Mutation of trimethyllysine 72 to alanine enhances his79-heme-mediated dynamics of iso-1-cytochrome c

Biochemistry

Volumn 52, Issue 5, 2013, Pages 837-846

  Cherney, Melisa M ^a,b   Junior, Carolyn C ^a   Bowler, Bruce E ^a  

^a UNIVERSITY OF MONTANA   (United States)

^b UNIVERSITY OF NORTHERN IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE TRANSITION; CONFORMATIONAL CHANGE; CYTOCHROME C; GLOBAL STABILITY; GUANIDINE HYDROCHLORIDE; ISO-1-CYTOCHROME; KINETIC STUDY; NEAR-NEUTRAL PH; PEROXIDASE ACTIVITIES; PH-JUMP;

ALKALINITY; AMINO ACIDS; CELL DEATH; DYNAMICS; THERMODYNAMICS;

PORPHYRINS;

ALANINE; CYTOCHROME C; GUANIDINE; HEME; ISO 1CYTOCHROME C; LYSINE DERIVATIVE; TRIMETHYLLYSINE 72; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DENATURATION; DYNAMICS; MUTATION; PH; PRIORITY JOURNAL; THERMODYNAMICS;

ALANINE; AMINO ACID SUBSTITUTION; CYTOCHROMES C; HEME; HYDROGEN-ION CONCENTRATION; KINETICS; LYSINE; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; THERMODYNAMICS;

EID: 84873388601     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301599g     Document Type: Article

References (65)

