Experimental models to study varicella-zoster virus infection of neurons

Current Topics in Microbiology and Immunology

Volumn 342, Issue 1, 2010, Pages 211-228

  Steain, Megan ^a   Slobedman, Barry ^b   Abendroth, Allison ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b WESTMEAD HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN INFECTION; HERPES ZOSTER; HUMAN; IN VITRO STUDY; NEUROBLASTOMA CELL; NEUROPATHIC PAIN; NONHUMAN; POSTHERPETIC NEURALGIA; PRIMARY INFECTION; PRIORITY JOURNAL; SENSORY NERVE CELL; SPINAL GANGLION; VARICELLA ZOSTER VIRUS; VIRUS LATENCY; VIRUS REACTIVATION; VIRUS REPLICATION; ANIMAL; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; REVIEW; SENSORY RECEPTOR; VIROLOGY;

ANIMALIA; HERPES ZOSTER; HUMAN HERPESVIRUS 3; RODENTIA;

ANIMALS; GANGLIA, SPINAL; HERPES ZOSTER; HERPESVIRUS 3, HUMAN; HUMANS; SENSORY RECEPTOR CELLS;

EID: 79952057920     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/82-2010-15     Document Type: Article

References (90)

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):200-209
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-S51 (Pubitemid 28514269)
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):834-844
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):2643-2652
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):90-97 (Pubitemid 20175057)
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-S78 (Pubitemid 36368850)
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):915-926 (Pubitemid 40037606)
8. Cohen JI (2010) Rodent models of varicella-zoster virus neurotropism. Curr Top Microbiol Immunol doi 10.1007/82-2010-11
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):306-316 (Pubitemid 28384044)
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):62-71 (Pubitemid 34158052)
11. Cohrs RJ, Gilden DH (2007) Prevalence and abundance of latently transcribed varicella-zoster virus genes in human ganglia. J Virol 81(6):2950-2956 (Pubitemid 46447058)
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):6660-6665 (Pubitemid 36666859)
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):223-227 (Pubitemid 41126216)
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):9773-9777 (Pubitemid 19027207)
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):52-58 (Pubitemid 41773651)
16. Denny-Brown D, Adam R, Fitzgerald P (1944) Pathological features of herpes zoster. Am Med Assoc Arch Dermatol 75:193-196
17. Dworkin RH, Nagasako EM, Johnson RW, Griffin DR (2001) Acute pain in herpes zoster: the famciclovir database project. Pain 94(1):113-119 (Pubitemid 32907563)
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):991-1003 (Pubitemid 30660487)
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 varicellazoster virus. J Gen Virol 80(Pt 9):2433-2436 (Pubitemid 29408372)
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):97-111 (Pubitemid 41566589)
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, USA
22. Gershon AA, Chen J, Gershon MD (2008) A model of lytic, latent, and reactivating varicellazoster virus infections in isolated enteric neurons. J Infect Dis 197(Suppl 2):S61-S65 (Pubitemid 351590148)
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):145-147 (Pubitemid 33020688)
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):377-380 (Pubitemid 17137902)
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):478-480 (Pubitemid 14235569)
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):105-117 (Pubitemid 8263975)
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):755-767 (Pubitemid 44366677)
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):6752-6756 (Pubitemid 46878079)
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):85-90 (Pubitemid 38681022)
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):553-560
31. Hanani M (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev 48(3):457-476 (Pubitemid 40725401)
32. Head H, Campbell W (1900) The pathology of herpes zoster and its bearing on sensory localization. Brain 23:353-523
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):69-72 (Pubitemid 28481532)
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):8503-8511 (Pubitemid 29441714)
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):1025-1031 (Pubitemid 43062913)
36. Hood C, Cunningham AL, Slobedman B, Boadle RA, Abendroth A (2003) Varicella-zoster virusinfected 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):12852-12864 (Pubitemid 37430679)
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): 1022-1030 (Pubitemid 44521803)
38. Hyman RW, Ecker JR, Tenser RB (1983) Varicella-zoster virus RNA in human trigeminal ganglia. Lancet 2(8354):814-816 (Pubitemid 13009267)
39. Joly E, Mucke L, Oldstone MB (1991) Viral persistence in neurons explained by lack of major histocompatibility class I expression. Science 253(5025):1283-1285 (Pubitemid 21917279)
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):218-223 (Pubitemid 33141001)
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):4658-4662 (Pubitemid 28207969)
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):1037-1043 (Pubitemid 32290792)
