNA 29; MICRORNA 29B; MICRORNA 29C; MICRORNA 375; MICRORNA 505; MICRORNA 98; PEPTIDES AND PROTEINS; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PROTEIN BCL 3; PROTEIN BCL X; PROTEIN P53; TRANSCRIPTION FACTOR HOXA10; TRANSCRIPTION FACTOR SOX4; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN A;

ALTERNATIVE RNA SPLICING; CANCER ASSOCIATED GENE; CANCER DIAGNOSIS; CANCER GROWTH; CELL DIFFERENTIATION; DNA METHYLATION; ENDOMETRIUM CANCER; EPIGENETIC DEREPRESSION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; GYNECOLOGIC CANCER; HISTONE MODIFICATION; HUMAN; MICROARRAY ANALYSIS; OVARY CANCER; REVIEW; TUMOR GENE; UTERINE CERVIX CANCER; VAGINA CANCER; WART VIRUS;

EID: 84897994861     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00012     Document Type: Review

References (146)

1. Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature (2001) 411:342-8. doi: 10.1038/35077213
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell (2011) 144:646-74. doi:10.1016/j.cell.2011.02.013
3. Lee EY, Muller WJ. Oncogenes and tumor suppressor genes. Cold Spring Harb Perspect Biol (2010) 2(10):a003236. doi:10.1101/cshperspect.a003236
4. Oren M. The involvement of oncogenes and tumor suppressor genes in the control of apoptosis. Cancer Metastasis Rev (1992) 11:141-8. doi:10.1007/BF00048060
5. Sadikovic B, Al-Romaih K, Squire JA, Zielenska M. Cause and consequences of genetic and epigenetic alterations in human cancer. Curr Genomics (2008) 9:394-408. doi:10.2174/138920208785699580
6. Aguilera O, Fernandez AF, Munoz A, Fraga MF. Epigenetics and environment: a complex relationship. J Appl Physiol (2010) 109:243-51. doi:10.1152/japplphysiol.00068.2010
7. Boffetta P, Nyberg F. Contribution of environmental factors to cancer risk. Br Med Bull (2003) 68:71-94. doi:10.1093/bmp/ldg023
8. Lichtenstein P, Holm NV, Verkasalo PK, Iliadou A, Kaprio J, Koskenvuo M, et al. Environmental and heritable factors in the causation of cancer-analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med (2000) 343:78-85. doi:10.1056/NEJM200007133430201
9. Baccarelli A, Bollati V. Epigenetics and environmental chemicals. Curr Opin Pediatr (2009) 21:243. doi:10.1097/MOP.0b013e32832925cc
10. Herceg Z, Paliwal A. Epigenetic mechanisms in hepatocellular carcinoma: how environmental factors influence the epigenome. Mutat Res (2011) 727:55-61. doi:10.1016/j.mrrev.2011.04.001
11. Widschwendter M, Jones A, Teschendorff AE. Epigenetics makes its mark on women-specific cancers-an opportunity to redefine oncological approaches? Gynecol Oncol (2013) 128:134-43. doi:10.1016/j.ygyno.2012.09.027
12. Ehrlich M. DNA hypomethylation in cancer cells. Epigenomics (2009) 1:239-59. doi:10.2217/epi.09.33
13. Kwon MJ, Kim SS, Choi YL, Jung HS, Balch C, Kim SH, et al. Derepression of CLDN3 and CLDN4 during ovarian tumorigenesis is associated with loss of repressive histone modifications. Carcinogenesis (2010) 31:974-83. doi:10.1093/carcin/bgp336
14. Kwon MJ, Kim SH, Jeong HM, Jung HS, Kim SS, Lee JE, et al. Claudin-4 overexpression is associated with epigenetic derepression in gastric carcinoma. Lab Invest (2011) 91:1652-67. doi:10.1038/labinvest.2011.117
15. Saito Y, Jones PM. Epigenetic activation of tumor suppressor microRNAs in human cancer cells. Cell Cycle (2006) 5:2220-2. doi:10.4161/cc.5.19.3340
16. Zhang J, Benavente CA, McEvoy J, Flores-Otero J, Ding L, Chen X, et al. A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature (2012) 481:329-34. doi:10.1038/nature10733
17. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin (2012) 62(1):10-29. doi:10.3322/caac.20138
18. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S. Human papillomavirus and cervical cancer. Lancet (2007) 370:890-907. doi:10.1016/S0140-6736(07)61416-0
19. Morgan RJ, Alvarez RD, Armstrong DK, Boston B, Burger RA, Chen L-M, et al. Epithelial ovarian cancer. J Natl Compr Canc Netw (2011) 9:82-113.
