Establishment of a cell line persistently infected with bovine herpesvirus-4 by use of a recombinant virus Free

Abstract

Bovine herpesvirus-4 (BHV-4), a gammaherpesvirus lacking a clear disease association, productively infects multiple cell lines of various species and causes cell death. A human rhabdomyosarcoma cell line, RD-4, infected with BHV-4 produced low levels of early and late viral RNAs and infectious virus, but exhibited no cytopathic effect. Using a recombinant BHV-4 containing a neomycin-resistance gene, we established RD-4-derived cell lines persistently infected with BHV-4. The viral genome in these cells was predominantly circular. Because of drug selection, every cell contained a viral genome. In addition, all cells stained with a BHV-4-specific antiserum. Therefore, these cell lines are not carrier cultures. These cells produced infectious virus at all passages tested. Even though cells were selected and maintained at a concentration of geneticin at least 2·5 times that necessary to kill uninfected RD-4 cells, selected cells contained only approximately one viral genome per diploid host cell genome. Persistently infected cells grew more slowly than uninfected cells, even in the absence of drug. The slower growth of these cells suggests that any growth advantage conferred by multiple copies of the neomycin-gene-carrying viral genome might be offset by the detrimental effects of viral gene expression. This situation contrasts with other gammaherpesviruses, which are able to growth-transform cells.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-7-1807
2000-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/7/0811807a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-7-1807&mimeType=html&fmt=ahah