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):8571-8577 (Pubitemid 29441721)
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):801-811 (Pubitemid 47057285)
45. LawsonSN(2005) The peripheral sensory nervous system: dorsal root ganglion neurons. In:Dyck PJ, Thomas PK (eds) Peripheral Neuropathy. Elsevier Saunders, Philadelphia, PA, pp 163-202
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):6979-6987 (Pubitemid 36666890)
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):78-83 (Pubitemid 23002840)
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):10980-10984
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):7080-7085 (Pubitemid 28278110)
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):2122-2124 (Pubitemid 26079891)
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):2381-2384 (Pubitemid 23088418)
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):444-448
53. Matsunaga Y, Yamanishi K, Takahashi M (1982) Experimental infection and immune response of guinea pigs with varicella-zoster virus. Infect Immun 37(2):407-412 (Pubitemid 12100018)
54. Merville-Louis MP, Sadzot-Delvaux C, Delree P, Piette J, Moonen G, Rentier B (1989) Varicellazoster virus infection of adult rat sensory neurons in vitro. J Virol 63(7):3155-3160 (Pubitemid 19156039)
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):11821-11826 (Pubitemid 33063273)
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):5934-5944 (Pubitemid 29274881)
57. Myers MG, Duer HL, Hausler CK (1980) Experimental infection of guinea pigs with varicellazoster virus. J Infect Dis 142(3):414-420 (Pubitemid 10024579)
58. Myers MG, Stanberry LR, Edmond BJ (1985) Varicella-zoster virus infection of strain 2 guinea pigs. J Infect Dis 151(1):106-113 (Pubitemid 15192887)
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):6529-6533 (Pubitemid 24200695)
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):420-426 (Pubitemid 26269496)
61. Reichelt M, Zerboni L, Arvin AM (2008) Mechanisms of varicella-zoster virus neuropathogenesis in human dorsal root ganglia. J Virol 82(8):3971-3983 (Pubitemid 351521233)
62. Ross RA, Spengler BA, Biedler JL (1983) Coordinate morphological and biochemical interconversion of human neuroblastoma cells. J Natl Cancer Inst 71(4):741-747 (Pubitemid 14232388)
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-S47 (Pubitemid 28514268)
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-S20 (Pubitemid 26163678)
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):83-89 (Pubitemid 20175056)
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):11012-11023 (Pubitemid 35176218)
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-S81 (Pubitemid 36368851)
68. Schaap A, Fortin JF, Sommer M, Zerboni L, Stamatis S, Ku CC, Nolan GP, ArvinAM(2005) T-cell tropism and the role of ORF66 protein in pathogenesis of varicella-zoster virus infection. J Virol 79(20):12921-12933 (Pubitemid 41433211)
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):383-398
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-S89 (Pubitemid 36368852)
71. Smith FP (1978) Pathological studies of spinal nerve ganglia in relation to intractable intercostal pain. Surg Neurol 10(1):50-53 (Pubitemid 8369666)
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):241-243 (Pubitemid 23204102)
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):699-703
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):1497-1512 (Pubitemid 43134106)
75. Steain MC, Sutherland JP, Rodriguez M, BucklandM,Cunningham AL, Slobedman B, AbendrothA (2009) Comparison of naturally infected ganglia during and after herpes zoster. The 34th Annual International Herpesvirus Workshop. Ithaca, New York, USA
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):2179-2184 (Pubitemid 37466462)
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):35-40 (Pubitemid 34195604)
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):2362-2366 (Pubitemid 24315892)
79. van Velzen M, Laman JD, Kleinjan A, Poot A, Osterhaus AD, Verjans GM (2009) Neuroninteracting satellite glial cells in human trigeminal ganglia have an APC phenotype. J Immunol 183(4):2456-2461
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):3496-3501 (Pubitemid 46364187)
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):8673-8686
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):105-117
83. Watson CP, Morshead C, Van der Kooy D, Deck J, Evans RJ (1988) Post-herpetic neuralgia: postmortem analysis of a case. Pain 34(2):129-138
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):340-346
85. Weller TH, Stoddard MB (1952) Intranuclear inclusion bodies in cultures of human tissue inoculated with varicella vesicle fluid. J Immunol 68(3):311-319
86. Wigdahl B, Rong BL, Kinney-Thomas E (1986) Varicella-zoster virus infection of human sensory neurons. Virology 152(2):384-399 (Pubitemid 16065069)
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):141-151
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):6490-6495 (Pubitemid 40617470)
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 10.1007/82-2009-8
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):14086-14091 (Pubitemid 350003339)