Primate Models for Gammaherpesvirus-Associated Malignancies

  • Ilhem Messaoudi
  • Blossom Damania
  • Scott W. Wong


Non-human primates (NHP) represent an invaluable resource for elucidating and understanding disease processes in humans, as humans and NHP share close developmental, physiological and evolutionary relationships (Hendrickx and Binkerd 1990). For infectious disease research, NHP have historically played an important role as they are either susceptible to infectious agents that cause disease in humans (Kirschstein et al. 1960) or harbor infectious agents that are closely related to those that infect and cause disease in humans (Wenner et al. 1975). For example, NHP harbor herpesviruses that have co-evolved with their hosts and are genetically more closely related to human herpesviruses than other mammalian herpesviruses. More importantly, these simian herpesvirus homologues, which include alpha (α), beta (β) and gamma(γ)herpesviruses, are capable of causing similar, if not identical, disease manifestations in their natural host, which makes them excellent models to dissect...


Rhesus Macaque Simian Immunodeficiency Virus Squirrel Monkey World Monkey World Primate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Albrecht, J. C. (2000) Primary structure of the Herpesvirus ateles genome. J Virol. 74, 1033–1037.PubMedGoogle Scholar
  2. Albrecht, J. C., Friedrich, U., Kardinal, C., Koehn, J., Fleckenstein, B., Feller, S. M. and Biesinger, B. (1999) Herpesvirus ateles gene product Tio interacts with nonreceptor protein tyrosine kinases. J Virol. 73, 4631–4639.PubMedGoogle Scholar
  3. Albrecht, J. C., Nicholas, J., Biller, D., Cameron, K. R., Biesinger, B., Newman, C., Wittmann, S., Craxton, M. A., Coleman, H., Fleckenstein, B. and et al. (1992) Primary structure of the herpesvirus saimiri genome. J Virol. 66, 5047–5058.PubMedGoogle Scholar
  4. Alexander, L., Denekamp, L., Knapp, A., Auerbach, M. R., Damania, B. and Desrosiers, R. C. (2000) The primary sequence of rhesus monkey rhadinovirus isolate 26-95: sequence similarities to Kaposi’s sarcoma-associated herpesvirus and rhesus monkey rhadinovirus isolate 17577. J Virol. 74, 3388–3398.PubMedGoogle Scholar
  5. AuCoin, D. P., Colletti, K. S., Xu. Y., Cei, S. A., Pari, G. S. (2002) Kaposi’s sarcoma-associated herpesvirus (human herpesvirus 8) contains two functional lytic origins of DNA replication. J Virol. 76, 7890–7896.Google Scholar
  6. Baskin, G. B., Roberts, E. D., Kuebler, D., Martin, L. N., Blauw, B., Heeney, J. and Zurcher, C. (1995) Squamous epithelial proliferative lesions associated with rhesus Epstein-Barr virus in simian immunodeficiency virus-infected rhesus monkeys. J Infect Dis. 172, 535–539.PubMedGoogle Scholar
  7. Bellows, D. S., Chau, B. N., Lee, P., Lazebnik, Y., Burns, W. H. and Hardwick, J. M. (2000) Antiapoptotic herpesvirus Bcl-2 homologs escape caspase-mediated conversion to proapoptotic proteins. J Virol. 74, 5024–5031.PubMedGoogle Scholar
  8. Berend, K. R., Jung, J. U., Boyle, T. J., DiMaio, J. M., Mungal, S. A., Desrosiers, R. C. and Lyerly, H. K. (1993) Phenotypic and functional consequences of herpesvirus saimiri infection of human CD8+ cytotoxic T lymphocytes. J Virol. 67, 6317–6321.PubMedGoogle Scholar
  9. Bergquam, E. P., Avery, N., Shiigi, S. M., Axthelm, M. K. and Wong, S. W. (1999) Rhesus rhadinovirus establishes a latent infection in B lymphocytes in vivo. J Virol. 73, 7874-7876.PubMedGoogle Scholar
  10. Biesinger, B., Muller-Fleckenstein, I., Simmer, B., Lang, G., Wittmann, S., Platzer, E., Desrosiers, R. C. and Fleckenstein, B. (1992) Stable growth transformation of human T lymphocytes by herpesvirus saimiri. Proc Natl Acad Sci U S A. 89, 3116–3119.PubMedGoogle Scholar
  11. Biesinger, B., Trimble, J. J., Desrosiers, R. C. and Fleckenstein, B. (1990) The divergence between two oncogenic Herpesvirus saimiri strains in a genomic region related to the transforming phenotype. Virology. 176, 505–514.PubMedGoogle Scholar
  12. Biesinger, B., Tsygankov, A. Y., Fickenscher, H., Emmrich, F., Fleckenstein, B., Bolen, J. B. and Broker, B. M. (1995) The product of the Herpesvirus saimiri open reading frame 1 (tip) interacts with T cell-specific kinase p56lck in transformed cells. J Biol Chem. 270, 4729–4734.PubMedGoogle Scholar
  13. Bilello, J. P., Morgan, J. S., Damania, B., Lang, S. M. and Desrosiers, R. C. (2006) A genetic system for rhesus monkey rhadinovirus: use of recombinant virus to quantitate antibody-mediated neutralization. J Virol. 80, 1549–1562.PubMedGoogle Scholar
  14. Blake, N. W., Moghaddam, A., Rao, P., Kaur, A., Glickman, R., Cho, Y. G., Marchini, A., Haigh, T., Johnson, R. P., Rickinson, A. B. and Wang, F. (1999) Inhibition of antigen presentation by the glycine/alanine repeat domain is not conserved in simian homologues of Epstein-Barr virus nuclear antigen 1. J Virol. 73, 7381–7389.PubMedGoogle Scholar
