Epstein-Barr virus and gastric carcinoma: Virus-host interactions leading to carcinoma

Cancer Science

Volumn 99, Issue 9, 2008, Pages 1726-1733

  Fukayama, Masashi ^a   Hino, Rumi ^a   Uozaki, Hiroshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LATENT MEMBRANE PROTEIN 2; LATENT MEMBRANE PROTEIN 2A; SURVIVIN; VIRUS ENZYME;

APOPTOSIS; CANCER CHEMOTHERAPY; CANCER GROWTH; CELLULAR IMMUNITY; CONTROLLED STUDY; CPG ISLAND; CPG ISLAND METHYLATOR PHENOTYPE; DISEASE ASSOCIATION; DNA METHYLATION; DNA TUMOR VIRUS; EPSTEIN BARR VIRUS; GASTRIC STEM CELL; GENE EXPRESSION; GENE REPRESSION; HELICOBACTER PYLORI; HISTOPATHOLOGY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; STEM CELL; STOMACH CARCINOMA; STOMACH MUCOSA; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GENE; TUMOR SUPPRESSOR GENE; UPREGULATION; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS RESISTANCE;

EPITHELIAL CELLS; EPSTEIN-BARR VIRUS INFECTIONS; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS;

EID: 50149120544     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2008.00888.x     Document Type: Review

References (80)

