Multifaceted Effects of ATP on Cardiolipin-bound Cytochrome C

Overview

Journal Biochemistry

Specialty Biochemistry

Date 2013 Jan 22

PMID 23331169

Citations 13

Authors

Erik J Snider

Julia Muenzner

Jason R Toffey

Yuning Hong

Ekaterina V Pletneva

Affiliations

Soon will be listed here.

Abstract

Using a collection of dye-labeled cytochrome c (cyt c) variants, we identify transformations of the heterogeneous cardiolipin (CL)-bound cyt c ensemble with added ATP. Distributions of dye-to-heme distances P(r) from time-resolved fluorescence resonance energy transfer show that ATP decreases the population of largely unfolded cyt c conformers, but its effects are distinct from those of a simple salt. The high peroxidase activity of CL-bound cyt c with added ATP suggests binding interactions that favor protein structures with the open heme pocket. Although ATP weakens cyt c-CL binding interactions, it also boosts the apoptosis-relevant peroxidase activity of CL-bound cyt c.

Citing Articles

Binding of yeast and human cytochrome c to cardiolipin nanodiscs at physiological ionic strength.

Frederick A, Bowler B J Inorg Biochem. 2024; 260:112699.

PMID: 39181020 PMC: 11404356. DOI: 10.1016/j.jinorgbio.2024.112699.

Binding of S. cerevisiae iso-1 cytochrome c and its surface lysine-to-alanine variants to cardiolipin: charge effects and the role of the lipid to protein ratio.

Paradisi A, Bellei M, Paltrinieri L, Bortolotti C, Di Rocco G, Ranieri A J Biol Inorg Chem. 2020; 25(3):467-487.

PMID: 32189145 DOI: 10.1007/s00775-020-01776-1.

The Role of Cardiolipin and Mitochondrial Damage in Kidney Transplant.

Miranda-Diaz A, Cardona-Munoz E, Pacheco-Moises F Oxid Med Cell Longev. 2019; 2019:3836186.

PMID: 31885786 PMC: 6899302. DOI: 10.1155/2019/3836186.

Relating the multi-functionality of cytochrome c to membrane binding and structural conversion.

Schweitzer-Stenner R Biophys Rev. 2018; 10(4):1151-1185.

PMID: 29574621 PMC: 6082307. DOI: 10.1007/s12551-018-0409-4.

Revisiting Kadenbach: Electron flux rate through cytochrome c-oxidase determines the ATP-inhibitory effect and subsequent production of ROS.

Vogt S, Rhiel A, Weber P, Ramzan R Bioessays. 2016; 38(6):556-67.

PMID: 27171124 PMC: 5084804. DOI: 10.1002/bies.201600043.

References

Tuominen E, Zhu K, Wallace C, Clark-Lewis I, Craig D, Rytomaa M . ATP induces a conformational change in lipid-bound cytochrome c. J Biol Chem. 2001; 276(22):19356-62. DOI: 10.1074/jbc.M100853200. View

Pletneva E, Gray H, Winkler J . Nature of the cytochrome c molten globule. J Am Chem Soc. 2005; 127(44):15370-1. DOI: 10.1021/ja0555318. View

Patriarca A, Eliseo T, Sinibaldi F, Piro M, Melis R, Paci M . ATP acts as a regulatory effector in modulating structural transitions of cytochrome c: implications for apoptotic activity. Biochemistry. 2009; 48(15):3279-87. DOI: 10.1021/bi801837e. View

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.... Biophys J. 1996; 71(2):848-57. PMC: 1233541. DOI: 10.1016/S0006-3495(96)79286-X. View

Beales P, Bergstrom C, Geerts N, Groves J, Vanderlick T . Single vesicle observations of the cardiolipin-cytochrome C interaction: induction of membrane morphology changes. Langmuir. 2011; 27(10):6107-15. PMC: 3103708. DOI: 10.1021/la104924c. View

