Journal of NeuroVirology

, Volume 9, Issue 2, pp 194–204

Herpes simplex virus-1 and varicella-zoster virus latency in ganglia

  • Bradley M. Mitchell
  • David C. Bloom
  • Randall J. Cohrs
  • Donald H. Gilden
  • Peter G. E. Kennedy
Article

Abstract

Two human alpha-herpesviruses, herpes simplex virus (HSV)-1 and varicella zoster virus (VZV), account for the most frequent and serious neurologic disease caused by any of the eight human herpesviruses. Both HSV-1 and VZV become latent in ganglia. In this review, the authors describe features of latency for these viruses, such as distribution, prevalence, abundance, and configuration of viral DNA in latently infected human ganglia, as well as transcription, translation, and cell type infected. Studies of viral latency in animal models are also discussed. For each virus, remaining questions and future studies to understand the mechanism of latency are discussed with respect to prevention of serious cutaneous, ocular, and neurologic disease produced by virus reactivation.

Keywords

HSV latency VZV 

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References

  1. Abendroth A, Arvin AM (2000). Host response to primary infection. In: Varicella-zoster virus. Arvin AM, Gershon AA (eds). New York: Cambridge University Press, pp 142–156.CrossRefGoogle Scholar
  2. Ahmed M, Lock M, Miller CG, Fraser NW (2002). Regions of the herpes simplex virus type 1 latency-associated transcript that protect cells from apoptosis in vitro and protect neural cells in vivo. J Virol 76: 717–728.PubMedCrossRefGoogle Scholar
  3. Arthur JL, Scarpini CG, Connor V, Lachmann RH, Tolkovsky AM, Efstathiou S (2001). Herpes simplex virus type 1 promoter activity during latency establishment, maintenance, and reactivation in primary dorsal root neurons in vitro. J Virol 75: 3885–3895.PubMedCrossRefGoogle Scholar
  4. Arvin AM, Gershon AA (1996). Live attenuated varicella vaccine. Annu Rev Microbiol 50: 59–100.PubMedCrossRefGoogle Scholar
  5. Balraj V, John TJ (1994). An epidemic of varicella in rural southern India. J Trop Med Hyg 97: 113–116.PubMedGoogle Scholar
  6. Baringer JR, Pisani P (1994). Herpes simplex virus genomes in human nervous system tissue analyzed by polymerase chain reaction. Ann Neurol 36: 823–829.PubMedCrossRefGoogle Scholar
  7. Baringer JR, Swoveland P (1973). Recovery of herpes simplex virus from human trigeminal ganglions. N Engl J Med 288: 648–650.PubMedCrossRefGoogle Scholar
  8. Bastian FO, Rabson AS, Yee CL (1972). Herpesvirus hominis: isolation from human trigeminal ganglion. Science 178: 306.PubMedCrossRefGoogle Scholar
  9. Bloom DC, Devi-Rao GB, Hill JM, Stevens JG, Wagner EK (1994). Molecular analysis of herpes simplex virus type 1 during epinephrine-induced reactivation of latently infected rabbits in vivo. J Virol 68: 1283–1292.PubMedGoogle Scholar
  10. Bloom DC, Hill JM, Devi-Rao G, Wagner EK, Feldman LT, Stevens JG (1996). A 348-base-pair region in the latency-associated transcript facilitates herpes simplex virus type 1 reactivation. J Virol 70: 2449–2459.PubMedGoogle Scholar
  11. Borchers K, Wolfinger U, Lawrenz B, Schellenbach A, Ludwig H (1997). Equine herpesvirus 4 DNA in trigeminal ganglia of naturally infected horses detected by direct in situ PCR. J Gen Virol 78: 1109–1114.PubMedGoogle Scholar
  12. Bratanich AC, Hanson ND, Jones CJ (1992). The latencyrelated gene of bovine herpesvirus 1 inhibits the activity of immediate-early transcription unit 1. Virology 191: 988–991.PubMedCrossRefGoogle Scholar
  13. Bustos DE, Atherton SS (2002). Detection of herpes simplex virus type 1 in human ciliary ganglia. Invest Ophthalmol Vis Sci 43: 2244–2249.PubMedGoogle Scholar
