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Simian Varicella Virus Pathogenesis

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Book cover Varicella-zoster Virus

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 342))

Abstract

Because varicella zoster virus (VZV) is an exclusively human pathogen, the development of an animal model is necessary to study pathogenesis, latency, and reactivation. The pathological, virological, and immunological features of simian varicella virus (SVV) infection in nonhuman primates are similar to those of VZV infection in humans. Both natural infection of cynomolgus and African green monkeys as well as intrabronchial inoculation of rhesus macaques with SVV provide the most useful models to study viral and immunological aspects of latency and the host immune response. Experimental immunosuppression of monkeys latently infected with SVV results in zoster, thus providing a new model system to study how the loss of adaptive immunity modulates virus reactivation.

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Abbreviations

CMI:

Cell-mediated immunity

MNCs:

Mononuclear cells

ORF:

Open reading frame

SVV:

Simian varicella virus

VZV:

Varicella zoster virus

References

  • Abendroth A, Lin I, Slobedman B et al (2001) Varicella-zoster virus retains major histocompatibility complex class I proteins in the Golgi compartment of infected cells. J Virol 75:4878–4888

    Article  PubMed  CAS  Google Scholar 

  • Achilli G, Sarasini A, Gerna G et al (1984) Antibody response of patas monkeys to experimental infection with Delta herpesvirus. Eur J Clin Microbiol 3:158–159

    Article  PubMed  CAS  Google Scholar 

  • Annunziato P, LaRussa P, Lee P et al (1998) Evidence of latent varicella-zoster virus in rat dorsal root ganglia. J Infect Dis 178(Suppl 1):S48–S51

    Article  PubMed  Google Scholar 

  • Arbeit RD, Zaia JA, Valerio MA et al (1982) Infection of human peripheral blood mononuclear cells by varicella-zoster virus. Intervirology 18:56–65

    Article  PubMed  CAS  Google Scholar 

  • Chen JJ, Gershon AA, Li ZS et al (2003) Latent and lytic infection of isolated guinea pig enteric ganglia by varicella zoster virus. J Med Virol 70(Suppl 1):S71–S78

    Article  PubMed  Google Scholar 

  • Clarkson MJ, Thorpe E, McCarthy K (1967) A virus disease of captive vervet monkeys (Cercopithecus aethiops) caused by a new herpesvirus. Arch Gesamte Virusforsch 22:219–234

    Article  PubMed  CAS  Google Scholar 

  • Cohen JI (1998) Infection of cells with varicella-zoster virus down-regulates surface expression of class I major histocompatibility complex antigens. J Infect Dis 177:1390–1393

    Article  PubMed  CAS  Google Scholar 

  • Cohen JI, Moskal T, Shapiro M et al (1996) Varicella in chimpanzees. J Med Virol 50:289–292

    Article  PubMed  CAS  Google Scholar 

  • Debrus S, Sadzot-Delvaux C, Nikkels AF et al (1995) Varicella-zoster virus gene 63 encodes an immediate-early protein that is abundantly expressed during latency. J Virol 69:3240–3245

    PubMed  CAS  Google Scholar 

  • Dolin R, Reichman RC, Mazur MH et al (1978) NIH conference. Herpes zoster-varicella infections in immunosuppressed patients. Ann Intern Med 89:375–388

    PubMed  CAS  Google Scholar 

  • Dueland AN, Martin JR, Devlin ME et al (1992) Acute simian varicella infection: clinical, laboratory, pathologic, and virologic features. Lab Invest 66:762–773

    PubMed  CAS  Google Scholar 

  • Eisfeld AJ, Yee MB, Erazo A et al (2007) Downregulation of class I major histocompatibility complex surface expression by varicella-zoster virus involves open reading frame 66 protein kinase-dependent and -independent mechanisms. J Virol 81:9034–9049

