Autoxidation of Reduced Horse Heart Cytochrome c Catalyzed by Cardiolipin-Containing Membranes

Journal of Physical Chemistry B

Volumn 120, Issue 48, 2016, Pages 12219-12231

  Serpas, Lee ^a   Milorey, Bridget ^a   Pandiscia, Leah A ^a   Addison, Anthony W ^a   Schweitzer Stenner, Reinhard ^a  

^a DREXEL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCULAR DICHROISM SPECTROSCOPY; DICHROISM; FLUORESCENCE SPECTROSCOPY; LIPOSOMES; OXIDATION; PHOSPHOLIPIDS; QUANTUM THEORY; REACTION INTERMEDIATES; SODIUM CHLORIDE; SPIN DYNAMICS;

ACTIVATION BARRIERS; AEROBIC ENVIRONMENTS; ANAEROBIC CONDITIONS; CONFORMATIONAL CHANGE; CONFORMATIONAL TRANSITIONS; LIPID CONCENTRATION; MEMBRANE-BOUND PROTEINS; OXIDIZED CYTOCHROME;

PROTEINS;

CARDIOLIPIN; CYTOCHROME C; LIPOSOME;

ANIMAL; BIOCATALYSIS; CHEMISTRY; HEART; HORSE; METABOLISM; OXIDATION REDUCTION REACTION;

ANIMALS; BIOCATALYSIS; CARDIOLIPINS; CYTOCHROMES C; HEART; HORSES; LIPOSOMES; OXIDATION-REDUCTION;

EID: 85017025426     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.6b05620     Document Type: Article

References (77)

