1.2Å-resolution crystal structures reveal the second tetrahedral intermediates of streptogrisin B (SGPB)

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1784, Issue 2, 2008, Pages 319-334

  Lee, Ting Wai ^a   James, Michael N G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Catalytic intermediates; Serine peptidase mechanism; Streptogrisin B; X ray crystallography

Indexed keywords

BACTERIAL ENZYME; OVOMUCOID; PEPTIDASE; STREPTOGRISIN B; TETRAPEPTIDE; UNCLASSIFIED DRUG; SERINE PROTEINASE;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ANALYSIS; BACTERIAL GENOME; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; HYDROGEN BOND; METABOLISM; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STREPTOMYCES GRISEUS; X RAY CRYSTALLOGRAPHY;

BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; ELECTRONS; GENOME, BACTERIAL; HYDROGEN BONDING; MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SERINE ENDOPEPTIDASES; STREPTOMYCES GRISEUS; SUBSTRATE SPECIFICITY;

EID: 38549157529     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2007.11.012     Document Type: Article

References (74)

1. Qasim M.A. Streptogrisin B. In: Barrett A.J., Rawlings N.D., and Woessner J.F. (Eds). Handbook of Proteolytic Enzymes (2004), Elsevier, London 1458-1462
2. Jurášek J., Johnson P., Olafson R.W., and Smillie L.B. An improved fractionation system for Pronase on CM-sephadex. Can. J. Biochem. 49 (1971) 1195-1201
3. Henderson G., Krygsman P., Liu C.J., Davey C.C., and Malek L.T. Characterization and structure of genes for proteases A and B from Streptomyces griseus. J. Bacteriol. 169 (1987) 3778-3784
4. Tomono A., Tsai Y., Ohnishi Y., and Horinouchi S. Three chymotrypsin genes are members of the AdpA regulon in the A-factor regulatory cascade in Streptomyces griseus. J. Bacteriol. 187 (2005) 6341-6353
5. Jurášek L., Carpenter M.R., Smillie L.B., Gertler A., Levy S., and Ericsson L.H. Amino acid sequence of Streptomyces griseus protease B, a major component of Pronase. Biochem. Biophys. Res. Commun. 61 (1974) 1095-1100
6. Codding P.W., Delbaere L.T., Hayakawa K., Hutcheon W.L., James M.N.G., and Jurášek L. The 4.5 Å resolution structure of a bacterial serine protease from Streptomyces griseus. Can. J. Biochem. 52 (1974) 208-220
7. Delbaere L.T., Hutcheon W.L., James M.N.G., and Thiessen W.E. Tertiary structural differences between microbial serine proteases and pancreatic serine enzymes. Nature 257 (1975) 758-763
8. Delbaere L.T., Brayer G.D., and James M.N.G. The 2.8 Å resolution structure of Streptomyces griseus protease B and its homology with alpha-chymotrypsin and Streptomyces griseus protease A. Can. J. Biochem. 57 (1979) 135-144
9. Shotton D.M., and Watson H.C. Three-dimensional structure of tosyl-elastase. Nature 225 (1970) 811-816
10. Birktoft J.J., and Blow D.M. Structure of crystalline alpha-chymotrypsin: V. The atomic structure of tosyl-alpha-chymotrypsin at 2 Å resolution. J. Mol. Biol. 68 (1972) 187-240
11. Stroud R.M., Kay L.M., and Dickerson R.E. The structure of bovine trypsin: electron density maps of the inhibited enzyme at 5 Å and at 2.7 Å resolution. J. Mol. Biol. 83 (1974) 185-208
12. James M.N.G., Delbaere L.T., and Brayer G.D. Amino acid sequence alignment of bacterial and mammalian pancreatic serine proteases based on topological equivalences. Can. J. Biochem. 56 (1978) 396-402
13. Gertler A. Inhibition of Streptomyces griseus protease B by peptide chloromethyl ketones: partial mapping of the binding site and identification of the reactive residue. FEBS Lett. 43 (1974) 81-85
14. Schechter I., and Berger A. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27 (1967) 157-162
15. Bauer C.A. Active centers of Streptomyces griseus protease 1, Streptomyces griseus protease 3, and alpha-chymotrypsin: enzyme-substrate interactions. Biochemistry 17 (1978) 375-380
