Varicella-zoster virus open reading frame 66 protein kinase is required for efficient viral growth in primary human corneal stromal fibroblast cells

Journal of Virology

Volumn 82, Issue 15, 2008, Pages 7653-7665

  Erazo, Angela ^a   Yee, Michael B ^a   Osterrieder, Nikolaus ^b   Kinchington, Paul R ^a  

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

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; GREEN FLUORESCENT PROTEIN; IE62 PROTEIN; OPEN READING FRAME 66 PROTEIN KINASE; PROTEIN KINASE; REGULATOR PROTEIN;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; CORNEA STROMA; FIBROBLAST; GROWTH DISORDER; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROGENY; VARICELLA ZOSTER VIRUS; VIRION; VIROGENESIS; VIRUS INFECTION; VIRUS REPLICATION;

AMINO ACID SUBSTITUTION; CELL NUCLEUS; CELLS, CULTURED; FIBROBLASTS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HERPESVIRUS 3, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; MUTAGENESIS, SITE-DIRECTED; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE DELETION; STAINING AND LABELING; TRANS-ACTIVATORS; VIRAL ENVELOPE PROTEINS; VIRAL NONSTRUCTURAL PROTEINS; VIRION; VIRUS REPLICATION;

HUMAN HERPESVIRUS 3;

EID: 47749123866     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00311-08     Document Type: Article

References (68)

