Journal of Shandong University (Health Sciences) ›› 2021, Vol. 59 ›› Issue (5): 30-39.doi: 10.6040/j.issn.1671-7554.0.2021.0272

• Current Advance of Basic and Clinical Medical Virology • Previous Articles     Next Articles

Impact of EBV on the epigenetics of gastric carcinoma

Bing LUO*()   

  1. Department of Pathogen Biology, School of Basic Medical Sciences, Qingdao University, Qingdao 266071, Shandong, China
  • Received:2021-03-12 Online:2021-05-10 Published:2021-06-01
  • Contact: Bing LUO E-mail:qdluobing@163.com

Abstract:

Epstein-Barr virus (EBV), an important human tumor virus, is closely related to the occurrence of a variety of tumors, including 10% gastric cancer. The role of EBV in gastric carcinogenesis has received increasing attention and EBV is considered to be another pathogenic factor in addition to Helicobacter pylori. In EBV-associated gastric carcinoma (EBVaGC), a typical characteristic is the extensive methylation of viral and host genomes, which expresses a limited number of viral genes including EBV nuclear antigen 1, EBV encoded small RNAs, Bam HI-A rightward transcripts, latent membrane protein 2A and miRNAs. Combined with other epigenetic mechanisms, EBV infection acts as an epigenetic driver of EBVaGC oncogenesis. This review will discuss the impact of EBV on the epigenetic alterations in EBVaGC and its role in oncogenesis.

Key words: DNA methylation, Epstein-Barr virus, Epigenetics, Gastric carcinoma, MicroRNA

CLC Number: 

  • R373.9
1 Young LS , Yap LF , Murray PG . Epstein-Barr virus: more than 50 years old and still providing surprises[J]. Nat Rev Cancer, 2016, 16 (12): 789- 802.
doi: 10.1038/nrc.2016.92
2 Saha A , Kaul R , Murakami M , et al. Tumor viruses and cancer biology: modulating signaling pathways for therapeutic intervention[J]. Cancer Biol Ther, 2010, 10 (10): 961- 978.
doi: 10.4161/cbt.10.10.13923
3 Tsao SW , Tsang CM , To KF . The role of Epstein-Barr virus in epithelial malignancies[J]. J Pathol, 2015, 235 (2): 323- 333.
doi: 10.1002/path.4448
4 Tsao SW , Tsang CM , Lo KW . Epstein-Barr virus infection and nasopharyngeal carcinoma[J]. Philos Trans R Soc Lond B Biol Sci, 2017, 372 (1732): 20160270.
doi: 10.1098/rstb.2016.0270
5 Nishikawa J , Yoshiyama H , Iizasa H , et al. Epstein-Barr virus in gastric carcinoma[J]. Cancers (Basel), 2014, 6 (4): 2259- 2274.
doi: 10.3390/cancers6042259
6 Iizasa H , Nanbo A , Nishikawa J , et al. Epstein-Barr virus (EBV)-associated gastric carcinoma[J]. Viruses, 2012, 4 (12): 3420- 3439.
doi: 10.3390/v4123420
7 Chen XZ , Chen H , Castro FA , et al. Epstein-Barr virus infection and gastric cancer: a systematic review[J]. Medicine (Baltimore), 2015, 94 (20): e792.
doi: 10.1097/MD.0000000000000792
8 Bae JM , Kim EH . Epstein-Barr virus and gastric cancer risk: a meta-analysis with meta-regression of case-control studies[J]. J Prev Med Public Health, 2016, 49 (2): 97- 107.
doi: 10.3961/jpmph.15.068
9 Qiao YW , Zhao XQ , Liu J . Clinicopathological features of Epstein-Barr virus-associated gastric carcinoma: a systematic review and meta-analysis[J]. J BUON, 2019, 24 (3): 1092- 1099.
