Integrative identification of Epstein-Barr virus-associated mutations and epigenetic alterations in gastric cancer

Gastroenterology

Volumn 147, Issue 6, 2014, Pages 1350-1362.e4

  Liang, Qiaoyi ^a   Yao, Xiaotian ^b   Tang, Senwei ^b   Zhang, Jingwan ^a   Yau, Tung On ^a   Li, Xiaoxing ^a   Tang, Ceen Ming ^c   Kang, Wei ^a   Lung, Raymond W M ^a   Li, Jing Woei ^a   Chan, Ting Fung ^a   Xing, Rui ^d   Lu, Youyong ^d   Lo, Kwok Wai ^a   Wong, Nathalie ^a   To, Ka Fai ^a   Yu, Chang ^b   Chan, Francis K L ^a   Sung, Joseph J Y ^a   Yu, Jun ^a,e  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b BGI SHENZHEN   (China)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d PEKING UNIVERSITY CANCER HOSPITAL AND INSTITUTE   (China)

^e CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

AKT2; Genome Sequencing; Methylation; Transcriptome

Indexed keywords

EPSTEIN BARR VIRUS ANTIGEN 1; IMMEDIATE EARLY PROTEIN BZLF1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B BETA; SONIC HEDGEHOG PROTEIN; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; AKT2 PROTEIN, HUMAN; CCNA1 PROTEIN, HUMAN; CYCLIN A1; MAP3K4 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 4; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; TGF-BETA TYPE I RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ACSS1 GENE; ACTIN FILAMENT; ARTICLE; BARF0 GENE; BARF1 GENE; BCLF1 GENE; BFRF1A GENE; BFRF2 GENE; BFRF3 GENE; BHRF1 GENE; BKRF3 GENE; BKRF4 GENE; BLLF1 GENE; BMRF1 GENE; BMRF2 GENE; BNLF2A GENE; BNLF2B GENE; BRLF1 GENE; BZLF1 GENE; CANCER CELL; CANCER PATIENT; CANCER SURVIVAL; CCNA1 GENE; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; EPSTEIN BARR VIRUS ANTIGEN 1 GENE; EPSTEIN BARR VIRUS INFECTION; FAM3B GENE; FOCAL ADHESION; GASTRIC CANCER CELL LINE; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LMP2A GENE; MAJOR CLINICAL STUDY; MAP3K4 GENE; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PRIMARY TUMOR; PROMOTER REGION; PROTEIN KINASE B BETA GENE; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SONIC HEDGEHOG GENE; STOMACH ADENOCARCINOMA; STOMACH CANCER; STOMACH CARCINOGENESIS; SURVIVAL RATE; SURVIVAL TIME; TRAB DOMAIN CONTAINING GENE; TRANSCRIPTION REGULATION; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1 GENE; TUMOR GENE; VIRUS GENE; ADENOCARCINOMA; EPSTEIN BARR VIRUS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; STOMACH TUMOR; TUMOR CELL LINE; VIROLOGY;

ADENOCARCINOMA; CELL LINE, TUMOR; CYCLIN A1; DNA METHYLATION; EPIGENESIS, GENETIC; EPSTEIN-BARR VIRUS INFECTIONS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE EXPRESSION REGULATION, VIRAL; GENES, VIRAL; GENOME-WIDE ASSOCIATION STUDY; HERPESVIRUS 4, HUMAN; HUMANS; MAP KINASE KINASE KINASE 4; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; STOMACH NEOPLASMS; TRANSCRIPTOME;

EID: 84913534546     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.08.036     Document Type: Article

References (50)

