Varicella-zoster Virus pp 211-228

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

Experimental Models to Study Varicella-Zoster Virus Infection of Neurons

Chapter

Abstract

Varicella zoster virus (VZV) infection results in the establishment of latency in human sensory neurons. Reactivation of VZV leads to herpes zoster which can be followed by persistent neuropathic pain, termed post-herpetic neuralgia (PHN). Humans are the only natural host for VZV, and the strict species specificity of the virus has restricted the development of an animal model of infection which mimics all phases of disease. In order to elucidate the mechanisms which control the establishment of latency and reactivation as well as the effect of VZV replication on neuronal function, in vitro models of neuronal infection have been developed. Currently these models involve culturing and infecting dissociated human fetal neurons, with or without their supporting cells, an intact explant fetal dorsal root ganglia (DRG) model, neuroblastoma cell lines and rodent neuronal cell models. Each of these models has distinct advantages as well as disadvantages, and all have contributed towards our understanding of VZV neuronal infection. However, as yet none have been able to recapitulate the full virus lifecycle from primary infection to latency through to reactivation. The development of such a model will be a crucial step towards advancing our understanding of the mechanisms involved in VZV replication in neuronal cells, and the design of new therapies to combat VZV-related disease.

References

  1. Ambagala AP, Bosma T, Ali MA, Poustovoitov M, Chen JJ, Gershon MD, Adams PD, Cohen JI (2009) Varicella-zoster virus immediate-early 63 protein interacts with human antisilencing function 1 protein and alters its ability to bind histones h3.1 and h3.3. J Virol 83(1):200–209PubMedCrossRefGoogle Scholar
  2. Annunziato P, LaRussa P, Lee P, Steinberg S, Lungu O, Gershon AA, Silverstein S (1998) Evidence of latent varicella-zoster virus in rat dorsal root ganglia. J Infect Dis 178(Suppl 1):S48–S51PubMedCrossRefGoogle Scholar
  3. Assouline JG, Levin MJ, Major EO, Forghani B, Straus SE, Ostrove JM (1990) Varicella-zoster virus infection of human astrocytes, Schwann cells, and neurons. Virology 179(2):834–844PubMedCrossRefGoogle Scholar
  4. Biedler JL, Helson L, Spengler BA (1973) Morphology and growth, tumorigenicity, and cytogenetics of human neuroblastoma cells in continuous culture. Cancer Res 33(11):2643–2652PubMedGoogle Scholar
  5. Bourdon-Wouters C, Merville-Louis MP, Sadzot-Delvaux C, Marc P, Piette J, Delree P, Moonen G, Rentier B (1990) Acute and persistent varicella-zoster virus infection of human and murine neuroblastoma cell lines. J Neurosci Res 26(1):90–97PubMedCrossRefGoogle Scholar
  6. Chen JJ, Gershon AA, Li ZS, Lungu O, Gershon MD (2003) Latent and lytic infection of isolated guinea pig enteric ganglia by varicella zoster virus. J Med Virol 70(Suppl 1):S71–S78PubMedCrossRefGoogle Scholar
  7. Chen JJ, Zhu Z, Gershon AA, Gershon MD (2004) Mannose 6-phosphate receptor dependence of varicella zoster virus infection in vitro and in the epidermis during varicella and zoster. Cell 119(7):915–926PubMedCrossRefGoogle Scholar
  8. Cohen JI (2010) Rodent models of varicella-zoster virus neurotropism. Curr Top Microbiol Immunol doi 10.1007/82_2010_11Google Scholar
  9. Cohen JI, Nguyen H (1998) Varicella-zoster virus ORF61 deletion mutants replicate in cell culture, but a mutant with stop codons in ORF61 reverts to wild-type virus. Virology 246(2):306–316PubMedCrossRefGoogle Scholar