  15. Bosch, M. L., Harper, E., Schmidt, A., Strand, K. B., Thormahlen, S., Thouless, M. E. and Wang, Y. (1999) Activation in vivo of retroperitoneal fibromatosis-associated herpesvirus, a simian homologue of human herpesvirus-8. J Gen Virol. 80, 467–475.PubMedGoogle Scholar
  16. Brinkmann, M. M. and Schulz, T. F. (2006) Regulation of intracellular signalling by the terminal membrane proteins of members of the Gammaherpesvirinae. J Gen Virol. 87, 1047–1074.PubMedGoogle Scholar
  17. Bueno, C., Criado, G., McCormick, J. K., Madrenas, J. (2007) T cell signalling induced by bacterial superantigens. Chem Immunol Allergy. 93, 161–80.Google Scholar
  18. Cai, X., Schafer, A., Lu, S., Bilello, J. P., Desrosiers, R. C., Edwards, R., Raab-Traub, N. and Cullen, B. R. (2006) Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. 2, e23.PubMedGoogle Scholar
  19. Calderwood, M. A., Hall, K. T., Matthews, D. A. and Whitehouse, A. (2004) The herpesvirus saimiri ORF73 gene product interacts with host-cell mitotic chromosomes and self-associates via its C terminus. J Gen Virol. 85, 147–153.PubMedGoogle Scholar
  20. Cho, Y., Ramer, J., Rivailler, P., Quink, C., Garber, R. L., Beier, D. R. and Wang, F. (2001) An Epstein-Barr-related herpesvirus from marmoset lymphomas. Proc Natl Acad Sci U S A. 98, 1224–1229.PubMedGoogle Scholar
  21. Cho, Y. G., Gordadze, A. V., Ling, P. D. and Wang, F. (1999) Evolution of two types of rhesus lymphocryptovirus similar to type 1 and type 2 Epstein-Barr virus. J Virol. 73, 9206–9212.PubMedGoogle Scholar
  22. Choi, J. K., Ishido, S. and Jung, J. U. (2000) The collagen repeat sequence is a determinant of the degree of herpesvirus saimiri STP transforming activity. J Virol. 74, 8102–8110.PubMedGoogle Scholar
  23. Cleary, M. L., Epstein, M. A., Finerty, S., Dorfman, R. F., Bornkamm, G. W., Kirkwood, J. K., Morgan, A. J. and Sklar, J. (1985) Individual tumors of multifocal EB virus-induced malignant lymphomas in tamarins arise from different B-cell clones. Science. 228, 722–724.PubMedGoogle Scholar
  24. Dalbies-Tran, R., Stigger-Rosser, E., Dotson, T. and Sample, C. E. (2001) Amino acids of Epstein-Barr virus nuclear antigen 3A essential for repression of Jkappa-mediated transcription and their evolutionary conservation. J Virol. 75, 90–99.PubMedGoogle Scholar
  25. Damania, B., DeMaria, M., Jung, J. U. and Desrosiers, R. C. (2000) Activation of lymphocyte signaling by the R1 protein of rhesus monkey rhadinovirus. J Virol. 74, 2721–2730.PubMedGoogle Scholar
  26. Damania, B., Li, M., Choi, J. K., Alexander, L., Jung, J. U. and Desrosiers, R. C. (1999) Identification of the R1 oncogene and its protein product from the rhadinovirus of rhesus monkeys. J Virol. 73, 5123–5131.PubMedGoogle Scholar
  27. Dambaugh, T., Beisel, C., Hummel, M., King, W., Fennewald, S., Cheung, A., Heller, M., Raab-Traub, N. and Kieff, E. (1980) Epstein-Barr virus (B95-8) DNA VII: molecular cloning and detailed mapping. Proc Natl Acad Sci U S A. 77, 2999–3003.PubMedGoogle Scholar
  28. Dambaugh, T., Hennessy, K., Chamnankit, L. and Kieff, E. (1984) U2 region of Epstein-Barr virus DNA may encode Epstein-Barr nuclear antigen 2. Proc Natl Acad Sci U S A. 81, 7632–7636.PubMedGoogle Scholar
  29. Daniel, M. D., Hunt, R. D., Dubose, D., Silva, D. and Melendez, L. V. (1975) Induction of herpesvirus saimiri lymphoma in New Zealand white rabbits inoculated intravenously. IARC scientific publications. 205–208.Google Scholar
  30. De Carli, M., Berthold, S., Fickenscher, H., Fleckenstein, I. M., D’Elios, M. M., Gao, Q., Biagiotti, R., Giudizi, M. G., Kalden, J. R., Fleckenstein, B. and et al. (1993) Immortalization with herpesvirus saimiri modulates the cytokine secretion profile of established Th1 and Th2 human T cell clones. J Immunol. 151, 5022–5030.PubMedGoogle Scholar
  31. de Thoisy, B., Pouliquen, J. F., Lacoste, V., Gessain, A. and Kazanji, M. (2003) Novel gamma-1 herpesviruses identified in free-ranging new world monkeys (golden-handed tamarin [Saguinus midas], squirrel monkey [Saimiri sciureus], and white-faced saki [Pithecia pithecia]) in French Guiana. J Virol. 77, 9099–9105.PubMedGoogle Scholar
  32. Derfuss, T., Fickenscher, H., Kraft, M. S., Henning, G., Lengenfelder, D., Fleckenstein, B. and Meinl, E. (1998) Antiapoptotic activity of the herpesvirus saimiri-encoded Bcl-2 homolog: stabilization of mitochondria and inhibition of caspase-3-like activity. J Virol. 72, 5897–5904.PubMedGoogle Scholar
  33. Desgranges, C., Lenoir, G., de-The, G., Seigneurin, J. M., Hilgers, J. and Dubouch, P. (1976) In vitro transforming activity of EBV. I-Establishment and properties of two EBV strains (M81 and M72) produced by immortalized Callithrix jacchus lymphocytes. Biomedicine. 25, 349–352.PubMedGoogle Scholar
  34. Desrosiers, R. C., Bakker, A., Kamine, J., Falk, L. A., Hunt, R. D. and King, N. W. (1985) A region of the Herpesvirus saimiri genome required for oncogenicity. Science. 228, 184–187.PubMedGoogle Scholar
  35. Desrosiers, R. C. and Falk, L. A. (1982) Herpesvirus saimiri strain variability. J Virol. 43, 352–356.PubMedGoogle Scholar
