High-molecular-weight protein (pUL48) of human cytomegalovirus is a competent deubiquitinating protease: Mutant viruses altered in its active-site cysteine or histidine are viable

Journal of Virology

Volumn 80, Issue 12, 2006, Pages 6003-6012

  Wang, Jianlei ^a   Loveland, Amy N ^a   Kattenhorn, Lisa M ^b   Ploegh, Hidde L ^b   Gibson, Wade ^a  

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

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYSTEINE; CYSTEINE PROTEINASE; HISTIDINE; ISOLEUCINE; PROTEIN PUL48; PROTEINASE; UBIQUITIN; UNCLASSIFIED DRUG; VIRUS ENZYME;

AMINO ACID SUBSTITUTION; ARTICLE; CELL LYSATE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MOLECULAR SIZE; MOLECULAR WEIGHT; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS MUTANT; VIRUS PARTICLE; VIRUS REPLICATION;

BINDING SITES; CELLS, CULTURED; CYSTEINE; CYSTEINE ENDOPEPTIDASES; CYTOMEGALOVIRUS; FIBROBLASTS; HISTIDINE; HUMANS; MUTATION, MISSENSE; VIRAL PROTEINS; VIRION; VIRUS REPLICATION;

HUMAN HERPESVIRUS 5;

EID: 33744917811     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00401-06     Document Type: Article

References (50)