    Article  PubMed  CAS  Google Scholar 

  • Felsenfeld AD, Schmidt NJ (1977) Antigenic relationships among several simian varicella-like viruses and varicella-zoster virus. Infect Immun 15:807–812

    PubMed  CAS  Google Scholar 

  • Felsenfeld AD, Schmidt NJ (1979) Varicella-zoster virus immunizes patas monkeys against simian varicella-like disease. J Gen Virol 42:171–178

    Article  PubMed  CAS  Google Scholar 

  • Fletcher TM, Gray WL (1992) Simian varicella virus: characterization of virion and infected cell polypeptides and the antigenic cross-reactivity with varicella-zoster virus. J Gen Virol 73:1209–1215

    Article  PubMed  CAS  Google Scholar 

  • Gilden DH, Hayward AR, Krupp J et al (1987) Varicella-zoster virus infection of human mononuclear cells. Virus Res 7:117–129

    Article  PubMed  CAS  Google Scholar 

  • Gray WL (2003) Pathogenesis of simian varicella virus. J Med Virol 70(Suppl 1):S4–S8

    Article  PubMed  Google Scholar 

  • Gray WL (2004) Simian varicella: a model for human varicella-zoster virus infections. Rev Med Virol 14:363–381

    Article  PubMed  Google Scholar 

  • Gray WL, Gusick NJ (1996) Viral isolates derived from simian varicella epizootics are genetically related but are distinct from other primate herpesviruses. Virology 224:161–166

    Article  PubMed  CAS  Google Scholar 

  • Gray WL, Pumphrey CY, Ruyechan WT et al (1992) The simian varicella virus and varicella zoster virus genomes are similar in size and structure. Virology 186:562–572

    Article  PubMed  CAS  Google Scholar 

  • Gray WL, Gusick NJ, Fletcher TM et al (1995) Simian varicella virus antibody response in experimental infection of African green monkeys. J Med Primatol 24:246–251

    Article  PubMed  CAS  Google Scholar 

  • Gray WL, Williams RJ, Chang R et al (1998) Experimental simian varicella virus infection of St. Kitts vervet monkeys. J Med Primatol 27:177–183

    Article  PubMed  CAS  Google Scholar 

  • Gray WL, Starnes B, White MW et al (2001) The DNA sequence of the simian varicella virus genome. Virology 284:123–130

    Article  PubMed  CAS  Google Scholar 

  • Gray WL, Mullis L, Soike KF (2002) Viral gene expression during acute simian varicella virus infection. J Gen Virol 83:841–846

    PubMed  CAS  Google Scholar 

  • Grinfeld E, Kennedy PG (2007) The pattern of viral persistence in monkeys intra-tracheally infected with simian varicella virus. Virus Genes 35:289–292

    Article  PubMed  CAS  Google Scholar 

  • Iltis JP, Arrons MC, Castellano GA et al (1982) Simian varicella virus (delta herpesvirus) infection of patas monkeys leading to pneumonia and encephalitis. Proc Soc Exp Biol Med 169:266–279

    PubMed  CAS  Google Scholar 

  • Iltis JP, Achilli G, Madden DL et al (1984) Serologic study by enzyme-linked immunosorbent assay of the IgM antibody response in the patas monkey following experimental simian varicella virus infection. Diagn Immunol 2:137–142

    PubMed  CAS  Google Scholar 

  • Kennedy PG, Grinfeld E, Bontems S et al (2001) Varicella-zoster virus gene expression in latently infected rat dorsal root ganglia. Virology 289:218–223

    Article  PubMed  CAS  Google Scholar 

  • Kennedy PGE, Grinfeld E, Traina-Dorge V et al (2004) Neuronal localization of simian varicella virus DNA in ganglia of naturally infected African green monkeys. Virus Genes 28:273–276

    Article  PubMed  CAS  Google Scholar 

  • Kolappaswamy K, Mahalingam R, Traina-Dorge V et al (2007) Disseminated simian varicella virus infection in an irradiated rhesus macaque (Macaca mulatta). J Virol 81:411–415