20. Li J, Fadare O, Xiang L, Kong B, Zheng W. Ovarian serous carcinoma: recent concepts on its origin and carcinogenesis. J Hematol Oncol (2012) 5:8-8. doi:10.1186/1756-8722-5-8
21. Kurman RJ, Shih IeM. Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum Pathol (2011) 42:918-31. doi:10.1016/j.humpath.2011.03.003
22. Holschneider CH, Berek JS. Ovarian cancer: epidemiology, biology, and prognostic factors. Semin Surg Oncol (2000) 19:3-10. doi:10.1002/1098-2388(200007/08)19:1<3::AID-SSU2>3.0.CO;2-S
23. Alsop K, Fereday S, Meldrum C, Defazio A, Emmanuel C, George J, et al. BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian Ovarian Cancer Study Group. J Clin Oncol (2012) 30:2654-63. doi:10.1200/JCO.2011.39.8545
24. TCGA-ResearchNetwork. Integrated genomic analyses of ovarian carcinoma. Nature (2011) 474:609-15. doi:10.1038/nature10166
25. Cooper BC, Sood AK, Davis CS, Ritchie JM, Sorosky JI, Anderson B, et al. Preoperative CA 125 levels: an independent prognostic factor for epithelial ovarian cancer. Obstet Gynecol (2002) 100:59-64. doi:10.1016/S0029-7844(02)02057-4
26. Rustin GJ, Bast RC Jr, Kelloff GJ, Barrett JC, Carter SK, Nisen PD, et al. Use of Ca-125 in clinical trial evaluation of new therapeutic drugs for ovarian cancer. Clin Cancer Res (2004) 10:3919-26. doi:10.1158/1078-0432.CCR-03-0787
27. Pignata S, Cannella L, Leopardo D, Bruni GS, Facchini G, Pisano C. Follow-up with CA125 after primary therapy of advanced ovarian cancer: in favor of continuing to prescribe CA125 during follow-up. Ann Oncol (2011) 22(Suppl 8):viii40-4. doi:10.1093/annonc/mdr470
28. Duenas-Gonzalez A, Lizano M, Candelaria M, Cetina L, Arce C, Cervera E. Epigenetics of cervical cancer. An overview and therapeutic perspectives. Mol Cancer (2005) 4:38. doi:10.1186/1476-4598-4-38
29. Jeong DH, Youm MY, Kim YN, Lee KB, Sung MS, Yoon HK, et al. Promoter methylation of p16, Dapk, CDH1, and Timp-3 genes in cervical cancer: correlation with clinicopathologic characteristics. Int J Gynecol Cancer (2006) 16:1234-40. doi:10.1111/j.1525-1438.2006.00522.x
30. Su P, Lin Y, Huang R, Liao Y, Lee H, Wang H, et al. Epigenetic silencing of PTPRR activates MAPK signaling, promotes metastasis and serves as a biomarker of invasive cervical cancer. Oncogene (2012) 32(1):15-26. doi:10.1038/onc.2012.29
31. Matias-Guiu X, Catasus L, Bussaglia E, Lagarda H, Garcia A, Pons C, et al. Molecular pathology of endometrial hyperplasia and carcinoma. Hum Pathol (2001) 32:569-77. doi:10.1053/hupa.2001.25929
32. Fukuchi T, Sakamoto M, Tsuda H, Maruyama K, Nozawa S, Hirohashi S. Beta-catenin mutation in carcinoma of the uterine endometrium. Cancer Res (1998) 58:3526-8.