1. Adman, E. T. A comparison of the structures of electron transfer proteins Biochim. Biophys. Acta 1979, 549, 107-144 10.1016/0304-4173(79)90012-0
2. Colón, W.; Elöve, G. A.; Waken, L. P.; Sherman, F.; Roder, H. Side Chain Packing of the N-and C-Terminal Helices Plays a Critical Role in the Kinetics of Cytochrome c Folding Biochemistry 1996, 35, 5538-5549 10.1021/bi960052u
3. Jiang, X.; Wang, X. Cytochrome c-Mediated Apoptosis Annu. Rev. Biochem. 2004, 73, 87-106 10.1146/annurev.biochem.73.011303.073706
4. Ott, M.; Robertson, J. D.; Gogvadze, V.; Zhivotovsky, B.; Orrenius, S. Cytochrome c release from mitochrondria proceed by a two-step process Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 1259-1263 10.1073/pnas.241655498
5. Vincent, J. S.; Kon, H.; Levin, I. W. Low-Temperature Electron Paramagnetic Resonance Study of the Ferricytochrome c-Cardiolipin Complex Biochemistry 1987, 26, 2312-2314 10.1021/bi00382a036
6. Rytömaa, M.; Mustonen, P.; Kinnunen, P. K. J. Reversible, Nonionic and pH-dependent Association of Cytochrome c with Cardiolipin-Phosphatidylcholine Liposomes J. Biol. Chem. 1992, 267, 22243-22248
7. Rietveld, A.; Dijens, P.; Verkleij, J.; de Kruiff, B. Interaction of cytochrome c and its precursor apocytochrome c with various phospholipids EMBO J. 1983, 2, 907-913
8. Rytömaa, M.; Kinnunen, P. K. J. Evidence for two Distinct Acidic Phospholipid-binding Sites in Cytochrome c J. Biol. Chem. 1994, 269, 1770-1774
9. Tuominen, E. K. J.; Zhu, K.; Wallace, C. J. A.; Clark-Lewis, I.; Craig, D. B.; Rytömaa, M.; Kinnunen, P. K. J. ATP Induces a Conformational Change in Lipid-bound Cytochrome c J. Biol. Chem. 2001, 276, 19356-19362 10.1074/jbc.M100853200
10. Tuominen, E. K. J.; Wallace, C. J. A.; Kinnunen, P. K. J. Phospholipid-Cytochrome c Interaction J. Biol. Chem. 2002, 277, 8822 10.1074/jbc.M200056200
11. Gorbenko, G. P.; Molotkovsky, J. G.; Kinnunen, P. K. J. Cytochrome c Interaction with Cardiolipin/Phosphatidylcholine Model Membranes: Effect of Cardiolipin Protonation Biophys. J. 2006, 90, 4093 10.1529/biophysj.105.080150
12. Kawai, C.; Prado, F. M.; Nunes, G. I. C.; Mascio, P. D.; Carmona-Ribeiro, A. M.; Nantes, I. L. pH Dependent Interactions of Cytochrome c with Mitochondrial mimetic Membranes. The Role of An Array of Positively Charged Amino Acids J. Biol. Chem. 2005, 280 434709 10.1074/jbc.M412532200
13. Kawai, C.; Ferreira, J. C.; Baptista, M. S.; Nantes, I. L. Not Only Oxidation of Cardiolipin Affects the Affinity of Cytochrome c for Lipid Bilayers J. Phys. Chem. B 2014, 118, 11863-11872 10.1021/jp504518g
14. Hong, Y.; Muenzner, J.; Grimm, S. K.; Pletneva, E. V. Origin of the Conformational Heterogeneity of Cardiolipin-Bound Cytochrome c J. Am. Chem. Soc. 2012, 134, 18713-18723 10.1021/ja307426k
15. Hanske, J.; Toffey, J. R.; Morenz, A. M.; Bonilla, A. J.; Schiavoni, K. H.; Pletneva, E. V. Conformational properties of cardiolipin-bound cytochrome c Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 125-130 10.1073/pnas.1112312108
16. Sinibaldi, F.; Fiorucci, L.; Patriarca, A.; Lauceri, R.; Ferri, T.; Coletta, M.; Santucci, R. Insights into Cytochrome c-Cardiolipin Interaction. Role Played by Ionic Strength Biochemistry 2008, 47, 6928-6935 10.1021/bi800048v
17. Patriarca, A.; Eliseo, T.; Sinibaldi, F.; Piro, M. C.; Melis, R.; Paci, M.; Cicero, D. O.; Polticelli, F.; Santucci, R.; Fiorucci, L. ATP Acts as a Regulatory Effector in Modulating Structural Transitions of Cytochrome c: Implications for Apoptotic Activity Biochemistry 2009, 48, 3279-3287 10.1021/bi801837e
