The detective, prognostic, and predictive value of DNA methylation in human esophageal squamous cell carcinoma

Clinical Epigenetics

Volumn 8, Issue 1, 2016, Pages

  Ma, Kai ^a   Cao, Baoping ^b   Guo, Mingzhou ^b  

^a QINGDAO UNIVERSITY   (China)

^b CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

CHFR; DNA damage repair; DNA methylation; Epigenome; Esophageal cancer; Wnt signaling

Indexed keywords

ATROGIN 1; BENZO[A]PYRENE; BIOLOGICAL MARKER; CYCLIN DEPENDENT KINASE; FRAGILE HISTIDINE TRIAD PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; MISMATCH REPAIR PROTEIN PMS2; NICOTINE; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH6; PROTEIN P100; PROTEIN P105; PROTEIN P16; PROTEIN P50; PROTEIN P52; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; SECRETED FRIZZLED RELATED PROTEIN 2; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB; TRANSCRIPTION FACTOR RUNX3; TRANSCRIPTION FACTOR SOX17; TRANSFORMING GROWTH FACTOR BETA;

ALCOHOL CONSUMPTION; CANCER PROGNOSIS; CARCINOGENESIS; CELL CYCLE; CHEMOSENSITIVITY; CHFR GENE; DACH1 GENE; DACT2 GENE; DIAGNOSTIC VALUE; DNA METHYLATION; DNA REPAIR; DOWN REGULATION; DUST EXPOSURE; EPIGENETICS; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; FHIT GENE; GENE; HIN1 GENE; HUMAN; MGMT GENE; MISMATCH REPAIR; MLH1 GENE; MLH3 GENE; MSH2 GENE; MSH6 GENE; NONHUMAN; PMS1 GENE; PMS2 GENE; PRIORITY JOURNAL; PROGNOSTIC ASSESSMENT; RASSF1 GENE; REVIEW; RISK FACTOR; SFRP2 GENE; SMOKING; SOX17 GENE; TFPI 2 GENE; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; WNT SIGNALING PATHWAY; ZNF382 GENE; CPG ISLAND; ESOPHAGUS TUMOR; GENE REGULATORY NETWORK; GENETIC EPIGENESIS; GENETICS; PATHOLOGY; PREDICTIVE VALUE; PROGNOSIS; PROMOTER REGION; SQUAMOUS CELL CARCINOMA;

CARCINOMA, SQUAMOUS CELL; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; ESOPHAGEAL NEOPLASMS; GENE REGULATORY NETWORKS; HUMANS; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROMOTER REGIONS, GENETIC;

EID: 84964264794     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-016-0210-9     Document Type: Review

References (138)

1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86. doi:10.1002/ijc.29210.
2. Pennathur A, Gibson MK, Jobe BA, Luketich JD. Oesophageal carcinoma. Lancet. 2013;381(9864):400–12. doi:10.1016/s0140-6736(12)60643-6.
3. De Stefani E, Barrios E, Fierro L. Black (air-cured) and blond (flue-cured) tobacco and cancer risk. III: oesophageal cancer. Eur J Cancer. 1993;29A(5):763–6.
4. Lee CH, Wu DC, Lee JM, Wu IC, Goan YG, Kao EL, et al. Carcinogenetic impact of alcohol intake on squamous cell carcinoma risk of the oesophagus in relation to tobacco smoking. Eur J Cancer. 2007;43(7):1188–99. doi:10.1016/j.ejca.2007.01.039.
5. Vaughan TL, Davis S, Kristal A, Thomas DB. Obesity, alcohol, and tobacco as risk factors for cancers of the esophagus and gastric cardia: adenocarcinoma versus squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 1995;4(2):85–92.
6. Lagergren J, Bergstrom R, Lindgren A, Nyren O. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med. 1999;340:825–31.
7. Veugelers PJ, Porter GA, Guernsey DL, Casson AG. Obesity and lifestyle risk factors for gastroesophageal reflux disease, Barrett esophagus and esophageal adenocarcinoma. DisEsophagus. 2006;19:321–8.
8. Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med. 2003;349(23):2241–52. doi:10.1056/NEJMra035010.
9. Pennathur A, Farkas A, Krasinskas AM, Ferson PF, Gooding WE, Gibson MK, et al. Esophagectomy for T1 esophageal cancer: outcomes in 100 patients and implications for endoscopic therapy. Ann Thorac Surg. 2009;87(4):1048–54. doi:10.1016/j.athoracsur.2008.12.060. discussion 54-5.
10. Ahrens TD, Werner M, Lassmann S. Epigenetics in esophageal cancers. Cell Tissue Res. 2014;356(3):643–55. doi:10.1007/s00441-014-1876-y.