1. IRC monograph on the evaluation of carcinogenic risks to humans. Schistosomes, Liver Flukes and Helicobactor Pylori. Lyon: IRC, 1994; 177-240.
2. Weinberg RA. The Biology of Cancer. New York: Garland Science, 2007; 61.
3. Correa P, Houghton J. Carcinogenesis of Helicobactor pylori. Gastroenterology 2007; 133: 659-72.
4. Hatakeyama M. Helicobacter pylori CagA - a bacterial intruder conspiring gastric carcinogenesis. Int J Cancer 2006; 119: 1217-23.
5. Imai S, Koizumi S, Sugiura M et al. Gastric carcinoma: Monoclonal epithelial malignant cells expressing Epstein-Barr virus latent infection protein. Proc Natl Acad Sci USA 1994; 91: 9131-5.
6. Fukayama M, Hayashi Y, Iwasaki Y et al. Epstein-Barr virus-associated gastric carcinoma and Epstein-Barr virus infection of the stomach. Laboratory Invest 1994; 71: 73-81.
7. Uozaki H, Fukayama M. Epstein-Barr virus associated gastric carcinoma-viral carcinogenesis through epigenetic mechanisms. Int J Clin Exp Pathol 2008; 1: 198-216.
8. Epstein MA, Barr YM, Achong BG. Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet 1964; 15: 702-3.
9. Young LS, Rickinson AB. Epstein-Barr virus: 40 years on. Nat Rev Cancer 2004; 4: 757-68.
10. Kutok JL, Wang F. Spectrum of Epstein-Barr virus-associated diseases. Annu Rev Pathol Mech Dis 2006; 1: 375-404.
11. Fukayama M, Ibuka T, Hayashi Y, Ooba T, Koike M, Mizutani S. Epstein-Barr virus in pyothorax-associated pleural lymphoma. Am J Pathol 1993; 143: 1044-9.
12. Akiba S, Koriyama C, Herrera-Goepfert R, Eizuru Y. Epstein-Barr virus associated gastric carcinoma: Epidemiological and clinicopathological features. Cancer Sci 2008; 99: 195-201.
13. Watanabe H, Enjoji M, Imai T. Gastric carcinoma with lymphoid stroma. Its morphologic characteristics and prognostic correlations. Cancer 1976; 38: 232-43.
14. Nakamura S, Ueki T, Yao T, Ueyama T, Tsuneyoshi M. Epstein-Barr virus in gastric carcinoma with lymphoid stroma. Special reference to its detection by the polymerase chain reaction and in situ hybridization in 99 tumors, including a morphologic analysis. Cancer 1994; 73: 2239-49.
15. Matsunou H, Konishi F, Hori H et al. Characteristics of Epstein-Barr virus-associated gastric carcinoma with lymphoid stroma in Japan. Cancer 1996; 77: 1998-2004.
16. Tokunaga M, Land CE, Uemura Y, Tokudome T, Tanaka S, Sato E. Epstein-Barr virus in gastric carcinoma. Am J Pathol 1993; 143: 1250-4.
17. Arikawa J, Tokunaga M, Satoh E, Tanaka S, Land CE. Morphological characteristics of Epstein-Barr virus-related early gastric carcinoma: A case-control study. Pathol Int 1997; 47: 360-7.
18. Uozaki H, Chong JM, Fujimoto E et al. Soft and hard keratin expression in Epstein-Barr-virus-associated gastric carcinoma. Anticancer Res 2005; 25: 3183-90.
19. Barua RR, Uozaki H, Chong JM et al. Phenotype analysis by MUC2, MUC5AC, MUC6, and CD10 expression in Epstein-Barr virus-associated gastric carcinoma. J Gastroenterol 2006; 41: 733-9.
20. Shimizu N, Tanabe-Tochikura A, Kuroiwa Y, Takada K. Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBV-positive Burkitt's lymphoma (BL) line Akata. J Virol 1994; 68: 6069-73.
21. Hino R, Uozaki H, Inoue Y et al. Survival advantage of EBV-associated gastric carcinoma: Survivin up-regulation by viral latent membrane protein 2A. Cancer Res 2008; 68: 1427-35.
22. Imai S, Nishikawa J, Takada K. Cell-to-cell contact as an efficient mode of Epstein-Barr virus infection of diverse human epithelial cells. J Virol 1998; 72: 4371-8.
23. Ohfuji S, Osaki M, Tsujitani S, Ikeguchi M, Sairenji T, Ito H. Low frequency of apoptosis in Epstein-Barr virus-associated gastric carcinoma with lymphoid stroma. Int J Cancer 1996; 68: 710-15.
24. Brinkmann MM, Schuz TF. Regulation of intracellular signaling by terminal membrane proteins of members of the. Gammaherpesvirinae J General Virol 2006; 87: 1047-74.
25. Longan L, Longnecker R. Epstein-Barr virus latent membrane protein 2A has no growth-altering effects when expressed in differentiating epithelia. J General Virol 2000; 81: 2245-52.
26. Scholle F, Bendt KM, Raab Traub N. Epstein-Barr virus LMP2A transforms epithelial cells, inhibits cell differentiation, and activates Akt. J Virol 2000; 74: 10681-9.
27. Morrison JA, Klingelhutz AJ, Raab Traub N. Epstein-Barr virus latent membrane protein 2A activates beta-catenin signaling in epithelial cells. J Virol 2003; 77: 12276-84.
