Increase of SARS-CoV 3CL peptidase activity due to macromolecular crowding effects in the milieu composition

Biological Chemistry

Volumn 391, Issue 12, 2010, Pages 1461-1468

  Okamoto, Debora N ^a   Oliveira, Lilian C G ^a   Kondo, Marcia Y ^a   Cezari, Maria H S ^a   Szeltner, Zoltán ^b   Juhász, Tünde ^b   Juliano, Maria A ^a   Polgár, László ^b   Juliano, Luiz ^a   Gouvea, Iuri E ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Coronavirus; Hofmeister series; Kosmotropic salt; Macromolecular crowding; Molecular crowding; Protease

Indexed keywords

3C LIKE PEPTIDASE; ACETIC ACID; ANION; BOVINE SERUM ALBUMIN; CITRATE SODIUM; DIMER; KOSMOTROPIC SALT; MACROGOL; MONOMER; PEPTIDASE; SODIUM CHLORIDE; SODIUM DIHYDROGEN PHOSPHATE; SODIUM SULFATE; UNCLASSIFIED DRUG; VIRUS ENZYME; 3C LIKE PROTEASE, SARS CORONAVIRUS; 3C-LIKE PROTEASE, SARS CORONAVIRUS; CYSTEINE PROTEINASE; VIRUS PROTEIN;

ARTICLE; DISSOCIATION CONSTANT; ENZYME ACTIVATION; ENZYME ACTIVITY; HOST CELL; MACROMOLECULE; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; RNA VIRUS INFECTION; SARS CORONAVIRUS; VIRUS REPLICATION; CHEMISTRY; ENZYMOLOGY; HYDROLYSIS; KINETICS; METABOLISM;

BOVINAE; CORONAVIRUS; PICORNAVIRIDAE; RNA VIRUSES; SARS CORONAVIRUS;

CYSTEINE ENDOPEPTIDASES; HYDROLYSIS; KINETICS; SARS VIRUS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 79952551619     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2010.145     Document Type: Article

References (36)

