Cleavage specificity of the UL48 deubiquitinating protease activity of human cytomegalovirus and the growth of an active-site mutant virus in cultured cells

Journal of Virology

Volumn 83, Issue 23, 2009, Pages 12046-12056

  Kim, Eui Tae ^a   Oh, Se Eun ^a   Lee, Yun Ok ^a   Gibson, Wade ^b   Ahn, Jin Hyun ^a  

^a Sungkyunkwan University School of Medicine   (South Korea)

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

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DEUBIQUITINASE; DIMER; HISTIDINE; HYDROLASE; LYSINE; OLIGOMER; PEPTIDASE; PROTEIN UL48; PROTEINASE; UBIQUITIN; UNCLASSIFIED DRUG; VIRUS HEMAGGLUTININ; VIRUS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IMMUNOPRECIPITATION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROGENY; PROTEIN CLEAVAGE; PROTEIN DOMAIN; UBIQUITINATION; VIROGENESIS; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS MUTANT; VIRUS REPLICATION; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELLS, CULTURED; CYTOMEGALOVIRUS; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PEPTIDE HYDROLASES; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY; UBIQUITIN; VIRAL PROTEINS; VIRUS REPLICATION;

HUMAN HERPESVIRUS 5; MIRIDAE; SIMPLEXVIRUS;

EID: 70450176023     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00411-09     Document Type: Article

References (44)

