Activity, specificity, and probe design for the smallpox virus protease K7L

Journal of Biological Chemistry

Volumn 287, Issue 47, 2012, Pages 39470-39479

  Aleshin, Alexander E ^a   Drag, Marcin ^a   Gombosuren, Naran ^a   Wei, Ge ^a   Mikolajczyk, Jowita ^a   Satterthwait, Arnold C ^a   Strongin, Alex Y ^a   Liddington, Robert C ^a   Salvesen, Guy S ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY-BASED PROBE; BIOCHEMICAL MECHANISMS; CLEAVAGE ACTIVITIES; CYSTEINE PROTEASE; GENE PRODUCTS; HIGH LEVEL EXPRESSION; HOMODIMERIZATION; INFECTED CELLS; LYSATES; PATHOGENIC BACTERIUM; PREFERENCE ANALYSIS; PROBE DESIGN; PROOF OF CONCEPT; PROTEIN SUBSTRATE; SUBSTRATE PROTEINS; SYNTHETIC PEPTIDE; VIRAL PROTEINS;

AMINO ACIDS; DESIGN; ENZYME ACTIVITY; GLYCEROL; PEPTIDES; PROBES; RNA;

VIRUSES;

ALANINE; GLYCEROL; PROTEIN K7L; PROTEIN P25K; PROTEIN P4A; PROTEIN P4B; PROTEINASE; SERINE; THREONINE; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS PROTEIN;

ALLOSTERISM; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CATALYSIS; COVALENT BOND; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; GEL PERMEATION CHROMATOGRAPHY; NONHUMAN; PEPTIDE MAPPING; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN MOTIF; SMALLPOX VIRUS; ULTRACENTRIFUGATION;

AMINO ACID MOTIFS; ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CRICETINAE; DRUG DESIGN; MOLECULAR PROBES; PEPTIDE HYDROLASES; PEPTIDE LIBRARY; PROTEASE INHIBITORS; SMALLPOX; VARIOLA VIRUS; VIRAL PROTEINS;

EUKARYOTA; VARIOLA VIRUS;

EID: 84869210337     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.388678     Document Type: Article

References (47)