  14. Cai GY, Pizer LI, Levin MJ (2002). Fractionation of neurons and satellite cells from human sensory ganglia in order to study herpesvirus latency. J Virol Methods 104: 21–32.PubMedCrossRefGoogle Scholar
  15. Chen XP, Mata M, Kelley M, Glorioso JC, Fink DJ (2002). The relationship of herpes simplex virus latency associated transcript expression to genome copy number: a quantitative study using laser capture microdissection. J NeuroVirol 8: 204–210.PubMedCrossRefGoogle Scholar
  16. Clarke P, Beer T, Cohrs R, Gilden DH (1995). Configuration of latent varicella-zoster virus DNA. J Virol 69: 8151–8154.PubMedGoogle Scholar
  17. Cohrs RJ, Barbour M, Gilden DH (1996). Varicella-zoster virus (VZV) transcription during latency in human ganglia: detection of transcripts mapping to genes 21, 29, 62, and 63 in a cDNA library enriched for VZV RNA. J Virol 70: 2789–2796.PubMedGoogle Scholar
  18. Cohrs RJ, Barbour MB, Mahalingam R, Wellish M, Gilden DH (1995). Varicella-zoster virus (VZV) transcription during latency in human ganglia: prevalence of VZV gene 21 transcripts in latently infected human ganglia. J Virol 69: 2674–2678.PubMedGoogle Scholar
  19. Cohrs RJ, Randall J, Smith J, Gilden DH, Dabrowski C, van Der KH, Tal-Singer R (2000). Analysis of individual human trigeminal ganglia for latent herpes simplex virus type 1 and varicella-zoster virus nucleic acids using realtime PCR. J Virol 74: 11464–11471.PubMedCrossRefGoogle Scholar
  20. Cohrs RJ, Srock K, Barbour MB, Owens G, Mahalingam R, Devlin ME, Wellish M, Gilden DH (1994). Varicellazoster virus (VZV) transcription during latency in human ganglia: construction of a cDNA library from latently infected human trigeminal ganglia and detection of a VZV transcript. J Virol 68: 7900–7908.PubMedGoogle Scholar
  21. Colgin MA, Smith RL, Wilcox CL (2001). Inducible cyclic AMP early repressor produces reactivation of latent herpes simplex virus type 1 in neurons in vitro. J Virol 75: 2912–2920.PubMedCrossRefGoogle Scholar
  22. 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: 9773–9777.PubMedCrossRefGoogle Scholar
  23. Croen KD, Ostrove JM, Dragovic L, Straus SE (1991). Characterization of herpes simplex virus type 2 latencyassociated transcription in human sacral ganglia and in cell culture. J Infect Dis 163: 23–28.PubMedCrossRefGoogle Scholar
  24. Danaher RJ, Jacob RJ, Miller CS (1999). Establishment of a quiescent herpes simplex virus type 1 infection in neurally-differentiated PC12 cells. J NeuroVirol 5: 258–267.PubMedCrossRefGoogle Scholar
  25. Davison AJ, Scott JE (1986). The complete DNA sequence of varicella-zoster virus. J Gen Virol 67: 1759–1816.PubMedCrossRefGoogle Scholar
  26. de Jong MD, Weel JF, Schuurman T, Wertheim-van Dillen PM, Boom R (2000). Quantitation of varicella-zoster virus DNA in whole blood, plasma, and serum by PCR and electrochemiluminescence. JClin Microbiol 38: 2568–2573.Google Scholar
  27. Debrus S, Sadzot-Delvaux C, Nikkels AF, Piette J, Rentier B (1995). Varicella-zoster virus gene 63 encodes an immediate-early protein that is abundantly expressed during latency. J Virol 69: 3240–3245.PubMedGoogle Scholar
  28. Devi-Rao GB, Bloom DC, Stevens JG, Wagner EK (1994). Herpes simplex virus type 1 DNA replication and gene expression during explant induced reactivation of latently infected murine sensory ganglia. J Virol 68: 12 71—1282.Google Scholar
  29. Dressler GR, Rock DL, Fraser NW (1987). Latent herpes simplex virus type 1 DNA is not extensively methylated in vivo. J Gen Virol 68: 1761–1765.PubMedCrossRefGoogle Scholar