33. Oda K, Stokoe D, Taketani Y, McCormick F. High frequency of coexistent mutations of PIK3CA and PTEN genes in endometrial carcinoma. Cancer Res (2005) 65:10669-73. doi:10.1158/0008-5472.CAN-05-2620
34. Risinger JI, Dent GA, Ignar-Trowbridge D, McLachlan JA, Tsao MS, Senterman M, et al. p53 gene mutations in human endometrial carcinoma. Mol Carcinog (1992) 5:250-3. doi:10.1002/mc.2940050403
35. Ghurani GB, Penalver MA. An update on vulvar cancer. Am J Obstet Gynecol (2001) 185:294-9. doi:10.1067/mob.2001.117401
36. Esteller M. Epigenetics in cancer. N Engl J Med (2008) 358:1148-59. doi:10.1056/NEJMra072067
37. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet (2002) 3:415-28. doi:10.1038/nrg816
38. Kanwal R, Gupta S. Epigenetics and cancer. J Appl Physiol (2010) 109:598-605. doi:10.1152/japplphysiol.00066.2010
39. Gronbaek K, Hother C, Jones PA. Epigenetic changes in cancer. APMIS (2007) 115:1039-59. doi:10.1111/j.1600-0463.2007.apm_636.xml.x
40. Gibney ER, Nolan CM. Epigenetics and gene expression. Heredity (Edinb) (2010) 105:4-13. doi:10.1038/hdy.2010.54
41. Hervouet E, Vallette FM, Cartron PF. Dnmt3/transcription factor interactions as crucial players in targeted DNA methylation. Epigenetics (2009) 4:487-99. doi:10.4161/epi.4.7.9883
42. Wade PA. Methyl CpG binding proteins: coupling chromatin architecture to gene regulation. Oncogene (2001) 20:3166-73. doi:10.1038/sj.onc.1204340
43. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature (1983) 301:89-92. doi:10.1038/301089a0
44. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science (2009) 324:930-5. doi:10.1126/science.1170116
45. Cimmino L, Abdel-Wahab O, Levine RL, Aifantis I. TET family proteins and their role in stem cell differentiation and transformation. Cell Stem Cell (2011) 9:193-204. doi:10.1016/j.stem.2011.08.007
46. Niehrs C, Schafer A. Active DNA demethylation by Gadd45 and DNA repair. Trends Cell Biol (2012) 22:220-7. doi:10.1016/j.tcb.2012.01.002
47. Costa Y, Ding J, Theunissen TW, Faiola F, Hore TA, Shliaha PV, et al. Nanog-dependent function of TET1 and TET2 in establishment of pluripotency. Nature (2013) 495:370-4. doi:10.1038/nature11925
48. Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell (2011) 8:200-13. doi:10.1016/j.stem.2011.01.008
49. Sun M, Song CX, Huang H, Frankenberger CA, Sankarasharma D, Gomes S, et al. HMGA2/TET1/HOXA9 signaling pathway regulates breast cancer growth and metastasis. Proc Natl Acad Sci U S A (2013) 110:9920-5. doi:10.1073/pnas.1305172110
50. Liu C, Liu L, Chen X, Shen J, Shan J, Xu Y, et al. Decrease of 5-hydroxymethylcytosine is associated with progression of hepatocellular carcinoma through downregulation of TET1. PLoS One (2013) 8:e62828. doi:10.1371/journal.pone.0062828
51. Nephew KP, Balch C, Zhang S, Huang THM. Epigenetics and ovarian cancer. Cancer Treat Res (2010) 149:131-46. doi:10.1007/978-0-387-98094-2_6
52. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res (2011) 21:381-95. doi:10.1038/cr.2011.22
53. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet (2007) 8:286-98. doi:10.1038/nrg2005
54. Baer C, Claus R, Plass C. Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Res (2013) 73:473-7. doi:10.1158/0008-5472.CAN-12-3731
55. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer (2006) 6:857-66. doi:10.1038/nrc1997
56. Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol (2008) 9:219-30. doi:10.1038/nrm2347
57. Farazi TA, Spitzer JI, Morozov P, Tuschl T. miRNAs in human cancer. J Pathol (2011) 223:102-15. doi:10.1002/path.2806
58. Olive V, Jiang I, He L. mir-17-92, a cluster of miRNAs in the midst of the cancer network. Int J Biochem Cell Biol (2010) 42:1348-54. doi:10.1016/j.biocel.2010.03.004
59. Selcuklu SD, Donoghue MT, Spillane C. miR-21 as a key regulator of oncogenic processes. Biochem Soc Trans (2009) 37:918-25. doi:10.1042/BST0370918
60. Wang Y, Lee CG. MicroRNA and cancer-focus on apoptosis. J Cell Mol Med (2009) 13:12-23. doi:10.1111/j.1582-4934.2008.00510.x
61. Feng B, Wang R, Chen LB. Review of miR-200b and cancer chemosensitivity. Biomed Pharmacother (2012) 66:397-402. doi:10.1016/j.biopha.2012.06.002
62. Kent O, Mendell J. A small piece in the cancer puzzle: microRNAs as tumor suppressors and oncogenes. Oncogene (2006) 25:6188-96. doi:10.1038/sj.onc.1209913
63. Ghigna C, Moroni M, Porta C, Riva S, Biamonti G. Altered expression of heterogeneous nuclear ribonucleoproteins and SR factors in human colon adenocarcinomas. Cancer Res (1998) 58:5818-24.