18. Sinibaldi, F.; Howes, B. D.; Droghetto, E.; Polticelli, F.; Piro, M. C.; Pierro, D. D.; Fiorucci, L.; Coletta, M.; Smulevich, G.; Santucci, R. Role of Lysines in Cytochrome c-Cardiolipin Interaction Biochemistry 2013, 52, 4578-4588 10.1021/bi400324c
19. Pandiscia, L. A.; Schweitzer-Stenner, R. Salt as a Catalyst in the Mitochondria: Returning Cytochrome c to its Native State after it Misfolds on the Surface of Cardiolipin Containing Membranes Chem. Commun. 2014, 50, 3674-3676 10.1039/c3cc48709a
20. Pandiscia, L. A.; Schweitzer-Stenner, R. Coexistence of native-like and Non-native partially Unfolded Ferricytpchrome c on the Surface of Cardiolipin-Containing Liposomes J. Phys. Chem. B 2015, 119, 1334-1349 10.1021/jp5104752
21. Pandiscia, L. A.; Schweitzer-Stenner, R. Coexistence of Native-Like and Non-Native Cytochrome c on Anionic Liposomes with Different Cardiolipin Content J. Phys. Chem. B 2015, 119, 12846-59 10.1021/acs.jpcb.5b07328
22. Kagan, V. E.; Tyurin, V. A.; Jiang, J.; Tyurin, V. A.; Ritov, V. B.; Amoscato, A.; Osipov, A. N.; Belikova, N. A.; Kapralov, A. A.; Kini, V. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors Nat. Chem. Biol. 2005, 1, 223-232 10.1038/nchembio727
23. Amacher, J. F.; Zhong, F.; Lisi, G. P.; Zhu, M. Q.; Alden, S. L.; Hoke, K. R.; Madden, D. R.; Pletneva, E. V. A Compact Structure of Cytochrome c Trapped in a Lysine-Ligated State: Loop Refolding and Functional Implications of a Conformational Switch J. Am. Chem. Soc. 2015, 137, 8435-49 10.1021/jacs.5b01493
24. Döpner, S.; Hildebrandt, P.; Rosell, F. I.; Mauk, A. G. The alkaline conformational transitions of ferricytochrome c studied by resonance Raman spectroscopy J. Am. Chem. Soc. 1998, 120, 11246-11255 10.1021/ja9717572
25. Barker, P. D.; Mauk, A. G. pH-Linked conformational regulation of a metalloprotein oxidation-reduction equilibrium: electrochemical analysis of the alkaline form of cytochrome c J. Am. Chem. Soc. 1992, 114, 3619-3624 10.1021/ja00036a006
26. Dyson, H. J.; Beattle, J. K. Spin state and unfolding equilibria of ferri-cytochrome c in acidic solution J. Biol. Chem. 1982, 257, 2267-2273
27. Elöve, G. A.; Bhuyan, A. K.; Roder, H. Kinetic Mechanism of Cytochrome c Folding: Involvement of the Heme and Its Ligands Biochemistry 1994, 33, 6925-6935 10.1021/bi00188a023
28. Colón, W.; Roder, H. Kinetic intermediates in the formation of the cytochrome c molten globule Nat. Struct. Biol. 1996, 3, 1019-1025 10.1038/nsb1296-1019
29. Verbaro, D.; Hagarman, A.; Soffer, J.; Schweitzer-Stenner, R. 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 2009, 48, 2990-2996 10.1021/bi802208f
30. Hanske, J.; Toffey, J. R.; Morenz, A. M.; Bonilla, A. J.; Schiavoni, K. H.; Pletneva, E. V. Conformational properties of cardiolipin-bound cytochrome c Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 125-30 10.1073/pnas.1112312108
31. Iwase, H.; Takatori, T.; Nagao, M.; Iwadate, K.; Nakajima, M. Monoexpoxide Production from Linoleic Acid by Cytochrome c in the Presence of Cardiolipin Biochem. Biophys. Res. Commun. 1996, 222, 83-89 10.1006/bbrc.1996.0701
32. Nantes, I. L.; Zucchi, M. R.; Nascimento, O. R.; Faljoni-Alario, A. Effect of heme Iron Valence State on the Conformation of Cytochrome c and its Association with Membrane Interfaces J. Biol. Chem. 2001, 276, 153-158 10.1074/jbc.M006338200
