Formation of oligomeric cytochrome c during folding by intermolecular hydrophobic interaction between N- and C-terminal α-helices

Biochemistry

Volumn 52, Issue 48, 2013, Pages 8732-8744

  Parui, Partha Pratim ^a,b   Deshpande, Megha Subhash ^a   Nagao, Satoshi ^a   Kamikubo, Hironari ^a   Komori, Hirofumi ^c,d   Higuchi, Yoshiki ^c,d   Kataoka, Mikio ^a   Hirota, Shun ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b JADAVPUR UNIVERSITY   (India)

^c UNIVERSITY OF HYOGO   (Japan)

^d RIKEN SPring 8 Center   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL REGIONS; GUANIDINE HYDROCHLORIDE; HYDROPHOBIC RESIDUES; INTERMOLECULAR HYDROPHOBIC INTERACTIONS; LIGAND EXCHANGES; LOW TEMPERATURES; OLIGOMERIC PROTEINS; PROTEIN CONCENTRATIONS;

HYDROPHOBICITY; PROTEINS;

OLIGOMERS;

CYTOCHROME C; DIMER; GLYCINE; GUANIDINE; HETERODIMER; LIGAND; OLIGOMER; OLIGOMERIC CYTOCHROME C; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIMERIZATION; HYDROPHOBICITY; LOW TEMPERATURE; MOLECULAR INTERACTION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE;

EID: 84889257382     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400986g     Document Type: Article

References (58)

