Structural aspects of recently discovered viral deubiquitinating activities

Biological Chemistry

Volumn 387, Issue 7, 2006, Pages 853-862

  Sulea, Traian ^a   Lindner, Holger A ^a   Ménard, Robert ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Adenovirus protease; Herpesvirus UL36 tegument protein; Protein structure comparison; SARS coronavirus papain like protease; Ubiquitin; Ubiquitin like modifiers

Indexed keywords

ADENAIN; NEDD8 PROTEIN; PROTEINASE; SUMO PROTEIN; UBIQUITIN; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG; VIRUS ENZYME;

ADENOVIRUS; AMINO ACID SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL ACTIVITY; CONFERENCE PAPER; CORONAVIRUS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME DEGRADATION; ENZYME PURIFICATION; ENZYME SPECIFICITY; HERPES VIRUS; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN MOTIF; SEQUENCE HOMOLOGY; UBIQUITINATION; VIRION; VIRUS GENOME; VIRUS INFECTION;

AMINO ACID SEQUENCE; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUITIN; VIRAL PROTEINS; VIRUSES;

ADENOVIRIDAE; CORONAVIRUS; HERPESVIRIDAE;

EID: 33746192122     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2006.108     Document Type: Conference Paper

References (77)

1. Ambroggio, X.I., Rees, D.C., and Deshaies, R.J. (2004). JAMM: a metalloprotease-like zinc site in the proteasome and signalosome. PLoS Biol. 2, e2.
2. Amerik, A.Y. and Hochstrasser, M. (2004). Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695, 189-207.
3. Andreeva, A., Howorth, D., Brenner, S.E., Hubbard, T.J.P., Chothia, C., and Murzin, A.G. (2004). SCOP database in 2004: refinements integrate structure and sequence family data. Nucleic Acids Res. 32, D226-D229.
4. Balakirev, M.Y., Jaquinod, M., Haas, A.L., and Chroboczek, J. (2002). Deubiquitinating function of adenovirus proteinase. J. Virol. 76, 6323-6331.
5. Balakirev, M.Y., Tcherniuk, S.O., Jaquinod, M., and Chroboczek, J. (2003). Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep. 4, 517-522.
6. Baniecki, M.L., McGrath, W.J., McWhirter, S.M., Li, C., Toledo, D.L., Pellicena, P., Barnard, D.L., Thorn, K.S., and Mangel, W.F. (2001). Interaction of the human adenovirus proteinase with its 11-amino acid cofactor pVlc. Biochemistry 40, 12349-12356.
7. Banks, L., Pim, D., and Thomas, M. (2003). Viruses and the 26S proteasome: hacking into destruction. Trends Biochem. Sci. 28, 452-459.
8. Baroth, M., Orlich, M., Thiel, H.J., and Becher, P. (2000). Insertion of cellular NEDD8 coding sequences in a pestivirus. Virology 278, 456-466.
9. Barretto, N., Jukneliene, D., Ratia, K., Chen, Z., Mesecar, A.D., and Baker, S.C. (2005). The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J. Virol. 79, 15189-15198.
10. Borodovsky, A., Ovaa, H., Kolli, N., Gan-Erdene, T., Wilkinson, K.D., Ploegh, H.L., and Kessler, B.M. (2002). Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 9, 1149-1159.
11. Brown, M.T. and Mangel, W.F. (2004). Interaction of actin and its 11-amino acid C-terminal peptide as cofactors with the adenovirus proteinase. FEBS Lett. 563, 213-218.
12. Brown, M.T., McBride, K.M., Baniecki, M.L., Reich, N.C., Marriott, G., and Mangel, W.F. (2002). Actin can act as a cofactor for a viral proteinase in the cleavage of the cytoskeleton. J. Biol. Chem. 277, 46298-46303.
13. Chen, P.H., Ornelles, D.A., and Shenk, T. (1993). The adenovirus L3 23-kilodalton proteinase cleaves the amino-terminal head domain from cytokeratin 18 and disrupts the cytokeratin network of HeLa cells. J. Virol. 67, 3507-3514.
14. Cotten, M. and Weber, J.M. (1995). The adenovirus protease is required for virus entry into host cells. Virology 213, 494-502.
15. d'Azzo, A., Bongiovanni, A., and Nastasi, T. (2005). E3 ubiquitin ligases as regulators of membrane protein trafficking and degradation. Traffic 6, 429-441.
