Study of a major intermediate in the oxidative folding of leech carboxypeptidase inhibitor: Contribution of the fourth disulfide bond

Journal of Molecular Biology

Volumn 352, Issue 4, 2005, Pages 961-975

  Arolas, Joan L ^a   Popowicz, Grzegorz M ^b   Bronsoms, Sílvia ^a   Aviles, Francesc X ^a   Huber, Robert ^b   Holak, Tad A ^b   Ventura, Salvador ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Carboxypeptidase inhibitor; Crystal structures; Folding intermediates; Oxidative folding; Protein stability

Indexed keywords

ALANINE; CARBOXYPEPTIDASE; CARBOXYPEPTIDASE A; CYSTEINE; HYDROLASE INHIBITOR;

ARTICLE; DISULFIDE BOND; DRUG BINDING; DRUG STRUCTURE; ENZYME SPECIFICITY; ENZYME STABILITY; ISOMER; LEECH; MUTATION; OXIDATION; PRIORITY JOURNAL; PROTEIN FOLDING; WILD TYPE; X RAY CRYSTALLOGRAPHY;

HIRUDINIDA;

EID: 24644503006     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.07.065     Document Type: Article

References (52)

1. K.A. Dill, and H.S. Chan From Levinthal to pathways to funnels Nature Struct. Biol. 4 1997 10 19
2. B. Honig Protein folding: from the levinthal paradox to structure prediction J. Mol. Biol. 293 1999 283 293
3. T.E. Creighton, N.J. Darby, and J. Kemmink The roles of partly folded intermediates in protein folding FASEB J. 10 1996 110 118
4. T.E. Creighton Disulfide bonds as probes of protein folding pathways Methods Enzymol. 131 1986 83 106
5. J.S. Weissman, and P.S. Kim Reexamination of the folding of BPTI: predominance of native intermediates Science 253 1991 1386 1393
6. D.P. Goldenberg Native and non-native intermediates in the BPTI folding pathway Trends Biochem. Sci. 17 1992 257 261
7. W.J. Wedemeyer, E. Welker, M. Narayan, and H.A. Scheraga Disulfide bonds and protein folding Biochemistry 39 2000 4207 4216
8. H.A. Scheraga, W.J. Wedemeyer, and E. Welker Bovine pancreatic ribonuclease A: oxidative and conformational folding studies Methods Enzymol. 341 2001 189 221
9. B. van den Berg, E.W. Chung, C.V. Robinson, P.L. Mateo, and C.M. Dobson The oxidative refolding of hen lysozyme and its catalysis by protein disulfide isomerase EMBO J. 18 1999 4794 4803
10. B. van den Berg, E.W. Chung, C.V. Robinson, and C.M. Dobson Characterisation of the dominant oxidative folding intermediate of hen lysozyme J. Mol. Biol. 290 1999 781 796
11. D. Reverter, J. Vendrell, F. Canals, J. Horstmann, F.X. Aviles, H. Fritz, and C.P. Sommerhoff A carboxypeptidase inhibitor from the medical leech Hirudo medicinalis. Isolation, sequence analysis, cDNA cloning, recombinant expression, and characterization J. Biol. Chem. 273 1998 32927 32933
12. W. Wang, M.B. Boffa, L. Bajzar, J.B. Walker, and M.E. Nesheim A study of the mechanism of inhibition of fibrinolysis by activated thrombin-activable fibrinolysis inhibitor J. Biol. Chem. 273 1998 27176 27181
13. B.N. Bouma, and J.C.M. Meijers Thrombin-activatable fibrinolysis inhibitor (TAFI, plasma procarboxypeptidase B, procarboxypeptidase R, procarboxypeptidase U) J. Thromb. Haemost. 1 2003 1566 1574
14. A. Silveira, K. Schatteman, F. Goossens, E. Moor, S. Scharpe, and M. Stromqvist Plasma procarboxypeptidase U in men with symptomatic coronary artery disease Thromb. Haemost. 84 2000 364 368
15. S. Eichinger, V. Schönauer, A. Weltermann, E. Minar, C. Bialonczyk, and M. Hirschi Thrombin-activatable fibrinolysis inhibitor and the risk for recurrent venous thromboembolism Blood 103 2004 3773 3776