33. Droghetti, E.; Oellerich, S.; Hildebrandt, P.; Smulevich, G. Heme Coordination States of Unfolded Ferrous Cytochrome c Biophys. J. 2006, 91, 3022-3031 10.1529/biophysj.105.079749
34. Kalanxhi, E.; Wallace, C. J. A. Cytochrome c impaled: investigation of the extended lipid anchorage of a soluble protein to mitochondrial membrane models Biochem. J. 2007, 407, 179-187 10.1042/BJ20070459
35. Kapetanaki, S. M.; Silkstone, G.; Husu, I.; Liebl, U.; Wilson, M. T.; Vos, M. H. Interaction of Carbon Monoxide with the Apoptosis-Inducing Cytochrome c-Cardiolipin Complex Biochemistry 2009, 48, 1613-1610 10.1021/bi801817v
36. Cortese, J. D.; Voglino, A. L.; Hackenbrock, C. R. Multiple Conformations of Physiological Membrane-Bound Cytochrome c Biochemistry 1998, 37, 6402-6409 10.1021/bi9730543
37. Basova, L. V.; Kurnikov, I. V.; Wang, L.; Ritov, V. B.; Belikova, N. A.; Vlasova, I. I.; Pacheco, A. A.; Winnica, D. E.; Peterson, J.; Bayir, H. Cardiolipin Switch in Mitochondria: shutting off the Reduction of Cytochrome c and Turning on the Peroxidase Activity Biochemistry 2007, 46, 3423-3434 10.1021/bi061854k
38. Varhač, R.; Antalik, M.; Baro, M. Effect of temperature and guanidine hydrochloride on ferrocytochrome c at neutral pH JBIC, J. Biol. Inorg. Chem. 2004, 9, 12-22 10.1007/s00775-003-0492-1
39. Jentzen, W.; Unger, E.; Karvounis, G.; Shelnutt, J. A.; Dreybrodt, W.; Schweitzer-Stenner, R. Conformational Properties of Nickel(II) Octaethylporphyrin in Solution. 1. Resonance Excitation Profiles and Temperature Dependence of Structure-Sensitive Raman Lines J. Phys. Chem. 1996, 100, 14184-14191 10.1021/jp9533032
40. Malyshka, D.; Pandiscia, L. A.; Schweitzer-Stenner, R. Cardiolipin containing liposomes are fully ionized at physiological pH. An FT-IR study of phosphate group ionization Vib. Spectrosc. 2014, 75, 86-92 10.1016/j.vibspec.2014.10.003
41. Oellerich, S.; Lecomte, S.; Paternostre, M.; Heimburg, T.; Hildebrandt, P. Peripheral and Integral Binding of Cytochrome c to Phospholipids Vesicles J. Phys. Chem. B 2004, 108, 3871-3878 10.1021/jp036799t
42. Beales, P. A.; Bergstrom, C. L.; Geerts, N.; Grioves, J. T.; Vanderlick, T. K. l. Single Vesicle Observations of the Cardiolipin-Cytochrome c Interaction: Induction of Membrane Morphology Changes Langmuir 2011, 27, 6107-6115 10.1021/la104924c
43. Bergstrom, C. L.; Beales, P. A.; Lv, Y.; Vanderlick, T. K.; Groves, J. T. Cytochrome c causes pore formation in cardiolipin-containing membranes Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 6269-6274 10.1073/pnas.1303819110
44. Gallet, P. F.; Petit, J. M.; Maftah, A.; Zachowski, A.; Julien, R. Asymmetrical distribution of cardiolipin in yeast inner mitochondrial membrane triggered by carbon catabolite repression Biochem. J. 1997, 324, 627-34 10.1042/bj3240627
45. Dragomir, I.; Hagarman, A.; Wallace, C.; Schweitzer-Stenner, R. Optical band splitting and electronic perturbations of the heme chromophore in cytochrome c at room temperature probed by visible electronic circular dichroism spectroscopy Biophys. J. 2007, 92, 989-998 10.1529/biophysj.106.095976
46. Urry, D. W.; Doty, P. On the conformation of horse heart ferri-and ferrocytochrome-c J. Am. Chem. Soc. 1965, 87, 2756-2758 10.1021/ja01090a041
47. Hagarman, A.; Duitch, L.; Schweitzer-Stenner, R. The Conformational Manifold of Ferricytochrome c Explored by Visible and Far-UV Electronic Circular Dichroism Spectroscopy Biochemistry 2008, 47, 9667-9677 10.1021/bi800729w