10 Li S , Du H , Wang Z . Meta-analysis of the relationship between Epstein-Barr virus infection and clinicopathological features of patients with gastric carcinoma[J]. Sci China Life Sci, 2010, 53 (4): 524- 530.
doi: 10.1007/s11427-010-0082-8
11 Ribeiro J , Oliveira A , Malta M , et al. Clinical and pathological characterization of Epstein-Barr virus-associated gastric carcinomas in Portugal[J]. World J Gastroenterol, 2017, 23 (40): 7292- 7302.
doi: 10.3748/wjg.v23.i40.7292
12 Castaneda CA , Castillo M , Chavez I , et al. Prevalence of Helicobacter pylori infection, its virulent genotypes, and Epstein-Barr virus in Peruvian patients with chronic gastritis and gastric cancer[J]. J Glob Oncol, 2019, 5, 1- 9.
doi: 10.1200/JGO.19.00122
13 Chen JN , He D , Tang F . Epstein-Barr virus-associated gastric carcinoma: a newly defined entity[J]. J Clin Gastroenterol, 2012, 46 (4): 262- 271.
doi: 10.1097/MCG.0b013e318249c4b8
14 Fukayama M , Kunita A , Kaneda A . Gastritis-infection-cancer sequence of Epstein-Barr virus-associated gastric cancer[J]. Adv Exp Med Biol, 2018, 1045, 437- 457.
doi: 10.1007/978-981-10-7230-7_20
15 Vistarop AG , Cohen M , De Matteo E . Analysis of Epstein-Barr virus infection models in a series of pediatric carriers from a developing country[J]. Sci Rep, 2016, 6, 23303.
doi: 10.1038/srep23303
16 Cho J , Kang MS , Kim KM . Epstein-Barr virus-associated gastric carcinoma and specific features of the accompanying immune response[J]. J Gastric Cancer, 2016, 16 (1): 1- 7.
doi: 10.5230/jgc.2016.16.1.1
17 Cancer Genome Atlas Research Network . Comprehensive molecular characterization of gastric adenocarcinoma[J]. Nature, 2014, 513 (7517): 202- 209.
doi: 10.1038/nature13480
18 Klutstein M , Nejman D , Greenfield R . DNA methylation in cancer and aging[J]. Cancer Res, 2016, 76 (12): 3446- 3450.
doi: 10.1158/0008-5472.CAN-15-3278
19 Fialkova V , Vidomanova E , Balharek T , et al. DNA methylation as mechanism of apoptotic resistance development in endometrial cancer patients[J]. Gen Physiol Biophys, 2017, 36 (5): 521- 529.
doi: 10.4149/gpb_2017032
20 Calcagno DQ , Gigek CO , Chen ES . DNA and histone methylation in gastric carcinogenesis[J]. World J Gastroenterol, 2013, 19 (8): 1182- 1192.
doi: 10.3748/wjg.v19.i8.1182
21 Scott RS . Epstein-Barr virus: a master epigenetic manipulator[J]. Curr Opin Virol, 2017, 26, 74- 80.
doi: 10.1016/j.coviro.2017.07.017
22 Shinozaki-Ushiku A , Kunita A , Fukayama M . Update on Epstein-Barr virus and gastric cancer[J]. Int J Oncol, 2015, 46 (4): 1421- 1434.
doi: 10.3892/ijo.2015.2856
23 Ribeiro J , Oliveira C , Malta M . Epstein-Barr virus gene expression and latency pattern in gastric carcinomas: a systematic review[J]. Future Oncol, 2017, 13 (6): 567- 579.
doi: 10.2217/fon-2016-0475
24 Sugiura M , Imai S , Tokunaga M , et al. Transcriptional analysis of Epstein-Barr virus gene expression in EBV-positive gastric carcinoma: unique viral latency in the tumour cells[J]. Br J Cancer, 1996, 74 (4): 625- 631.
doi: 10.1038/bjc.1996.412
25 Chong JM , Sakuma K , Sudo M , et al. Global and non-random CpG-island methylation in gastric carcinoma associated with Epstein-Barr virus[J]. Cancer Sci, 2003, 94 (1): 76- 80.
doi: 10.1111/j.1349-7006.2003.tb01355.x
26 Kang GH , Lee S , Kim WH , et al. Epstein-Barr virus-positive gastric carcinoma demonstrates frequent aberrant methylation of multiple genes and constitutes CpG island methylator phenotype-positive gastric carcinoma[J]. Am J Pathol, 2002, 160 (3): 787- 794.
doi: 10.1016/S0002-9440(10)64901-2
27 Tempera I , Lieberman PM . Epigenetic regulation of EBV persistence and oncogenesis[J]. Semin Cancer Biol, 2014, 26, 22- 29.
doi: 10.1016/j.semcancer.2014.01.003
28 Cohen JI . Epstein-Barr virus infection[J]. N Engl J Med, 2000, 343 (7): 481- 492.
doi: 10.1056/NEJM200008173430707
29 Kieff E , Rickinson AB . Epstein-Barr virus and its replication. In: Fields Virology 5th. Knipe DM, Howley PM (Eds.)[M]. Philadelphia: Lippincott, Williams & Wilkins, 2007: 2603- 2654.