  10. Cohen JI, Sato H, Srinivas S, Lekstrom K (2001) Varicella-zoster virus (VZV) ORF65 virion protein is dispensable for replication in cell culture and is phosphorylated by casein kinase II, but not by the VZV protein kinases. Virology 280(1):62–71PubMedCrossRefGoogle Scholar
  11. Cohrs RJ, Gilden DH (2007) Prevalence and abundance of latently transcribed varicella-zoster virus genes in human ganglia. J Virol 81(6):2950–2956PubMedCrossRefGoogle Scholar
  12. Cohrs RJ, Gilden DH, Kinchington PR, Grinfeld E, Kennedy PG (2003) Varicella-zoster virus gene 66 transcription and translation in latently infected human Ganglia. J Virol 77(12):6660–6665PubMedCrossRefGoogle Scholar
  13. Cohrs RJ, Laguardia JJ, Gilden D (2005) Distribution of latent herpes simplex virus type-1 and varicella zoster virus DNA in human trigeminal Ganglia. Virus Genes 31(2):223–227PubMedCrossRefGoogle Scholar
  14. Croen KD, Ostrove JM, Dragovic LJ, Straus SE (1988) Patterns of gene expression and sites of latency in human nerve ganglia are different for varicella-zoster and herpes simplex viruses. Proc Natl Acad Sci USA 85(24):9773–9777PubMedCrossRefGoogle Scholar
  15. Dekker LV, Daniels Z, Hick C, Elsegood K, Bowden S, Szestak T, Burley JR, Southan A, Cronk D, James IF (2005) Analysis of human Nav1.8 expressed in SH-SY5Y neuroblastoma cells. Eur J Pharmacol 528(1–3):52–58PubMedCrossRefGoogle Scholar
  16. Denny-Brown D, Adam R, Fitzgerald P (1944) Pathological features of herpes zoster. Am Med Assoc Arch Dermatol 75:193–196Google Scholar
  17. Dworkin RH, Nagasako EM, Johnson RW, Griffin DR (2001) Acute pain in herpes zoster: the famciclovir database project. Pain 94(1):113–119PubMedCrossRefGoogle Scholar
  18. Encinas M, Iglesias M, Liu Y, Wang H, Muhaisen A, Cena V, Gallego C, Comella JX (2000) Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J Neurochem 75(3):991–1003PubMedCrossRefGoogle Scholar
  19. Fleetwood-Walker SM, Quinn JP, Wallace C, Blackburn-Munro G, Kelly BG, Fiskerstrand CE, Nash AA, Dalziel RG (1999) Behavioural changes in the rat following infection with varicella-zoster virus. J Gen Virol 80(Pt 9):2433–2436PubMedGoogle Scholar
  20. Garry EM, Delaney A, Anderson HA, Sirinathsinghji EC, Clapp RH, Martin WJ, Kinchington PR, Krah DL, Abbadie C, Fleetwood-Walker SM (2005) Varicella zoster virus induces neuropathic changes in rat dorsal root ganglia and behavioral reflex sensitisation that is attenuated by gabapentin or sodium channel blocking drugs. Pain 118(1–2):97–111PubMedCrossRefGoogle Scholar
  21. Gershon AA, Chen J, Davis L, Krinsky C, Cowles R, Gershon MD (2009) Distribution of latent varicella zoster virus (VZV) in sensory ganglia and gut after vaccination and wild-type infection: evidence for viremic spread. The 34th Annual International Herpesvirus Workshop. Ithaca, New York, USAGoogle Scholar
  22. Gershon AA, Chen J, Gershon MD (2008) A model of lytic, latent, and reactivating varicella-zoster virus infections in isolated enteric neurons. J Infect Dis 197(Suppl 2):S61–S65PubMedCrossRefGoogle Scholar
  23. Gilden DH, Gesser R, Smith J, Wellish M, Laguardia JJ, Cohrs RJ, Mahalingam R (2001) Presence of VZV and HSV-1 DNA in human nodose and celiac ganglia. Virus Genes 23(2):145–147PubMedCrossRefGoogle Scholar
  24. Gilden DH, Rozenman Y, Murray R, Devlin M, Vafai A (1987) Detection of varicella-zoster virus nucleic acid in neurons of normal human thoracic ganglia. Ann Neurol 22(3):377–380PubMedCrossRefGoogle Scholar
  25. Gilden DH, Vafai A, Shtram Y, Becker Y, Devlin M, Wellish M (1983) Varicella-zoster virus DNA in human sensory ganglia. Nature 306(5942):478–480PubMedCrossRefGoogle Scholar
