Modulation of innate immunity system by Epstein-Barr virus-encoded non-coding RNA and oncogenesis

Cancer Science

Volumn 101, Issue 1, 2010, Pages 29-35

  Samanta, Mrinal ^a   Takada, Kenzo ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; EPSTEIN BARR VIRUS ENCODED SMALL RNA 1; EPSTEIN BARR VIRUS ENCODED SMALL RNA 2; EPSTEIN BARR VIRUS UNTRANSLATED RNA; FAS LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 1; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON STIMULATED GENE FACTOR 3; INTERLEUKIN 10; INTERLEUKIN 6; LA ANTIGEN; LATENT MEMBRANE PROTEIN 1; PROTEIN BCL 2; PROTEIN KINASE R; RECOMBINANT INTERLEUKIN 6; RETINOIC ACID INDUCIBLE PROTEIN I; RIBOSOME PROTEIN; RIBOSOME PROTEIN L22; SOMATOMEDIN C; TATA BINDING PROTEIN; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

APOPTOSIS; AUTOCRINE EFFECT; B LYMPHOCYTE; BURKITT LYMPHOMA; CARCINOGENESIS; CELL PROLIFERATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EPSTEIN BARR VIRUS; GENE EXPRESSION; HUMAN; IMMUNOMODULATION; INNATE IMMUNITY; LYMPHOBLASTOID CELL LINE; NASOPHARYNX CARCINOMA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STOMACH CARCINOMA; T LYMPHOCYTE; TRANSCRIPTION REGULATION; UPREGULATION; VIROGENESIS;

ANIMALS; APOPTOSIS; BURKITT LYMPHOMA; HUMANS; IMMUNITY, INNATE; MICE; RNA, UNTRANSLATED; RNA, VIRAL; TRANSCRIPTION, GENETIC;

EID: 71849091764     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2009.01377.x     Document Type: Review

References (72)