30 Kaneda A , Matsusaka K , Aburatani H . Epstein-Barr virus infection as an epigenetic driver of tumorigenesis[J]. Cancer Res, 2012, 72 (14): 3445- 3450.
doi: 10.1158/0008-5472.CAN-11-3919
31 Wang LW , Jiang S , Gewurz BE . Epstein-Barr virus LMP1-mediated oncogenicity[J]. J Virol, 2017, 91 (21): e01718-16.
doi: 10.1128/JVI.01718-16
32 Tsai CL , Li HP , Lu YJ , et al. Activation of DNA methyltransferase 1 by EBV LMP1 involves c-Jun NH(2)-terminal kinase signaling[J]. Cancer Res, 2006, 66 (24): 11668- 11676.
doi: 10.1158/0008-5472.CAN-06-2194
33 Lu F , Weidmer A , Liu CG . Epstein-Barr virus-induced miR-155 attenuates NF-kappaB signaling and stabilizes latent virus persistence[J]. J Virol, 2008, 82 (21): 10436- 10443.
doi: 10.1128/JVI.00752-08
34 Hino R , Uozaki H , Murakami N , et al. Activation of DNA methyltransferase 1 by EBV latent membrane protein 2A leads to promoter hypermethylation of PTEN gene in gastric carcinoma[J]. Cancer Res, 2009, 69 (7): 2766- 2774.
doi: 10.1158/0008-5472.CAN-08-3070
35 Wang J , Liu W , Zhang X . LMP2A induces DNA methylation and expression repression of AQP3 in EBV-associated gastric carcinoma[J]. Virology, 2019, 534, 87- 95.
doi: 10.1016/j.virol.2019.06.006
36 Zhao J , Liang Q , Cheung KF , et al. Genome-wide identification of Epstein-Barr virus-driven promoter methylation profiles of human genes in gastric cancer cells[J]. Cancer, 2013, 119 (2): 304- 312.
doi: 10.1002/cncr.27724
37 Pathania R , Ramachandran S , Elangovan S , et al. DNMT1 is essential for mammary and cancer stem cell maintenance and tumorigenesis[J]. Nat Commun, 2015, 6, 6910.
doi: 10.1038/ncomms7910
38 Honeywell RJ , Sarkisjan D , Kristensen MH , et al. DNA methyltransferases expression in normal tissues and various human cancer cell lines, xenografts and tumors[J]. Nucleosides Nucleotides Nucleic Acids, 2018, 37 (12): 696- 708.
doi: 10.1080/15257770.2018.1498516
39 Piyathilake CJ , Badiga S , Borak SG , et al. A higher degree of expression of DNA methyl transferase 1 in cervical cancer is associated with poor survival outcome[J]. Int J Womens Health, 2017, 9, 413- 420.
doi: 10.2147/IJWH.S133441
40 Ding WJ , Fang JY , Chen XY , et al. The expression and clinical significance of DNA methyltransferase proteins in human gastric cancer[J]. Dig Dis Sci, 2008, 53 (8): 2083- 2089.
doi: 10.1007/s10620-007-0145-2
41 Scholle F , Bendt KM , Raab-T raub N . Epstein-Barr virus LMP2A transforms epithelial cells, inhibits cell differentiation, and activates Akt[J]. J Virol, 2000, 74 (22): 10681- 10689.
doi: 10.1128/JVI.74.22.10681-10689.2000
42 Shair KH , Bendt KM , Edwards RH , et al. Epstein-Barr virus-encoded latent membrane protein 1(LMP1) and LMP2A function cooperatively to promote carcinoma development in a mouse carcinogenesis model[J]. J Virol, 2012, 86 (9): 5352- 5365.
doi: 10.1128/JVI.07035-11
43 Pang MF , Lin KW , Peh SC . The signaling pathways of Epstein-Barr virus-encoded latent membrane protein 2A (LMP2A) in latency and cancer[J]. Cell Mol Biol Lett, 2009, 14 (2): 222- 247.
