Investigation of the Susceptibility of Human Cell Lines to Bovine Herpesvirus 4 Infection: Demonstration that Human Cells Can Support a Nonpermissive Persistent Infection Which Protects Them against Tumor Necrosis Factor Alpha-Induced Apoptosis

Journal of Virology

Volumn 78, Issue 5, 2004, Pages 2336-2347

  Gillet, L ^a   Minner, F ^a   Detry, B ^a   Farnir, F ^a   Willems, L ^a   Lambot, M ^a   Thiry, E ^a   Pastoret, P P ^b   Schynts, F ^a   Vanderplasschen, A ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOHEXIMIDE; GREEN FLUORESCENT PROTEIN; MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR ALPHA; VIRUS DNA;

APOPTOSIS; ARTICLE; BOVINE HERPES VIRUS; BOVINE HERPES VIRUS 4; CELL MEMBRANE; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VIRUS CELL INTERACTION; VIRUS RECOMBINANT;

EID: 10744230493     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.5.2336-2347.2004     Document Type: Article

References (66)

1. Barahona, H. H., L. V. Meléndez, N. W. King, M. D. Daniel, C. E. O. Fraser, and A. C. Preville. 1973. Herpesvirus aotus type 2: a new viral agent from owl monkeys (Aotus trivirgatus). J. Infect. Dis. 127:171-178.
2. Bartha, A., M. Juhasz, and H. Liebermann. 1966. Isolation of a bovine herpesvirus from calves with respiratory disease and keratoconjunctivitis: a preliminary report. Acta Vet. Acad. Sci. Hung. 16:357-358.
3. Bechtel, J. T., Y. Liang, J. Hvidding, and D. Ganem. 2003. Host range of Kaposi's sarcoma-associated herpesvirus in cultured cells. J. Virol. 77:6474-6481.
4. Bishop, G. A., and L. K. Busch. 2002. Molecular mechanisms of B-lymphocyte transformation by Epstein-Barr virus. Microbes Infect. 4:853-857.
5. Boneva, R. S., T. M. Folks, and L. E. Chapman. 2001. Infectious disease issues in xenotransplantation. Clin. Microbiol. Rev. 14:1-14.
6. Borchers, K., J. Brackmann, and O. Kershaw. 2002. The mouse is not permissive for equine herpesvirus 2 (EHV-2), however viral DNA persisted in lung and spleen depending on the inoculation route. Arch. Virol. 147:1437-1444.
7. Bublot, M., J. Dubuisson, M. F. Van Bressem, S. Danyi, P. P. Pastoret, and E. Thiry. 1991. Antigenic and genomic identity between simian herpesvirus aotus type 2 and bovine herpesvirus type 4. J. Gen. Virol. 72:715-719.
8. Chmielewicz, B., M. Goltz, K. H. Lahrmann, and B. Ehlers. 2003. Approaching virus safety in xenotransplantation: a search for unrecognized herpesviruses in pigs. Xenotransplantation 10:349-356.
9. Dahlberg, J. E., D. V. Ablashi, J. S. Rhim, A. Fladger, and S. Z. Salahuddin. 1988. Replication of Herpesvirus saimiri is semipermissive in human cells because of a block in the synthesis of certain late proteins. Intervirology 29:234-277.
10. Davison, A. J. 2002. Evolution of the herpesviruses. Vet. Microbiol. 86:69-88.
11. Donofrio, G., S. Cavirani, T. Simone, and V. L. van Santen. 2002. Potential of bovine herpesvirus 4 as a gene delivery vector. J. Virol. Methods 101:49-61.
12. Donofrio, G., S. Cavirani, and V. L. van Santen. 2000. Establishment of a cell line persistently infected with bovine herpesvirus-4 by use of a recombinant virus. J. Gen. Virol. 81:1807-1814.
13. Donofrio, G., C. F. Flammini, F. Scatozza, and S. Cavirani. 2000. Detection of bovine herpesvirus 4 (BoHV-4) DNA in the cell fraction of milk of dairy cattle with history of BoHV-4 infection. J. Clin. Microbiol. 38:4668-4671.
14. Dourmishev, L. A., A. L. Dourmishev, D. Palmeri, R. A. Schwartz, and D. M. Lukac. 2003. Molecular genetics of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) epidemiology and pathogenesis. Microbiol. Mol. Biol. Rev. 67:175-212.