  36. Desrosiers, R. C., Mulder, C. and Fleckenstein, B. (1979) Methylation of Herpesvirus saimiri DNA in lymphoid tumor cell lines. Proc Natl Acad Sci U S A. 76, 3839–3843.PubMedGoogle Scholar
  37. Desrosiers, R. C., Sasseville, V. G., Czajak, S. C., Zhang, X., Mansfield, K. G., Kaur, A., Johnson, R. P., Lackner, A. A. and Jung, J. U. (1997) A herpesvirus of rhesus monkeys related to the human Kaposi sarcoma-associated herpesvirus. J. Virol. 71, 9764–9769.PubMedGoogle Scholar
  38. DeWire, S. M. and Damania, B. (2005) The latency-associated nuclear antigen of rhesus monkey rhadinovirus inhibits viral replication through repression of Orf50/Rta transcriptional activation. J Virol. 79, 3127–3138.PubMedGoogle Scholar
  39. DeWire, S. M., McVoy, M. A. and Damania, B. (2002) Kinetics of expression of rhesus monkey rhadinovirus (RRV) and identification and characterization of a polycistronic transcript encoding the RRV Orf50/Rta, RRV R8, and R8.1 genes. J Virol. 76, 9819–9831.PubMedGoogle Scholar
  40. Duboise, M., Guo, J., Czajak, S., Lee, H., Veazey, R., Desrosiers, R. C. and Jung, J. U. (1998) A role for herpesvirus saimiri orf14 in transformation and persistent infection. J Virol. 72, 6770–6776.PubMedGoogle Scholar
  41. Duboise, S. M., Lee, H., Guo, J., Choi, J. K., Czajak, S., Simon, M., Desrosiers, R. C. and Jung, J. U. (1998) Mutation of the Lck-binding motif of Tip enhances lymphoid cell activation by herpesvirus saimiri. J Virol. 72, 2607–2614.PubMedGoogle Scholar
  42. Dunkel, V. C., Pry, T. W., Henle, G. and Henle, W. (1972) Immunofluorescence tests for antibodies to Epstein-Barr virus with sera of lower primates. J Natl Cancer Inst. 49, 435–440.PubMedGoogle Scholar
  43. Ehlers, B., Ochs, A., Leendertz, F., Goltz, M., Boesch, C. and Matz-Rensing, K. (2003) Novel simian homologues of Epstein-Barr virus. J Virol. 77, 10695–10699.PubMedGoogle Scholar
  44. Eliopoulos, A. G. and Young, L. S. (1998) Activation of the cJun N-terminal kinase (JNK) pathway by the Epstein- Barr virus-encoded latent membrane protein 1 (LMP1). Oncogene. 16, 1731–1742.PubMedGoogle Scholar
  45. Ensser, A. and Fleckenstein, B. (2005) T-cell transformation and oncogenesis by gamma2-herpesviruses. Adv Cancer Res. 93, 91–128.PubMedGoogle Scholar
  46. Ensser, A., Thurau, M., Wittmann, S. and Fickenscher, H. (2003) The genome of herpesvirus saimiri C488 which is capable of transforming human T cells. Virology. 314, 471–487.PubMedGoogle Scholar
  47. Epstein, M. A., Hunt, R. D. and Rabin, H. (1973a) Pilot experiments with EB virus in owl monkeys (Aotus trivirgatus). I Reticuloproliferative disease in an inoculated animal. Int J Cancer. 12, 309–318.Google Scholar
  48. Epstein, M. A., Rabin, H., Ball, G., Rickinson, A. B., Jarvis, J. and Melendez, L. V. (1973b) Pilot experiments with EB virus in owl monkeys (Aotus trivirgatus). II. EB virus in a cell line from an animal with reticuloproliferative disease. Int J Cancer. 12, 319–332.Google Scholar
  49. Estep, R. D., Axthelm, M. K. and Wong, S. W. (2003) A G Protein-Coupled Receptor Encoded by Rhesus Rhadinovirus Is Similar to ORF74 of Kaposi’s Sarcoma-Associated Herpesvirus. J Virol. 77, 1738–1746.PubMedGoogle Scholar
  50. Estep, R. D., Powers, M. F., Yen, B. K., Li, H. and Wong, S. W. (2007) Construction of an infectious rhesus rhadinovirus bacterial artificial chromosome for the analysis of Kaposi’s sarcoma-associated herpesvirus-related disease development. J Virol. 81, 2957–2969.PubMedGoogle Scholar
  51. Falk, L. A., Henle, G., Henle, W., Deinhardt, F. and Schudel, A. (1977) Transformation of lymphocytes by Herpesvirus papio. Int J Cancer. 20, 219–226.PubMedGoogle Scholar
  52. Falk, L. A., Wolfe, L. G. and Deinhardt, F. (1972) Isolation of Herpesvirus saimiri from blood of squirrel monkeys (Saimiri sciureus). J Natl Cancer Inst. 48, 1499–1505.PubMedGoogle Scholar
  53. Faucher, S., Dimock, K. and Wright, K. E. (2002) Characterization of the Cyno-EBV LMP1 homologue and comparison with LMP1s of EBV and other EBV-like viruses. Virus Res. 90, 63–75.PubMedGoogle Scholar
  54. Feichtinger, H., Kaaya, E., Putkonen, P., Li, S. L., Ekman, M., Gendelman, R., Biberfeld, G. and Biberfeld, P. (1992a) Malignant lymphoma associated with human AIDS and with SIV-induced immunodeficiency in macaques. AIDS Res Hum Retroviruses. 8, 339–348.Google Scholar
  55. Feichtinger, H., Li, S. L., Kaaya, E., Putkonen, P., Grunewald, K., Weyrer, K., Bottiger, D., Ernberg, I., Linde, A., Biberfeld, G. and et al. (1992b) A monkey model for Epstein Barr virus-associated lymphomagenesis in human acquired immunodeficiency syndrome. J Exp Med. 176, 281–286.Google Scholar
  56. Fickenscher, H., Bokel, C., Knappe, A., Biesinger, B., Meinl, E., Fleischer, B., Fleckenstein, B. and Broker, B. M. (1997) Functional phenotype of transformed human alphabeta and gammadelta T cells determined by different subgroup C strains of herpesvirus Saimiri. J Virol. 71, 2252–2263.PubMedGoogle Scholar