16. D. Reverter, C. Fernandez-Catalan, R. Baumgartner, R. Pfander, R. Huber, and W. Bode Structure of a novel leech carboxypeptidase inhibitor determined free in solution and in complex with human carboxypeptidase A2 Nature Struct. Biol. 7 2000 322 328
17. S. Salamanca, V. Villegas, J. Vendrell, L. Li, F.X. Aviles, and J.Y. Chang The unfolding pathway of leech carboxypeptidase inhibitor J. Biol. Chem. 277 2002 17538 17543
18. S. Salamanca, L. Li, J. Vendrell, F.X. Aviles, and J.Y. Chang Major kinetic traps for the oxidative folding of leech carboxypeptidase inhibitor Biochemistry 42 2003 6754 6761
19. J.L. Arolas, S. Bronsoms, J. Lorenzo, F.X. Aviles, J.Y. Chang, and S. Ventura Role of kinetic intermediates in the folding of leech carboxypeptidase inhibitor J. Biol. Chem. 279 2004 37261 37270
20. J.L. Arolas, L. D'Silva, G.M. Popowicz, F.X. Aviles, T.A. Holak, and S. Ventura NMR structural characterization and computational predictions of the major intermediate in the oxidative folding of leech carboxypeptidase inhibitor Structure (Camb) 13 2005 1193 1202
21. J.Y. Chang, L. Li, and P.H. Lai A major kinetic trap for the oxidative folding of human epidermal growth factor J. Biol. Chem. 276 2001 4845 4852
22. J.Y. Chang A two-stage mechanism for the reductive unfolding of disulfide-containing proteins J. Biol. Chem. 272 1997 69 75
23. J.Y. Chang, L. Li, and A. Bulychev The underlying mechanism for the diversity of disulfide folding pathways J. Biol. Chem. 275 2000 8287 8289
24. J.Y. Chang Denatured states of tick anticoagulant peptide. Compositional analysis of unfolded scrambled isomers J. Biol. Chem. 274 1999 123 128
25. G. Xu, M. Narayan, E. Welker, and H.A. Scheraga A novel method to determine thermal transition curves of disulfide-containing proteins and their structured folding intermediates Biochem. Biophys. Res. Commun. 311 2005 514 517
26. A. Matouschek, J.T. Kellis Jr, L. Serrano, M. Bycroft, and A.R. Fersht Transient folding intermediates characterized by protein engineering Nature 346 1990 440 445
27. S. Ventura, M.C. Vega, E. Lacroix, I. Angrand, L. Spagnolo, and L. Serrano Conformational strain in the hydrophobic core and its implications for protein folding and design Nature Struct. Biol. 9 2002 485 493
28. J.K. Myers, C.N. Pace, and J.M. Scholtz Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding Protein Sci. 4 1995 2138 2148
29. B. Chatrenet, and J.Y. Chang The disulfide folding pathway of hirudin elucidated by stop/go folding experiments J. Biol. Chem. 268 1993 20988 20996
30. J.Y. Chang, F. Canals, P. Schindler, E. Querol, and F.X. Aviles The disulfide folding pathway of potato carboxypeptidase inhibitor J. Biol. Chem. 269 1994 22087 22094
31. J.Y. Chang, L. Li, F. Canals, and F.X. Aviles The unfolding pathway and conformational stability of potato carboxypeptidase inhibitor J. Biol. Chem. 275 2000 14205 14211
32. M.R. Hurle, C.D. Eads, D.A. Pearlman, G.L. Seibel, J. Thomason, and P.A. Kosen Comparison of solution structures of mutant bovine pancreatic trypsin inhibitor proteins using two-dimensional nuclear magnetic resonance Protein Sci. 1 1992 91 106
33. 1H NMR analysis of the partly folded non-native two-disulphide intermediates (30-51,5-14) and (30-51,5-38) in the folding pathway of bovine pancreatic trypsin inhibitor J. Mol. Biol. 235 1994 1044 1061