  30. Dueland AN, Ranneberg-Nilsen T, Degre M (1995). Detection of latent varicella zoster virus DNA and human gene sequences in human trigeminal ganglia by in situ amplification combined with in situ hybridization. Arch Virol 140: 2055–2066.PubMedCrossRefGoogle Scholar
  31. Ecker JR, Kudler L, Hyman RW (1984). Variation in the structure of varicella-zoster virus DNA. Intervirology 21: 25–37.PubMedCrossRefGoogle Scholar
  32. Efstathiou S, Minson AC, Field HJ, Anderson JR, Wildy P (1986). Detection of herpes simplex virus-specific DNA sequences in latently infected mice and in humans. J Virol 57: 446–455.PubMedGoogle Scholar
  33. Feldman LT, Ellison AR, Voytek CC, Yang L, Krause P, Margolis TP (2002). Spontaneous molecular reactivation of herpes simplex virus type 1 latency in mice. Proc Natl Acad Sci USA 99: 978–983.PubMedCrossRefGoogle Scholar
  34. Fraser NW, Lawrence WC, Wroblewska Z, Gilden DH, Koprowski H (1981). Herpes simplex type 1 DNA in human brain tissue. Proc Natl Acad Sci USA 78: 6461–6465.PubMedCrossRefGoogle Scholar
  35. Gershon AA, LaRussa P, Hardy I, Steinberg S, Silverstein S (1992). Varicella vaccine: the American experience. J Infect Dis 166(Suppl 1): S63-S68.PubMedCrossRefGoogle Scholar
  36. 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: 145–147.PubMedCrossRefGoogle Scholar
  37. Gilden DH, Hayward AR, Krupp J, Hunter-Laszlo M, Huff JC, Vafai A (1987). Varicella-zoster virus infection of human mononuclear cells. Virus Res 7: 117–129.PubMedCrossRefGoogle Scholar
  38. Gilden DH, Kleinschmidt-DeMasters BK, LaGuardia JJ, Mahalingam R, Cohrs RJ (2000). Neurologic complications of the reactivation of varicella-zoster virus. NEngl JMed 342: 635–645.CrossRefGoogle Scholar
  39. Gilden DH, Vafai A, Shtram Y, Becker Y, Devlin M, Wellish M (1983). Varicella-zoster virus DNA in human sensory ganglia. Nature 306: 478–480.PubMedCrossRefGoogle Scholar
  40. Hawrami K, Harper D, Breuer J (1996). Typing of varicella zoster virus by amplification of DNA polymorphisms. J Virol Methods 57: 169–174.PubMedCrossRefGoogle Scholar
  41. Hayakawa Y, Yamamoto T, Yamanishi K, Takahashi M (1986). Analysis of varicella-zoster virus DNAs of clinical isolates by endonuclease HpaI. J Gen Virol 67: 1817–1829.PubMedCrossRefGoogle Scholar
  42. Hill JM, Dudley JB, Shimomura Y, Kaufman HE (1986). Quantitation and kinetics of induced HSV-1 ocular shedding. CurrEye Res 5: 241–246.Google Scholar
  43. Hyman RW, Ecker JR, Tenser RB (1983). Varicella-zoster virus RNA in human trigeminal ganglia. Lancet 2: 814–816.PubMedCrossRefGoogle Scholar
  44. Jerant AF, DeGaetano JS, Epperly TD, Hannapel AC, Miller DR, Lloyd AJ (1998). Varicella susceptibility and vaccination strategies in young adults. J Am Board Fam Pract 11: 296–306.PubMedGoogle Scholar
  45. Kemble GW, Annunziato P, Lungu O, Winter RE, Cha TA, Silverstein SJ, Spaete RR (2000). Open reading frame S/L of varicella-zoster virus encodes a cytoplasmic protein expressed in infected cells. J Virol 74: 11311–11321.PubMedCrossRefGoogle Scholar
  46. Kennedy PGE, Grinfeld E, Bell JE (2000). Varicella-zoster virus gene expression in latently infected and explanted ganglia. J Virol 74: 11893–11898.PubMedCrossRefGoogle Scholar
  47. Kennedy PGE, Grinfeld E, Gow JW (1998). Latent varicella-zoster virus is located predominantly in neurons in human trigeminal ganglia. Proc Natl Acad Sci USA 95: 4658–4662.PubMedCrossRefGoogle Scholar
  48. Kennedy PGE, Grinfeld E, Gow JW (1999). Latent varicella-zoster virus in human dorsal root ganglia. Virology 258: 451–454.PubMedCrossRefGoogle Scholar
  49. Kennedy PGE, Grinfeld E, Bontems S, Sadzot-Delvaux C (2001). Varicella-zoster virus gene expression in latently infected rat dorsal root ganglia. Virology 289: 218–223.PubMedCrossRefGoogle Scholar