15. Dubuisson, J., D. Boulanger, M. Bublot, E. Thiry, and P. P. Pastoret. 1989. Proteins specified by bovine herpesvirus type 4: structural proteins of the virion and identification of two major glycoproteins by using monoclonal antibodies. J. Gen. Virol. 70:1743-1753.
16. Dubuisson, J., P. P. Pastoret, and E. Thiry. 1991. Temporal control of bovine herpesvirus type 4 glycoprotein synthesis. J. Gen. Virol. 72:1429-1434.
17. Egyed, L. 1998. Replication of bovine herpesvirus type 4 in human cells in vitro. J. Clin. Microbiol. 36:2109-2111.
18. Egyed, L., J. P. Kluge, and A. Bartha. 1997. Histological studies of bovine herpesvirus type 4 infection in non-ruminant species. Vet. Microbiol. 57:283-289.
19. Ehlers, B., S. Ulrich, and M. Goltz. 1999. Detection of two novel porcine herpesviruses with high similarity to gammaherpesviruses. J. Gen. Virol. 80:971-978.
20. Fabricant, C. G., J. H. Gillespsie, and L. Krook. 1971. Intracellular and extracellular mineral crystal formation induced by viral infection of cell cultures. Infect. Immun. 3:416-419.
21. Fejer, G., M. M. Medveczky, E. Horvath, B. Lane, Y. Chang, and P. G. Medveczky. 2003. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus interacts preferentially with the terminal repeats of the genome in vivo and this complex is sufficient for episomal DNA replication. J. Gen. Virol. 84:1451-1462.
22. Fickenscher, H., and B. Fleckenstein. 2001. Herpesvirus saimiri. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:545-567.
23. Frolova-Jones, E. A., A. Ensser, A. J. Stevenson, S. E. Kinsey, and D. M. Meredith. 2000. Stable marker gene transfer into human bone marrow stromal cells and their progenitors using novel herpesvirus saimiri-based vectors. J. Hematother. Stem Cell Res. 9:573-581.
24. Garber, A. C., J. Hu, and R. Renne. 2002. Latency-associated nuclear antigen (LANA) cooperatively binds to two sites within the terminal repeat, and both sites contribute to the ability of LANA to suppress transcription and to facilitate DNA replication. J. Biol. Chem. 277:27401-27411.
25. Gollackner, B., N. J. Mueller, S. Houser, I. Qawi, D. Soizic, C. Knosalla, L. Buhler, F. J. Dor, M. Awwad, D. H. Sachs, D. K. Cooper, S. C. Robson, and J. A. Fishman. 2003. Porcine cytomegalovirus and coagulopathy in pig-to-primate xenotransplantation. Transplantation 75:1841-1847.
26. Grundhoff, A., and D. Ganem. 2003. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus permits replication of terminal repeat-containing plasmids. J. Virol. 77:2779-2783.
27. Gunzburg, W. H., and B. Salmons. 2000. Xenotransplantation: is the risk of viral infection as great as we thought? Mol. Med. Today 6:199-208.
28. Hall, K. T., M. S. Giles, D. J. Goodwin, M. A. Calderwood, I. M. Carr, A. J. Stevenson, A. F. Markham, and A. Whitehouse. 2000. Analysis of gene expression in a human cell line stably transduced with herpesvirus saimiri. J. Virol. 74:7331-7337.
29. Holm, M., M. Thomsen, M. Hoyer, and P. Hokland. 1998. Optimization of a flow cytometric method for the simultaneous measurement of cell surface antigen, DNA content, and in vitro BrdUrd incorporation into normal and malignant hematopoietic cells. Cytometry 32:28-36.
30. Hu, J., A. C. Garber, and R. Renne. 2002. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus supports latent DNA replication in dividing cells. J. Virol. 76:11677-11687.
31. Jenson, H. B., Y. Ench, S. J. Gao, K. Rice, D. Carey, R. C. Kennedy, J. R. Arrand, and M. Mackett. 2000. Epidemiology of herpesvirus papio infection in a large captive baboon colony: similarities to Epstein-Barr virus infection in humans. J. Infect. Dis. 181:1462-1466.