1. Rickinson AB, Kieff E, Knipe DM, Howley PM. Epstein-Barr virus. Fields Virology: Epstein-Barr virus 2001, 2575-628. In, eds, Vol. 2, 4th edn, Philadelphia, PA, Lippincott Williams & Wilkins
2. Kieff E, Rickinson AB, Knipe DM, Howley PM. Epstein-Barr virus and its replication. Fields Virology: Epstein-Barr virus 2001, 2511-73. In, eds, Vol. 2, 4th edn, Philadelphia, PA, Lippincott Williams & Wilkins
3. Lerner MR, Andrews NC, Miller G, Steitz JA. Two small RNAs encoded by Epstein-Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus. Proc Natl Acad Sci USA 1981, 78:805-9.
4. Howe JG, Shu MD. Epstein-Barr virus small RNA (EBER) genes: unique transcription units that combine RNA polymerase II and III promoter elements. Cell 1989, 57:825-34.
5. Arrand JR, Rymo L. Characterization of the major Epstein-Barr virus-specific RNA in Burkitt lymphoma-derived cells. J Virol 1982, 41:376-89.
6. Glickman JN, Howe JG, Steitz JA. Structural analyses of EBER1 and EBER2 ribonucleoprotein particles present in Epstein-Barr virus-infected cells. J Virol 1988, 62:902-11.
7. Arrand JR, Young LS, Tugwood JD. Two families of sequences in the small RNA-encoding region of Epstein-Barr virus (EBV) correlate with EBV types A and B. J Virol 1989, 63:983-6.
8. Kitagawa N, Goto M, Kurozumi K. Epstein-Barr virus-encoded poly(A)(-) RNA supports Burkitt's lymphoma growth through interleukin-10 induction. EMBO J 2000, 19:6742-50.
9. 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.
10. Iwakiri D, Sheen TS, Chen JY, Huang DP, Takada K. Epstein-Barr virus-encoded small RNA induces insulin-like growth factor 1 and supports growth of nasopharyngeal carcinoma-derived cell lines. Oncogene 2005, 24:1767-73.
11. Yang L, Aozasa K, Oshimi K, Takada K. Epstein-Barr virus (EBV)-encoded RNA promotes growth of EBV-infected T cells through interleukin-9 induction. Cancer Res 2004, 64:5332-7.
12. Wu Y, Maruo S, Yajima M, Kanda T, Takada K. Epstein-Barr virus (EBV)-encoded RNA 2 (EBER2) but not EBER1 plays a critical role in EBV-induced B-cell growth transformation. J Virol 2007, 80:11236-45.
13. Nanbo A, Inoue K, Adachi-Takasawa K, Takada K. Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt's lymphoma. EMBO J 2002, 21:954-65.
14. Nanbo A, Yoshiyama H, Takada K. Epstein-Barr virus-encoded poly(A)- RNA confers resistance to apoptosis mediated through Fas by blocking the PKR pathway in human epithelial intestine 407 cells. J Virol 2005, 79:12280-5.
15. Wong HL, Wang X, Chang RCC. Stable expression of EBERs in immortalized nasopharyngeal epithelial cells confers resistance to apoptotic stress. Mol Carcinog 2005, 44:92-101.
16. Komono J, Sugiura M, Takada K. Epstein-Barr virus contributes to the malignant phenotype and to apoptosis resistance in Burkitt's lymphoma cell line Akata. J Virol 1998, 72:9150-6.
17. Yajima M, Kanda T, Takada K. Critical role of Epstein-Barr Virus (EBV)-encoded RNA in efficient EBV-induced B-lymphocyte growth transformation. J Virol 2005, 79:4298-307.
18. Baer R, Bankier AT, Biggin MD. DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature 1984, 310:207-11.
19. Clemens MJ. The small RNAs of Epstein-Barr virus. Mol Biol Report 1993, 17:81-92.
20. Dumpelmann E, Mittendorf H, Benecke BJ. Efficient transcription of the EBER2 gene depends on the structural integrity of the RNA. RNA 2003, 9:432-42.
21. Minarovits J, Hu LF, Marcsek Z, Kormuta SM, Klein G, Ernberg I. RNA polymerase III-transcribed EBER 1 and 2 transcription units are expressed and hypomethylated in the major Epstein-Barr virus-carrying cell types. J Gen Virol 1992, 73:1687-92.
22. Komano J, Maruo S, Kurozumi K, Oda T, Takada K. Oncogenic role of Epstein-Barr virus-encoded RNAs in Burkitt's lymphoma cell line Akata. J Virol 1999, 73:9827-31.
23. Clarke PA, Sharp NA, Clemens MJ. Expression of genes for the Epstein-Barr virus small RNAs EBER-1 and EBER-2 in Daudi Burkitt's lymphoma cells: effects of interferon treatment. J Gen Virol 1992, 73:3169-75.
24. Rooney C, Howe JG, Speck SH, Miller G. Influence of Burkitt's lymphoma and primary B cells on latent gene expression by the nonimmortalizing P3J-HR-1 strain of Epstein-Barr virus. J Virol 1989, 63:1531-9.