  50. Kleinschmidt-DeMasters BK, Gilden DH (2001). The expanding spectrum of herpesvirus infections of the nervous system. Brain Pathol 11: 440–451.PubMedCrossRefGoogle Scholar
  51. Koskiniemi M, Rantalaiho T, Piiparinen H, von Bonsdorff CH, Farkkila M, Jarvinen A, Kinnunen E, Koskiniemi S, Mannonen L, Muttilainen M, Linnavuori K, Porras J, Puolakkainen M, Raiha K, Salonen EM, Ukkonen P, Vaheri A, Valtonen V (2001). Infections of the central nervous system of suspected viral origin: a collaborative study from Finland. J NeuroVirol 7: 400–408.PubMedCrossRefGoogle Scholar
  52. Kramer MF, Coen DM (1995). Quantification of transcripts from the ICP4 and thymidine kinase genes in mouse ganglia latently infected with herpes simplex virus. J Virol 69: 1389–1399.PubMedGoogle Scholar
  53. Krause PR, Klinman DM (2000). Varicella vaccination: evidence for frequent reactivation of the vaccine strain in healthy children. Nat Med 6: 451–454.PubMedCrossRefGoogle Scholar
  54. Kutish G, Mainprize T, Rock D (1990). Characterization of the latency-related transcriptionally active region of bovine herpesvirus 1 genome. J Virol 64: 5730–5737.PubMedGoogle Scholar
  55. 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: 8571–8577.PubMedGoogle Scholar
  56. Lagunoff M (1995). The regulation of synthesis and properties of the protein product of open reading frame P of the herpes simplex virus 1 genome. J Virol 69: 3615–3623.PubMedGoogle Scholar
  57. Lagunoff M, Roizman B (1994). Expression of a Herpes Simplex Virus 1 open reading frame antisense to the gamma 34.5 gene and transcribed by an RNA 3′ coterminal with the unspliced latency-associated transcript. J Virol 68: 6021–6028.PubMedGoogle Scholar
  58. LaRussa P, Steinberg SP, Shapiro E, Vazquez M, Gershon AA (2000). Viral strain identification in varicella vaccinees with disseminated rashes. Pediatr Infect Dis J 19: 1037–1039.PubMedCrossRefGoogle Scholar
  59. Lokensgard JR, Bloom DC, Dobson AT, Feldman LT (1994). Long-term promoter activity during herpes simplex virus latency. J Virol 68: 7148–7158.PubMedGoogle Scholar
  60. Loutsch JM, Perng GC, Hill JM, Zheng X, Marquart ME, Block TM, Nesburn AB, Wechsler SL (1999). Identical 371-base-pair deletion mutations in the LAT genes of herpes simplex virus type 1 McKrae and 17syn+ results in different in vivo reactivation phenotypes. J Virol 73: 767–771.PubMedGoogle Scholar
  61. 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: 10980–10984.PubMedCrossRefGoogle Scholar
  62. 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: 7080–7085.PubMedCrossRefGoogle Scholar
  63. Mahalingam R, Kennedy PG, Gilden DH (1999). The problems of latent varicella zoster virus in human ganglia: precise cell location and viral content. J NeuroVirol 5: 445–448.PubMedCrossRefGoogle Scholar
  64. Mahalingam R, Traina-Dorge V, Wellish M, Smith J, Gilden DH (2002). Naturally acquired simian varicella virus infection in African green monkeys. J Virol 76: 8548–8550.PubMedCrossRefGoogle Scholar
  65. 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: 2122–2124.PubMedCrossRefGoogle Scholar
  66. 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: 2381–2384.PubMedGoogle Scholar
  67. Mahalingam R, Wellish M, Wolf W, Dueland AN, Cohrs R, Vafai A, Gilden DH (1990). Latent varicella zoster virus DNA in human trigeminal and thoracic ganglia. N Engl J Med 323: 627–631.PubMedCrossRefGoogle Scholar
  68. 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: 444–448.PubMedCrossRefGoogle Scholar
