A role for Epstein-Barr viral BALF1 in facilitating tumor formation and metastasis potential

Virus Research

Volumn 163, Issue 2, 2012, Pages 617-627

  Hsu, Wen Li ^a   Chung, Pei Jung ^b   Tsai, Ming Hsien ^a   Chang, Cicero Lee Tian ^c   Liang, Chih Lung ^d  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^d CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

Author keywords

BALF1; EBV; Metastasis; Transformation; Tumor

Indexed keywords

BALF1 PROTEIN; COMPLEMENTARY DNA; PEPTIDES AND PROTEINS; PLASMID DNA; TUMOR MARKER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL STRUCTURE; CELL SURVIVAL; CELL TRANSFORMATION; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GENE EXPRESSION; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; MALE; METASTASIS; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR VIRUS; WESTERN BLOTTING;

ANIMALS; DISEASE MODELS, ANIMAL; HERPESVIRUS 4, HUMAN; LYMPHOMA; MALE; MICE; MICE, INBRED BALB C; NEOPLASM METASTASIS; VIRAL PROTEINS; VIRULENCE FACTORS;

HERPESVIRIDAE; HUMAN HERPESVIRUS 4; MUS;

EID: 84862828335     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2011.12.017     Document Type: Article

References (60)

1. Altmann M., Hammerschmidt W. Epstein-Barr virus provides a new paradigm: a requirement for the immediate inhibition of apoptosis. PLoS Biol. 2005, 3(12):e404.
2. Baichwal V.R., Sugden B. Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus. Oncogene 1988, 2(5):461-467.
3. Beierle E.A., Strande L.F., Chen M.K. VEGF upregulates Bcl-2 expression and is associated with decreased apoptosis in neuroblastoma cells. J. Pediatr. Surg. 2002, 37(3):467-471.
4. Bellows D.S., Howell M., Pearson C., Hazlewood S.A., Hardwick J.M. Epstein-Barr virus BALF1 is a Bcl-2-like antagonist of the herpesvirus antiapoptotic Bcl-2 proteins. J. Virol. 2002, 76(5):2469-2479.
5. Bond M., Fabunmi R.P., Baker A.H., Newby A.C. Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-kappa B. FEBS Lett. 1998, 435(1):29-34.
6. Brun A., Rivas C., Esteban M., Escribano J.M., Alonso C. African swine fever virus gene A179L, a viral homologue of Bcl-2, protects cells from programmed cell death. Virology 1996, 225(1):227-230.
7. Cabras G., Decaussin G., Zeng Y., Djennaoui D., Melouli H., Broully P., Bouguermouh A.M., Ooka T. Epstein-Barr virus encoded BALF1 gene is transcribed in Burkitt's lymphoma cell lines and in nasopharyngeal carcinoma's biopsies. J. Clin. Virol. 2005, 34(1):26-34.
8. Carmeliet P., Lampugnani M.G., Moons L., Breviario F., Compernolle V., Bono F., Balconi G., Spagnuolo R., Oosthuyse B., Dewerchin M., Zanetti A., Angellilo A., Mattot V., Nuyens D., Lutgens E., Clotman F., de Ruiter M.C., Gittenberger-de Groot A., Poelmann R., Lupu F., Herbert J.M., Collen D., Dejana E. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 1999, 98(2):147-157.
9. Chang Y.S., Shih L.Y., Peng C.L., Chen S.H., Liu S.T. Characterization of two newly established EBV-containing lymphoblastoid cell lines from patients with myeloid leukemias. Leuk. Res. 1990, 14(4):309-320.
10. Chen J., Ou-Yang X., Gao J., Zhu J., He X., Rong J. Knockdown of ribonuclease inhibitor expression with siRNA in non-invasive bladder cancer cell line BIU-87 promotes growth and metastasis potentials. Mol. Cell Biochem. 2011, 349(1-2):83-95.
