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. 1990 Jan 1;265(1):227–232. doi: 10.1042/bj2650227

1H-n.m.r. evaluation of the ferricytochrome c-cardiolipin interaction. Effect of superoxide radicals.

B Soussi 1, A C Bylund-Fellenius 1, T Scherstén 1, J Angström 1
PMCID: PMC1136634  PMID: 2154181

Abstract

The interaction between ferricytochrome c and cardiolipin was investigated by 1H n.m.r. at 270 MHz. From the phospholipid-induced changes of the protein spectral features it is concluded that the first 2 equivalents of cardiolipin cause a conformational change at the lower part of the solvent-exposed haem edge, involving a rearrangement of the hydrogen-bond interactions of propionate 6, thus partly accounting for the lowered redox potential of cytochrome c in the presence of cardiolipin. The increased value for the pK of the alkaline isomerization of ferricytochrome c shows that cardiolipin stabilizes the native structure of the protein, indicating that the oxidized form assumes ferrocytochrome c-like properties. Peroxidation of cardiolipin by superoxide radical ions drastically decreases the protein binding to this phospholipid. The implications of this finding, and the likelihood of the ternary cytochrome c-cardiolipin-cytochrome c oxidase complex, for the binding of cytochrome c to cytochrome c oxidase in vivo, are discussed in relation to peroxidative damage following ischaemia and reperfusion.