44 Fukuda M , Kawaguchi Y . Role of the immunoreceptor tyrosine-based activation motif of latent membrane protein 2A (LMP2A) in Epstein-Barr virus LMP2A-induced cell transformation[J]. J Virol, 2014, 88 (9): 5189- 5194.
doi: 10.1128/JVI.03714-13
45 Kong QL , Hu LJ , Cao JY , et al. Epstein-Barr virus-encoded LMP2A induces an epithelial-mesenchymal transition and increases the number of side population stem-like cancer cells in nasopharyngeal carcinoma[J]. PLoS Pathog, 2010, 6 (6): e1000940.
doi: 10.1371/journal.ppat.1000940
46 Seo JS , Jun SM , Kwon SW , et al. Establishment and characterization of gastric carcinoma cell clones expressing LMP2A of Epstein-Barr virus[J]. Int J Mol Med, 2010, 25 (1): 11- 16.
47 Hino R , Uozaki H , Inoue Y , et al. Survival advantage of EBV-associated gastric carcinoma: survivin up-regulation by viral latent membrane protein 2A[J]. Cancer Res, 2008, 68 (5): 1427- 1435.
doi: 10.1158/0008-5472.CAN-07-3027
48 Frappier L . EBNA1[J]. Curr Top Microbiol Immunol, 2015, 391, 3- 34.
doi: 10.1007/978-3-319-22834-1_1
49 Yates JL , Warren N , Sugden B . Stable replication of plasmids derived from Epstein-Barr virus in various mammalian cells[J]. Nature, 1985, 313 (6005): 812- 815.
doi: 10.1038/313812a0
50 Mansouri S , Pan Q , Blencowe BJ , et al. Epstein-Barr virus EBNA1 protein regulates viral latency through effects on let-7 microRNA and dicer[J]. J Virol, 2014, 88 (19): 11166- 11177.
doi: 10.1128/JVI.01785-14
51 Wang L , Tian WD , Xu X , et al. Epstein-Barr virus nuclear antigen 1 (EBNA1) protein induction of epithelial-mesenchymal transition in nasopharyngeal carcinoma cells[J]. Cancer, 2014, 120 (3): 363- 372.
doi: 10.1002/cncr.28418
52 Frappier L . Role of EBNA1 in NPC tumourigenesis[J]. Semin Cancer Biol, 2012, 22 (2): 154- 161.
doi: 10.1016/j.semcancer.2011.12.002
53 Sheng Y , Saridakis V , Sarkari F , et al. Molecular recognition of p53 and MDM2 by USP7/HAUSP[J]. Nat Struct Mol Biol, 2006, 13 (3): 285- 291.
doi: 10.1038/nsmb1067
54 Iwakiri D , T akada K . Role of EBERs in the pathogenesis of EBV Infection[J]. Adv Cancer Res, 2010, 107, 119- 136.
doi: 10.1016/S0065-230X(10)07004-1
55 Fukayama M , Hayashi Y , Iwasaki Y , et al. Epstein-Barr virus-associated gastric carcinoma and Epstein-Barr virus infection of the stomach[J]. Lab Invest, 1994, 71 (1): 73- 81.
56 Chen X , Fan S , Song E . Noncoding RNAs: new players in cancers[J]. Adv Exp Med Biol, 2016, 927, 1- 47.
doi: 10.1007/978-981-10-1498-7_1
57 Banerjee AS , Pal AD , Banerjee S . Epstein-Barr virus-encoded small non-coding RNAs induce cancer cell chemoresistance and migration[J]. Virology, 2013, 443 (2): 294- 305.
doi: 10.1016/j.virol.2013.05.020
58 Iwakiri D . Epstein-Barr virus-encoded RNAs: key molecules in viral pathogenesis[J]. Cancers (Basel), 2014, 6 (3): 1615- 1630.
doi: 10.3390/cancers6031615
59 Samanta M , Iwakiri D , T akada K . Epstein-Barr virus-encoded small RNA induces IL-10 through RIG-I-mediated IRF-3 signaling[J]. Oncogene, 2008, 27 (30): 4150- 4160.
doi: 10.1038/onc.2008.75
60 Takada K . Role of EBER and BARF1 in nasopharyngeal carcinoma (NPC) tumorigenesis[J]. Semin Cancer Biol, 2012, 22 (2): 162- 165.
doi: 10.1016/j.semcancer.2011.12.007
61 Iwakiri D , Eizuru Y , T okunaga M , et al. Autocrine growth of Epstein-Barr virus-positive gastric carcinoma cells mediated by an Epstein-Barr virus-encoded small RNA[J]. Cancer Res, 2003, 63 (21): 7062- 7067.