  57. Fickenscher, H. and Fleckenstein, B. (2001) Herpesvirus saimiri. Philos Trans R Soc Lond B Biol Sci. 356, 545–567.PubMedGoogle Scholar
  58. Fodor, W. L., Rollins, S. A., Bianco-Caron, S., Rother, R. P., Guilmette, E. R., Burton, W. V., Albrecht, J. C., Fleckenstein, B., Squinto, S. P. (1995) The complement control protein homolog of herpesvirus saimiri regulates serum complement by inhibiting C3 convertase activity. J Virol. 69(6), 3889–92.Google Scholar
  59. Foster-Cuevas, M., Wright, G. J., Puklavec, M. J., Brown, M. H. and Barclay, A. N. (2004) Human herpesvirus 8 K14 protein mimics CD200 in down-regulating macrophage activation through CD200 receptor. J Virol. 78, 7667–7676.PubMedGoogle Scholar
  60. Frank, A., Andiman, W. A. and Miller, G. (1976) Epstein-Barr virus and nonhuman primates: natural and experimental infection. Adv Cancer Res. 23, 171–201.PubMedGoogle Scholar
  61. Franken, M., Devergne, O., Rosenzweig, M., Annis, B., Kieff, E. and Wang, F. (1996) Comparative analysis identifies conserved tumor necrosis factor receptor-associated factor 3 binding sites in the human and simian Epstein-Barr virus oncogene LMP1. J Virol. 70, 7819–7826.PubMedGoogle Scholar
  62. Gerber, P., Branch, J. W. and Rosenblum, E. N. (1969) Attempts to transmit infectious mononucleosis to rhesus monkeys and marmosets and to isolate herpes-like virus. Proc Soc Exp Biol Med. 130, 14–19.PubMedGoogle Scholar
  63. Gerber, P., Kalter, S. S., Schidlovsky, G., Peterson, W. D., Jr. and Daniel, M. D. (1977) Biologic and antigenic characteristics of Epstein-Barr virus-related Herpesviruses of chimpanzees and baboons. Int J Cancer. 20, 448–459.PubMedGoogle Scholar
  64. Giddens, W. E., Jr., Tsai, C. C., Morton, W. R., Ochs, H. D., Knitter, G. H. and Blakley, G. A. (1985) Retroperitoneal fibromatosis and acquired immunodeficiency syndrome in macaques. Pathologic observations and transmission studies. Am J Pathol. 119, 253–263.PubMedGoogle Scholar
  65. Goodwin, D. J., Hall, K. T., Giles, M. S., Calderwood, M. A., Markham, A. F. and Whitehouse, A. (2000) The carboxy terminus of the herpesvirus saimiri ORF 57 gene contains domains that are required for transactivation and transrepression. J Gen Virol. 81, 2253–2265.PubMedGoogle Scholar
  66. Goodwin, D. J., Hall, K. T., Stevenson, A. J., Markham, A. F. and Whitehouse, A. (1999) The open reading frame 57 gene product of herpesvirus saimiri shuttles between the nucleus and cytoplasm and is involved in viral RNA nuclear export. J Virol. 73, 10519–10524.PubMedGoogle Scholar
  67. Greensill, J., Sheldon, J. A., Murthy, K. K., Bessonette, J. S., Beer, B. E. and Schulz, T. F. (2000a) A chimpanzee rhadinovirus sequence related to Kaposi’s sarcoma-associated herpesvirus/human herpesvirus 8: increased detection after HIV-1 infection in the absence of disease. AIDS. 14, F129–135.Google Scholar
  68. Greensill, J., Sheldon, J. A., Renwick, N. M., Beer, B. E., Norley, S., Goudsmit, J. and Schulz, T. F. (2000b) Two distinct gamma-2 herpesviruses in African green monkeys: a second gamma-2 herpesvirus lineage among old world primates? J Virol. 74, 1572–1577.Google Scholar
  69. Hall, K. T., Giles, M. S., Goodwin, D. J., Calderwood, M. A., Markham, A. F. and Whitehouse, A. (2000) Characterization of the herpesvirus saimiri ORF73 gene product. J Gen Virol. 81, 2653–2658.PubMedGoogle Scholar
  70. Hendrickx, A. G. and Binkerd, P. E. (1990) Nonhuman primates and teratological research. J Med Primatol. 19, 81–108.PubMedGoogle Scholar
  71. Hor, S., Ensser, A., Reiss, C., Ballmer-Hofer, K. and Biesinger, B. (2001) Herpesvirus saimiri protein StpB associates with cellular Src. J Gen Virol. 82, 339–344.PubMedGoogle Scholar
  72. Ishida, T. and Yamamoto, K. (1987) Survey of nonhuman primates for antibodies reactive with Epstein-Barr virus (EBV) antigens and susceptibility of their lymphocytes for immortalization with EBV. J Med Primatol. 16, 359–371.PubMedGoogle Scholar
  73. Jenson, H. B., Ench, Y., Zhang, Y., Gao, S. J., Arrand, J. R. and Mackett, M. (2002) Characterization of an Epstein-Barr virus-related gammaherpesvirus from common marmoset (Callithrix jacchus). J Gen Virol. 83, 1621–1633.PubMedGoogle Scholar
  74. Jiang, H., Cho, Y. G. and Wang, F. (2000) Structural, functional, and genetic comparisons of Epstein-Barr virus nuclear antigen 3A, 3B, and 3C homologues encoded by the rhesus lymphocryptovirus. J Virol. 74, 5921–5932.PubMedGoogle Scholar
  75. Johnson, D. R., Wolfe, L. G., Levan, G., Klein, G., Ernberg, I. and Aman, P. (1983) Epstein-Barr virus (EBV)-induced lymphoproliferative disease in cotton-topped marmosets. Int J Cancer. 31, 91–97.PubMedGoogle Scholar
  76. Jung, J. U. and Desrosiers, R. C. (1995) Association of the viral oncoprotein STP-C488 with cellular ras. Molecular and cellular biology. 15, 6506–6512.PubMedGoogle Scholar
  77. Jung, J. U., Lang, S. M., Friedrich, U., Jun, T., Roberts, T. M., Desrosiers, R. C. and Biesinger, B. (1995a) Identification of Lck-binding elements in tip of herpesvirus saimiri. J Biol Chem. 270, 20660–20667.Google Scholar