48. Oellerich, S.; Wackerbarth, H.; Hildebrandt, P. Spectroscopic Characterization of Nonnative Conformational States of Cytochrome c J. Phys. Chem. B 2002, 106, 6566-6580 10.1021/jp013841g
49. Huang, Q.; Szigeti, V.; Fidy, J.; Schweitzer-Stenner, R. Structural Disorder of Native Horseradish Peroxidase Probed by Resonance Raman and Low Temperature Optical Absorption Spectroscopy J. Phys. Chem. B 2003, 107, 2822 10.1021/jp026935e
50. Shah, R.; Schweitzer-Stenner, R. Structural changes of horse heart ferricytochrome c induced by changes of ionic strength and anion binding Biochemistry 2008, 47, 5250-5257 10.1021/bi702492n
51. Soffer, J. B.; Schweitzer-Stenner, R. Near-exact enthalpy-entropy compensation governs the thermal unfolding of protonation states of oxidized cytochrome c J. Biol. Inorg. Chem. 2014, 19, 1181-94 10.1007/s00775-014-1174-x
52. Schweitzer-Stenner, R.; Shah, R.; Hagarman, A.; Dragomir, I. Conformational substates of horse heart cytochrome c exhibit different thermal unfolding of the heme cavity J. Phys. Chem. B 2007, 111, 9603-9607 10.1021/jp069022j
53. Soffer, J. B.; Fradkin, E.; Pandiscia, L. A.; Schweitzer-Stenner, R. The (Not Completely Irreversible) Population of a Misfolded State of Cytochrome c at Folding Conditions Biochemistry 2013, 52, 1397 10.1021/bi301586e
54. Eaton, W. A.; Hochstrasser, R. M. Single-crystal spectra of ferrimyoglobin complexes in polarized light J. Chem. Phys 1968, 49, 985-995 10.1063/1.1670263
55. Eaton, W. A.; Hochstrasser, R. M. Electronic spectrum of single crystals of ferricytochrome-c J. Chem. Phys. 1967, 46, 2533 10.1063/1.1841081
56. Huang, Q.; Al-Azzam, W.; Griebenow, K.; Schweitzer-Stenner, R. Heme Structural Perturbation of PEG-Modified Horseradish Peroxidase C in Aromatic Organic Solvents Probed by Optical Absorption and Resonance Raman Dispersion Spectroscopy Biophys. J. 2003, 84, 3285-3298 10.1016/S0006-3495(03)70053-8
57. Indiani, C.; Feis, A.; Howes, B. D.; Marzocchi, M. P.; Smulevich, G. Benzohydoxamic acid-peroxidase complexes: spectroscopic characterization of a novel spin species J. Am. Chem. Soc. 2000, 122, 7368-7376 10.1021/ja000587h
58. Howes, B. D.; Schiódt, C. B.; Welinder, K. G.; Marzocchi, M. P.; Ma, J.-G.; Zhang, J.; Shelnutt, J. A.; Smulevich, G. The quantum-mixed-spin heme state of barley peroxidase: a paradigm of class III peroxidases Biophys. J. 1999, 77, 478-492 10.1016/S0006-3495(99)76905-5
59. Verbaro, D.; Hagarman, A.; Kohli, A.; Schweitzer-Stenner, R. Microperoxidase 11: a model system for porphyrin networks and heme-protein interactions J. Biol. Inorg. Chem. 2009, 14, 1289-1300 10.1007/s00775-009-0574-9
60. Hong, M. K.; Braunstein, D.; Cowen, B. R.; Frauenfelder, H.; Iben, I. E. T.; Mourant, J. R.; Ormos, P.; Scholl, R.; Schulte, A.; Steinbach, P. J. Conformational substates and motions in myoglobin-external influences on structure and dynamics Biophys. J. 1990, 58, 429-436 10.1016/S0006-3495(90)82388-2
61. Heimburg, T.; Marsh, D. Protein Surface-Distribution and Protein-Protein Interactions in the Binding of Peripheral Proteins to Charged Lipid Membranes Biophys. J. 1995, 68, 536-546 10.1016/S0006-3495(95)80215-8
62. Marchenkova, M. A.; Dyakova, Y. A.; Tereschenko, E. Y.; Kovalchuk, M. V.; Vladimirov, Y. A. Cytochrome c Complexes with Cardiolipin Monolayer Formed under Different Surface Pressure Langmuir 2015, 31, 12426-12436 10.1021/acs.langmuir.5b03155
