The PK domain of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10) is required for immediate-early gene expression and virus growth

Journal of Virology

Volumn 72, Issue 11, 1998, Pages 9131-9141

  Smith, C C ^a   Peng, T ^a,b   Kulka, M ^a   Aurelian, L ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEOTIDE REDUCTASE;

ANIMAL CELL; ARTICLE; ENZYME ACTIVITY; HERPES SIMPLEX VIRUS 2; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIROGENESIS; VIRUS GENE; VIRUS REPLICATION;

EID: 0031684594     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.11.9131-9141.1998     Document Type: Article

References (83)

1. Ace, C. I., T. A. McKee, M. Ryan, J. M. Cameron, and C. M. Preston. 1989. Construction and characterization of a herpes simplex virus type 1 mutant unable to transinduce immediate-early gene expression. J. Virol. 63:2260-2269.
2. Ali, M. A., S. S. Prakash, and R. J. Jariwalla. 1992. Localization of the antigenic sites and intrinsic protein kinase domain within a 300 amino acid segment of the ribonucleotide reductase large subunit from herpes simplex virus tvpe 2. Virology 187:360-367.
3. Anderson, K. P., R. J. Frink, G. B. Devi, B. H. Gaylord, and E. K. Wagner. 1981. Detailed characterization of the mRNA mapping in the HindIII fragment K region of the herpes simplex virus type 1 genome. J. Virol. 37:1011-1027.
4. Aurelian, L., P. Terzano, C. C. Smith, T. D. Chung, A. Shamsuddin, S. Costa, and C. Orlandi. 1989. Amino-terminal epitope of herpes simplex virus type 2 ICP10 protein as a molecular diagnostic marker for cervical intraepithehal neoplasia. Cancer Cells 7:187-191.
5. Aurelian, L., et al. Unpublished data.
6. Aurelian, L. 1992. Herpes simplex viruses, p. 473-494. In S. Specter, and G. Lancz (ed.), Clinical virology manual, 2nd ed. Elsevier Science Publishers, New York, N.Y.
7. Bacchetti, S., M. J. Evelegh, B. Muirhead, C. S. Sartari, and D. Huszar. 1984. Immunological characterization of herpes simplex virus type 1 and 2 polypeptide(s) involved in viral ribonucleotide reductase activity. J. Gen. Virol. 49:591-593.
8. Cameron, J. M., I. McDougall, H. W. Marsden, V. G. Preston, D. M. Ryan, and S. H. Subak-Sharpe. 1988. Ribonucleotide reductase encoded by herpes simplex virus is a determinant of the pathogenicity of the virus in mice and a valid antiviral target. J. Virol. 69:2607-2612.
9. Campbell, M. E. M., J. W. Palfreyman, and C. M. Preston. 1984. Identification of herpes simplex virus DNA sequences which encode a trans-acting polypeptide responsible for stimulation of immediate early transcription. J. Mol. Biol. 180:1-19.
10. Chen, S. H., M. F. Kramer, P. A. Schaffer, and D. M. Coen. 1997. A viral function represses accumulation of transcripts from productive-cycle genes in mouse ganglia latently infected with herpes simplex virus. J. Virol. 71: 5878-5884.
11. Chung, T. D., J. P. Wymer, C. C. Smith, M. Kulka, and L. Aurelian. 1989. Protein kinase activity associated with the large subunit of the herpes simplex virus type 2 ribonucleolide reductase (ICP10). J. Virol. 63:3389-3398.
12. Chung, T. D., J. P. Wymer, M. Kulka, C. C. Smith, and L. Aurelian. 1990. Myristylation and polylysine-mediated activation of the protein kinase domain of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10). Virology 179:168-178.
13. Chung, T. D., J. H. Luo, J. P. Wymer, C. C. Smith, and L. Aurelian. 1991. Leucine repeats in the large subunit of herpes simplex virus type 2 ribonucleotide reductase (RR; ICP10) are involved in RR activity and subunit complex formation. J. Gen. Virol. 72:1139-1144.
14. Cohen, G. H. 1972. Ribonucleotide reductase activity of synchronized KB cells infected with herpes simplex virus. J. Virol. 9:408-418.
15. Conner, J., J. Cooper, J. Furlong, and J. B. Clements. 1992. An autophosphorylating but not transphosphorylating activity is associated with the unique N terminus of the herpes simplex virus type 1 ribonucleotide reductase large subunit. J. Virol. 66:7511-7516.
16. Conner, J., J. Macfarlene, H. Lankinen, and H. Marsden. 1992. The unique N-terminus of the herpes simplex virus type 1 large subunit is not required for ribonucleotide reductase activity. J. Gen. Virol. 73:103-112.
