Mutational analysis of open reading frames 62 and 71, encoding the varicella-zoster virus immediate-early transactivating protein, IE62, and effects on replication in vitro and in skin xenografts in the SCID-hu mouse in vivo

Journal of Virology

Volumn 77, Issue 10, 2003, Pages 5607-5620

  Sato, Bunji ^a,b   Ito, Hideki ^a   Hinchliffe, Stewart ^a,c   Sommer, Marvin H ^a   Zerboni, Leigh ^a   Arvin, Ann M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ASTELLAS PHARMA INC   (Japan)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN IE62; PROTEIN ORF9; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS VACCINE;

ANIMAL MODEL; ARTICLE; BINDING SITE; CELL CULTURE; COMBINED IMMUNODEFICIENCY; CONTROLLED STUDY; COSMID; GENE DELETION; GENE EXPRESSION; GENE INSERTION; GENETIC TRANSFECTION; GENOME; HUMAN; HUMAN CELL; HUMAN TISSUE; LONG TERMINAL REPEAT; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGENY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; SKIN GRAFT; SOUTHERN BLOTTING; TISSUE DIFFERENTIATION; TRANSACTIVATION; VARICELLA ZOSTER VIRUS; VIRUS INFECTIVITY; VIRUS RECOMBINATION; VIRUS REPLICATION; XENOGRAFT;

ANIMALS; COSMIDS; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 3, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; MELANOMA; MICE; MICE, SCID; OPEN READING FRAMES; PLASMIDS; RECOMBINATION, GENETIC; SKIN TRANSPLANTATION; TRANS-ACTIVATORS; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED; VIRAL ENVELOPE PROTEINS; VIRUS REPLICATION;

EID: 0038371404     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.10.5607-5620.2003     Document Type: Article

References (65)

