Interferons regulate the phenotype of wild-type and mutant herpes simplex viruses in vivo

Journal of Experimental Medicine

Volumn 189, Issue 4, 1999, Pages 663-672

  Leib, David A ^a   Harrison, Travis E ^a   Laslo, Kathleen M ^a   Machalek, Michael A ^a   Moorman, Nathaniel J ^a   Virgin, Herbert W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Herpes simplex virus mutants; Interferons; Mice; Pathogenesis

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GAMMA INTERFERON; INTERFERON RECEPTOR; RIBONUCLEOTIDE REDUCTASE; THYMIDINE KINASE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EYE; GANGLION; GENE MUTATION; HERPES SIMPLEX VIRUS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; VIRUS INFECTION; VIRUS REPLICATION;

ANIMALS; CERCOPITHECUS AETHIOPS; CORNEA; IMMEDIATE-EARLY PROTEINS; IMMUNOCOMPETENCE; INTERFERON TYPE II; INTERFERON-ALPHA; INTERFERON-BETA; INTERFERONS; KERATITIS, HERPETIC; MICE; MICE, KNOCKOUT; PHENOTYPE; RECEPTOR, INTERFERON ALPHA-BETA; RECEPTORS, INTERFERON; RIBONUCLEOTIDE REDUCTASES; SIMPLEXVIRUS; THYMIDINE KINASE; TRIGEMINAL GANGLION; UBIQUITIN-PROTEIN LIGASES; VERO CELLS; VIRAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

EID: 0033557288     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.4.663     Document Type: Article

References (65)