64. Kornblihtt AR, Schor IE, ALL M, Dujardin G, Petrillo E, Muñoz MJ. Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol (2013) 14(3):153-65. doi:10.1038/nrm3525
65. Lixia M, Zhijian C, Chao S, Chaojiang G, Congyi Z. Alternative splicing of breast cancer associated gene BRCA1 from breast cancer cell line. J Biochem Mol Biol (2007) 40:15-21. doi:10.5483/BMBRep.2007.40.1.015
66. Karni R, DE Stanchina E, Lowe SW, Sinha R, Mu D, Krainer AR. The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat Struct Mol Biol (2007) 14:185-93. doi:10.1038/nsmb1209
67. Anczuków O, Rosenberg AZ, Akerman M, Das S, Zhan L, Karni R, et al. The splicing factor SRSF1 regulates apoptosis and proliferation to promote mammary epithelial cell transformation. Nat Struct Mol Biol (2012) 19:220-8. doi:10.1038/nsmb.2207
68. Huff V. Wilms' tumours: about tumour suppressor genes, an oncogene and a chameleon gene. Nat Rev Cancer (2011) 11:111-21. doi:10.1038/nrc3002
69. Ladomery M. Aberrant alternative splicing is another hallmark of cancer. Int J Cell Biol (2013) 2013:463786. doi:10.1155/2013/463786
70. Venables JP. Unbalanced alternative splicing and its significance in cancer. Bioessays (2006) 28:378-86. doi:10.1002/bies.20390
71. Chen K-C, Liao Y-C, Hsieh IC, Wang Y-S, Hu C-Y, Juo S-HH. OxLDL causes both epigenetic modification and signaling regulation on the microRNA-29b gene: novel mechanisms for cardiovascular diseases. J Mol Cell Cardiol (2012) 52:587-95. doi:10.1016/j.yjmcc.2011.12.005
72. Li Y, Kong D, Ahmad A, Bao B, Dyson G, Sarkar FH. Epigenetic deregulation of miR-29a and miR-1256 by isoflavone contributes to the inhibition of prostate cancer cell growth and invasion. Epigenetics (2012) 7:940-9. doi:10.4161/epi.21236
73. Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A (2007) 104:15805-10. doi:10.1073/pnas.0707628104
74. Meunier L, Siddeek B, Vega A, Lakhdari N, Inoubli L, Bellon RP, et al. Perinatal programming of adult rat germ cell death after exposure to xenoestrogens: role of microRNA miR-29 family in the down-regulation of DNA methyltransferases and Mcl-1. Endocrinology (2012) 153:1936-47. doi:10.1210/en.2011-1109
75. Wang Y, Zhang X, Li H, Yu J, Ren X. The role of miRNA-29 family in cancer. Eur J Cell Biol (2012) 92(3):123-8. doi:10.1016/j.ejcb.2012.11.004
76. Li Q, Zhu F, Chen P. miR-7 and miR-218 epigenetically control tumor suppressor genes RASSF1A and Claudin-6 by targeting HoxB3 in breast cancer. Biochem Biophys Res Commun (2012) 424:28-33. doi:10.1016/j.bbrc.2012.06.028
77. Verduci L, Simili M, Rizzo M, Mercatanti A, Evangelista M, Mariani L, et al. MicroRNA (miRNA)-mediated interaction between leukemia/lymphoma-related factor (LRF) and alternative splicing factor/splicing factor 2 (ASF/SF2) affects mouse embryonic fibroblast senescence and apoptosis. J Biol Chem (2010) 285:39551-63. doi:10.1074/jbc.M110.114736
78. Creighton CJ, Hernandez-Herrera A, Jacobsen A, Levine DA, Mankoo P, Schultz N, et al. Integrated analyses of microRNAs demonstrate their widespread influence on gene expression in high-grade serous ovarian carcinoma. PLoS One (2012) 7:e34546. doi:10.1371/journal.pone.0034546
79. Raeder MB, Birkeland E, Trovik J, Krakstad C, Shehata S, Schumacher S, et al. Integrated genomic analysis of the 8q24 amplification in endometrial cancers identifies ATAD2 as essential to Myc-dependent cancers. PLoS One (2013) 8:e54873. doi:10.1371/journal.pone.0054873
80. La DE, Rica L, Urquiza JM, Gomez-Cabrero D, Islam AB, Lopez-Bigas N, et al. Identification of novel markers in rheumatoid arthritis through integrated analysis of DNA methylation and microRNA expression. J Autoimmun (2013) 41:6-16. doi:10.1016/j.jaut.2012.12.005