1. Amerik, A. Y., and M. Hochstrasser. 2004. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695:189-207.
2. Baldick, C. J., Jr., A. Marchini, C. E. Patterson, and T. Shenk. 1997. Human cytomegalovirus tegument protein pp71 (ppUL82) enhances the infectivity of viral DNA and accelerates the infectious cycle. J. Virol. 71:4400-4408.
3. Bottcher, S., H. Granzow, C. Maresch, B. Mohl, B. G. Klupp, and T. C. Mettenleiter. 2007. Identification of functional domains within the essential large tegument protein pUL36 of pseudorabies virus. J. Virol. 81:13403-13411. (Pubitemid 350247837)
4. Bottcher, S., C. Maresch, H. Granzow, B. G. Klupp, J. P. Teifke, and T. C. Mettenleiter. 2008. Mutagenesis of the active-site cysteine in the ubiquitin-specific protease contained in large tegument protein pUL36 of pseudorabies virus impairs viral replication in vitro and neuroinvasion in vivo. J. Virol. 82:6009-6016. (Pubitemid 351822274)
5. Britt, W. J., and S. Boppana. 2004. Human cytomegalovirus virion proteins. Hum. Immunol. 65:395-402.
6. Browne, E. P., and T. Shenk. 2003. Human cytomegalovirus UL83-coded pp65 virion protein inhibits antiviral gene expression in infected cells. Proc. Natl. Acad. Sci. USA 100:11439-11444.
7. Ciechanover, A. 2005. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat. Rev. Mol. Cell Biol. 6:79-87.
8. Desai, P. J. 2000. A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J. Virol. 74:11608-11618.
9. Dunn, W., C. Chou, H. Li, R. Hai, D. Patterson, V. Stolc, H. Zhu, and F. Liu. 2003. Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. USA 100:14223-14228.
10. Edelmann, M. J., A. Iphofer, M. Akutsu, M. Altun, K. di Gleria, H. B. Kramer, E. Fiebiger, S. Dhe-Paganon, and B. M. Kessler. 2009. Structural basis and specificity of human otubain 1-mediated deubiquitination. Biochem. J. 418:379-390.
11. Evans, P. C., H. Ovaa, M. Hamon, P. J. Kilshaw, S. Hamm, S. Bauer, H. L. Ploegh, and T. S. Smith. 2004. Zinc-finger protein A20, a regulator of inflammation and cell survival, has de-ubiquitinating activity. Biochem. J.378:727-734.
12. Fuchs, W., B. G. Klupp, H. Granzow, and T. C. Mettenleiter. 2004. Essential function of the pseudorabies virus UL36 gene product is independent of its interaction with the UL37 protein. J. Virol. 78:11879-11889. (Pubitemid 39390774)
13. Gebert, S., S. Schmolke, G. Sorg, S. Floss, B. Plachter, and T. Stamminger. 1997. The UL84 protein of human cytomegalovirus acts as a transdominant inhibitor of immediate-early-mediated transactivation that is able to prevent viral replication. J. Virol. 71:7048-7060. (Pubitemid 27355371)
14. Gibson, W. 2008. Structure and formation of the cytomegalovirus virion. Curr. Top. Microbiol. Immunol. 325:187-204.
15. Glickman, M. H., and A. Ciechanover. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82:373-428.
16. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
17. Huh, Y. H., Y. E. Kim, E. T. Kim, J. J. Park, M. J. Song, H. Zhu, G. S. Hayward, and J.-H. Ahn. 2008. Binding STAT2 by the acidic domain of human cytomegalovirus IE1 promotes viral growth and is negatively regulated by SUMO. J. Virol. 82:10444-10454.
18. Jarosinski, K., L. Kattenhorn, B. Kaufer, H. Ploegh, and N. Osterrieder. 2007. A herpesvirus ubiquitin-specific protease is critical for efficient T cell lymphoma formation. Proc. Natl. Acad. Sci. USA 104:20025-20030.
19. 1 phase of the cell cycle. J. Virol. 77:3451-3459.
20. 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.
21. Kattenhorn, L. M., R. Mills, M. Wagner, A. Lomsadze, V. Makeev, M. Borodovsky, H. L. Ploegh, and B. M. Kessler. 2004. Identification of proteins associated with murine cytomegalovirus virions. J. Virol. 78:11187-11197. (Pubitemid 39299658)
22. Kim, J. H., K. C. Park, S. S. Chung, O. Bang, and C. H. Chung. 2003. Deubiquitinating enzymes as cellular regulators. J. Biochem. (Tokyo) 134: 9-18.
23. Lee, J. I., G. W. Luxton, and G. A. Smith. 2006. Identification of an essential domain in the herpesvirus VP1/2 tegument protein: the carboxy terminus directs incorporation into capsid assemblons. J. Virol. 80:12086-12094.
24. 1 phase of the cell cycle. J. Virol. 73:676-683.
25. Marchini, A., H. Liu, and H. Zhu. 2001. Human cytomegalovirus with IE-2 (UL122) deleted fails to express early lytic genes. J. Virol. 75:1870-1878. (Pubitemid 32110177)
26. Mocarski, E. S., T. Shenk, and R. F. Pass. 2007. Cytomegaloviruses. 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, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
27. Muranyi, W., J. Haas, M. Wagner, G. Krohne, and U. H. Koszinowski. 2002. Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 297:854-857. (Pubitemid 34839639)
28. Nijman, S. M., M. P. Luna-Vargas, A. Velds, T. R. Brummelkamp, A. M. Dirac, T. K. Sixma, and R. Bernards. 2005. A genomic and functional inventory of deubiquitinating enzymes. Cell 123:773-786. (Pubitemid 41721026)
29. Park, J. J., Y. E. Kim, H. T. Pham, E. T. Kim, Y. H. Chung, and J. H. Ahn. 2007. Functional interaction of the human cytomegalovirus IE2 protein with histone deacetylase 2 in infected human fibroblasts. J. Gen. Virol. 88:3214-3223.
30. 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. (Pubitemid 43032341)
31. Schlieker, C., W. A. Weihofen, E. Frijns, L. M. Kattenhorn, R. Gaudet, and H. L. Ploegh. 2007. Structure of a herpesvirus-encoded cysteine protease reveals a unique class of deubiquitinating enzymes. Mol. Cell 25:677-687. (Pubitemid 46341922)
32. Schmolke, S., P. Drescher, G. Jahn, and B. Plachter. 1995. Nuclear targeting of the tegument protein pp65 (UL83) of human cytomegalovirus: an unusual bipartite nuclear localization signal functions with other portions of the protein to mediate its efficient nuclear transport. J. Virol. 69:1071-1078.
33. Seo, J. Y., and W. J. Britt. 2007. Cytoplasmic envelopment of human cytomegalovirus requires the postlocalization function of tegument protein pp28 within the assembly compartment. J. Virol. 81:6536-6547.
34. Seo, J. Y., and W. J. Britt. 2006. Sequence requirements for localization of human cytomegalovirus tegument protein pp28 to the virus assembly compartment and for assembly of infectious virus. J. Virol. 80:5611-5626.
35. Silva, M. C., Q. C. Yu, L. Enquist, and T. Shenk. 2003. Human cytomegalovirus UL99-encoded pp28 is required for the cytoplasmic envelopment of tegument-associated capsids. J. Virol. 77:10594-10605.
36. Soboleva, T. A., and R. T. Baker. 2004. Deubiquitinating enzymes: their functions and substrate specificity. Curr. Protein Pept. Sci. 5:191-200.
37. Stamminger, T., M. Gstaiger, K. Weinzierl, K. Lorz, M. Winkler, and W. Schaffner. 2002. Open reading frame UL26 of human cytomegalovirus encodes a novel tegument protein that contains a strong transcriptional activation domain. J. Virol. 76:4836-4847. (Pubitemid 34441689)
38. Sun, S. C. 2008. Deubiquitylation and regulation of the immune response. Nat. Rev. Immunol. 8:501-511.
39. Wang, J., A. N. Loveland, L. M. Kattenhorn, H. L. Ploegh, and W. Gibson. 2006. High-molecular-weight protein (pUL48) of human cytomegalovirus is a competent deubiquitinating protease: mutant viruses altered in its activesite cysteine or histidine are viable. J. Virol. 80:6003-6012. (Pubitemid 43849178)
40. Wertz, I. E., K. M. O'Rourke, H. Zhou, M. Eby, L. Aravind, S. Seshagiri, P. Wu, C. Wiesmann, R. Baker, D. L. Boone, A. Ma, E. V. Koonin, and V. M. Dixit. 2004. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430:694-699.
41. Wilkinson, K. D., and M. Hochstrasser. 1998. The ubiquitinating enzymes. Plenum Press, New York, NY.
42. Winborn, B. J., S. M. Travis, S. V. Todi, K. M. Scaglione, P. Xu, A. J. Williams, R. E. Cohen, J. Peng, and H. L. Paulson. 2008. The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J. Biol. Chem. 283:26436-26443.
43. Winkler, M., S. A. Rice, and T. Stamminger. 1994. UL69 of human cytomegalovirus, an open reading frame with homology to ICP27 of herpes simplex virus, encodes a transactivator of gene expression. J. Virol. 68:3943-3954. (Pubitemid 24177420)
44. Yu, D., M. C. Silva, and T. Shenk. 2003. Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc. Natl. Acad. Sci. USA 100:12396-12401.