11. Zhang XM, Guo MZ. The value of epigenetic markers in esophageal cancer. Front Med China. 2010;4(4):378–84. doi:10.1007/s11684-010-0230-3.
12. Kanwal R, Gupta S. Epigenetic modifications in cancer. Clinical genetics. 2012;81(4):303–11. doi:10.1111/j.1399-0004.2011.01809.x.
13. Talukdar FR, Ghosh SK, Laskar RS, Mondal R. Epigenetic, genetic and environmental interactions in esophageal squamous cell carcinoma from northeast India. PloS one. 2013;8(4):e60996. doi:10.1371/journal.pone.0060996.
14. Kulkarni V, Saranath D. Concurrent hypermethylation of multiple regulatory genes in chewing tobacco associated oral squamous cell carcinomas and adjacent normal tissues. Oral Oncol. 2004;40(2):145–53.
15. Pulling LC, Klinge DM, Belinsky SA. p16INK4a and beta-catenin alterations in rat liver tumors induced by NNK. Carcinogenesis. 2001;22(3):461–6.
16. Pulling LC, Vuillemenot BR, Hutt JA, Devereux TR, Belinsky SA. Aberrant promoter hypermethylation of the death-associated protein kinase gene is early and frequent in murine lung tumors induced by cigarette smoke and tobacco carcinogens. Cancer Res. 2004;64(11):3844–8. doi:10.1158/0008-5472.can-03-2119.
17. Vuillemenot BR, Hutt JA, Belinsky SA. Gene promoter hypermethylation in mouse lung tumors. Mol Cancer Res. 2006;4(4):267–73. doi:10.1158/1541-7786.mcr-05-0218.
18. Lin RK, Hsieh YS, Lin P, Hsu HS, Chen CY, Tang YA, et al. The tobacco-specific carcinogen NNK induces DNA methyltransferase 1 accumulation and tumor suppressor gene hypermethylation in mice and lung cancer patients. J Clin Invest. 2010;120(2):521–32. doi:10.1172/jci40706.
19. Denissenko MF, Pao A, Tang M, Pfeifer GP. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science. 1996;274(5286):430–2.
20. Mass MJ, Jeffers AJ, Ross JA, Nelson G, Galati AJ, Stoner GD, et al. Ki-ras oncogene mutations in tumors and DNA adducts formed by benz[j]aceanthrylene and benzo[a]pyrene in the lungs of strain A/J mice. Mol Carcinog. 1993;8(3):186–92.
21. Venkatachalam S, Denissenko MF, Alvi N, Wani AA. Rapid activation of apoptosis in human promyelocytic leukemic cells by (+/-)-anti-benzo[a]pyrene diol epoxide induced DNA damage. Biochem Biophys Res Commun. 1993;197(2):722–9. doi:10.1006/bbrc.1993.2539.
22. Wang D, You L, Sneddon J, Cheng SJ, Jamasbi R, Stoner GD. Frameshift mutation in codon 176 of the p53 gene in rat esophageal epithelial cells transformed by benzo[a]pyrene dihydrodiol. Mol Carcinog. 1995;14(2):84–93.
23. Ye F, Xu XC. Benzo[a]pyrene diol epoxide suppresses retinoic acid receptor-beta2 expression by recruiting DNA (cytosine-5-)-methyltransferase 3A. Mol Cancer. 2010;9:93. doi:10.1186/1476-4598-9-93.
24. Lee EJ, Lee BB, Kim JW, Shim YM, Hoseok I, Han J, et al. Aberrant methylation of Fragile Histidine Triad gene is associated with poor prognosis in early stage esophageal squamous cell carcinoma. European journal of cancer (Oxford, England: 1990). 2006;42(7):972–80. doi:10.1016/j.ejca.2006.01.021.
25. Vogelsang M, Paccez JD, Schafer G, Dzobo K, Zerbini LF, Parker MI. Aberrant methylation of the MSH3 promoter and distal enhancer in esophageal cancer patients exposed to first-hand tobacco smoke. Journal of cancer research and clinical oncology. 2014. doi:10.1007/s00432-014-1736-x.
26. Mohammad Ganji S, Miotto E, Callegari E, Sayehmiri K, Fereidooni F, Yazdanbod M, et al. Associations of risk factors obesity and occupational airborne exposures with CDKN2A/p16 aberrant DNA methylation in esophageal cancer patients. Diseases of the esophagus: official journal of the International Society for Diseases of the Esophagus / ISDE. 2010;23(7):597–602. doi:10.1111/j.1442-2050.2010.01059.x.