62 Pang PS , Liu T , Lin W , et al. Defining early events of Epstein-Barr virus (EBV) infection in immortalized nasopharyngeal epithelial cells using cell-free EBV infection[J]. J Gen Virol, 2019, 100 (6): 999- 1012.
doi: 10.1099/jgv.0.001243
63 Allday MJ . EBV finds a polycomb-mediated, epigenetic solution to the problem of oncogenic stress responses triggered by infection[J]. Front Genet, 2013, 4, 212.
doi: 10.3389/fgene.2013.00212
64 Chen H , Huang J , Wu FY , et al. Regulation of expression of the Epstein-Barr virus BamHI-A rightward transcripts[J]. J Virol, 2005, 79 (3): 1724- 1733.
doi: 10.1128/JVI.79.3.1724-1733.2005
65 Kuzembayeva M , Hayes M , Sugden B . Multiple functions are mediated by the miRNAs of Epstein-Barr virus[J]. Curr Opin Virol, 2014, 7, 61- 65.
doi: 10.1016/j.coviro.2014.04.003
66 Piccaluga PP , Navari M , De Falco G , et al. Virus-encoded microRNA contributes to the molecular profile of EBV-positive Burkitt lymphomas[J]. Oncotarget, 2016, 7 (1): 224- 240.
doi: 10.18632/oncotarget.4399
67 De Falco G , Antonicelli G , Onnis A , et al. Role of EBV in microRNA dysregulation in Burkitt lymphoma[J]. Semin Cancer Biol, 2009, 19 (6): 401- 406.
doi: 10.1016/j.semcancer.2009.07.003
68 Dong M , Chen JN , Huang JT , et al. The roles of EBV-encoded microRNAs in EBV-associated tumors[J]. Crit Rev Oncol Hematol, 2019, 135, 30- 38.
doi: 10.1016/j.critrevonc.2019.01.014
69 Marquitz AR , Raab-T raub N . The role of miRNAs and EBV BART s in NPC[J]. Semin Cancer Biol, 2012, 22 (2): 166- 172.
doi: 10.1016/j.semcancer.2011.12.001
70 Shinozaki-Ushiku A , Kunita A , Isogai M , et al. Profiling of virus-encoded microRNAs in Epstein-Barr virus-associated gastric carcinoma and their roles in gastric carcinogenesis[J]. J Virol, 2015, 89 (10): 5581- 5591.
doi: 10.1128/JVI.03639-14
71 Kim DN , Chae HS , Oh ST , et al. Expression of viral microRNAs in Epstein-Barr virus-associated gastric carcinoma[J]. J Virol, 2007, 81 (2): 1033- 1036.
doi: 10.1128/JVI.02271-06
72 Tsai CY , Liu YY , Liu KH , et al. Comprehensive profiling of virus microRNAs of Epstein-Barr virus-associated gastric carcinoma: highlighting the interactions of ebv-Bart9 and host tumor cells[J]. J Gastroenterol. Hepatol, 2017, 32 (1): 82- 91.
doi: 10.1111/jgh.13432
73 Choi H , Lee SK . TAX1BP1 downregulation by EBV-miR-BART15-3p enhances chemosensitivity of gastric cancer cells to 5-FU[J]. Arch Virol, 2017, 162 (2): 369- 377.
doi: 10.1007/s00705-016-3109-z
74 Kang D , Skalsky RL , Cullen BR . EBV BART microRNAs target multiple pro-apoptotic cellular genes to promote epithelial cell survival[J]. PLoS Pathog, 2015, 11 (6): e1004979.
doi: 10.1371/journal.ppat.1004979
75 Choy EY , Siu KL , Kok KH , et al. An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival[J]. J Exp Med, 2008, 205 (11): 2551- 2560.
doi: 10.1084/jem.20072581
76 Marquitz AR , Mathur A , Nam CS , et al. The Epstein-Barr virus BART microRNAs target the pro-apoptotic protein Bim[J]. Virology, 2011, 412 (2): 392- 400.
doi: 10.1016/j.virol.2011.01.028
77 Kim H , Choi H , Lee SK . Epstein-Barr virus miR-BART20-5p regulates cell proliferation and apoptosis by targeting BAD[J]. Cancer Lett, 2015, 356 (2 Pt B): 733- 742.