11. Cheng E.H., Nicholas J., Bellows D.S., Hayward G.S., Guo H.G., Reitz M.S., Hardwick J.M. A Bcl-2 homolog encoded by Kaposi sarcoma-associated virus, human herpesvirus 8, inhibits apoptosis but does not heterodimerize with Bax or Bak. Proc. Natl. Acad. Sci. U.S.A. 1997, 94(2):690-694.
12. Cuconati A., White E. Viral homologs of Bcl-2: role of apoptosis in the regulation of virus infection. Genes Dev. 2002, 16(19):2465-2478.
13. de-The G., Geser A., Day N.E., Tukei P.M., Williams E.H., Beri D.P., Smith P.G., Dean A.G., Bronkamm G.W., Feorino P., Henle W. Epidemiological evidence for causal relationship between Epstein-Barr virus and Burkitt's lymphoma from Ugandan prospective study. Nature 1978, 274(5673):756-761.
14. Del Bufalo D., Biroccio A., Leonetti C., Zupi G. Bcl-2 overexpression enhances the metastatic potential of a human breast cancer line. FASEB J. 1997, 11(12):947-953.
15. Desbaillets I., Diserens A.C., de Tribolet N., Hamou M.F., Van Meir E.G. Regulation of interleukin-8 expression by reduced oxygen pressure in human glioblastoma. Oncogene 1999, 18(7):1447-1456.
16. Dirmeier U., Neuhierl B., Kilger E., Reisbach G., Sandberg M.L., Hammerschmidt W. Latent membrane protein 1 is critical for efficient growth transformation of human B cells by Epstein-Barr virus. Cancer Res. 2003, 63(11):2982-2989.
17. Fanidi A., Hancock D.C., Littlewood T.D. Suppression of c-myc-induced apoptosis by the Epstein-Barr virus gene product BHRF1. J. Virol. 1998, 72(10):8392-8395.
18. Fanidi A., Harrington E.A., Evan G.I. Cooperative interaction between c-myc and Bcl-2 proto-oncogenes. Nature 1992, 359(6395):554-556.
19. Foghsgaard L., Jaattela M. The ability of BHRF1 to inhibit apoptosis is dependent on stimulus and cell type. J. Virol. 1997, 71(10):7509-7517.
20. Fontanini G., Boldrini L., Vignati S., Chine S., Basolo F., Silvestri V., Lucchi M., Mussi A., Angeletti C.A., Bevilacqua G. Bcl-2 and p53 regulate vascular endothelial growth factor (VEGF)-mediated angiogenesis in non-small cell lung carcinoma. Eur. J. Cancer 1998, 34(5):718-723.
21. Harmey J.H., Dimitriadis E., Kay E., Redmond H.P., Bouchier-Hayes D. Regulation of macrophage production of vascular endothelial growth factor (VEGF) by hypoxia and transforming growth factor β-1. Ann. Surg. Oncol. 1998, 5(3):271-278.
22. Hatfull G., Bankier A.T., Barrell B.G., Farrell P.J. Sequence analysis of Raji Epstein-Barr virus DNA. Virology 1988, 164(2):334-340.
23. Henderson S., Huen D., Rowe M., Dawson C., Johnson G., Rickinson A. Epstein-Barr virus-coded BHRF1 protein, a viral homologue of Bcl-2, protects human B cells from programmed cell death. Proc. Natl. Acad. Sci. U.S.A. 1993, 90(18):8479-8483.
24. Henle G., Henle W. Epstein-Barr virus-specific IgA serum antibodies as an outstanding feature of nasopharyngeal carcinoma. Int. J. Cancer 1976, 17(1):1-7.
25. Henle W., Henle G. Evidence for a relation of Epstein-Barr virus to Burkitt's lymphoma and nasopharyngeal carcinoma. Bibl Haematol. 1970, 706-713.
26. Humme S., Reisbach G., Feederle R., Delecluse H.J., Bousset K., Hammerschmidt W., Schepers A. The EBV nuclear antigen 1 (EBNA1) enhances B cell immortalization several thousandfold. Proc. Natl. Acad. Sci. U.S.A. 2003, 100(19):10989-10994.
27. Iervolino A., Trisciuoglio D., Ribatti D., Candiloro A., Biroccio A., Zupi G., Del Bufalo D. Bcl-2 overexpression in human melanoma cells increases angiogenesis through VEGF mRNA stabilization and HIF-1-mediated transcriptional activity. FASEB J. 2002, 16(11):1453-1455.