17. Cooper, J., J. Conner, and J. B. Clements. 1995. Characterization of the novel protein kinase activity present in the R1 subunit of herpes simplex virus ribonucleotide reductase. J. Virol. 69:4979-4985.
18. DeLuca, N. A., and P. A. Schaffer. 1985. Activation of immediate-early, early, and late promoters by temperature-sensitive and wild-type forms of herpes simplex virus type 1 protein 1CP4. Mol. Cell. Biol. 5:1997-2008.
19. Desai, P., R. Ramakrishnan, Z. W. Lin, B. Osak, J. C. Glorioso, and M. Levine. 1993. The RR1 gene of herpes simplex virus type 1 is uniquely trans activated by ICP0 during infection. J. Virol. 67:6125-6135.
20. Dixon, R. A. F., and P. A. Schaffer. 1980. Fine-structure mapping and functional analysis of temperature-sensitive mutants in the gene encoding the herpes simplex virus type 1 immediate early protein VP175. J. Virol. 36:189-203.
21. Everett, R. E., C. M. Preston, and N. W. Stow. 1991. Functional and genetic analysis of the role of Vmw110 in herpes simplex virus replication, p. 49-76. In E. K. Wagner (ed.), Herpesvirus transcription. CRC Press, Inc., Boca Raton, Fla.
22. Fawl, R. L., and B. Roizman. 1993. Induction of reactivation of herpes simplex virus in murine sensory ganglia in vivo by cadmium. J. Virol. 67: 7025-7031.
23. Feng, C. P., M. Kulka, C. C. Smith, and L. Aurelian. 1996. Herpes simplex virus-mediated activation of human immunodeficiency virus is inhibited by oligonucleotide methylphosphonates that target immediate-early mRNAs 1 and 3. Antisense Nucleic Acid Drug Dev. 6:25-35.
24. Fisher, R. P., P. Jin, H. M. Chamberlin, and D. O. Morgan. 1995. Alternative mechanisms of CAK assembly require an assembly factor or an activating kinase. Cell 83:47-57.
25. Frame, M. C., H. S. Marsden, and B. M. Dutia. 1985. The ribonucleotide reductase induced by herpes simplex virus type 1 involves minimally a complex of two polypeptides (136K and 38K). J. Gen. Virol. 66:1581-1587.
26. 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.
27. Goldstein, D. J., and S. K. Weller. 1988. Factor(s) present in the 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.
28. Harris-Hamilton, E., and S. L. Bachenheimer. 1985. Accumulation of herpes simplex virus tvpe 1 RNAs of different kinetic classes in the cytoplasm of infected cells. J. Virol. 53:144-151.
29. Hermann, C. H., M. O. Gold, and A. P. Rice. 1995. Viral tansactivators specifically target distinct cellular protein kinases that phosphorylate the RNA polymerase II C-terminal domain. Nucleic Acids Res. 24:501-504.
30. Honess, R. W., and B. Roizman. 1974. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups viral proteins. J. Virol. 14:8-19.
31. Hunter, J. C. R., C. C. Smith, D. Bose, M. Kulka, R. Broderick, and L. Aurelian. 1995. Intracellular internalization and signaling pathways triggered by the large subunit of HSV-2 ribonucleotide reductase (ICP10). Virology 210:345-360.
32. Idowu, A. D., E. B. Fraser-Smith, K. L. Paflenberger, and R. C. Herman. 1992. Deletion of herpes simplex virus type 1 ribonucleotide reductase gene alters virulence and latency in vitro. Antiviral Res. 17:145-156.
33. Ingemarson, R., and H. Lankinen. 1987. The herpes simplex virus type 1 ribonucleotide reductase is a tight complex of the type alpha 2 and beta 2 composed of 40K and 140K proteins, of which the latter shows multiple forms due to proteolysis. Virology 156:417-422.
34. 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.
35. Jin, P., and N. R. Ringertz. 1990. Cadmium induces transcription of proto-oncogenes c-jun and c-myc in rat L6 myoblasts. J. Biol. Chem. 265:14061-14064.
36. 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.
37. Langelier, Y., and G. Buttin. 1981. Characterization of ribonucleotide reductase induction in BHK-21/C13 Syrian hamster cell line upon infection by herpes simplex virus. J. Gen. Virol. 57:21-31.
38. Lankinen, H., E. Telford, D. MacDonald, and H. Marsden. 1989. The unique N-terminal domain of the large subunit of herpes simplex virus ribonucleotide reductase is preferentially sensitive to proteolysis. J. Gen. Virol. 70: 3159-3169.
39. LeBlanc, J. F., and J. Hiscott. 1992. Differential response of human interferon-beta promoter elements to trans-activation by HSV VP16 and IRF-1. Virology 186:760-763.
40. 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.