1. Alconada, A., U. Bauer, L. Baudoux, J. Piette, and B. Hoflack. 1998. Intracellular transport of the glycoproteins gE and gI of the varicella-zoster virus. gE accelerates the maturation of gI and determines its accumulation in the trans-Golgi network. J. Biol. Chem. 273:13430-13436.
2. Allen, K. E., and R. D. Everett. 1997. Mutations which alter the DNA binding properties of the herpes simplex virus type 1 transactivating protein Vmw175 also affect its ability to support virus replication. J. Gen. Virol. 78:2913-2922.
3. Argaw, T., J. I. Cohen, M. Klutch, K. Lekstrom, T. Yoshikawa, Y. Asano, and P. R. Krause. 2000. Nucleotide sequences that distinguish Oka vaccine from parental Oka and other varicella-zoster virus isolates. J. Infect. Dis. 181: 1153-1157.
4. Arvin, A. M. 2001. Varicella-zoster virus, p. 2731-2767. In D. M. Knipe and P. M. Howley (ed.), Fields virology. Lippincott-Raven, Philadelphia, Pa.
5. 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.
6. Casey, T. A., W. T. Ruyechan, M. N. Flora, W. Reinhold, S. E. Straus, and J. Hay. 1985. Fine mapping and sequencing of a variable segment in the inverted repeat region of varicella-zoster virus DNA. J. Virol. 54:639-642.
7. Cheung, A. K. 1989. DNA nucleotide sequence analysis of the immediate early gene of pseudorabies virus. Nucleic Acids Res. 17:4637-4646.
8. Cohen, J. I., and S. E. Straus. 2001. Varicella-zoster virus and its replication, p. 2707-2730. In D. M. Knipe and P. M. Howley (ed.), Fields virology. Lippincott-Raven, Philadelphia, Pa.
9. Davison, A. J., and J. E. Scott. 1986. The complete DNA sequence of varicella-zoster virus. J. Gen. Virol. 67:1759-1816.
10. DeLuca, N. A., A. M. McCarthy, and P. A. Schaffer. 1985. Isolation and characterization of deletion mutants of herpes simplex virus type 1 in the gene encoding immediate-early regulatory protein ICP4. J. Virol. 56:558-570.
11. 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.
12. Disney, G. H., T. A. Mckee, C. M. Preston, and R. D. Everett. 1990. The product of varicella-zoster virus gene 62 autoregulates its own promoter. J. Gen. Virol. 71:2999-3003.
13. Dumas, A. M., J. L. Geelen, M. W. Weststrate, P. Wertheim, and J. van der Noordaa. 1981. Xba I, Pst I, and Bgl II restriction endonuclease maps of the two orientations of the varicella-zoster virus genome. J. Virol. 39:390-400.
14. Ecker, J. R., and R. W. Hyman. 1982. Varicella-zoster virus DNA exists as two isomers. Proc. Natl. Acad. Sci. USA 79:156-160.
15. Felser, J. M., S. E. Straus, and J. M. Ostrove. 1987. Varicella-zoster virus complements herpes simplex virus type 1 temperature-sensitive mutants. J. Virol. 61:225-228.
16. 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.
17. Gomi, Y., H. Sunamachi, Y. Mori, K. Nagaike, M. Takahashi, and K. Yamanishi. 2002. Comparison of the complete DNA sequences of the Oka varicella vaccine and its parental virus. J. Virol. 76:11447-11459.
18. Gomi, Y., T. Imagawa, M. Takahashi, and K. Yamanishi. 2000. Oka varicella vaccine is distinguishable from its parental virus in DNA sequence of open reading frame 62 and its transactivation activity. J. Med. Virol. 61:497-503.
19. Grondin, B., and N. DeLuca. 2000. Herpes simplex virus type 1 ICP4 promotes transcription preinitiation complex formation by enhancing the binding of TFIID to DNA. J. Virol. 74:11504-11510.
20. Inchauspe, G., S. Nagpal, and J. M. Ostrove. 1989. Mapping of two varicellazoster virus-encoded genes that activate the expression of viral early and late genes. Virology. 173:700-709.
21. Ito, H., M. H. Sommer, L. H. Zerboni, H. He, D. Boucaud, J. Hay, W. Ruyechan, and A. Arvin. 2003. Promoter sequences of varicella-zoster virus glycoprotein I targeted by cellular transactivating factors, Sp1 and USF, determine virulence in skin and T cells in SCID-hu mice in vivo. J. Virol. 77:489-498.
22. Katano, H., T. Iwasaki, N. Baba, M. Terai, S. Mori, A. Iwamoto, T. Kurata, and T. Sata. 2000. Identification of antigenic proteins encoded by human herpesvirus 8 and seroprevalence in the general population and among patients with and without Kaposi's sarcoma. J. Virol. 74:3478-3485.
23. Kemble, G. W., P. Annunziato, O. Lungu, R. E. Winter, T. A. Cha, S. J. Silverstein, and R. R. Spaete. 2000. Open reading frame S/L of varicellazoster virus encodes a cytoplasmic protein expressed in infected cells. J. Virol. 74:11311-11321.