27. Bagnardi V, Blangiardo M, La Vecchia C, Corrao G. A meta-analysis of alcohol drinking and cancer risk. Br J Cancer. 2001;85(11):1700–5. doi:10.1054/bjoc.2001.2140.
28. Liu Y, Chen H, Sun Z, Chen X. Molecular mechanisms of ethanol-associated oro-esophageal squamous cell carcinoma. Cancer Lett. 2015;361(2):164–73. doi:10.1016/j.canlet.2015.03.006.
29. Oze I, Matsuo K, Suzuki T, Kawase T, Watanabe M, Hiraki A, et al. Impact of multiple alcohol dehydrogenase gene polymorphisms on risk of upper aerodigestive tract cancers in a Japanese population. Cancer Epidemiol Biomarkers Prev. 2009;18(11):3097–102. doi:10.1158/1055-9965.epi-09-0499.
30. Tanaka F, Yamamoto K, Suzuki S, Inoue H, Tsurumaru M, Kajiyama Y, et al. Strong interaction between the effects of alcohol consumption and smoking on oesophageal squamous cell carcinoma among individuals with ADH1B and/or ALDH2 risk alleles. Gut. 2010;59(11):1457–64. doi:10.1136/gut.2009.205724.
31. Wu C, Kraft P, Zhai K, Chang J, Wang Z, Li Y, et al. Genome-wide association analyses of esophageal squamous cell carcinoma in Chinese identify multiple susceptibility loci and gene-environment interactions. Nat Genet. 2012;44(10):1090–7. doi:10.1038/ng.2411.
32. Anantharaman D, Marron M, Lagiou P, Samoli E, Ahrens W, Pohlabeln H, et al. Population attributable risk of tobacco and alcohol for upper aerodigestive tract cancer. Oral Oncol. 2011;47(8):725–31. doi:10.1016/j.oraloncology.2011.05.004.
33. Pelucchi C, Gallus S, Garavello W, Bosetti C, La Vecchia C. Cancer risk associated with alcohol and tobacco use: focus on upper aero-digestive tract and liver. Alcohol Res Health. 2006;29(3):193–8.
34. Bell-Parikh LC, Guengerich FP. Kinetics of cytochrome P450 2E1-catalyzed oxidation of ethanol to acetic acid via acetaldehyde. J Biol Chem. 1999;274(34):23833–40.
35. Kunitoh S, Imaoka S, Hiroi T, Yabusaki Y, Monna T, Funae Y. Acetaldehyde as well as ethanol is metabolized by human CYP2E1. J Pharmacol Exp Ther. 1997;280(2):527–32.
36. Seitz HK, Stickel F. Molecular mechanisms of alcohol-mediated carcinogenesis. Nat Rev Cancer. 2007;7(8):599–612. doi:10.1038/nrc2191.
37. Lu SC, Mato JM. Role of methionine adenosyltransferase and S-adenosylmethionine in alcohol-associated liver cancer. Alcohol. 2005;35(3):227–34. doi:10.1016/j.alcohol.2005.03.011.
38. Mason JB, Choi SW. Effects of alcohol on folate metabolism: implications for carcinogenesis. Alcohol. 2005;35(3):235–41. doi:10.1016/j.alcohol.2005.03.012.
39. Varela-Rey M, Woodhoo A, Martinez-Chantar ML, Mato JM, Lu SC. Alcohol, DNA methylation, and cancer. Alcohol Res. 2013;35(1):25–35.
40. Baba Y, Watanabe M, Baba H. Review of the alterations in DNA methylation in esophageal squamous cell carcinoma. Surg Today. 2013;43(12):1355–64. doi:10.1007/s00595-012-0451-y.
41. Guo M, Yan W. Epigenetics of gastric cancer. Methods Mol Biol. 2015;1238:783–99. doi:10.1007/978-1-4939-1804-1_41.
42. Jia Y, Guo M. Epigenetic changes in colorectal cancer. Chin J Cancer. 2013;32(1):21–30. doi:10.5732/cjc.011.10245.
43. Yan W, Guo M. Epigenetics of colorectal cancer. Methods Mol Biol. 2015;1238:405–24. doi:10.1007/978-1-4939-1804-1_22.
44. Guo M, Ren J, House MG, Qi Y, Brock MV, Herman JG. Accumulation of promoter methylation suggests epigenetic progression in squamous cell carcinoma of the esophagus. Clin Cancer Res. 2006;12(15):4515–22. doi:10.1158/1078-0432.ccr-05-2858.