  69. Mainka C, Fuss B, Geiger H, Hofelmayr H, Wolff MH (1998). Characterization of viremia at different stages of varicella-zoster virus infection. J Med Virol 56: 91–98.PubMedCrossRefGoogle Scholar
  70. Margolis TP, Dawson CR, LaVail JH (1992). Herpes simplex viral infection of the mouse trigeminal ganglion. Immunohistochemical analysis of cell populations. Invest Ophthalmol Vis Sci 33: 259–267.PubMedGoogle Scholar
  71. McMillan DJ, Kay J, Mills JS (1997). Characterization of the proteinase specified by varicella-zoster virus gene 33. J Gen Virol 78: 2153–2157.PubMedGoogle Scholar
  72. Mehta A, Maggioncalda J, Bagasra O, Thikkavarapu S, Saikumari P, Valyi-Nagy T, Fraser NW, Block TM (1995). In situ DNA PCR and RNA hybridization detection of herpes simplex virus sequences in trigeminal ganglia of latently infected mice. Virology 206: 633–640.PubMedCrossRefGoogle Scholar
  73. Meier JL, Holman RP, Croen KD, Smialek JE, Straus SE (1993). Varicella-zoster virus transcription in human trigeminal ganglia. Virology 193: 193–200.PubMedCrossRefGoogle Scholar
  74. Mellerick DM, Fraser NW (1987). Physical state of the latent herpes simplex virus genome in a mouse model system: evidence suggesting an episomal state. Virology 158: 265–275.PubMedCrossRefGoogle Scholar
  75. Mitchell WJ, Deshmane SL, Dolan A, McGeoch DJ, Fraser NW (1990). Characterization of herpes simplex virus type 2 transcription during latent infection of mouse trigeminal ganglia. J Virol 64: 5342–5348.PubMedGoogle Scholar
  76. Muir WB, Nichols R, Breuer J (2002). Phylogenetic analysis of varicella-zoster virus: evidence of intercontinental spread of genotypes and recombination. J Virol 76: 1971–1979.PubMedCrossRefGoogle Scholar
  77. Nesburn AB, Elliot JH, Leibowitz HM (1967). Spontaneous reactivation of experimental herpes simplex keratitis in rabbits. Arch Ophthalmol 78: 523–529.PubMedGoogle Scholar
  78. Perng GC, Jones C, Ciacci-Zanella J, Stone M, Henderson G, Yukht A, Slanina SM, Hofman FM, Ghiasi H, Nesburn AB, Wechsler SL (2000b). Virus-induced neuronal apoptosis blocked by the herpes simplex virus latency-associated transcript. Science 287: 1500–1503.PubMedCrossRefGoogle Scholar
  79. Perng GC, Maguen B, Jin L, Mott KR, Kurylo J, BenMohamed L, Yukht A, Osorio N, Nesburn AB, Henderson G, Inman M, Jones C, Wechsler SL (2002). A novel herpes simplex virus type 1 transcript (AL-RNA) antisense to thje 5′ end of the latency associated transcript produces a protein in infected rabbits. J Virol 76: 8003–8010.PubMedCrossRefGoogle Scholar
  80. Perng GC, Slanina SM, Ghiasi H, Nesburn AB, Wechsler SL (1996). A 371-nucleotide region between the herpes simplex virus type 1 (HSV-1) LAT promoter and the 2-kilobase LAT is not essential for efficient spontaneous reactivation of latent HSV-1. J Virol 70: 2014–2018.PubMedGoogle Scholar
  81. Perng GC, Slanina SM, Ghiasi H, Nesburn AB, Wechsler SL (2001). The effect of latency-associated transcript on the herpes simplex virus type 1 latency-reactivation pheno-type is mouse strain-dependent. J Gen Virol 82: 1117–1122.PubMedGoogle Scholar
  82. Perng GC, Slanina SM, Yukht A, Ghiasi H, Nesburn AB, Wechsler SL (2000a). The latency-associated transcript gene enhances establishment of herpes simplex virus type 1 latency in rabbits. J Virol 74: 1885–1891.PubMedCrossRefGoogle Scholar
  83. Pevenstein SR, Williams RK, McChesney D, Mont EK, Smialek JE, Straus SE (1999). Quantitation of latent varicella-zoster virus and herpes simplex virus genomes in human trigeminal ganglia. J Virol 73: 10514–10518.PubMedGoogle Scholar
  84. Preston VG, Kennard J, Rixon FJ, Logan AJ, Mansfield RW, McDougall IM (1997). Efficient herpes simplex virus type 1 (HSV-1) capsid formation directed by the varicella-zoster virus scaffolding protein requires the carboxy-terminal sequences from the HSV-1 homologue. J Gen Virol 78: 1633–1646.PubMedGoogle Scholar