1. Haber, E. and Anfinsen, C. B. (1962) Side-chain interactions governing the pairing of half-cystine residues in ribonuclease J. Biol. Chem. 237, 1839-1844
2. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains Science 181, 223-230
3. Henzler-Wildman, K. and Kern, D. (2007) Dynamic personalities of proteins Nature 450, 964-972 (Pubitemid 350273626)
4. Lang, P. T., Ng, H.-L., Fraser, J. S., Corn, J. E., Echols, N., Sales, M., Holton, J. M., and Alber, T. (2010) Automated electron-density sampling reveals widespread conformation polymorphism in proteins Protein Sci. 19, 1420-1431
5. Eisenmesser, E. Z., Millet, O., Labeikovsky, W., Korzhnev, D. M., Wolf-Watz, M., Bosco, D. A., Skalicky, J. J., Kay, L. E., and Kern, D. (2005) Intrinsic dynamics of an enzyme underlies catalysis Nature 438, 117-121 (Pubitemid 41599831)
6. Fraser, J. S., Clarkson, M. W., Degnan, S. C., Erion, R., Kern, D., and Alber, T. (2009) Hidden alternative structures of proline isomerase essential for catalysis Nature 462, 669-673
7. Bouvignies, G., Vallurupalli, P., Hansen, D. F., Correia, B. E., Lange, O., Bah, A., Vernon, R. M., Dahlquist, F. W., Baker, D., and Kay, L. E. (2011) Solution structure of a minor and transiently formed state of a T4 lysozyme mutant Nature 477, 111-114
8. Henzler-Wildman, K. A., Thai, V., Lei, M., Ott, M., Wolf-Watz, M., Fenn, T., Pozharski, E., Wilson, M. A., Petsko, G. A., Karplus, M., Huebner, C. G., and Kern, D. (2007) Intrinsic motions along an enzymatic reaction trajectory Nature 450, 838-844 (Pubitemid 350231334)
9. Wilson, M. T. and Greenwood, C. (1996) The alkaline transition in ferricytochrome c. In Cytochrome c: A Multidisciplinary Approach (Scott, R. A. and Mauk, A. G., Eds.) pp 611-634, University Science Books, Sausalito, CA.
10. Cherney, M. M. and Bowler, B. E. (2011) Protein dynamics and function: Making new strides with an old warhorse, the alkaline conformational transition of cytochrome c Coord. Chem. Rev. 255, 664-677
11. Rosell, F. I., Ferrer, J. C., and Mauk, A. G. (1998) Proton-linked protein conformational switching: Definition of the alkaline conformational transition of yeast iso-1-ferricytochrome c J. Am. Chem. Soc. 120, 11234-11245 (Pubitemid 28531064)
12. Assfalg, M., Bertini, I., Dolfi, A., Turano, P., Mauk, A. G., Rosell, F. I., and Gray, H. B. (2003) Structural model for an alkaline form of ferricytochrome c J. Am. Chem. Soc. 125, 2913-2922 (Pubitemid 36512516)
13. Kristinsson, R. and Bowler, B. E. (2005) Communication of stabilizing energy between substructures of a protein Biochemistry 44, 2349-2359 (Pubitemid 40279539)
14. Nelson, C. J. and Bowler, B. E. (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
15. Ow, Y. P., Green, D. R., Hao, Z., and Mak, T. W. (2008) Cytochrome c: Functions beyond respiration Nat. Rev. Mol. Cell Biol. 9, 532-542 (Pubitemid 351881842)
16. Yu, T., Wang, X., Purring-Koch, C., Wei, Y., and McLendon, G. L. (2001) A mutational epitope for cytochrome c binding to the apoptosis protease activation factor-1 J. Biol. Chem. 276, 13034-13038
17. Olteanu, A., Patel, C. N., Dedmon, M. M., Kennedy, S., Linhoff, M. W., Minder, C. M., Potts, P. R., Deshmukh, M., and Pielak, G. J. (2003) Stability and apoptotic activity of recombinant human cytochrome c Biochem. Biophys. Res. Commun. 312, 733-740 (Pubitemid 37468232)
18. Kluck, R. M., Martin, S. J., Hoffman, B. M., Zhou, J. S., Green, D. R., and Newmeyer, D. D. (1997) Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system EMBO J. 16, 4639-4649 (Pubitemid 27326601)
19. Ellerby, H. M., Martin, S. J., Ellerby, L. M., Naiem, S. S., Rabizadeh, S., Salvesen, G. S., Casiano, C. A., Cashman, N. R., Green, D. R., and Bredesen, D. E. (1997) Establishment of a cell-free system of neuronal apoptosis: Comparison of premitochondrial, mitochondrial, and postmitochondrial phases J. Neurosci. 17, 6165-6178 (Pubitemid 27329892)
20. Kluck, R. M., Ellerby, L. M., Ellerby, H. M., Naiem, S., Yaffe, M. P., Margoliash, E., Bredesen, D., Mauk, A. G., Sherman, F., and Newmeyer, D. D. (2000) Determinants of cytochrome c pro-apoptotic activity. The role of lysine 72 trimethylation J. Biol. Chem. 275, 16127-16133 (Pubitemid 30366922)