45. Rong R, Jiang LY, Sheikh MS, Huang Y. Mitotic kinase Aurora-A phosphorylates RASSF1A and modulates RASSF1A-mediated microtubule interaction and M-phase cell cycle regulation. Oncogene. 2007;26(55):7700–8. doi:10.1038/sj.onc.1210575.
46. Du Z, Ma K, Sun X, Li A, Wang H, Zhang L, et al. Methylation of RASSF1A gene promoter and the correlation with DNMT1 expression that may contribute to esophageal squamous cell carcinoma. World J Surg Oncol. 2015;13(1):141. doi:10.1186/s12957-015-0557-y.
47. Kuroki T, Trapasso F, Yendamuri S, Matsuyama A, Alder H, Mori M, et al. Promoter hypermethylation of RASSF1A in esophageal squamous cell carcinoma. Clin Cancer Res. 2003;9(4):1441–5.
48. Mao WM, Li P, Zheng QQ, Wang CC, Ge MH, Hu FJ, et al. Hypermethylation-modulated downregulation of RASSF1A expression is associated with the progression of esophageal cancer. Arch Med Res. 2011;42(3):182–8. doi:10.1016/j.arcmed.2011.04.002.
49. Lu D, Ma J, Zhan Q, Li Y, Qin J, Guo M. Epigenetic silencing of RASSF10 promotes tumor growth in esophageal squamous cell carcinoma. Discov Med. 2014;17(94):169–78.
50. Summers MK, Bothos J, Halazonetis TD. The CHFR mitotic checkpoint protein delays cell cycle progression by excluding Cyclin B1 from the nucleus. Oncogene. 2005;24(16):2589–98. doi:10.1038/sj.onc.1208428.
51. Guo H, Yan W, Yang Y, Guo M. Promoter region methylation of DNA damage repair genes in human gastric cancer. Zhonghua Yi Xue Za Zhi. 2014;94(28):2193–6.
52. Guo M, Alumkal J, Drachova T, Gao D, Marina SS, Jen J, et al. CHFR methylation strongly correlates with methylation of DNA damage repair and apoptotic pathway genes in non-small cell lung cancer. Discov Med. 2015;19(104):151–8.
53. Vitiello M, Tuccoli A, Poliseno L. Long non-coding RNAs in cancer: implications for personalized therapy. Cell Oncol (Dordr). 2015;38(1):17–28. doi:10.1007/s13402-014-0180-x.
54. Yun T, Liu Y, Gao D, Linghu E, Brock MV, Yin D, et al. Methylation of CHFR sensitizes esophageal squamous cell cancer to docetaxel and paclitaxel. Genes Cancer. 2015;6(1-2):38–48.
55. Waters CE, Saldivar JC, Hosseini SA, Huebner K. The FHIT gene product: tumor suppressor and genome “caretaker”. Cellular and molecular life sciences: CMLS. 2014;71(23):4577–87. doi:10.1007/s00018-014-1722-0.
56. Croce CM, Sozzi G, Huebner K. Role of FHIT in human cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 1999;17(5):1618–24.
57. Hsieh P, Yamane K. DNA mismatch repair: molecular mechanism, cancer, and ageing. Mechanisms of ageing and development. 2008;129(7-8):391–407. doi:10.1016/j.mad.2008.02.012.
58. Curtin NJ. DNA repair dysregulation from cancer driver to therapeutic target. Nat Rev Cancer. 2012;12(12):801–17. doi:10.1038/nrc3399.
59. Boland CR, Goel A. Microsatellite instability in colorectal cancer. Gastroenterology. 2010;138(6):2073–87. doi:10.1053/j.gastro.2009.12.064. e3.
60. Li Y, Yang Y, Lu Y, Herman JG, Brock MV, Zhao P, et al. Predictive value of CHFR and MLH1 methylation in human gastric cancer. Gastric Cancer. 2015;18(2):280–7. doi:10.1007/s10120-014-0370-2.
61. Matsushita M, Takeuchi S, Yang Y, Yoshino N, Tsukasaki K, Taguchi H, et al. Methylation of the MLH1 gene in hematological malignancies. Oncol Rep. 2005;14(1):191–4.
62. Shigeyasu K, Nagasaka T, Mori Y, Yokomichi N, Kawai T, Fuji T, et al. Clinical significance of MLH1 methylation and CpG island methylator phenotype as prognostic markers in patients with gastric cancer. PLoS One. 2015;10(6):e0130409. doi:10.1371/journal.pone.0130409.
63. Ling ZQ, Li P, Ge MH, Hu FJ, Fang XH, Dong ZM, et al. Aberrant methylation of different DNA repair genes demonstrates distinct prognostic value for esophageal cancer. Dig Dis Sci. 2011;56(10):2992–3004. doi:10.1007/s10620-011-1774-z.