  78. Jung, J. U., Lang, S. M., Jun, T., Roberts, T. M., Veillette, A. and Desrosiers, R. C. (1995b) Downregulation of Lck-mediated signal transduction by tip of herpesvirus saimiri. J Virol. 69, 7814–7822.Google Scholar
  79. Jung, J. U., Stager, M. and Desrosiers, R. C. (1994) Virus-encoded cyclin. Molecular and cellular biology. 14, 7235–7244.PubMedGoogle Scholar
  80. Jung, J. U., Trimble, J. J., King, N. W., Biesinger, B., Fleckenstein, B. W., Desrosiers, R. C. (1991) Identification of transforming genes of subgroup A and C strains of Herpesvirus saimiri. Proc Natl Acad Sci USA. 15;88(16), 7051–5.Google Scholar
  81. Kaleeba, J. A., Bergquam, E. P. and Wong, S. W. (1999) A rhesus macaque rhadinovirus related to Kaposi’s sarcoma-associated Herpesvirus/Human herpesvirus 8 encodes a functional homologue of interleukin-6. J Virol. 73, 6177–6181.PubMedGoogle Scholar
  82. Kalter, S. S., Heberling, R. L. and Ratner, J. J. (1972) EBV antibody in sera of non-human primates. Nature. 238, 353–354.PubMedGoogle Scholar
  83. Kapadia, S. B., Levine, B., Speck, S. H. and Virgin, H. W. t. (2002) Critical role of complement and viral evasion of complement in acute, persistent, and latent gamma-herpesvirus infection. Immunity. 17, 143–155.PubMedGoogle Scholar
  84. Kaschka-Dierich, C., Werner, F. J., Bauer, I. and Fleckenstein, B. (1982) Structure of nonintegrated, circular Herpesvirus saimiri and Herpesvirus ateles genomes in tumor cell lines and in vitro-transformed cells. J Virol. 44, 295–310.PubMedGoogle Scholar
  85. Kirschstein, R., Baron, S., Borman, G. S., Murray, R., Perkins, F. T. and Hottle, G. (1960) Neurovirulence of attenuated type 1 poliovirus vaccine strains after intramuscular inoculation of rhesus monkeys. Virology. 11, 300–302.PubMedGoogle Scholar
  86. Knappe, A., Feldmann, G., Dittmer, U., Meinl, E., Nisslein, T., Wittmann, S., Matz-Rensing, K., Kirchner, T., Bodemer, W. and Fickenscher, H. (2000) Herpesvirus saimiri-transformed macaque T cells are tolerated and do not cause lymphoma after autologous reinfusion. Blood. 95, 3256–3261.PubMedGoogle Scholar
  87. Knappe, A., Hiller, C., Thurau, M., Wittmann, S., Hofmann, H., Fleckenstein, B. and Fickenscher, H. (1997) The superantigen-homologous viral immediate-early gene ie14/vsag in herpesvirus saimiri-transformed human T cells. J Virol. 71, 9124–9133.PubMedGoogle Scholar
  88. Koomey, J. M., Mulder, C., Burghoff, R. L., Fleckenstein, B. and Desrosiers, R. C. (1984) Deletion of DNA sequence in a nononcogenic variant of Herpesvirus saimiri. J Virol. 50, 662–665.PubMedGoogle Scholar
  89. Lacoste, V., Mauclere, P., Dubreuil, G., Lewis, J., Georges-Courbot, M. C. and Gessain, A. (2000) KSHV-like herpesviruses in chimps and gorillas. Nature. 407, 151–152.PubMedGoogle Scholar
  90. Landon, J. C. and Malan, L. B. (1971) Seroepidemiologic studies of Epstein-Barr virus antibody in monkeys. J Natl Cancer Inst. 46, 881–884.PubMedGoogle Scholar
  91. Langlais, C. L., Jones, J. M., Estep, R. D. and Wong, S. W. (2006) Rhesus rhadinovirus R15 encodes a functional homologue of human CD200. J Virol. 80, 3098–3103.PubMedGoogle Scholar
  92. Lee, S. H., Chung, Y. H., Cho, N. H., Gwack, Y., Feng, P. and Jung, J. U. (2004) Modulation of T-cell receptor signal transduction by herpesvirus signaling adaptor protein. Molecular and cellular biology. 24, 5369–5382.PubMedGoogle Scholar
  93. Levine, P. H., Leiseca, S. A., Hewetson, J. F., Traul, K. A., Andrese, A. P., Granlund, D. J., Fabrizio, P. and Stevens, D. A. (1980) Infection of rhesus monkeys and chimpanzees with Epstein-Barr virus. Arch Virol. 66, 341–351.PubMedGoogle Scholar
  94. Levitskaya, J., Coram, M., Levitsky, V., Imreh, S., Steigerwald-Mullen, P. M., Klein, G., Kurilla, M. G. and Masucci, M. G. (1995) Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature. 375, 685–688.PubMedGoogle Scholar
  95. Levy, J. A., Levy, S. B., Hirshaut, Y., Kafuko, G. and Prince, A. (1971) Presence of EBV antibodies in sera from wild chimpanzees. Nature. 233, 559–560.PubMedGoogle Scholar
  96. Lin, S. F., Robinson, D. R., Oh, J., Jung, J. U., Luciw, P. A. and Kung, H. J. (2002) Identification of the bZIP and Rta homologues in the genome of rhesus monkey rhadinovirus. Virology. 298, 181–188.PubMedGoogle Scholar
  97. Ling, P. D. and Hayward, S. D. (1995) Contribution of conserved amino acids in mediating the interaction between EBNA2 and CBF1/RBPJk. J Virol. 69, 1944–1950.PubMedGoogle Scholar
  98. Ling, P. D., Ryon, J. J. and Hayward, S. D. (1993) EBNA-2 of herpesvirus papio diverges significantly from the type A and type B EBNA-2 proteins of Epstein-Barr virus but retains an efficient transactivation domain with a conserved hydrophobic motif. J Virol. 67, 2990–3003.PubMedGoogle Scholar
  99. Lund, T. C., Prator, P. C., Medveczky, M. M. and Medveczky, P. G. (1999) The Lck binding domain of herpesvirus saimiri tip-484 constitutively activates Lck and STAT3 in T cells. J Virol. 73, 1689–1694.PubMedGoogle Scholar