78 Kim H , Choi H , Lee SK . Epstein-Barr virus MicroRNA miR-BART20-5p suppresses lytic induction by inhibiting BAD-mediated caspase-3-dependent apoptosis[J]. J Virol, 2015, 90 (3): 1359- 1368.
79 Choi H , Lee H , Kim SR , et al. Epstein-Barr virus-encoded microRNA BART15-3p promotes cell apoptosis partially by targeting BRUCE[J]. J Virol, 2013, 87 (14): 8135- 8144.
doi: 10.1128/JVI.03159-12
80 He B , Li W , Wu Y , et al. Epstein-Barr virus-encoded miR-BART6-3p inhibits cancer cell metastasis and invasion by targeting long non-coding RNA LOC553103[J]. Cell Death Dis, 2016, 7 (9): e2353.
doi: 10.1038/cddis.2016.253
81 Cai LM , Lyu XM , Luo WR , et al. EBV-miR-BART7-3p promotes the EMT and metastasis of nasopharyngeal carcinoma cells by suppressing the tumor suppressor PTEN[J]. Oncogene, 2015, 34 (17): 2156- 2166.
doi: 10.1038/onc.2014.341
82 Cai L , Ye Y , Jiang Q , et al. Epstein-Barr virus-encoded microRNA BART1 induces tumour metastasis by regulating PTEN-dependent pathways in nasopharyngeal carcinoma[J]. Nat Commun, 2015, 6, 7353.
doi: 10.1038/ncomms8353
83 Jung YJ , Choi H , Kim H , et al. MicroRNA miR-BART20-5p stabilizes Epstein-Barr virus latency by directly targeting BZLF1 and BRLF1[J]. J Virol, 2014, 88 (16): 9027- 9037.
doi: 10.1128/JVI.00721-14
84 Kang BW , Choi Y , Kwon OK , et al. High level of viral microRNA-BART20-5p expression is associated with worse survival of patients with Epstein-Barr virus-associated gastric cancer[J]. Oncotarget, 2017, 8 (9): 14988- 14994.
doi: 10.18632/oncotarget.14744
85 Qiu J , Smith P , Leahy L , Thorley-Lawson DA . The Epstein-Barr virus encoded BART miRNAs potentiate tumor growth in vivo[J]. PLoS Pathog, 2015, 11 (1): e1004561.
doi: 10.1371/journal.ppat.1004561
86 Hooykaas MJG , Van Gent M , Soppe JA , et al. EBV microRNA BART16 suppresses type I IFN signaling[J]. J Immunol, 2017, 198 (10): 4062- 4073.
doi: 10.4049/jimmunol.1501605
87 Lung RW , Tong JH , To KF . Emerging roles of small Epstein-Barr virus derived non-coding RNAs in epithelial malignancy[J]. Int J Mol Sci, 2013, 14 (9): 17378- 17409.
doi: 10.3390/ijms140917378
88 Kim DN , Seo MK , Choi H , et al. Characterization of naturally Epstein-Barr virus-infected gastric carcinoma cell line YCCEL1[J]. J Gen Virol, 2013, 94 (Pt 3): 497- 506.
89 Qiu J , Cosmopoulos K , Pegtel M , et al. A novel persistence associated EBV miRNA expression profile is disrupted in neoplasia[J]. PLoS Pathog, 2011, 7 (8): e1002193.
doi: 10.1371/journal.ppat.1002193
90 Balatti V , Croce CM . MicroRNA dysregulation and multi-targeted therapy for cancer treatment[J]. Adv Biol Regul, 2019, 75, 100669.
doi: 10.1016/j.jbior.2019.100669
91 Wu JF , Ho MC , Ni YH , et al. Dysregulation of liver developmental microRNA contribute to hepatic carcinogenesis[J]. J Formos Med Assoc, 2019, 119 (6): 1041- 1051.