81. Kresse SH, Rydbeck H, Skarn M, Namlos HM, Barragan-Polania AH, Cleton-Jansen AM, et al. Integrative analysis reveals relationships of genetic and epigenetic alterations in osteosarcoma. PLoS One (2012) 7:e48262. doi:10.1371/journal.pone.0048262
82. Balch C, Huang THM, Brown R, Nephew KP. The epigenetics of ovarian cancer drug resistance and resensitization. Am J Obstet Gynecol (2004) 191:1552-72. doi:10.1016/j.ajog.2004.05.025
83. Cao J, Yan Q. Histone ubiquitination and deubiquitination in transcription, DNA damage response, and cancer. Front Oncol (2012) 2:26. doi:10.3389/fonc.2012.00026
84. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell (2007) 129:823-37. doi:10.1016/j.cell.2007.05.009
85. Rosenfeld JA, Wang Z, Schones DE, Zhao K, Desalle R, Zhang MQ. Determination of enriched histone modifications in non-genic portions of the human genome. BMC Genomics (2009) 10:143. doi:10.1186/1471-2164-10-143
86. Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, et al. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev (2004) 18:1251-62. doi:10.1101/gad.300704
87. Benevolenskaya EV. Histone H3K4 demethylases are essential in development and differentiation. Biochem Cell Biol (2007) 85:435-43. doi:10.1139/O07-057
88. Koch CM, Andrews RM, Flicek P, Dillon SC, Karaoz U, Clelland GK, et al. The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res (2007) 17:691-707. doi:10.1101/gr.5704207
89. Steger DJ, Lefterova MI, Ying L, Stonestrom AJ, Schupp M, Zhuo D, et al. DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol Cell Biol (2008) 28:2825-39. doi:10.1128/MCB.02076-07
90. Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Annu Rev Biochem (2001) 70:81-120. doi:10.1146/annurev.biochem.70.1.81
91. Costa FF, Paixao VA, Cavalher FP, Ribeiro KB, Cunha IW, Rinck JA Jr, et al. Satr-1 hypomethylation is a common and early event in breast cancer. Cancer Genet Cytogenet (2006) 165:135-43. doi:10.1016/j.cancergencyto.2005.07.023
92. Widschwendter M, Jiang G, Woods C, Muller HM, Fiegl H, Goebel G, et al. DNA hypomethylation and ovarian cancer biology. Cancer Res (2004) 64:4472-80. doi:10.1158/0008-5472.CAN-04-0238
93. Hur K, Cejas P, Feliu J, Moreno-Rubio J, Burgos E, Boland CR, et al. Hypomethylation of long interspersed nuclear element-1 (Line-1) leads to activation of proto-oncogenes in human colorectal cancer metastasis. Gut (2013). doi:10.1136/gutjnl-2012-304219
94. Pavicic W, Joensuu EI, Nieminen T, Peltomaki P. LINE-1 hypomethylation in familial and sporadic cancer. J Mol Med (Berl) (2012) 90:827-35. doi:10.1007/s00109-011-0854-z
95. Sunami E, DE Maat M, Vu A, Turner RR, Hoon DS. LINE-1 hypomethylation during primary colon cancer progression. PLoS One (2011) 6:e18884. doi:10.1371/journal.pone.0018884
96. Gao XD, Qu JH, Chang XJ, Lu YY, Bai WL, Wang H, et al. Hypomethylation of long interspersed nuclear element-1 promoter is associated with poor outcomes for curative resected hepatocellular carcinoma. Liver Int (2014) 34(1):136-46. doi:10.1111/liv.12264
97. Shigaki H, Baba Y, Watanabe M, Murata A, Iwagami S, Miyake K, et al. LINE-1 hypomethylation in gastric cancer, detected by bisulfite pyrosequencing, is associated with poor prognosis. Gastric Cancer (2012) 16(4):480-7. doi:10.1007/s10120-012-0209-7
98. Aoki Y, Nojima M, Suzuki H, Yasui H, Maruyama R, Yamamoto E, et al. Genomic vulnerability to LINE-1 hypomethylation is a potential determinant of the clinicogenetic features of multiple myeloma. Genome Med (2012) 4:101. doi:10.1186/gm402
99. Chan KYK, OZ Elik H, Cheung ANY, Ngan HYS, Khoo US. Epigenetic factors controlling the BRCA1 and BRCA2 genes in sporadic ovarian cancer. Cancer Res (2002) 62:4151-6.