1. Buller, R. M., and Palumbo, G. J. (1991) Poxvirus pathogenesis. Microbiol. Rev. 55, 80-122 (Pubitemid 21895147)
2. Moss, B. (2001) Poxviridae. The viruses and their replication. in Fields Virology (Fields, B. N., Knipe, D. M., and Howley, P. M., eds) pp. 2849-2883, 4 Ed., Lippincott-Raven Publishers
3. Katz, E., and Moss, B. (1970) Formation of a vaccinia virus structural polypeptide from a higher molecular weight precursor. Inhibition by rifampicin. Proc. Natl. Acad. Sci. U.S.A. 66, 677-684
4. Kane, E. M., and Shuman, S. (1993) Vaccinia virus morphogenesis is blocked by a temperature-sensitive mutation in the I7 gene that encodes a virion component. J. Virol. 67, 2689-2698 (Pubitemid 23118866)
5. Lee, P., and Hruby, D. E. (1993) Trans-processing of vaccinia virus core proteins. J. Virol. 67, 4252-4263 (Pubitemid 23180752)
6. Whitehead, S. S., and Hruby, D. E. (1994) A transcriptionally controlled trans-processing assay. Putative identification of a vaccinia virus-encoded proteinase, which cleaves precursor protein P25K. J. Virol. 68, 7603-7608 (Pubitemid 24328823)
7. Byrd, C. M., Bolken, T. C., and Hruby, D. E. (2002) The vaccinia virus I7L gene product is the core protein proteinase. J. Virol. 76, 8973-8976 (Pubitemid 34864093)
8. Ansarah-Sobrinho, C., and Moss, B. (2004) Vaccinia virus G1 protein, a predicted metalloprotease, is essential for morphogenesis of infectious virions but not for cleavage of major core proteins. J. Virol. 78, 6855-6863 (Pubitemid 38781523)
9. Harrison, S. C., Alberts, B., Ehrenfeld, E., Enquist, L., Fineberg, H., McKnight, S. L., Moss, B., O'Donnell, M., Ploegh, H., Schmid, S. L., Walter, K. P., and Theriot, J. (2004) Discovery of antivirals against smallpox. Proc. Natl. Acad. Sci. U.S.A. 101, 11178-11192 (Pubitemid 39038322)
10. Byrd, C. M., Bolken, T. C., Mjalli, A. M., Arimilli, M. N., Andrews, R. C., Rothlein, R., Andrea, T., Rao, M., Owens, K. L., and Hruby, D. E. (2004) New class of orthopoxvirus antiviral drugs that block viral maturation. J. Virol. 78, 12147-12156 (Pubitemid 39458734)
11. Katritch, V., Byrd, C. M., Tseitin, V., Dai, D., Raush, E., Totrov, M., Abagyan, R., Jordan, R., and Hruby, D. E. (2007) Discovery of small molecule inhibitors of ubiquitin-like poxvirus proteinase I7L using homology modeling and covalent docking approaches. J. Comput. Aided Mol. Des. 21, 549-558 (Pubitemid 350238547)
12. Byrd, C. M., and Hruby, D. E. (2006) Vaccinia virus proteolysis. A review. Rev. Med. Virol. 16, 187-202
13. Aleshin, A. E., Gramatikova, S., Hura, G. L., Bobkov, A., Strongin, A. Y., Stec, B., Tainer, J. A., Liddington, R. C., and Smith, J. W. (2009) Crystal and solution structures of a prokaryotic M16B peptidase. An open and shut case. Structure 17, 1465-1475
14. Hedengren-Olcott, M., Byrd, C. M., Watson, J., and Hruby, D. E. (2004) The vaccinia virus G1L putative metalloproteinase is essential for viral replication in vivo. J. Virol. 78, 9947-9953 (Pubitemid 39187113)
15. Barrett, A. J., and Rawlings, N. D. (2001) Evolutionary lines of cysteine peptidases. Biol. Chem. 382, 727-733 (Pubitemid 32631709)
16. Ansarah-Sobrinho, C., and Moss, B. (2004) Role of the I7 protein in proteolytic processing of vaccinia virus membrane and core components. J. Virol. 78, 6335-6343 (Pubitemid 38715932)
17. Byrd, C. M., and Hruby, D. E. (2005) Development of an in vitro cleavage assay system to examine vaccinia virus I7L cysteine proteinase activity. Virol. J. 2, 63
18. Byrd, C. M., Bolken, T. C., and Hruby, D. E. (2003) Molecular dissection of the vaccinia virus I7L core protein proteinase. J. Virol. 77, 11279-11283 (Pubitemid 37204318)
19. Yang, S. J., and Hruby, D. E. (2007) Vaccinia virus A12L protein and its AG/A proteolysis play an important role in viral morphogenic transition. Virol. J. 4, 73
20. 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
21. Kerscher, O., Felberbaum, R., and Hochstrasser, M. (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159-180
22. Love, K. R., Catic, A., Schlieker, C., and Ploegh, H. L. (2007) Mechanisms, biology, and inhibitors of deubiquitinating enzymes. Nat. Chem. Biol. 3, 697-705 (Pubitemid 47609116)
23. Quesada, V., Díaz-Perales, A., Gutiérrez-Fernández, A., Garabaya, C., Cal, S., and López-Otín, C. (2004) Cloning and enzymatic analysis of 22 novel human ubiquitin-specific proteases. Biochem. Biophys. Res. Commun. 314, 54-62 (Pubitemid 38058368)