1. Abendroth, A., I. Lin, B. Slobedman, H. Ploegh, and A. M. Arvin. 2001. Varicella-zoster virus retains major histocompatihility complex class I proteins in the Golgi compartment of infected cells. J. Virol. 75:4878-4888.
2. Aubert, M., and J. A. Blaho. 2001. Modulation of apoptosis during herpes simplex virus infection in human cells. Microbes Infect. 3:859-866.
3. Benetti, L., and B. Roizman. 2004. Herpes simplex virus protein kinase US3 activates and functionally overlaps protein kinase A to block apoptosis. Proc. Natl. Acad. Sci. USA 101:9411-9416.
4. Benetti, L., and B. Roizman. 2007. In transduced cells, the US3 protein kinase of herpes simplex virus 1 precludes activation and induction of apoptosis by transfected procaspase 3. J. Virol. 81:10242-10248.
5. Besser, J., M. Ikoma, K. Fabel, M. H. Sommer, L. Zerboni, C. Grose, and A. M. Arvin. 2004. Differential requirement for cell fusion and virion formation in the pathogenesis of varicella-zoster virus infection in skin and T cells. J. Virol. 78:13293-13305.
6. Besser, J., M. H. Sommer, L. Zerboni, C. P. Bagowski, H. Ito, J. Moffat, C. C. Ku, and A. M. Arvin. 2003. Differentiation of varicella-zoster virus ORF47 protein kinase and IE62 protein binding domains and their contributions to replication in human skin xenografts in the SCID-hu mouse. J. Virol. 77:5964-5974.
7. Che, X., L. Zerboni, M. H. Sommer, and A. M. Arvin. 2006. Varicella-zoster virus open reading frame 10 is a virulence determinant in skin cells but not in T cells in vivo. J. Virol. 80:3238-3248.
8. Cilloniz, C., W. Jackson, C. Grose, D. Czechowski, J. Hay, and W. T. Ruyechan. 2007. The varicella-zoster virus (VZV) ORF9 protein interacts with the IE62 major VZV transactivator. J. Virol. 81:761-774.
9. Cohen, J. I., T. Krogmann, S. Bontems, C. Sadzot-Delvaux, and L. Pesnicak. 2005. Regions of the varicella-zoster virus open reading frame 63 latency-associated protein important for replication in vitro are also critical for efficient establishment of latency. J. Virol. 79:5069-5077.
10. Cohen, J. I., and H. Nguyen. 1997. Varicella-zoster virus glycoprotein I is essential for growth of virus in Vero cells. J. Virol. 71:6913-6920.
11. Cohen, J. I., and S. E. Straus. 2001. Varicella-zoster virus and its replication, p. 2707-2729. 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, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
12. Deruelle, M., K. Geenen, H. J. Nauwynck, and H. W. Favoreel. 2007. A point mutation in the putative ATP binding site of the pseudorabies virus US3 protein kinase prevents Bad phosphorylation and cell survival following apoptosis induction. Virus Res. 128:65-70.
13. Disney, G. H., and R. D. Everett. 1990. A herpes simplex virus type 1 recombinant with both copies of the Vmw175 coding sequences replaced by the homologous varicella-zoster virus open reading frame. J. Gen. Virol. 71:2681-2689.
14. Eisfeld, A. J., S. E. Turse, S. A. Jackson, E. C. Lerner, and P. R. Kinchington. 2006. Phosphorylation of the varicella-zoster virus (VZV) major transcriptional regulatory protein IE62 by the VZV open reading frame 66 protein kinase. J. Virol. 80:1710-1723.
15. Eisfeld, A. J., M. B. Yee, A. Erazo, A. Abendroth, and P. R. Kinchington. 2007. Downregulation of class I major histocompatibility complex surface expression by varicella-zoster virus involves open reading frame 66 protein kinase-dependent and -independent mechanisms. J. Virol. 81:9034-9049.
16. Favoreel, H. W., G. Van Minnebruggen, D. Adriaensen, and H. J. Nauwynck. 2005. Cytoskeletal rearrangements and cell extensions induced by the US3 kinase of an alphaherpesvirus are associated with enhanced spread. Proc. Natl. Acad. Sci. USA 102:8990-8995.
17. Felser, J. M., P. R. Kinchington, G. Inchauspe, S. E. Straus, and J. M. Ostrove. 1988. Cell lines containing varicella-zoster virus open reading frame 62 and expressing the "IE" 175 protein complement ICP4 mutants of herpes simplex virus type 1. J. Virol. 62:2076-2082.
18. Heineman, T. C., and J. I. Cohen. 1995. The varicella-zoster virus (VZV) open reading frame 47 (ORF47) protein kinase is dispensable for viral replication and is not required for phosphorylation of ORF63 protein, the VZV homolog of herpes simplex virus ICP22. J. Virol. 69:7367-7370.
19. Heineman, T. C., K. Seidel, and J. I. Cohen. 1996. The varicella-zoster virus ORF66 protein induces kinase activity and is dispensable for viral replication. J. Virol. 70:7312-7317.
20. Hu, H., and J. I. Cohen. 2005. Varicella-zoster virus open reading frame 47 (ORF47) protein is critical for virus replication in dendritic cells and for spread to other cells. Virology 337:304-311.