1. Wildy, P., H.J. Field, and A.A. Nash. 1982. Classical herpes latency revisited. In Virus Persistence, B.W.J. Mahy, A.C. Minson, and G.K. Darby, editors. Cambridge University Press, Cambridge, UK. 133-167.
2. Leib, D.A., D.M. Coen, C.L. Bogard, K.A. Hicks, D.R. Yager, D.M. Knipe, K.L. Tyler, and P.A. Schaffer. 1989. Immediate-early regulatory gene mutants define different stages in the establishment and reactivation of herpes simplex virus latency. J. Virol. 63:759-768.
3. Perng, G.C., E.C. Dunkel, P.A. Geary, S.M. Slanina, H. Ghiasi, R. Kaiwar, A.B. Nesburn, and S.L. Wechsler. 1994. The latency-associated transcript gene of herpes simplex virus type 1 (HSV-1) is required for efficient in vivo spontaneous reactivation of HSV-1 from latency. J. Virol. 68:8045-8055.
4. Coen, D.M., M. Kosz-Vnenchak, J.G. Jacobson, D.A. Leib, C.L. Bogard, P.A. Schaffer, K.L. Tyler, and D.M. Knipe. 1989. Thymidine kinase negative herpesvirus mutants establish latency in mouse trigeminal ganglia, but do not reactivate. Proc. Natl. Acad. Sci. USA. 86:4736-4740.
5. + T cell response. J. Exp. Med. 187:341-348.
6. Yamada, Y., H. Kimura, T. Morishima, T. Daikoku, K. Maeno, and Y. Nishiyama. 1991. The pathogenicity of ribonucleotide reductase-null mutants of herpes simplex virus type 1 in mice. J. Infect. Dis. 164:1091-1097.
7. McGeoch, D.J., and P.A. Schaffer. 1993. Herpes simplex virus. In Genetic Maps: Locus Maps of Complex Genomes. 3rd Edition. S.J. O'Brien, editor. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 1.147-1.156.
8. Chou, J., and B. Roizman. 1990. Mapping of herpes simplex virus-1 neurovirulence to gl 34.5, a gene nonessential for growth in culture. Science. 250:1262-1266.
9. Bolovan, C.A., N.M. Sawtell, and R.L. Thompson. 1994. ICP34.5 mutants of herpes simplex virus type 1 strain 17syn+ are attenuated for neurovirulence in mice and for replication in confluent primary mouse embryo cell cultures. J. Virol. 68:48-55.
10. Tenser, R.B., and W.A. Edris. 1987. Trigeminal ganglion infection by thymidine kinase-negative mutants of herpes simplex virus after in vivo complementation. J. Virol. 61:2171-2174.
11. Su, Y.H., J.E. Oakes, and R.N. Lausch. 1993. Mapping the genetic region coding for herpes simplex virus resistance to mouse interferon alpha/beta. J. Gen. Virol. 74:2325-2332.
12. Narita, M., Y. Ando, S. Soushi, T. Karata, and Y. Arao. 1998. The BgIII-N fragment of herpes simplex virus type 2 contains a region responsible for resistance to antiviral effects of interferon. J. Gen. Virol. 79:565-572.
13. Sacks, W.R., and P.A. Schaffer. 1987. Deletion mutants in the gene encoding the herpes simplex virus type 1 immediate-early protein ICP0 exhibit impaired growth in cell culture. J. Virol. 61:829-839.
14. Stow, N.D , and E.C. Stow. 1986. Isolation and characterization of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw 110. J. Gen. Virol. 67:2571-2585.
15. Goldstein, D.J., and S.K. Weller. 1988. Herpes simplex virus type 1-induced ribonucleotide reductase activity is dispensable for virus growth and DNA synthesis: isolation and characterization of an ICP6 lacZ insertion mutant. J. Virol. 62:196-205.
16. Field, H.J., and P. Wildy. 1978. The pathogenicity of thymidine kinase-deficient mutants of herpes simplex virus in mice. J. Hyg. 81:267-277.
17. Everett, R.D. 1984. Transactivation of transcription by a herpes simplex virus product: requirement for two HSV-1 immediate-early polypeptides for maximal activity. EMBO (Eur. Mol. Biol. Organ.) J. 3:3135-3141.
18. Gelman, I.H., and S. Silverstein. 1985. Identification of immediate-early genes from herpes simplex virus that transactivate the virus thymidine kinase gene. Proc. Natl. Acad. Sci. USA. 82:5265-5269.
19. O'Hare, P., and G.S. Hayward. 1985. Three trans-acting regulatory proteins of herpes simplex virus modulate immediate-early gene expression in a pathway involving positive and negative feedback regulation. J. Virol. 56:723-733.
20. Jordan, R., and P.A. Schaffer. 1997. Activation of gene expression by herpes simplex virus type 1 ICP0 occurs at the level of mRNA synthesis. J. Virol. 71:6850-6862.
21. Samaniego, L.A., N. Wu, and N.A. DeLuca. 1997. The herpes simplex virus immediate-early protein ICP0 affects transcription from the viral genome and infected-cell survival in the absence of ICP4 and ICP27. J. Virol. 71:4614-4625.
22. Maul, G.G., H.H. Guldner, and J.G. Spivack. 1993. Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0). J. Gen. Virol. 74:2679-2690.