  100. Mansfield, K. G., Westmoreland, S. V., DeBakker, C. D., Czajak, S., Lackner, A. A. and Desrosiers, R. C. (1999) Experimental infection of rhesus and pig-tailed macaques with macaque rhadinoviruses. J Virol. 73, 10320–10328.PubMedGoogle Scholar
  101. Marechal, V., Dehee, A., Chikhi-Brachet, R., Piolot, T., Coppey-Moisan, M. and Nicolas, J. C. (1999) Mapping EBNA-1 domains involved in binding to metaphase chromosomes. J Virol. 73, 4385–4392.PubMedGoogle Scholar
  102. Mark, L., Spiller, O. B., Okroj, M., Chanas, S., Aitken, J. A., Wong, S. W., Damania, B., Blom, A. M. and Blackbourn, D. J. (2007) Molecular Characterization of the Rhesus Rhadinovirus (RRV) ORF4 Gene and the RRV Complement Control Protein It Encodes. J Virol. 81, 4166–4176.PubMedGoogle Scholar
  103. Melendez, L. V., Daniel, M. D., Hunt, R. D. and Garcia, F. G. (1968) An apparently new herpesvirus from primary kidney cultures of the squirrel monkey (Saimiri sciureus). Laboratory animal care. 18, 374–381.PubMedGoogle Scholar
  104. Melendez, L. V., Hunt, R. D., King, N. W., Barahona, H. H., Daniel, M. D., Fraser, C. E. and Garcia, F. G. (1972) Herpesvirus ateles, a new lymphoma virus of monkeys. Nature: New biology. 235, 182–184.Google Scholar
  105. Miller, G., Niederman, J. C. and Stitt, D. A. (1972) Infectious mononucleosis: appearance of neutralizing antibody to Epstein-Barr virus measured by inhibition of formation of lymphoblastoid cell lines. J Infect Dis. 125, 403–406.PubMedGoogle Scholar
  106. Miller, G., Shope, T., Coope, D., Waters, L., Pagano, J., Bornkamn, G. and Henle, W. (1977) Lymphoma in cotton-top marmosets after inoculation with Epstein-Barr virus: tumor incidence, histologic spectrum antibody responses, demonstration of viral DNA, and characterization of viruses. J Exp Med. 145, 948–967.PubMedGoogle Scholar
  107. Moghaddam, A., Koch, J., Annis, B. and Wang, F. (1998) Infection of human B lymphocytes with lymphocryptoviruses related to Epstein-Barr virus. J Virol. 72, 3205–3212.PubMedGoogle Scholar
  108. Moghaddam, A., Rosenzweig, M., Lee-Parritz, D., Annis, B., Johnson, R. P. and Wang, F. (1997) An animal model for acute and persistent Epstein-Barr virus infection. Science. 276, 2030–2033.PubMedGoogle Scholar
  109. Mohle, R., Green, D., Moore, M. A., Nachman, R. L. and Rafii, S. (1997) Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc Natl Acad Sci U S A. 94, 663–668.PubMedGoogle Scholar
  110. Naito, M., Ono, K., Doi, T., Kato, S. and Tanabe, S. (1971) Antibodies in human and monkey sera to herpes-type virus from a chicken with Marek’s disease and to EB virus detected by the immunofluorescence test. Biken J. 14, 161–166.PubMedGoogle Scholar
  111. Nava, V. E., Cheng, E. H., Veliuona, M., Zou, S., Clem, R. J., Mayer, M. L. and Hardwick, J. M. (1997) Herpesvirus saimiri encodes a functional homolog of the human bcl-2 oncogene. J Virol. 71, 4118–4122.PubMedGoogle Scholar
  112. Nicholas, J., Cameron, K. R. and Honess, R. W. (1992) Herpesvirus saimiri encodes homologues of G protein-coupled receptors and cyclins. Nature. 355, 362–365.PubMedGoogle Scholar
  113. Nicholas, J., Coles, L. S., Newman, C. and Honess, R. W. (1991) Regulation of the herpesvirus saimiri (HVS) delayed-early 110-kilodalton promoter by HVS immediate-early gene products and a homolog of the Epstein-Barr virus R trans activator. J Virol. 65, 2457–2466.PubMedGoogle Scholar
  114. Nick, S., Fickenscher, H., Biesinger, B., Born, G., Jahn, G. and Fleckenstein, B. (1993) Herpesvirus saimiri transformed human T cell lines: a permissive system for human immunodeficiency viruses. Virology. 194, 875–877.PubMedGoogle Scholar
  115. Orzechowska, B., Powers, MF, Yen, B, Li, H, Axthelm, MK and Wong, SW (2008) Experimental rhesus macaque rhadinovirus infection in immunodeficient rhesus macaques leads to lymphoma. Blood. in press.Google Scholar
  116. Pari, G. S., AuCoin, D., Colletti, K., Cei, S. A., Kirchoff, V., Wong, S. W. (2001) Identification of the rhesus macaque rhadinovirus lytic origin of DNA replication. J Virol. 75, 11401–11407.Google Scholar
  117. Park, J., Seo, T., Jung, J. and Choe, J. (2004) Herpesvirus saimiri STP A11 protein interacts with STAT3 and stimulates its transcriptional activity. Biochemical and biophysical research communications. 320, 279–285.PubMedGoogle Scholar
  118. Peng, R., Gordadze, A. V., Fuentes Panana, E. M., Wang, F., Zong, J., Hayward, G. S., Tan, J. and Ling, P. D. (2000) Sequence and functional analysis of EBNA-LP and EBNA2 proteins from nonhuman primate lymphocryptoviruses. J Virol. 74, 379–389.PubMedGoogle Scholar
  119. Pfeffer, S., Sewer, A., Lagos-Quintana, M., Sheridan, R., Sander, C., Grasser, F. A., van Dyk, L. F., Ho, C. K., Shuman, S., Chien, M., Russo, J. J., Ju, J., Randall, G., Lindenbach, B. D., Rice, C. M., Simon, V., Ho, D. D., Zavolan, M. and Tuschl, T. (2005) Identification of microRNAs of the herpesvirus family. Nat Methods. 2, 269–276.PubMedGoogle Scholar