92 Iorio MV , Croce CM . MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review[J]. EMBO Mol Med, 2017, 9 (6): 852.
doi: 10.15252/emmm.201707779
93 Marquitz AR , Mathur A , Chugh PE , et al. Expression profile of microRNAs in Epstein-Barr virus-infected AGS gastric carcinoma cell[J]. J Virol, 2014, 88 (2): 1389- 1393.
doi: 10.1128/JVI.02662-13
94 Shinozaki A , Sakatani T , Ushiku T , et al. Downregulation of microRNA-200 in EBV-associated gastric carcinoma[J]. Cancer Res, 2010, 70 (11): 4719- 4727.
doi: 10.1158/0008-5472.CAN-09-4620
95 Namba-Fukuyo H , Funata S , Matsusaka K , et al. TET2 functions as a resistance factor against DNA methylation acquisition during Epstein-Barr virus infection[J]. Oncotarget, 2016, 7 (49): 81512- 81526.
doi: 10.18632/oncotarget.13130
96 Kohli RM , Zhang Y . TET enzymes, TDG and the dynamics of DNA demethylation[J]. Nature, 2013, 502 (7472): 472- 479.
doi: 10.1038/nature12750
97 Yang F , Liu Q , Hu CM . Epstein-Barr virus-encoded LMP1 increases miR-155 expression, which promotes radioresistance of nasopharyngeal carcinoma via suppressing UBQLN1[J]. Eur Rev Med Pharmacol Sci, 2015, 19 (23): 4507- 4515.
98 Du ZM , Hu LF , Wang HY , et al. Upregulation of MiR-155 in nasopharyngeal carcinoma is partly driven by LMP1 and LMP2A and downregulates a negative prognostic marker JMJD1A[J]. PLoS One, 2011, 6 (4): e19137.
doi: 10.1371/journal.pone.0019137
99 Yin Q , Wang X , Roberts C , et al. Methylation status and AP1 elements are involved in EBV-mediated miR-155 expression in EBV positive lymphoma cells[J]. Virology, 2016, 494, 158- 167.
doi: 10.1016/j.virol.2016.04.005
100 Shi Q , Zhang Y , Liu W , et al. Latent membrane protein 2A inhibits expression level of Smad2 through regulating miR-155-5p in EBV-associated gastric cancer cell lines[J]. J Med Virol, 2019, 92 (1): 96- 106.
101 Toyota M , Ahuja N , Suzuki H , et al. Aberrant methylation in gastric cancer associated with the CpG island methylator phenotype[J]. Cancer Res, 1999, 59 (21): 5438- 5442.
102 Liang Q , Yao X , Tang S , et al. Integrative identification of Epstein-Barr virus-associated mutations and epigenetic alterations in gastric cancer[J]. Gastroenterology, 2014, 147 (6): 1350- 1362.
doi: 10.1053/j.gastro.2014.08.036
103 Zhao J , Liang Q , Cheung KF , et al. Somatostatin receptor 1, a novel EBV-associated CpG hypermethylated gene, contributes to the pathogenesis of EBV-associated gastric cancer[J]. Br J Cancer, 2013, 108 (12): 2557- 2564.
doi: 10.1038/bjc.2013.263
104 Ushiku T , Chong JM , Uozaki H , et al. p73 gene promoter methylation in Epstein-Barr virus-associated gastric carcinoma[J]. Int J Cancer, 2007, 120 (1): 60- 66.
doi: 10.1002/ijc.22275
105 Geddert H , Zur Hausen A , Gabbert HE , et al. EBV-infection in cardiac and non-cardiac gastric adenocarcinomas is associated with promoter methylation of p16, p14 and APC, but not hMLH1[J]. Cell Oncol. (Dordr), 2010, 33 (3): 209- 214.
106 Sudo M , Chong JM , Sakuma K , et al. Promoter hypermethylation of E-cadherin and its abnormal expression in Epstein-Barr virus-associated gastric carcinoma[J]. Int J Cancer, 2004, 109 (2): 194- 199.
doi: 10.1002/ijc.11701
107 Chang MS , Uozaki H , Chong JM , et al. CpG island methylation status in gastric carcinoma with and without infection of Epstein-Barr virus[J]. Clin Cancer Res, 2006, 12 (10): 2995- 3002.
doi: 10.1158/1078-0432.CCR-05-1601
108 Kosari-Monfared M , Nikbakhsh N , Fattahi S , et al. CTNNBIP1 downregulation is associated with tumor grade and viral infections in gastric adenocarcinoma[J]. J Cell Physiol, 2019, 234 (3): 2895- 2904.
doi: 10.1002/jcp.27106
109 Yu J , Liang Q , Wang J , et al. REC8 functions as a tumor suppressor and I epigenetically downregulated in gastric cancer, especially in EBV-positive subtype[J]. Oncogene, 2017, 36 (2): 182- 193.
doi: 10.1038/onc.2016.187
110 Saito M , Nishikawa J , Okada T , et al. Role of DNA methylation in the development of Epstein-Barr virus-associated gastric carcinoma[J]. J Med Virol, 2013, 85 (1): 121- 127.
doi: 10.1002/jmv.23405
111 Shi J , Zhang G , Yao D , et al. Prognostic significance of aberrant gene methylation in gastric cancer[J]. Am J Cancer Res, 2012, 2 (1): 116- 129.
