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Journal of bioenergetics and biomembranes1997; 29(3); 211-221; doi: 10.1023/a:1022401825287

Interaction of horse heart cytochrome c with lipid bilayer membranes: effects on redox potentials.

Abstract: Cyclic voltammetry has been used to study the effects of interactions between horse cytochrome c and solid-supported planar lipid membranes, comprised of either egg phosphatidylcholine (PC) or PC plus 20 mol.% cardiolipin (CL), on the redox potential and the electrochemical electron transfer rate between the protein and a semiconductor electrode. Experiments were performed over a wide range of cytochrome c concentrations (0-440 microM) at low (20 mM) and medium (160 mM) ionic strengths. Three types of electrochemical behavior were observed, which varied as a function of the experimental conditions. At very low cytochrome c concentration (approximately 0.1 microM), and under conditions where electrostatic forces dominated the protein-lipid membrane interaction (i.e., low ionic strength with membranes containing CL), a redox potential (approximately 265 mV) and an electrochemical electron transfer rate constant (0.09 s[-1])were obtained which compare well with those measured in other laboratories using a variety of different chemical modifications of the working electrode. Two other electrochemical signals (not reported with chemically modified electrodes) were also observed to occur at higher cytochrome c concentrations with this membrane system, as well as with two other systems (membranes containing CL under medium ionic strength conditions, and PC only at low ionic strength). These involved positive shifts of the cytochrome c redox potential (by 40 and 60 mV) and large decreases in the electron transfer rate (to 0.03 and 0.003 s[-1]). The observations can be rationalized in terms of a structural model of the cytochrome c-membrane interaction, in which association involves both electrostatic and hydrophobic forces and results in varying degrees of insertion of the protein into the hydrophobic interior of the membrane.
Publication Date: 1997-06-01 PubMed ID: 9298706DOI: 10.1023/a:1022401825287Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study investigates how the interaction of horse heart cytochrome c with lipid membranes affects its redox potential using a method called cyclic voltammetry, demonstrating that variables like membrane composition, ionic strength, and protein concentration can influence the redox potential and electron transfer rate.

Research Methodology and Observations

  • The researchers employed cyclic voltammetry, a type of electrochemical measurement, to examine the impacts of interactions between horse cytochrome c and specific lipid membranes on the redox potential and electrochemical electron transfer rate.
  • The membranes were made of either egg phosphatidylcholine (PC) or a mixture of PC and cardiolipin (CL). The experiments were conducted at low to medium ionic strengths and varying levels of cytochrome c concentrations.
  • Three distinctive kinds of electrochemical behavior were observed, their occurrence was influenced by the specific experimental conditions.

Key Findings

  • In scenarios where electrostatic forces primarily dictated the interaction between the protein and lipid membrane (low ionic strength with membranes that contain cardiolipin), certain redox potential and electron transfer rate constants were noted. These values align with results obtained from other laboratories using different chemical modifications of the working electrode.
  • Two additional electrochemical signals were recorded at higher cytochrome c concentrations with specific membrane systems. These included positive shifts in cytochrome c redox potential and significant decreases in the electron transfer rate.

Interpretation and Model Proposal

  • The researchers offered an interpretation of their observations, suggesting that a combination of electrostatic and hydrophobic forces govern the association between the cytochrome c and the membrane. The degree of the protein’s insertion into the hydrophobic membrane interior varies, hence influencing the electrochemical behavior.
  • Consequently, the study proposed a structural model for the interaction between cytochrome c and the membrane, which can explain the observed changes in redox potential and electron transfer rate constants under different conditions.