64. Su Y, Yin L, Liu R, Sheng J, Yang M, Wang Y, et al. Promoter methylation status of MGMT, hMSH2, and hMLH1 and its relationship to corresponding protein expression and TP53 mutations in human esophageal squamous cell carcinoma. Medical oncology (Northwood, London, England). 2014;31(2):784. doi:10.1007/s12032-013-0784-4.
65. Tzao C, Hsu HS, Sun GH, Lai HL, Wang YC, Tung HJ, et al. Promoter methylation of the hMLH1 gene and protein expression of human mutL homolog 1 and human mutS homolog 2 in resected esophageal squamous cell carcinoma. The Journal of thoracic and cardiovascular surgery. 2005;130(5):1371. doi:10.1016/j.jtcvs.2005.06.004.
66. Zhao JJ, Li HY, Wang D, Yao H, Sun DW. Abnormal MGMT promoter methylation may contribute to the risk of esophageal cancer: a meta-analysis of cohort studies. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine. 2014. doi:10.1007/s13277-014-2276-3.
67. Hasina R, Surati M, Kawada I, Arif Q, Carey GB, Kanteti R, et al. O-6-methylguanine-deoxyribonucleic acid methyltransferase methylation enhances response to temozolomide treatment in esophageal cancer. Journal of carcinogenesis. 2013;12:20. doi:10.4103/1477-3163.120632.
68. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell. 2006;127(3):469–80. doi:10.1016/j.cell.2006.10.018.
69. Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer. 2008;8(5):387–98. doi:10.1038/nrc2389.
70. Clement G, Braunschweig R, Pasquier N, Bosman FT, Benhattar J. Alterations of the Wnt signaling pathway during the neoplastic progression of Barrett’s esophagus. Oncogene. 2006;25(21):3084–92. doi:10.1038/sj.onc.1209338.
71. Saito T, Mitomi H, Imamhasan A, Hayashi T, Mitani K, Takahashi M, et al. Downregulation of sFRP-2 by epigenetic silencing activates the beta-catenin/Wnt signaling pathway in esophageal basaloid squamous cell carcinoma. Virchows Archiv: an international journal of pathology. 2014;464(2):135–43. doi:10.1007/s00428-014-1538-1.
72. Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Munsterberg A, et al. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature. 1990;346(6281):245–50. doi:10.1038/346245a0.
73. Jia Y, Yang Y, Zhan Q, Brock MV, Zheng X, Yu Y, et al. Inhibition of SOX17 by microRNA 141 and methylation activates the WNT signaling pathway in esophageal cancer. J Mol Diagn. 2012;14(6):577–85. doi:10.1016/j.jmoldx.2012.06.004.
74. Kuo IY, Wu CC, Chang JM, Huang YL, Lin CH, Yan JJ, et al. Low SOX17 expression is a prognostic factor and drives transcriptional dysregulation and esophageal cancer progression. International journal of cancer Journal international du cancer. 2014;135(3):563–73. doi:10.1002/ijc.28695.
75. Roperch JP, Incitti R, Forbin S, Bard F, Mansour H, Mesli F, Baumgaertner I, Brunetti F, Sobhani I. Aberrant methylation of NPY, PENK, and WIF1 as a promising marker for blood-based diagnosis of colorectal cancer. BMC Cancer. 2013;13. doi:10.1186/1471-2407-13-566.
76. Veeck J, Wild PJ, Fuchs T, Schüffler PJ, Hartmann A, Knüchel R, Dahl E. Prognostic relevance of Wnt-inhibitory factor-1 (WIF1) and Dickkopf-3 (DKK3) promoter methylation in human breast cancer. BMC cancer. 2009;9. doi:10.1186/1471-2407-9-217.
77. Li J, Ying J, Fan Y, Wu L, Ying Y, Chan AT, et al. WNT5A antagonizes WNT/beta-catenin signaling and is frequently silenced by promoter CpG methylation in esophageal squamous cell carcinoma. Cancer biology & therapy. 2010;10(6):617–24.
78. Brock MV, Gou M, Akiyama Y, Muller A, Wu TT, Montgomery E, et al. Prognostic importance of promoter hypermethylation of multiple genes in esophageal adenocarcinoma. Clin Cancer Res. 2003;9(8):2912–9.
79. Zare M, Jazii FR, Alivand MR, Nasseri NK, Malekzadeh R, Yazdanbod M. Qualitative analysis of adenomatous polyposis Coli promoter: hypermethylation, engagement and effects on survival of patients with esophageal cancer in a high risk region of the world, a potential molecular marker. BMC cancer. 2009;9:24. doi:10.1186/1471-2407-9-24.
80. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer. 2003;3(11):807–21. doi:10.1038/nrc1208.
81. Bierie B, Moses HL. TGF-beta and cancer. Cytokine Growth Factor Rev. 2006;17(1-2):29–40. doi:10.1016/j.cytogfr.2005.09.006.
82. Pardali K, Moustakas A. Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim Biophys Acta. 2007;1775(1):21–62. doi:10.1016/j.bbcan.2006.06.004.
83. Imamura T, Hikita A, Inoue Y. The roles of TGF-beta signaling in carcinogenesis and breast cancer metastasis. Breast Cancer. 2012;19(2):118–24. doi:10.1007/s12282-011-0321-2.
84. Zheng Y, Zhang Y, Huang X, Chen L. Analysis of the RUNX3 gene methylation in serum DNA from esophagus squamous cell carcinoma, gastric and colorectal adenocarcinoma patients. Hepatogastroenterology. 2011;58(112):2007–11. doi:10.5754/hge10016.
85. Wu L, Herman JG, Brock MV, Wu K, Mao G, Yan W, et al. Silencing DACH1 promotes esophageal cancer growth by inhibiting TGF-beta signaling. PLoS One. 2014;9(4):e95509. doi:10.1371/journal.pone.0095509.
86. Qin H, Chan MW, Liyanarachchi S, Balch C, Potter D, Souriraj IJ, et al. An integrative ChIP-chip and gene expression profiling to model SMAD regulatory modules. BMC systems biology. 2009;3:73. doi:10.1186/1752-0509-3-73.
87. Guo W, Zhang M, Shen S, Guo Y, Kuang G, Yang Z, et al. Aberrant methylation and decreased expression of the TGF-beta/Smad target gene FBXO32 in esophageal squamous cell carcinoma. Cancer. 2014;120(16):2412–23. doi:10.1002/cncr.28764.
88. Shishodia S, Aggarwal BB. Nuclear factor-kappaB activation mediates cellular transformation, proliferation, invasion angiogenesis and metastasis of cancer. Cancer Treat Res. 2004;119:139–73.
89. Aggarwal BB. Nuclear factor-kappaB: the enemy within. Cancer Cell. 2004;6(3):203–8. doi:10.1016/j.ccr.2004.09.003.
90. Ahn KS, Aggarwal BB. Transcription factor NF-kappaB: a sensor for smoke and stress signals. Ann N Y Acad Sci. 2005;1056:218–33. doi:10.1196/annals.1352.026.
91. Sethi G, Sung B, Aggarwal BB. Nuclear factor-kappaB activation: from bench to bedside. Exp Biol Med (Maywood). 2008;233(1):21–31. doi:10.3181/0707-mr-196.
92. Garg A, Aggarwal BB. Nuclear transcription factor-kappaB as a target for cancer drug development. Leukemia. 2002;16(6):1053–68. doi:10.1038/sj.leu.2402482.
93. Karin M, van Hogerlinden M, Rozell BL, Ahrlund-Richter L, Toftgard R. Nuclear factor-kappaB in cancer development and progression squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-kappaB signaling. Nature. 2006;441(7092):431–6. doi:10.1038/nature04870.
94. van Hogerlinden M, Auer G, Toftgard R. Inhibition of Rel/Nuclear Factor-kappaB signaling in skin results in defective DNA damage-induced cell cycle arrest and Ha-ras- and p53-independent tumor development. Oncogene. 2002;21(32):4969–77. doi:10.1038/sj.onc.1205620.
95. van Hogerlinden M, Rozell BL, Ahrlund-Richter L, Toftgard R. Squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-kappaB signaling. Cancer Res. 1999;59(14):3299–303.
96. Li J, Minnich DJ, Camp ER, Brank A, Mackay SL, Hochwald SN. Enhanced sensitivity to chemotherapy in esophageal cancer through inhibition of NF-kappaB. J Surg Res. 2006;132(1):112–20. doi:10.1016/j.jss.2005.10.005.
97. Li B, Li YY, Tsao SW, Cheung AL. Targeting NF-kappaB signaling pathway suppresses tumor growth, angiogenesis, and metastasis of human esophageal cancer. Mol Cancer Ther. 2009;8(9):2635–44. doi:10.1158/1535-7163.mct-09-0162.
98. Cheng Y, Geng H, Cheng SH, Liang P, Bai Y, Li J, et al. KRAB zinc finger protein ZNF382 is a proapoptotic tumor suppressor that represses multiple oncogenes and is commonly silenced in multiple carcinomas. Cancer Res. 2010;70(16):6516–26. doi:10.1158/0008-5472.can-09-4566.