21. Kagan, V. E., Tyurin, V. A., Jiang, J., Tyurina, Y. Y., Ritov, V. B., Amoscato, A. A., Osipov, A. N., Belikova, N. A., Kapralov, A. A., Kini, V., Vlasova, I. I., Zhao, Q., Zou, M., Di, P., Svistunenko, D. A., Kurnikov, I. V., and Borisenko, G. G. (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors Nat. Chem. Biol. 1, 223-232
22. Kapetanaki, S. M., Silkstone, G., Husu, I., Liebl, U., Wilson, M. T., and Vos, M. H. (2009) Interaction of carbon monoxide with the apoptosis-inducing cytochrome c -cardiolipin complex Biochemistry 48, 1613-1619
23. Silkstone, G., Kapetanaki, S. M., Husu, I., Vos, M. H., and Wilson, M. T. (2012) Nitric oxide binding to the cardiolipin complex of ferric cytochrome c Biochemistry 51, 6760-6766
24. Bradley, J. M., Silkstone, G., Wilson, M. T., Cheesman, M. R., and Butt, J. N. (2011) Probing a complex of cytochrome c and cardiolipin by magnetic circular dichroism spectroscopy: Implications for the initial events in apoptosis J. Am. Chem. Soc. 133, 19676-19679
25. Jemmerson, R., Liu, J., Hausauer, D., Lam, K. P., Mondino, A., and Nelson, R. D. (1999) 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, 3599-3609
26. Diederix, R. E. M., Ubbink, M., and Canters, G. W. (2002) Peroxidase activity as a tool for studying the folding of c-type cytochromes Biochemistry 41, 13067-13077 (Pubitemid 35215792)
27. Berghuis, A. M. and Brayer, G. D. (1992) Oxidation state-dependent conformational changes in cytochrome c J. Mol. Biol. 223, 959-976
28. 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)
29. Bandi, S., Baddam, S., and Bowler, B. E. (2007) Alkaline conformational transition and gated electron transfer with a Lys 79 → His variant of iso-1-cytochrome c Biochemistry 46, 10643-10654 (Pubitemid 47417257)
30. Duncan, M. G., Williams, M. D., and Bowler, B. E. (2009) Compressing the free energy range of substructure stabilities in iso-1-cytochrome c Protein Sci. 18, 1155-1164
31. Rosell, F. I. and Mauk, A. G. (2002) Spectroscopic properties of a mitochondrial cytochrome c with a single thioether bond to the heme prosthetic group Biochemistry 41, 7811-7818 (Pubitemid 34627808)
32. Rumbley, J. N., Hoang, L., and Englander, S. W. (2002) Recombinant equine cytochrome c in Escherichia coli: High-level expression, characterization, and folding and assembly mutants Biochemistry 41, 13894-13901 (Pubitemid 35364863)
33. Kurchan, E., Roder, H., and Bowler, B. E. (2005) Kinetics of loop formation and breakage in the denatured state of iso-1-cytochrome c J. Mol. Biol. 353, 730-743 (Pubitemid 41414744)
34. Wandschneider, E., Hammack, B. N., and Bowler, B. E. (2003) Evaluation of cooperative interactions between substructures of iso-1-cytochrome c using double mutant cycles Biochemistry 42, 10659-10666 (Pubitemid 37102105)
35. Redzic, J. S. and Bowler, B. E. (2005) Role of hydrogen bond networks and dynamics in positive and negative cooperative stabilization of a protein Biochemistry 44, 2900-2908 (Pubitemid 40293664)
36. Santoro, M. M. and Bolen, D. W. (1992) A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range Biochemistry 31, 4901-4907
37. Hagihara, Y., Tan, Y., and Goto, Y. (1994) Comparison of the conformational stability of the molten globule and native states of horse cytochrome c J. Mol. Biol. 237, 336-348
38. Godbole, S., Hammack, B., and Bowler, B. E. (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
39. Moore, G. R. and Pettigrew, G. W. (1990) Cytochromes c: Evolutionary, Structural and Physicochemical Aspects, Springer-Verlag, New York.
40. Baddam, S. and Bowler, B. E. (2005) Thermodynamics and kinetics of formation of the alkaline state of a Lys 79→Ala/Lys 73→His variant of iso-1-cytochrome c Biochemistry 44, 14956-14968 (Pubitemid 41612274)
41. Margoliash, E. and Frohwirt, N. (1959) Spectrum of horse-heart cytochrome c Biochem. J. 71, 570-572
42. Battistuzzi, G., Borsari, M., De Rienzo, F., Di Rocco, G., Ranieri, A., and Sola, M. (2007) Free energy of transition for the individual alkaline conformers of yeast iso-1-cytochrome c Biochemistry 46, 1694-1702
43. Hammack, B. N., Smith, C. R., and Bowler, B. E. (2001) Denatured state thermodynamics: Residual structure, chain stiffness and scaling factors J. Mol. Biol. 311, 1091-1104 (Pubitemid 32803723)