Cite This Article

APA
Salamon Z, Tollin G. (1997). Interaction of horse heart cytochrome c with lipid bilayer membranes: effects on redox potentials. J Bioenerg Biomembr, 29(3), 211-221. https://doi.org/10.1023/a:1022401825287

Publication

ISSN: 0145-479X
NlmUniqueID: 7701859
Country: United States
Language: English
Volume: 29
Issue: 3
Pages: 211-221

Researcher Affiliations

Salamon, Z
  • Department of Biochemistry, University of Arizona, Tucson 85721, USA.
Tollin, G

    MeSH Terms

    • Animals
    • Cytochrome c Group / metabolism
    • Electrochemistry
    • Electron Transport
    • Horses
    • Lipid Bilayers / metabolism
    • Models, Molecular
    • Myocardium / enzymology
    • Oxidation-Reduction
    • Stereoisomerism

    References

    This article includes 58 references
    1. Shui-Pong-Van, Griffith OH. Bilayer structure in phospholipid-cytochrome c model membranes.. J Membr Biol 1975;20(1-2):155-70.
      pubmed: 164553doi: 10.1007/BF01870633google scholar: lookup
    2. Rietveld A, Sijens P, Verkleij AJ, Kruijff B. Interaction of cytochrome c and its precursor apocytochrome c with various phospholipids.. EMBO J 1983;2(6):907-13.
    3. Cortese JD, Voglino AL, Hackenbrock CR. The ionic strength of the intermembrane space of intact mitochondria is not affected by the pH or volume of the intermembrane space.. Biochim Biophys Acta 1992 May 20;1100(2):189-97.
      pubmed: 1610874doi: 10.1016/0005-2728(92)90081-cgoogle scholar: lookup
    4. Shipley GG, Leslie RB, Chapman D. Small-angle x-ray scattering studies of cytochrome c-phospholipid complexes.. Biochim Biophys Acta 1969 Jan 28;173(1):1-10.
      pubmed: 5813300doi: 10.1016/0005-2736(69)90031-5google scholar: lookup
    5. Rytömaa M, Kinnunen PK. Reversibility of the binding of cytochrome c to liposomes. Implications for lipid-protein interactions.. J Biol Chem 1995 Feb 17;270(7):3197-202.
      pubmed: 7852404doi: 10.1074/jbc.270.7.3197google scholar: lookup
    6. de Jongh HH, Killian JA, de Kruijff B. A water-lipid interface induces a highly dynamic folded state in apocytochrome c and cytochrome c, which may represent a common folding intermediate.. Biochemistry 1992 Feb 18;31(6):1636-43.
      pubmed: 1310614doi: 10.1021/bi00121a008google scholar: lookup
    7. Kassner RJ. A theoretical model for the effects of local nonpolar heme environments on the redox potentials in cytochromes.. J Am Chem Soc 1973 Apr 18;95(8):2674-7.
      pubmed: 4348492doi: 10.1021/ja00789a044google scholar: lookup
    8. Vanderkooi J, Erecińska M. Cytochrome c interaction with membranes. Interaction of cytochrome c with isolated membrane fragments and purified enzymes.. Arch Biochem Biophys 1974 Jun;162(2):385-91.
      pubmed: 4366145doi: 10.1016/0003-9861(74)90196-9google scholar: lookup
    9. Salamon Z, Wang Y, Brown MF, Macleod HA, Tollin G. Conformational changes in rhodopsin probed by surface plasmon resonance spectroscopy.. Biochemistry 1994 Nov 22;33(46):13706-11.
      pubmed: 7947780doi: 10.1021/bi00250a022google scholar: lookup
    10. Teissie J. Interaction of cytochrome c with phospholipid monolayers. Orientation and penetration of protein as functions of the packing density of film, nature of the phospholipids, and ionic content of the aqueous phase.. Biochemistry 1981 Mar 17;20(6):1554-60.