    Article  PubMed  CAS  Google Scholar 

  • Koropchak CM, Solem SM, Diaz PS et al (1989) Investigation of varicella-zoster virus infection of lymphocytes by in situ hybridization. J Virol 63:2392–2395

    PubMed  CAS  Google Scholar 

  • Ku CC, Zerboni L, Ito H et al (2004) Varicella-zoster virus transfer to skin by T cells and modulation of viral replication by epidermal cell interferon-alpha. J Exp Med 200:917–925

    Article  PubMed  CAS  Google Scholar 

  • Ku CC, Besser J, Abendroth A et al (2005) Varicella-zoster virus pathogenesis and immunobiology: new concepts emerging from investigations with the SCIDhu mouse model. J Virol 79:2651–2658

    Article  PubMed  CAS  Google Scholar 

  • Lowry PW, Sabella C, Koropchak CM et al (1993) Investigation of the pathogenesis of varicella-zoster virus infection in guinea pigs by using polymerase chain reaction. J Infect Dis 167:78–83

    Article  PubMed  CAS  Google Scholar 

  • Mahalingam R, Wellish M, Cohrs R et al (1996) Expression of protein encoded by varicella-zoster virus open reading frame 63 in latently infected human ganglionic neurons. Proc Natl Acad Sci USA 93:2122–2124

    Article  PubMed  CAS  Google Scholar 

  • Mahalingam R, Wellish M, Soike K (2001) Simian varicella virus infects ganglia before rash in experimentally infected monkeys. Virology 279:339–342

    Article  PubMed  CAS  Google Scholar 

  • Mahalingam R, Traina-Dorge V, Wellish M et al (2002) Naturally acquired simian varicella virus infection in African green monkeys. J Virol 76:8548–8550

    Article  PubMed  CAS  Google Scholar 

  • Matsunaga Y, Yamanishi K, Takahashi M (1982) Experimental infection and immune response of guinea pigs with varicella-zoster virus. Infect Immun 37:407–412

    PubMed  CAS  Google Scholar 

  • McCarthy K, Thorpe E, Laursen AC et al (1968) Exanthematous disease in patas monkeys caused by a herpes virus. Lancet 2:856–857

    Article  PubMed  CAS  Google Scholar 

  • Messaoudi I, Barron A, Wellish M et al (2009) Simian varicella virus infection of rhesus macaques recapitulates essential features of varicella zoster virus infection in humans. PLoS Pathog 5(11):1–14

    Google Scholar 

  • Moffat JF, Stein MD, Kaneshima H et al (1995) Tropism of varicella-zoster virus for human CD4+ and CD8+ T lymphocytes and epidermal cells in SCID-hu mice. J Virol 69:5236–5242

    PubMed  CAS  Google Scholar 

  • Myers MG, Connelly BL (1992) Animal models of varicella. J Infect Dis 166(Suppl 1):S48–S50

    Article  PubMed  Google Scholar 

  • Myers MG, Duer HL, Hausler CK (1980) Experimental infection of guinea pigs with varicella-zoster virus. J Infect Dis 142:414–420

    Article  PubMed  CAS  Google Scholar 

  • Myers MG, Stanberry LR, Edmond BJ (1985) Varicella-zoster virus infection of strain 2 guinea pigs. J Infect Dis 151:106–113

    Article  PubMed  CAS  Google Scholar 

  • Myers MG, Connelly BL, Stanberry LR (1991) Varicella in hairless guinea pigs. J Infect Dis 163:746–751

    Article  PubMed  CAS  Google Scholar 

  • Ou Y, Davis KA, Traina-Dorge V et al (2007) Simian varicella virus expresses a latency-associated transcript that is antisense to open reading frame 61 (ICP0) mRNA in neural ganglia of latently infected monkeys. J Virol 81:8149–8156