24. Kenyon, T. K., J. I. Cohen, and C. Grose. 2002. Phosphorylation by the varicella-zoster virus ORF47 protein serine kinase determines whether endocytosed viral gE traffics to the trans-Golgi network or recycles to the cell membrane. J. Virol. 76:10980-10993.
25. Kim, D. B., S. Zabierowski, and N. A. DeLuca. 2002. The initiator element in a herpes simplex virus type 1 late-gene promoter enhances activation by ICP4, resulting in abundant late-gene expression. J. Virol. 76:1548-1558.
26. Kinchington, P. R., and J. I. Cohen. 2000. Viral proteins, p. 74-104, In A. M. Arvin and A. A. Gershon (ed.), Varicella zoster virus: basic virology and clinical management. Cambridge University Press, Cambridge United Kingdom.
27. Kinchington, P. R., and S. E. Turse. 1998. Regulated nuclear localization of the varicella zoster virus major regulatory protein IE62. J. Infect. Dis. 178: S16-S21.
28. 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.
29. 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. 74:2256-2277.
30. Lynch, J. M., T. K. Kenyon, C. Grose, J. Hay, and W. T. Ruyechan. 2002. Physical and functional interaction between the varicella zoster virus IE63 and IE62 proteins. Virology 302:71-82.
31. Mallory, S., M. Sommer, and A. M. Arvin. 1997. Mutational analysis of the role of glycoprotein I in varicella-zoster virus replication and its effects on glycoprotein conformation and trafficking. J. Virol. 71:8279-8288.
32. Mckee, T. A., and C. M. Preston. 1991. Identification of two protein binding sites within the varicella-zoster virus major immediate-early promoter. Virus Res. 20:59-69.
33. Meier, J. L., X. Luo, M. Sawadogo, and S. E. Straus. 1994. The cellular transcription factor USF cooperates with varicella-zoster virus immediate early protein 62 to symmetrically activate a bidirectional viral promoter. Mol. Cell. Biol. 14:6896-6906.
34. Mo, C., J. Lee, M. Sommer, R. Santos, C. Grose, and A. M. Arvin. 2002. The requirement of varicella-zoster virus glycoprotein E for viral replication and the effects of glycoprotein I on gE trafficking and maturation. Virology 304:176-186.
35. Mo, C., J. Suen, M. Sommer, and A. M. Arvin. 1999. Glycoprotein K (ORF5) of varicella-zoster virus is essential for virus growth in melanoma cells. J. Virol. 73:4197-4207.
36. + T-lymphocytes and epidermal cells in SCID-hu mice. J. Virol. 69:5236-5242,
37. Moffat, J., L. Zerboni, M. Stein, C. Grose, H. Kaneshima, and A. Arvin. 1998. The attenuation of the vaccine Oka strain of varicella-zoster virus and the role of glycoprotein C in alphaherpesvirus virulence demonstrated in the SCID-hu mouse. J. Virol. 72:965-974.
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. 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.
40. Moriuchi, M., H. Moriuchi, S. E. Straus, and J. I. Cohen. 1993. Varicellazoster virus open reading frame 10 protein, the herpes simplex virus VP16 homolog, transactivates herpesvirus immediate-early gene promoters. J. Virol. 67:2739-2746.
41. Moriuchi, M., H. Moriuchi, S. E. Straus, and J. I. Cohen. 1994. Varicellazoster virus (VZV) virion-associated transactivator open reading frame 62 protein enhances the infectivity of VZV DNA. Virology 200:297-300.
42. Moriuchi, H., M. Moriuchi, and J. I. Cohen. 1995. Proteins and cis -acting elements associated with transactivation of the varicella-zoster virus (VZV) immediate-early gene 62 promoter by VZV open reading frame 10 protein. J. Virol. 69:4693-4701.
43. Moriuchi, H., M. Moriuchi, R. Pichyangkura, S. J. Triezenberg, S. E. Straus, and J. I. Cohen. 1995. Hydrophobic cluster-analysis predicts an aminoterminal domain of varicella-zoster virus open-reading-frame-10 required for transcriptional activation. Proc. Nat. Acad. Sci. USA 92:9333-9337.
44. Ng, T. I., and C. Grose. 1992. Serine protein kinase associated with varicellazoster virus ORF 47. Virology. 19:9-18.
45. 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.
46. Niizuma, T., L. Zerboni, M. H. Sommer, H. Ito, S. Hinchliffe, and A. M. Arvin. 2003. Construction of varicella-zoster virus recombinants from parent Oka cosmids and demonstration that ORF65 protein is dispensable for infection of human skin and T cells in the SCID-hu mouse model. J. Virol. 77:6062-6065.