21. Kinchington, P. R., D. Bookey, and S. E. Turse. 1995. The transcriptional regulatory proteins encoded by varicella-zoster virus open reading frames (ORFs) 4 and 63, but not ORF 61, are associated with purified virus particles. J. Virol. 69:4274-4282.
22. Kinchington, P. R., K. Fite, A. Seman, and S. E. Turse. 2001. Virion association of IE62, the varicella-zoster virus (VZV) major transcriptional regulatory protein, requires expression of the VZV open reading frame 66 protein kinase. J. Virol. 75:9106-9113.
23. Kinchington, P. R., K. Fite, and S. E. Turse. 2000. Nuclear accumulation of IE62, the varicella-zoster virus (VZV) major transcriptional regulatory protein, is inhibited by phosphorylation mediated by the VZV open reading frame 66 protein kinase. J. Virol. 74:2265-2277.
24. Kinchington, P. R., J. K. Hougland, A. M. Arvin, W. T. Ruyechan, and J. Hay. 1992. The varicella-zoster virus immediate-early protein IE62 is a major component of virus particles. J. Virol. 66:359-366.
25. Kinchington, P. R., G. Inchauspe, J. H. Subak-Sharpe, F. Robey, J. Hay, and W. T. Ruyechan. 1988. Identification and characterization of a varicella-zoster virus DNA-binding protein by using antisera directed against a predicted synthetic oligopeptide. J. Virol. 62:802-809.
26. Kinchington, P. R., and S. E. Turse. 1998. Regulated nuclear localization of the varicella-zoster virus major regulatory protein, IE62. J. Infect. Dis. 178(Suppl. 1):S16-S21.
27. 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.
28. Ku, C. C., J. Besser, A. Abendroth, C. Grose, and A. M. Arvin. 2005. Varicella-zoster virus pathogenesis and immunobiology: new concepts emerging from investigations with the SCIDhu mouse model. J. Virol. 79:2651-2658.
29. + T lymphocytes that express activation, memory, and skin homing markers. J. Virol. 76:11425-11433.
30. Ku, C. C., L. Zerboni, H. Ito, B. S. Graham, M. Wallace, and A. M. Arvin. 2004. Varicella-zoster virus transfer to skin by T Cells and modulation of viral replication by epidermal cell interferon-alpha. J. Exp. Med. 200:917-925.
31. Leach, N., S. L. Bjerke, D. K. Christensen, J. M. Bouchard, F. Mou, R. Park, J. Baines, T. Haraguchi, and R. J. Roller. 2007. Emerin is hyperphosphorylated and redistributed in herpes simplex virus type 1-infected cells in a manner dependent on both UL34 and US3. J. Virol. 81:10792- 10803.
32. Li, H., J. Zhang, A. Kumar, M. Zheng, S. S. Atherton, and F. S. Yu. 2006. Herpes simplex virus 1 infection induces the expression of proinflammatory cytokines, interferons and TLR7 in human corneal epithelial cells. Immunology 117:167-176.
33. McKnight, J. L., M. Doerr, and Y. Zhang. 1994. An 85-kilodalton herpes simplex virus type 1 alpha trans-induction factor (VP16)-VP13/14 fusion protein retains the transactivation and structural properties of the wild-type molecule during virus infection. J. Virol. 68:1750-1757.
34. Michael, K., B. G. Klupp, T. C. Mettenleiter, and A. Karger. 2006. Composition of pseudorabies virus particles lacking tegument protein US3, UL47, or UL49 or envelope glycoprotein E. J. Virol. 80:1332-1339.
35. Miles, D. H., M. D. Willcox, and S. Athmanathan. 2004. Ocular and neuronal cell apoptosis during HSV-1 infection: a review. Curr. Eye Res. 29:79-90.
36. Moffat, J., H. Ito, M. Sommer, S. Taylor, and A. M. Arvin. 2002. Glycoprotein I of varicella-zoster virus is required for viral replication in skin and T cells. J. Virol. 76:8468-8471.
37. + T lymphocytes and epidermal cells in SCID-hu mice. J. Virol. 69:5236-5242.
38. Moffat, J. F., L. Zerboni, M. H. Sommer, T. C. Heineman, J. I. Cohen, H. Kaneshima, and A. M. Arvin. 1998. The ORF47 and ORF66 putative protein kinases of varicella-zoster virus determine tropism for human T cells and skin in the SCID-hu mouse. Proc. Natl. Acad. Sci. USA 95:11969-11974.
39. Morris, J. B., H. Hofemeister, and P. O'Hare. 2007. Herpes simplex virus infection induces phosphorylation and delocalization of emerin, a key inner nuclear membrane protein. J. Virol. 81:4429-4437.
40. Morrow, G., B. Slobedman, A. L. Cunningham, and A. Abendroth. 2003. Varicella-zoster virus productively infects mature dendritic cells and alters their immune function. J. Virol. 77:4950-4959.
41. Mou, F., T. Forest, and J. D. Baines. 2007. US3 of herpes simplex virus type 1 encodes a promiscuous protein kinase that phosphorylates and alters localization of lamin A/C in infected cells. J. Virol. 81:6459-6470.
42. Muller, L. J., L. Pels, and G. F. Vrensen. 1995. Novel aspects of the ultrastructural organization of human corneal keratocytes. Investig. Ophthalmol. Vis. Sci. 36:2557-2567.
43. Murata, T., F. Goshima, Y. Yamauchi, T. Koshizuka, H. Takakuwa, and Y. Nishiyama. 2002. Herpes simplex virus type 2 US3 blocks apoptosis induced by sorbitol treatment. Microbes Infect. 4:707-712.