100. Dann RB, Deloia JA, Timms KM, Zorn KK, Potter J, Flake DD II, et al. BRCA1/2 mutations and expression: response to platinum chemotherapy in patients with advanced stage epithelial ovarian cancer. Gynecol Oncol (2012) 125:677-82. doi:10.1016/j.ygyno.2012.03.006
101. Hsu YT, Gu F, Huang YW, Liu J, Ruan J, Huang RL, et al. Promoter hypomethylation of EpCAM-regulated bone morphogenetic protein gene family in recurrent endometrial cancer. Clin Cancer Res (2013) 19:6272-85. doi:10.1158/1078-0432.CCR-13-1734
102. Lee TS, Kim JW, Kang GH, Park NH, Song YS, Kang SB, et al. DNA hypomethylation of CAGE promotors in squamous cell carcinoma of uterine cervix. Ann N Y Acad Sci (2006) 1091:218-24. doi:10.1196/annals.1378.068
103. Honda H, Pazin MJ, Ji H, Wernyj RP, Morin PJ. Crucial roles of Sp1 and epigenetic modifications in the regulation of the CLDN4 promoter in ovarian cancer cells. J Biol Chem (2006) 281:21433-44. doi:10.1074/jbc.M603767200
104. Honda H, Pazin MJ, D'Souza T, Ji H, Morin PJ. Regulation of the CLDN3 gene in ovarian cancer cells. Cancer Biol Ther (2007) 6:1733-42. doi:10.4161/cbt.6.11.4832
105. Cheng W, Jiang Y, Liu C, Shen O, Tang W, Wang X. Identification of aberrant promoter hypomethylation of HOXA10 in ovarian cancer. J Cancer Res Clin Oncol (2010) 136:1221-7. doi:10.1007/s00432-010-0772-4
106. Lee PS, Teaberry VS, Bland AE, Huang Z, Whitaker RS, Baba T, et al. Elevated MAL expression is accompanied by promoter hypomethylation and platinum resistance in epithelial ovarian cancer. Int J Cancer (2010) 126:1378-89. doi:10.1002/ijc.24797
107. Gupta A, Godwin AK, Vanderveer L, Lu A, Liu J. Hypomethylation of the synuclein gamma gene CpG Island promotes its aberrant expression in breast carcinoma and ovarian carcinoma. Cancer Res (2003) 63:664-73.
108. Izutsu N, Maesawa C, Shibazaki M, Oikawa H, Shoji T, Sugiyama T, et al. Epigenetic modification is involved in aberrant expression of class III beta-tubulin, TUBB3, in ovarian cancer cells. Int J Oncol (2008) 32:1227. doi:10.3892/ijo_32_6_1227
109. Dahl KDC, Dahl R, Kruichak JN, Hudson LG. The epidermal growth factor receptor responsive miR-125a represses mesenchymal morphology in ovarian cancer cells. Neoplasia (2009) 11:1208. doi:10.1593/neo.09942
110. Guan Y, Yao H, Zheng Z, Qiu G, Sun K. MiR-125b targets BCL3 and suppresses ovarian cancer proliferation. Int J Cancer (2011) 128:2274-83. doi:10.1002/ijc.25575
111. Bhattacharya R, Nicoloso M, Arvizo R, Wang E, Cortez A, Rossi S, et al. MiR-15a and MiR-16 control Bmi-1 expression in ovarian cancer. Cancer Res (2009) 69:9090-5. doi:10.1158/0008-5472.CAN-09-2552
112. Yang Z, Chen S, Luan X, Li Y, Liu M, Li X, et al. MicroRNA-214 is aberrantly expressed in cervical cancers and inhibits the growth of HeLa cells. IUBMB Life (2009) 61:1075-82. doi:10.1002/iub.252
113. Guo LM, Pu Y, Han Z, Liu T, Li YX, Liu M, et al. MicroRNA-9 inhibits ovarian cancer cell growth through regulation of NF-?B1. FEBS J (2009) 276:5537-46. doi:10.1111/j.1742-4658.2009.07237.x
114. Huang F, Lin C, Shi YH, Kuerban G. MicroRNA-101 inhibits cell proliferation, invasion, and promotes apoptosis by regulating cyclooxygenase-2 in Hela cervical carcinoma cells. Asian Pac J Cancer Prev (2013) 14:5915-20. doi:10.7314/APJCP.2013.14.10.5915
115. Yamamoto N, Kinoshita T, Nohata N, Yoshino H, Itesako T, Fujimura L, et al. Tumor-suppressive microRNA-29a inhibits cancer cell migration and invasion via targeting HSP47 in cervical squamous cell carcinoma. Int J Oncol (2013) 43:1855-63. doi:10.3892/ijo.2013.2145
