Herpes Simplex Virus Type 1 Primary Envelopment: UL34 Protein Modification and the US3-UL34 Catalytic Relationship

Journal of Virology

Volumn 78, Issue 1, 2004, Pages 399-412

  Ryckman, Brent J ^a   Roller, Richard J ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN UL34; UNCLASSIFIED DRUG; US3 KINASE; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL NUCLEUS MEMBRANE; CELL TYPE; CONTROLLED STUDY; ENZYME SUBSTRATE; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; MEMBRANE BINDING; MEMBRANE VESICLE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; VIRION; VIROGENESIS; VIRUS NUCLEOCAPSID;

ANIMALS; BASE SEQUENCE; CELL LINE; CERCOPITHECUS AETHIOPS; EPITHELIAL CELLS; HERPESVIRUS 1, HUMAN; HUMANS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC; VERO CELLS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 0346365295     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.1.399-412.2004     Document Type: Article

References (42)

1. Asano, S., T. Honda, F. Goshima, D. Watanabe, Y. Miyake, Y. Sugiura, and Y. Nishiyama. 1999. US3 protein kinase of herpes simplex virus type 2 plays a role in protecting corneal epithelial cells from apoptosis in infected mice. J. Gen. Virol. 80:51-56.
2. Baines, J. D., R. J. Jacob, L. Simmerman, and B. Roizman. 1995. The herpes simplex virus 1 UL11 proteins are associated with cytoplasmic and nuclear membranes and with nuclear bodies of infected cells. J. Virol. 69:825-833.
3. Baines, J. D., and B. Roizman. 1992. The UL11 gene of herpes simplex virus 1 encodes a function that facilitates nucleocapsid envelopment and egress from cells. J. Virol. 66:5168-5174.
4. Baines, J. D., P. L. Ward, G. Campadelli-Fiume, and B. Roizman. 1991. The UL20 gene of herpes simplex virus 1 encodes a function necessary for viral egress. J. Virol. 65:6414-6424.
5. Bibor-Hardy, V., M. Suh, M. Pouchelet, and R. Simard. 1982. Modifications of the nuclear envelope of BHK cells after infection with herpes simplex virus type 1. J. Gen. Virol. 63:81-94.
6. Bjerke, S. L., J. M. Cowan, J. K. Kerr, A. E. Reynolds, J. D. Baines, and R. J. Roller. 2003. Effects of charged cluster mutations on the function of herpes simplex virus type 1 UL34 protein. J. Virol. 77:7601-7610.
7. Brandimarti, R., and B. Roizman. 1997. US9, a stable lysine-less herpes simplex virus 1 protein, is ubiquitinated before packaging into virions and associates with proteasomes. Proc. Natl. Acad. Sci. USA 94:13973-13978.
8. Courvalin, J. C., N. Segil, G. Blobel, and H. J. Worman. 1992. The lamin B receptor of the inner nuclear membrane undergoes mitosis specific phosphorylation and is a substrate for the p34cdc2-type protein kinase. J. Biol. Chem. 267:19035-19038.
9. Daikoku, T., R. Kurachi, T. Tsurumi, and Y. Nishiyama. 1994. Identification of a target protein of US3 protein kinase of herpes simplex virus type 2. J. Gen. Virol. 75:2065-2068.
10. Ejercito, P. M., E. D. Kieff, and B. Roizman. 1968. Characteristics of herpes simplex virus strains differing in their effect on social behavior of infected cells. J. Gen. Virol. 2:357-364.
11. Fuchs, W., B. G. Klupp, H. Granzow, and T. C. Mettenleiter. 1997. The UL20 gene product of pseudorabies virus functions in virus egress. J. Virol. 71:5639-5646.
12. Galvan, V., and B. Roizman. 1998. Herpes simplex virus 1 induces and blocks apoptosis at multiple steps during infection and protects cells from exogenous inducers in a cell-type-dependent manner. Proc. Natl. Acad. Sci. USA 95:3931-3936.
13. Granzow, H., B. G. Klupp, W. Fuchs, J. Veits, N. Osterrieder, and T. C. Mettenleiter. 2001. Egress of alphaherpesviruses: comparative ultrastructural study. J. Virol. 75:3675-3684.
14. Hanks, S. K., A. M. Quinn, and T. Hunter. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
15. Klupp, B. G., H. Granzow, and T. C. Mettenleiter. 2001. Effect of the pseudorabies virus US3 protein on nuclear membrane localization of the UL34 protein and virus egress from the nucleus. J. Gen. Virol. 82:2363-2371.
16. Klupp, B. G., H. Granzow, and T. C. Mettenleiter. 2000. Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product. J. Virol. 74:10063-10073.
17. Kurachi, R., T. Daikoku, T. Tsurumi, K. Maeno, Y. Nishiyama, and T. Kurata. 1993. The pathogenicity of a US3 protein kinase-deficient mutant of herpes simplex virus type 2 in mice. Arch. Virol. 133:259-273.
18. Leader, D. P., A. D. Deana, F. Marchiori, F. C. Purves, and L. A. Pinna. 1991. Further definition of the substrate specificity of the alpha-herpesvirus protein kinase and comparison with protein kinases a and c. Biochim. Biophys. Acta 1091:426-431.