24. Drag, M., and Salvesen, G. S. (2008) DeSUMOylating enzymes. SENPs. IUBMB Life 60, 734-742
25. Catic, A., Misaghi, S., Korbel, G. A., and Ploegh, H. L. (2007) ElaD, a deubiquitinating protease expressed by E. coli. PLoS One 2, e381
26. Orth, K., Xu, Z., Mudgett, M. B., Bao, Z. Q., Palmer, L. E., Bliska, J. B., Mangel, W. F., Staskawicz, B., and Dixon, J. E. (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290, 1594-1597
27. Roden, J., Eardley, L., Hotson, A., Cao, Y., and Mudgett, M. B. (2004) Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells. Mol. Plant Microbe Interact. 17, 633-643 (Pubitemid 38642207)
28. Rytkönen, A., Poh, J., Garmendia, J., Boyle, C., Thompson, A., Liu, M., Freemont, P., Hinton, J. C., and Holden, D. W. (2007) SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl. Acad. Sci. U.S.A. 104, 3502-3507 (Pubitemid 46364188)
29. 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 (Pubitemid 23034481)
30. Andrés, G., Alejo, A., Simón-Mateo, C., and Salas, M. L. (2001) African swine fever virus protease, a new viral member of the SUMO-1-specific protease family. J. Biol. Chem. 276, 780-787 (Pubitemid 32050378)
31. Anderson, C. W. (1990) The proteinase polypeptide of adenovirus serotype 2 virions. Virology 177, 259-272
32. Chen, P. H., Ornelles, D. A., and Shenk, T. (1993) The adenovirus L3 23-kDa proteinase cleaves the amino-terminal head domain from cytokeratin 18 and disrupts the cytokeratin network of HeLa cells. J. Virol. 67, 3507-3514 (Pubitemid 23143728)
33. 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 (Pubitemid 35417623)
34. Balakirev, M. Y., Jaquinod, M., Haas, A. L., and Chroboczek, J. (2002) Deubiquitinating function of adenovirus proteinase. J. Virol. 76, 6323-6331 (Pubitemid 34556327)
35. 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 (Pubitemid 26119213)
36. 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. DNAbinding and stimulation of proteinase activity by DNA. Biochemistry 40, 13237-13245 (Pubitemid 33043538)
37. Isaacs, S. N. (2004) Vaccinia virus and poxvirology. Methods and Protocols, pp. 101-118, Humana Press, Totowa, NJ
38. Golicnik, M. (2011) Evaluation of enzyme kinetic parameters using explicit analytic approximations to the solution of the Michaelis-Menten equation. Biochemical Engineering Journal 53, 234-238
39. Drag, M., Mikolajczyk, J., Bekes, M., Reyes-Turcu, F. E., Ellman, J. A., Wilkinson, K. D., and Salvesen, G. S. (2008) Positional-scanning fluorogenic substrate libraries reveal unexpected specificity determinants of DUBs (deubiquitinating enzymes). Biochem. J. 415, 367-375
40. Drag, M., Mikolajczyk, J., Krishnakumar, I. M., Huang, Z., and Salvesen, G. S. (2008) Activity profiling of human deSUMOylating enzymes (SENPs) with synthetic substrates suggests an unexpected specificity of two newly characterized members of the family. Biochem. J. 409, 461-469 (Pubitemid 351184964)
41. Vedrenne, E., Dupont, H., Oualef, S., Elkaim, L., and Goličnik, M. (2005) Dramatic effect of boron-based Lewis acid in cross-metathesis réactions. Synlett 4, 670-672 (Pubitemid 40395576)
42. Lee, P., and Hruby, D. E. (1995) Analysis of the role of the amino-terminal peptide of vaccinia virus structural protein precursors during proteolytic processing. Virology 207, 229-233
43. Lee, P., and Hruby, D. E. (1994) Proteolytic cleavage of vaccinia virus virion proteins. Mutational analysis of the specificity determinants. J. Biol. Chem. 269, 8616-8622
44. Bayliss, C. D., and Smith, G. L. (1997) Vaccinia virion protein VP8, the 25-kDa product of the L4R gene, binds single-stranded DNA and RNA with similar affinity. Nucleic acids research 25, 3984-3990 (Pubitemid 27443324)
45. Rawlings, N. D., Morton, F. R., Kok, C. Y., Kong, J., and Barrett, A. J. (2008) MEROPS. The peptidase database. Nucleic Acids Res. 36, D320-D325
46. López-Otín, C., Simón-Mateo, C., Martínez, L., and Viñuela, E. (1989) Gly-Gly-X, a novel consensus sequence for the proteolytic processing of viral and cellular proteins. J. Biol. Chem. 264, 9107-9110
47. McGrath, W. J., Abola, A. P., Toledo, D. L., Brown, M. T., and Mangel, W. F. (1996) Characterization of human adenovirus proteinase activity in disrupted virus particles. Virology 217, 131-138 (Pubitemid 26103604)