Mutation of single hydrophobic residue I27, L35, F39, L58, L65, L67, or L71 in the N terminus of VP5 abolishes interaction with the scaffold protein and prevents closure of herpes simplex virus type 1 capsid shells

Journal of Virology

Volumn 77, Issue 7, 2003, Pages 4043-4059

  Walters, Jewell N ^a   Sexton, Gerry L ^b   McCaffery, J Michael ^b   Desai, Prashant ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; CAPSID PROTEIN; PROTEIN VP5; SCAFFOLD PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENETIC ANALYSIS; GENETIC MARKER; HERPES SIMPLEX VIRUS 1; HYDROPHOBICITY; LETHALITY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REVERTANT; TWO HYBRID SYSTEM; VIROGENESIS; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS GENOME; VIRUS MUTANT;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CAPSID; CAPSID PROTEINS; CERCOPITHECUS AETHIOPS; GENOME, VIRAL; HERPESVIRUS 1, HUMAN; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; POINT MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TWO-HYBRID SYSTEM TECHNIQUES; VERO CELLS; VIRAL STRUCTURAL PROTEINS;

EID: 0037379174     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.7.4043-4059.2003     Document Type: Article

References (39)

1. Bartel, P. L., C-T. Chien, R. Sternglanz, and S. Fields. 1993. With the two-hybrid system to detect protein-protein interactions, p. 153-179. In D. A. Hartley (ed.), Cellular interactions in development: a practical approach. Oxford University Press, Oxford, United Kingdom.
2. Beaudet-Miller, M., R. Zhang, J. Durkin, W. Gibson, A. D. Kwong, and Z. Hong. 1996. Virus-specific interaction between the human cytomegalovirus major capsid protein and the C terminus of the assembly protein precursor. J. Virol. 70:8081-8088.
3. Breeden, L., and K. Nasmyth. 1985. Regulation of the yeast HO gene. Cold Spring Harb. Symp. Quant. Biol. 50:643-650.
4. Chien, C.-T., P. L. Bartel, R. Sternglanz, and S. Fields. 1991. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. USA 88:9578-9582.
5. 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.
6. Desai, P., N. A. DeLuca, J. C. Glorioso, and S. Person. 1993. Mutations in herpes simplex virus type 1 genes encoding VP5 and VP23 inhibit capsid formation and cleavage of replicated DNA. J. Virol. 67:1357-1364.
7. Desai, P., F. L. Homa, S. Person, and J. C. Glorioso. 1994. A genetic selection method for the transfer of HSV-1 glycoprotein B mutations from plasmid to the viral genome: preliminary characterization of transdominance and entry kinetics of mutant viruses. Virology 204:312-322.
8. Desai, P., S. C. Watkins, and S. Person. 1994. The size and symmetry of B capsids of herpes simplex virus type 1 are determined by the gene products of the UL26 open reading frame. J. Virol. 68:5365-5374.
9. Desai, P., and S. Person. 1996. Molecular interactions between the HSV-1 capsid proteins as measured by the yeast two-hybrid system. Virology 220:516-521.
10. Desai, P., N. A. DeLuca, and S. Person. 1998. Herpes simplex virus type 1 VP26 is not essential for replication in cell culture but influences production of infectious virus in the nervous system of infected mice. Virology 247:115-124.
11. Desai, P., and S. Person. 1999. Second site mutations in the N terminus of the major capsid protein (VP5) overcome a block at the maturation cleavage site of the capsid scaffold proteins of herpes simplex virus type 1. Virology 261:357-366.
12. Fields, S., and O.-K. Song. 1989. A novel genetic system to detect proteinprotein interactions. Nature 340:245-246.
13. Gibson, W., and B. Roizman. 1972. Proteins specified by herpes simplex virus. VIII. Characterization and composition of multiple capsid forms of subtypes 1 and 2. J. Virol. 10:1044-1052.
14. Hendricks, L. C., J. M. McCaffery, G. E. Palade, and M. G. Farquhar. 1993. Disruption of ER to Golgi transport leads to the accumulation of large aggregates containing β-COP in pancreatic acinar cells. Mol. Biol. Cell 4:413-424.
15. Hong, Z., M. Beaudet-Miller, J. Durkin, R. Zhang, and A. D. Kwong. 1996. Identification of a minimal hydrophobic domain in the HSV-1 scaffolding protein which is required for its interaction with the major capsid protein. J. Virol. 70:533-540.
16. Kennard, J., F. J. Rixon, I. M. McDougall, J. D. Tatman, and V. G. Preston. 1995. The 25 amino acid residues at the carboxy terminus of the herpes simplex virus type 1 UL26.5 protein are required for the formation of the capsid shell around the scaffold. J. Gen. Virol. 76:1611-1621.