28. Fukuda M, Longnecker R. Latent membrane protein 2A inhibits transforming growth factor-beta 1-induced apoptosis through the phosphatidylinositol 3-kinase/Akt pathway. J Virol 2004; 78: 1697-705.
29. Fukuda M, Longnecker R. Epstein-Barr virus latent membrane protein 2A mediates transformation through constitutive activation of the Ras/PI3-K/ Akt Pathway. J Virol 2007; 81: 9299-306.
30. Jo H, Zhang R, Zhang H et al. NF-κB is required for H- ras oncogene induced abnormal cell proliferation and tumorigenesis. Oncogene 2000; 19: 841-9.
31. Anderson LJ, Longnecker R. An auto-regulatory loop for EBV LMP2A involves activation of Notch. Virology 2008; 371: 257-66.
32. zur Hausen A, van Grieken NC, Meijer GA et al. Distinct chromosomal aberrations in Epstein-Barr virus-carrying gastric carcinomas tested by comparative genomic hybridization. Gastroenterology 2001; 121: 612-18.
33. Chan WY, Liu Y, Li CY et al. Recurrent genomic aberrations in gastric carcinomas associated with Helicobacter pylori and Epstein-Barr virus. Diagn Mol Pathol 2002; 11: 127-34.
34. Chong JM, Fukayama M, Hayashi Y et al. Microsatellite instability in the progression of gastric carcinoma. Cancer Res 1994; 54: 4595-7.
35. van Rees BP, Caspers E, zur Hausen A et al. Different pattern of allelic loss in Epstein-Barr virus-positive gastric cancer with emphasis on the p53 tumor suppressor pathway. Am J Pathol 2002; 161: 1207-13.
36. Chang MS, Lee HS, Kim HS et al. Epstein-Barr virus and microsatellite instability in gastric carcinogenesis. J Pathol 2003; 199: 447-52.
37. Ushiku T, Chong JM, Uozaki H et al. p73 gene promoter methylation in Epstein-Barr virus-associated gastric carcinoma. Int J Cancer 2007; 120: 60-6.
38. Kusano M, Toyota M, Suzuki H et al. Genetic, epigenetic, and clinicopathologic features of gastric carcinomas with the CpG island methylator phenotype and an association with Epstein-Barr virus. Cancer 2006; 106: 1467-79.
39. 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. Am J Pathol 2002; 160: 787-94.
40. Chang MS, Uozaki H, Chong JM et al. CpG island methylation status in gastric carcinoma with and without infection of Epstein-Barr virus. Clin Cancer Res 2006; 12: 2995-3002.
41. Enomoto S, Maekita T, Tsukamoto T et al. Lack of association between CpG island methylator phenotype in human gastric cancers and methylation in their background non-cancerous gastric mucosae. Cancer Sci 2007; 98: 1853-61.
42. Chong JM, Sakuma K, Sudo M et al. Global and non-random CpG-island methylation in gastric carcinoma associated with Epstein-Barr virus. Cancer Sci 2003; 94: 76-80.
43. Kang GH, Lee S, Cho NY et al. DNA methylation profiles of gastric carcinoma characterized by quantitative DNA methylation analysis. Lab Invest 2008; 88: 161-70.
44. Esteller M. Epigenetics in cancer. N Engl J Med 2008; 358: 1148-59.
45. Toyota M, Ahuja N, Ohe Toyota M, Herman JG, Baylin SB, Issa JP. CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 1999; 96: 8681-6.
46. Kaneda A, Kaminishi M, Yanagihara K, Sugimura T, Ushijima T. Identification of silencing of nine genes in human gastric cancers. Cancer Res 2002; 62: 6645-50.
47. Osawa T, Chong JM, Sudo M et al. Reduced expression and promoter methylation of p16 gene in Epstein-Barr virus-associated gastric carcinoma. Jap J Cancer Res 2002; 93: 1195-200.
48. Sudo M, Chong JM, Sakuma K et al. Promoter hypermethylation of E-cadherin and its abnormal expression in Epstein-Barr virus-associated gastric carcinoma. Int J Cancer 2004; 109: 194-9.
49. Sakuma K, Chong JM, Sudo M et al. High-density methylation of p14ARF and p16INK4A in Epstein-Barr virus-associated gastric carcinoma. Int J Cancer 2004; 112: 273-8.
50. Tao Q, Chan AT. Nasopharyngeal carcinoma: Molecular pathogenesis and therapeutic developments. Expert Rev Mol Med 2007; 9: 1-24.
51. Siu LL, Chan JK, Wong KF, Kwong YL. Specific patterns of gene methylation in natural killer cell lymphomas: P73 is consistently involved. Am J Pathol 2002; 160: 59-66.
52. Dutton A, Woodman CB, Chukwuma MB et al. Bmi-1 is induced by the Epstein-Barr virus oncogene LMP1 and regulates the expression of viral target genes in Hodgkin lymphoma cells. Blood 2007; 109: 2597-603.
53. Flanagan JM. Host epigenic modifications by oncogenic viruses. Br J Cancer 2007; 96: 183-8.
54. Kanai Y, Hirohashi S. Alterations of DNA methylation associated with abnormalities of DNA methyltransferases in human cancers during transition from a precancerous to a malignant state. Carcinogenesis 2007; 28: 2434-42.