25. Greifenegger N, Jager M, Schughart LAK, Wolf H, Schwarzmann F. Epstein-Barr virus small RNA (EBER) genes: differential regulation during lytic viral replication. J Virol 1998, 72:9323-8.
26. Wu TC, Mann RB, Charache P. Detection of EBV gene expression in Reed-Sternberg cells of Hodgkin's disease. Int J Cancer 1990, 46:801-4.
27. Labrecque LG, Lampert I, Kazembe P, Phillips J, Griffin BE. Correlation between cytopathological results and in situ hybridisation on needle aspiration biopsies of suspected African Burkitt's lymphomas. Int J Cancer 1994, 59:591-6.
28. Burke AP, Yen TSB, Shekitka KM, Sobin LH. Lymphoepithelial carcinoma of the stomach with Epstein-Barr virus demonstrated by polymerase chain reaction. Mod Pathol 1990, 3:377-80.
29. 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.
30. Tokunaga M, Uemara Y, Tokudome T. Epstein-Barr virus related gastric cancer in Japan: a molecular patho-epidemiological study. Acta Pathol Jpn 1993, 43:574-81.
31. Imai S, Koizumi S, Sugiura M. Gastric carcinoma: monoclonal epithelial malignant cells expressing Epstein-Barr virus latent infection protein. Proc Natl Acad Sci USA 1994, 91:9131-5.
32. 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.
33. Pathmanathan R, Prasad U, Sadler R, Flynn K, Raab-Traub N. Clonal proliferations of cells infected with Epstein-Barr virus in preinvasive lesions related to nasopharyngeal carcinoma. N Engl J Med 1995, 333:693-8.
34. Yao Y, Minter HA, Chen X, Reynolds GM, Bromley M, Arrand JR. Heterogeneity of HLA and EBER expression in Epstein-Barr virus-associated nasopharyngeal carcinoma. Int J Cancer 2000, 88:949-55.
35. Fina F, Romain S, Ouafik L. Frequency and genome load of Epstein-Barr virus in 509 breast cancers from different geographical areas. Br J Cancer 2001, 84:783-90.
36. Gilligan K, Rajadurai P, Resnick L, Raab-Traub N. Epstein-Barr virus small nuclear RNAs are not expressed in permissively infected cells in AIDS-associated leukoplakia. Proc Natl Acad Sci USA 1990, 87:8790-4.
37. Wen S, Shimizu N, Yoshiyama H, Mizugaki Y, Shinozaki F, Takada K. Association of Epstein-Barr virus (EBV) with Sjögren's syndrome: differential EBV expression between epithelial cells and lymphocytes in salivary glands. Am J Pathol 1996, 149:1511-7.
38. Wen S, Mizugaki Y, Shinozaki F, Takada K. Epstein-Barr virus (EBV) infection in salivary gland tumors: lytic EBV infection in nonmalignant epithelial cells surrounded by EBV-positive T-lymphoma cells. Virol 1997, 227:484-7.
39. Mizugaki Y, Sugawara Y, Shinozaki F, Takada K. Detection of Epstein-Barr virus in oral papilloma. Jpn J Cancer Res 1998, 89:604-7.
40. Rosa MD, Gottlieb E, Lerner MR, Steiz JA. Striking similarities are exhibited by two small Epstein-Barr virus-encoded ribonucleic acids and the adenovirus associated ribonucleic acids VAI and VAII Mol Cell Biol 1981, 1:785-96.
41. Howe JG, Shu MD. Isolation and characterization of the genes for two small RNAs of herpesvirus papio and their comparison with Epstein-Barr virus-encoded EBER RNAs. J Virol 1988, 62:2790-8.
42. Clarke PA, Schwemmle M, Schickinger J, Hilse K, Clemens MJ. Binding of Epstein-Barr virus small RNA EBER-1 to the double stranded RNA-activated protein kinase DAI. Nucleic Acids Res 1991, 19:243-8.
43. Chnag KL, Chen YY, Shibata D, Weiss LM. Description of an in situ hybridization methodology for detection of Epstein-Barr virus RNA in paraffin-embedded tissues, with a survey of normal and neoplastic tissues. Diagn Mol Pathol 1992, 1:246-55.
44. Howe JG, Steiz JA. Localization of Epstein-Barr virus-encoded small RNAs by in situ hybridization. Proc Natl Acad Sci USA 1986, 83:9006-10.
45. Schwemmle M, Clemens MJ, Hilse K. Localization of Epstein-Barr virus-encoded RNAs EBER-1 and EBER-2 in interphase and mitotic Burkitt lymphoma cells. Proc Natl Acad Sci USA 1992, 89:10292-6.
46. Barletta JM, Kingma DW, Ling Y, Charache P, Mann RB, Ambinder RF. Rapid in situ hybridization for the diagnosis of latent Epstein-Barr virus infection. Mol Cell Probes 1993, 7:105-9.
47. Rymo L. Identification of transcribed regions of Epstein-Barr virus DNA in Burkitt lymphoma-derived cells. J Virol 1979, 32:8-18.
48. Fok V, Friend K, Steiz JA. Epstein-Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nucleocytoplasmic shuttling. J Cell Biol 2006, 3:319-25.