23. Lees-Miller, S.P., M.C. Long, M.A. Kilvert, V. Lam, S.A. Rice, and C.A. Spencer. 1996. Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0. J. Virol. 70: 7471-7477.
24. Cai, W., and P.A. Schaffer. 1991. A cellular function can enhance gene expression and plating efficiencies of a mutant defective in the gene for ICP0, a transactivating protein of herpes simplex virus type 1. J. Virol. 65:4078-4090.
25. Clements, J.B., and N.D. Stow. 1989. A herpes simplex virus type 1 mutant containing a deletion within immediate early gene 1 is latency-competent in mice. J. Gen. Virol. 70:2501-2506.
26. Jamieson, A.T., and J.H. Subak-Sharpe. 1974. Biochemical studies on the herpes simplex virus-specified deoxypyrimidine kinase activity. J. Gen. Virol. 24:481-492.
27. Bachetti, S., M.J. Everlegh, and B. Muirhead. 1986. Identification and separation of the two subunits of the herpes simplex virus ribonucleotide reductase. J. Virol. 57:1177-1181.
28. Jacobson, J.G., D.A. Leib, D.J. Goldstein, C.L. Bogard, P.A. Schaffer, S.K. Weller, and D.M. Coen. 1989. A herpes simplex virus ribonucleotide reductase deletion mutant is defective for productive, acute and reactivatable latent infections of mice and for replication in mouse cells. Virology. 173:276-283.
29. Strelow, L.I., and D.A. Leib. 1995. Role of the virion host shutoff (vhs) of herpes simplex virus type 1 in latency and pathogenesis. J. Virol. 69:6779-6786.
30. Read, G.S., and N. Frenkel. 1983. Herpes simplex virus mutants defective in the virion-associated shutoff of host polypeptide synthesis and exhibiting abnormal synthesis of a (immediate early) viral polypeptides. J. Virol. 46:498-512.
31. Strelow, L.I., T. Smith, and D.A. Leib. 1997. The virion host shutoff function of herpes simplex virus type 1 plays a role in corneal invasion and functions independently of the cell cycle. Virology. 231:28-34.
32. He, B., J. Chou, D.A. Lieberman, B. Huffman, and B. Roizman. 1996. The carboxy terminus of murine MyD116 gene substitutes for the corresponding domain of the g134.5 gene of herpes simplex virus to preclude the premature shutoff of total protein synthesis in infected human cells. J. Virol. 70:84-90.
33. Chou, J., J.-J. Chen, M. Gross, and B. Roizman. 1995. Association of a Mr 90,000 phosphoprotein with protein kinase PKR in cells exhibiting enhanced phosphorylation of translation initiation factor eIF-2 and premature shutoff of protein synthesis after infection with g134.5 mutants of herpes simplex virus 1. Proc. Natl. Acad. Sci. USA. 92:10516-10520.
34. Perng, G.C., R.L. Thompson, N.M. Sawtell, W.E. Taylor, S.M. Slanina, H. Ghiasi, R. Kaiwar, A.B. Nesburn, and S.L. Wechsler. 1995. An avirulent ICP34.5 deletion mutant of herpes simplex virus type 1 is capable of in vivo spontaneous reactivation. J. Virol. 69:3033-3041.
35. Spivack, J.G., M.U. Fareed, T. Valyi-Nagy, T.C. Nash, J.S. O'Keefe, R.M. Gesser, E.A. McKie, A.R. MacLean, N.W. Fraser, and S.M. Brown. 1995. Replication, establishment of latent infection, expression of the latency-associated transcripts and explant reactivation of herpes simplex virus type 1 gamma 34.5 mutants in a mouse eye model. J. Gen. Virol. 76:321-332.
36. 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.
37. Oberman, F., and A. Panet. 1988. Inhibition of transcription of herpes simplex virus immediate early genes in interferon-treated human cells. J. Gen. Virol. 69:1167-1177.
38. Mittnacht, S., P. Straub, H. Kirchner, and H. Jacobsen. 1988. Interferon treatment inhibits onset of herpes simplex virus immediate-early transcription. Virology. 164:201-210.
39. Nicholl, M.J., and C.M. Preston. 1992. Inhibition of herpes simplex virus type 1 immediate-early gene expression by alpha interferon is not VP16 specific. J. Virol. 70:6336-6339.
40. Balish, M.J., M.E. Abrams, A.M. Pumfery, and C.R. Brandt. 1992. Enhanced inhibition of herpes simplex virus type 1 growth in human corneal fibroblasts by combinations of interferon-alpha and-gamma. J. Infect. Dis. 166:1401-1403.
41. Bouley, D.M., S. Kanangat, and B.T. Rouse. 1996. The role of the innate immune system in the reconstituted SCID mouse model of herpetic stromal keratitis. Clin. Immunol. Immunopathol. 80:23-30.
42. Halford, W.P., L.A. Veress, B.M. Gebhart, and D.J. Carr. 1997. Innate and acquired immunity to herpes simplex virus type 1. Virology. 236:328-337.
43. Taylor, J.L., S.D. Little, and W.J. O'Brien. 1998. The comparative anti-herpes simplex virus effects of human interferons. J. Interferon Cytokine Res. 18:159-165.