      pubmed: 6261801doi: 10.1021/bi00509a023google scholar: lookup
    11. Cullis PR, de Kruijff B. Lipid polymorphism and the functional roles of lipids in biological membranes.. Biochim Biophys Acta 1979 Dec 20;559(4):399-420.
      pubmed: 391283doi: 10.1016/0304-4157(79)90012-1google scholar: lookup
    12. Heimburg T, Marsh D. Protein surface-distribution and protein-protein interactions in the binding of peripheral proteins to charged lipid membranes.. Biophys J 1995 Feb;68(2):536-46.
      pubmed: 7696507doi: 10.1016/S0006-3495(95)80215-8google scholar: lookup
    13. Kimelberg HK, Lee CP. Interactions of cytochromec with phospholipid membranes : Reactivity of cytochromec bound to phospholipid liquid crystals.. J Membr Biol 1970 Dec;2(1):252-62.
      pubmed: 24174150doi: 10.1007/BF01869863google scholar: lookup
    14. MacNaughtan W, Snook KA, Caspi E, Franks NP. An X-ray diffraction analysis of oriented lipid multilayers containing basic proteins.. Biochim Biophys Acta 1985 Aug 27;818(2):132-48.
      pubmed: 2411290doi: 10.1016/0005-2736(85)90556-5google scholar: lookup
    15. Salamon Z, Tollin G. Surface plasmon resonance studies of complex formation between cytochrome c and bovine cytochrome c oxidase incorporated into a supported planar lipid bilayer. II. Binding of cytochrome c to oxidase-containing cardiolipin/phosphatidylcholine membranes.. Biophys J 1996 Aug;71(2):858-67.
      pubmed: 8842224doi: 10.1016/S0006-3495(96)79287-1google scholar: lookup
    16. Spooner PJ, Watts A. Reversible unfolding of cytochrome c upon interaction with cardiolipin bilayers. 1. Evidence from deuterium NMR measurements.. Biochemistry 1991 Apr 23;30(16):3871-9.
      pubmed: 1850290doi: 10.1021/bi00230a010google scholar: lookup
    17. Hildebrandt P, Stockburger M. Cytochrome c at charged interfaces. 1. Conformational and redox equilibria at the electrode/electrolyte interface probed by surface-enhanced resonance Raman spectroscopy.. Biochemistry 1989 Aug 8;28(16):6710-21.
      pubmed: 2551378doi: 10.1021/bi00442a026google scholar: lookup
    18. Spooner PJ, Watts A. Reversible unfolding of cytochrome c upon interaction with cardiolipin bilayers. 2. Evidence from phosphorus-31 NMR measurements.. Biochemistry 1991 Apr 23;30(16):3880-5.
      pubmed: 1850291doi: 10.1021/bi00230a011google scholar: lookup
    19. Kimelberg HK, Papahadjopoulos D. Interactions of basic proteins with phospholipid membranes. Binding and changes in the sodium permeability of phosphatidylserine vesicles.. J Biol Chem 1971 Feb 25;246(4):1142-8.
      pubmed: 5543681
    20. Gulik-Krzywicki T, Shechter E, Vittorio Luzzati, Faure M. Interactions of proteins and lipids: structure and polymorphism of protein-lipid-water phases.. Nature 1969 Sep 13;223(5211):1116-21.
      pubmed: 4309344doi: 10.1038/2231116a0google scholar: lookup
    21. Pinheiro TJ, Watts A. Resolution of individual lipids in mixed phospholipid membranes and specific lipid-cytochrome c interactions by magic-angle spinning solid-state phosphorus-31 NMR.. Biochemistry 1994 Mar 8;33(9):2459-67.
