Compressing the free energy range of substructure stabilities in iso-1-cytochrome c

Protein Science

Volumn 18, Issue 6, 2009, Pages 1155-1164

  Duncan, Michael G ^a   Williams, Michael D ^a   Bowler, Bruce E ^a  

^a UNIVERSITY OF MONTANA   (United States)

Author keywords

Alkaline transition; Evolutionary conservation; Folding cooperativity; Limited proteolysis; Protein folding; Protein substructures

Indexed keywords

CYTOCHROME C; ISOCYTOCHROME C1; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME CONFORMATION; ENZYME STABILITY; ENZYME STRUCTURE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING;

ANIMALS; CYTOCHROMES C; ENTROPY; EVOLUTION, MOLECULAR; HORSES; PEPTIDE HYDROLASES; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EQUIDAE;

EID: 66349104530     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.120     Document Type: Article

References (50)

1. Jackson SE (1992) How do small single-domain proteins fold? Fold Des 3:R81-R91.
2. Wildes D, Marqusee S (2004) Hydrogen exchange strategies applied to energetics of intermediate processes in protein folding. Methods Enzymol 380:328-349. (Pubitemid 38297502)
3. Englander SW, Mayne L, Rumbley JN (2002) Submolecular cooperativity produces multi-state protein unfolding and refolding. Biophys Chem 101:57-65. (Pubitemid 35462036)
4. Bai Y, Sosnick TR, Mayne L, Englander SW (1995) Protein folding intermediates: native-state hydrogen exchange. Science 269:192-197.
5. Krishna MMG, Lin J, Rumbley JN, Englander SW (2003) Cooperative omega loops in cytochrome c: role in folding and function. J Mol Biol 331:29-36. (Pubitemid 36870774)
6. Dobson CM (2003) Protein folding and misfolding. Nature 426:884-890. (Pubitemid 38056880)
7. Maity H, Maiti M, Englander SW (2004) How cytochrome c folds and why: submolecular folding units and their stepwise sequential stabilization. J Mol Biol 343:223-233. (Pubitemid 39277460)
8. Krishna MMG, Maity H, Rumbley JN, Lin Y, Englander SW (2006) Order of steps in the cytochrome c folding pathway: evidence for a sequential stabilization mechanism. J Mol Biol 359:1410-1419. (Pubitemid 43903495)
9. Krishna MMG, Maity H, Rumbley JN, Englander SW (2007) Branching in the sequential folding pathway of cytochrome c. Protein Sci 16:1946-1956. (Pubitemid 47367117)
10. Hoang L, Maity H, Krishna MMG, Lin Y, Englander SW (2003) Folding units govern the cytochrome c alkaline transition. J Mol Biol 331:37-43. (Pubitemid 36870775)
11. Maity H, Rumbley JN, Englander SW (2006). Functional role of a foldon - an Φ-loop folding controls the alkaline transition of ferricytochrome c. Proteins 63:349-355.
12. Berghuis AM, Brayer GD (1992) Oxidation state-dependent conformational changes in cytochrome c. J Mol Biol 223:959-976.
13. Hollien J, Marqusee S (1999) Structural distribution of stability in a thermophilic enzyme. Proc Natl Acad Sci USA 96:13674-13678.
14. Godbole S, Bowler BE (1999) Effect of pH on formation of a nativelike intermediate on the unfolding pathway of a Lys 73→His variant of yeast iso-1-cytochrome c. Biochemistry 38:487-495. (Pubitemid 29035720)
15. Godbole S, Hammack B, Bowler BE (2000) Measuring denatured state energetics: deviations from random coil behavior and implications for the folding of iso-1-cytochrome c. J Mol Biol 296:217-228.
16. Knapp JA, Pace CN (1974) Guanidine hydrochloride and acid denaturation of horse, cow, and Candida krusei cytochrome c. Biochemistry 13:1289-1294.
17. McLendon G, Smith M (1978) Equilibrium and kinetic studies of protein folding. J Biol Chem 253:4004-4008.
18. Dickerson RE, Timkovich R, Cytochromes c. In: Boyer PD, Ed. (1975) The enzymes, 3rd ed., Vol.11. New York: Academic Press, pp 397-547.
19. Godbole S, Dong A, Garbin K, Bowler BE (1997) A lysine 73→histidine variant of yeast iso-1-cytochrome c: evidence for a native-like intermediate on the unfolding pathway and implications for m-value effects. Biochemistry 36:119-126. (Pubitemid 27024685)
20. Nelson CJ, Bowler BE (2000) pH dependence of formation of a partially unfolded state of a Lys 73 → His variant of iso-1-cytochrome c: implications for the alkaline conformational transition of cytochrome c. Biochemistry 39:13584-13594.
21. Nelson CJ, LaConte MJ, Bowler BE (2001) Direct detection of heat and cold denaturation for partial unfolding of a protein. J Am Chem Soc 123:7453-7454. (Pubitemid 32879475)
22. Kristinsson R, Bowler BE (2005) Communication of stabilizing energy between substructures of a protein. Biochemistry 44:2349-2359. (Pubitemid 40279539)
23. Bai Y, Englander SW (1996) Future directions in folding: the multi-state nature of protein structure. Proteins 24:145-151. (Pubitemid 26076364)
