Epstein-Barr virus encodes three bona fide ubiquitin-specific proteases

Journal of Virology

Volumn 82, Issue 21, 2008, Pages 10477-10486

  Sompallae, Ramakrishna ^a   Gastaldello, Stefano ^a,b   Hildebrand, Sebastian ^a   Zinin, Nikolay ^a   Hassink, Gerco ^a   Lindsten, Kristina ^a   Haas, Juergen ^c,d   Persson, Bengt ^a,e   Masucci, Maria G ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF MUNICH   (Germany)

^e LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; HISTIDINE; PROTEINASE; UBIQUITIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; UBIQUITIN SPECIFIC PROTEASE; UBIQUITIN-SPECIFIC PROTEASE; VIRUS PROTEIN;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; EPSTEIN BARR VIRUS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; AMINO ACID SUBSTITUTION; BIOLOGY; ENZYMOLOGY; GENE FUSION; GENETICS; METABOLISM; PROTEIN MOTIF; REPORTER GENE; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

HUMAN HERPESVIRUS 4;

AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; ARTIFICIAL GENE FUSION; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; ENDOPEPTIDASES; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HERPESVIRUS 4, HUMAN; MUTAGENESIS, SITE-DIRECTED; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

EID: 55249087477     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01113-08     Document Type: Article