32. Kit, S., M. Kit, H. Ichimura, R. Crandell, and S. McConnell. 1986. Induction of thymidine kinase activity by viruses with group B DNA genomes: bovine cytomegalovirus (bovine herpesvirus 4). Virus Res. 4:197-212.
33. Kokles, V. R. 1986. Zum Vorkommen von Herpes-Orphan-Virusinfektionen des Rindes. Mh. Vet. Med. 41:551-555.
34. Lafemina, R. L., and G. S. Hayward. 1988. Differences in cell-type-specific blocks to immediate-early gene expression and DNA replication of human, simian and murine cytomegalovirus. J. Gen. Virol. 69:355-374.
35. Lim, C., D. Lee, T. Seo, C. Choi, and J. Choe. 2003. Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus functionally interacts with heterochromatin protein 1. J. Biol. Chem. 278:7397-7405.
36. Lomonte, P., M. Bublot, V. van Santen, G. M. Keil, P. P. Pastoret, and E. Thiry. 1995. Analysis of bovine herpesvirus 4 genomic regions located outside the conserved gammaherpesvirus gene blocks. J. Gen. Virol. 76:1835-1841.
37. MacGregor, G. R., and C. T. Caskey. 1989. Construction of plasmids that express Escherichia coli beta-galactosidase in mammalian cells. Nucleic Acids Res. 17:2365.
38. Macsween, K. F., and D. H. Crawford. 2003. Epstein-Barr virus-recent advances. Lancet Infect. Dis. 3:131-140.
39. McGeoch, D. J. 2001. Molecular evolution of the gamma-Herpesvirinae. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:421-435.
40. McGeoch, D. J., S. Cook, A. Dolan, F. E. Jamieson, and E. A. Telford. 1995. Molecular phylogeny and evolutionary timescale for the family of mammalian herpesviruses. J. Mol. Biol. 247:443-458.
41. McGeoch, D. J., A. Dolan, and A. C. Ralph. 2000. Toward a comprehensive phylogeny for mammalian and avian herpesviruses. J. Virol. 74:10401-10406.
42. Moreno-Lopez, J., M. Goltz, C. Rehbinder, K. V. Valsala, and H. Ludwig. 1989. A bovine herpesvirus (BHV-4) as passenger virus in ethmoidal tumours in Indian cattle. Zentbl. Vetmed. B 36:481-486.
43. Mueller, N. J., R. N. Barth, S. Yamamoto, H. Kitamura, C. Patience, K. Yamada, D. K. Cooper, D. H. Sachs, A. Kaur, and J. A. Fishman. 2002. Activation of cytomegalovirus in pig-to-primate organ xenotransplantation. J. Virol. 76:4734-4740.
44. Nakamichi, K., Y. Matsumoto, and H. Otsuka. 2001. Defective infection of bovine herpesvirus 1 in non-permissive murine cells. J. Vet. Med. Sci. 63:1139-1142.
45. Nash, A. A., B. M. Dutia, J. P. Stewart, and A. J. Davison. 2001. Natural history of murine gamma-herpesvirus infection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:569-579.
46. Nixdorf, R., J. Schmidt, A. Karger, and T. C. Mettenleiter. 1999. Infection of Chinese hamster ovary cells by pseudorabies virus. J. Virol. 73:8019-8026.
47. Peterson, R. B., and S. M. Goyal. 1988. Propagation and quantitation of animal herpesviruses in eight cell culture systems. Comp. Immunol. Microbiol. Infect. Dis. 11:93-98.
48. Plowright, W., R. D. Ferris, and G. R. Scott. 1960. Blue wildebeest and the etiological agent of bovine malignant fever. Nature 188:1167-1169.
49. Roizman, B., and P. E. Pellet. 2001. The family Herpesviridae: a brief introduction, p. 2381-2397. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott/The Williams & Wilkins Co., Philadelphia, Pa.
50. Rossiter, P. B., I. D. Gumm, D. A. Stagg, P. A. Conrad, S. Mukolwe, F. G. Davies, and H. White. 1989. Isolation of bovine herpesvirus-3 from African buffaloes (Syncerus caffer). Res. Vet. Sci. 46:337-343.
