Dissecting the role of disulfide bonds on the amyloid formation of insulin

Biochemical and Biophysical Research Communications

Volumn 423, Issue 2, 2012, Pages 373-378

  Li, Yang ^a   Gong, Hao ^a   Sun, Yue ^b   Yan, Juan ^a   Cheng, Biao ^a   Zhang, Xin ^a   Huang, Jing ^b   Yu, Mengying ^a   Guo, Yu ^a   Zheng, Ling ^b   Huang, Kun ^a,c  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b WUHAN UNIVERSITY   (China)

^c Centre for Biomedicine Research   (China)

Author keywords

Diabetes; Disulfide bonds; Fibrillation; Hemolysis; Insulin; Oligomerization

Indexed keywords

AMYLOID; INSULIN 2; INSULIN 3; INSULIN 6; INSULIN DERIVATIVE; IODOACETAMIDE; PIG INSULIN; THIOFLAVINE; TRIS(2 CARBOXYETHYL)PHOSPHINE; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; CYTOTOXICITY; DISULFIDE BOND; ERYTHROCYTE; FLUORESCENCE; HUMAN; HUMAN CELL; NONHUMAN; NORMAL HUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN STRUCTURE; PROTEIN UNFOLDING; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET SPECTROSCOPY;

ALKYLATION; AMINO ACID SEQUENCE; AMYLOID; ANIMALS; CELLS, CULTURED; CIRCULAR DICHROISM; DISULFIDES; ERYTHROCYTES; HEMOLYSIS; HUMANS; INSULIN; MOLECULAR SEQUENCE DATA; SWINE; THIAZOLES; ULTRAVIOLET RAYS;

SUS;

EID: 84862902127     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.05.133     Document Type: Article

References (28)