1. J. Zhao, H. Jin, and K.F. Cheung Zinc finger E-box binding factor 1 plays a central role in regulating Epstein-Barr virus (EBV) latent-lytic switch and acts as a therapeutic target in EBV-associated gastric cancer Cancer 118 2012 924 936
2. M. Fukayama, R. Hino, and H. Uozaki Epstein-Barr virus and gastric carcinoma: virus-host interactions leading to carcinoma Cancer Sci 99 2008 1726 1733
3. J. Zhao, Q. Liang, and K.F. Cheung Genome-wide identification of Epstein-Barr virus-driven promoter methylation profiles of human genes in gastric cancer cells Cancer 119 2013 304 312
4. R. Hino, H. Uozaki, and N. Murakami Activation of DNA methyltransferase 1 by EBV latent membrane protein 2A leads to promoter hypermethylation of PTEN gene in gastric carcinoma Cancer Res 69 2009 2766 2774
5. K. Wang, J. Kan, and S.T. Yuen Exome sequencing identifies frequent mutation of ARID1A in molecular subtypes of gastric cancer Nat Genet 43 2011 1219 1223
6. M.S. Chang, H.S. Lee, and H.S. Kim Epstein-Barr virus and microsatellite instability in gastric carcinogenesis J Pathol 199 2003 447 452
7. W.Y. Chan, Y. Liu, and C.Y. Li Recurrent genomic aberrations in gastric carcinomas associated with Helicobacter pylori and Epstein-Barr virus Diagn Mol Pathol 11 2002 127 134
8. J. Zhao, Q. Liang, and K.F. Cheung Somatostatin receptor 1, a novel EBV-associated CpG hypermethylated gene, contributes to the pathogenesis of EBV-associated gastric cancer Br J Cancer 108 2013 2557 2564
9. J.L. Ryan, R.J. Jones, and S.C. Kenney Epstein-Barr virus-specific methylation of human genes in gastric cancer cells Infect Agent Cancer 5 2010 27
10. A.R. Marquitz, A. Mathur, and K.H. Shair Infection of Epstein-Barr virus in a gastric carcinoma cell line induces anchorage independence and global changes in gene expression Proc Natl Acad Sci U S A 109 2012 9593 9598
11. C. Shannon-Lowe, E. Adland, and A.I. Bell Features distinguishing Epstein-Barr virus infections of epithelial cells and B cells: viral genome expression, genome maintenance, and genome amplification J Virol 83 2009 7749 7760
12. Z. Lin, G. Xu, and N. Deng Quantitative and qualitative RNA-Seq-based evaluation of Epstein-Barr virus transcription in type I latency Burkitt's lymphoma cells J Virol 84 2010 13053 13058
13. C.W. Dawson, J. Dawson, and R. Jones Functional differences between BHRF1, the Epstein-Barr virus-encoded Bcl-2 homologue, and Bcl-2 in human epithelial cells J Virol 72 1998 9016 9024
14. B. Luo, Y. Wang, and X.F. Wang Correlation of Epstein-Barr virus and its encoded proteins with Helicobacter pylori and expression of c-met and c-myc in gastric carcinoma World J Gastroenterol 12 2006 1842 1848
15. P.J. Stephens, P.S. Tarpey, and H. Davies The landscape of cancer genes and mutational processes in breast cancer Nature 486 2012 400 404
16. Y.H. Soung, J.W. Lee, and S.W. Nam Mutational analysis of AKT1, AKT2 and AKT3 genes in common human carcinomas Oncology 70 2006 285 289
17. P. Yanatatsaneejit, T. Chalermchai, and V. Kerekhanjanarong Promoter hypermethylation of CCNA1, RARRES1, and HRASLS3 in nasopharyngeal carcinoma Oral Oncol 44 2008 400 406
18. M.A. Sartor, D.C. Dolinoy, and T.R. Jones Genome-wide methylation and expression differences in HPV(+) and HPV(-) squamous cell carcinoma cell lines are consistent with divergent mechanisms of carcinogenesis Epigenetics 6 2011 777 787
19. B. Wegiel, A. Bjartell, and J. Tuomela Multiple cellular mechanisms related to cyclin A1 in prostate cancer invasion and metastasis J Natl Cancer Inst 100 2008 1022 1036
20. R.D. Coletta, K. Christensen, and K.J. Reichenberger The Six1 homeoprotein stimulates tumorigenesis by reactivation of cyclin A1 Proc Natl Acad Sci U S A 101 2004 6478 6483
21. J.P. Arnault, C. Mateus, and B. Escudier Skin tumors induced by sorafenib; paradoxic RAS-RAF pathway activation and oncogenic mutations of HRAS, TP53, and TGFBR1 Clin Cancer Res 18 2012 263 272
22. L.G. Carvajal-Carmona, M. Churchman, and C. Bonilla Comprehensive assessment of variation at the transforming growth factor beta type 1 receptor locus and colorectal cancer predisposition Proc Natl Acad Sci U S A 107 2010 7858 7862
23. M. Takekawa, F. Posas, and H. Saito A human homolog of the yeast Ssk2/Ssk22 MAP kinase kinase kinases, MTK1, mediates stress-induced activation of the p38 and JNK pathways EMBO J 16 1997 4973 4982