  120. Portis, T., Cooper, L., Dennis, P. and Longnecker, R. (2002) The LMP2A signalosome--a therapeutic target for Epstein-Barr virus latency and associated disease. Front Biosci. 7, d414–426.PubMedGoogle Scholar
  121. Rabin, H., Neubauer, R. H., Hopkins, R. F., 3rd, Dzhikidze, E. K., Shevtsova, Z. V. and Lapin, B. A. (1977a) Transforming activity and antigenicity of an Epstein-Barr-like virus from lymphoblastoid cell lines of baboons with lymphoid disease. Intervirology. 8, 240–249.Google Scholar
  122. Rabin, H., Neubauer, R. H., Hopkins, R. F. and Levy, B. M. (1977b) Characterization of lymphoid cell lines established from multiple Epstein-Barr virus (EBV) -induced lymphomas in a cotton-topped marmoset. Int J Cancer. 20, 44–50.Google Scholar
  123. Ramer, J. C., Garber, R. L., Steele, K. E., Boyson, J. F., O’Rourke, C. and Thomson, J. A. (2000) Fatal lymphoproliferative disease associated with a novel gammaherpesvirus in a captive population of common marmosets. Comp Med. 50, 59–-68.PubMedGoogle Scholar
  124. Randall, R. E., Newman, C. and Honess, R. W. (1985) Asynchronous expression of the immediate-early protein of herpesvirus saimiri in populations of productively infected cells. J Gen Virol. 66 (Pt 10), 2199–2213.PubMedGoogle Scholar
  125. Rao, P., Jiang, H. and Wang, F. (2000) Cloning of the rhesus lymphocryptovirus viral capsid antigen and Epstein-Barr virus-encoded small RNA homologues and use in diagnosis of acute and persistent infections. J Clin Microbiol. 38, 3219–3225.PubMedGoogle Scholar
  126. Renne, R., Dittmer, D., Kedes, D., Schmidt, K., Desrosiers, R. C., Luciw, P. A. and Ganem, D. (2004) Experimental transmission of Kaposi’s sarcoma-associated herpesvirus (KSHV/HHV-8) to SIV-positive and SIV-negative rhesus macaques. J Med Primatol. 33, 1–9.PubMedGoogle Scholar
  127. Rivailler, P., Cho, Y. G. and Wang, F. (2002a) Complete genomic sequence of an Epstein-Barr virus-related herpesvirus naturally infecting a new world primate: a defining point in the evolution of oncogenic lymphocryptoviruses. J Virol. 76, 12055–12068.Google Scholar
  128. Rivailler, P., Jiang, H., Cho, Y. G., Quink, C. and Wang, F. (2002b) Complete nucleotide sequence of the rhesus lymphocryptovirus: genetic validation for an Epstein-Barr virus animal model. J Virol. 76, 421–426.Google Scholar
  129. Rivailler, P., Quink, C. and Wang, F. (1999) Strong selective pressure for evolution of an Epstein-Barr virus LMP2B homologue in the rhesus lymphocryptovirus. J Virol. 73, 8867–8872.PubMedGoogle Scholar
  130. Rose, T. M., Strand, K. B., Schultz, E. R., Schaefer, G., Rankin, G. W., Jr., Thouless, M. E., Tsai, C. C. and Bosch, M. L. (1997) Identification of two homologs of the Kaposi’s sarcoma-associated herpesvirus (human herpesvirus 8) in retroperitoneal fibromatosis of different macaque species. J Virol. 71, 4138–4144.PubMedGoogle Scholar
  131. Rother, R. P., Rollins, S. A., Fodor, W. L., Albrecht, J. C., Setter, E., Fleckenstein, B. and Squinto, S. P. (1994) Inhibition of complement-mediated cytolysis by the terminal complement inhibitor of herpesvirus saimiri. J Virol. 68, 730–737.PubMedGoogle Scholar
  132. Rouvier, E., Luciani, M. F., Mattei, M. G., Denizot, F. and Golstein, P. (1993) CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus saimiri gene. J Immunol. 150, 5445–5456.PubMedGoogle Scholar
  133. Rowe, D. T. and Clarke, J. R. (1989) The type-specific epitopes of the Epstein-Barr virus nuclear antigen 2 are near the carboxy terminus of the protein. J Gen Virol. 70 (Pt 5), 1217–1229.PubMedGoogle Scholar
  134. Rowe, M., Young, L. S., Cadwallader, K., Petti, L., Kieff, E. and Rickinson, A. B. (1989) Distinction between Epstein-Barr virus type A (EBNA 2A) and type B (EBNA 2B) isolates extends to the EBNA 3 family of nuclear proteins. J Virol. 63, 1031–1039.PubMedGoogle Scholar
  135. Ruf, I. K., Moghaddam, A., Wang, F. and Sample, J. (1999) Mechanisms that regulate Epstein-Barr virus EBNA-1 gene transcription during restricted latency are conserved among lymphocryptoviruses of Old World primates. J Virol. 73, 1980–1989.PubMedGoogle Scholar
  136. Russo, J. J., Bohenzky, R. A., Chien, M. C., Chen, J., Yan, M., Maddalena, D., Parry, J. P., Peruzzi, D., Edelman, I. S., Chang, Y. and Moore, P. S. (1996) Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci U S A. 93, 14862–14867.PubMedGoogle Scholar
  137. Sample, J. and Kieff, E. (1990) Transcription of the Epstein-Barr virus genome during latency in growth- transformed lymphocytes. J Virol. 64, 1667–1674.PubMedGoogle Scholar
  138. Schafer, A., Cai, X., Bilello, J. P., Desrosiers, R. C. and Cullen, B. R. (2007) Cloning and analysis of microRNAs encoded by the primate gamma-herpesvirus rhesus monkey rhadinovirus. Virology. 364, 21–27.PubMedGoogle Scholar
  139. Schafer, A., Lengenfelder, D., Grillhosl, C., Wieser, C., Fleckenstein, B. and Ensser, A. (2003) The latency-associated nuclear antigen homolog of herpesvirus saimiri inhibits lytic virus replication. J Virol. 77, 5911–5925.PubMedGoogle Scholar