51. Skinner, G. R., A. Ahmad, and J. A. Davies. 2001. The infrequency of transmission of herpesviruses between humans and animals: postulation of an unrecognized protective host mechanism. Comp. Immunol. Microbiol. Infect. Dis. 24:255-269.
52. Stevenson, A. J., E. Frolova-Jones, K. T. Hall, S. E. Kinsey, A. F. Markham, A. Whitehouse, and D. M. Meredith. 2000. A herpesvirus saimiri-based gene therapy vector with potential for use in cancer immunotherapy. Cancer Gene Ther. 7:1077-1085.
53. Theodoridis, A. 1985. Studies on bovine herpesviruses. Part 1. Isolation and characterization of viruses isolated from the genital tract of cattle. Onderstepoort J. Vet. Res. 52:239-254.
54. Thiry, E., P. Lomonte, A. Vanderplasschen, and P. P. Pastoret. 1997. Bovine herpesvirus 4 (Movar herpesvirus), p. 439-445. IARC Monographs on the evaluation of carcinogenic risks to human, vol. 70. Epstein-Barr virus and Kaposi's sarcoma herpesvirus/human herpesvirus 8. International Agency for Research on Cancer, Lyon, France.
55. Thiry, E., P. P. Pastoret, and C. M. Calberg-Bacq. 1981. Isolement d'un herpesvirus chez un taureau infertile. Ann. Med. Vet. 125:143.
56. Todd, W. J., and J. Storz. 1983. Morphogenesis of a cytomegalovirus from an American bison affected with malignant catarrhal fever. J. Gen. Virol. 64:1025-1030.
57. Vanderplasschen, A., M. Goltz, J. Lyaku, C. Benarafa, H.-J. Buhk, E. Thiry, and P.-P. Pastoret. 1995. The replication in vitro of the gammaherpesvirus bovine herpesvirus 4 is restricted by its DNA synthesis dependence on the S phase of the cell cycle. Virology 213:328-340.
58. Vanderplasschen, A., and G. L. Smith. 1997. A novel virus binding assay using confocal microscopy: demonstration that the intracellular and extracellular vaccinia virions bind to different cellular receptors. J. Virol. 71:4032-4041.
59. Van Opdenbosch, E., G. Wellemans, and J. Oudewater. 1986. Toevallige isolatie van het boviene herpesvirus 4 uit de long van een schaap. Vlaams Diergeneesk. Tijdschr. 55:432-433.
60. Wajant, H., E. Haas, R. Schwenzer, F. Muhlenbeck, S. Kreuz, G. Schubert, M. Grell, C. Smith, and P. Scheurich. 2000. Inhibition of death receptor-mediated gene induction by a cycloheximide-sensitive factor occurs at the level of or upstream of Fas-associated death domain protein (FADD). J. Biol. Chem. 275:24357-24366.
61. Wang, G. H., J. Bertin, Y. Wang, D. A. Martin, J. Wang, K. J. Tomaselli, R. C. Armstrong, and J. I. Cohen. 1997. Bovine herpesvirus 4 BORFE2 protein inhibits Fas- and tumor necrosis factor receptor 1-induced apoptosis and contains death effector domains shared with other gamma-2 herpesviruses. J. Virol. 71:8928-8932.
62. Wellenberg, G. J., W. H. M. Van Der Poel, T. J. K. Van Der Vorst, P. H. R. Van Valkengoed, Y. H. Schukken, F. Wagenaar, and J. T. Van Oirschot. 2000. Bovine herpesvirus 4 in bovine clinical mastitis. Vet. Rec. 147:222-225.
63. Wellenberg, G. J., E. R. Verstraten, S. Belak, S. B. Verschuren, F. A. Rijsewijk, R. Peshev, and J. T. Van Oirschot. 2001. Detection of bovine herpesvirus 4 glyCoprotein B and thymidine kinase DNA by PCR assays in bovine milk. J. Virol. Methods 97:101-112.
64. Whitby, D., A. Stossel, C. Gamache, J. Papin, M. Bosch, A. Smith, D. H. Kedes, G. White, R. Kennedy, and D. P. Dittmer. 2003. Novel Kaposi's sarcoma-associated herpesvirus homolog in baboons. J. Virol. 77:8159-8165.
65. Whitehouse, A. 2003. Herpesvirus saimiri: a potential gene delivery vector. Int. J. Mol. Med. 11:139-148.
66. Zimmermann, W., H. Broll, B. Ehlers, H. J. Buhk, A. Rosenthal, and M. Goltz. 2001. Genome sequence of bovine herpesvirus 4, a bovine rhadinovirus, and identification of an origin of DNA replication. J. Virol. 75:1186-1194.