116. Zhu X, Er K, Mao C, Yan Q, Xu H, Zhang Y, et al. miR-203 suppresses tumor growth and angiogenesis by targeting VEGFA in cervical cancer. Cell Physiol Biochem (2013) 32:64-73. doi:10.1159/000350125
117. 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. doi:10.1158/0008-5472.CAN-09-1499
118. Yang N, Kaur S, Volinia S, Greshock J, Lassus H, Hasegawa K, et al. MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer. Cancer Res (2008) 68:10307-14. doi:10.1158/0008-5472.CAN-08-1954
119. Wilting SM, Verlaat W, Jaspers A, Makazaji NA, Agami R, Meijer CJ, et al. Methylation-mediated transcriptional repression of microRNAs during cervical carcinogenesis. Epigenetics (2013) 8(2):220-8. doi:10.4161/epi.23605
120. Pereira PM, Marques JP, Soares AR, Carreto L, Santos MA. MicroRNA expression variability in human cervical tissues. PLoS One (2010) 5:e11780. doi:10.1371/journal.pone.0011780
121. Agarwal R, D'Souza T, Morin PJ. Claudin-3 and claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity. Cancer Res (2005) 65:7378-85. doi:10.1158/0008-5472.CAN-05-1036
122. Yao T, Rao Q, Liu L, Zheng C, Xie Q, Liang J, et al. Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in cervical cancer. Virol J (2013) 10:175. doi:10.1186/1743-422X-10-175
123. Aaboe M, Birkenkamp-Demtroder K, Wiuf C, Sorensen FB, Thykjaer T, Sauter G, et al. SOX4 expression in bladder carcinoma: clinical aspects and in vitro functional characterization. Cancer Res (2006) 66:3434-42. doi:10.1158/0008-5472.CAN-05-3456
124. Liao YL, Sun YM, Chau GY, Chau YP, Lai TC, Wang JL, et al. Identification of SOX4 target genes using phylogenetic footprinting-based prediction from expression microarrays suggests that overexpression of SOX4 potentiates metastasis in hepatocellular carcinoma. Oncogene (2008) 27:5578-89. doi:10.1038/onc.2008.168
125. Liu P, Ramachandran S, ALI Seyed M, Scharer CD, Laycock N, Dalton WB, et al. Sex-determining region Y box 4 is a transforming oncogene in human prostate cancer cells. Cancer Res (2006) 66:4011-9. doi:10.1158/0008-5472.CAN-05-3055
126. Medina PP, Castillo SD, Blanco S, Sanz-Garcia M, Largo C, Alvarez S, et al. The Sry-HMG box gene, SOX4, is a target of gene amplification at chromosome 6p in lung cancer. Hum Mol Genet (2009) 18:1343-52. doi:10.1093/hmg/ddp034
127. Samartzis N, Imesch P, Dedes KJ, Samartzis EP, Fedier A, Fink D, et al. Expression pattern of class I histone deacetylases in vulvar intraepithelial neoplasia and vulvar cancer: a tissue microarray study. BMC Cancer (2011) 11:463. doi:10.1186/1471-2407-11-463
128. Feng Q, Balasubramanian A, Hawes SE, Toure P, Sow PS, Dem A, et al. Detection of hypermethylated genes in women with and without cervical neoplasia. J Natl Cancer Inst (2005) 97:273-82. doi:10.1093/jnci/dji318
129. Kalantari M, Osann K, Calleja-Macias IE, Kim S, Yan B, Jordan S, et al. Methylation of human papillomavirus 16, 18, 31, and 45 L2 and L1 genes and the cellular DAPK gene: considerations for use as biomarkers of the progression of cervical neoplasia. Virology (2014) 448:314-21. doi:10.1016/j.virol.2013.10.032
130. Bryant D, Tristram A, Liloglou T, Hibbitts S, Fiander A, Powell N. Quantitative measurement of human papillomavirus type 16 L1/L2 DNA methylation correlates with cervical disease grade. J Clin Virol (2013) 59(1):24-9. doi:10.1016/j.jcv.2013.10.029
131. Lai HC, Lin YW, Huang TH, Yan P, Huang RL, Wang HC, et al. Identification of novel DNA methylation markers in cervical cancer. Int J Cancer (2008) 123:161-7. doi:10.1002/ijc.23519
132. Fiegl H, Gattringer C, Widschwendter A, Schneitter A, Ramoni A, Sarlay D, et al. Methylated DNA collected by tampons-a new tool to detect endometrial cancer. Cancer Epidemiol Biomarkers Prev (2004) 13:882-8.