1. Dickerson, R. E., Takano, T., Eisenberg, D., Kallai, O. B., Samson, L., Cooper, A., and Margoliash, E. (1971) Ferricytochrome c. I. General features of the horse and bonito proteins at 2.8 Å resolution J. Biol. Chem. 246, 1511-1535
2. Bushnell, G. W., Louie, G. V., and Brayer, G. D. (1990) High-resolution three-dimensional structure of horse heart cytochrome c J. Mol. Biol. 214, 585-595 (Pubitemid 20261984)
3. Banci, L., Bertini, I., Gray, H. B., Luchinat, C., Reddig, T., Rosato, A., and Turano, P. (1997) Solution structure of oxidized horse heart cytochrome c Biochemistry 36, 9867-9877 (Pubitemid 27364698)
4. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade Cell 91, 479-489 (Pubitemid 27508237)
5. Spierings, D., McStay, G., Saleh, M., Bender, C., Chipuk, J., Maurer, U., and Green, D. R. (2005) Connected to death: The (unexpurgated) mitochondrial pathway of apoptosis Science 310, 66-67 (Pubitemid 41434533)
6. Hirota, S., Hattori, Y., Nagao, S., Taketa, M., Komori, H., Kamikubo, H., Wang, Z., Takahashi, I., Negi, S., Sugiura, Y., Kataoka, M., and Higuchi, Y. (2010) Cytochrome c polymerization by successive domain swapping at the C-terminal helix Proc. Natl. Acad. Sci. U.S.A. 107, 12854-12859
7. Wang, Z., Matsuo, T., Nagao, S., and Hirota, S. (2011) Peroxidase activity enhancement of horse cytochrome c by dimerization Org. Biomol. Chem. 9, 4766-4769
8. Soffer, J. B., Fradkin, E., Pandiscia, L. A., and Schweitzer-Stenner, R. (2013) The (not completely irreversible) population of a misfolded state of cytochrome c under folding conditions Biochemistry 52, 1397-1408
9. Newcomer, M. E. (2002) Protein folding and three-dimensional domain swapping: A strained relationship? Curr. Opin. Struct. Biol. 12, 48-53 (Pubitemid 34142720)
10. Rousseau, F., Schymkowitz, J. W., and Itzhaki, L. S. (2003) The unfolding story of three-dimensional domain swapping Structure 11, 243-251 (Pubitemid 36287689)
11. Bennett, M. J., Sawaya, M. R., and Eisenberg, D. (2006) Deposition diseases and 3D domain swapping Structure 14, 811-824 (Pubitemid 43674098)
12. Gronenborn, A. M. (2009) Protein acrobatics in pairs: Dimerization via domain swapping Curr. Opin. Struct. Biol. 19, 39-49
13. Janowski, R., Kozak, M., Jankowska, E., Grzonka, Z., Grubb, A., Abrahamson, M., and Jaskolski, M. (2001) Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping Nat. Struct. Biol. 8, 316-320 (Pubitemid 32275015)
14. Staniforth, R. A., Giannini, S., Higgins, L. D., Conroy, M. J., Hounslow, A. M., Jerala, R., Craven, C. J., and Waltho, J. P. (2001) Three-dimensional domain swapping in the folded and molten-globule states of cystatins, an amyloid-forming structural superfamily EMBO J. 20, 4774-4781 (Pubitemid 32848630)
15. Knaus, K. J., Morillas, M., Swietnicki, W., Malone, M., Surewicz, W. K., and Yee, V. C. (2001) Crystal structure of the human prion protein reveals a mechanism for oligomerization Nat. Struct. Biol. 8, 770-774 (Pubitemid 32803594)
16. Guo, Z. and Eisenberg, D. (2006) Runaway domain swapping in amyloid-like fibrils of T7 endonuclease I Proc. Natl. Acad. Sci. U.S.A. 103, 8042-8047 (Pubitemid 43801049)
17. 2- Microglobulin forms three-dimensional domain-swapped amyloid fibrils with disulfide linkages Nat. Struct. Mol. Biol. 18, 49-55
18. Liu, Y., Gotte, G., Libonati, M., and Eisenberg, D. (2001) A domain-swapped RNase A dimer with implications for amyloid formation Nat. Struct. Biol. 8, 211-214 (Pubitemid 32180044)
19. Liu, Y., Gotte, G., Libonati, M., and Eisenberg, D. (2002) Structures of the two 3D domain-swapped RNase A trimers Protein Sci. 11, 371-380 (Pubitemid 34075800)
20. Liu, Y., Hart, P. J., Schlunegger, M. P., and Eisenberg, D. (1998) The crystal structure of a 3D domain-swapped dimer of RNase A at a 2.1-Å resolution Proc. Natl. Acad. Sci. U.S.A. 95, 3437-3442