28. Jacquemier J.D., Penault-Llorca F.M., Bertucci F., Sun Z.Z., Houvenaeghel G.F., Geneix J.A., Puig B.D., Bardou V.J., Hassoun J.A., Birnbaum D., Viens P.J. Angiogenesis as a prognostic marker in breast carcinoma with conventional adjuvant chemotherapy: a multiparametric and immunohistochemical analysis. J. Pathol. 1998, 184(2):130-135.
29. Kass L., Erler J.T., Dembo M., Weaver V.M. Mammary epithelial cell: influence of extracellular matrix composition and organization during development and tumorigenesis. Int. J. Biochem. Cell Biol. 2007, 39(11):1987-1994.
30. Kawanishi M. Expression of Epstein-Barr virus latent membrane protein 1 protects Jurkat T cells from apoptosis induced by serum deprivation. Virology 1997, 228(2):244-250.
31. Kieff E., Rickinson A.B. Epstein-Barr virus and its replication. Fields Virology 2007, 2603-2654. Lippincott-Williams & Wilkins, Philadephia. 5th edition. B.N. Fields, D.M. Knipe, P.M. Howley (Eds.).
32. Kieser A., Weich H.A., Brandner G., Marme D., Kolch W. Mutant p53 potentiates protein kinase C induction of vascular endothelial growth factor expression. Oncogene 1994, 9(3):963-969.
33. Kilger E., Pichler B., Goetz A.E., Rank N., Welte M., Morstedt K., Vetter H.O., Godje O., Schmitz C., Lamm P., Engelschalk E., Muehlbeyer D., Frey L. Procalcitonin as a marker of systemic inflammation after conventional or minimally invasive coronary artery bypass grafting. Thorac. Cardiovasc. Surg. 1998, 46(3):130-133.
34. Kirsch D.G., Doseff A., Chau B.N., Lim D.S., de Souza-Pinto N.C., Hansford R., Kastan M.B., Lazebnik Y.A., Hardwick J.M. Caspase-3-dependent cleavage of Bcl-2 promotes release of cytochrome C. J. Biol. Chem. 1999, 274(30):21155-21161.
35. Lal A., Peters H., St Croix B., Haroon Z.A., Dewhirst M.W., Strausberg R.L., Kaanders J.H., van der Kogel A.J., Riggins G.J. Transcriptional response to hypoxia in human tumors. J. Natl. Cancer Inst. 2001, 93(17):1337-1343.
36. Leight E.R., Sugden B. EBNA-1: a protein pivotal to latent infection by Epstein-Barr virus. Rev. Med. Virol. 2000, 10(2):83-100.
37. Leonetti C., D'Agnano I., Lozupone F., Valentini A., Geiser T., Zon G., Calabretta B., Citro G.C., Zupi G. Antitumor effect of c-myc antisense phosphorothioate oligodeoxynucleotides on human melanoma cells in vitro and and in mice. J. Natl. Cancer Inst. 1996, 88(7):419-429.
38. Linette G.P., Hess J.L., Sentman C.L., Korsmeyer S.J. Peripheral T-cell lymphoma in lckpr-Bcl-2 transgenic mice. Blood 1995, 86(4):1255-1260.
39. Marshall W.L., Yim C., Gustafson E., Graf T., Sage D.R., Hanify K., Williams L., Fingeroth J., Finberg R.W. Epstein-Barr virus encodes a novel homolog of the Bcl-2 oncogene that inhibits apoptosis and associates with Bax and Bak. J. Virol. 1999, 73(6):5181-5185.
40. Mazure N.M., Chen E.Y., Yeh P., Laderoute K.R., Giaccia A.J. Oncogenic transformation and hypoxia synergistically act to modulate vascular endothelial growth factor expression. Cancer Res. 1996, 56(15):3436-3440.
41. McDonnell T.J., Korsmeyer S.J. Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14; 18). Nature 1991, 349(6306):254-256.
42. Mignatti P., Rifkin D.B. Biology and biochemistry of proteinases in tumor invasion. Physiol. Rev. 1993, 73(1):161-195.
43. Mori S., Rempel R.E., Chang J.T., Yao G., Lagoo A.S., Potti A., Bild A., Nevins J.R. Utilization of pathway signatures to reveal distinct types of B lymphoma in the Emicro-myc model and human diffuse large B-cell lymphoma. Cancer Res. 2008, 68(20):8525-8534.
