1887

Abstract

Two novel gammaherpesviruses were isolated, one from a field vole () and the other from wood mice (). The genome of the latter, designated wood mouse herpesvirus (WMHV), was completely sequenced. WMHV had the same genome structure and predicted gene content as murid herpesvirus 4 (MuHV4; murine gammaherpesvirus 68). Overall nucleotide sequence identity between WMHV and MuHV4 was 85 % and most of the 10 kb region at the left end of the unique region was particularly highly conserved, especially the viral tRNA-like sequences and the coding regions of genes and . The partial sequence (71 913 bp) of another gammaherpesvirus, Brest herpesvirus (BRHV), which was isolated ostensibly from a white-toothed shrew (), was also determined. The BRHV sequence was 99.2 % identical to the corresponding portion of the WMHV genome. Thus, WMHV and BRHV appeared to be strains of a new virus species. Biological characterization of WMHV indicated that it grew with similar kinetics to MuHV4 in cell culture. The pathogenesis of WMHV in wood mice was also extremely similar to that of MuHV4, except for the absence of inducible bronchus-associated lymphoid tissue at day 14 post-infection and a higher load of latently infected cells at 21 days post-infection.

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2010-04-01
2024-03-28
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References

  1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J.(1997). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402.[CrossRef] [Google Scholar]
  2. Baldick, C. J., Jr, Marchini, A., Patterson, C. E. & Shenk, T.(1997). Human cytomegalovirus tegument protein pp71 (ppUL82) enhances the infectivity of viral DNA and accelerates the infectious cycle. J Virol 71, 4400–4408. [Google Scholar]
  3. Bell, M. J., Brennan, R., Miles, J. J., Moss, D. J., Burrows, J. M. & Burrows, S. R.(2008). Widespread sequence variation in Epstein–Barr virus nuclear antigen 1 influences the antiviral T cell response. J Infect Dis 197, 1594–1597.[CrossRef] [Google Scholar]
  4. Bennett, M., Crouch, A. J., Begon, M., Duffy, B., Feore, S., Gaskell, R. M., Kelly, D. F., McCracken, C. M., Vicary, L. & Baxby, D.(1997). Cowpox in British voles and mice. J Comp Pathol 116, 35–44.[CrossRef] [Google Scholar]
  5. Blasdell, K., McCracken, C., Morris, A., Nash, A. A., Begon, M., Bennett, M. & Stewart, J. P.(2003). The wood mouse is a natural host for Murid herpesvirus 4. J Gen Virol 84, 111–113.[CrossRef] [Google Scholar]
  6. Blaskovic, D., Stancekova, M., Svobodova, J. & Mistrikova, J.(1980). Isolation of five strains of herpesviruses from two species of free living small rodents. Acta Virol 24, 468 [Google Scholar]
  7. Bowden, R. J., Simas, J. P., Davis, A. J. & Efstathiou, S.(1997). Murine gammaherpesvirus 68 encodes tRNA-like sequences which are expressed during latency. J Gen Virol 78, 1675–1687. [Google Scholar]
  8. Bridgeman, A., Stevenson, P. G., Simas, J. P. & Efstathiou, S.(2001). A secreted chemokine binding protein encoded by murine gammaherpesvirus-68 is necessary for the establishment of a normal latent load. J Exp Med 194, 301–312.[CrossRef] [Google Scholar]
  9. Carver, T. J., Rutherford, K. M., Berriman, M., Rajandream, M. A., Barrell, B. G. & Parkhill, J.(2005).act: the Artemis Comparison Tool. Bioinformatics 21, 3422–3423.[CrossRef] [Google Scholar]
  10. Chastel, C., Beaucournu, J. P., Chastel, O., Legrand, M. C. & Le Goff, F.(1994). A herpesvirus from an European shrew (Crocidura russula). Acta Virol 38, 309 [Google Scholar]
  11. Ciampor, F., Stancekova, M. & Blaskovic, D.(1981). Electron microscopy of rabbit embryo fibroblasts infected with herpesvirus isolates from Clethrionomys glareolus and Apodemus flavicollis. Acta Virol 25, 101–107. [Google Scholar]
  12. Clambey, E. T., Virgin, H. W., IV & Speck, S. H.(2002). Characterization of a spontaneous 9.5-kilobase-deletion mutant of murine gammaherpesvirus 68 reveals tissue-specific genetic requirements for latency. J Virol 76, 6532–6544.[CrossRef] [Google Scholar]
  13. Clarke, J. R.(1998). Voles. In UFAW Handbook on the Care and Management of Laboratory Animals. Edited by T. B. Poole. Oxford: Blackwell Scientific.