133. Zheng H, Zhang L, Zhao Y, Yang D, Song F, Wen Y, et al. Plasma miRNAs as diagnostic and prognostic biomarkers for ovarian cancer. PLoS One (2013) 8:e77853. doi:10.1371/journal.pone.0077853
134. Strathdee G, Davies B, Vass J, Siddiqui N, Brown R. Cell type-specific methylation of an intronic CpG Island controls expression of the MCJ gene. Carcinogenesis (2004) 25:693-701. doi:10.1093/carcin/bgh066
135. Strathdee G, Vass JK, Oien KA, Siddiqui N, Curto-Garcia J, Brown R. Demethylation of the MCJ gene in stage III/IV epithelial ovarian cancer and response to chemotherapy. Gynecol Oncol (2005) 97:898-903. doi:10.1016/j.ygyno.2005.03.023
136. Fiegl H, Windbichler G, Mueller-Holzner E, Goebel G, Lechner M, Jacobs IJ, et al. HOXA11 DNA methylation-a novel prognostic biomarker in ovarian cancer. Int J Cancer (2008) 123:725-9. doi:10.1002/ijc.23563
137. Guerrero D, Guarch R, Ojer A, Casas JM, Mendez-Meca C, Esteller M, et al. Differential hypermethylation of genes in vulvar cancer and lichen sclerosus coexisting or not with vulvar cancer. Int J Cancer (2011) 128:2853-64. doi:10.1002/ijc.25629
138. Stephen JK, Chen KM, Raitanen M, Grenman S, Worsham MJ. DNA hypermethylation profiles in squamous cell carcinoma of the vulva. Int J Gynecol Pathol (2009) 28:63-75. doi:10.1097/PGP.0b013e31817d9c61
139. Pakneshan P, Tetu B, Rabbani SA. Demethylation of urokinase promoter as a prognostic marker in patients with breast carcinoma. Clin Cancer Res (2004) 10:3035-41. doi:10.1158/1078-0432.CCR-03-0545
140. Paredes J, Albergaria A, Oliveira JT, Jeronimo C, Milanezi F, Schmitt FC. P-cadherin overexpression is an indicator of clinical outcome in invasive breast carcinomas and is associated with CDH3 promoter hypomethylation. Clin Cancer Res (2005) 11:5869-77. doi:10.1158/1078-0432.CCR-05-0059
141. Itano O, Ueda M, Kikuchi K, Hashimoto O, Hayatsu S, Kawaguchi M, et al. Correlation of postoperative recurrence in hepatocellular carcinoma with demethylation of repetitive sequences. Oncogene (2002) 21:789-97. doi:10.1038/sj.onc.1205124
142. Pattamadilok J, Huapai N, Rattanatanyong P, Vasurattana A, Triratanachat S, Tresukosol D, et al. LINE-1 hypomethylation level as a potential prognostic factor for epithelial ovarian cancer. Int J Gynecol Cancer (2008) 18:711-7. doi:10.1111/j.1525-1438.2007.01117.x
143. Kaminskas E, Farrell AT, Wang YC, Sridhara R, Pazdur R. FDA drug approval summary: azacitidine (5-azacytidine, Vidaza) for injectable suspension. Oncologist (2005) 10:176-82. doi:10.1634/theoncologist.10-3-176
144. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, et al. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell (2006) 9:435-43. doi:10.1016/j.ccr.2006.04.020
145. Wang QZ, Lv YH, Gong YH, Li ZF, Xu W, Diao Y, et al. Double-stranded Let-7 mimics, potential candidates for cancer gene therapy. J Physiol Biochem (2012) 68:107-19. doi:10.1007/s13105-011-0124-0
146. Spandidos D, Dokianakis D, Kallergi G, Aggelakis E. Molecular basis of gynecological cancer. Ann N Y Acad Sci (2000) 900:56-64. doi:10.1111/j.1749-6632.2000.tb06216.x