16. Sidhu S.S., and Borgford T.J. Selection of Streptomyces griseus protease B mutants with desired alterations in primary specificity using a library screening strategy. J. Mol. Biol. 257 (1996) 233-245
17. Elliott R.J., Bennet A.J., Braun C.A., MacLeod A.M., and Borgford T.J. Active-site variants of Streptomyces griseus protease B with peptide-ligation activity. Chem. Biol. 7 (2000) 163-171
18. Qasim M.A., Ranjbar M.R., Wynn R., Anderson S., and Laskowski Jr. M. Ionizable P1 residues in serine proteinase inhibitors undergo large pK shifts on complex formation. J. Biol. Chem. 270 (1995) 27419-27422
19. Ardelt W., and Laskowski Jr. M. Effect of single amino acid replacements on the thermodynamics of the reactive site peptide bond hydrolysis in ovomucoid third domain. J. Mol. Biol. 220 (1991) 1041-1053
20. Truhlar S.M., Cunningham E.L., and Agard D.A. The folding landscape of Streptomyces griseus protease B reveals the energetic costs and benefits associated with evolving kinetic stability. Protein Sci. 13 (2004) 381-390
21. Baardsnes J., Sidhu S., MacLeod A., Elliott J., Morden D., Watson J., and Borgford T. Streptomyces griseus protease B: secretion correlates with the length of the propeptide. J. Bacteriol. 180 (1998) 3241-3244
22. Fujinaga M., Read R.J., Sielecki A., Ardelt W., Laskowski Jr. M., and James M.N.G. Refined crystal structure of the molecular complex of Streptomyces griseus protease B, a serine protease, with the third domain of the ovomucoid inhibitor from turkey. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 4868-4872
23. Read R.J., Fujinaga M., Sielecki A.R., and James M.N.G. Structure of the complex of Streptomyces griseus protease B and the third domain of the turkey ovomucoid inhibitor at 1.8-Å resolution. Biochemistry 22 (1983) 4420-4433
24. Bode W., Wei A.Z., Huber R., Meyer E., Travis J., and Neumann S. X-ray crystal structure of the complex of human leukocyte elastase (PMN elastase) and the third domain of the turkey ovomucoid inhibitor. EMBO J. 5 (1986) 2453-2458
25. Fujinaga M., Sielecki A.R., Read R.J., Ardelt W., Laskowski Jr. M., and James M.N.G. Crystal and molecular structures of the complex of alpha-chymotrypsin with its inhibitor turkey ovomucoid third domain at 1.8 Å resolution. J. Mol. Biol. 195 (1987) 397-418
26. Huang K., Lu W., Anderson S., Laskowski Jr. M., and James M.N.G. Water molecules participate in proteinase-inhibitor interactions: crystal structures of Leu18, Ala18, and Gly18 variants of turkey ovomucoid inhibitor third domain complexed with Streptomyces griseus proteinase B. Protein Sci. 4 (1995) 1985-1997
27. Bateman K.S., Anderson S., Lu W., Qasim M.A., Laskowski Jr. M., and James M.N.G. Deleterious effects of beta-branched residues in the S1 specificity pocket of Streptomyces griseus proteinase B (SGPB): crystal structures of the turkey ovomucoid third domain variants Ile18I, Val18I, Thr18I, and Ser18I in complex with SGPB. Protein Sci. 9 (2000) 83-94
28. Bateman K.S., Huang K., Anderson S., Lu W., Qasim M.A., Laskowski Jr. M., and James M.N.G. Contribution of peptide bonds to inhibitor-protease binding: crystal structures of the turkey ovomucoid third domain backbone variants OMTKY3-Pro18I and OMTKY3-psi[COO]-Leu18I in complex with Streptomyces griseus proteinase B (SGPB) and the structure of the free inhibitor, OMTKY-3-psi[CH2NH2+]-Asp19I. J. Mol. Biol. 305 (2001) 839-849
29. Maynes J.T., Cherney M.M., Qasim M.A., Laskowski Jr. M., and James M.N.G. Structure of the subtilisin Carlsberg-OMTKY3 complex reveals two different ovomucoid conformations. Acta Cryst. D61 (2005) 580-588
30. Lee T.-W., Qasim M.A., Laskowski Jr. M., and James M.N.G. Structural insights into the non-additivity effects in the sequence-to-reactivity algorithm for serine peptidases and their inhibitors. J. Mol. Biol. 367 (2007) 527-546
31. K. Huang, Structural studies of the interactions between serine proteinases and protein inhibitors, PhD thesis, University of Alberta, 1995.
32. K.S. Bateman, Structural studies of protein-protein interactions, PhD thesis, University of Alberta, 1999.