1. Bacchetti, S., M. J. Evelegh, and B. Muirhead. 1986. Identification and separation of the two subunits of the herpes simplex virus ribonucleotide reductase. J. Virol. 57:1177-1181.
2. Banks, L. M., I. W. Halliburton, D. J. Purifoy, R. A. Killington, and K. L. Powell. 1985. Studies on the herpes simplex virus alkaline nuclease: detection of type-common and type-specific epitopes on the enzyme. J. Gen. Virol. 66:1-14.
3. Batterson, W., D. Furlong, and B. Roizman. 1983. Molecular genetics of herpes simplex virus. VIII. Further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of viral reproductive cycle. J. Virol. 45:397-407.
4. Bechtel, J. T., and T. Shenk. 2002. Human cytomegalovirus UL47 tegument protein functions after entry and before immediate-early gene expression. J. Virol. 76:1043-1050.
5. Borodovsky, A., H. Ovaa, N. Kolli, T. Gan-Erdene, K. D. Wilkinson, H. L. Ploegh, and B. M. Kessler. 2002. Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 9:1149-1159.
6. Borst, E., and M. Messerle. 2000. Development of a cytomegalovirus vector for somatic gene therapy. Bone Marrow Transplant. 25(Suppl. 2):S80-S82.
7. Boutell, C., S. Sadis, and R. D. Everett. 2002. Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases in vitro. J. Virol. 76:841-850.
8. Caradonna, S., D. Worrad, and R. Lirette. 1987. Isolation of a herpes simplex virus cDNA encoding the DNA repair enzyme uracil-DNA glycosylase. J. Virol. 61:3040-3047.
9. Coscoy, L., D. J. Sanchez, and D. Ganem. 2001. A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J. Cell Biol. 155:1265-1273.
10. Crute, J. J., T. Tsurumi, L. A. Zhu, S. K. Weller, P. D. Olivo, M. D. Challberg, E. S. Mocarski, and I. R. Lehman. 1989. Herpes simplex virus 1 helicase-primase: a complex of three herpes-encoded gene products. Proc. Natl. Acad. Sci. USA 86:2186-2189.
11. Cunningham, C., A. J. Davison, A. Dolan, M. C. Frame, D. J. McGeoch, D. M. Meredith, H. W. Moss, and A. C. Orr. 1992. The UL13 virion protein of herpes simplex virus type 1 is phosphorylated by a novel virus-induced protein kinase. J. Gen. Virol. 73:303-311.
12. Desai, P. 2000. A null mutation in the UL36 gene of herpes simplex virus type 1 results in the accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J. Virol. 74:11608-11618.
13. Desai, P., J. C. Akpa, and S. Person. 2003. Residues of VP26 of herpes simplex virus type 1 that are required for its interaction with capsids. J. Virol. 77:391-404.
14. Desai, P., G. Sexton, J. McCaffery, and S. Person. 2001. A null mutation in the gene encoding the UL37 polypeptide of herpes simplex virus type 1 abrogates virus maturation. J. Virol. 75:10259-10271.
15. Dunn, W., C. Chou, H. Li, R. Hai, D. Patterson, V. Stoic, H. Zhu, and F. Liu. 2003. Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. USA 100:14223-14228.
16. Frame, M. C., F. C. Purves, D. J. McGeoch, H. S. Marsden, and D. P. Leader. 1987. Identification of the herpes simplex virus protein kinase as the product of viral gene US3. J. Gen. Virol. 68:2699-2704.
17. Gibson, W. 1981. Structural and nonstructural proteins of strain Colburn cytomegalovirus. Virology 111:516-537.
18. 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.
19. Harmon, M.-E., and W. Gibson. 1996. High molecular weight virion protein of human cytomegalovirus forms complex with product of adjacent open reading frame, abstr. W35-4, p. 144. Proc. Am. Soc. Virol.
20. He, Z., Y. S. He, Y. Kim, L. Chu, C. Ohmstede, K. K. Biron, and D. M. Coen. 1997. The human cytomegalovirus UL97 protein is a protein kinase that autophosphorylates on serines and threonines. J. Virol. 71:405-411.
21. Honess, R. W., and B. Roizman. 1974. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J. Virol. 14:8-19.
22. Irmiere, A., and W. Gibson. 1983. Isolation and characterization of a noninfectious virion-like particle released from cells infected with human strains of cytomegalovirus. Virology 130:118-133.
23. Kattenhorn, L. M., G. A. Korbel, B. M. Kessler, E. Spooner, and H. L. Ploegh. 2005. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol. Cell 19:547-557.
24. Kaufmann, S. H., C. M. Ewing, and J. H. Shaper. 1987. The erasable western blot. Anal. Biochem. 161:89-95.
25. Kit, S., and D. R. Dubbs. 1965. Properties of deoxythymidine kinase partially purified from noninfected mouse fibroblast cells. Virology 26:16-27.
26. Klupp, B. G., W. Fuchs, H. Granzow, R. Nixdorf, and T. C. Mettenleiter. 2002. Pseudorabies virus UL36 tegument protein physically interacts with the UL37 protein. J. Virol. 76:3065-3071.
