Cooperative omega loops in cytochrome c: Role in folding and function

Journal of Molecular Biology

Volumn 331, Issue 1, 2003, Pages 29-36

  Krishna, Mallela M G ^a   Lin, Yan ^a   Rumbley, Jon N ^a   Englander, S Walter ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cytochrome c; Hydrogen exchange; Omega loop; Protein folding; Protein function

Indexed keywords

CYTOCHROME C;

ARTICLE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE;

EID: 0038786579     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00697-1     Document Type: Article

References (40)

1. Leszczynski J.F., Rose G.D. Loops in globular proteins: a novel category of secondary structure. Science. 234:1986;849-855.
2. Fetrow J.S. Omega loops: nonregular secondary structures significant in protein function and stability. FASEB J. 9:1995;708-717.
3. Hoang L., Maity H., Krishna M.M.G., Lin Y., Englander S.W. Folding units of cytochrome c govern its alkaline transition. J. Mol. Biol. 331:2003;37-43.
4. Bai Y., Sosnick T.R., Mayne L., Englander S.W. Protein folding intermediates: native-state hydrogen exchange. Science. 269:1995;192-197.
5. Bai Y., Englander S.W. Future directions in folding: the multi-state nature of protein structure. Proteins: Struct. Funct. Genet. 24:1996;145-151.
6. Hoang L., Bedard S., Krishna M.M.G., Lin Y., Englander S.W. Cytochrome c folding pathway: kinetic native-state hydrogen exchange. Proc. Natl Acad. Sci. USA. 99:2002;12173-12178.
7. Xu Y., Mayne L., Englander S.W. Evidence for an unfolding and refolding pathway in cytochrome c. Nature Struct. Biol. 5:1998;774-778.
8. Milne J.S., Xu Y., Mayne L.C., Englander S.W. Experimental study of the protein folding landscape: unfolding reactions in cytochrome c. J. Mol. Biol. 290:1999;811-822.
9. Zimm G.H., Bragg J.K. Theory of the phase transition between helix and random coil in polypeptide chains. J. Chem. Phys. 31:1959;526-535.
10. Lifson S., Roig A. On the theory of the helix-coil transition in polypeptides. J. Chem. Phys. 34:1961;1963-1974.
11. Milne J.S., Mayne L., Roder H., Wand A.J., Englander S.W. Determinants of protein hydrogen exchange studied in equine cytochrome c. Protein Sci. 7:1998;739-745.
12. Maity H., Lim W.K., Rumbley J.N., Englander S.W. Protein hydrogen exchange mechanism: local fluctuations. Protein Sci. 12:2003;153-160.
13. Bushnell G.W., Louie G.V., Brayer G.D. High-resolution three-dimensional structure of horse heart cytochrome c. J. Mol. Biol. 214:1990;585-595.
14. Moore G.R., Pettigrew G.W. Springer Series in Molecular Biology. Springer Series in Molecular Biology. 1990;Springer-Verlag, Berlin, Heidelberg, New York.
15. Rumbley J.N., Hoang L., Englander S.W. Recombinant equine cytochrome c in Escherichia coli: high-level expression, characterization, and folding and assembly mutants. Biochemistry. 41:2002;13894-13901.
16. 2O. Biochemistry. 32:1993;11878-11885.
17. Roder H., Elove G.A., Englander S.W. Structural characterization of folding intermediates in cytochrome c by H-exchange labeling and proton NMR. Nature. 335:1988;700-704.
18. Bai Y. Kinetic evidence for an on-pathway intermediate in the folding of cytochrome c. Proc. Natl Acad. Sci. USA. 96:1999;477-480.
19. Englander S.W. Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomol. Struct. 29:2000;213-238.
20. Chamberlain A.K., Marqusee S. Comparison of equilibrium and kinetic approaches for determining protein folding mechanisms. Advan. Protein Chem. 53:2000;283-328.