  85. Priola SA, Gustafson DP, Wagner EK, Stevens JC (1990). A major portion of the latent pseudorabies virus genome is transcribed in trigeminal ganglia of pigs. J Virol 64: 4755–4760.PubMedGoogle Scholar
  86. Randall G, Lagunoff M, Roizman B (2000). Herpes simplex virus 1 open reading frames O and P are not necessary for establishment of latent infection in mice. J Virol 74: 9019–9022.PubMedCrossRefGoogle Scholar
  87. Rantalaiho T, Farkkila M, Vaheri A, Koskiniemi M (2001). Acute encephalitis from 1967 to 1991. J Neurol Sci 184: 169–177.PubMedCrossRefGoogle Scholar
  88. Rawson H, Crampin A, Noah N (2001). Deaths from chickenpox in England and Wales 1995–7: analysis of routine mortality data. BMJ 323: 1091–1093.PubMedCrossRefGoogle Scholar
  89. Robertson GR, Scott NA, Miller JM, Sabine M, Zheng M, Bell CW, Whalley JM (1991). Sequence characteristics of a gene in equine herpesvirus 1 homologous to glycoprotein H of herpes simplex virus. DNA Seq 1: 241–249.PubMedGoogle Scholar
  90. Rock DL, Fraser NW (1983). Detection of HSV-1 genome in central nervous system of latently infected mice. Nature 302: 523–525.PubMedCrossRefGoogle Scholar
  91. Rock DL, Fraser NW (1985). Latent herpes simplex virus type 1 DNA contains two copies of the virion DNA joint region. J Virol 55: 849–852.PubMedGoogle Scholar
  92. Roizman B, Knipe DM (2001). Herpes simplex viruses and their replication. In: Fields virology, 4th ed, vol 2. Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (eds). Philadephia: Lippincott-Raven, pp 2399–2460.Google Scholar
  93. Ross J, Williams M, Cohen JI (1997). Disruption of the varicella-zoster virus dUTPase and the adjacent ORF9A gene results in impaired growth and reduced syncytia formation in vitro. Virology 234: 186–195.PubMedCrossRefGoogle Scholar
  94. Sawtell NM (1997). Comprehensive quantification of herpes simplex virus latency at the single-cell level. J Virol 71: 5423–5431.PubMedGoogle Scholar
  95. Sawtell NM, Poon DK, Tansky CS, Thompson RL (1998). The latent herpes simplex virus type 1 genome copy number in individual neurons is virus strain specific and correlates with reactivation. J Virol 72: 5343–5350.PubMedGoogle Scholar
  96. Sawtell NM, Thompson RL (1992). Rapid in vivo reactivation of herpes simplex virus in latently infected murine ganglionic neurons after transient hyperthermia. J Virol 66: 2150–2156.PubMedGoogle Scholar
  97. Sedarati F, Margolis TP, Stevens JG (1993). Latent infection can be established with drastically restricted transcription and replication of the HSV-1 genome. Virology 192: 687–691.PubMedCrossRefGoogle Scholar
  98. Spivack JG, Fraser NW (1987). Detection of herpes simplex virus type 1 transcripts during latent infection in mice. J Virol 61: 3841–3847.PubMedGoogle Scholar
  99. Stephanopoulos DE, Kappes JC, Bernstein DI (1988). Enhanced in vitro reactivation of herpes simplex virus type 2 from latently infected guinea-pig neural tissues by 5-azacytidine. J Gen Virol 69: 1079–1083.PubMedCrossRefGoogle Scholar
  100. Stevens JG, Cook ML (1971). Latent herpes simplex virus in spinal ganglia. Science 173: 843.PubMedCrossRefGoogle Scholar
  101. Stevens JG, Wagner EK, Devi-Rao GB, Cook ML, Feldman LT (1987). RNA complementary to a herpesvirus alpha gene mRNA is prominent in latently infected neurons. Science 235: 1056–1059.PubMedCrossRefGoogle Scholar
  102. Stroop WG, Rock DL, Fraser NW (1984). Localization of herpes simplex virus in the trigeminal and olfactory systems of the mouse central nervous system during acute and latent infections by in situ hybridization. Lab Invest 51: 27–38.PubMedGoogle Scholar