  14. Coleman, H. M., Efstathiou, S. & Stevenson, P. G.(2005). Transcription of the murine gammaherpesvirus 68 ORF73 from promoters in the viral terminal repeats. J Gen Virol 86, 561–574.[CrossRef] [Google Scholar]
  15. Cunningham, C. & Davison, A. J.(1993). A cosmid-based system for constructing mutants of herpes simplex virus type 1. Virology 197, 116–124.[CrossRef] [Google Scholar]
  16. Davison, A. J., Eberle, R., Ehlers, B., Hayward, G. S., McGeoch, D. J., Minson, A. C., Pellett, P. E., Roizman, B., Studdert, M. J. & Thiry, E.(2009). The order Herpesvirales. Arch Virol 154, 171–177.[CrossRef] [Google Scholar]
  17. Do, N. V., Ingemar, E., Phi, P. T., Jenny, A., Chinh, T. T., Zeng, Y. & Hu, L.(2008). A major EBNA1 variant from Asian EBV isolates shows enhanced transcriptional activity compared to prototype B95.8. Virus Res 132, 15–24.[CrossRef] [Google Scholar]
  18. Ebrahimi, B., Dutia, B. M., Roberts, K. L., Garcia-Ramirez, J. J., Dickinson, P., Stewart, J. P., Ghazal, P., Roy, D. J. & Nash, A. A.(2003). Transcriptome profile of murine gammaherpesvirus-68 lytic infection. J Gen Virol 84, 99–109.[CrossRef] [Google Scholar]
  19. Efstathiou, S., Minson, A. C., Field, H. J., Anderson, J. R. & Wildy, P.(1986). Detection of herpes simplex virus-specific DNA sequences in latently infected mice and in humans. J Virol 57, 446–455. [Google Scholar]
  20. Efstathiou, S., Ho, Y. M., Hall, S., Styles, C. J., Scott, S. D. & Gompels, U. A.(1990). Murine herpesvirus 68 is genetically related to the gammaherpesviruses Epstein–Barr virus and herpesvirus saimiri. J Gen Virol 71, 1365–1372.[CrossRef] [Google Scholar]
  21. Ehlers, B., Borchers, K., Grund, C., Frolich, K., Ludwig, H. & Buhk, H. J.(1999). Detection of new DNA polymerase genes of known and potentially novel herpesviruses by PCR with degenerate and deoxyinosine-substituted primers. Virus Genes 18, 211–220.[CrossRef] [Google Scholar]
  22. Ehlers, B., Kuchler, J., Yasmum, N., Dural, G., Voigt, S., Schmidt-Chanasit, J., Jakel, T., Matuschka, F. R., Richter, D. & other authors(2007). Identification of novel rodent herpesviruses, including the first gammaherpesvirus of Mus musculus. J Virol 81, 8091–8100.[CrossRef] [Google Scholar]
  23. Evans, A. G., Moorman, N. J., Willer, D. O. & Speck, S. H.(2006). The M4 gene of γHV68 encodes a secreted glycoprotein and is required for the efficient establishment of splenic latency. Virology 344, 520–531.[CrossRef] [Google Scholar]
  24. Evans, A. G., Moser, J. M., Krug, L. T., Pozharskaya, V., Mora, A. L. & Speck, S. H.(2008). A gammaherpesvirus-secreted activator of Vβ4+ CD8+ T cells regulates chronic infection and immunopathology. J Exp Med 205, 669–684.[CrossRef] [Google Scholar]
  25. Feore, S. M., Bennett, M., Chantrey, J., Jones, T., Baxby, D. & Begon, M.(1997). The effect of cowpox virus infection on fecundity in bank voles and wood mice. Proc Biol Sci 264, 1457–1461.[CrossRef] [Google Scholar]
  26. Fowler, P., Marques, S., Simas, J. P. & Efstathiou, S.(2003). ORF73 of murine herpesvirus-68 is critical for the establishment and maintenance of latency. J Gen Virol 84, 3405–3416.[CrossRef] [Google Scholar]
  27. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D. & Bairoch, A.(2003). ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31, 3784–3788.[CrossRef] [Google Scholar]
  28. Geere, H. M., Ligertwood, Y., Templeton, K. M., Bennet, I., Gangadharan, B., Rhind, S. M., Nash, A. A. & Dutia, B. M.(2006). The M4 gene of murine gammaherpesvirus 68 modulates latent infection. J Gen Virol 87, 803–807.[CrossRef] [Google Scholar]