112 He D , Zhang YW , Zhang NN , et al. Aberrant gene promoter methylation of p16, FHIT, CRBP1, WWOX, and DLC-1 in Epstein-Barr virus-associated gastric carcinomas[J]. Med Oncol, 2015, 32 (4): 92.
doi: 10.1007/s12032-015-0525-y
113 Yang P , Wang Y , Chen J , et al. RCOR2 is a subunit of the LSD1 complex that regulates ESC property and substitutes for SOX2 in reprogramming somatic cells to pluripotency[J]. Stem Cells, 2011, 29 (5): 791- 801.
doi: 10.1002/stem.634
114 Ghadami E , Nikbakhsh N , Fattahi S , et al. Epigenetic alterations of CYLD promoter modulate its expression in gastric adenocarcinoma: a footprint of infections[J]. J Cell Physiol, 2019, 234 (4): 4115- 4124.
doi: 10.1002/jcp.27220
115 Pandey S , Jha HC , Shukla SK , et al. Epigenetic regulation of tumor suppressors by Helicobacter pylori enhances EBV-induced proliferation of gastric epithelial cells[J]. mBio, 2018, 9 (2): e00649- 18.
doi: 10.1128/mBio.00649-18
116 Lam WKJ , Jiang P , Chan KCA , et al. Methylation analysis of plasma DNA informs etiologies of Epstein-Barr virus-associated diseases[J]. Nat Commun, 2019, 10 (1): 3256.
doi: 10.1038/s41467-019-11226-5
117 Deng X , Su R , Weng H , et al. RNA N (6)-methyladenosine modification in cancers: current status and perspectives[J]. Cell Res, 2018, 28 (5): 507- 517.
doi: 10.1038/s41422-018-0034-6
118 Lang F , Singh RK , Pei Y , et al. EBV epitranscriptome reprogramming by METTL14 is critical for viral-associated tumorigenesis[J]. PLoS Pathog, 2019, 15 (6): e1007796.
doi: 10.1371/journal.ppat.1007796
119 Sasaki S , Nishikawa J , Sakai K , et al. EBV-associated gastric cancer evades T -cell immunity by PD-1/PD-L1 interactions[J]. Gastric Cancer, 2019, 22 (3): 486- 496.
doi: 10.1007/s10120-018-0880-4
120 Yau TO , T ang CM , Yu J . Epigenetic dysregulation in Epstein-Barr virus-associated gastric carcinoma: disease and treatments[J]. World J Gastroenterol, 2014, 20 (21): 6448- 6456.
doi: 10.3748/wjg.v20.i21.6448
121 Hui KF , Cheung AK , Choi CK , et al. Inhibition of class I histone deacetylases by romidepsin potently induces Epstein-Barr virus lytic cycle and mediates enhanced cell death with ganciclovir[J]. Int J Cancer, 2016, 138 (1): 125- 136.
doi: 10.1002/ijc.29698
122 Hudler P . Outlook on epigenetic therapeutic approaches for treatment of gastric cancer[J]. Curr Cancer Drug Targets, 2018, 18 (1): 65- 88.
123 Nebbioso A , Carafa V , Benedetti R , et al. Trials with 'epigenetic' drugs: an update[J]. Mol Oncol, 2012, 6 (6): 657- 682.
doi: 10.1016/j.molonc.2012.09.004
124 Naveja JJ , Medina-Franco JL . Activity landscape of DNA methyltransferase inhibitors bridges chemoinformatics with epigenetic drug discovery[J]. Expert Opin Drug Discov, 2015, 10 (10): 1059- 1070.
doi: 10.1517/17460441.2015.1073257
125 Park JK , Seo JS , Lee SK , et al. Combinatorial antitumor activity of oxaliplatin with epigenetic modifying agents, 5-Aza-CdR and FK228, in human gastric cancer cells[J]. Biomol Ther (Seoul), 2018, 26 (6): 591- 598.
doi: 10.4062/biomolther.2018.061
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