17. Matusick-Kumar, L., W. W. Newcomb, J. C. Brown, P. J. McCann, I. I. I., W. Hurlburt, S. P. Weinheimer, and M. Gao. 1995. The C-terminal 25 amino acids of the protease and its substrate ICP35 of herpes simplex virus type 1 are involved in the formation of sealed capsids. J. Virol. 69 4347-4356.
18. McGeoch, D. J., M. A. Dalrymple, A. J. Davison, A. Dolan, M. C. Frame, D. McNab, L. J. Perry, J. E. Scott, and P. Taylor. 1988. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J. Gen. Virol. 69:1531-1574.
19. Newcomb, W. W., B. L. Trus, N. Cheng, A. C. Steven, A. K. Sheaffer, D. J. Tenney, S. K. Weller, and J. C. Brown. 2000. Isolation of herpes simplex virus procapsids from cells infected with a protease-deficient mutant virus. J. Virol. 74:1663-1673.
20. Nicholson, P., C. Addison, A. M. Cross, J. Kennard, V. G. Preston, and F. J. Rixon. 1994. Localization of the herpes simplex virus type 1 major capsid protein VP5 to the cell nucleus requires the abundant scaffolding protein VP22a. J. Gen. Virol. 75:1091-1099.
21. Oien, N. L., D. R. Thomsen, M. W. Wathen, W. W. Newcomb, J. C. Brown, and F. L. Homa. 1997. Assembly of herpes simplex virus capsids with the human cytomegalovirus scaffold protein: critical role of the C terminus. J. Virol. 71:1281-1291.
22. Pelletier, A., F. Do, J. J. Brisebois, L. Lagace, and M. G. Cordingly. 1997. Self-association of herpes simplex virus type 1 ICP35 is via coiled-coil interactions and promotes stable interaction with the major capsid protein. J. Virol. 71:5197-5208.
23. Person, S., and P. Desai. 1998. Capsids are formed in a mutant virus blocked at the maturation site of the UL26 and UL26.5 open reading frame of HSV-1 but are not formed in a null mutant of UL38 (VP19C). Virology 242:193-203.
24. Rixon, F. J. 1993. Structure and assembly of herpesviruses. Semin. Virol. 4:135-144.
25. Rixon, F. J., C. Addison, A. McGregor, S. J. McNab, P. Nicholson, V. G. Preston, and J. D. Tatman. 1996. Multiple interactions control the intracellular localization of the herpes simplex virus type 1 capsid proteins. J. Gen. Virol. 77:2251-2260.
26. Rixon, F. J., and D. McNab. 1999. Packaging-competent capsids of a herpes simplex virus temperature-sensitive mutant have properties similar to those of in vitro-assembled procapsids. J. Virol. 73:5714-5721.
27. Roizman, B., and A. Sears. 1996. Herpes simplex viruses and their replication, p. 2223-2295. In B. N. Fields, D. M. Knipe, P. M. Howley, et al. (ed.), Fields virology. Lippincott-Raven, Philadelphia, Pa.
28. Rose, M., M. J. Casadaban, and D. Botstein. 1981. Yeast genes fused to β-galactosidase in Escherichia coli can be expressed normally in yeast. Proc. Natl. Acad. Sci. USA 78:2460-2464.
29. Rost, B., and C. Sander. 1994. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19:55-72.
30. Southern, P. J., and P. Berg. 1982. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under the control of the SV40 early region promoter. J. Mol. Appl. Genet. 1:327-341.
31. Steven, A. C., and P. G. Spear. 1996. Herpesvirus capsid assembly and envelopment, p. 312-351. In R. Burnett et al. (ed.), Structural biology of viruses. Oxford University Press, New York, N.Y.
32. Sweet, R. M., and D. Eisenberg. 1983. Correlation of sequence hydrophobicities measures similarity in three-dimensional protein structure. J. Mol. Biol. 171:479-488.
33. Tatman, J. D., V. G. Preston, P. Nicholson, R. M. Elliot, and F. J. Rixon. 1994. Assembly of herpes simplex virus type 1 capsids with a panel of recombinant baculoviruses. J. Gen. Virol. 75:1101-1113.
34. Thomsen, D. R., W. W. Newcomb, J. C. Brown, and F. L. Homa. 1995. Assembly of herpes simplex virus capsid: requirement for the carboxy-terminal twenty-five amino acids of the proteins encoded by the UL26 and UL26.5 genes. J. Virol. 69:3690-3703.
35. Thomsen, D. R., L. L. Roof, and F. L. Homa. 1994. Assembly of herpes simplex virus (HSV) intermediate capsids in insect cells infected with recombinant baculoviruses expressing HSV capsid proteins. J. Virol. 68:2442-2457.
36. Warner, S. C., P. Desai, and S. Person. 2000. Second site mutations encoding residues 34 and 78 of the major capsid protein (VP5) of herpes simplex virus type 1 are important for overcoming a blocked maturation cleavage site of the capsid scaffold proteins. Virology 278:217-226.
37. Warner, S. C., G. Chytrova, P. Desai, and S. Person. 2001. Mutations in the N terminus of VP5 alter its interaction with the scaffold proteins of herpes simplex virus type 1. Virology 284:308-316.
38. Wood, L. J., M. K. Baxter, S. M. Plafker, and W. Gibson. 1997. Human cytomegalovirus capsid assembly protein precursor (pUL80.5) interacts with itself and with the major capsid protein (pUL86) through two different domains. J. Virol. 71:179-190.
39. A. Science 288:877-880.