  26. Gilden DH, Wroblewska Z, Kindt V, Warren KG, Wolinsky JS (1978) Varicella-zoster virus infection of human brain cells and ganglion cells in tissue culture. Arch Virol 56(1–2):105–117PubMedCrossRefGoogle Scholar
  27. Gimenez-Cassina A, Lim F, Diaz-Nido J (2006) Differentiation of a human neuroblastoma into neuron-like cells increases their susceptibility to transduction by herpesviral vectors. J Neurosci Res 84(4):755–767PubMedCrossRefGoogle Scholar
  28. Gowrishankar K, Slobedman B, Cunningham AL, Miranda-Saksena M, Boadle RA, Abendroth A (2007) Productive varicella-zoster virus infection of cultured intact human ganglia. J Virol 81(12):6752–6756PubMedCrossRefGoogle Scholar
  29. Grinfeld E, Sadzot-Delvaux C, Kennedy PG (2004) Varicella-Zoster virus proteins encoded by open reading frames 14 and 67 are both dispensable for the establishment of latency in a rat model. Virology 323(1):85–90PubMedCrossRefGoogle Scholar
  30. Hamza MA, Higgins DM, Ruyechan WT (2007) Two alphaherpesvirus latency-associated gene products influence calcitonin gene-related peptide levels in rat trigeminal neurons. Neurobiol Dis 25(3):553–560PubMedCrossRefGoogle Scholar
  31. Hanani M (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev 48(3):457–476PubMedCrossRefGoogle Scholar
  32. Head H, Campbell W (1900) The pathology of herpes zoster and its bearing on sensory localization. Brain 23:353–523CrossRefGoogle Scholar
  33. Holland DJ, Cunningham AL, Boadle RA (1998) The axonal transmission of herpes simplex virus to epidermal cells: a novel use of the freeze substitution technique applied to explant cultures retained on cover slips. J Microsc 192(Pt 1):69–72PubMedCrossRefGoogle Scholar
  34. Holland DJ, Miranda-Saksena M, Boadle RA, Armati P, Cunningham AL (1999) Anterograde transport of herpes simplex virus proteins in axons of peripheral human fetal neurons: an immunoelectron microscopy study. J Virol 73(10):8503–8511PubMedGoogle Scholar
  35. Hood C, Cunningham AL, Slobedman B, Arvin AM, Sommer MH, Kinchington PR, Abendroth A (2006) Varicella-zoster virus ORF63 inhibits apoptosis of primary human neurons. J Virol 80(2):1025–1031PubMedCrossRefGoogle Scholar
  36. Hood C, Cunningham AL, Slobedman B, Boadle RA, Abendroth A (2003) Varicella-zoster virus-infected human sensory neurons are resistant to apoptosis, yet human foreskin fibroblasts are susceptible: evidence for a cell-type-specific apoptotic response. J Virol 77(23):12852–12864PubMedCrossRefGoogle Scholar
  37. Hufner K, Derfuss T, Herberger S, Sunami K, Russell S, Sinicina I, Arbusow V, Strupp M, Brandt T, Theil D (2006) Latency of alpha-herpes viruses is accompanied by a chronic inflammation in human trigeminal ganglia but not in dorsal root ganglia. J Neuropathol Exp Neurol 65(10):1022–1030PubMedCrossRefGoogle Scholar
  38. Hyman RW, Ecker JR, Tenser RB (1983) Varicella-zoster virus RNA in human trigeminal ganglia. Lancet 2(8354):814–816PubMedCrossRefGoogle Scholar
  39. Joly E, Mucke L, Oldstone MB (1991) Viral persistence in neurons explained by lack of major histocompatibility class I expression. Science 253(5025):1283–1285PubMedCrossRefGoogle Scholar
  40. Kennedy PG, Grinfeld E, Bontems S, Sadzot-Delvaux C (2001) Varicella-Zoster virus gene expression in latently infected rat dorsal root ganglia. Virology 289(2):218–223PubMedCrossRefGoogle Scholar
  41. Kennedy PG, Grinfeld E, Gow JW (1998) Latent varicella-zoster virus is located predominantly in neurons in human trigeminal ganglia. Proc Natl Acad Sci USA 95(8):4658–4662PubMedCrossRefGoogle Scholar