1. Dobson C.M. Protein folding and its links with human disease. Biochem. Soc. Symp. 2001, 1-26.
2. Mehlhorn I., Groth D., Stockel J., Moffat B., Reilly D., Yansura D., Willett W.S., Baldwin M., Fletterick R., Cohen F.E., Vandlen R., Henner D., Prusiner S.B. High-level expression and characterization of a purified 142-residue polypeptide of the prion protein. Biochemistry 1996, 35:5528-5537.
3. Cao A., Hu D., Lai L. Formation of amyloid fibrils from fully reduced hen egg white lysozyme. Protein Sci. 2004, 13:319-324.
4. Yonemoto I.T., Kroon G.J., Dyson H.J., Balch W.E., Kelly J.W. Amylin proprotein processing generates progressively more amyloidogenic peptides that initially sample the helical state. Biochemistry 2008, 47:9900-9910.
5. Apostolidou M., Jayasinghe S.A., Langen R. Structure of alpha-helical membrane-bound human islet amyloid polypeptide and its implications for membrane-mediated misfolding. J. Biol. Chem. 2008, 283:17205-17210.
6. Nielsen J.T., Bjerring M., Jeppesen M.D., Pedersen R.O., Pedersen J.M., Hein K.L., Vosegaard T., Skrydstrup T., Otzen D.E., Nielsen N.C. Unique identification of supramolecular structures in amyloid fibrils by solid-state NMR spectroscopy. Angew. Chem., Int. Ed. Engl. 2009, 48:2118-2121.
7. Blundell T.L., Cutfield J.F., Cutfield S.M., Dodson E.J., Dodson G.G., Hodgkin D.C., Mercola D.A. Three-dimensional atomic structure of insulin and its relationship to activity. Diabetes 1972, 21:492-505.
8. Hua Q.X., Mayer J.P., Jia W., Zhang J., Weiss M.A. The folding nucleus of the insulin superfamily: a flexible peptide model foreshadows the native state. J. Biol. Chem. 2006, 281:28131-28142.
9. Nielsen L., Khurana R., Coats A., Frokjaer S., Brange J., Vyas S., Uversky V.N., Fink A.L. Effect of environmental factors on the kinetics of insulin fibril formation: elucidation of the molecular mechanism. Biochemistry 2001, 40:6036-6046.
10. Maeda R., Ado K., Takeda N., Taniguchi Y. Promotion of insulin aggregation by protein disulfide isomerase. Biochim. Biophys. Acta 2007, 1774:1619-1627.
11. Givol D., Delorenzo F., Goldberger R.F., Anfinsen C.B. Disulfide interchange and the three-dimensional structure of proteins. Proc. Natl. Acad. Sci. USA 1965, 53:676-684.
12. Huang K., Maiti N.C., Phillips N.B., Carey P.R., Weiss M.A. Structure-specific effects of protein topology on cross-beta assembly: studies of insulin fibrillation. Biochemistry 2006, 45:10278-10293.
13. Sreerama N., Woody R.W. Computation and analysis of protein circular dichroism spectra. Methods Enzymol. 2004, 383:318-351.
14. Huang K., Dong J., Phillips N.B., Carey P.R., Weiss M.A. Proinsulin is refractory to protein fibrillation: topological protection of a precursor protein from cross-beta assembly. J. Biol. Chem. 2005, 280:42345-42355.
15. Zhang X., Cheng B., Gong H., Li C., Chen H., Zheng L., Huang K. Porcine islet amyloid polypeptide fragments are refractory to amyloid formation. FEBS Lett. 2011, 585:71-77.
16. Bitan G., Teplow D.B. Rapid photochemical cross-linking-a new tool for studies of metastable, amyloidogenic protein assemblies. Acc. Chem. Res. 2004, 37:357-364.
17. Cheng B., Liu X., Gong H., Huang L., Chen H., Zhang X., Li C., Yang M., Ma B., Jiao L., Zheng L., Huang K. Coffee components inhibit amyloid formation of human islet amyloid polypeptide in vitro: possible link between coffee consumption and diabetes mellitus. J. Agric. Food Chem. 2011, 59:13147-13155.
18. Wang J.B., Wang Y.M., Zeng C.M. Quercetin inhibits amyloid fibrillation of bovine insulin and destabilizes preformed fibrils. Biochem. Biophys. Res. Commun. 2011, 415:675-679.
19. Gray W.R. Disulfide structures of highly bridged peptides: a new strategy for analysis. Protein Sci. 1993, 2:1732-1748.
20. Jia X.Y., Guo Z.Y., Wang Y., Xu Y., Duan S.S., Feng Y.M. Peptide models of four possible insulin folding intermediates with two disulfides. Protein Sci. 2003, 12:2412-2419.
21. Hua Q. Insulin: a small protein with a long journey. Protein Cell 2010, 1:537-551.
22. Hua Q.X., Hu S.Q., Frank B.H., Jia W., Chu Y.C., Wang S.H., Burke G.T., Katsoyannis P.G., Weiss M.A. Mapping the functional surface of insulin by design: structure and function of a novel A-chain analogue. J. Mol. Biol. 1996, 264:390-403.
23. Weiss M.A., Hua Q.X., Jia W., Chu Y.C., Wang R.Y., Katsoyannis P.G. Hierarchical protein " un-design" : insulin's intrachain disulfide bridge tethers a recognition alpha-helix. Biochemistry 2000, 39:15429-15440.
24. Hua Q.X., Nakagawa S.H., Jia W., Hu S.Q., Chu Y.C., Katsoyannis P.G., Weiss M.A. Hierarchical protein folding: asymmetric unfolding of an insulin analogue lacking the A7-B7 interchain disulfide bridge. Biochemistry 2001, 40:12299-12311.
25. Chang S.G., Choi K.D., Jang S.H., Shin H.C. Role of disulfide bonds in the structure and activity of human insulin. Mol. Cells 2003, 16:323-330.
26. Dobson C.M. Protein folding and misfolding. Nature 2003, 426:884-890.
27. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., Taddei N., Ramponi G., Dobson C.M., Stefani M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 2002, 416:507-511.
28. Stefani M., Dobson C.M. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. (Berl) 2003, 81:678-699.