      pubmed: 8117706doi: 10.1021/bi00175a014google scholar: lookup
    22. Morse PD 2nd, Deamer DW. Interaction of cytochrome c with lipid monolayers.. Biochim Biophys Acta 1973 Apr 16;298(4):769-82.
      pubmed: 4354123doi: 10.1016/0005-2736(73)90381-7google scholar: lookup
    23. Daum G. Lipids of mitochondria.. Biochim Biophys Acta 1985 Jun 12;822(1):1-42.
      pubmed: 2408671doi: 10.1016/0304-4157(85)90002-4google scholar: lookup
    24. Salamon Z, Tollin G. Surface plasmon resonance studies of complex formation between cytochrome c and bovine cytochrome c oxidase incorporated into a supported planar lipid bilayer. I. Binding of cytochrome c to cardiolipin/phosphatidylcholine membranes in the absence of oxidase.. Biophys J 1996 Aug;71(2):848-57.
      pubmed: 8842223doi: 10.1016/S0006-3495(96)79286-Xgoogle scholar: lookup
    25. Cortese JD, Voglino AL, Hackenbrock CR. Persistence of cytochrome c binding to membranes at physiological mitochondrial intermembrane space ionic strength.. Biochim Biophys Acta 1995 Mar 14;1228(2-3):216-228.
      pubmed: 7893728doi: 10.1016/0005-2728(94)00178-8google scholar: lookup
    26. Bychkova VE, Pain RH, Ptitsyn OB. The 'molten globule' state is involved in the translocation of proteins across membranes?. FEBS Lett 1988 Oct 10;238(2):231-4.
      pubmed: 3049159doi: 10.1016/0014-5793(88)80485-xgoogle scholar: lookup
    27. Hoch FL. Cardiolipins and biomembrane function.. Biochim Biophys Acta 1992 Mar 26;1113(1):71-133.
      pubmed: 1550861doi: 10.1016/0304-4157(92)90035-9google scholar: lookup
    28. Heimburg T, Marsh D. Investigation of secondary and tertiary structural changes of cytochrome c in complexes with anionic lipids using amide hydrogen exchange measurements: an FTIR study.. Biophys J 1993 Dec;65(6):2408-17.
      pubmed: 8312479doi: 10.1016/S0006-3495(93)81299-2google scholar: lookup
    29. Jori G, Tamburro AM, Azzi A. Photooxidative and spectral studies on cytochrome c. Conformational changes induced by binding of cardiolipin.. Photochem Photobiol 1974 May;19(5):337-45.
    30. van der Goot FG, Lakey JH, Pattus F. The molten globule intermediate for protein insertion or translocation through membranes.. Trends Cell Biol 1992 Nov;2(11):343-8.
      pubmed: 14731513
    31. Spooner PJ, Watts A. Cytochrome c interactions with cardiolipin in bilayers: a multinuclear magic-angle spinning NMR study.. Biochemistry 1992 Oct 20;31(41):10129-38.
      pubmed: 1327134doi: 10.1021/bi00156a037google scholar: lookup
    32. Salamon Z, Hazzard JT, Tollin G. Direct measurement of cyclic current-voltage responses of integral membrane proteins at a self-assembled lipid-bilayer-modified electrode: cytochrome f and cytochrome c oxidase.. Proc Natl Acad Sci U S A 1993 Jul 15;90(14):6420-3.
      pubmed: 8393566doi: 10.1073/pnas.90.14.6420google scholar: lookup
    33. Bychkova VE, Dujsekina AE, Klenin SI, Tiktopulo EI, Uversky VN, Ptitsyn OB. Molten globule-like state of cytochrome c under conditions simulating those near the membrane surface.. Biochemistry 1996 May 14;35(19):6058-63.
      pubmed: 8634247doi: 10.1021/bi9522460google scholar: lookup