  29. Gillet, L., May, J. S., Colaco, S. & Stevenson, P. G.(2007). The murine gammaherpesvirus-68 gp150 acts as an immunogenic decoy to limit virion neutralization. PLoS One 2, e705[CrossRef] [Google Scholar]
  30. Hamelin, C. & Lussier, G.(1992). Characterization of the DNA of rodent herpesviruses by restriction endonuclease analysis and hybridization. Lab Anim Sci 42, 142–145. [Google Scholar]
  31. Herskowitz, J. H., Siegel, A. M., Jacoby, M. A. & Speck, S. H.(2008). Systematic mutagenesis of the murine gammaherpesvirus 68 M2 protein identifies domains important for chronic infection. J Virol 82, 3295–3310.[CrossRef] [Google Scholar]
  32. Hughes, D. J., Kipar, A., Sample, J. T. & Stewart, J. P.(2010). Pathogenesis of a model gammaherpesvirus in a natural host. J Virol (Feb 3; Epub ahead of print) doi:10.1128/JVI.02085-09.. [Google Scholar]
  33. Husain, S. M., Usherwood, E. J., Dyson, H., Coleclough, C., Coppola, M. A., Woodland, D. L., Blackman, M. A., Stewart, J. P. & Sample, J. T.(1999). Murine gammaherpesvirus M2 gene is latency-associated and its protein a target for CD8+ T lymphocytes. Proc Natl Acad Sci U S A 96, 7508–7513.[CrossRef] [Google Scholar]
  34. Jacoby, M. A., Virgin, H. W., IV & Speck, S. H.(2002). Disruption of the M2 gene of murine gammaherpesvirus 68 alters splenic latency following intranasal, but not intraperitoneal, inoculation. J Virol 76, 1790–1801.[CrossRef] [Google Scholar]
  35. Kalderon, D., Oostra, B. A., Ely, B. K. & Smith, A. E.(1982). Deletion loop mutagenesis: a novel method for the construction of point mutations using deletion mutants. Nucleic Acids Res 10, 5161–5171.[CrossRef] [Google Scholar]
  36. Katoh, K. & Toh, H.(2008). Recent developments in the mafft multiple sequence alignment program. Brief Bioinform 9, 286–298.[CrossRef] [Google Scholar]
  37. Kolpakov, R., Bana, G. & Kucherov, G.(2003). mreps: efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Res 31, 3672–3678.[CrossRef] [Google Scholar]
  38. Lopes, F. B., Colaco, S., May, J. S. & Stevenson, P. G.(2004). Characterization of murine gammaherpesvirus 68 glycoprotein B. J Virol 78, 13370–13375.[CrossRef] [Google Scholar]
  39. Macakova, K., Matis, J., Rezuchova, I., Kudela, O., Raslova, H. & Kudelova, M.(2003). Murine gammaherpesvirus (MHV) M7 gene encoding glycoprotein 150 (gp150): difference in the sequence between 72 and 68 strains. Virus Genes 26, 89–95.[CrossRef] [Google Scholar]
  40. Macrae, A. I., Dutia, B. M., Milligan, S., Brownstein, D. G., Allen, D. J., Mistrikova, J., Davison, A. J., Nash, A. A. & Stewart, J. P.(2001). Analysis of a novel strain of murine gammaherpesvirus reveals a genomic locus important for acute pathogenesis. J Virol 75, 5315–5327.[CrossRef] [Google Scholar]
  41. Macrae, A. I., Usherwood, E. J., Husain, S. M., Flano, E., Kim, I. J., Woodland, D. L., Nash, A. A., Blackman, M. A., Sample, J. T. & Stewart, J. P.(2003). Murid herpesvirus 4 strain 68 M2 protein is a B-cell-associated antigen important for latency but not lymphocytosis. J Virol 77, 9700–9709.[CrossRef] [Google Scholar]
  42. Madureira, P. A., Matos, P., Soeiro, I., Dixon, L. K., Simas, J. P. & Lam, E. W.(2005). Murine gamma-herpesvirus 68 latency protein M2 binds to Vav signaling proteins and inhibits B-cell receptor-induced cell cycle arrest and apoptosis in WEHI-231 B cells. J Biol Chem 280, 37310–37318.[CrossRef] [Google Scholar]
  43. Mai, S. J., Ooka, T., Li, D. J., Zeng, M. S., Jiang, R. C., Yu, X. J., Zhang, R. H., Chen, S. P. & Zeng, Y. X.(2007). Functional advantage of NPC-related V-val subtype of Epstein–Barr virus nuclear antigen 1 compared with prototype in epithelial cell line. Oncol Rep 17, 141–146. [Google Scholar]