  140. Schultz, E. R., Rankin, G. W., Jr., Blanc, M. P., Raden, B. W., Tsai, C. C. and Rose, T. M. (2000) Characterization of two divergent lineages of macaque rhadinoviruses related to Kaposi’s sarcoma-associated herpesvirus. J Virol. 74, 4919–4928.PubMedGoogle Scholar
  141. Searles, R. P., Bergquam, E. P., Axthelm, M. K. and Wong, S. W. (1999) Sequence and genomic analysis of a Rhesus macaque rhadinovirus with similarity to Kaposi’s sarcoma-associated herpesvirus/human herpesvirus 8. J Virol. 73, 3040–3053.PubMedGoogle Scholar
  142. Shope, T., Dechairo, D. and Miller, G. (1973) Malignant lymphoma in cottontop marmosets after inoculation with Epstein-Barr virus. Proc Natl Acad Sci U S A. 70, 2487–2491.PubMedGoogle Scholar
  143. Stockinger, B., Veldhoen, M., Martin, B. (2007) Th17 T cells: linking innate and adaptive immunity. Semin Immunol. 19(6), 353–61.Google Scholar
  144. Strand, K., Harper, E., Thormahlen, S., Thouless, M. E., Tsai, C., Rose, T. and Bosch, M. L. (2000) Two distinct lineages of macaque gamma herpesviruses related to the Kaposi’s sarcoma associated herpesvirus. J Clin Virol. 16, 253–269.PubMedGoogle Scholar
  145. Thome, M., Schneider, P., Hofmann, K., Fickenscher, H., Meinl, E., Neipel, F., Mattmann, C., Burns, K., Bodmer, J. L., Schroter, M., Scaffidi, C., Krammer, P. H., Peter, M. E. and Tschopp, J. (1997) Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature. 386, 517–521.PubMedGoogle Scholar
  146. Vella, C., Gregory, J., Bristow, R., Troop, M., Easterbrook, P., Zheng, N. and Daniels, R. (1999a) Isolation of HIV type 1 from long-term nonprogressors in Herpesvirus saimiri-immortalized T cells. AIDS Res Hum Retroviruses. 15, 1145–1147.Google Scholar
  147. Vella, C., Zheng, N. N., Vella, G., Atkins, C., Bristow, R. G., Fickenscher, H. and Daniels, R. S. (1999b) Enhanced replication of M-tropic HIV-1 strains in Herpesvirus saimiri immortalised T-cells which express CCR5. Journal of virological methods. 79, 51–63.Google Scholar
  148. Wang, F. (2001) A new animal model for epstein-barr virus pathogenesis. Curr Top Microbiol Immunol. 258, 201–219.PubMedGoogle Scholar
  149. Wehner, L. E., Schroder, N., Kamino, K., Friedrich, U., Biesinger, B. and Ruther, U. (2001) Herpesvirus saimiri Tip gene causes T-cell lymphomas in transgenic mice. DNA and cell biology. 20, 81–88.PubMedGoogle Scholar
  150. Wenner, H. A., Barrick, S., Abel, D. and Seshumurty, P. (1975) The pathogenesis of simian varicella virus in cynomolgus monkeys. Proc Soc Exp Biol Med. 150, 318–323.PubMedGoogle Scholar
  151. Werner, J., Wolf, H., Apodaca, J. and zur Hausen, H. (1975) Lymphoproliferative disease in a cotton-top marmoset after inoculation with infectious mononucleosis-derived Epstein-Barr virus. Int J Cancer. 15, 1000–1008.PubMedGoogle Scholar
  152. Whitehouse, A., Cooper, M. and Meredith, D. M. (1998) The immediate-early gene product encoded by open reading frame 57 of herpesvirus saimiri modulates gene expression at a posttranscriptional level. J Virol. 72, 857–861.PubMedGoogle Scholar
  153. Wong, S. W., Bergquam, E. P., Swanson, R. M., Lee, F. W., Shiigi, S. M., Avery, N. A., Fanton, J. W. and Axthelm, M. K. (1999) Induction of B cell hyperplasia in simian immunodeficiency virus- infected rhesus macaques with the simian homologue of Kaposi’s sarcoma- associated herpesvirus. J Exp Med. 190, 827–840.PubMedGoogle Scholar
  154. Yalamanchili, R., Harada, S. and Kieff, E. (1996) The N-terminal half of EBNA2, except for seven prolines, is not essential for primary B-lymphocyte growth transformation. J Virol. 70, 2468–2473.PubMedGoogle Scholar
  155. Yates, J. L., Camiolo, S. M., Ali, S. and Ying, A. (1996) Comparison of the EBNA1 proteins of Epstein-Barr virus and herpesvirus papio in sequence and function. Virology. 222, 1–13.PubMedGoogle Scholar
  156. Yoon, D. W., Lee, H., Seol, W., DeMaria, M., Rosenzweig, M. and Jung, J. U. (1997) Tap: a novel cellular protein that interacts with tip of herpesvirus saimiri and induces lymphocyte aggregation. Immunity. 6, 571–582.PubMedGoogle Scholar
  157. Zhao, B., Dalbies-Tran, R., Jiang, H., Ruf, I. K., Sample, J. T., Wang, F. and Sample, C. E. (2003) Transcriptional regulatory properties of Epstein-Barr virus nuclear antigen 3C are conserved in simian lymphocryptoviruses. J Virol. 77, 5639–5648.PubMedGoogle Scholar
  158. Zimber, U., Adldinger, H. K., Lenoir, G. M., Vuillaume, M., Knebel-Doeberitz, M. V., Laux, G., Desgranges, C., Wittmann, P., Freese, U. K., Schneider, U. and et al. (1986) Geographical prevalence of two types of Epstein-Barr virus. Virology. 154, 56–66.PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media, LLC 2009

Authors and Affiliations

  • Ilhem Messaoudi
  • Blossom Damania
  • Scott W. Wong
    • 1
  1. 1.Vaccine and Gene Therapy Institute, Oregon Health & Science UniversityOregon 97006USA

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