Comparison of herpes simplex virus reactivation in ganglia in vivo and in explants demonstrates quantitative and qualitative differences

Journal of Virology

Volumn 78, Issue 14, 2004, Pages 7784-7794

  Sawtell, N M ^a   Thompson, R L ^b  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS DNA; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYTOCHROME C; GEMININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; EXPLANT; HERPES SIMPLEX; HISTOPATHOLOGY; HYPERTHERMIA; MALE; MOUSE; NERVE DEGENERATION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS CELL INTERACTION; VIRUS REACTIVATION; VIRUS REPLICATION;

ANIMALS; CULTURE TECHNIQUES; HERPESVIRUS 1, HUMAN; IN SITU NICK-END LABELING; MICE; NEURONS; TRIGEMINAL GANGLION; VIRUS ACTIVATION; VIRUS LATENCY; VIRUS REPLICATION;

EID: 3142767683     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.14.7784-7794.2004     Document Type: Article

References (45)

1. Berkelaar, M., D. B. Clarke, Y. C. Wang, G. M. Bray, and A. J. Aguayo. 1994. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 14:4368-4374.
2. Burnet, F. M., and S. W. Williams. 1939. Herpes simplex: a point of view. Med. J. Aust. 1:637-642.
3. Carr, D. J., S. Noisakran, W. P. Halford, N. Lukacs, V. Asensio, and I. L. Campbell. 1998. Cytokine and chemokine production in HSV-1 latently infected trigeminal ganglion cell cultures: effects of hyperthermic stress. J. Neuroimmunol. 85:111-121.
4. Devi-Rao, G. B., D. C. Bloom, J. G. Stevens, and E. K. Wagner. 1994. Herpes simplex virus type 1 DNA replication and gene expression during explant-induced reactivation of latently infected murine sensory ganglia. J. Virol. 68:1271-1282.
5. Groves, M. J., T. Christopherson, B. Giometto, and F. Scaravilli. 1997. Axotomy-induced apoptosis in adult rat primary sensory neurons. J. Neurocytol. 26:615-624.
6. Halford, W. P., B. M. Gebhardt, and D. J. Carr. 1996. Mechanisms of herpes simplex virus type 1 reactivation. J. Virol. 70:5051-5060.
7. Hill, J. M., J. B. Dudley, Y. Shimomura, and H. E. Kaufman. 1986. Quantitation and kinetics of induced HSV-1 ocular shedding. Curr. Eye Res. 5:241-246.
8. Klein, R. J. 1982. Treatment of experimental latent herpes simplex virus infections with acyclovir and other antiviral compounds. Am. J. Med. 73:138-142.
9. Knotts, F. B., M. L. Cook, and J. G. Stevens. 1973. Latent herpes simplex virus in the central nervous system of rabbits and mice. J. Exp. Med. 138:740-744.
10. Kosz-Vnenchak, M., J. Jacobson, D. M. Coen, and D. M. Knipe. 1993. Evidence for a novel regulatory pathway for herpes simplex virus gene expression in trigeminal ganglion neurons. J. Virol. 67:5383-5393.
11. Leib, D. A., K. L. Ruffner, C. Hildebrand, P. A. Schaffer, G. E. Wright, and D. M. Coen. 1990. Specific inhibitors of herpes simplex virus thymidine kinase diminish reactivation of latent virus from explanted murine ganglia. Antimicrob. Agents Chemother. 34:1285-1286.
12. Luque, J. M., W. B. Adams, and J. G. Nicholls. 1998. Procedures for whole-mount immunohistochemistry and in situ hybridization of immature mammalian CNS. Brain Res. Protoc. 2:165-173.
13. Lygerou, Z., and P. Nurse. 2000. Cell cycle. License withheld-geminin blocks DNA replication. Science 290:2271-2273.
14. McGarry, T. J., and M. W. Kirschner. 1998. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93:1043-1053.
15. McLennan, J. L., and G. Darby. 1980. Herpes simplex virus latency: the cellular location of virus in dorsal root ganglia and the fate of the infected cell following virus activation. J. Gen. Virol. 51:233-243.
16. Pereira, R. A., D. C. Tscharke, and A. Simmons, 1994, Upregulation of class I major histocompatibility complex gene expression in primary sensory neurons, satellite cells, and Schwann cells of mice in response to acute but not latent herpes simplex virus infection in vivo. J. Exp. Med. 180:841-850.
17. Plummer, G., C. R. Goodheart, M. Miyagi, G. R. Skinner, M. E. Thouless, and P. Wildy. 1974. Herpes simplex viruses: discrimination of types and correlation between different characteristics. Virology 60:206-216.
18. Rezuchova, I., M. Kudelova, V. Durmanova, A. Vojvodova, J. Kosovsky, and J. Rajcani. 2003. Transcription at early stages of herpes simplex virus 1 infection and during reactivation. Intervirology 46:25-34.
19. Sawtell, N. M. 1997. Comprehensive quantification of herpes simplex virus latency at the single-cell level. J. Virol. 71:5423-5431.
20. Sawtell, N. M. 1998. The probability of in vivo reactivation of herpes simplex virus type 1 increases with the number of latently infected neurons in the ganglia. J. Virol. 72:6888-6892.
21. Sawtell, N. M. 2003. Quantitative analysis of herpes simplex virus reactivation in vivo demonstrates that reactivation in the nervous system is not inhibited at early times postinoculation. J. Virol. 77:4127-4138.