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Selected References

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  1. Andersson T., Angström J., Falk K. E., Forsén S. Perchlorate binding to cytochrome c: a magnetic and optical study. Eur J Biochem. 1980 Sep;110(2):363–369. doi: 10.1111/j.1432-1033.1980.tb04876.x. [DOI] [PubMed] [Google Scholar]
  2. Bacon B. R., O'Neill R., Park C. H. Iron-induced peroxidative injury to isolated rat hepatic mitochondria. J Free Radic Biol Med. 1986;2(5-6):339–347. doi: 10.1016/s0748-5514(86)80034-4. [DOI] [PubMed] [Google Scholar]
  3. Bosshard H. R., Zürrer M. The conformation of cytochrome c in solution. Localization of a conformational difference between ferri- and ferrocytochrome c on the surface of the molecule. J Biol Chem. 1980 Jul 25;255(14):6694–6699. [PubMed] [Google Scholar]
  4. Brautigan D. L., Ferguson-Miller S., Margoliash E. Mitochondrial cytochrome c: preparation and activity of native and chemically modified cytochromes c. Methods Enzymol. 1978;53:128–164. doi: 10.1016/s0076-6879(78)53021-8. [DOI] [PubMed] [Google Scholar]
  5. Brown L. R., Wüthrich K. A spin label study of lipid oxidation catalyzed by heme proteins. Biochim Biophys Acta. 1977 Jan 21;464(2):356–369. doi: 10.1016/0005-2736(77)90010-4. [DOI] [PubMed] [Google Scholar]
  6. Brown L. R., 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. doi: 10.1016/0005-2736(77)90290-5. [DOI] [PubMed] [Google Scholar]
  7. Brzezinski P., Malmström B. G. Electron-transport-driven proton pumps display nonhyperbolic kinetics: Simulation of the steady-state kinetics of cytochrome c oxidase. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4282–4286. doi: 10.1073/pnas.83.12.4282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brzezinski P., Malmström B. G. The mechanism of electron gating in proton pumping cytochrome c oxidase: the effect of pH and temperature on internal electron transfer. Biochim Biophys Acta. 1987 Oct 29;894(1):29–38. doi: 10.1016/0005-2728(87)90209-x. [DOI] [PubMed] [Google Scholar]
  9. Cheneval D., Müller M., Toni R., Ruetz S., Carafoli E. Adriamycin as a probe for the transversal distribution of cardiolipin in the inner mitochondrial membrane. J Biol Chem. 1985 Oct 25;260(24):13003–13007. [PubMed] [Google Scholar]
  10. Devaux P. F., Hoatson G. L., Favre E., Fellmann P., Farren B., MacKay A. L., Bloom M. Interaction of cytochrome c with mixed dimyristoylphosphatidylcholine-dimyristoylphosphatidylserine bilayers: a deuterium nuclear magnetic resonance study. Biochemistry. 1986 Jul 1;25(13):3804–3812. doi: 10.1021/bi00361a011. [DOI] [PubMed] [Google Scholar]
  11. Fry M., Green D. E. Cardiolipin requirement by cytochrome oxidase and the catalytic role of phospholipid. Biochem Biophys Res Commun. 1980 Apr 29;93(4):1238–1246. doi: 10.1016/0006-291x(80)90622-1. [DOI] [PubMed] [Google Scholar]
  12. Halliwell B. Superoxide, iron, vascular endothelium and reperfusion injury. Free Radic Res Commun. 1989;5(6):315–318. doi: 10.3109/10715768909073413. [DOI] [PubMed] [Google Scholar]
  13. Huang Y. Y., Kimura T. Thermodynamic parameters for the reduction reaction of membrane-bound cytochrome c in comparison with those of the membrane-free form: spectropotentiostatic determination with use of an optically transparent thin-layer electrode. Biochemistry. 1984 May 8;23(10):2231–2236. doi: 10.1021/bi00305a021. [DOI] [PubMed] [Google Scholar]
  14. McCord J. M. Free radicals and myocardial ischemia: overview and outlook. Free Radic Biol Med. 1988;4(1):9–14. doi: 10.1016/0891-5849(88)90005-6. [DOI] [PubMed] [Google Scholar]
  15. Nicholls P. Cytochrome c binding to enzymes and membranes. Biochim Biophys Acta. 1974 Dec 30;346(3-4):261–310. doi: 10.1016/0304-4173(74)90003-2. [DOI] [PubMed] [Google Scholar]
  16. Okayasu T., Curtis M. T., Farber J. L. Structural alterations of the inner mitochondrial membrane in ischemic liver cell injury. Arch Biochem Biophys. 1985 Feb 1;236(2):638–645. doi: 10.1016/0003-9861(85)90668-x. [DOI] [PubMed] [Google Scholar]
  17. Rietveld A., Sijens P., Verkleij A. J., Kruijff B. Interaction of cytochrome c and its precursor apocytochrome c with various phospholipids. EMBO J. 1983;2(6):907–913. doi: 10.1002/j.1460-2075.1983.tb01520.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Robinson N. C., Capaldi R. A. Interaction of detergents with cytochrome c oxidase. Biochemistry. 1977 Feb 8;16(3):375–381. doi: 10.1021/bi00622a006. [DOI] [PubMed] [Google Scholar]
  19. Robinson N. C., Strey F., Talbert L. Investigation of the essential boundary layer phospholipids of cytochrome c oxidase using Triton X-100 delipidation. Biochemistry. 1980 Aug 5;19(16):3656–3661. doi: 10.1021/bi00557a003. [DOI] [PubMed] [Google Scholar]
  20. Santos H., Turner D. L. Proton NMR studies of horse ferricytochrome c. Completion of the assignment of the well resolved hyperfine shifted resonances. FEBS Lett. 1987 Dec 21;226(1):179–185. doi: 10.1016/0014-5793(87)80575-6. [DOI] [PubMed] [Google Scholar]
  21. Smith M. W., Collan Y., Kahng M. W., Trump B. F. Changes in mitochondrial lipids of rat kidney during ischemia. Biochim Biophys Acta. 1980 May 28;618(2):192–201. doi: 10.1016/0005-2760(80)90025-9. [DOI] [PubMed] [Google Scholar]
  22. Takano T., Dickerson R. E. Conformation change of cytochrome c. II. Ferricytochrome c refinement at 1.8 A and comparison with the ferrocytochrome structure. J Mol Biol. 1981 Nov 25;153(1):95–115. doi: 10.1016/0022-2836(81)90529-5. [DOI] [PubMed] [Google Scholar]
  23. Taylor C. P. The EPR of low spin heme complexes. Relation of the t2g hole model to the directional properties of the g tensor, and a new method for calculating the ligand field parameters. Biochim Biophys Acta. 1977 Mar 28;491(1):137–148. doi: 10.1016/0005-2795(77)90049-6. [DOI] [PubMed] [Google Scholar]
  24. Verkleij A. J. Lipidic intramembranous particles. Biochim Biophys Acta. 1984 Jan 27;779(1):43–63. doi: 10.1016/0304-4157(84)90003-0. [DOI] [PubMed] [Google Scholar]
  25. Vik S. B., Georgevich G., Capaldi R. A. Diphosphatidylglycerol is required for optimal activity of beef heart cytochrome c oxidase. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1456–1460. doi: 10.1073/pnas.78.3.1456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Vincent J. S., Kon H., Levin I. W. Low-temperature electron paramagnetic resonance study of the ferricytochrome c-cardiolipin complex. Biochemistry. 1987 Apr 21;26(8):2312–2314. doi: 10.1021/bi00382a036. [DOI] [PubMed] [Google Scholar]
  27. Weber C., Michel B., Bosshard H. R. Spectroscopic analysis of the cytochrome c oxidase-cytochrome c complex: circular dichroism and magnetic circular dichroism measurements reveal change of cytochrome c heme geometry imposed by complex formation. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6687–6691. doi: 10.1073/pnas.84.19.6687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. de Kruijff B., Cullis P. R. Cytochrome c specifically induces non-bilayer structures in cardiolipin-containing model membranes. Biochim Biophys Acta. 1980 Nov 18;602(3):477–490. doi: 10.1016/0005-2736(80)90327-2. [DOI] [PubMed] [Google Scholar]

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