  42. Kress M, Fickenscher H (2001) Infection by human varicella-zoster virus confers norepinephrine sensitivity to sensory neurons from rat dorsal root ganglia. FASEB J 15(6):1037–1043PubMedCrossRefGoogle Scholar
  43. LaGuardia JJ, Cohrs RJ, Gilden DH (1999) Prevalence of varicella-zoster virus DNA in dissociated human trigeminal ganglion neurons and nonneuronal cells. J Virol 73(10):8571–8577PubMedGoogle Scholar
  44. Lam PM, Hainsworth AH, Smith GD, Owen DE, Davies J, Lambert DG (2007) Activation of recombinant human TRPV1 receptors expressed in SH-SY5Y human neuroblastoma cells increases [Ca(2+)](i), initiates neurotransmitter release and promotes delayed cell death. J Neurochem 102(3):801–811PubMedCrossRefGoogle Scholar
  45. Lawson SN (2005) The peripheral sensory nervous system: dorsal root ganglion neurons. In: Dyck PJ, Thomas PK (eds) Peripheral Neuropathy. Elsevier Saunders, Philadelphia, PA, pp 163–202CrossRefGoogle Scholar
  46. Levin MJ, Cai GY, Manchak MD, Pizer LI (2003) Varicella-zoster virus DNA in cells isolated from human trigeminal ganglia. J Virol 77(12):6979–6987PubMedCrossRefGoogle Scholar
  47. Lowry PW, Sabella C, Koropchak CM, Watson BN, Thackray HM, Abbruzzi GM, Arvin AM (1993) Investigation of the pathogenesis of varicella-zoster virus infection in guinea pigs by using polymerase chain reaction. J Infect Dis 167(1):78–83PubMedCrossRefGoogle Scholar
  48. Lungu O, Annunziato PW, Gershon A, Staugaitis SM, Josefson D, LaRussa P, Silverstein SJ (1995) Reactivated and latent varicella-zoster virus in human dorsal root ganglia. Proc Natl Acad Sci USA 92(24):10980–10984PubMedCrossRefGoogle Scholar
  49. Lungu O, Panagiotidis CA, Annunziato PW, Gershon AA, Silverstein SJ (1998) Aberrant intracellular localization of Varicella-Zoster virus regulatory proteins during latency. Proc Natl Acad Sci USA 95(12):7080–7085PubMedCrossRefGoogle Scholar
  50. Mahalingam R, Wellish M, Cohrs R, Debrus S, Piette J, Rentier B, Gilden DH (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(5):2122–2124PubMedCrossRefGoogle Scholar
  51. Mahalingam R, Wellish M, Lederer D, Forghani B, Cohrs R, Gilden D (1993) Quantitation of latent varicella-zoster virus DNA in human trigeminal ganglia by polymerase chain reaction. J Virol 67(4):2381–2384PubMedGoogle Scholar
  52. Mahalingam R, Wellish MC, Dueland AN, Cohrs RJ, Gilden DH (1992) Localization of herpes simplex virus and varicella zoster virus DNA in human ganglia. Ann Neurol 31(4):444–448PubMedCrossRefGoogle Scholar
  53. Matsunaga Y, Yamanishi K, Takahashi M (1982) Experimental infection and immune response of guinea pigs with varicella-zoster virus. Infect Immun 37(2):407–412PubMedGoogle Scholar
  54. Merville-Louis MP, Sadzot-Delvaux C, Delree P, Piette J, Moonen G, Rentier B (1989) Varicella-zoster virus infection of adult rat sensory neurons in vitro. J Virol 63(7):3155–3160PubMedGoogle Scholar
  55. Mikloska Z, Cunningham AL (2001) Alpha and gamma interferons inhibit herpes simplex virus type 1 infection and spread in epidermal cells after axonal transmission. J Virol 75(23):11821–11826PubMedCrossRefGoogle Scholar
  56. Mikloska Z, Sanna PP, Cunningham AL (1999) Neutralizing antibodies inhibit axonal spread of herpes simplex virus type 1 to epidermal cells in vitro. J Virol 73(7):5934–5944PubMedGoogle Scholar
  57. Myers MG, Duer HL, Hausler CK (1980) Experimental infection of guinea pigs with varicella-zoster virus. J Infect Dis 142(3):414–420PubMedCrossRefGoogle Scholar
  58. Myers MG, Stanberry LR, Edmond BJ (1985) Varicella-zoster virus infection of strain 2 guinea pigs. J Infect Dis 151(1):106–113PubMedCrossRefGoogle Scholar