44. Bouley, D.M., S. Kanangat, W. Wire, and B.T. Rouse. 1995. Characterization of herpes simplex virus type-1 infection and herpetic stromal keratitis development in IFN-gamma knockout mice. J. Immunol. 155:3964-3971.
45. Geiger, K.D., T.C. Nash, S. Sawyer, T. Krahl, G. Patstone, J.C. Reed, S. Krajewski, D. Dalton, M.J. Buchmeier, and N. Sarvetnick. 1997. Interferon-gamma protects against herpes simplex virus type 1-mediated neuronal death. Virology. 238:189-197.
46. Rader, K.A., C.E. Ackland-Berglund, J. Kelvin Miller, J.S. Pepose, and D.A. Leib. 1993. In vivo characterization of site-directed mutations in the promoter of the herpes simplex virus type 1 latency-associated transcripts. J. Gen. Virol. 74:1859-1869.
47. Kaplitt, M.G., J.G. Tjuvajev, D.A. Leib, J. Berk, K.D. Pettigrew, J.B. Posner, D.W. Pfaff, S.D. Rabkin, and R.G. Blasberg. 1994. Mutant herpes simplex virus induced regression of tumors growing in immunocompetent rats. J. Neuro-Oncol. 19:137-147.
48. Muller, U., U. Steinhoff, L.F. Reis, S. Hemmi, J. Pavlovic, R.M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science. 264: 1918-1921.
49. Davido, D.J., and D.A. Leib. 1996. Role of cis-acting sequences of the ICP0 promoter of herpes simplex virus type 1 in viral pathogenesis, latency and reactivation, J. Gen. Virol. 77:1853-1863.
50. Cantin, E.M., D.R. Hinton, J. Chen, and H. Openshaw. 1995. Gamma interferon expression during acute and latent nervous system infection by herpes simplex virus type 1. J. Virol. 69:4898-4905.
51. Arvidson, B. 1977. Retrograde axonal transport of horseradish peroxidase from cornea to trigeminal ganglion. Acta Neuropathol. 38:49-51.
52. Su, Y.H., J.E. Oakes, and R.N. Lausch. 1990. Ocular avirulence of a herpes simplex virus type 1 strain is associated with heightened sensitivity to alpha/beta Interferon. J. Virol. 64: 2187-2192.
53. Bukowski, J.F., and R.M. Welsh. 1986. The role of natural killer cells and interferon in resistance to acute infection of mice with herpes simplex virus type 1. J. Immunol. 136:3481-3485.
54. Valyi-Nagy, T., R.M. Gesser, B. Raengsakulrach, S.L. Deshmane, B.P. Randazzo, A.J. Dillner, and N.W. Fraser. 1994. A thymidine kinase-negative HSV-1 strain establishes a persistent infection in SCID mice that features uncontrolled peripheral replication but only marginal nervous system involvement. Virology. 199:484-490.
55. Valyi-Nagy, T., M.U. Fareed, J.S. O'Keefe, R.M. Cesser, A.R. MacLean, S.M. Brown, J.G. Spivack, and N.W. Fraser. 1994. The herpes simplex virus type 1 strain 17+ gamma 34.5 deletion mutant 1716 is avirulent in SCID mice. J. Gen. Virol. 75:2059-2063.
56. Heise, M.T., and H.W. Virgin. 1995. The T cell independent role of gamma interferon and tumor necrosis factor alpha in macrophage activation during murine cytomegalovirus and herpes simplex virus infections. J. Virol. 69:904-909.
57. Kramer, M.F., and D.M. Coen. 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.
58. Tenser, R.B., A. Gaydos, and K.A. Hay. 1996. Reactivation of thymidine kinase-defective herpes simplex virus is enhanced by nucleoside. J. Virol. 70:1271-1276.
59. O'Brien, W.J., K. Piotrowski, and J.L Taylor. 1995. Effect of interferon-alpha on the steady-state levels of thymine, thymidine, guanine, and guanosine metabolites in herpes simplex virus-type 1-infected cells. Intervirology. 38:249-255.
60. McKie, E.A., D.I. Graham, and S.M. Brown. 1998. Selective astrocytic transgene expression in vitro and in vivo from the GFAP promoter in a HSV RL1 null mutant vector - potential glioblastoma targeting. Gene Ther. 5:440-450.
61. Mineta, T., S.D. Rabkin, T. Yazaki, W.D. Hunter, and R.L. Martuza. 1995. Attenuated multi-mutated herpes simplex virus-1 for the treatment of malignant gliomas. Nat. Med. 1:938-943.
62. Tigges, M.A., S. Leng, D.C. Johnson, and R.L. Burke. 1996. Human herpes simplex virus (HSV)-specific CDS+ CTL clones recognize HSV-2-infected fibroblasts after treatment with IFN-gamma or when virion host shutoff functions are disabled. J. Immunol. 156:3901-3910.
63. Tenser, R.B., and R.H. Hyman. 1987. Latent herpesvirus infections of neurons in guinea pigs and humans. Yale J. Biol. Med. 60:159-167.
64. Smith, K.O. 1964. Relationships between the envelope and the infectivity of herpes simplex virus. Proc. Soc. Exp. Biol. Med. 115:814-816.
65. Goldstein, D.J., and S.K. Weller. 1988. Factor(s) present in herpes simplex virus type 1-infected cells can compensate for the loss of the large subunit of the viral ribonucleotide reductase: characterization of an ICP6 deletion mutant. Virology. 166:41-51.