Structural stability of human α-thrombin studied by disulfide reduction and scrambling

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1651, Issue 1-2, 2003, Pages 85-92

  Singh, R Rajesh ^a   Chang, Jui Yoa ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Disulfide scrambling; Reductive unfolding; Structure of denatured thrombin; Thrombin denaturation

Indexed keywords

GUANIDINE; THIOL REAGENT; THROMBIN; UREA; DISULFIDE; HEMOSTATIC AGENT; ISOENZYME; MERCAPTOETHANOL;

ALPHA CHAIN; AMINO ACID SEQUENCE; ARTICLE; BETA CHAIN; CONCENTRATION RESPONSE; DENATURATION; DISULFIDE BOND; DISULFIDE SCRAMBLING; ENZYME CONFORMATION; HUMAN; ISOMER; MITOSIS INHIBITION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STABILITY; RESIDUE ANALYSIS; TECHNIQUE; CHEMISTRY; ENZYME STABILITY; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN DENATURATION; PROTEIN TERTIARY STRUCTURE;

DISULFIDES; ENZYME STABILITY; GUANIDINE; HEMOSTATICS; HUMANS; ISOENZYMES; MERCAPTOETHANOL; OXIDATION-REDUCTION; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; THROMBIN;

EID: 1242296243     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1570-9639(03)00238-3     Document Type: Article

References (36)