99. Harris RA, Wang T, Coarfa C, Nagarajan RP, Hong C, Downey SL, et al. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat Biotechnol. 2010;28(10):1097–105. doi:10.1038/nbt.1682.
100. Cordaux R, Batzer MA. The impact of retrotransposons on human genome evolution. Nat Rev Genet. 2009;10(10):691–703. doi:10.1038/nrg2640.
101. Saito K, Kawakami K, Matsumoto I, Oda M, Watanabe G, Minamoto T. Long interspersed nuclear element 1 hypomethylation is a marker of poor prognosis in stage IA non-small cell lung cancer. Clin Cancer Res. 2010;16(8):2418–26. doi:10.1158/1078-0432.ccr-09-2819.
102. Murata A, Baba Y, Watanabe M, Shigaki H, Miyake K, Ishimoto T, et al. IGF2 DMR0 methylation, loss of imprinting, and patient prognosis in esophageal squamous cell carcinoma. Ann Surg Oncol. 2014;21(4):1166–74. doi:10.1245/s10434-013-3414-7.
103. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science. 2011;333(6047):1303–7. doi:10.1126/science.1210944.
104. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature. 2010;466(7310):1129–33. doi:10.1038/nature09303.
105. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science. 2011;333(6047):1300–3. doi:10.1126/science.1210597.
106. 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(2):200–13. doi:10.1016/j.stem.2011.01.008.
107. 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(5929):930–5. doi:10.1126/science.1170116.
108. Zhang H, Zhang X, Clark E, Mulcahey M, Huang S, Shi YG. TET1 is a DNA-binding protein that modulates DNA methylation and gene transcription via hydroxylation of 5-methylcytosine. Cell Res. 2010;20(12):1390–3. doi:10.1038/cr.2010.156.
109. Chen K, Zhang J, Guo Z, Ma Q, Xu Z, Zhou Y, et al. Loss of 5-hydroxymethylcytosine is linked to gene body hypermethylation in kidney cancer. Cell Res. 2016;26(1):103–18. doi:10.1038/cr.2015.150.
110. Murata A, Baba Y, Ishimoto T, Miyake K, Kosumi K, Harada K, et al. TET family proteins and 5-hydroxymethylcytosine in esophageal squamous cell carcinoma. Oncotarget. 2015;6(27):23372–82. doi:10.18632/oncotarget.4281.
111. Guo M, Ren J, Brock MV, Herman JG, Carraway HE. Promoter methylation of HIN-1 in the progression to esophageal squamous cancer. Epigenetics. 2008;3(6):336–41.
112. Jia Y, Yang Y, Brock MV, Cao B, Zhan Q, Li Y, et al. Methylation of TFPI-2 is an early event of esophageal carcinogenesis. Epigenomics. 2012;4(2):135–46. doi:10.2217/epi.12.11.
113. Wang JS, Guo M, Montgomery EA, Thompson RE, Cosby H, Hicks L, et al. DNA promoter hypermethylation of p16 and APC predicts neoplastic progression in Barrett’s esophagus. Am J Gastroenterol. 2009;104(9):2153–60. doi:10.1038/ajg.2009.300.
114. Takeno S, Noguchi T, Fumoto S, Kimura Y, Shibata T, Kawahara K. E-cadherin expression in patients with esophageal squamous cell carcinoma: promoter hypermethylation, Snail overexpression, and clinicopathologic implications. Am J Clin Pathol. 2004;122(1):78–84. doi:10.1309/p2cd-fgu1-u7cl-v5yr.
115. Sato F, Shimada Y, Watanabe G, Uchida S, Makino T, Imamura M. Expression of vascular endothelial growth factor, matrix metalloproteinase-9 and E-cadherin in the process of lymph node metastasis in oesophageal cancer. Br J Cancer. 1999;80(9):1366–72. doi:10.1038/sj.bjc.6690530.
116. Lee EJ, Lee BB, Han J, Cho EY, Shim YM, Park J, et al. CpG island hypermethylation of E-cadherin (CDH1) and integrin alpha4 is associated with recurrence of early stage esophageal squamous cell carcinoma. Int J Cancer. 2008;123(9):2073–9. doi:10.1002/ijc.23598.
117. Fukuoka T, Hibi K, Nakao A. Aberrant methylation is frequently observed in advanced esophageal squamous cell carcinoma. Anticancer Res. 2006;26(5A):3333–5.
118. Yamaguchi S, Kato H, Miyazaki T, Sohda M, Kimura H, Ide M, et al. RASSF1A gene promoter methylation in esophageal cancer specimens. Dis Esophagus. 2005;18(4):253–6. doi:10.1111/j.1442-2050.2005.00501.x.