  59. Penfold ME, Armati P, Cunningham AL (1994) Axonal transport of herpes simplex virions to epidermal cells: evidence for a specialized mode of virus transport and assembly. Proc Natl Acad Sci USA 91(14):6529–6533PubMedCrossRefGoogle Scholar
  60. Penfold ME, Armati PJ, Mikloska Z, Cunningham AL (1996) The interaction of human fetal neurons and epidermal cells in vitro. Cell Dev Biol Anim 32(7):420–426PubMedCrossRefGoogle Scholar
  61. Reichelt M, Zerboni L, Arvin AM (2008) Mechanisms of varicella-zoster virus neuropathogenesis in human dorsal root ganglia. J Virol 82(8):3971–3983PubMedCrossRefGoogle Scholar
  62. Ross RA, Spengler BA, Biedler JL (1983) Coordinate morphological and biochemical interconversion of human neuroblastoma cells. J Natl Cancer Inst 71(4):741–747PubMedGoogle Scholar
  63. Sadzot-Delvaux C, Arvin AM, Rentier B (1998) Varicella-zoster virus IE63, a virion component expressed during latency and acute infection, elicits humoral and cellular immunity. J Infect Dis 178(Suppl 1):S43–S47PubMedCrossRefGoogle Scholar
  64. Sadzot-Delvaux C, Debrus S, Nikkels A, Piette J, Rentier B (1995) Varicella-zoster virus latency in the adult rat is a useful model for human latent infection. Neurology 45(12 Suppl 8):S18–S20PubMedCrossRefGoogle Scholar
  65. Sadzot-Delvaux C, Merville-Louis MP, Delree P, Marc P, Piette J, Moonen G, Rentier B (1990) An in vivo model of varicella-zoster virus latent infection of dorsal root ganglia. J Neurosci Res 26(1):83–89PubMedCrossRefGoogle Scholar
  66. Sato H, Callanan LD, Pesnicak L, Krogmann T, Cohen JI (2002) Varicella-zoster virus (VZV) ORF17 protein induces RNA cleavage and is critical for replication of VZV at 37 degrees C but not 33 degrees C. J Virol 76(21):11012–11023PubMedCrossRefGoogle Scholar
  67. 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–S81PubMedCrossRefGoogle Scholar
  68. Schaap A, Fortin JF, Sommer M, Zerboni L, Stamatis S, Ku CC, Nolan GP, Arvin AM (2005) T-cell tropism and the role of ORF66 protein in pathogenesis of varicella-zoster virus infection. J Virol 79(20):12921–12933PubMedCrossRefGoogle Scholar
  69. Schmidbauer M, Budka H, Pilz P, Kurata T, Hondo R (1992) Presence, distribution and spread of productive varicella zoster virus infection in nervous tissues. Brain 115(Pt 2):383–398PubMedCrossRefGoogle Scholar
  70. Schmidt M, Kress M, Heinemann S, Fickenscher H (2003) Varicella-zoster virus isolates, but not the vaccine strain OKA, induce sensitivity to alpha-1 and beta-1 adrenergic stimulation of sensory neurones in culture. J Med Virol 70(Suppl 1):S82–S89PubMedCrossRefGoogle Scholar
  71. Smith FP (1978) Pathological studies of spinal nerve ganglia in relation to intractable intercostal pain. Surg Neurol 10(1):50–53PubMedGoogle Scholar
  72. Somekh E, Levin MJ (1993) Infection of human fetal dorsal root neurons with wild type varicella virus and the Oka strain varicella vaccine. J Med Virol 40(3):241–243PubMedCrossRefGoogle Scholar
  73. Somekh E, Tedder DG, Vafai A, Assouline JG, Straus SE, Wilcox CL, Levin MJ (1992) Latency in vitro of varicella-zoster virus in cells derived from human fetal dorsal root ganglia. Pediatr Res 32(6):699–703PubMedCrossRefGoogle Scholar
  74. Stallings CL, Duigou GJ, Gershon AA, Gershon MD, Silverstein SJ (2006) The cellular localization pattern of Varicella-Zoster virus ORF29p is influenced by proteasome-mediated degradation. J Virol 80(3):1497–1512PubMedCrossRefGoogle Scholar
  75. Steain MC, Sutherland JP, Rodriguez M, Buckland M, Cunningham AL, Slobedman B, Abendroth A (2009) Comparison of naturally infected ganglia during and after herpes zoster. The 34th Annual International Herpesvirus Workshop. Ithaca, New York, USAGoogle Scholar
