Pathway of oxidative folding of secretory leucocyte protease inhibitor: An 8-disulfide protein exhibits a unique mechanism of folding

Biochemistry

Volumn 45, Issue 19, 2006, Pages 6231-6240

  Lin, Curtis C J ^a   Chang, Jui Yoa ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYST ACTIVITY; ENZYME INHIBITION; ISOMERS; OXIDATION; REDOX REACTIONS;

FOLDING PATHWAY; HETEROGENEOUS POPULATIONS; KINETIC INTERMEDIATES; QUANTITATIVE RECOVERY;

PROTEINS;

AMINO ACID; BUFFER; DISULFIDE; OXIDIZING AGENT; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; THIOL;

AIR; ARTICLE; CATALYST; CORRELATION ANALYSIS; DISULFIDE BOND; ISOMER; KINETICS; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING;

AMINO ACID SEQUENCE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISULFIDES; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PROTEIN FOLDING; PROTEINASE INHIBITORY PROTEINS, SECRETORY; PROTEINS;

EID: 33646566869     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060259f     Document Type: Article

References (35)

1. Creighton, T. E. (1986) Disulfide bonds as probes of protein folding pathways, Methods Enzymol. 131, 83-106.
2. Scheraga, H. A., Wedemeyer, W. J., and Welker, E. (2001) Bovine pancreatic ribonuclease A: Oxidative and conformational folding studies, Methods Enzymol. 341, 189-221.
3. Creighton, T. E. (1992) The disulfide folding pathway of BPTI, Science 256, 111-114.
4. Goldenberg, D. P. (1992) Native and non-native intermediates in the BPTI folding pathway, Trends Biochem. Sci. 17, 257-261.
5. Weissman, J. S., and Kim, P. S. (1991) Re-examination of the folding of BPTI: Predominance of native intermediates, Science 253, 1386-1393.
6. Rothwarf, D., Li, Y.-J., and Scheraga, H. A. (1998) Regeneration of Bovine Pancreatic Ribonuclease A: Identification of Two Native-like Three-Disulfide Intermediates Involved in Separate Pathways, Biochemistry 37, 3760-3766.
7. Welker, E., Narayan, M., Wedemeyer, W. J., and Scheraga, H. A. (2001) Structural determinants of oxidative folding in proteins, Proc. Natl. Acad. Sci. U.S.A. 98, 2312-2316.
8. Dadlez, M., and Kim, P. S. (1996) Rapid formation of the native 14-38 disulfide bond in the early stages of BPTI folding, Biochemistry 35, 16153-16164.
9. Chatrenet, B., and Chang, J.-Y. (1993) The disulfide folding pathway of hirudin elucidated by stop/go folding experiments, J. Biol. Chem. 268, 20988-20996.
10. Chang, J.-Y. (1994) Controlling the speed of hirudin folding, Biochem. J. 300, 643-650.
11. Chang, J.-Y. (1996) The disulfide folding pathway of tick anticoagulant peptide, a kunitz-type inhibitor structurally homologous to BPTI, Biochemistry 35, 11702-11709.
12. Chang, J.-Y., Li, L., and Lai, P. H. (2001) A major kinetic trap for the oxidative folding of human epidermal growth factor, J. Biol. Chem. 276, 4845-4852.
13. Chang, J.-Y., Cannais, F., Schindler, P., Querol, E., and Aviles, F. X. (1994) The disulfide folding pathway of potato carboxypeptidase inhibitor, J. Biol. Chem. 269, 22087-22094.
14. Salamanca, S., Li, L., Vendrell, J., Aviles, F. X., and Chang, J.-Y. (2003) Major kinetic traps for the oxidative folding of leech carboxypeptidase inhibitor, Biochemistry 42, 6754-6761,
15. Arolas, J. L., Bronsoms, S., Lorenzo, J., Aviles, F. X., Chang, J.-Y., and Ventura, S. (2004) Role of kinetic intermediates in the folding of carboxypeptidase inhibitor, J. Biol. Chem. 279, 37261-37270.
16. Chang, J.-Y., and Li, L. (2002) Pathway of oxidative folding of α-lactalbumin: A model for illustrating the diversity of disulfide folding pathway, Biochemistry 41, 8405-8413.
17. Ewbank, J. J., and Creighton, T. E. (1993) Pathway of disulfide-coupled unfolding and refolding of bovine α-lactalbumin, Biochemistry 32, 3677-3693.
18. Cemazar, M., Zahariev, S., Lopez, J. J., Carugo, O., Jones, J. A., Hore, P. J., and Pongor, S. (2003) Oxidative folding intermediates with nonnative disulfide bridges between adjacent cysteine residues, Proc. Natl. Acad. Sci. U.S.A. 100, 5754-5759.