    34. Pinheiro TJ. The interaction of horse heart cytochrome c with phospholipid bilayers. Structural and dynamic effects.. Biochimie 1994;76(6):489-500.
      pubmed: 7880888doi: 10.1016/0300-9084(94)90173-2google scholar: lookup
    35. Pinheiro TJ, Watts A. Lipid specificity in the interaction of cytochrome c with anionic phospholipid bilayers revealed by solid-state 31P NMR.. Biochemistry 1994 Mar 8;33(9):2451-8.
      pubmed: 8117705doi: 10.1021/bi00175a013google scholar: lookup
    36. van der Goot FG, González-Mañas JM, Lakey JH, Pattus F. A 'molten-globule' membrane-insertion intermediate of the pore-forming domain of colicin A.. Nature 1991 Dec 5;354(6352):408-10.
      pubmed: 1956406doi: 10.1038/354408a0google scholar: lookup
    37. Heimburg T, Hildebrandt P, Marsh D. Cytochrome c-lipid interactions studied by resonance Raman and 31P NMR spectroscopy. Correlation between the conformational changes of the protein and the lipid bilayer.. Biochemistry 1991 Sep 17;30(37):9084-9.
      pubmed: 1654089doi: 10.1021/bi00101a025google scholar: lookup
    38. Brown LR, Wüthrich K. NMR and ESR studies of the interactions of cytochrome c with mixed cardiolipin-phosphatidylcholine vesicles.. Biochim Biophys Acta 1977 Aug 1;468(3):389-410.
      pubmed: 195609doi: 10.1016/0005-2736(77)90290-5google scholar: lookup
    39. Soulages JL, Salamon Z, Wells MA, Tollin G. Low concentrations of diacylglycerol promote the binding of apolipophorin III to a phospholipid bilayer: a surface plasmon resonance spectroscopy study.. Proc Natl Acad Sci U S A 1995 Jun 6;92(12):5650-4.
      pubmed: 7777564doi: 10.1073/pnas.92.12.5650google scholar: lookup
    40. Pfanner N, Hartl FU, Neupert W. Import of proteins into mitochondria: a multi-step process.. Eur J Biochem 1988 Aug 1;175(2):205-12.
    41. Hennig B, Neupert W. Assembly of cytochrome c. Apocytochrome c is bound to specific sites on mitochondria before its conversion to holocytochrome c.. Eur J Biochem 1981 Dec;121(1):203-12.
    42. de Kruijff B, Cullis PR. Cytochrome c specifically induces non-bilayer structures in cardiolipin-containing model membranes.. Biochim Biophys Acta 1980 Nov 18;602(3):477-90.
      pubmed: 6254562doi: 10.1016/0005-2736(80)90327-2google scholar: lookup
    43. Papahadjopoulos D, Moscarello M, Eylar EH, Isac T. Effects of proteins on thermotropic phase transitions of phospholipid membranes.. Biochim Biophys Acta 1975 Sep 2;401(3):317-35.
      pubmed: 52374doi: 10.1016/0005-2736(75)90233-3google scholar: lookup
    44. Hildebrandt P, Stockburger M. Cytochrome c at charged interfaces. 2. Complexes with negatively charged macromolecular systems studied by resonance Raman spectroscopy.. Biochemistry 1989 Aug 8;28(16):6722-8.
      pubmed: 2551379doi: 10.1021/bi00442a027google scholar: lookup
    45. Salamon Z, Wang Y, Soulages JL, Brown MF, Tollin G. Surface plasmon resonance spectroscopy studies of membrane proteins: transducin binding and activation by rhodopsin monitored in thin membrane films.. Biophys J 1996 Jul;71(1):283-94.
      pubmed: 8804611doi: 10.1016/S0006-3495(96)79224-Xgoogle scholar: lookup