21. Yan S., Kennedy S.D., Koide S. Thermodynamic and kinetic exploration of the energy landscape of Borrelia budgdorferi OspA by native-state hydrogen exchange. J. Mol. Biol. 323:2002;363-375.
22. Chu R., Pei W., Takei J., Bai Y. Relationship between the native-state hydrogen exchange and folding pathways of a four-helix bundle protein. Biochemistry. 41:2002;7998-8003.
23. Rumbley J., Hoang L., Mayne L., Englander S.W. An amino acid code for protein folding. Proc. Natl Acad. Sci. USA. 98:2001;105-112.
24. Wang L., Kallenbach N.R. Proteolysis as a measure of the free energy difference between cytochrome c and its derivatives. Protein Sci. 7:1998;2460-2464.
25. Spolaore B., Bermejo R., Zambonin M., Fontana A. Protein interactions leading to conformational changes monitored by limited proteolysis: Apo form and fragments of horse cytochrome c. Biochemistry. 40:2001;9460-9468.
26. Linderstrøm-Lang K.U., Schellman J.A. Protein structure and enzyme activity. Boyer P.D., Lardy H., Myrback K. The Enzymes. 1959;443-510 Academic Press, New York.
27. Fetrow J.S., Cardillo T.S., Sherman F. Deletions and replacements of omega loops in yeast iso-1-cytochrome c. Proteins: Struct. Funct. Genet. 6:1989;372-381.
28. Fetrow J.S., Dreher U., Wiland D.J., Schaak D.L., Boose T.L. Mutagenesis of histidine-26 demonstrates the importance of loop-loop and loop-protein interactions for the function of iso-1-cytochrome c. Protein Sci. 7:1998;994-1005.
29. Garcia A.E., Hummer G. Conformational dynamics of cytochrome c: correlation to hydrogen exchange. Proteins: Struct. Funct. Genet. 36:1999;175-191.
30. 15N relaxation measurements for oxidized and reduced iso-1-cytochrome c. Biochemistry. 38:1999;4480-4492.
31. 15N]-labeled oxidized and reduced iso-1-cytochrome c. Biochemistry. 38:1999;4493-4503.
32. Jemmerson R., Liu J., Hausauer D., Lam K.-P., Mondino A., Nelson R.D. A conformational change in cytochrome c of apoptotic and necrotic cells is detected by monoclonal antibody binding and mimicked by association of the native antigen with synthetic phospholipid vesicles. Biochemistry. 38:1999;3599-3609.
33. Wallace C.J.A. Functional consequences of the excision of an Ω loop, residues 40-55, from mitochondrial cytochrome c. J. Biol. Chem. 262:1987;16767-16770.
34. Wallace C.J.A. Understanding cytochrome c function: engineering protein structure by semisynthesis. FASEB J. 7:1993;505-515.
35. Westerhuis L.W., Tesser G.I., Nivard R.J.F. A functioning complex of two cytochrome c fragments with deletion of (39-58) eicosapeptide. Int. J. Pept. Protein Res. 19:1982;290-299.
36. Qin W., Sanishvili R., Plotkin B., Schejter A., Margoliash E. The role of histidines 26 and 33 in the structural stabilization of cytochrome c. Biochim. Biophys. Acta. 1252:1995;87-94.
37. Pettigrew G.W., Moore G.R. Cytochromes c. Biological aspects. Rich A. Springer Series in Molecular Biology. 1987;Springer-Verlag, Berlin, Heidelberg, New York.
38. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;945-949.
39. Bai Y., Milne J.S., Mayne L., Englander S.W. Primary structure effects on peptide group hydrogen exchange. Proteins: Struct. Funct. Genet. 17:1993;75-86.
40. Connelly G.P., Bai Y., Jeng M.-F., Englander S.W. Isotope effects in peptide group hydrogen exchange. Proteins: Struct. Funct. Genet. 17:1993;87-92.