34. 15N resonance assignments for wild-type and [C65S, C72S] mutant forms Biochemistry 36 1997 6915 6929
35. J.H. Laity, C.C. Lester, S. Shimotakahara, D.E. Zimmerman, G.T. Montelione, and H.A. Scheraga Structural characterization of an analog of the major rate-determining disulfide folding intermediate of bovine pancreatic ribonuclease A Biochemistry 36 1997 12683 12699
36. M. Narayan, E. Welker, W.J. Wedemeyer, and H.A. Scheraga Oxidative folding of proteins Accts Chem. Res. 33 2000 805 812
37. E. Welker, M. Narayan, W.J. Wedemeyer, and H.A. Scheraga Structural determinants of oxidative folding in proteins Proc. Natl Acad. Sci. USA 98 2001 2312 2316
38. A. Yokota, K. Hirai, H. Miyauchi, S. Iimura, Y. Noda, and K. Inoue NMR characterization of three-disulfide variants of lysozyme, C64A/C80A, C76A/C94A, and C30A/C115A-a marginally stable state in folded proteins Biochemistry 43 2004 6663 6669
39. A. Yokota, K. Izutani, M. Takai, Y. Kubo, Y. Noda, and Y. Koumoto The transition state in the folding-unfolding reaction of four species of three-disulfide variant of hen lysozyme: the role of each disulfide bridge J. Mol. Biol. 295 2000 1275 1288
40. Z.Y. Guo, L. Shen, and Y.M. Feng The different energetic state of the intra A-chain/domain disulfide of insulin and insulin-like growth factor 1 is mainly controlled by their B-chain/domain Biochemistry 41 2002 10585 10592
41. Z.Y. Guo, and Y.M. Feng Effects of cysteine to serine substitutions in the two inter-chain disulfide bonds of insulin Biol. Chem. 382 2001 443 448
42. Q.X. Hua, S.H. Nakagawa, W. Jia, S.Q. Hu, Y.C. Chu, P.G. Katsoyannis, and M.A. Weiss Hierarchical protein folding: asymmetric unfolding of an insulin analogue lacking the A7-B7 interchain disulfide bridge Biochemistry 40 2001 12299 12311
43. M. Nagashima, M. Werner, M. Wang, L. Zhao, D.R. Light, and R. Pagila An inhibitor of activated thrombin-activatable fibrinolysis inhibitor potentiates tissue-type plasminogen activator-induced thrombolysis in a rabbit jugular vein thrombolysis model Thromb. Res. 98 2000 333 342
44. J.B. Walker, B. Hughes, I. James, P. Haddock, C. Kluft, and L. Bajzar Stabilization versus inhibition of TAFIa by competitive inhibitors in vitro J. Biol. Chem. 278 2003 8913 8921
45. J. Peranen, M. Rikkonen, M. Hyvonen, and L. Kaariainen T7 vectors with modified T7lac promoter for expression of proteins in Escherichia coli Anal. Biochem. 236 1996 371 373
46. J.F. Morrison The slow-binding and slow, tight-binding inhibition of enzyme-catalysed reactions Trends Biochem. Sci. 7 1982 102 105
47. D. Reverter, S. Ventura, V. Villegas, J. Vendrell, and F.X. Aviles Overexpression of human procarboxypeptidase A2 in Pichia pastoris and detailed characterization of its activation pathway J. Biol. Chem. 273 1998 3535 3541
48. P.J. Barbosa Pereira, S. Segura-Martín, B. Oliva, C. Ferrer-Orta, F.X. Aviles, and M. Coll Human procarboxypeptidase B: three-dimensional structure and implications for thrombin-activatable fibrinolysis inhibitor (TAFI) J. Mol. Biol. 321 2002 537 547
49. W. Kabsch Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Crystallog. 26 1993 795 800
50. Collaborative Computational Project Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
51. D.E. McRee XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density J. Struct. Biol. 125 1999 156 165
52. V.S. Lamzin, and K.S. Wilson Automated refinement of protein models Acta Crystallog. sect. D 49 1993 129 149