References

  1. Ballestas, M. E., Chatis, P. A. & Kaye, K. M. (1999). Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen.Science 284, 641-644.[CrossRef] [Google Scholar]
  2. Bartha, A., Fadol, A. M., Liebermann, H., Ludwig, H., Mohanty, S. B., Osorio, F. A., Reed, D. E., Storz, J., Straub, O. C., Van der Maaten, M. J. & Wellermans, G. (1987). Problems concerning the taxonomy of the ‘Movar-Type’ bovine herpesvirus.Intervirology 28, 1-7.[CrossRef] [Google Scholar]
  3. Bataille, D. & Epstein, A. (1994). Herpes simplex virus replicative concatemers contain L components in inverted orientation.Virology 203, 384-388.[CrossRef] [Google Scholar]
  4. Bermudez-Cruz, R., Zhang, L. & van Santen, V. L. (1997). Characterization of an abundant, unique 1·7-kilobase bovine herpesvirus 4 (BHV-4) late RNA and mapping of a BHV-4 IE2 transactivator-binding site in its promoter-regulatory region.Journal of Virology 71, 527-538. [Google Scholar]
  5. Broll, H., Buhk, H.-J., Zimmermann, W. & Goltz, M. (1999). Structure and function of the prDNA and the genomic termini of the γ2-herpesvirus bovine herpesvirus type 4.Journal of General Virology 80, 979-986. [Google Scholar]
  6. Cesarman, E., Moore, P. S., Rao, P. H., Inghirami, G., Knowles, D. M. & Chang, Y. (1995). In vitro establishment and characterization of two acquired immunodeficiency syndrome-related lymphoma cell lines (BC-1 and BC-2) containing Kaposi’s sarcoma-associated herpesvirus-like (KSHV) DNA sequences.Blood 86, 2708-2714. [Google Scholar]
  7. Chang, L.-Y. & van Santen, V. L. (1992). Immediate-early, early, and late RNAs in bovine herpesvirus-4-infected cells.Virology 191, 909-920.[CrossRef] [Google Scholar]
  8. Decker, L. L., Shankar, P., Khan, G., Freeman, R. B., Dezube, B. J., Lieberman, J. & Thorley-Lawson, D. A. (1996). The Kaposi sarcoma-associated herpesvirus (KSHV) is present as an intact latent genome in KS tissue but replicates in the peripheral blood mononuclear cells of KS patients.Journal of Experimental Medicine 184, 283-288.[CrossRef] [Google Scholar]
  9. Desrosiers, R. C., Kamine, J., Bakker, A., Silva, D., Woychik, R. P., Sakai, D. D. & Rottman, F. M. (1985). Synthesis of bovine growth hormone in primates by using a herpesvirus vector.Molecular and Cellular Biology 5, 2796-2803. [Google Scholar]
  10. Drexler, H. G., Uphoff, C. C., Gaidano, G. & Carbone, A. (1998). Lymphoma cell lines: in vitro models for the study of HHV-8+ primary effusion lymphomas (body cavity-based lymphomas).Leukemia 12, 1507-1517.[CrossRef] [Google Scholar]
  11. Dubuisson, J., Boulanger, D., Bublot, M., Thiry, E. & Pastoret, P.-P. (1989a). Proteins specified by bovine herpesvirus type 4: structural proteins of the virion and identification of two major glycoproteins by using monoclonal antibodies.Journal of General Virology 70, 1743-1753.[CrossRef] [Google Scholar]
  12. Dubuisson, J., Thiry, E., Bublot, M., Thomas, I., van Bressem, M. F., Coignoul, F. & Pastoret, P.-P. (1989b). Experimental infection of bulls with a genital isolate of bovine herpesvirus-4 and reactivation of latent virus with dexamethasone.Veterinary Microbiology 21, 97-114.[CrossRef] [Google Scholar]
  13. Dubuisson, J., Pastoret, P.-P. & Thiry, E. (1991). Temporal control of bovine herpesvirus 4 glycoprotein synthesis.Journal of General Virology 72, 1429-1434.[CrossRef] [Google Scholar]
  14. Egyed, L. (1998). Replication of bovine herpesvirus type 4 in human cells in vitro.Journal of Clinical Microbiology 36, 2109-2111. [Google Scholar]
  15. Egyed, L. & Bartha, A. (1998). PCR studies on the potential sites for latency of BHV-4 in calves.Veterinary Research Communications 22, 209-216.[CrossRef] [Google Scholar]
  16. Ehlers, B., Buhk, H.-J. & Ludwig, H. (1985). Analysis of bovine cytomegalovirus genome structure: cloning and mapping of the monomeric polyrepetitive DNA unit, and comparison of European and American strains.Journal of General Virology 66, 55-68.[CrossRef] [Google Scholar]
  17. Flore, O., Rafii, S., Ely, S., O’Leary, J. J., Hyjek, E. M. & Cesarman, E. (1998). Transformation of primary human endothelial cells by Kaposi’s sarcoma-associated herpesvirus.Nature 394, 588-592.[CrossRef] [Google Scholar]
  18. Galik, P. K., van Santen, V. L., Stringfellow, D. A., Bird, R. C., Wright, J. C. & Smith, P. C. (1993). Development of a DNA probe for identification of bovine herpesvirus 4.American Journal of Veterinary Research 54, 653-659. [Google Scholar]
  19. Gardella, T., Medveczky, P., Sairenji, T. & Mulder, C. (1984). Detection of circular and linear herpesvirus DNA molecules in mammalian cells by gel electrophoresis.Journal of Virology 50, 248-254. [Google Scholar]
  20. Grassmann, R. & Fleckenstein, B. (1989). Selectable recombinant herpesvirus saimiri is capable of persisting in a human T-cell line.Journal of Virology 63, 1818-1821. [Google Scholar]
  21. Huang, E.-S. (1975). Human cytomegalovirus. IV. Specific inhibition of virus-induced DNA polymerase activity and viral DNA replication by phosphonoacetic acid.Journal of Virology 16, 1560-1565. [Google Scholar]
  22. Jung, J. U., Choi, J. K., Ensser, A. & Biesinger, B. (1999). Herpesvirus saimiri as a model for gammaherpesvirus oncogenesis.Seminars in Cancer Biology 9, 231-239.[CrossRef] [Google Scholar]
  23. Keil, G. M., Heinze, A. & Mächtig, B. (1990). Bovine herpesvirus 4 vector for life-virus vaccines?Zentralblatt für Bakteriologie 272, 375. [Google Scholar]
  24. Kieff, E. (1996). Epstein–Barr virus and its replication. In Fields Virology, pp. 1109-1162. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: Lippincott–Raven Publishers.
  25. Krogman, L. A. & McAdaragh, J. P. (1982). Recrudescence of bovine herpesvirus-5 in experimentally infected calves.American Journal of Veterinary Research 43, 336-338. [Google Scholar]
  26. Kung, S. H. & Medveczky, P. G. (1996). Identification of a herpesvirus saimiri cis-acting DNA fragment that permits stable replication of episomes in transformed T cells.Journal of Virology 70, 1738-1744. [Google Scholar]