1. Anand, K., Ziebuhr, J., Wadhwani, P., Mesters, J.R., and Hilgenfeld, R. (2003). Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science 300, 1763-1767. (Pubitemid 36712575)
2. Andrade, D., Assis, D.M., Lima, A.R., Oliveira, J.R., Araujo, M.S., Blaber, S.I., Blaber, M., Juliano, M.A., and Juliano, L. (2010). Substrate specificity and inhibition of human kallikrein-related peptidase 3 (KLK3 or PSA) activated with sodium citrate and glycosaminoglycans. Arch. Biochem. Biophys. 498, 74-82.
3. Araujo, M.C., Melo, R.L., Cesari, M.H., Juliano, M.A., Juliano, L., and Carmona, A.K. (2000). Peptidase specificity characterization of C- and N-terminal catalytic sites of angiotensin I-converting enzyme. Biochemistry 39, 8519-8525. (Pubitemid 30489949)
4. Barrila, J., Gabelli, S.B., Bacha, U., Amzel, L.M., and Freire, E. (2010). Mutation of Asn28 disrupts the dimerization and enzymatic activity of SARS 3CL(pro). Biochemistry 49, 4308-4317.
5. Chen, H., Wei, P., Huang, C., Tan, L., Liu, Y., and Lai, L. (2006). Only one protomer is active in the dimer of SARS 3C-like proteinase. J. Biol. Chem. 281, 13894-13898. (Pubitemid 43848313)
6. Dietrich, C.P., Tersariol, I.L., Toma, L., Moraes, C.T., Porcionatto, M.A., Oliveira, F.W., and Nader, H.B. (1998). Structure of heparan sulfate: identification of variable and constant oligosaccharide domains in eight heparan sulfates of different origins. Cell. Mol. Biol. (Noisy-le-grand) 44, 417-429.
7. Drosten, C., Gunther, S., Preiser, W., van der Werf, S., Brodt, H.R., Becker, S., Rabenau, H., Panning, M., Kolesnikova, L., Fouchier, R.A.M., et al. (2003). Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348, 1967-1976. (Pubitemid 36569985)
8. Ellis, R.J. (2001). Macromolecular crowding: obvious but underappreciated. Trends Biochem. Sci. 26, 597-604. (Pubitemid 32925190)
9. Fan, K., Wei, P., Feng, Q., Chen, S., Huang, C., Ma, L., Lai, B., Pei, J., Liu, Y., Chen, J., et al. (2004). Biosynthesis, purification, and substrate specificity of severe acute respiratory syndrome coronavirus 3C-like proteinase. J. Biol. Chem. 279, 1637-1642. (Pubitemid 38084429)
10. Fan, K., Ma, L., Han, X., Liang, H., Wei, P., Liu, Y., and Lai, L. (2005). The substrate specificity of SARS coronavirus 3C-like proteinase. Biochem. Biophys. Res. Commun. 329, 934-940. (Pubitemid 40341367)
11. Fulton, A.B. (1982). How crowded is the cytoplasm? Cell 30, 345-347.
12. Gao, F., Ou, H.Y., Chen, L.L., Zheng, W.X., and Zhang, C.T. (2003). Prediction of proteinase cleavage sites in polyproteins of coronaviruses and its applications in analyzing SARS-CoV genomes. FEBS Lett. 553, 451-456. (Pubitemid 37315648)
13. Goetz, D.H., Choe, Y., Hansell, E., Chen, Y.T., McDowell, M., Jonsson, C.B., Roush, W.R., McKerrow, J., and Craik, C.S. (2007). Substrate specificity profiling and identification of a new class of inhibitor for the major protease of the SARS coronavirus. Biochemistry 46, 8744-8752. (Pubitemid 47204440)
14. Gouvea, I.E., Judice, W.A.S., Cezari, M.H.S., Juliano, M.A., Juhasz, T., Szeltner, Z., Polgar, L., and Juliano, L. (2006). Kosmotropic salt activation and substrate specificity of poliovirus protease 3C. Biochemistry 45, 12083-12089. (Pubitemid 44497834)
15. Graziano, V., McGrath, W.J., DeGruccio, A.M., Dunn, J.J., and Mangel, W.F. (2006a). Enzymatic activity of the SARS coronavirus main proteinase dimer. FEBS Lett. 580, 2577-2583.
16. Graziano, V., McGrath, W.J., Yang, L., and Mangel, W.F. (2006b). SARS CoV main proteinase: the monomer-dimer equilibrium dissociation constant. Biochemistry 45, 14632-14641. (Pubitemid 44906979)
17. Hall, D.L. and Darke, P.L. (1995). Activation of the herpes-simplex virus type-1 protease. J. Biol. Chem. 270, 22697-22700.
18. Hsu, N.Y., Ilnytska, O., Belov, G., Santiana, M., Chen, Y.H., Takvorian, P.M., Pau, C., van der Schaar, H., Kaushik-Basu, N., Balla, T., et al. (2010). Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141, 799-811.