    Article  PubMed  CAS  Google Scholar 

  • Pavan-Langston D, Dunkel EC (1989) Ocular varicella-zoster virus infection in the guinea pig: a new in vivo model. Arch Ophthalmol 107:1058–1072

    Article  Google Scholar 

  • Padovan D, Cantrell CA (1986) Varicella-like herpesvirus infections of nonhuman primates. Lab Anim Sci 36:7–13

    PubMed  CAS  Google Scholar 

  • Pumphrey CY, Gray WL (1992) The genomes of simian varicella virus and varicella zoster virus are colinear. Virus Res 26:255–266

    Article  PubMed  CAS  Google Scholar 

  • Roberts ED, Baskin GB, Soike K et al (1984) Pathologic changes of experimental simian varicella (Delta herpesvirus) infection in African green monkeys (Cercopithecus aethiops). Am J Vet Res 45:523–530

    PubMed  CAS  Google Scholar 

  • Sadzot-Delvaux C, Merville-Louis MP, Delree P et al (1990) An in vivo model of varicella-zoster virus latent infection of dorsal root ganglia. J Neurosci Res 26:83–89

    Article  PubMed  CAS  Google Scholar 

  • Sato H, Pesnicak L, Cohen JI (2003) Use of a rodent model to show that varicella-zoster virus ORF61 is dispensable for establishment of latency. J Med Virol 70(Suppl 1):S79–S81

    Article  PubMed  CAS  Google Scholar 

  • Schoeb TR, Eberle R, Black DH et al (2008) Diagnostic exercise: papulovesicular dermatitis in rhesus macaques (Macaca mulatta). Vet Pathol 45:592–594

    Article  PubMed  CAS  Google Scholar 

  • Soike KF (1992) Simian varicella virus infection in African and Asian monkeys. The potential for development of antivirals for animal diseases. Ann NY Acad Sci 653:323–333

    Article  PubMed  CAS  Google Scholar 

  • Soike KF, Baskin G, Cantrell C et al (1984a) Investigation of antiviral activity of 1-beta-D-arabinofuranosylthymine (ara-T) and 1-beta-D-arabinofuranosyl-E-5-(2-bromovinyl)uracil (BV-ara-U) in monkeys infected with simian varicella virus. Antiviral Res 4:245–257

    Article  PubMed  CAS  Google Scholar 

  • Soike KF, Rangan SR, Gerone PJ (1984b) Viral disease models in primates. Adv Vet Sci Comp Med 28:151–199

    PubMed  CAS  Google Scholar 

  • Soike KF, Keller PM, Ellis RW (1987) Immunization of monkeys with varicella-zoster virus glycoprotein antigens and their response to challenge with simian varicella virus. J Med Virol 22:307–313

    Article  PubMed  CAS  Google Scholar 

  • Soong W, Schultz JC, Patera AC et al (2000) Infection of human T lymphocytes with varicella-zoster virus: an analysis with viral mutants and clinical isolates. J Virol 74:1864–1870

    Article  PubMed  CAS  Google Scholar 

  • Tenser RB, Hyman RW (1987) Latent herpesvirus infections of neurons in guinea pigs and humans. Yale J Biol Med 60:159–167

    PubMed  CAS  Google Scholar 

  • Treuting PM, Johnson-Delaney C, Birkebak TA (1998) Diagnostic exercise: vesicular epidermal rash, mucosal ulcerations, and hepatic necrosis in a Cynomolgus monkey (Macaca fascicularis). Lab Anim Sci 48:384–386

    PubMed  CAS  Google Scholar 

  • Verjans GM, Hintzen RQ, van Dun JM et al (2007) Selective retention of herpes simplex virus-specific T cells in latently infected human trigeminal ganglia. Proc Natl Acad Sci USA 104:3496–3501

    Article  PubMed  CAS  Google Scholar 

  • Walz-Cicconi MA, Rose RM, Dammin GJ et al (1986) Inoculation of guinea pigs with varicella-zoster virus via the respiratory route. Arch Virol 88:265–277