  44. Marques, S., Alenquer, M., Stevenson, P. G. & Simas, J. P.(2008). A single CD8+ T cell epitope sets the long-term latent load of a murid herpesvirus. PLoS Pathog 4, e1000177[CrossRef] [Google Scholar]
  45. McGeoch, D. J., Gatherer, D. & Dolan, A.(2005). On phylogenetic relationships among major lineages of the Gammaherpesvirinae. J Gen Virol 86, 307–316.[CrossRef] [Google Scholar]
  46. McGeoch, D. J., Rixon, F. J. & Davison, A. J.(2006). Topics in herpesvirus genomics and evolution. Virus Res 117, 90–104.[CrossRef] [Google Scholar]
  47. Mistríková, J., Raslova, H., Mrmusova, M. & Kudelova, M.(2000). A murine gammaherpesvirus. Acta Virol 44, 211–226. [Google Scholar]
  48. Muller, U., Steinhoff, U., Reis, L. F., Hemmi, S., Pavlovic, J., Zinkernagel, R. M. & Aguet, M.(1994). Functional role of type I and type II interferons in antiviral defense. Science 264, 1918–1921.[CrossRef] [Google Scholar]
  49. Nash, A. A., Dutia, B. M., Stewart, J. P. & Davison, A. J.(2001). Natural history of murine gamma-herpesvirus infection. Philos Trans R Soc Lond B Biol Sci 356, 569–579.[CrossRef] [Google Scholar]
  50. Oda, W., Mistrikova, J., Stancekova, M., Dutia, B. M., Nash, A. A., Takahata, H., Jin, Z., Oka, T. & Hayashi, K.(2005). Analysis of genomic homology of murine gammaherpesvirus (MHV)-72 to MHV-68 and impact of MHV-72 on the survival and tumorigenesis in the MHV-72-infected CB17scid/scid and CB17+/+ mice. Pathol Int 55, 558–568.[CrossRef] [Google Scholar]
  51. Ottinger, M., Pliquet, D., Christalla, T., Frank, R., Stewart, J. P. & Schulz, T. F.(2009). The interaction of the gammaherpesvirus 68 orf73 protein with cellular BET proteins affects the activation of cell cycle promoters. J Virol 83, 4423–4434.[CrossRef] [Google Scholar]
  52. Parry, C. M., Simas, J. P., Smith, V. P., Stewart, C. A., Minson, A. C., Efstathiou, S. & Alcami, A.(2000). A broad spectrum secreted chemokine binding protein encoded by a herpesvirus. J Exp Med 191, 573–578.[CrossRef] [Google Scholar]
  53. Pearson, W. R. & Lipman, D. J.(1988). Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A 85, 2444–2448.[CrossRef] [Google Scholar]
  54. Pfeffer, S., Zavolan, M., Grasser, F. A., Chien, M., Russo, J. J., Ju, J., John, B., Enright, A. J., Marks, D. & other authors(2004). Identification of virus-encoded microRNAs. Science 304, 734–736.[CrossRef] [Google Scholar]
  55. Pires de Miranda, M., Alenquer, M., Marques, S., Rodrigues, L., Lopes, F., Bustelo, X. R. & Simas, J. P.(2008). The gammaherpesvirus m2 protein manipulates the Fyn/Vav pathway through a multidocking mechanism of assembly. PLoS One 3, e1654[CrossRef] [Google Scholar]
  56. Raslova, H., Matis, J., Rezuchova, I., Macakova, K., Berebbi, M. & Kudelova, M.(2000). The bystander effect mediated by the new murine gammaherpesvirus 72–thymidine kinase/5′-fluoro-2′-deoxyuridine (MHV72–TK/5-FUdR) system in vitro. Antivir Chem Chemother 11, 273–282.[CrossRef] [Google Scholar]
  57. Reynolds, S. M., Kall, L., Riffle, M. E., Bilmes, J. A. & Noble, W. S.(2008). Transmembrane topology and signal peptide prediction using dynamic Bayesian networks. PLOS Comput Biol 4, e1000213[CrossRef] [Google Scholar]
  58. Rice, P., Longden, I. & Bleasby, A.(2000).emboss: the European Molecular Biology Open Software Suite. Trends Genet 16, 276–277.[CrossRef] [Google Scholar]
  59. Rodrigues, L., Pires de Miranda, M., Caloca, M. J., Bustelo, X. R. & Simas, J. P.(2006). Activation of Vav by the gammaherpesvirus M2 protein contributes to the establishment of viral latency in B lymphocytes. J Virol 80, 6123–6135.[CrossRef] [Google Scholar]
  60. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M. A. & Barrell, B.(2000). Artemis: sequence visualization and annotation. Bioinformatics 16, 944–945.[CrossRef] [Google Scholar]