22. Sawtell, N. M., D. I. Bernstein, and L. R. Stanberry. 1999. A temporal analysis of acyclovir inhibition of induced herpes simplex virus type 1 in vivo reactivation in the mouse trigeminal ganglia. J. Infect. Dis. 180:821-823.
23. Sawtell, N. M., D. K. Poon, C. S. Tansky, and R. L. Thompson. 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.
24. Sawtell, N. M., and R. L. Thompson. 1992. Herpes simplex virus type 1 latency-associated transcription unit promotes anatomical site-dependent establishment and reactivation from latency. J. Virol. 66:2157-2169.
25. Sawtell, N. M., and R. L. Thompson. 1992. Rapid in vivo reactivation of herpes simplex virus in latently infected murine ganglionic neurons after transient hyperthermia. J. Virol. 66:2150-2156.
26. Schang, L. M., A. Bantly, and P. A. Schaffer. 2002. Explant-induced reactivation of herpes simplex virus occurs in neurons expressing nuclear cdk2 and cdk4. J. Virol. 76:7724-7735.
27. Sears, A. E., and B. Roizman. 1990. Amplification by host cell factors of a sequence contained within the herpes simplex virus 1 genome. Proc. Natl. Acad. Sci. USA 87:9441-9444.
28. Shimeld, C., D. L. Easty, and T. J. Hill. 1999. Reactivation of herpes simplex virus type 1 in the mouse trigeminal ganglion: an in vivo study of virus antigen and cytokines. J. Virol. 73:1767-1773.
29. Shimeld, C., T. Hill, B. Blyth, and D. Easty. 1989. An improved model of recurrent herpetic eye disease in mice. Curr. Eye Res. 8:1193-1205.
30. Shimeld, C., J. L. Whiteland, N. A. Williams, D. L. Easty, and T. J. Hill. 1996. Reactivation of herpes simplex virus type 1 in the mouse trigeminal ganglion: an in vivo study of virus antigen and immune cell infiltration. J. Gen. Virol. 77:2583-2590.
31. Speck, P. G., and A. Simmons. 1992. Synchronous appearance of antigen-positive and latently infected neurons in spinal ganglia of mice infected with a virulent strain of herpes simplex virus. J. Gen. Virol. 73:1281-1285.
32. Stevens, J. G., and M. L. Cook. 1971. Latent herpes simplex virus in spinal ganglia of mice. Science 173:843-945.
33. Tal-Singer, R., T. M. Lasner, W. Podrzucki, A. Skokotas, J. J. Leary, S. L. Berger, and N. W. Fraser. 1997. Gene expression during reactivation of herpes simplex virus type 1 from latency in the peripheral nervous system is different from that during lytic infection of tissue cultures. J. Virol. 71:5268-5276.
34. Tanaka, S., H. Minagawa, Y. Toh, Y. Liu, and R. Mori. 1994. Analysis by RNA-PCR of latency and reactivation of herpes simplex virus in multiple neuronal tissues. J. Gen. Virol. 75:2691-2698.
35. Tenser, R. B., K. A. Hay, and W. A. Edris. 1989. Latency-associated transcript but not reactivatable virus is present in sensory ganglion neurons after inoculation of thymidine kinase-negative mutants of herpes simplex virus type 1. J. Virol. 63:2861-2865.
36. Thompson, R. L., M. L. Cook, G. B. Devi-Rao, E. K. Wagner, and J. G. Stevens. 1986. Functional and molecular analyses of the avirulent wild-type herpes simplex virus type 1 strain KOS. J. Virol. 58:203-211.
37. Thompson, R. L., S. K. Rogers, and M. A. Zerhusen. 1989. Herpes simplex virus neurovirulence and productive infection of neural cells is associated with a function which maps between 0.82 and 0.832 map units on the HSV genome. Virology 172:435-450.
38. Thompson, R. L., and N. M. Sawtell. 2001. Herpes simplex virus type 1 latency-associated transcript gene promotes neuronal survival. J. Virol. 75:6660-6675.
39. Thompson, R. L., and N. M. Sawtell. 1997. The herpes simplex virus type 1 latency-associated transcript gene regulates the establishment of latency. J. Virol. 71:5432-5440.
40. Thompson, R. L., and N. M. Sawtell. 2000. Replication of herpes simplex virus type 1 within trigeminal ganglia is required for high frequency but not high viral genome copy number latency. J. Virol. 74:965-974.
41. Thompson, R. L., and J. G. Stevens. 1983. Biological characterization of a herpes simplex virus intertypic recombinant which is completely and specifically non-neurovirulent, Virology 131:171-179.
42. Wagner, E. K., and D. C. Bloom. 1997. Experimental investigation of herpes simplex virus latency. Clin. Microbiol. Rev. 10:419-443.
43. Whitley, R. J. 2001. Herpes simplex viruses, p. 2461-2510. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, vol. 2. Lippincott Williams & Wilkins, Philadelphia, Pa.
44. Wilcox, C. L., R. L. Smith, C. R. Freed, and E. M. Johnson, Jr. 1990. Nerve growth factor-dependence of herpes simplex virus latency in peripheral sympathetic and sensory neurons in vitro. J. Neurosci. 10:1268-1275.
45. Wohlschlegel, J. A., B. T. Dwyer, S. K. Dhar, C. Cvetic, J. C. Walter, and A. Dutta. 2000. Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290:2309-2312.