33. Bigler T.L., Lu W., Park S.J., Tashiro M., Wieczorek M., Wynn R., and Laskowski Jr. M. Binding of amino acid side chains to preformed cavities: interaction of serine proteinases with turkey ovomucoid third domains with coded and noncoded P1 residues. Protein Sci. 2 (1993) 786-799
34. Lu W., Apostol I., Qasim M.A., Warne N., Wynn R., Zhang W.L., Anderson S., Chiang Y.W., Ogin E., Rothberg I., Ryan K., and Laskowski Jr. M. Binding of amino acid side-chains to S1 cavities of serine proteinases. J. Mol. Biol. 266 (1997) 441-461
35. Lu S.M., Lu W., Qasim M.A., Anderson S., Apostol I., Ardelt W., Bigler T., Chiang Y.W., Cook J., James M.N.G., Kato I., Kelly C., Kohr W., Komiyama T., Lin T.Y., Ogawa M., Otlewski J., Park S.J., Qasim S., Ranjbar M., Tashiro M., Warne N., Whatley H., Wieczorek A., Wieczorek M., Wilusz T., Wynn R., Zhang W., and Laskowski Jr. M. Predicting the reactivity of proteins from their sequence alone: Kazal family of protein inhibitors of serine proteinases. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 1410-1415
36. Laskowski Jr. M., Qasim M.A., and Yi Z. Additivity-based prediction of equilibrium constants for some protein-protein associations. Curr. Opin. Struct. Biol. 13 (2003) 130-139
37. Fujinaga M., Huang K., Bateman K.S., and James M.N. Computational analysis of the binding of P1 variants of domain 3 of turkey ovomucoid inhibitor to Streptomyces griseus protease B. J. Mol. Biol. 284 (1998) 1683-1694
38. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. In: Carter Jr. C.W., and Sweet R.M. (Eds). Methods in Enzymology (1997), Academic Press, New York, NY 307-326
39. N. Collaborative Computational Project. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50 (1994) 760-763
40. Potterton E., Briggs P., Turkenburg M., and Dodson E. A graphical user interface to the CCP4 program suite. Acta Crystallogr. D59 (2003) 1131-1137
41. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025
42. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53 (1997) 240-255
43. McRee D.E. XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
44. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
45. Evans P., and Fermi J. GEOMCALC, Computer Program (1995), Medical Research Council Laboratory of Molecular Biology, Cambridge
46. Satow Y., Cohen G.H., Padlan E.A., and Davies D.R. Phosphocholine binding immunoglobulin Fab McPC603. An X-ray diffraction study at 2.7 Å. J. Mol. Biol. 190 (1986) 593-604
47. Cohen G.H. ALIGN: a program to superimpose protein coordinates, accounting for insertions and deletions. J. Appl. Crystallogr. 30 (1997) 1160-1161
48. Cruickshank D.W.J. Remarks about protein structure precision. Acta Crystallogr. D55 (1999) 583-601
49. Stroud R.M., Kossiakoff A.A., and Chambers J.L. Mechanisms of zymogen activation. Annu. Rev. Biophys. Bioeng. 6 (1977) 177-193
50. Greenblatt H.M., Ryan C.A., and James M.N.G. Structure of the complex of Streptomyces griseus proteinase B and polypeptide chymotrypsin inhibitor-1 from Russet Burbank potato tubers at 2.1 Å resolution. J. Mol. Biol. 205 (1989) 201-228
51. Yennawar N.H., Yennawar H.P., and Farber G.K. X-ray crystal structure of gamma-chymotrypsin in hexane. Biochemistry 33 (1994) 7326-7336
52. Rypniewski W.R., Østergaard P.R., Nørregaard-Madsen M., Dauter M., and Wilson K.S. Fusarium oxysporum trypsin at atomic resolution at 100 and 283 K: a study of ligand binding. Acta Crystallogr. D57 (2001) 8-19
53. Dixon M.M., and Matthews B.W. Is gamma-chymotrypsin a tetrapeptide acyl-enzyme adduct of alpha-chymotrypsin?. Biochemistry 28 (1989) 7033-7038
54. Dixon M.M., Brennan R.G., and Matthews B.W. Structure of gamma-chymotrypsin in the range pH 2.0 to pH 10.5 suggests that gamma-chymotrypsin is a covalent acyl-enzyme adduct at low pH. Int. J. Biol. Macromol. 13 (1991) 89-96