24. Fuentes EJ, Wand AJ (1998) Local dynamics and stability of apocytochrome b562 examined by hydrogen exchange. Biochemistry 37:3687-3698. (Pubitemid 28162923)
25. Fontana A, Polverino de Laureto P, Spolaore B, Frare E, Picotti P, Zambonin M (2004) Probing protein structure by limited proteolysis. Acta Biochim Pol 51:299-321. (Pubitemid 38969296)
26. Park C, Marqusee S (2004) Probing the high energy states in proteins by proteolysis. J Mol Biol 343:1467-1476. (Pubitemid 39387837)
27. Pollock WBR, Rosell FI, Twitchett MB, Dumont ME, Mauk AG (1998) Bacterial expression of a mitochondrial cytochrome c. Trimethylation of lys72 in yeast iso-1-cytochrome c and the alkaline conformational transition. Biochemistry 37:6124-6131.
28. Hammack BN, Smith CR, Bowler BE (2001) Denatured state thermodynamics: residual structure, chain stiffness and scaling factors. J Mol Biol 311:1091-1104. (Pubitemid 32803723)
29. Qin W, Sanishvili R, Plotkin B, Schejter A, Margoliash E (1995) The role of histidines 26 and 33 in the structural stabilization of cytochrome c. Biochim Biophys Acta 1252:87-94.
30. Fetrow JS, Dreher U, Wiland DJ, Schaak DL, Boose TL (1998) Mutagenesis of histidine 26 demonstrates the importance of loop-loop and loop-protein interactions for the function of iso-1-cytochrome c. Protein Sci 7:994-1005. (Pubitemid 28216541)
31. Hubbard SJ, Eisenmenger F, Thornton JM (1994) Modeling studies of the change in conformation required for cleavage of limited proteolytic sites. Protein Sci 3:757-768. (Pubitemid 24139901)
32. Kristjánsson MM, Magnusson ÓT, Gudmunsson HM, Alfredsson GÁ, Matsuzawa H (1999) Properties of a subtilisin-like proteinase from a psychrotrophic Vibrio species. Comparison with proteinase K and aqualysin I. Eur J Biochem 260:752-760. (Pubitemid 29148641)
33. Wang L, Chen RX, Kallenbach NR (1998) Proteolysis as a probe of thermal unfolding of cytochrome c. Proteins 30:435-444 (Pubitemid 28117663)
34. 15N]-labeled oxidized and reduced iso-1-cytochrome c. Biochemistry 38:4493-4503.
35. 15N relaxation measurements for oxidized and reduced iso-1-cytochrome c. Biochemistry 38:4480-4492.
36. Betz SF, Pielak GJ (1992) Introduction of a disulfide bond in cytochrome c stabilizes a compact denatured state. Biochemistry 31:12337-12344. (Pubitemid 23163108)
37. Pace CN (1975) The stability of globular proteins. CRC Crit Rev Biochem 3:1-43.
38. Michel LV, Bren KL (2008) Submolecular unfolding units of Pseudomonas aeruginosa cytochrome c-551. J Biol Inorg Chem 13:837-845.
39. Pielak GJ, Auld DS, Beasley JR, Betz SF, Cohen DS, Doyle DF, Finger SA, Fredericks ZL, Hilgen-Willis S, Saunders AJ, Trojak SK (1995) Protein thermal denaturation, side-chain models, and evolution: amino acid substitutions at a conserved helix-helix interface. Biochemistry 34:3268-3276.
40. Roder H, Elöve GA, Englander SW (1988) Structural characterization of folding intermediates in cytochrome c by H-exchange labeling and protein NMR. Nature 335:700-704. (Pubitemid 18242892)
41. Pletneva EV, Gray HB, Winkler JR (2005) Snapshots of cytochrome c folding. Proc Natl Acad Sci USA 102:18397-18402. (Pubitemid 43011237)
42. Gianni S, Travaglini-Allocatelli C, Cutruzzolà F, Brunori M, Shastry MCR, Roder H (2003) Parallel pathways in cytochrome c551 folding. J Mol Biol 330:1145-1152. (Pubitemid 36818909)
43. Travaglini-Allocatelli C, Gianni S, Brunori, M (2004) A common folding mechanism in the cytochrome c family. Trends Biochem Sci 29:535-541. (Pubitemid 39265170)
44. Borgia A, Bonivento D, Travaglini-Allocatelli C, Di Matteo A, Brunori M (2006) Unveiling a hidden folding intermediate in c-type cytochomes by protein engineering. J Biol Chem 281:9331-9336. (Pubitemid 43864649)
45. Sinibaldi F, Piro MC, Howes BD, Smulevich G, Ascoli F, Santucci R (2003) Rupture of the hydrogen bond linking two Φ-loops induces the molten globule state at neutral pH in cytochrome c. Biochemistry 42:7604-7610. (Pubitemid 36735838)
46. Rosell FI, Mauk AG (2002) Spectroscopic properties of a mitochondrial cytochrome c with a single thioether bond to the heme prosthetic group. Biochemistry 41:7811-7818. (Pubitemid 34627808)
47. Kurchan EW (2005) Kinetics and thermodynamics in the denatured state of iso-1-cytochrome c, Ph.D. Thesis, University of Denver, Denver, CO.
48. Rumbley JN, Hoang L, Englander SW (2002) Recombinant equine cytochrome c in Escherichia coli: high-level expression, characterization, and folding and assembly mutants. Biochemistry 41:13894-13901. (Pubitemid 35364863)
49. Kurchan E, Roder H, Bowler BE (2005) Kinetics of loop formation and breakage in the denatured state of iso-1-cytochrome c. J Mol Biol 353:730-743. (Pubitemid 41414744)
50. Ebeling W, Hennrich N, Klockow M, Metz H, Orth HD, Lang H (1974) Proteinase K from Tritirachium album limber. Eur J Biochem 47:91-97.