16. Dao, C.T. and Zhang, D.E. (2005). ISG15: a ubiquitin-like enigma. Front. Biosci. 10, 2701-2722.
17. Ding, J., McGrath, W.J., Sweet, R.M., and Mangel, W.F. (1996). Crystal structure of the human adenovirus proteinase with its 11 amino acid cofactor. EMBO J. 15, 1778-1783.
18. Dong, S. and Baker, S.C. (1994). Determinants of the p28 cleavage site recognized by the first papain-like cysteine proteinase of murine coronavirus. Virology 204, 541-549.
19. Everett, R.D., Meredith, M., Orr, A., Cross, A., Kathoria, M., and Parkinson, J. (1997). A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein. EMBO J. 16, 1519-1530.
20. Giannakopoulos, N.V., Luo, J.K., Papov, V., Zou, W., Lenschow, D.J., Jacobs, B.S., Borden, E.C., Li, J., Virgin, H.W., and Zhang, D.E. (2005). Proteomic identification of proteins conjugated to ISG15 in mouse and human cells. Biochem. Biophys. Res. Commun. 336, 496-506.
21. Glickman, M.H. and Ciechanover, A. (2002). The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82, 373-428.
22. Greber, U.F., Webster, P., Weber, J., and Helenius, A. (1996). The role of the adenovirus protease on virus entry into cells. EMBO J. 15, 1766-1777.
23. Haglund, K. and Dikic, I. (2005). Ubiquitylation and cell signaling. EMBO J. 24, 3353-3359.
24. Han, Y.S., Chang, G.G., Juo, C.G., Lee, H.J., Yeh, S.H., Hsu, J.T., and Chen, X. (2005). Papain-like protease 2 (PLP2) from severe acute respiratory syndrome coronavirus (SARS-CoV): expression, purification, characterization, and inhibition. Biochemistry 44, 10349-10359.
25. Harcourt, B.H., Jukneliene, D., Kanjanahaluethai, A., Bechill, J., Severson, K.M., Smith, C.M., Rota, P.A., and Baker, S.C. (2004). Identification of severe acute respiratory syndrome coronavirus replicase products and characterization of papain-like protease activity. J. Virol. 78, 13600-13612.
26. 2+-binding finger connecting the two domains of a papain-like fold. J. Biol. Chem. 274, 14918-14925.
27. Hetfeld, B.K.J., Helfrich, A., Kapelari, B., Scheel, H., Hofmann, K., Guterman, A., Glickman, M., Schade, R., Kloetzel, P.M., and Dubiel, W. (2005). The zinc finger of the CSN-associated deubiquitinating enzyme USP15 is essential to rescue the E3 ligase Rbx1. Curr. Biol. 15, 1217-1221.
28. Honig, J.E., Osborne, J.C., and Nichol, S.T. (2004). Crimean-Congo hemorrhagic fever virus genome L RNA segment and encoded protein. Virology 321, 29-35.
29. Hu, M., Li, P., Li, M., Li, W., Yao, T., Wu, J.W., Gu, W., Cohen, R.E., and Shi, Y. (2002). Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 111, 1041-1054.
30. Hu, M., Li, P., Sing, L., Jeffrey, P., Chenova, T., Wilkinson, K.D., Cohen, R.E., and Shi, Y. (2005). Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. EMBO J. 24, 3747-3756.
31. Iyer, L.M., Koonin, E.V., and Aravind, L. (2004). Novel predicted peptidases with a potential role in the ubiquitin signaling pathway. Cell Cycle 3, 1440-1450.
32. Johnston, S.C., Riddle, S.M., Cohen, R.E., and Hill, C.P. (1999). Structural basis for the specificity of ubiquitin C-terminal hydrolases. EMBO J. 18, 3877-3887.
33. Kattenhorn, L.M., Korbel, G.A., Kessler, B.M., Spooner, E., and Ploegh, H.L. (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.
34. Katze, M.G., He, Y., and Gale, M. Jr. (2002). Viruses and interferon: a fight for supremacy. Nat. Rev. Immunol. 2, 675-687.
35. Kiel, C. and Serrano, L. (2006). The ubiquitin domain superfold: structure-based sequence alignments and characterization of binding epitopes. J. Mol. Biol. 355, 821-844.
36. Krishna, S.S. and Grishin, N.V. (2004). The finger domain of the human deubiquitinating enzyme HAUSP is a zinc ribbon. Cell Cycle 3, 1046-1049.