41. Leopardi, R., and B. Riozman. 1996. Functional interaction and colocalization of the herpes simplex virus 1 major regulatory protein with EAP, a nucleolar-ribosomal protein. Proc. Natl. Acad. Sci. USA 93:4562-4576.
42. Luo, J., and L. Aurelian. 1992. The transmembrane helical segment but not the invariant lysine is required for the kinase activity of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10). J. Biol. Chem. 267:9645-9653.
43. Luo, J. H., C. C. Smith, M. Kulka, and L. Aurelian. 1991. A truncated protein kinase domain of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10) expressed in Escherichia coli. J. Biol. Chem. 266:20976-20983.
44. Marsden, H. S., I. K. Crombie, and J. H. Subak-Sharpe. 1976. Control of protein synthesis in herpesvirus-infected cells: analysis of the polypeptides induced by wild type and sixteen temperature sensitive mutants of strain 17. J. Gen. Virol. 31:347-372.
45. McCarthy, A. M., L. McMahan, and P. A. Schaffer. 1989. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient. J. Virol. 63:18-27.
46. McLauchlan, J., and J. B. Clements. 1983. DNA sequence homology between two co-linear loci on the HSV genome which have different transforming abilities. EMBO J. 2:1953-1961.
47. Nelson, J. W., J. Zhu, C. C. Smith, M. Kulka, and L. Aurelian. 1996. ATP and SH3 binding sites in the protein kinase of the large subunit of herpes simplex virus type 2 of ribonucleotide reductase (ICP10). J. Biol. Chem. 271:17021-17027.
48. O'Hare, P., and G. S. Hayward. 1985. Evidence for a direct role for both the 175,000- and 110,000-molecular-weight immediate-early proteins of herpes simplex virus in the transactivation of delayed-early promoters. J. Virol. 53:751-760.
49. O'Reilly, D., O. Hanscombe, and P. O'Hare. 1997. A single serine residue at position 375 of VP16 is critical for complex assembly with Oct-1 and HCF and is a target of phosphorylation by casein kinase II. EMBO J. 16:2420-2430.
50. Overton, H., D. McMillan, L. Hope, and P. Wong-Kai-In. 1994. Production of host shutoff-defective mutants of herpes simplex virus type 1 by inactivation of the UL13 gene. Virology 202:97-106.
51. Peng, T., J. R. C. Hunter, and J. W. Nelson. 1996. The novel protein kinase of the RR1 subunit of herpes simplex virus has autophosphorylation and transphosphorylation activity that differs in its ATP requirements for HSV-1 and HSV-2. Virology 216:184-196.
52. Pereira, L., M. H. Wolff, M. Fenwick, and B. Roizman. 1977. Regulation of herpesvirus macromolecular synthesis. V. Properties of a polypeptides made in HSV-1 and HSV-2 infected cells. Virology 77:733-749.
53. Pignatti, P. F., E. Cassai, G. Meneguzzi, N. Chencinger, and G. Milanesi. 1979. Herpes simplex virus DNA isolation from infected cells with a novel procedure. Virology 93:260-264.
54. Post, L. E., S. Mackem, and B. Roizman. 1981. Regulation of a genes of herpes simplex virus: expression of chimeric genes produced by fusion of thymidine kinase with a gene promoters. Cell 24:555-565.
55. 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 α (immediate early) viral polypeptides. J. Virol. 46: 498-512.
56. Read, G. S., B. M. Karr, and K. Knight. 1993. Isolation of a herpes simplex virus type 1 mutant with a deletion in the virion host shutoff gene and identification of multiple forms of the vhs (UL41) polypeptide. J. Virol. 67:7149-7160.
57. Rice, S. A., M. C. Long, V. Lam, and C. A. Spencer. 1994. RNA polymerase II is aberrantly phosphorylated and localized to viral replication compartments following herpes simplex virus infection. J. Virol. 68:988-1001.
58. Rice, S. A., M. C. Long, V. Lam, P. A. Schaffer, and C. Spencer. 1995. Herpes simplex virus immediate-early protein ICP22 is required for viral modification of host RNA polymerase II and establishment of the normal viral transcription program. J. Virol. 69:5550-5559.
59. Russell, J., N. D. Stow, E. C. Stow, and C. M. Preston. 1987. Herpes simplex virus genes involved in latency in vitro. J. Gen. Virol. 68:3009-3018.
60. 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.
61. Samaniego, L. A., A. L. Webb, and N. A. DeLuca. 1995. Functional interactions between herpes simplex virus immediate-early proteins during infection: gene expression as a consequence of ICP27 and different domains of ICP4. J. Virol. 69:5705-5715.