References (52)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Amerik, A. Y., and M. Hochstrasser. 2004. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695:189-207.
3. Baer, R., A. T. Bankier, M. D. Biggin, P. L. Deininger, P. J. Farrell, T. J. Gibson, G. Hatfull, G. S. Hudson, S. C. Satchwell, C. Seguin, et al. 1984. DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature 310:207-211.
4. Bairoch, A., R. Apweiler, C. H. Wu, W. C. Barker, B. Boeckmann, S. Ferro, E. Gasteiger, H. Huang, R. Lopez, M. Magrane, M. J. Martin, D. A. Natale, C. O'Donovan, N. Redaschi, and L. S. Yeh. 2005. The universal protein resource (UniProt). Nucleic Acids Res. 33:D154-D159.
5. Balakirev, M. Y., M. Jaquinod, A. L. Haas, and J. Chroboczek. 2002. Deubiquitinating function of adenovirus proteinase. J. Virol. 76:6323-6331.
6. Barretto, N., D. Jukneliene, K. Ratia, Z. Chen, A. D. Mesecar, and S. C. Baker. 2005. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J. Virol. 79:15189-15198.
7. 2+ finger motif of UL52 severely affects the biochemical activities of the HSV-1 helicase-primase subcomplex. J. Biol. Chem. 274:8068-8076.
8. Carrington-Lawrence, S. D., and S. K. Weller. 2003. Recruitment of polymerase to herpes simplex virus type 1 replication foci in cells expressing mutant primase (UL52) proteins. J. Virol. 77:4237-4247.
9. Catic, A., S. Misaghi, G. A. Korbel, and H. L. Ploegh. 2007. ElaD, a deubiquitinating protease expressed by Escherichia coli. PLoS ONE 2:e381.
10. Chen, Y., S. D. Carrington-Lawrence, P. Bai, and S. K. Weller. 2005. Mutations in the putative zinc-binding motif of UL52 demonstrate a complex interdependence between the UL5 and UL52 subunits of the human herpes simplex virus type 1 helicase/primase complex. J. Virol. 79:9088-9096.
11. Ciechanover, A., A. Orian, and A. L. Schwartz. 2000. Ubiquitin-mediated proteolysis: biological regulation via destruction. Bioessays 22:442-451.
12. Crute, J. J., and I. R. Lehman. 1991. Herpes simplex virus-1 helicase-primase: physical and catalytic properties. J. Biol. Chem. 266:4484-4488.
13. 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.
14. D'Andrea, A., and D. Pellman. 1998. Deubiquitinating enzymes: a new class of biological regulators. Crit. Rev. Biochem. Mol. Biol. 33:337-352.
15. Dracheva, S., E. V. Koonin, and J. J. Crute. 1995. Identification of the primase active site of the herpes simplex virus type 1 helicase-primase. J. Biol. Chem. 270:14148-14153.
16. Drake, J. W. 2006. Chaos and order in spontaneous mutation. Genetics 173:1-8.
17. Eddy, S. R. 1998. Profile hidden Markov models. Bioinformatics 14:755-763.
18. Frias-Staheli, N., N. V. Giannakopoulos, M. Kikkert, S. L. Taylor, A. Bridgen, J. Paragas, J. A. Richt, R. R. Rowland, C. S. Schmaljohn, D. J. Lenschow, E. J. Snijder, A. Garcia-Sastre, and H. W. ten Virgin. 2007. Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2:404-416.
19. Gardberg, A., L. Shuvalova, C. Monnerjahn, M. Konrad, and A. Lavie. 2003. Structural basis for the dual thymidine and thymidylate kinase activity of herpes thymidine kinases. Structure 11:1265-1277.
20. Gill, M. B., J. L. Kutok, and J. D. Fingeroth. 2007. Epstein-Barr virus thymidine kinase is a centrosomal resident precisely localized to the periphery of centrioles. J. Virol. 81:6523-6535.
21. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
22. Hewitt, E. W., L. Duncan, D. Mufti, J. Baker, P. G. Stevenson, and P. J. Lehner. 2002. Ubiquitylation of MHC class I by the K3 viral protein signals internalization and TSG101-dependent degradation. EMBO J. 21:2418-2429.
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. Klinedinst, D. K., and M. D. Challberg. 1994. Helicase-primase complex of herpes simplex virus type 1: a mutation in the UL52 subunit abolishes primase activity. J. Virol. 68:3693-3701.
25. Kovalenko, A., C. Chable-Bessia, G. Cantarella, A. Israel, D. Wallach, and G. Courtois. 2003. The tumour suppressor CYLD negatively regulates NF-κB signalling by deubiquitination. Nature 424:801-805.
26. Larsen, C. N., J. S. Price, and K. D. Wilkinson. 1996. Substrate binding and catalysis by ubiquitin C-terminal hydrolases: identification of two active site residues. Biochemistry 35:6735-6744.
27. Lee, J. C., and M. E. Peter. 2003. Regulation of apoptosis by ubiquitination. Immunol. Rev. 193:39-47.
28. Lehner, P. J., S. Hoer, R. Dodd, and L. M. Duncan. 2005. Downregulation of cell surface receptors by the K3 family of viral and cellular ubiquitin E3 ligases. Immunol. Rev. 207:112-125.
29. Lindner, H. A., N. Fotouhi-Ardakani, V. Lytvyn, P. Lachance, T. Sulea, and R. Menard. 2005. The papain-like protease from the severe acute respiratory syndrome coronavirus is a deubiquitinating enzyme. J. Virol. 79:15199-15208.
30. Littler, E., J. Zeuthen, A. A. McBride, E. Trost Sorensen, K. L. Powell, J. E. Walsh-Arrand, and J. R. Arrand. 1986. Identification of an Epstein-Barr virus-coded thymidine kinase. EMBO J. 5:1959-1966.
31. Loureiro, J., and H. L. Ploegh. 2006. Antigen presentation and the ubiquitin-proteasome system in host-pathogen interactions. Adv. Immunol. 92:225-305.
32. Lu, G., and E. N. Moriyama. 2004. Vector NTI, a balanced all-in-one sequence analysis suite. Brief Bioinform. 5:378-388.
33. Lynch, O. T., and M. Gadina. 2004. Ubiquitination for activation: new directions in the NF-κB roadmap. Mol. Interv. 4:144-146.
34. Masucci, M. G. 2004. Epstein-Barr virus oncogenesis and the ubiquitin-proteasome system. Oncogene 23:2107-2115.
35. Menard, R., H. E. Khouri, C. Plouffe, R. Dupras, D. Ripoll, T. Vernet, D. C. Tessier, F. Lalberte, D. Y. Thomas, and A. C. Storer. 1990. A protein engineering study of the role of aspartate 158 in the catalytic mechanism of papain. Biochemistry 29:6706-6713.
36. Moldovan, G. L., B. Pfander, and S. Jentsch. 2007. PCNA, the maestro of the replication fork. Cell 129:665-679.
37. Nijman, S. M., T. T. Huang, A. M. Dirac, T. R. Brummelkamp, R. M. Kerkhoven, A. D. D'Andrea, and R. Bernards. 2005. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol. Cell 17:331-339.
38. 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.
39. Rice, P., I. Longden, and A. Bleasby. 2000. EMBOSS: the European molecular biology open software suite. Trends Genet. 16:276-277.
40. Rytkonen, A., J. Poh, J. Garmendia, C. Boyle, A. Thompson, M. Liu, P. Freemont, J. C. Hinton, and D. W. Holden. 2007. SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl. Acad. Sci. USA 104:3502-3507.
41. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
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. 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.
44. Schwartz, A. L., and A. Ciechanover. 1999. The ubiquitin-proteasome pathway and pathogenesis of human diseases. Annu. Rev. Med. 50:57-74.
45. Shackelford, J., and J. S. Pagano. 2004. Tumor viruses and cell signaling pathways: deubiquitination versus ubiquitination. Mol. Cell. Biol. 24:5089-5093.
46. Sun, L., and Z. J. Chen. 2004. The novel functions of ubiquitination in signaling. Curr. Opin. Cell Biol. 16:119-126.
47. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
48. Uetz, P., Y. A. Dong, C. Zeretzke, C. Atzler, A. Baiker, B. Berger, S. V. Rajagopala, M. Roupelieva, D. Rose, E. Fossum, and J. Haas. 2006. Herpesviral protein networks and their interaction with the human proteome. Science 311:239-242.
49. Verma, R., L. Aravind, R. Oania, W. H. McDonald, J. R. Yates III, E. V. Koonin, and R. J. Deshaies. 2002. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298:611-615.
50. Wing, S. S. 2003. Deubiquitinating enzymes: the importance of driving in reverse along the ubiquitin-proteasome pathway. Int. J. Biochem. Cell. Biol. 35:590-605.
51. Yokoyama, N., K. Fujii, M. Hirata, K. Tamai, T. Kiyono, K. Kuzushima, Y. Nishiyama, M. Fujita, and T. Tsurumi. 1999. Assembly of the Epstein-Barr virus BBLF4, BSLF1 and BBLF2/3 proteins and their interactive properties. J. Gen. Virol. 80(Pt. 11):2879-2887.
52. Zhou, H., D. M. Monack, N. Kayagaki, I. Wertz, J. Yin, B. Wolf, and V. M. Dixit. 2005. Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-κB activation. J. Exp. Med. 202:1327-1332.