63. Windren, D. A.; Plachy, W. Z. The diffusion-solubility of oxygen in lipid bilayers Biochim. Biophys. Acta, Biomembr. 1980, 600, 655-665 10.1016/0005-2736(80)90469-1
64. Dzikovski, B. G.; Livshits, V. A.; Marsh, D. Oxygen Permeation Profile in Lipid Membranes: Comparison with Transmembrane Polarity Profile Biophys. J. 2003, 85, 1005-1012 10.1016/S0006-3495(03)74539-1
65. Kawai, C.; Pessoto, F. S.; Rodrigues, T.; Mugnol, K. C. U.; Tortora, V.; Castro, L.; Milicchio, V. A.; Tersariol, I. L. S.; Di Mascio, P.; Radi, R. pH-Sensitive Binding of Cytochrome c to the Inner Mitochondrial membrane. Implications for the Participation of the Protein in Cell Respiration and Apoptosis Biochemistry 2009, 48, 8335 10.1021/bi9006463
66. Cassatt, J. C.; Marini, C. P. The Kinetics of Oxidation of Reduced Cytochrome c by Ferricyanide Derivatives Biochemistry 1974, 13, 5323-5328 10.1021/bi00723a011
67. Musatov, A.; Fabian, M.; Varhac, R. Elucidating the mechanism of ferrocytochrome c heme disruption by peroxidized cardiolipin J. Biol. Inorg. Chem. 2013, 18, 137-44 10.1007/s00775-012-0958-0
68. Huang, Q.; Huang, Q.; Pinto, R. A.; Griebenow, K.; Schweitzer-Stenner, R.; Weber, W. J. Inactivation of Horseradish Peroxidase by Phenoxyl Radical Attack J. Am. Chem. Soc. 2005, 127, 1431-1437 10.1021/ja045986h
69. Schweitzer-Stenner, R. The Internal Electric Field in Cytochrome C Explored by Visible Electronic Circular Dichroism Spectroscopy J. Phys. Chem. B 2008, 112, 10358-10366 10.1021/jp802495q
70. Dahlberg, M.; Maliniak, A. Molecular dynamics simulations of cardiolipin bilayers J. Phys. Chem. B 2008, 112, 11655-63 10.1021/jp803414g
71. Vácha, R.; Sui, S. W. I.; Petrov, M.; Böckmann, R. A.; Barucha-Kraszewska, J.; Jurkiewicz, P.; Hof, M.; Berkowitz, M. L.; Jungwirth, P. Effects of Alkali and halide Anions on the DOPC Lipid Membrane J. Phys. Chem. A 2009, 113, 7235-7243 10.1021/jp809974e
72. Clarke, R. J.; Lupfert, C. Influence of anions and cations on the dipole potential of phosphatidylcholine vesicles: a basis for the Hofmeister effect Biophys. J. 1999, 76, 2614-24 10.1016/S0006-3495(99)77414-X
73. Salamon, Z.; Tollin, G. Interaction of Horse Heart Cytochrome c with Lipid Bilayer Membranes: Effects on Redox Potentials J. Bioenerg. Biomembr. 1997, 29, 211-220 10.1023/A:1022401825287
74. Bradley, J. M.; Silkstone, G.; Wilson, M. H.; Cheesman, M. R.; Butt, J. M. Probing a Complex of Cytochrome c and Cardiolipin by Magnetic Circular Dichroism Spectroscopy: Implications for the Initial Events in Apoptosis J. Am. Chem. Soc. 2011, 133, 19676-19679 10.1021/ja209144h
75. Pielak, G. J.; Oikawa, K.; Mauk, A. G.; Smith, M.; Kay, C. M. Elimination of the Negative Soret Cotton Effect of Cytochrome c by Replacement of the Invariant Phenylalanine Using Site-Directed Mutagenesis J. Am. Chem. Soc. 1986, 108, 2724-2727 10.1021/ja00270a035
76. Alvarez-Paggi, D.; Castro, M. A.; Tórtora, V.; Castro, L.; Radi, R.; Murgida, D. H. Electrostatically Driven Second-Sphere Ligand Switch between High and Low Reorganization Energy Forms of Native Cytochrome c J. Am. Chem. Soc. 2013, 135, 4389-4397 10.1021/ja311786b
77. Mandal, A.; Hopp, C. D.; DeLucia, M.; Kodali, R.; Kagan, V. E.; Ahn, J.; van der Wel, P. C. A. Structural Changes and Proapoptic Peroxidase Activity of Cardiolipin-Bound Mitochondrial Cytochrome c Biophys. J. 2015, 109, 1873-1884 10.1016/j.bpj.2015.09.016