19. Leopardi, R., C. Van Sant, and B. Roizman. 1997. The herpes simplex virus I protein kinase US3 is required for protection from apoptosis induced by the virus. Proc. Natl. Acad. Sci. USA 94:7891-7896.
20. Longnecker, R., and B. Roizman. 1987. Clustering of genes dispensable for growth in culture in the s component of the HSV-1 genome. Science 236: 573-576.
21. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
22. Munger, J., A. V. Chee, and B. Roizman. 2001. The US3 protein kinase blocks apoptosis induced by the d120 mutant of herpes simplex virus 1 at a premitochondrial stage. J. Virol. 75:5491-5497.
23. Muranyi, W., J. Haas, M. Wagner, and U. H. Koszinowski. 2002. Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 287:854-856.
24. Murata, T., F. Goshima, Y. Nishizawa, T. Daikoku, H. Takakuwa, K. Ohtsuka, T. Yoshikawa, and Y. Nishiyama. 2002. Phosphorylation of cytokeratin 17 by herpes simplex virus type 2 US3 protein kinase. Microbiol. Immunol. 46:707-719.
25. Nikolakaki, E., J. Meier, G. Simos, S. D. Georgatos, and T. Giannakouros. 1997. Mitotic phosphorylation of the lamin B receptor by a serine/arginine kinase and p34cdc2. J. Biol. Chem. 272:6208-6213.
26. Nikolakaki, E., G. Simos, S. D. Georgatos, and T. Giannakouros. 1996. A nuclear envelope-associated kinase phosphorylates arginine-serine motifs and modulates interactions between the lamin B receptor and other nuclear proteins. J. Biol. Chem. 271:8365-8372.
27. Nishiyama, Y., R. Kurachi, T. Daikoku, and K. Umene. 1993. The US9, 10, 11, and 12 genes of herpes simplex virus type 1 are of no importance for its neurovirulence and latency in mice. Virology 194:419-423.
28. Nishiyama, Y., Y. Yamada, R. Kurachi, and T. Daikoku. 1992. Construction of a US3 lacZ insertion mutant of herpes simplex virus type 2 and characterization of its phenotype in vitro and in vivo. Virology 190:256-268.
29. Purves, F. C., A. D. Deana, F. Marchiori, D. P. Leader, and L. A. Pinna. 1986. The substrate specificity of the protein kinase induced in cells infected with herpesviruses: studies with synthetic substrates indicate structural requirements distinct from other protein kinases. Biochim. Biophys. Acta 889:208-215.
30. Purves, F. C., R. M. Longnecker, D. P. Leader, and B. Roizman. 1987. Herpes simplex virus 1 protein kinase is encoded by open reading frame US3 which is not essential for virus growth in cell culture. J. Virol. 61:2896-2901.
31. S3 gene mediates posttranslational modification of the phosphoprotein encoded by the UL34 gene. J. Virol. 65:5757-5764.
32. S3 protein kinase, is a membrane protein which in its unphosphorylated state associates with novel phosphoproteins. J. Virol. 66: 4295-4303.
33. Rauch, D. A., N. Rodriguez, and R. J. Roller. 2000. Mutations in herpes simplex virus glycoprotein D distinguish entry of free virus from cell-cell spread. J. Virol. 74:11437-11446.
34. Reynolds, A. E., B. J. Ryckman, J. D. Baines, Y. Zhou, L. Liang, and R. J. Roller. 2001. UL31 and UL34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids. J. Virol. 75:8803-8817.
35. Reynolds, A. E., E. G. Wills, R. J. Roller, B. J. Ryckman, and J. D. Baines. 2002. Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J. Virol. 76:8939-8952.
36. S11 is a virion component and associates with ribosomal 60S subunits. J. Virol. 66:3624-3632.
37. L34 gene product is required for viral envelopment. J. Virol. 74:117-129.
38. Schlehofer, J. R., H. Hampl, and K. O. Habermehl. 1979. Differences in the morphology of herpes simplex virus infected cells. I. Comparative scanning and transmission electron microscopic studies on HSV-1 infected Hep-2 and chick embryo fibroblast cells. J. Gen. Virol. 44:433-442.
39. Scott, E., and P. O'Hare. 2001. Fate of the inner nuclear membrane protein lamin B receptor and nuclear lamins in herpes simplex virus type 1 infection. J. Virol. 75:8818-8830.
40. Shao, L., L. M. Rapp, and S. K. Weller. 1993. Herpes simplex virus 1 alkaline nuclease is required for efficient egress of capsids from the nucleus. Virology 196:146-162.
41. Skepper, J. N., A. Whiteley, H. Browne, and A. Minson. 2001. Herpes simplex virus nucleocapsids mature to progeny virions by an envelopment-deenvelopment-reenvelopment pathway. J. Virol. 75:5697-5702.
42. Wagenaar, F., J. M. Pol, B. Peeters, A. L. Gielkens, N. de Wind, and T. G. Kimman. 1995. The US3-encoded protein kinase from pseudorabies virus affects egress of virions from the nucleus. J. Gen. Virol. 76:1851-1859.