37. Krylov, D.M. and Koonin, E.V. (2001). A novel family of predicted retroviral-like aspartyl proteases with a possible key role in eukaryotic cell cycle control. Curr. Biol. 11, R584-R587.
38. Li, M., Brooks, C.L., Kon, N., and Gu, W. (2004). A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol. Cell 13, 879-886.
39. Li, S.J. and Hochstrasser, M. (1999). A new protease required for cell-cycle progression in yeast. Nature 398, 246-251.
40. Li, S.J. and Hochstrasser, M. (2000). The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell. Biol. 20, 2367-2377.
41. Lindner, H.A., Fotouhi-Ardakani, N., Lytvyn, V., Lachance, P., Sulea, T., and Menard, R. (2005). The papain-like protease from the severe acute respiratory syndrome coronavirus is a deubiquitinating enzyme. J. Virol. 79, 15199-15208.
42. Makarova, K.S., Aravind, L., and Koonin, E.V. (2000). A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem. Sci. 25, 50-52.
43. Mangel, W.F., McGrath, W.J., Toledo, D.L., and Anderson, C.W. (1993). Viral DNA and a viral peptide can act as cofactors of adenovirus virion proteinase activity. Nature 361, 274-275.
44. McGrath, W.J., Baniecki, M.L., Li, C., McWhirter, S.M., Brown, M.T., Toledo, D.L., and Mangel, W.F. (2001). Human adenovirus proteinase: DNA binding and stimulation of proteinase activity by DNA. Biochemistry 40, 13237-13245.
45. McGrath, W.J., Ding, J., Didwania, A., Sweet, R.M., and Mangel, W.F. (2003). Crystallographic structure at 1.6-Å resolution of the human adenovirus proteinase in a covalent complex with its 11-amino-acid peptide cofactor: insights on a new fold. Biochim. Biophys. Acta 1648, 1-11.
46. Mossessova, E. and Lima, C.D. (2000). Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5, 865-876.
47. Narasimhan, J., Wang, M., Fu, Z., Klein, J.M., Haas, A.L., and Kim, J.J. (2005). Crystal structure of the interferon-induced ubiquitin-like protein ISG15. J. Biol. Chem. 280, 27356-27365.
48. Nanao, M.H., Tcherniuk, S.O., Chroboczek, J., Dideberg, O., Dessen, A., and Balakirev, M.Y. (2004). Crystal structure of human otubain 2. EMBO Rep. 5, 783-788.
49. Nicastro, G., Menon, R.P., Masino, L., Knowles, P.P., McDonald, N.Q., and Pastore, A. (2005). The solution structure of the Josephin domain of ataxin-3: structural determinants for molecular recognition. Proc. Natl. Acad. Sci. USA 102, 10493-10498.
50. Nijman, S.M.B., Luna-Vargas, M.P.A., Velds, A., Brummelkamp, T.R., Dirac, A.M.G., Sixma, T.K., and Bernards, R. (2005). A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786.
51. Palacios, S., Perez, L.H., Welsch, S., Schleich, S., Chmielarska, K., Melchior, F., and Locker, J.K. (2005). Quantitative SUMO-1 modification of a vaccinia virus protein is required for its specific localization and prevents its self-association. Mol. Biol. Cell 16, 2822-2835.
52. Passmore, L.A. and Barford, D. (2004). Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochem. J. 379, 513-525.
53. Rawlings, N.D., Tolle, D.P., and Barrett, A.J. (2004). MEROPS: the peptidase database. Nucleic Acids Res. 32, D160-D164.
54. Reverter, D. and Lima, C.D. (2004). A basis for SUMO protease specificity provided by analysis of human Senp2 and a Senp2-SUMO complex. Structure 12, 1519-1531.
55. Reverter, D., Wu, K., Erdene, T.G., Pan, Z.Q., Wilkinson, K.D., and Lima, C.D. (2005). Structure of a complex between Nedd8 and the Ulp/Senp protease family member Den1. J. Mol. Biol. 345, 141-151.
56. Rubio, D., Alejo, A., Rodriguez, I., and Salas, M.L. (2003). Polyprotein processing protease of African swine fever virus: purification and biochemical characterization. J. Virol. 77, 4444-4448.