  27. Lomonte, P., Bublot, M., van Santen, V., Keil, G., Pastoret, P. P. & Thiry, E. (1996). Bovine herpesvirus 4: genomic organization and relationship with two other gammaherpesviruses, Epstein–Barr virus and herpesvirus saimiri.Veterinary Microbiology 53, 79-89.[CrossRef] [Google Scholar]
  28. Lupton, S. & Levine, A. J. (1985). Mapping genetic elements of Epstein–Barr virus that facilitate extrachromosomal persistence of Epstein–Barr virus-derived plasmids in human cells.Molecular and Cellular Biology 5, 2533-2542. [Google Scholar]
  29. Miller, G. (1990). Epstein–Barr virus. In Virology, pp. 1921-1958. Edited by B. N. Fields, D. M. Knipe, R. M. Chanock, M. S. Hirsch, J. L. Melnick, T. P. Monath & B. Roizman. New York: Raven Press.
  30. Moore, P. S. & Chang, Y. (1998). Kaposi’s sarcoma-associated herpesvirus-encoded oncogenes and oncogenesis.Journal of the National Cancer Institute Monograph Series 23, 65-71. [Google Scholar]
  31. Moses, A. V., Fish, K. N., Ruhl, R., Smith, P. P., Strussenberg, J. G., Zhu, L., Chandran, B. & Nelson, J. A. (1999). Long-term infection and transformation of dermal microvascular endothelial cells by human herpesvirus 8.Journal of Virology 73, 6892-6902. [Google Scholar]
  32. Naeem, K., Caywood, D. D., Goyal, S. M., Werdin, R. E. & Murtaugh, M. P. (1993). Persistence of bovid herpesvirus-4 in experimentally inoculated pregnant rabbits.Microbiologica 16, 87-94. [Google Scholar]
  33. Nilsson, K. (1979). The nature of lymphoid cell lines and their relationship to the virus. In The Epstein–Barr Virus, pp. 225-281. Edited by M. A. Epstein & B. G. Achong. Berlin: Springer-Verlag.
  34. Osorio, F. A. & Reed, D. E. (1983). Experimental inoculation of cattle with bovine herpesvirus-4: evidence for a lymphoid-associated persistent infection.American Journal of Veterinary Research 44, 975-980. [Google Scholar]
  35. Osorio, F. A., Reed, D. E. & Rock, D. L. (1982). Experimental infection of rabbits with bovine herpesvirus-4: acute and persistent infection.Veterinary Microbiology 7, 503-513.[CrossRef] [Google Scholar]
  36. Osorio, F. A., Rock, D. L. & Reed, D. E. (1985). Studies on the pathogenesis of a bovine cytomegalo-like virus in an experimental host.Journal of General Virology 66, 1941-1951.[CrossRef] [Google Scholar]
  37. Peterson, R. B. & Goyal, S. M. (1988). Propagation and quantitation of animal herpesviruses in eight cell culture systems.Comparative Immunology, Microbiology and Infectious Diseases 11, 93-98.[CrossRef] [Google Scholar]
  38. Poffenberger, K. M. & Roizman, B. (1985). A noninverting genome of a viable herpes simplex virus 1: presence of head-to-tail linkages in packaged genomes and requirements for circularization after infection.Journal of Virology 53, 587-595. [Google Scholar]
  39. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989).Molecular Cloning: A Laboratory Manual., 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  40. Severini, A., Morgan, A. R., Tovell, D. R. & Tyrrell, D. L. (1994). Study of the structure of replicative intermediates of HSV-1 DNA by pulsed-field gel electrophoresis.Virology 200, 428-435.[CrossRef] [Google Scholar]
  41. Simmer, B., Alt, M., Buckreus, I., Berthold, S., Fleckenstein, B., Platzer, E. & Grassmann, R. (1991). Persistence of selectable herpesvirus saimiri in various human haematopoietic and epithelial cell lines.Journal of General Virology 72, 1953-1958.[CrossRef] [Google Scholar]
  42. Sugden, B., Phelps, M. & Domoradzki, J. (1979). Epstein–Barr virus DNA is amplified in transformed lymphocytes.Journal of Virology 31, 590-595. [Google Scholar]
  43. Thiry, E., Bublot, M., Dubuisson, J. & Pastoret, P.-P. (1989). Bovine herpesvirus-4 (BHV-4) infections of cattle. In Herpesvirus Diseases of Cattle, Horses, and Pigs, pp. 96-115. Edited by G. Wittmann. Boston: Kluwer Academic Publishers.
  44. Truman, D., Ludwig, H. & Storz, J. (1986). Bovine herpesvirus type 4: studies on the biology and spread in cattle herds and in insemination bulls.Journal of Veterinary Medicine, Series B 33, 485-501.[CrossRef] [Google Scholar]
  45. Tsygankov, A. Y. & Romano, G. (1999). Mechanisms of cell transformation by Herpesvirus saimiri.Anticancer Research 19, 973-983. [Google Scholar]
  46. Usherwood, E. J., Stewart, J. P. & Nash, A. A. (1996). Characterization of tumor cell lines derived from murine gammaherpesvirus-68-infected mice.Journal of Virology 70, 6516-6518. [Google Scholar]
  47. van Santen, V. L. (1991). Characterization of the bovine herpesvirus 4 major immediate-early transcript.Journal of Virology 65, 5211-5224. [Google Scholar]
  48. van Santen, V. L. & Chang, L.-Y. (1992). Cloning and mapping of EcoRI, HindIII, and PstI fragments of bovine herpesvirus 4 (DN-599).Intervirology 34, 44-52. [Google Scholar]
  49. Vanderplasschen, A., Goltz, M., Lyaku, J., Benarafa, C., Buhk, H. J., Thiry, E. & Pastoret, P. P. (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.[CrossRef] [Google Scholar]
  50. Yates, J., Warren, N., Reisman, D. & Sugden, B. (1984). A cis-acting element from the Epstein–Barr viral genome that permits stable replication of recombinant plasmids in latently infected cells.Proceedings of the National Academy of Sciences, USA 81, 3806-3810.[CrossRef] [Google Scholar]
  51. Yates, J. L., Warren, N. & Sugden, B. (1985). Stable replication of plasmids derived from Epstein–Barr virus in various mammalian cells.Nature 313, 812-815.[CrossRef] [Google Scholar]
  52. Zhang, X., Efstathiou, S. & Simmons, A. (1994). Identification of novel herpes simplex virus replicative intermediates by field inversion gel electrophoresis: implications for viral DNA amplification strategies.Virology 202, 530-539.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-7-1807
Loading
/content/journal/jgv/10.1099/0022-1317-81-7-1807
Loading

Data & Media loading...

Most cited Most Cited RSS feed