  76. Theil D, Derfuss T, Paripovic I, Herberger S, Meinl E, Schueler O, Strupp M, Arbusow V, Brandt T (2003) Latent herpesvirus infection in human trigeminal ganglia causes chronic immune response. Am J Pathol 163(6):2179–2184PubMedCrossRefGoogle Scholar
  77. Turnley AM, Starr R, Bartlett PF (2002) Failure of sensory neurons to express class I MHC is due to differential SOCS1 expression. J Neuroimmunol 123(1–2):35–40PubMedCrossRefGoogle Scholar
  78. Vafai A, Murray RS, Wellish M, Devlin M, Gilden DH (1988) Expression of varicella-zoster virus and herpes simplex virus in normal human trigeminal ganglia. Proc Natl Acad Sci USA 85(7):2362–2366PubMedCrossRefGoogle Scholar
  79. van Velzen M, Laman JD, Kleinjan A, Poot A, Osterhaus AD, Verjans GM (2009) Neuron-interacting satellite glial cells in human trigeminal ganglia have an APC phenotype. J Immunol 183(4):2456–2461PubMedCrossRefGoogle Scholar
  80. Verjans GM, Hintzen RQ, van Dun JM, Poot A, Milikan JC, Laman JD, Langerak AW, Kinchington PR, Osterhaus AD (2007) Selective retention of herpes simplex virus-specific T cells in latently infected human trigeminal ganglia. Proc Natl Acad Sci USA 104(9):3496–3501PubMedCrossRefGoogle Scholar
  81. Walters MS, Kyratsous CA, Wan S, Silverstein S (2008) Nuclear import of the varicella-zoster virus latency-associated protein ORF63 in primary neurons requires expression of the lytic protein ORF61 and occurs in a proteasome-dependent manner. J Virol 82(17):8673–8686PubMedCrossRefGoogle Scholar
  82. Watson CP, Deck JH, Morshead C, Van der Kooy D, Evans RJ (1991) Post-herpetic neuralgia: further post-mortem studies of cases with and without pain. Pain 44(2):105–117PubMedCrossRefGoogle Scholar
  83. Watson CP, Morshead C, Van der Kooy D, Deck J, Evans RJ (1988) Post-herpetic neuralgia: post-mortem analysis of a case. Pain 34(2):129–138PubMedCrossRefGoogle Scholar
  84. Weller TH (1953) Serial propagation in vitro of agents producing inclusion bodies derived from varicella and herpes zoster. Proc Soc Exp Biol Med 83(2):340–346PubMedGoogle Scholar
  85. Weller TH, Stoddard MB (1952) Intranuclear inclusion bodies in cultures of human tissue inoculated with varicella vesicle fluid. J Immunol 68(3):311–319PubMedGoogle Scholar
  86. Wigdahl B, Rong BL, Kinney-Thomas E (1986) Varicella-zoster virus infection of human sensory neurons. Virology 152(2):384–399PubMedCrossRefGoogle Scholar
  87. Wroblewska Z, Valyi-Nagy T, Otte J, Dillner A, Jackson A, Sole DP, Fraser NW (1993) A mouse model for varicella-zoster virus latency. Microb Pathog 15(2):141–151PubMedCrossRefGoogle Scholar
  88. Zerboni L, Ku CC, Jones CD, Zehnder JL, Arvin AM (2005) Varicella-zoster virus infection of human dorsal root ganglia in vivo. Proc Natl Acad Sci USA 102(18):6490–6495PubMedCrossRefGoogle Scholar
  89. Zerboni L, Reichelt M, Arvin AM (2010) Varicella-zoster virus neurotropism in SCID mouse–human dorsal root ganglia xenografts. Curr Top Microbiol Immunol doi 10.1007/82_2009_8Google Scholar
  90. Zerboni L, Reichelt M, Jones CD, Zehnder JL, Ito H, Arvin AM (2007) Aberrant infection and persistence of varicella-zoster virus in human dorsal root ganglia in vivo in the absence of glycoprotein I. Proc Natl Acad Sci USA 104(35):14086–14091PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Megan Steain
    • 1
  • Barry Slobedman
    • 2
  • Allison Abendroth
    • 1
  1. 1.Department of Infectious Diseases and ImmunologyUniversity of SydneyCamperdownAustralia
  2. 2.Centre for Virus ResearchWestmead Millennium InstituteWestmeadAustralia

Personalised recommendations