    46. Jordi W, Zhou LX, Pilon M, Demel RA, de Kruijff B. The importance of the amino terminus of the mitochondrial precursor protein apocytochrome c for translocation across model membranes.. J Biol Chem 1989 Feb 5;264(4):2292-301.
      pubmed: 2536703
    47. Dutton PL, Wilson DF, Lee CP. Oxidation-reduction potentials of cytochromes in mitochondria.. Biochemistry 1970 Dec 22;9(26):5077-82.
      pubmed: 4320585doi: 10.1021/bi00828a006google scholar: lookup
    48. Kassner RJ. Effects of nonpolar environments on the redox potentials of heme complexes.. Proc Natl Acad Sci U S A 1972 Aug;69(8):2263-7.
      pubmed: 4506096doi: 10.1073/pnas.69.8.2263google scholar: lookup
    49. Muga A, Mantsch HH, Surewicz WK. Membrane binding induces destabilization of cytochrome c structure.. Biochemistry 1991 Jul 23;30(29):7219-24.
      pubmed: 1649625doi: 10.1021/bi00243a025google scholar: lookup
    50. Vincent JS, Kon H, Levin IW. Low-temperature electron paramagnetic resonance study of the ferricytochrome c-cardiolipin complex.. Biochemistry 1987 Apr 21;26(8):2312-4.
      pubmed: 3040088doi: 10.1021/bi00382a036google scholar: lookup
    51. Salamon Z, Meyer TE, Tollin G. Photobleaching of the photoactive yellow protein from Ectothiorhodospira halophila promotes binding to lipid bilayers: evidence from surface plasmon resonance spectroscopy.. Biophys J 1995 Feb;68(2):648-54.
      pubmed: 7696516doi: 10.1016/S0006-3495(95)80225-0google scholar: lookup
    52. Szebeni J, Tollin G. Interaction of cytochrome c with liposomes: covalent labeling of externally bound protein by the fluorescent probe, azidonaphthalenedisulfonic acid, enclosed in the inner aqueous compartment of unilamellar vesicles.. Biochim Biophys Acta 1988 Jan 20;932(1):153-9.
      pubmed: 2827768doi: 10.1016/0005-2728(88)90150-8google scholar: lookup
    53. Eilers M, Hwang S, Schatz G. Unfolding and refolding of a purified precursor protein during import into isolated mitochondria.. EMBO J 1988 Apr;7(4):1139-45.
    54. Kinnunen PK, Kõiv A, Lehtonen JY, Rytömaa M, Mustonen P. Lipid dynamics and peripheral interactions of proteins with membrane surfaces.. Chem Phys Lipids 1994 Sep 6;73(1-2):181-207.
      pubmed: 8001181doi: 10.1016/0009-3084(94)90181-3google scholar: lookup
    55. Mustonen P, Virtanen JA, Somerharju PJ, Kinnunen PK. Binding of cytochrome c to liposomes as revealed by the quenching of fluorescence from pyrene-labeled phospholipids.. Biochemistry 1987 Jun 2;26(11):2991-7.
      pubmed: 3038173doi: 10.1021/bi00385a006google scholar: lookup
    56. Elöve GA, Chaffotte AF, Roder H, Goldberg ME. Early steps in cytochrome c folding probed by time-resolved circular dichroism and fluorescence spectroscopy.. Biochemistry 1992 Aug 4;31(30):6876-83.
      pubmed: 1322172doi: 10.1021/bi00145a003google scholar: lookup
    57. Salamon Z, Wang Y, Tollin G, Macleod HA. Assembly and molecular organization of self-assembled lipid bilayers on solid substrates monitored by surface plasmon resonance spectroscopy.. Biochim Biophys Acta 1994 Nov 2;1195(2):267-75.
      pubmed: 7947920doi: 10.1016/0005-2736(94)90266-6google scholar: lookup
    58. Endo T, Schatz G. Latent membrane perturbation activity of a mitochondrial precursor protein is exposed by unfolding.. EMBO J 1988 Apr;7(4):1153-8.