44. Ng, T. I., L. Keenan, P. R. Kinchington, and C. Grose. 1994. Phosphorylation of varicella-zoster virus open reading frame (ORF) 62 regulatory product by viral ORF 47-associated protein kinase. J. Virol. 68:1350-1359.
45. Ogg, P. D., P. J. McDonell, B. J. Ryckman, C. M. Knudson, and R. J. Roller. 2004. The HSV-1 Us3 protein kinase is sufficient to block apoptosis induced by overexpression of a variety of Bcl-2 family members. Virology 319:212-224.
46. Pavan-Langston, D. 2000. Ophthalmic zoster, p. 276-298. In A. Arvin and A. Gershon (ed.), Varicella-zoster virus: virology and clinical management. Cambridge University Press, Cambridge, United Kingdom.
47. Perera, L. P., J. D. Mosca, W. T. Ruyechan, G. S. Hayward, S. E. Straus, and J. Hay. 1993. A major transactivator of varicella-zoster virus, the immediate-early protein IE62, contains a potent N-terminal activation domain. J. Virol. 67:4474-4483.
48. Perera, L. P., J. D. Mosca, M. Sadeghi-Zadeh, W. T. Ruyechan, and J. Hay. 1992. The varicella-zoster virus immediate early protein, IE62, can positively regulate its cognate promoter. Virology 191:346-354.
49. S3.5 protein kinases of herpes simplex virus 1 differ with respect to their functions in blocking apoptosis and in virion maturation and egress. J. Virol. 80:3752-3764.
50. Poon, A. P., H. Gu, and B. Roizman. 2006. ICP0 and the US3 protein kinase of herpes simplex virus 1 independently block histone deacetylation to enable gene expression. Proc. Natl. Acad. Sci. USA 103:9993-9998.
51. S3 protein can form functional heteromultimeric structures derived from overlapping truncated polypeptides. J. Virol. 81:1980-1989.
52. Punda-Polic, V., W. J. O'Brien, and J. L. Taylor. 1999. Synergistic antivaricella-zoster virus activity of interferon-alpha 2a and acyclovir in corneal cells. Zentralbl. Bakteriol. 289:203-210.
53. 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.
54. Ryckman, B. J., and R. J. Roller. 2004. Herpes simplex virus type 1 primary envelopment: UL34 protein modification and the US3-UL34 catalytic relationship. J. Virol. 78:399-412.
55. Sadaoka, T., H. Yoshii, T. Imazawa, K. Yamanishi, and Y. Mori. 2007. Deletion in open reading frame 49 of varicella-zoster virus reduces virus growth in human malignant melanoma cells but not in human embryonic fibroblasts. J. Virol. 81:12654-12665.
56. Sato, H., L. D. Callanan, L. Pesnicak, T. Krogmann, and J. I. Cohen. 2002. Varicella-zoster virus (VZV) ORF17 protein induces RNA cleavage and is critical for replication of VZV at 37 degrees C but not 33 degrees C. J. Virol. 76:11012-11023.
57. Schaap-Nutt, A., M. Sommer, X. Che, L. Zerboni, and A. M. Arvin. 2006. ORF66 protein kinase function is required for T-cell tropism of varicella-zoster virus in vivo. J. Virol. 80:11806-11816.
58. Schaap, A., J. F. Fortin, M. Sommer, L. Zerboni, S. Stamatis, C. C. Ku, G. P. Nolan, and A. M. Arvin. 2005. T-cell tropism and the role of ORF66 protein in pathogenesis of varicella-zoster virus infection. J. Virol. 79:12921-12933.
59. Schumacher, D., B. K. Tischer, S. Trapp, and N. Osterrieder. 2005. The protein encoded by the US3 orthologue of Marek's disease virus is required for efficient de-envelopment of perinuclear virions and involved in actin stress fiber breakdown. J. Virol. 79:3987-3997.
60. Soong, W., J. C. Schultz, A. C. Patera, M. H. Sommer, and J. I. Cohen. 2000. Infection of human T lymphocytes with varicella-zoster virus: an analysis with viral mutants and clinical isolates. J. Virol. 74:1864-1870.
61. Spengler, M., N. Niesen, C. Grose, W. T. Ruyechan, and J. Hay. 2001. Interactions among structural proteins of varicella zoster virus. Arch. Virol. Suppl. 17:71-79.
62. Tischer, B. K., B. B. Kaufer, M. Sommer, F. Wussow, A. M. Arvin, and N. Osterrieder. 2007. A self-excisable infectious bacterial artificial chromosome clone of varicella-zoster virus allows analysis of the essential tegument protein encoded by ORF9. J. Virol. 81:13200-13208.
63. Tischer, B. K., J. von Einem, B. Kaufer, and N. Osterrieder. 2006. Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. BioTechniques 40:191-197.
64. 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.
65. Wenkel, H., C. Rummelt, V. Rummelt, G. Jahn, B. Fleckenstein, and G. O. Naumann. 1993. Detection of varicella zoster virus DNA and viral antigen in human cornea after herpes zoster ophthalmicus. Cornea 12:131-137.
66. West-Mays, J. A., and D. J. Dwivedi. 2006. The keratocyte: corneal stromal cell with variable repair phenotypes. Int. J. Biochem. Cell. Biol. 38:1625-1631.
67. Wilson, S. E. 2000. Role of apoptosis in wound healing in the cornea. Cornea 19:S7-S12.
68. Yang, M., H. Peng, J. Hay, and W. T. Ruyechan. 2006. Promoter activation by the varicella-zoster virus major transactivator IE62 and the cellular transcription factor USF. J. Virol. 80:7339-7353.