27. Klupp, B. G., H. Granzow, E. Mundt, and T. C. Mettenleiter. 2001. Pseudorabies virus UL37 gene product is involved in secondary envelopment. J. Virol. 75:8927-8936.
28. Knipe, D. M., W. Batterson, C. Nosal, B. Roizman, and A. Buchan. 1981. Molecular genetics of herpes simplex virus. VI. Characterization of a temperature-sensitive mutant defective in the expression of all early viral gene products. J. Virol. 38:539-547.
29. Lemaster, S., and B. Roizman. 1980. Herpes simplex virus phosphoproteins. II. Characterization of the virion protein kinase and of the polypeptides phosphorylated in the virion. J. Virol. 35:798-811.
30. Little, S. P., and P. A. Schaffer. 1981. Expression of the syncytial (syn) phenotype in HSV-1, strain KOS: genetic and phenotypic studies of mutants in two syn loci. Virology 112:686-702.
31. Liu, F., and B. Roizman. 1991. The herpes simplex virus 1 gene encoding a protease also contains within its coding domain the gene encoding the more abundant substrate. J. Virol. 65:5149-5156.
32. Loveland, A. N., C. K. Chan, E. J. Brignole, and W. Gibson. 2005. Cleavage of human cytomegalovirus protease pUL80a at internal and cryptic sites is not essential but enhances infectivity. J. Virol. 79:12961-12968.
33. McNabb, D., and R. Courtney. 1992. Characterization of the large protein (ICP1/2) of herpes simplex virus type 1. Virology 190:221-232.
34. McNabb, D. S., and R. J. Courtney. 1992. Analysis of the UL36 open reading frame encoding the large tegument protein (ICP1/2) of herpes simplex virus type 1. J. Virol. 66:7581-7584.
35. Mettenleiter, T. C. 2002. Herpesvirus assembly and egress. J. Virol. 76:1537-1547.
36. Muyrers, J. P., Y. Zhang, V. Benes, G. Testa, W. Ansorge, and A. F. Stewart. 2000. Point mutation of bacterial artificial chromosomes by ET recombination. EMBO Rep. 1:239-243.
37. Ovaa, H., B. M. Kessler, U. Rolen, P. J. Galardy, H. L. Ploegh, and M. G. Masucci. 2004. Activity-based ubiquitin-specific protease (USP) profiling of virus-infected and malignant human cells. Proc. Natl. Acad. Sci. USA 101:2253-2258.
38. Preston, V. G., and F. B. Fisher. 1984. Identification of the herpes simplex virus type 1 gene encoding the dUTPase. Virology 138:58-68.
39. Purifoy, D. J., R. B. Lewis, and K. L. Powell. 1977. Identification of the herpes simplex virus DNA polymerase gene. Nature 269:621-623.
40. Roby, C., and W. Gibson. 1986. Characterization of phosphoproteins and protein kinase activity of virions, noninfectious enveloped particles, and dense bodies of human cytomegalovirus. J. Virol. 59:714-727.
41. Scheffczik, H., C. G. Savva, A. Holzenburg, L. Kolesnikova, and E. Bogner. 2002. The terminase subunits pUL56 and pUL89 of human cytomegalovirus are DNA-metabolizing proteins with toroidal structure. Nucleic Acids Res. 30:1695-1703.
42. Schlieker, C., G. A. Korbel, L. M. Kattenhorn, and H. L. Ploegh. 2005. A deubiquitinating activity is conserved in the large tegument protein of the herpesviridae. J. Virol. 79:15582-15585.
43. Spear, P. G., and B. Roizman. 1972. Proteins specified by herpes simplex virus. V. Purification and structural proteins of the herpesvirion. J. Virol. 9:143-159.
44. Trus, B. L., W. Gibson, N. Cheng, and A. C. Steven. 1999. Capsid structure of simian cytomegalovirus from cryoelectron microscopy: evidence for tegument attachment sites. J. Virol. 73:2181-2192. (Erratum, 73:4530.)
45. Underwood, M. R., R. J. Harvey, S. C. Stanat, M. L. Hemphill, T. Miller, J. C. Drach, L. B. Townsend, and K. K. Biron. 1998. Inhibition of human cytomegalovirus DNA maturation by a benzimidazole ribonucleoside is mediated through the UL89 gene product. J. Virol. 72:717-725.
46. Vittone, V., E. Diefenbach, D. Triffett, M. W. Douglas, A. L. Cunningham, and R. J. Diefenbach. 2005. Determination of interactions between tegument proteins of herpes simplex virus type 1. J. Virol. 79:9566-9571.
47. Welch, A. R., A. S. Woods, L. M. McNally, R. J. Cotter, and W. Gibson. 1991. A herpesvirus maturational protease, assemblin: identification of its gene, putative active site domain, and cleavage site. Proc. Natl. Acad. Sci. USA 88:10792-10796.
48. Zhang, Y., F. Buchholz, J. P. Muyrers, and A. F. Stewart. 1998. A new logic for DNA engineering using recombination in Escherichia coli. Nat. Genet. 20:123-128.
49. Zhou, Z. H., D. H. Chen, J. Jakana, F. J. Rixon, and W. Chiu. 1999. Visualization of tegument-capsid interactions and DNA in intact herpes simplex virus type 1 virions. J. Virol. 73:3210-3218.
50. Zhu, L. A., and S. K. Weller. 1992. The six conserved helicase motifs of the UL5 gene product, a component of the herpes simplex virus type 1 helicase-primase, are essential for its function. J. Virol. 66:469-479.