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    1. Díaz-Quintana A, Pérez-Mejías G, Guerra-Castellano A, De la Rosa MA, Díaz-Moreno I. Wheel and Deal in the Mitochondrial Inner Membranes: The Tale of Cytochrome c and Cardiolipin. Oxid Med Cell Longev 2020;2020:6813405.
      doi: 10.1155/2020/6813405pubmed: 32377304google scholar: lookup
    2. Lebègue E, Louro RO, Barrière F. Electrochemical Detection of pH-Responsive Grafted Catechol and Immobilized Cytochrome c onto Lipid Deposit-Modified Glassy Carbon Surface. ACS Omega 2018 Aug 31;3(8):9035-9042.
      doi: 10.1021/acsomega.8b01425pubmed: 31459037google scholar: lookup
    3. Li J, Du H, Zhang M, Zhang Z, Teng F, Zhao Y, Zhang W, Yu Y, Feng L, Cui X, Zhang M, Lu T, Guan F, Chen L. Amorphous solid dispersion of Berberine mitigates apoptosis via iPLA(2)β/Cardiolipin/Opa1 pathway in db/db mice and in Palmitate-treated MIN6 β-cells. Int J Biol Sci 2019;15(7):1533-1545.
      doi: 10.7150/ijbs.32020pubmed: 31337982google scholar: lookup
    4. Birk AV, Chao WM, Liu S, Soong Y, Szeto HH. Disruption of cytochrome c heme coordination is responsible for mitochondrial injury during ischemia. Biochim Biophys Acta 2015 Oct;1847(10):1075-84.
      doi: 10.1016/j.bbabio.2015.06.006pubmed: 26071084google scholar: lookup
    5. Song H, Wohltmann M, Tan M, Ladenson JH, Turk J. Group VIA phospholipase A2 mitigates palmitate-induced β-cell mitochondrial injury and apoptosis. J Biol Chem 2014 May 16;289(20):14194-210.
      doi: 10.1074/jbc.M114.561910pubmed: 24648512google scholar: lookup
    6. Kim N, Ripple MO, Springett R. Measurement of the mitochondrial membrane potential and pH gradient from the redox poise of the hemes of the bc1 complex. Biophys J 2012 Mar 7;102(5):1194-203.
      doi: 10.1016/j.bpj.2012.02.003pubmed: 22404942google scholar: lookup
    7. Abriata LA, Cassina A, Tórtora V, Marín M, Souza JM, Castro L, Vila AJ, Radi R. Nitration of solvent-exposed tyrosine 74 on cytochrome c triggers heme iron-methionine 80 bond disruption. Nuclear magnetic resonance and optical spectroscopy studies. J Biol Chem 2009 Jan 2;284(1):17-26.
      doi: 10.1074/jbc.M807203200pubmed: 18974097google scholar: lookup
    8. Lesnefsky EJ, Hoppel CL. Cardiolipin as an oxidative target in cardiac mitochondria in the aged rat. Biochim Biophys Acta 2008 Jul-Aug;1777(7-8):1020-7.
      doi: 10.1016/j.bbabio.2008.05.444pubmed: 18515061google scholar: lookup
    9. Kalanxhi E, Wallace CJ. Cytochrome c impaled: investigation of the extended lipid anchorage of a soluble protein to mitochondrial membrane models. Biochem J 2007 Oct 15;407(2):179-87.
      doi: 10.1042/BJ20070459pubmed: 17614790google scholar: lookup
    10. Basova LV, Kurnikov IV, Wang L, Ritov VB, Belikova NA, Vlasova II, Pacheco AA, Winnica DE, Peterson J, Bayir H, Waldeck DH, Kagan VE. Cardiolipin switch in mitochondria: shutting off the reduction of cytochrome c and turning on the peroxidase activity. Biochemistry 2007 Mar 20;46(11):3423-34.
      doi: 10.1021/bi061854kpubmed: 17319652google scholar: lookup
    11. La Penna G, Furlan S, Banci L. Molecular statistics of cytochrome c: structural plasticity and molecular environment. J Biol Inorg Chem 2007 Feb;12(2):180-93.
      doi: 10.1007/s00775-006-0178-6pubmed: 17053911google scholar: lookup
    12. Trejo-Solís C, Palencia G, Zúñiga S, Rodríguez-Ropon A, Osorio-Rico L, Luvia ST, Gracia-Mora I, Marquez-Rosado L, Sánchez A, Moreno-García ME, Cruz A, Bravo-Gómez ME, Ruiz-Ramírez L, Rodríguez-Enriquez S, Sotelo J. Cas IIgly induces apoptosis in glioma C6 cells in vitro and in vivo through caspase-dependent and caspase-independent mechanisms. Neoplasia 2005 Jun;7(6):563-74.
      doi: 10.1593/neo.04607pubmed: 16036107google scholar: lookup
    13. Salamon Z, Huang D, Cramer WA, Tollin G. Coupled plasmon-waveguide resonance spectroscopy studies of the cytochrome b6f/plastocyanin system in supported lipid bilayer membranes. Biophys J 1998 Oct;75(4):1874-85.
      doi: 10.1016/S0006-3495(98)77628-3pubmed: 9746528google scholar: lookup
    14. Kovilakath A, Mauro AG, Valentine YA, Raucci FJ, Jamil M, Carter C, Thompson J, Chen Q, Beutner G, Yue Y, Allegood J, Wang XX, Dail J, Devarakonda T, Myakala K, Windle JJ, Subler MA, Montefusco D, Willard B, Javaheri A, Bernas T, Mahata SK, Levi M, Liu J, Porter GA Jr, Lesnefsky EJ, Salloum FN, Cowart LA. SPTLC3 Is Essential for Complex I Activity and Contributes to Ischemic Cardiomyopathy. Circulation 2024 Aug 20;150(8):622-641.