21. Gotte, G., Vottariello, F., and Libonati, M. (2003) Thermal aggregation of ribonuclease A. A contribution to the understanding of the role of 3D domain swapping in protein aggregation J. Biol. Chem. 278, 10763-10769 (Pubitemid 36800348)
22. López-Alonso, J. P., Bruix, M., Font, J., Ribó, M., Vilanova, M., Rico, M., Gotte, G., Libonati, M., González, C., and Laurents, D. V. (2006) Formation, structure, and dissociation of the ribonuclease S three-dimensional domain-swapped dimer J. Biol. Chem. 281, 9400-9406 (Pubitemid 43864656)
23. López-Alonso, J. P., Bruix, M., Font, J., Ribó, M., Vilanova, M., Jiménez, M. A., Santoro, J., González, C., and Laurents, D. V. (2010) NMR spectroscopy reveals that RNase A is chiefly denatured in 40% acetic acid: Implications for oligomer formation by 3D domain swapping J. Am. Chem. Soc. 132, 1621-1630
24. Jerala, R. and Žerovnik, E. (1999) Accessing the global minimum conformation of stefin A dimer by annealing under partially denaturing conditions J. Mol. Biol. 291, 1079-1089 (Pubitemid 29423771)
25. Rousseau, F., Schymkowitz, J. W., Wilkinson, H. R., and Itzhaki, L. S. (2001) Three-dimensional domain swapping in p13suc1 occurs in the unfolded state and is controlled by conserved proline residues Proc. Natl. Acad. Sci. U.S.A. 98, 5596-5601 (Pubitemid 32435687)
26. 1H-NMR study of the Cyanovirin-N protein J. Am. Chem. Soc. 134, 4229-4235
27. Zegers, I., Deswarte, J., and Wyns, L. (1999) Trimeric domain-swapped barnase Proc. Natl. Acad. Sci. U.S.A. 96, 818-822 (Pubitemid 29072141)
28. Koharudin, L. M., Liu, L., and Gronenborn, A. M. (2013) Different 3D domain-swapped oligomeric cyanovirin-N structures suggest trapped folding intermediates Proc. Natl. Acad. Sci. U.S.A. 110, 7702-7707
29. Nagao, S., Osuka, H., Yamada, T., Uni, T., Shomura, Y., Imai, K., Higuchi, Y., and Hirota, S. (2012) Structural and oxygen binding properties of dimeric horse myoglobin Dalton Trans. 41, 11378-11385
30. Wu, L. C., Laub, P. B., Elove, G. A., Carey, J., and Roder, H. (1993) A noncovalent peptide complex as a model for an early folding intermediate of cytochrome c Biochemistry 32, 10271-10276 (Pubitemid 23312460)
31. Bai, Y., Sosnick, T. R., Mayne, L., and Englander, S. W. (1995) Protein folding intermediates: Native-state hydrogen exchange Science 269, 192-197
32. Colón, W., Elöve, G. A., Wakem, L. P., Sherman, F., and Roder, H. (1996) Side chain packing of the N- and C-terminal helices plays a critical role in the kinetics of cytochrome c folding Biochemistry 35, 5538-5549 (Pubitemid 26136531)
33. Shastry, M. C. and Roder, H. (1998) Evidence for barrier-limited protein folding kinetics on the microsecond time scale Nat. Struct. Biol. 5, 385-392 (Pubitemid 28211177)
34. Elöve, G. A., Bhuyan, A. K., and Roder, H. (1994) Kinetic mechanism of cytochrome c folding: Involvement of the heme and its ligands Biochemistry 33, 6925-6935 (Pubitemid 24190817)
35. Takahashi, S., Yeh, S. R., Das, T. K., Chan, C. K., Gottfried, D. S., and Rousseau, D. L. (1997) Folding of cytochrome c initiated by submillisecond mixing Nat. Struct. Biol. 4, 44-50 (Pubitemid 27020924)
36. Yeh, S. R., Takahashi, S., Fan, B., and Rousseau, D. L. (1997) Ligand exchange during cytochrome c folding Nat. Struct. Biol. 4, 51-56 (Pubitemid 27020925)
37. Yeh, S. R., Han, S. W., and Rousseau, D. L. (1998) Cytochrome c folding and unfolding: A biphasic mechanism Acc. Chem. Res. 31, 727-736 (Pubitemid 128474539)
38. Elöve, G. A., Chaffotte, A. F., Roder, H., and Goldberg, M. E. (1992) Early steps in cytochrome c folding probed by time-resolved circular dichroism and fluorescence spectroscopy Biochemistry 31, 6876-6883