44. Betz, S. F. and Pielak, G. J. (1992) Introduction of a disulfide bond into cytochrome c stabilizes a compact denatured state Biochemistry 31, 12337-12344 (Pubitemid 23163108)
45. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding Protein Sci. 4, 2138-2148
46. Bandi, S. and Bowler, B. E. (2013) A cytochrome c electron transfer switch modulated by heme ligation and isomerization of a peptidyl-prolyl bond Biopolymers DOI: 10.1002/bip.22164
47. Bandi, S. and Bowler, B. E. (2011) Probing the dynamics of a His73-heme alkaline conformer in a destabilized variant of yeast iso-1-cytochrome c with conformationally gated electron transfer methods Biochemistry 50, 10027-10040
48. Bandi, S. and Bowler, B. E. (2008) Probing the bottom of a folding funnel using conformationally gated electron transfer reactions J. Am. Chem. Soc. 130, 7540-7541 (Pubitemid 351842106)
49. Baddam, S. and Bowler, B. E. (2006) Tuning the rate and pH accessibility of a conformational electron transfer gate Inorg. Chem. 45, 6338-6346
50. Baddam, S. and Bowler, B. E. (2005) Conformationally gated electron transfer in iso-1-cytochrome c: Engineering the rate of a conformational switch J. Am. Chem. Soc. 127, 9702-9703 (Pubitemid 40981531)
51. Martinez, R. E. and Bowler, B. E. (2004) Proton-mediated dynamics of the alkaline conformational transition of yeast iso-1-cytochrome c J. Am. Chem. Soc. 126, 6751-6758 (Pubitemid 38697374)
52. Nelson, C. J., LaConte, M. J., and Bowler, B. E. (2001) Direct detection of heat and cold denaturation for partial unfolding of a protein J. Am. Chem. Soc. 123, 7453-7454 (Pubitemid 32879475)
53. Godbole, S. and Bowler, B. E. (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)
54. Godbole, S., Dong, A., Garbin, K., and Bowler, B. E. (1997) A lysine 73 → histidine variant of yeast iso-1-cytochrome c: Evidence for a native-like intermediate in the unfolding pathway and implications for m value effects Biochemistry 36, 119-126 (Pubitemid 27024685)
55. Davis, L. A., Schejter, A., and Hess, G. P. (1974) Alkaline isomerization of oxidized cytochrome c. Equilibrium and kinetic measurements J. Biol. Chem. 249, 2624-2632
56. Baddam, S. and Bowler, B. E. (2006) Mutation of asparagine 52 to glycine promotes the alkaline form of iso-1-cytochrome c and causes loss of cooperativity in acid unfolding Biochemistry 45, 4611-4619
57. Myer, Y. P., MacDonald, L. H., Verma, B. C., and Pande, A. (1980) Urea denaturation of horse heart ferricytochrome c. Equilibrium studies and characterization of intermediate forms Biochemistry 19, 199-207
58. Angström, J., Moore, G. R., and Williams, R. J. P. (1982) The magnetic-susceptibility of ferricytochrome c Biochim. Biophys. Acta 703, 87-94
59. Shah, R. and Schweitzer-Stenner, R. (2008) Structural changes of horse heart ferricytochrome c induced by changes of ionic strength and anion binding Biochemistry 47, 5250-5257 (Pubitemid 351620762)
60. Hagarman, A., Duitch, L., and Schweitzer-Stenner, R. (2008) The conformational manifold of ferricytochrome c explored by visible and far-UV electronic circular dichroism spectroscopy Biochemistry 47, 9667-9677
61. Robinson, M. N., Boswell, A. P., Huang, Z.-X., Eley, C. G. S., and Moore, G. R. (1983) The conformation of eukaryotic cytochrome c around residues 39, 57, 59 and 74 Biochem. J. 213, 687-700
62. Weinkam, P., Zimmermann, J., Sagle, L. B., Matsuda, S., Dawson, P. E., Wolynes, P. G., and Romesberg, F. E. (2008) Characterization of alkaline transitions in ferricytochrome c using carbon-deuterium infrared probes Biochemistry 47, 13470-13480
63. Verbaro, D., Hagarman, A., Soffer, J., and Schweitzer-Stenner, R. (2009) The pH dependence of the 695 nm charge transfer band reveals the population of an intermediate state of the alkaline transition of ferricytochrome c at low ion concentrations Biochemistry 48, 2990-2996
64. Sanchez, R. and Zhou, M.-M. (2011) The PHD finger: A versatile epigenomic reader Trends Biochem. Sci. 36, 364-372
65. Daze, K. D. and Hof, F. (2013) The cation-π interaction at protein-protein interaction interfaces: Developing and learning from synthetic mimics of protein that bind methylated lysines Acc. Chem. Res. DOI: 10.1021/ar300072g