49. Gottlieb E, Steiz JA. The RNA binding protein La influences both the accuracy and the efficiency of RNA polymerase III transcription in vitro. EMBO J 1989, 8:841-50.
50. Wolin SL, Cedervall T. The La protein. Annu Rev Biochem 2002, 71:375-403.
51. Fok V, Mitton-Fry RM, Grech A, Steitz JA. Multiple domains of EBER 1, an Epstein-Barr virus noncoding RNA, recruit human ribosomal protein L22. RNA 2006, 12:872-82.
52. Nucifora G, Begy CR, Erickson P, Drabkin HA, Rowley J D. The 3;21 translocation in myelodysplasia results in a fusion transcript between the AML 1 gene and the gene for EAP, a highly conserved protein associated with the Epstein-Barr virus small RNA EBER1. Proc Natl Acad Sci USA 1993, 90:7784-8.
53. Wood J, Frederickson RM, Fields S, Patel AH. Hepatitis C virus 3'X region interacts with human ribosomal proteins. J Virol 2001, 75:1348-58.
54. Toczyski DP, Steitz JA. EAP, a highly conserved cellular protein associated with Epstein-Barr virus small RNAs (EBERs). EMBO J 1991, 10:459-66.
55. Leopardi R, Roizman B. Functional interaction and colocalization of the herpes simplex virus 1 major regulatory protein ICP4 with EAP, a nucleolar-ribosomal protein. Proc Natl Acad Sci USA 1996, 93:4572-6.
56. Leopardi R, Ward PL, Ogle WO, Roizman B. Association of herpes simplex virus regulatory protein ICP22 with transcriptional complexes containing EAP, ICP4, RNA polymerase II, and viral DNA requires posttranslational modification by the U(L)13 proteinkinase. J Virol 1997, 71:1133-9.
57. Le S, Sternglanz R, Greider CW. Identification of two RNA-binding proteins associated with human telomerase RNA. Mol Biol Cell 2000, 11:999-1010.
58. Toczyski DP, Matera AG, Ward DC, Steitz JA. The Epstein-Barr virus (EBV) small RNA EBER1 binds and relocalizes ribosomal protein L22 in EBV-infected human B lymphocytes. Proc Natl Acad Sci USA 1994, 91:3463-7.
59. Toczyski DP, Steitz JA. The cellular RNA-binding protein EAP recognizes a conserved stem-loop in the Epstein-Barr virus small RNA EBER 1. Mol Cell Biol 1993, 13:703-10.
60. Dobbelstein M, Shenk T. In vitro selection of RNA ligands for the ribosomal L22 protein associated with Epstein-Barr virus-expressed RNA by using randomized and cDNA-derived RNA libraries. J Virol 1995, 69:8027-34.
61. Elia A, Vyas J, Laing KG, Clemens MJ. Ribosomal protein L22 inhibits regulation of cellular activities by the Epstein-Barr virus small RNA EBER-1. Eur J Biochem 2004, 271:1895-905.
62. Sharp TV, Schwemmle M, Jeffrey I. Comparative analysis of the regulation of the interferon-inducible protein kinase PKR by Epstein-Barr virus RNAs EBER-1 and EBER-2 and adenovirus VAI RNA. Nucleic Acids Res 1993, 21:4483-90.
63. Vuyisich M, Spanggord RJ, Beal PA. The binding site of the RNA-dependent protein kinase (PKR) on EBER1 RNA from Epstein-Barr virus. EMBO Rep 2002, 3:622-7.
64. Mckenna SA, Lindhout DA, Shimoike T, Aitken CE, Puglisis JD. Viral dsRNA inhibitors prevent self-association and autophosphorylation of PKR. J Mol Biol 2007, 372:103-13.
65. Yoneyama M, Kikuchi M, Natsukawa T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004, 5:730-7.
66. Samanta M, Iwakiri D, Kanda T, Imaizumi T, Takada K. EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 2006, 25:4207-14.
67. Samanta M, Iwakiri D, Takada K. Epstein-Barr virus-encoded small RNA induces IL-10 through RIG-I-mediated IRF-3 signaling. Oncogene 2008, 27:4150-60.
68. Yamamoto N, Takizawa T, Iwanaga Y, Shimizu N. Malignant transformation of B lymphoma cell line BJAB by Epstein-Barr virus-encoded small RNAs. FEBS Lett 2000, 484:153-8.
69. Ruf IK, Rhyne PW, Yang C, Cleveland JL, Sample JT. Epstein-Barr virus small RNAs potentiate tumorigenicity of Burkitt lymphoma cells independently of an effect on apoptosis. J Virol 2000, 74:10223-8.
70. Bhat RA, Thimmappaya B. Two small RNAs encoded by Epstein-Barr virus can functionally substitute for the virus-associated RNAs in the lytic growth of adenovirus 5. Proc Natl Acad Sci USA 1983, 80:4789-93.
71. Aparicio O, Razquin N, Zaratiegui M, Narvaiza I, Fortes P. Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J Virol 2006, 80:1376-84.
72. Sano M, Kato Y, Taira K. Sequence-specific interference by small RNAs derived from adenovirus VAI RNA. FEBS Lett 2006, 580:1553-64.