39. Segel, D. J., Eliezer, D., Uversky, V., Fink, A. L., Hodgson, K. O., and Doniach, S. (1999) Transient dimer in the refolding kinetics of cytochrome c characterized by small-angle X-ray scattering Biochemistry 38, 15352-15359 (Pubitemid 129520369)
40. Pollock, W. B., Rosell, F. I., Twitchett, M. B., Dumont, M. E., and Mauk, A. G. (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 (Pubitemid 28196769)
41. Wang, Z. H., Lin, Y. W., Rosell, F. I., Ni, F. Y., Lu, H. J., Yang, P. Y., Tan, X. S., Li, X. Y., Huang, Z. X., and Mauk, A. G. (2007) Converting cytochrome c into a peroxidase-like metalloenzyme by molecular design ChemBioChem 8, 607-609 (Pubitemid 47194849)
42. Dente, L. and Cortese, R. (1987) pEMBL: A new family of single-stranded plasmids for sequencing DNA Methods Enzymol. 155, 111-119
43. Berry, E. A. and Trumpower, B. L. (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra Anal. Biochem. 161, 1-15
44. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25, 495-503 (Pubitemid 23564996)
45. Svergun, D. I., Petoukhov, M. V., and Koch, M. H. (2001) Determination of domain structure of proteins from X-ray solution scattering Biophys. J. 80, 2946-2953 (Pubitemid 32521666)
46. 552 dimer Biochemistry 51, 8608-8616
47. Maity, H., Maity, M., and Englander, S. W. (2004) How cytochrome c folds, and why: Submolecular foldon units and their stepwise sequential stabilization J. Mol. Biol. 343, 223-233 (Pubitemid 39277460)
48. Pletneva, E. V., Gray, H. B., and Winkler, J. R. (2005) Many faces of the unfolded state: Conformational heterogeneity in denatured yeast cytochrome c J. Mol. Biol. 345, 855-867 (Pubitemid 39600938)
49. Pletneva, E. V., Gray, H. B., and Winkler, J. R. (2005) Snapshots of cytochrome c folding Proc. Natl. Acad. Sci. U.S.A. 102, 18397-18402 (Pubitemid 43011237)
50. Liptak, M. D., Fagerlund, R. D., Ledgerwood, E. C., Wilbanks, S. M., and Bren, K. L. (2011) The proapoptotic G41S mutation to human cytochrome c alters the heme electronic structure and increases the electron self-exchange rate J. Am. Chem. Soc. 133, 1153-1155
51. Pascher, T., Chesick, J. P., Winkler, J. R., and Gray, H. B. (1996) Protein folding triggered by electron transfer Science 271, 1558-1560
52. Okuno, T., Hirota, S., and Yamauchi, O. (2000) Folding character of cytochrome c studied by o -nitrobenzyl modification of methionine 65 and subsequent ultraviolet light irradiation Biochemistry 39, 7538-7545 (Pubitemid 30422072)
53. Nawrocki, J. P., Chu, R. A., Pannell, L. K., and Bai, Y. (1999) Intermolecular aggregations are responsible for the slow kinetics observed in the folding of cytochrome c at neutral pH J. Mol. Biol. 293, 991-995
54. Lu, Y., Casimiro, D. R., Bren, K. L., Richards, J. H., and Gray, H. B. (1993) Structurally engineered cytochromes with unusual ligand-binding properties: Expression of Saccharomyces cerevisiae Met-80 → Ala iso-1-cytochrome c Proc. Natl. Acad. Sci. U.S.A. 90, 11456-11459 (Pubitemid 24008657)
55. Bren, K. L. and Gray, H. B. (1993) Structurally engineered cytochromes with novel ligand-binding sites: Oxy and carbonmonoxy derivatives of semisynthetic horse heart Ala80 cvytochrome c J. Am. Chem. Soc. 115, 10382-10383
56. Silkstone, G. G., Cooper, C. E., Svistunenko, D., and Wilson, M. T. (2005) EPR and optical spectroscopic studies of Met80X mutants of yeast ferricytochrome c. Models for intermediates in the alkaline transition J. Am. Chem. Soc. 127, 92-99 (Pubitemid 40094373)
57. Behera, R. K., Nakajima, H., Rajbongshi, J., Watanabe, Y., and Mazumdar, S. (2013) Thermodynamic effects of the alteration of the axial ligand on the unfolding of thermostable cytochrome c Biochemistry 52, 1373-1384
58. Tzul, F. O., Kurchan, E., Roder, H., and Bowler, B. E. (2009) Competition between reversible aggregation and loop formation in denatured iso-1-cytochrome c Biochemistry 48, 481-491