  103. Su YH, Meegalla RL, Chowhan R, Cubitt C, Oakes JE, Lausch RN, Fraser NW, Block TM (1999). Human corneal cells and other fibroblasts can stimulate the appearance of herpes simplex virus from quiescently infected PC12 cells. J Virol 73: 4171–4180.PubMedGoogle Scholar
  104. Takayama N, Minamitani M, Takayama M (1997). High incidence of breakthrough varicella observed in healthy Japanese children immunized with live attenuated varicella vaccine (Oka strain). Acta Paediatr Jpn 39: 663–668.PubMedGoogle Scholar
  105. Thomas SK, Lilley CE, Latchman DS, Coffin RS (2002). A protein encoded by the herpes simplex virus (HSV) type 1 2-kilobase latency-associated transcript is phosphorylated, localized to the nucleus, and overcomes the repression of expression from exogenous promoters when inserted into the quiescent HSV genome. J Virol 76: 4056–4067.PubMedCrossRefGoogle Scholar
  106. Thompson RL, Sawtell NM (2001). Herpes simplex virus type 1 latency-associated transcript gene promotes neuronal survival. J Virol 75: 6660–6675.PubMedCrossRefGoogle Scholar
  107. Warren KG, Devlin M, Gilden DH, Wroblewska Z, Koprowski H, Brown SM, Subak-Sharpe J (1978). Herpes simplex virus latency in patients with multiple sclerosis, lymphoma and normal humans. In: Oncogenesis and herpesvirus III, part 2: Cell-virus interactions, host response to herpesvirus infection and associated tumors, role of co-factors. de-The G, Henle W, Rapp R. (eds.). International agency for research on cancer, Lyon, France, pp. 765–768.Google Scholar
  108. Weibel RE, Neff BJ, Kuter BJ, Guess HA, Rothenberger CA, Fitzgerald AJ, Connor KA, McLean AA, Hilleman MR, Buynak EB (1984). Live attenuated varicella virus vaccine. Efficacy trial in healthy children. N Engl J Med 310: 1409–1415.PubMedCrossRefGoogle Scholar
  109. Wilcox CL, Johnson EM Jr (1988). Characterization of nerve growth factor-dependent herpes simplex virus latency in neurons in vitro. J Virol 62: 393–399.PubMedGoogle Scholar
  110. Yang L, Voytek CC, Margolis TP (2000). Immunohistochemical analysis of primary sensory neurons latently infected with herpes simplex virus type 1. J Virol 74: 209–217.PubMedCrossRefGoogle Scholar
  111. Youssoufian H, Hammer SM, Hirsch MS, Mulder C (1982). Methylation of the viral genome in an in vitro model of herpes simplex virus latency. Proc Natl Acad Sci USA 79: 2207–2210.PubMedCrossRefGoogle Scholar
  112. Zhu J, Kang W, Marquart ME, Hill JM, Zheng X, Block TM, Fraser NW (1999). Identification of a novel 0.7 kb polyadenylated transcript in the LAT promoter region of HSV-1 that is strain specific and may contribute to virulence. Virology 265: 296–307.PubMedCrossRefGoogle Scholar

Copyright information

© Journal of NeuroVirology, Inc. 2003

Authors and Affiliations

  • Bradley M. Mitchell
    • 1
  • David C. Bloom
    • 2
  • Randall J. Cohrs
    • 3
  • Donald H. Gilden
    • 3
    • 4
  • Peter G. E. Kennedy
    • 5
  1. 1.Cullen Eye Institute, Department of Ophthalmology and Department of Molecular Virology and MicrobiologyBaylor College of MedicineHoustonUSA
  2. 2.Molecular Genetics and Microbiology, College of MedicineUniversity of FloridaGainesvilleUSA
  3. 3.Department of NeurologyUniversity of Colorado Health Sciences CenterDenverUSA
  4. 4.Department of MicrobiologyUniversity of Colorado Health Sciences CenterDenverUSA
  5. 5.Department of NeurologyUniversity of Glasgow, Institute of Neurological Sciences, Southern General Hospital NHS TrustGlasgowScotland, UK

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