55. Blanchard H., and James M.N.G. A crystallographic re-investigation into the structure of Streptomyces griseus proteinase A reveals an acyl-enzyme intermediate. J. Mol. Biol. 241 (1994) 574-587
56. Singh N., Jabeen T., Sharma S., Roy I., Gupta M.N., Bilgrami S., Somvanshi R.K., Dey S., Perbandt M., Betzel C., Srinivasan A., and Singh T.P. Detection of native peptides as potent inhibitors of enzymes. Crystal structure of the complex formed between treated bovine alpha-chymotrypsin and an autocatalytically produced fragment, IIe-Val-Asn-Gly-Glu-Glu-Ala-Val-Pro-Gly-Ser-Trp-Pro-Trp, at 2.2 Å resolution. FEBS J. 272 (2005) 562-572
57. Harel M., Su C.T., Frolow F., Silman I., and Sussman J.L. Gamma-chymotrypsin is a complex of alpha-chymotrypsin with its own autolysis products. Biochemistry 30 (1991) 5217-5225
58. Schmidt A., Jelsch C., Ostergaard P., Rypniewski W., and Lamzin V.S. Trypsin revisited: crystallography at (sub) atomic resolution and quantum chemistry revealing details of catalysis. J. Biol. Chem. 278 (2003) 43357-43362
59. James M.N.G., Brayer G.D., Delbaere L.T., Sielecki A.R., and Gertler A. Crystal structure studies and inhibition kinetics of tripeptide chloromethyl ketone inhibitors with Streptomyces griseus protease B. J. Mol. Biol. 139 (1980) 423-438
60. Laskowski Jr. M., and Qasim M.A. What can the structures of enzyme-inhibitor complexes tell us about the structures of enzyme substrate complexes?. Biochim. Biophys. Acta 1477 (2000) 324-337
61. Laskowski M.J., Qasim M.A., and Lu S.M. Interaction of standard mechanism, canonical protein inhibitors with serine proteinases. In: Kleanthous C. (Ed). Protein-Protein Recognition (2000), Oxford University Press, New York 228-279
62. Fuhrmann C.N., Kelch B.A., Ota N., and Agard D.A. The 0.83 Å resolution crystal structure of alpha-lytic protease reveals the detailed structure of the active site and identifies a source of conformational strain. J. Mol. Biol. 338 (2004) 999-1013
63. Fuhrmann C.N., Daugherty M.D., and Agard D.A. Subangstrom crystallography reveals that short ionic hydrogen bonds, and not a His-Asp low-barrier hydrogen bond, stabilize the transition state in serine protease catalysis. J. Am. Chem. Soc. 128 (2006) 9086-9102
64. Radisky E.S., and Koshland Jr. D.E. A clogged gutter mechanism for protease inhibitors. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 10316-10321
65. Radisky E.S., Lee J.M., Lu C.J., and Koshland Jr. D.E. Insights into the serine protease mechanism from atomic resolution structures of trypsin reaction intermediates. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 6835-6840
66. 1H NMR chemical shifts support (His) C(epsilon)1...O{double bond, short}{double bond, short}C H-bond: proposal for reaction-driven ring flip mechanism in serine protease catalysis. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 10371-10376
67. Wilmouth R.C., Edman K., Neutze R., Wright P.A., Clifton I.J., Schneider T.R., Schofield C.J., and Hajdu J. X-ray snapshots of serine protease catalysis reveal a tetrahedral intermediate. Nat. Struct. Biol. 8 (2001) 689-694
68. Liu B., Schofield C.J., and Wilmouth R.C. Structural analyses on intermediates in serine protease catalysis. J. Biol. Chem. 281 (2006) 24024-24035
69. Frey P.A., Whitt S.A., and Tobin J.B. A low-barrier hydrogen bond in the catalytic triad of serine proteases. Science 264 (1994) 1927-1930
70. Krem M.M., and Di Cera E. Molecular markers of serine protease evolution. EMBO J. 20 (2001) 3036-3045
71. Derewenda Z.S., Derewenda U., and Kobos P.M. (His) C(epsilon)-H...O{double bond, short}C < hydrogen bond in the active sites of serine hydrolases. J. Mol. Biol. 241 (1994) 83-93
72. Hedstrom L. Serine protease mechanism and specificity. Chem. Rev. 102 (2002) 4501-4523
73. Schmidt A., and Lamzin V.S. Veni, vidi, vici-Atomic resolution unravelling the mysteries of protein function. Curr. Opin. Struct. Biol. 12 (2002) 698-703
74. Brünger A.T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355 (1992) 472-475