47. Olson, J. K., and C. Grose. 1997. Endocytosis and recycling of varicellazoster virus Fc receptor glycoprotein gE: internalization mediated by a YXXL motif in the cytoplasmic tail. J. Virol. 71:4042-4054.
48. Olson, J. K., and C. Grose. 1998. Complex formation facilitates endocytosis of the varicella-zoster virus gE:gI Fc receptor. J. Virol. 72:1542-1551.
49. Paterson, T., and R. D. Everett. 1990. A prominent serine-rich region in Vmw175, the major transcriptional regulator protein of herpes simplex virus type 1, is not essential for virus growth in tissue culture. J. Gen. Virol. 71:1775-1783.
50. Perera, L. P., J. D. Mosca, W. T. Ruyechan, and J. Hay. 1992. Regulation of varicella-zoster virus gene expression in human T lymphocytes. J. Virol. 66:5298-5304.
51. 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.
52. Rasty, S., P. L. Poliani, D. J. Fink, and J. C. Glorioso. 1997. Deletion of the S component inverted repeat sequence c′ and the nonessential genes U(S)1 through U(S)5 from the herpes simplex virus type 1 genome substantially impairs productive viral infection in cell culture and pathogenesis in the rat central nervous system. J. Neurovirol. 3:247-264.
53. Roizman, B., and A. E. Sears. 2001. Herpes simplex viruses and their replication, p. 2399-2459. In D. M. Knipe and P. M. Howley (ed.), Fields virology. Lippincott- Raven, Philadelphia, Pa.
54. Ruyechan, W. T., and J. Hay. 2000. DNA replication, p. 51-73. In A. M. Arvin and A. A. Gershon (ed.), Varicella zoster virus: basic virology and clinical management. Cambridge University Press, Cambridge United Kingdom.
55. Santos, R. A., C. C. Hatfield, B. P. Faga, J. A. Padilla, N. L. Cole, J. F. Moffat, A. M. Arvin, W. T. Ruyechan, J. Hay, and C. Grose. 2000. Varicellazoster virus gE escape mutant VZV-MSP exhibits an accelerated cell-to-cell spread phenotype in both infected cell cultures and SCID-hu mice. Virology 275:306-317.
56. Sommer, M. H., E. Zagha, O. K. Serrano, C. C. Ku, L. Zerboni, A. Baiker, R. Santos, M. Spengler, J. Lynch, C. Grose, W. Ruyechan, J. Hay, and A. M. Arvin. 2001. Mutational analysis of the repeated open reading frames, ORFs 63 and 70 and ORFs 64 and 69, of varicella-zoster virus. J. Virol. 75:8224-8239.
57. Spengler, M. L., W. T. Ruyechan, and J. Hay. 2000. Physical interaction between two varicella zoster virus gene regulatory proteins, IE4 and IE62. Virology 272:375-381.
58. Spengler, M. L., W. T. Ruyechan, and J. Hay. 2001. Interactions among structural proteins of varicella zoster virus. Arch. Virol. 17:S71-79.
59. Straus. S. E., H. S. Aulakh, W. T. Ruyechan, J. Hay, T. A. Casey, G. F. Vande Woude, J. Owens, and H. A. Smith. 1981. Structure of varicella-zoster virus DNA. J. Virol. 40:516-525.
60. Takahashi, M., T. Otsuka, Y. Okuno, Y. Asano, and T. Yazaki. 1974. Live vaccine used to prevent the spread of varicella in children in hospital. Lancet 7892:1288-1290.
61. Tyler, J. K., and R. D. Everett. 1993. The DNA binding domain of the varicella zoster virus gene 62 protein interacts with multiple sequences which are similar to the binding site of the related protein of herpes simplex virus type 1. Nucleic Acids Res. 21:513-522.
62. Tyler, J. K., and R. D. Everett. 1994. The DNA binding domain of the varicella zoster virus gene 62 and herpes simplex virus type 1 ICP4 transactivator proteins heterodimerize and bind to DNA. Nucleic Acids Res. 22: 711-721.
63. Wang, Z. H., M. D. Gershon, O. Lungu, Z. Zhu, S. Mallory, A. M. Arvin, and A. A. Gershon. 2001. Essential role played by the C-terminal domain of glycoprotein I in envelopment of varicella-zoster virus in the trans-Golgi network: interactions of glycoproteins with tegument. J. Virol. 75:323-340.
64. Wu, C. L., and K. W. Wilcox. 1991. The conserved DNA-binding domains encoded by the herpes simplex virus type 1 ICP4, pseudorabies virus IE180, and varicella-zoster virus ORF62 genes recognizes similar binding sites in the corresponding promoters. J. Virol. 65:1149-1159.
65. Yao, F., and R. J. Courtney. 1989. A major transcriptional regulatory protein (ICP4) of herpes simplex virus type 1 is associated with purified virions. J. Virol. 63:3338-3344.