  61. Simas, J. P., Swann, D., Bowden, R. & Efstathiou, S.(1999). Analysis of murine gammaherpesvirus-68 transcription during lytic and latent infection. J Gen Virol 80, 75–82. [Google Scholar]
  62. Simas, J. P., Marques, S., Bridgeman, A., Efstathiou, S. & Adler, H.(2004). The M2 gene product of murine gammaherpesvirus 68 is required for efficient colonization of splenic follicles but is not necessary for expansion of latently infected germinal centre B cells. J Gen Virol 85, 2789–2797.[CrossRef] [Google Scholar]
  63. Stewart, J. P., Usherwood, E. J., Ross, A., Dyson, H. & Nash, T.(1998). Lung epithelial cells are a major site of murine gammaherpesvirus persistence. J Exp Med 187, 1941–1951.[CrossRef] [Google Scholar]
  64. Sunil-Chandra, N. P., Efstathiou, S., Arno, J. & Nash, A. A.(1992). Virological and pathological features of mice infected with murine gamma-herpesvirus 68. J Gen Virol 73, 2347–2356.[CrossRef] [Google Scholar]
  65. Svobodova, J., Blaskovic, D. & Mistrikova, J.(1982). Growth characteristics of herpesviruses isolated from free living small rodents. Acta Virol 26, 256–263. [Google Scholar]
  66. Taylor, P.(1986). A computer program for translating DNA sequences into protein. Nucleic Acids Res 14, 437–441.[CrossRef] [Google Scholar]
  67. Thompson, J. D., Higgins, D. G. & Gibson, T. J.(1994).clustalw: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef] [Google Scholar]
  68. Todaro, G. J. & Green, H.(1963). Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol 17, 299–313.[CrossRef] [Google Scholar]
  69. Usherwood, E. J., Roy, D. J., Ward, K., Surman, S. L., Dutia, B. M., Blackman, M. A., Stewart, J. P. & Woodland, D. L.(2000). Control of gammaherpesvirus latency by latent antigen-specific CD8+ T cells. J Exp Med 192, 943–952.[CrossRef] [Google Scholar]
  70. van Berkel, V., Preiter, K., Virgin, H. W. & Speck, S. H.(1999). Identification and initial characterization of the murine gammaherpesvirus 68 gene M3, encoding an abundantly secreted protein. J Virol 73, 4524–4529. [Google Scholar]
  71. van Berkel, V., Barrett, J., Tiffany, H. L., Fremont, D. H., Murphy, P. M., McFadden, G., Speck, S. H. & Virgin, H. W.(2000). Identification of a gammaherpesvirus selective chemokine binding protein that inhibits chemokine action. J Virol 74, 6741–6747.[CrossRef] [Google Scholar]
  72. van Berkel, V., Levine, B., Kapadia, S. B., Goldman, J. E., Speck, S. H. & Virgin, H. W., IV(2002). Critical role for a high-affinity chemokine-binding protein in gamma-herpesvirus-induced lethal meningitis. J Clin Invest 109, 905–914.[CrossRef] [Google Scholar]
  73. Virgin, H. W., Latreille, P., Wamsley, P., Hallsworth, K., Weck, K. E., Dal Canto, A. J. & Speck, S. H.(1997). Complete sequence and genomic analysis of murine gammaherpesvirus 68. J Virol 71, 5894–5904. [Google Scholar]
  74. Virgin, H. W., Presti, R. M., Li, X. Y., Liu, C. & Speck, S. H.(1999). Three distinct regions of the murine gammaherpesvirus 68 genome are transcriptionally active in latently infected mice. J Virol 73, 2321–2332. [Google Scholar]
  75. Wang, J. T., Sheeng, T. S., Su, I. J., Chen, J. Y. & Chen, M. R.(2003). EBNA-1 sequence variations reflect active EBV replication and disease status or quiescent latency in lymphocytes. J Med Virol 69, 417–425.[CrossRef] [Google Scholar]
  76. Wrightham, M. N., Stewart, J. P., Janjua, N. J., Pepper, S. D., Sample, C., Rooney, C. M. & Arrand, J. R.(1995). Antigenic and sequence variation in the C-terminal unique domain of the Epstein–Barr virus nuclear antigen EBNA-1. Virology 208, 521–530.[CrossRef] [Google Scholar]
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