62. Smith, C. C., L. Aurelian, M. P. Reddy, P. S. Miller, and P. O. P. Ts'o. 1986. Antiviral effect of an oligo(nucleoside methylphosphonate) complementary to the splice junction of herpes simplex virus type 1 immediate early pre-mRNAs 4 and 5. Proc. Natl. Acad. Sci. USA 83:2787-2791.
63. Smith, C. C., J. P. Wymer, J. H. Luo, and L. Aurelian. 1991. Genomic sequences homologous to the protein kinase region of the bifunctional herpes simplex virus type 2 protein ICP10. Virus Genes 5:3:215-226.
64. Smith, C. C., M. Kulka, J. P. Wymer, T. D. Chung, and L. Aurelian. 1992. Expression of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10) is required for virus growth and neoplastic transformation. J. Gen. Virol. 73:1417-1428.
65. Smith, C. C., J. H. Luo, J. C. R. Hunter, J. V. Ordonez, and L. Aurelian. 1994. The transmembrane domain of the large subunit of HSV-2 ribonucleotide reductase (ICP10) is required for the transformation-related signaling pathways that involve ras activation. Virology 200:598-612.
66. Smith, C. C., and L. Aurelian. 1997. The large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10) is associated with the virion tegument and has PK activity. Virology 234:235-242.
67. Smith, C. C., et al. Unpublished data.
68. Sodeik, B., M. W. Ebersold, and A. Helenius. 1997. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136:1007-1021.
69. Strnad, B., and L. Aurelian. 1978. Proteins of herpesvirus type 2. III. Isolation and immunologic characterization of a large molecular weight viral protein. Virology 87:401-415.
70. Strnad, B. C., and L. Aurelian. 1976. Proteins of herpesvirus type 2.1. Virion, non-virion and antigenic polypeptides in infected cells. Virology 69:438-452.
71. Strnad, B. C., and L. Aurelian. 1976. Proteins of herpesvirus type 2. II. Studies demonstrating a correlation between a tumor-associated antigen (AG-4) and a virion protein. Virology 73:244-258.
72. Sze, P., and R. C. Herman. 1992. The herpes simplex virus type 1 ICP6 gene is regulated by a "leaky" early promoter. Virus Res. 2:141-152.
73. Tal-Singer, R., T. M. Lasner, W. Podrzucki, A. Skokotas, J. J. Laeary, 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.
74. Valyi-Nagy, T., S. Deshmane, A. Dillner, and N. W. Fraser. 1991. Induction of cellular transcription factors in trigeminal ganglia of mice by corneal scarification, herpes simplex virus type 1 infection, and explantation of trigeminal ganglia. J. Virol. 65:4142-4152.
75. Wagner, E. 1983. Transcription patterns in HSV infections, p. 239-276. In G. Klein (ed.), Advances in viral oncology. Raven Press, New York, N.Y.
76. Wang, K., L. Pesnicak, and S. E. Straus. 1997. Mutations in the 5′ end of the herpes simplex virus type 2 latency-associated transcript (LAT) promoter affect LAT expression in vivo but not the rate of spontaneous reactivation of genital herpes. J. Virol. 71:7903-7910.
77. Watson, R. J., C. M. Preston, and J. B. Clements. 1979. Separation and characterization of herpes simplex virus type 1 immediate-early mRNA's. J. Virol. 31:42-52.
78. Wilcox, K. W., A. Kohn, E. Sklyanskaya, and B. Roizman. 1980. Herpes simplex virus phosphoproteins. I. Phosphate cycles on and off some viral polypeptides and can alter their affinity for DNA. J. Virol. 33:167-182.
79. Wymer, J. P., T. D. Chung, Y.-N. Chang, G. S. Hayward, and L. Aurelian. 1989. Identification of immediate-early-type cis-response elements in the promoter for the ribonucleotide reductase large subunit from herpes simplex virus type 2. J. Virol. 63:2773-2784.
80. Wymer, J. P., C. M. J. Aprhys, T. C. Chung, T. P. Feng, M. Kulka, and L. Aurelian. 1992. Immediate early and functional AP-1 cis-response elements are involved in the transcriptional regulation of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10). Virus Res. 23:253-270.
81. Yankulov, K., J. Blau, T. Purton, S. Roberts, and D. L. Bentley. 1994. Transcriptional elongation by RNA polymerase II is stimulated by transactivators. Cell 77:749-759.
82. Yao, F., and R. J. Courtney. 1992. Association of ICP0 but not ICP27 with purified virions of herpes simplex virus type 1. J. Virol. 66:2709-2716.
83. Zhu, J., and L. Aurelian. 1997. AP-1 cis-response elements are involved in basal expression and Vmw110 transactivation of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP0). Virology 231:301-312.