24. M. Le Gallo, A.J. O'Hara, and M.L. Rudd Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes Nat Genet 44 2012 1310 1315
25. G. Xu, H. Zhou, and Q. Wang Activin receptor-like kinase 7 induces apoptosis through up-regulation of Bax and down-regulation of Xiap in normal and malignant ovarian epithelial cell lines Mol Cancer Res 4 2006 235 246
26. S.K. Shukla, K.N. Prasad, and A. Tripathi Expression profile of latent and lytic transcripts of Epstein-Barr virus in patients with gastroduodenal diseases: a study from northern India J Med Virol 84 2012 1289 1297
27. Y. Hoshikawa, Y. Satoh, and M. Murakami Evidence of lytic infection of Epstein-Barr virus (EBV) in EBV-positive gastric carcinoma J Med Virol 66 2002 351 359
28. J. Qiu, K. Cosmopoulos, and M. Pegtel A novel persistence associated EBV miRNA expression profile is disrupted in neoplasia PLoS Pathog 7 2011 e1002193
29. A. zur Hausen, A.A. Brink, and M.E. Craanen Unique transcription pattern of Epstein-Barr virus (EBV) in EBV-carrying gastric adenocarcinomas: expression of the transforming BARF1 gene Cancer Res 60 2000 2745 2748
30. N. Kim do, H.S. Chae, and S.T. Oh Expression of viral microRNAs in Epstein-Barr virus-associated gastric carcinoma J Virol 81 2007 1033 1036
31. R. Hino, H. Uozaki, and Y. Inoue Survival advantage of EBV-associated gastric carcinoma: survivin up-regulation by viral latent membrane protein 2A Cancer Res 68 2008 1427 1435
32. L.S. Chang, J.T. Wang, and S.L. Doong Epstein-Barr virus BGLF4 kinase downregulates NF-kappaB transactivation through phosphorylation of coactivator UXT J Virol 86 2012 12176 12186
33. T. Ushiku, J.M. Chong, and H. Uozaki p73 gene promoter methylation in Epstein-Barr virus-associated gastric carcinoma Int J Cancer 120 2007 60 66
34. H. Geddert, A. Zur Hausen, and H.E. Gabbert EBV-infection in cardiac and non-cardiac gastric adenocarcinomas is associated with promoter methylation of p16, p14 and APC, but not hMLH1 Cell Oncol (Dordr) 34 2011 209 214
35. M. Sudo, J.M. Chong, and K. Sakuma Promoter hypermethylation of E-cadherin and its abnormal expression in Epstein-Barr virus-associated gastric carcinoma Int J Cancer 109 2004 194 199
36. J. Kassis, A. Maeda, and N. Teramoto EBV-expressing AGS gastric carcinoma cell sublines present increased motility and invasiveness Int J Cancer 99 2002 644 651
37. B. Zhao, J.C. Mar, and S. Maruo Epstein-Barr virus nuclear antigen 3C regulated genes in lymphoblastoid cell lines Proc Natl Acad Sci U S A 108 2011 337 342
38. A.M. Price, J.P. Tourigny, and E. Forte Analysis of Epstein-Barr virus-regulated host gene expression changes through primary B-cell outgrowth reveals delayed kinetics of latent membrane protein 1-mediated NF-kappaB activation J Virol 86 2012 11096 11106
39. H.J. Delecluse, T. Hilsendegen, and D. Pich Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells Proc Natl Acad Sci U S A 95 1998 8245 8250
40. W.H. Feng, R.J. Kraus, and S.J. Dickerson ZEB1 and c-Jun levels contribute to the establishment of highly lytic Epstein-Barr virus infection in gastric AGS cells J Virol 81 2007 10113 10122
41. A. Mortazavi, B.A. Williams, and K. McCue Mapping and quantifying mammalian transcriptomes by RNA-Seq Nat Methods 5 2008 621 628
42. H. Li, and R. Durbin Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 25 2009 1754 1760
43. H. Li, B. Handsaker, and A. Wysoker The Sequence Alignment/Map format and SAMtools Bioinformatics 25 2009 2078 2079
44. G.R. Abecasis, A. Auton, and L.D. Brooks An integrated map of genetic variation from 1,092 human genomes Nature 491 2012 56 65
45. A. McKenna, M. Hanna, and E. Banks The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data Genome Res 20 2010 1297 1303
46. K. Wang, M. Li, and H. Hakonarson ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data Nucleic Acids Res 38 2010 e164
47. J. Wang, C.G. Mullighan, and J. Easton CREST maps somatic structural variation in cancer genomes with base-pair resolution Nat Methods 8 2011 652 654
48. S. Audic, and J.M. Claverie The significance of digital gene expression profiles Genome Res 7 1997 986 995
49. J. Zhao, Q. Liang, and K.F. Cheung Genome-wide identification of Epstein-Barr virus-driven promoter methylation profiles of human genes in gastric cancer cells Cancer 119 2013 304 312
50. N. Kim do, M.K. Seo, and H. Choi Characterization of naturally Epstein-Barr virus-infected gastric carcinoma cell line YCCEL1 J Gen Virol 94 2013 497 506