44. Mukhopadhyay D., Tsiokas L., Zhou X.M., Foster D., Brugge J.S., Sukhatme V.P. Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation. Nature 1995, 375(6532):577-581.
45. Nakagawa M., Tsuzuki S., Honma K., Taguchi O., Seto M. Synergistic effect of Bcl-2, myc and ccnd1 transforms mouse primary B cells into malignant cells. Haematologica 2011, 96(9):1318-1326.
46. Nava V.E., Cheng E.H., Veliuona M., Zou S., Clem R.J., Mayer M.L., Hardwick J.M. Herpesvirus saimiri encodes a functional homolog of the human Bcl-2 oncogene. J. Virol. 1997, 71(5):4118-4122.
47. Pan M.H., Lin C.C., Lin J.K., Chen W.J. Tea polyphenol (-)-epigallocatechin 3-gallate suppresses heregulin-beta1-induced fatty acid synthase expression in human breast cancer cells by inhibiting phosphatidylinositol 3-kinase/Akt and mitogen-activated protein kinase cascade signaling. J. Agric. Food Chem. 2007, 55(13):5030-5037.
48. Pearson G.R., Luka J., Petti L., Sample J., Birkenbach M., Braun D., Kieff E. Identification of an Epstein-Barr virus early gene encoding a second component of the restricted early antigen complex. Virology 1987, 160(1):151-161.
49. Rao L., Debbas M., Sabbatini P., Hockenbery D., Korsmeyer S., White E. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc. Natl. Acad. Sci. U.S.A. 1992, 89(16):7742-7746.
50. Reed J.C., Haldar S., Croce C.M., Cuddy M.P. Complementation by BCL2 and C-HA-RAS oncogenes in malignant transformation of rat embryo fibroblasts. Mol. Cell Biol. 1990, 10(8):4370-4374.
51. Ricca A., Biroccio A., Del Bufalo D., Mackay A.R., Santoni A., Cippitelli M. Bcl-2 over-expression enhances NF-kappaB activity and induces mmp-9 transcription in human MCF7(ADR) breast-cancer cells. Int. J. Cancer 2000, 86(2):188-196.
52. Sarid R., Sato T., Bohenzky R.A., Russo J.J., Chang Y. Kaposi's sarcoma-associated herpesvirus encodes a functional Bcl-2 homologue. Nat. Med. 1997, 3(3):293-298.
53. Shweiki D., Itin A., Soffer D., Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992, 359(6398):843-845.
54. Stipa F., Lucandri G., Limiti M.R., Bartolucci P., Cavallini M., Di Carlo V., D'Amato A., Ribotta G., Stipa S. Angiogenesis as a prognostic indicator in pancreatic ductal adenocarcinoma. Anticancer Res. 2002, 445-449.
55. Strasser A., Harris A.W., Bath M.L., Cory S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and Bcl-2. Nature 1990, 348(6299):331-333.
56. Strasser A., Harris A.W., Cory S. E mu-Bcl-2 transgene facilitates spontaneous transformation of early pre-B and immunoglobulin-secreting cells but not T cells. Oncogene 1993, 8(1):1-9.
57. Ueba T., Nosaka T., Takahashi J.A., Shibata F., Florkiewicz R.Z., Vogelstein B., Oda Y., Kikuchi H., Hatanaka M. Transcriptional regulation of basic fibroblast growth factor gene by p53 in human glioblastoma and hepatocellular carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 1994, 91(19):9009-9013.
58. Vaux D.L. Immunopathology of apoptosis-introduction and overview. Springer Semin Immunopathol 1998, 19(3):271-278.
59. Watanabe A., Maruo S., Ito T., Ito M., Katsumura K.R., Takada K. Epstein-Barr virus-encoded Bcl-2 homologue functions as a survival factor in Wp-restricted Burkitt lymphoma cell line P3HR-1. J. Virol. 2010, 84(6):2893-2901.
60. Zhang P., Zhang C., Wei D., Zhao Z., Liu J., Cai M. Improved MTT colorimetric assay for serum TNF activity. Hua Xi Yi Ke Da Xue Xue Bao 1997, 28(4):445-447.