57. Saridakis, V., Sheng, Y., Sarkari, F., Holowaty, M.N., Shire, K., Nguyen, T., Zhang, R.G., Liao, J., Lee, W., and Edwards, A.M. (2005). Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein-Barr nuclear antigen 1: implications for EBV-mediated immortalization. Mol. Cell 18, 25-36.
58. Schlieker, C., Korbel, G.A., Kattenhorn, L.M., and Ploegh, H.L. (2005). A deubiquitinating activity is conserved in the large tegument protein of the herpesviridae. J. Virol. 79, 15582-15585.
59. Shackelford, J. and Pagano, J.S. (2005). Targeting of host-cell ubiquitin pathways by viruses. Essays Biochem. 41, 139-156.
60. Sheng, Y., Saridakis, V., Sarkari, F., Duan, S., Wu, T., Arrowsmith, C.H., and Frappier, L. (2006). Molecular recognition of p53 and MDM2 by USP7/HAUSR Nat. Struct. Mol. Biol. 13, 285-291.
61. Sircar, S., Ruzindana-Umunyana, A., Neugebauer, W., and Weber, J.M. (1998). Adenovirus endopeptidase and papain are inhibited by the same agents. Antiviral Res. 40, 45-51.
62. Snijder, E.J., Bredenbeek, P.J., Dobbe, J.C., Thiel, V., Ziebuhr, J., Poon, L.L.M., Guan, Y., Rozanov, M., Spaan, W.J.M., and Gorbalenya, A.E. (2003). Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 331, 991-1004.
63. Sou, Y.s., Tanida, I., Komatsu, M., Ueno, T., and Kominami, E. (2005). Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP and GATE-16. J. Biol. Chem. 281, 3017-3024.
64. Stephens, R.S., Kalman, S., Lammel, C., Fan, J., Marathe, R., Aravind, L., Mitchell, W., Olinger, L., Tatusov, R.L., Zhao, Q., et al. (1998). Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282, 754-759.
65. Strunnikov, A.V., Aravind, L., and Koonin, E.V. (2001). Saccharomyces cerevisiae SMT4 encodes an evolutionary conserved protease with a role in chromosome condensation regulation. Genetics 158, 95-107.
66. Sugawara, K., Suzuki, N.N., Fujioka, Y., Mizushima, N., Ohsumi, Y., and Inagaki, F. (2005). Structural basis for the specificity and catalysis of human Atg4B responsible for mammalian autophagy. J. Biol. Chem. 280, 40058-40065.
67. Sulea, T., Lindner, H.A., Purisima, E.O., and Menard, R. (2005). Deubiquitination, a new function of the severe acute respiratory syndrome coronavirus papain-like protease? J. Virol. 79, 4550-4551.
68. Sulea, T., Lindner, H.A., Purisima, E.O., and Menard, R. (2006). Binding site-based classification of coronaviral papain-like proteases. Proteins 62, 760-775.
69. Thiel, V., Ivanov, K.A., Putics, A., Hertzig, T., Schelle, B., Bayer, S., Weissbrich, B., Snijder, E.J., Rabenau, H., Doerr, H.W., et al. (2003). Mechanisms and enzymes involved in SARS coronavirus genome expression. J. Gen. Virol. 84, 2305-2315.
70. Weber, J. (1976). Genetic analysis of adenovirus type 2 III. Temperature sensitivity of processing viral proteins. J. Virol. 17, 462-471.
71. Weber, J.M. (1995). Adenovirus endopeptidase and its role in virus infection. Curr. Top. Microbiol. Immunol. 199, 227-235.
72. Webster, A., Russell, S., Talbot, P., Russell, W.C., and Kemp, G.D. (1989). Characterization of the adenovirus proteinase: substrate specificity. J. Gen. Virol. 70, 3225-3234.
73. Webster, A., Hay, R.T., and Kemp, G. (1993). The adenovirus protease is activated by a virus-coded disulphide-linked peptide. Cell 72, 97-104.
74. Welchman, R.L., Gordon, C., and Mayer, R.J. (2005). Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol. 6, 599-609.
75. Zhao, C., Denison, C., Huibregtse, J.M., Gygi, S., and Krug, R.M. (2005). Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc. Natl. Acad. Sci. USA 102, 10200-10205.
76. Zhu, M., Shao, F., Innes, R.W., Dixon, J.E., and Xu, Z. (2004). The crystal structure of Pseudomonas avirulence protein AvrPphB: a papain-like fold with a distinct substrate-binding site. Proc. Natl. Acad. Sci. USA 101, 302-307.
77. Ziebuhr, J. (2005). The coronavirus replicase. Curr. Top. Microbiol. Immunol. 287, 57-94.