55. Burgers WA, Blanchon L, Pradhan S, de Launoit Y, Kouzarides T, Fuks F. Viral oncoproteins target the DNA methyltransferases. Oncogene 2007; 26: 1650-5.
56. Jung JK, Arora P, Pagano JS, Jang KL. Expression of DNA methyltransferase 1 is activated by hepatitis B virus X protein via a regulatory circuit involving the p16INK4a-cyclin D1-CDK 4/6-pRb-E2F1 pathway. Cancer Res 2007; 67: 5771-8.
57. Tsai CL, Li HP, Lu YJ et al. Activation of DNA methyltransferase 1 by EBV LMP1 Involves c-Jun NH 2-terminal kinase signaling. Cancer Res 2006; 66: 11668-76.
58. Etoh T, Kanai Y, Ushijima S et al. Increased DNA methyltransferase 1 (DNMT1) protein expression correlates significantly with poorer tumor differentiation and frequent DNA hypermethylation of multiple CpG islands in gastric cancers. Am J Pathol 2004; 164: 689-99.
59. Li H, Minarovits J. Host cell-dependent expression of latent Epstein-Barr virus genomes: Regulation by DNA methylation. Adv Cancer Res 2003; 89: 133-56.
60. Lieberman PM. Chromatin organization and virus gene expression. J Cell Physiol 2008; 216: 295-302.
61. Chen X, Leung SY, Yuen ST et al. Variation in gene expression patterns in human gastric cancers. Mol Biol Cell 2003; 14: 3208-15.
62. Iwasaki Y, Chong JM, Hayashi Y et al. Establishment and characterization of a human Epstein-Barr virus-associated gastric carcinoma in SCID mice. J Virol 1998; 72: 8321-6.
63. Chong JM, Sakuma K, Sudo M et al. Interleukin-1beta expression in human gastric carcinoma with Epstein-Barr virus infection. J Virol 2002; 76: 6825-31.
64. El-Omar EM, Carrington M, Chow WH et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 2000; 404: 398-402. [Erratum in: Nature 2001; 412: 99].
65. Lee HS, Chang MS, Yang HK, Lee BL, Kim WH. Epstein-Barr virus-positive gastric carcinoma has a distinct protein expression profile in comparison with Epstein-Barr virus-negative carcinoma. Clin Cancer Res 2004; 10: 1698-705.
66. Chong JM, Fukayama M, Hayashi Y et al. Expression of CD44 variants in gastric carcinoma with or without Epstein-Barr virus. Int J Cancer 1997; 74: 450-4.
67. Iwakiri D, Eizuru Y, Tokunaga M, Takada K. Autocrine growth of Epstein-Barr virus-positive gastric carcinoma cells mediated by an Epstein-Barr virus-encoded small RNA. Cancer Res 2003; 63: 7062-7.
68. zur Hausen A, Brink AA, Craanen ME, Middeldorp JM, Meijer CJ, van den Brule AJ. Unique transcription pattern of Epstein-Barr virus (EBV) in EBV-carrying gastric adenocarcinomas: Expression of the transforming BARF1 gene. Cancer Res 2000; 60: 2745-8.
69. Seto E, Yang L, Middeldorp J et al. Epstein-Barr virus (EBV)-encoded BARF1 gene is expressed in nasopharyngeal carcinoma and EBV-associated gastric carcinoma tissues in the absence of lytic gene expression. J Med Virol 2005; 76: 82-8.
70. Kim DN, Chae HS, Oh ST et al. Expression of viral microRNAs in Epstein-Barr virus-associated gastric carcinoma. J Virol 2007; 81: 1033-6.
71. Borza CM, Hutt Fletcher LM. Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat Med 2002; 8: 594-9.
72. Au WY, Pang A, Chan EC, Chu KM, Shek TW, Kwong YL. Epstein-Barr virus-related gastric adenocarcinoma: An early secondary cancer post hemopoietic stem cell transplantation. Gastroenterology 2005; 129: 2058-63.
73. Duelli D, Lazebnik Y. Cell-to-cell fusion as a link between viruses and cancer. Nat Rev Cancer 2007; 7: 968-76.
74. Kaizaki Y, Sakurai S, Chong JM, Fukayama M. Atrophic gastritis, Epstein-Barr virus infection, and Epstein-Barr virus-associated gastric carcinoma. Gastric Cancer 1999; 2: 101-8.
75. Kaizaki Y, Hosokawa O, Sakurai S, Fukayama M. Epstein-Barr virus-associated gastric carcinoma in the remnant stomach: De novo and metachronous gastric remnant carcinoma. J Gastroenterol 2005; 40: 570-7.
76. Ushijima T. Epigenetic field for cancerization. J Biochem Mol Biol 2007; 40: 142-50.
77. Feinberg AP, Ohlsson R, Henikoff S. The epigenetic progenitor origin of human cancer. Nat Rev Genet 2006; 7: 21-33.
78. Ohnishi N, Yuasa H, Tanaka S et al. Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci USA 2008; 105: 1003-8.
79. Sakuma K, Uozaki H, Chong JM et al. Cancer risk to the gastric corpus in Japanese, its correlation with interleukin-1beta gene polymorphism (+ 3953*T) and Epstein-Barr virus infection. Int J Cancer 2005; 115: 93-7.
80. Fu DX, Tanhehco YC, Chen J et al. Bortezomib-induced enzyme-targeted radiotherapy in herpesvirus-associated tumors. Nat Med in press.