    Article  PubMed  CAS  Google Scholar 

  • Wenner HA, Abel D, Barrick S et al (1977) Clinical and pathogenetic studies of Medical Lake macaque virus infections in Cynomolgus monkeys (simian varicella). J Infect Dis 135:611–622

    Article  PubMed  CAS  Google Scholar 

  • White TM, Mahalingam R, Traina-Dorge V et al (2002a) Simian varicella virus DNA is present and transcribed months after experimental infection of adult African green monkeys. J Neurovirol 8:191–203

    Article  PubMed  CAS  Google Scholar 

  • White TM, Mahalingam R, Traina-Dorge V et al (2002b) Persistence of simian varicella virus DNA in CD4(+) and CD8(+) blood mononuclear cells for years after intratracheal inoculation of African green monkeys. Virology 303:192–198

    Article  PubMed  CAS  Google Scholar 

  • Wolf RH, Smetana HF, Allen WP et al (1974) Pathology and clinical history of Delta herpesvirus infection in patas monkeys. Lab Anim Sci 24:218–221

    PubMed  CAS  Google Scholar 

  • Wroblewska Z, Devlin M, Reilly K et al (1982) The production of varicella zoster virus antiserum in laboratory animals. Arch Virol 74:233–238

    Article  PubMed  CAS  Google Scholar 

  • Wroblewska Z, Valyi-Nagy T, Otte J et al (1993) A mouse model for varicella-zoster virus latency. Microb Pathog 15:141–151

    Article  PubMed  CAS  Google Scholar 

  • Zerboni L, Sommer M, Ware CF et al (2000) Varicella-zoster virus infection of a human CD4-positive T-cell line. Virology 270:278–285

    Article  PubMed  CAS  Google Scholar 

  • Zerboni K, Ku CC, Jones CD et al (2005) Varicella-zoster virus infection of human dorsal root ganglia in vivo. Proc Natl Acad Sci USA 102:6490–6495

    Google Scholar 

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Acknowledgments

This work was supported in part by Public Health Service grants AG006127, NS032623 and AG032958 from the National Institutes of Health. The authors thank Marina Hoffman for editorial review and Cathy Allen for preparing the manuscript.

Author information

Authors and Affiliations

  1. Departments of Neurology, University of Colorado Denver School of Medicine, 12700 E. 19th Avenue, Mailstop B182, Aurora, CO, 80045, USA

    Ravi Mahalingam & Don Gilden

  2. Vaccine and Gene Therapy and Division of Pathobiology and Immunology, Oregon National Primate Research Center, Oregon Health and Science, 505 NW 185th Avenue, Beaverton, OR, 97006, USA

    Ilhem Messaoudi

  3. Departments of Microbiology, University of Colorado Denver School of Medicine, 12700 E. 19th Avenue, Mailstop B182, Aurora, CO, 80045, USA

    Don Gilden

Authors
  1. Ravi Mahalingam
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  2. Ilhem Messaoudi
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  3. Don Gilden
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Corresponding author

Correspondence to Ravi Mahalingam .

Editor information

Editors and Affiliations

  1. Department of Infectious Diseases and Im, Head, VZV Research Laboratory, University of Sydney, Room 601 Blackburn Building D06, Sydney, 2006, New South Wales, Australia

    Allison Abendroth

  2. School of Medicine, Dept. Microbiology & Immunology, Stanford University, Pasteur Drive 300, Stanford, 94305-5124, California, USA

    Ann M. Arvin

  3. 2215 Weiskotten Hall, Upstate Medical University, East Adams Street 750, Syracuse, 13210, New York, USA

    Jennifer F. Moffat

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Mahalingam, R., Messaoudi, I., Gilden, D. (2010). Simian Varicella Virus Pathogenesis. In: Abendroth, A., Arvin, A., Moffat, J. (eds) Varicella-zoster Virus. Current Topics in Microbiology and Immunology, vol 342. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2009_6

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