19. Hua, Q. X., Jia, W., Frank, B. H., Phillips, N. F., and Weiss, M. A. (2002) A Protein Caught in a Kinetic Trap: Structures and Stabilities of Insulin Disulfide Isomers, Biochemistry 41, 14700-14715.
20. Hua, Q. X., Narhi, L., Jia, W., Arakawa, T., Rosenfeld, R., Hawkins, N., Miller, J. A., and Weiss, M. A. (1996) Native and Non-native Structure in a Protein-folding Intermediate: Spectroscopic Studies of Partially Reduced IGF-I and an Engineered Alanine Model, J. Mol. Biol. 259, 297-313.
21. Yang, Y., Wu, J., and Watson, J. T. (1999) Probing the folding pathways of long R(3) insulin-like growth factor-I (LR(S)IGF-I) and IGF-I via capture and identification of disulfide intermediates by cyanylation methodology and mass spectrometry, J. Biol. Chem. 274, 37598-37604.
22. Pattanaik, P., Sooryanarayana, A. P. R., and Visweswariah, S. S. (1998) Refolding of native and recombinant chicken riboflavin carrier (or binding) protein: Evidence for the formation of non-native intermediates during the generation of active protein, Eur. J. Biochem. 258, 411-418.
23. Qiao, Z. S., Min, C. Y., Hua, Q. X., Weiss, M. A., and Feng, Y. M. (2003) In vitro refolding of human proinsulin. Kinetic intermediates, putative disulfide-forming pathway folding initiation site, and potential role of C-peptide in folding process, J. Biol. Chem. 278, 17800-17809.
24. Rosenfeld, R. D., Miller, J. A., Narhi, L. O., Hawkins, N., Katta, V., Lauren, S., Weiss, M. A., and Arakawa, T. (1997) Putative folding pathway of insulin-like growth factor-I, Arch. Biochem. Biophys. 342, 298-305.
25. Seemuller, U., Arnhold, M., Fritz, H., Wiedenmann, K., Machleidt, W., Heinzel, R., Appelhans, H., Gassen, H. G., and Lottspeich, F. (1986) The acid-stable proteinase inhibitor of human mucous secretions (HUSI-I, antileukoprotease). Complete amino acid sequence as revealed by protein and cDNA sequencing and structural homology to whey proteins and Red Sea turtle proteinase inhibitor, FEBS Lett. 199, 43-48.
26. Thompson, R. C., and Ohlsson, K. (1986) Isolation, properties, and complete amino acid sequence of human secretory leukocyte protease inhibitor, a potent inhibitor of leukocyte elastase, Proc. Natl. Acad. Sci. U.S.A. 83, 6692-6696.
27. Gruetter, M., Fendrich, G., Huber, R., and Bode, W. (1988) The 2.5 Å X-ray crystal structure of the acid stable proteinase inhibitor from human mucous secretions analyzed in its complex with bovine α- chymotrypsin, EMBO J. 7, 345-352.
28. Dill, K. A. (1990) Dominant force in protein folding, Biochemistry 29, 7133-7155.
29. Chang, J.-Y., and Ballatore, A. (2000) Structure and heterogeneity of the one- and two-disulfide folding intermediates of tick anticoagulant peptide, J. Protein Chem. 19, 299-310.
30. Chang, J.-Y., Lu, B.-Y., Lin, C., and Chin, Y. (2005) Fully oxidized scrambled isomers are essential and predominant folding intermediates of cardiotoxin-III, FEBS Lett. (in press).
31. Chang, J.-Y., Li, L., and Bulychev, A. (2000) The underlying mechanism for the diversity of disulfide folding pathway, J. Biol. Chem. 275, 8287-8289.
32. Chang, J.-Y. (1997) A two-stage mechanism for the reductive unfolding of disulfide-containing proteins, J. Biol. Chem. 272, 69-75.
33. Arola, J. L., Popowicz, G. M., Bronsoms, S., Aviles, F. X., Huber, R., Holak, T. A., and Ventura, S. (2005) Study of a major intermediate in the oxidative folding of leech carboxypeptidase inhibitor: Contribution of the fourth disulfide bond, J. Mol. Biol. 352, 961-975,
34. Arolas, J. L., D'Silva, L., Popowicz, G. M., Aviles, F. X., Holak, T. A., and Ventura, S. (2005) NMR structural characterization and computational predictions of the major intermediate in oxidative folding of leech carboxypeptidase inhibitor, Structure 13, 1193-1202.
35. Seckler, R., and Jaenicke, R. (1992) Protein folding and protein refolding, FASEB J. 6, 2545-2552.