Brown L, Wuthrich K . NMR and ESR studies of the interactions of cytochrome c with mixed cardiolipin-phosphatidylcholine vesicles. Biochim Biophys Acta. 1977; 468(3):389-410. DOI: 10.1016/0005-2736(77)90290-5. View

Craig D, Wallace C . Studies of 8-azido-ATP adducts reveal two mechanisms by which ATP binding to cytochrome c could inhibit respiration. Biochemistry. 1995; 34(8):2686-93. DOI: 10.1021/bi00008a036. View

Rytomaa M, Kinnunen P . Evidence for two distinct acidic phospholipid-binding sites in cytochrome c. J Biol Chem. 1994; 269(3):1770-4. View

Goto Y, Okamura N, Aimoto S . ATP-induced conformational transition of denatured proteins. J Biochem. 1991; 109(5):746-50. DOI: 10.1093/oxfordjournals.jbchem.a123451. View

10.

Sinibaldi F, Mei G, Polticelli F, Piro M, Howes B, Smulevich G . ATP specifically drives refolding of non-native conformations of cytochrome c. Protein Sci. 2005; 14(4):1049-58. PMC: 2253445. DOI: 10.1110/ps.041069405. View

11.

Hanske J, Toffey J, Morenz A, Bonilla A, Schiavoni K, Pletneva E . Conformational properties of cardiolipin-bound cytochrome c. Proc Natl Acad Sci U S A. 2011; 109(1):125-30. PMC: 3252944. DOI: 10.1073/pnas.1112312108. View

12.

Jordan T, Eads J, Spiro T . Secondary and tertiary structure of the A-state of cytochrome c from resonance Raman spectroscopy. Protein Sci. 1995; 4(4):716-28. PMC: 2143105. DOI: 10.1002/pro.5560040411. View

13.

Sinibaldi F, Droghetti E, Polticelli F, Piro M, Pierro D, Ferri T . The effects of ATP and sodium chloride on the cytochrome c-cardiolipin interaction: the contrasting behavior of the horse heart and yeast proteins. J Inorg Biochem. 2011; 105(11):1365-72. DOI: 10.1016/j.jinorgbio.2011.07.022. View

14.

Ahluwalia U, Nayeem S, Deep S . The non-native conformations of cytochrome c in sodium dodecyl sulfate and their modulation by ATP. Eur Biophys J. 2010; 40(3):259-71. DOI: 10.1007/s00249-010-0643-6. View

15.

Forman H, Azzi A . On the virtual existence of superoxide anions in mitochondria: thoughts regarding its role in pathophysiology. FASEB J. 1997; 11(5):374-5. DOI: 10.1096/fasebj.11.5.9141504. View

16.

Kagan V, Tyurin V, Jiang J, Tyurina Y, Ritov V, Amoscato A . Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol. 2006; 1(4):223-32. DOI: 10.1038/nchembio727. View

17.

Kostrzewa A, Pali T, Froncisz W, Marsh D . Membrane location of spin-labeled cytochrome c determined by paramagnetic relaxation agents. Biochemistry. 2000; 39(20):6066-74. DOI: 10.1021/bi992559l. View

18.

Hong Y, Muenzner J, Grimm S, Pletneva E . Origin of the conformational heterogeneity of cardiolipin-bound cytochrome C. J Am Chem Soc. 2012; 134(45):18713-23. PMC: 3507619. DOI: 10.1021/ja307426k. View

19.

Feinberg B, Liu X, Ryan M, SCHEJTER A, Zhang C, MARGOLIASH E . Direct voltammetric observation of redox driven changes in axial coordination and intramolecular rearrangement of the phenylalanine-82-histidine variant of yeast iso-1-cytochrome c. Biochemistry. 1998; 37(38):13091-101. DOI: 10.1021/bi981037n. View

20.

Antalik M, Bagelova J . Effect of nucleotides on thermal stability of ferricytochrome C. Gen Physiol Biophys. 1995; 14(1):19-37. View