19. Huang, X.Y., Knoell, C.T., Frey, G., Hazegh-Azam, M., Tashijian, A.H., Hedstrom, L., Abeles, R.H., and Timasheff, S.N. (2001). Modulation of recombinant human prostate-specific antigen: activation by Hofmeister salts and inhibition by azapeptides. Biochemistry 40, 11734-11741. (Pubitemid 32906035)
20. Huang, C., Wei, P., Fan, K., Liu, Y., and Lai, L. (2004). 3C-like proteinase from SARS coronavirus catalyzes substrate hydrolysis by a general base mechanism. Biochemistry 43, 4568-4574. (Pubitemid 38500585)
21. Korkmaz, B., Attucci, S., Juliano, M.A., Kalupov, T., Jourdan, M.L., Juliano, L., and Gauthier, F. (2008). Measuring elastase, proteinase 3 and cathepsin G activities at the surface of human neutro phils with fluorescence resonance energy transfer substrates. Nat. Protoc. 3, 991-1000. (Pubitemid 351818687)
22. Lai, M.M.C. and Cavanagh, D. (1997). The molecular biology of coronaviruses. Adv. Virus Res. 48, 1-100.
23. Margosiak, S.A., Vanderpool, D.L., Sisson, W., Pinko, C., and Kan, C.C. (1996). Dimerization of the human cytomegalovirus protease: kinetic and biochemical characterization of the catalytic homodimer. Biochemistry 35, 5300-5307. (Pubitemid 26129471)
24. Marra, M.A., Jones, S.J., Astell, C.R., Holt, R.A., Brooks-Wilson, A., Butterfield, Y.S., Khattra, J., Asano, J.K., Barber, S.A., Chan, S.Y., et al. (2003). The genome sequence of the SARS-associated coronavirus. Science 300, 1399-1404. (Pubitemid 36638153)
25. Miller, S. and Krijnse-Locker, J. (2008). Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6, 363-374. (Pubitemid 351552657)
26. Minh, D.D., Chang, C.E., Trylska, J., Tozzini, V., and McCammon, J.A. (2006). The influence of macromolecular crowding on HIV-1 protease internal dynamics. J. Am. Chem. Soc. 128, 6006-6007.
27. Okamoto, D.N., Kondo, M.Y., Hiraga, K., Juliano, M.A., Juliano, L., Gouvea, I.E., and Oda, K. (2010). Salt effect on substrate specificity of a subtilisin-like halophilic protease. Protein Pept. Lett. 17, 796-802.
28. Pop, C., Fitzgerald, P., Green, D.R., and Salvesen, G.S. (2007). Role of proteolysis in caspase-8 activation and stabilization. Biochemistry 46, 4398-4407. (Pubitemid 46559405)
29. Sarkany, Z., Szeltner, Z., and Polgar, L. (2001). Thiolate-imidazolium ion pair is not an obligatory catalytic entity of cysteine peptidases: the active site of picornain 3C. Biochemistry 40, 10601-10606. (Pubitemid 32816671)
30. Schechter, I. and Berger, A. (1967). On size of active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
31. Shimizu, S., McLaren, W.M., and Matubayasi, N. (2006). The Hofmeister series and protein-salt interactions. J. Chem. Phys. 124, 234905.
32. Snijder, E.J., van der Meer, Y., Zevenhoven-Dobbe, J., Onderwater, J.J., van der Meulen, J., Koerten, H.K., and Mommaas, A.M. (2006). Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J. Virol. 80, 5927-5940. (Pubitemid 43849170)
33. Sun, H., Luo, H., Yu, C., Sun, T., Chen, J., Peng, S., Qin, J., Shen, J., Yang, Y., Xie, Y., et al. (2003). Molecular cloning, expression, purification, and mass spectrometric characterization of 3C-like protease of SARS coronavirus. Protein Expr. Purif. 32, 302-308. (Pubitemid 38039023)
34. Totani, K., Ihara, Y., Matsuo, I., and Ito, Y. (2008). Effects of macromolecular crowding on glycoprotein processing enzymes. J. Am. Chem. Soc. 130, 2101-2107. (Pubitemid 351238661)
35. Wang, Q.M. and Johnson, R.B. (2001). Activation of human rhinovirus-14 3C protease. Virology 280, 80-86. (Pubitemid 34158054)
36. Yang, H., Yang, M., Ding, Y., Liu, Y., Lou, Z., Zhou, Z., Sun, L., Mo, L., Ye, S., Pang, H., et al. (2003). The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor. Proc. Natl. Acad. Sci. USA 100, 13190-13195. (Pubitemid 37444717)