119. Li B, Wang B, Niu LJ, Jiang L, Qiu CC. Hypermethylation of multiple tumor-related genes associated with DNMT3b up-regulation served as a biomarker for early diagnosis of esophageal squamous cell carcinoma. Epigenetics. 2011;6(3):307–16.
120. Maesawa C, Tamura G, Nishizuka S, Ogasawara S, Ishida K, Terashima M, et al. Inactivation of the CDKN2 gene by homozygous deletion and de novo methylation is associated with advanced stage esophageal squamous cell carcinoma. Cancer Res. 1996;56(17):3875–8.
121. Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, et al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med. 2000;343(19):1350–4. doi:10.1056/nejm200011093431901.
122. Yan W, Herman JG, Guo M. Epigenome-based personalized medicine in human cancer. Epigenomics. 2015. doi:10.2217/epi.15.84.
123. Scolnick DM, Halazonetis TD. Chfr defines a mitotic stress checkpoint that delays entry into metaphase. Nature. 2000;406(6794):430–5. doi:10.1038/35019108.
124. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz Jr LA, Kinzler KW. Cancer genome landscapes. Science. 2013;339(6127):1546–58. doi:10.1126/science.1235122.
125. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, et al. The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol. 2010;28(10):1045–8. doi:10.1038/nbt1010-1045.
126. Adams D, Altucci L, Antonarakis SE, Ballesteros J, Beck S, Bird A, et al. BLUEPRINT to decode the epigenetic signature written in blood. Nat Biotechnol. 2012;30(3):224–6. doi:10.1038/nbt.2153.
127. Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet. 2012;13(10):679–92. doi:10.1038/nrg3270.
128. Toh Y, Egashira A, Yamamoto M. Epigenetic alterations and their clinical implications in esophageal squamous cell carcinoma. Gen Thorac Cardiovasc Surg. 2013;61(5):262–9. doi:10.1007/s11748-013-0235-3.
129. Kelly TK, De Carvalho DD, Jones PA. Epigenetic modifications as therapeutic targets. Nat Biotechnol. 2010;28(10):1069–78. doi:10.1038/nbt.1678.
130. Goel A, Boland CR. Epigenetics of colorectal cancer. Gastroenterology. 2012;143(6):1442–60. doi:10.1053/j.gastro.2012.09.032. e1.
131. Yan W, Herman JG, Guo M. Epigenome-based personalized medicine in human cancer. Epigenomics. 2016;8(1):119–33. doi:10.2217/epi.15.84.
132. Anupam K, Tusharkant C, Gupta SD, Ranju R. Loss of disabled-2 expression is an early event in esophageal squamous tumorigenesis. World J Gastroenterol. 2006;12(37):6041–5.
133. Mandelker DL, Yamashita K, Tokumaru Y, Mimori K, Howard DL, Tanaka Y et al. PGP9.5 promoter methylation is an independent prognostic factor for esophageal squamous cell carcinoma. Cancer Res. 2005;65(11):4963–8. doi:10.1158/0008-5472.can-04-3923.
134. Li LW, Yu XY, Yang Y, Zhang CP, Guo LP, Lu SH. Expression of esophageal cancer related gene 4 (ECRG4), a novel tumor suppressor gene, in esophageal cancer and its inhibitory effect on the tumor growth in vitro and in vivo. Int J Cancer. 2009;125(7):1505–13. doi:10.1002/ijc.24513.
135. Kawakami K, Brabender J, Lord RV, Groshen S, Greenwald BD, Krasna MJ et al. Hypermethylated APC DNA in plasma and prognosis of patients with esophageal adenocarcinoma. J Natl Cancer Inst. 2000;92(22):1805–11.
136. Jin Z, Mori Y, Yang J, Sato F, Ito T, Cheng Y et al. Hypermethylation of the nel-like 1 gene is a common and early event and is associated with poor prognosis in early-stage esophageal adenocarcinoma. Oncogene. 2007;26(43):6332–40. doi:10.1038/sj.onc.1210461.
137. Ohta M, Mimori K, Fukuyoshi Y, Kita Y, Motoyama K, Yamashita K et al. Clinical significance of the reduced expression of G protein gamma 7 (GNG7) in oesophageal cancer. Br J Cancer. 2008;98(2):410–7. doi:10.1038/sj.bjc.6604124.
138. Jiang S, Linghu E, Zhan Q, Han W, Guo M. Methylation of ZNF331 Promotes Cell Invasion and Migration in Human Esophageal Cancer. Curr Protein Pept Sci. 2015;16(4):322–8.