1. Fenton J.W. II Regulation of thrombin, generation and function. Semin. Thromb. Hemost. 14:1988;234-240.
2. Vergnolle N., Derian C.K., D'Andrea M.R., Steinhoff M., Andrade-Gordon P. Characterization of thrombin-induced leukocyte rolling and adherence: a potential proinflammatory role for proteinase-activated receptor-4. J. Immunol. 169:2002;1467-1473.
3. Sambrano G.R., Weiss E.J., Zheng Y.W., Helang W., Coughlin S.R. Role of thrombin signalling in platelets in haemostasis and thrombosis. Nature. 413:2001;74-78.
4. Esmon C.T., Lollar P. Involvement of thrombin anion-binding exosites 1 and 2 in the activation of factor V and factor VIII. J. Biol. Chem. 271:1996;13882-13887.
5. Baglia F.A., Walsh P.N. Thrombin-mediated feedback activation of factor XI on the activated platelet surface is preferred over contact activation by factor XIIa or factor Xia. J. Biol. Chem. 275:2000;20514-20519.
6. Sadasivan C., Yee V.C. Interaction of the factor XIII activation peptide with α-thrombin. Crystal structure of its enzyme-substrate analog complex. J. Biol. Chem. 275:2000;36942-36948.
7. Esmon C.T. Hematology. Hofman R., Benz E.J., Shattel S.J., Furie B., Cohen H.J., Silberstein L.E., Mc Glave P. Basic Principles and Practice. 2000;1714-1824 Churchill Livingstone, New york.
8. Liem R.K.H., Scheraga H.A. Mechanism of action of thrombin or fibrinogen: IV. Further mapping on the active sites of thrombin and trypsin. Arch. Biochem. Biophys. 160:1974;333-339.
9. Lottenberg R., Hall J.A., Blinder M., Binder E.P., Jackson C.M. The action of thrombin on peptide p-nitroanilide substrates: substrate selectivity and examination of hydrolysis under different reaction conditions. Biochim. Biophys. Acta. 742:1983;539-557.
10. Butkowski R.J., Elion J., Downing M.R., Mann K.G. Primary structure of human prothrombin 2 and alpha-thrombin. J. Biol. Chem. 252:1977;4942-4957.
11. Degen S.J.F., Mac Gillivray R.T.A., Davie E.W. Characterization of the complementary deoxyribonucleic acid and gene coding for human prothrombin. Biochemistry. 22:1983;2087-2097.
12. Fenton J.W. II, Fasco M.J., Stackrow A.B., Aronson D.L., Young A.M., Finlayson J.S. Human thrombins. Production, evaluation, and properties of alpha-thrombin. J. Biol. Chem. 252:1977;3587-3598.
13. Fenton J.W. II, Landis B.H., Walz D.A., Finlayson J.S. Lundbald R.L. II, Fenton J.W., Mann K.G. Human Thrombins. 1977;43-70 Ann Arbor Science Publishers, Michigan.
14. Berliner L.J., Shen Y.Y. Lundbald R.L., Fenton J.W. II, Mann K.G. Chemistry and Biology of Thrombin. 1977;197-216 Ann Arbor Science Publishers, Michigan.
15. Chang J.-Y., Li L. The structure of denatured α-lactalbumin elucidated by the technique of disulfide scrambling. Fractionation of conformational isomers of α-lactalbumin. J. Biol. Chem. 276:2001;9705-9712.
16. Chang J.-Y., Li L. The unfolding mechanism and the disulfide structures of denatured lysozyme. FEBS. Lett. 511:2002;73-78.
17. Chang J.-Y. Denatured states of tick anticoagulant peptide. Compositional analysis of unfolded scrambled isomers. J. Biol. Chem. 274:1999;123-128.
18. Chang J.-Y., Li L., Canals F., Aviles F.X. The unfolding pathway and conformational stability of potato carboxypeptidase inhibitor. J. Biol. Chem. 275:2000;14205-14211.
19. Chang J.-Y., Ballatore A. The structure of denatured bovine pancreatic trypsin inhibitor (BPTI). FEBS Lett. 473:2000;183-187.
20. Labhardt A.M. Folding intermediates studied by circular dichroism. Methods Enzymol. 131:1986;126-135.
21. Surewicz W.E., Mantsh H.H., Chapman D. Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry. 32:1993;389-394.
22. Triullier A., Reinstadler D., Dupont Y., Naumann D., Forge V. Transient non-native secondary structures during the refolding of alpha-lactalbumin detected by infrared spectroscopy. Nat. Struct. Biol. 7:2000;78-86.
23. Kim P.S. Amide proton exchange as a probe of protein folding pathways. Methods Enzymol. 131:1986;136-156.
24. Forge V., Wijesinha R.T., Balbach J., Brew K., Robinson C.V., Redfield C., Dobson C.M. Rapid collapse and slow structural reorganisation during the refolding of bovine alpha-lactalbumin. J. Mol. Biol. 288:1999;673-688.
25. Klefhaber T., Labhardt A.M., Baldwin R.L. Direct NMR evidence for an intermediate preceding the rate-limiting step in the unfolding of ribonuclease A. Nature. 375:1995;513-515.
26. 120 disulfide bond. Biochemistry. 29:1990;8240-8249.
27. Kress L.F., Laskowski M. Sr. The basic trypsin inhibitor of bovine pancreas: VII. Reduction with borohydride of disulfide bond linking half-cystine residues 14 and 38. J. Biol. Chem. 242:1967;4925-4929.
28. Liu W.K., Meienhofer J. Preparation of 14,38-bis-[S-carbamidomethyl]- (basic trypsin inhibitor) possessing full biological activity. Biochem. Biophys. Res. Commun. 31:1968;467-473.
29. Hollecker M., Creighton T.E. Evolutionary conservation and variation of protein folding pathways. Two protease inhibitor homologues from black mamba venom. J. Mol. Biol. 168:1983;409-437.
30. Chang J.-Y. A two-stage mechanism for the reductive unfolding of disulfide-containing proteins. J. Biol. Chem. 272:1997;69-75.
31. Chang J.-Y. Quantitative analysis of the composition of the native and scrambled ribonuclease A. Anal. Biochem. 268:1999;147-150.
32. Chang J.-Y., Grossenbacher H., Meyhack B., Maerki W. Production of disulfide-linked hirudin dimer by in vitro folding. FEBS Lett. 336:1993;53-56.
33. Bode W., Turk D., Karashikov A. The refined 1.9-A X-ray crystal structure of D-Phe-Pro-Arg chloromethylketone-inhibited human alpha-thrombin: structure analysis, overall structure, electrostatic properties, detailed active-site geometry, and structure-function relationships. Protein Sci. 1:1992;426-471.
34. Gruetter M., Priestle J.P., Rahuel J., Grossenbacher H., Bode W., Hofsteenge J., Stone S.R. Crystal structure of the thrombin-hirudin complex: a novel mode of serine protease inhibition. EMBO J. 9:1990;2361-2365.
35. Rydel T.J., Ravichandran K.G., Tulinsky A., Bode W., Huber R., Roitsch C., Fenton J.W. II The structure of a complex of recombinant hirudin and human alpha-thrombin. Science. 249:1990;277-280.
36. White C.E., Hunter M.J., Meininger D.P., Garrod S., Komives E.A. The fifth epidermal growth factor-like domain of thrombomodulin does not have an epidermal growth factor-like disulfide bonding pattern. Proc. Natl. Acad. Sci. U. S. A. 93:1996;10177-10182.