Activation of Cytochrome C Peroxidase Function Through Coordinated Foldon Loop Dynamics upon Interaction with Anionic Lipids.

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Abstrakt

Tytuł:: Activation of Cytochrome C Peroxidase Function Through Coordinated Foldon Loop Dynamics upon Interaction with Anionic Lipids.
Autorzy:: Li M; Department of Structural Biology, University of Pittsburgh, Pittsburgh, PA 15213, USA.
Sun W; Department of Environmental and Occupational Health, University of Pittsburgh, Pittsburgh, PA 15213, USA; Center for Free Radical and Antioxidant Health, University of Pittsburgh, Pittsburgh, PA 15213, USA.
Tyurin VA; Department of Environmental and Occupational Health, University of Pittsburgh, Pittsburgh, PA 15213, USA; Center for Free Radical and Antioxidant Health, University of Pittsburgh, Pittsburgh, PA 15213, USA.
DeLucia M; Department of Structural Biology, University of Pittsburgh, Pittsburgh, PA 15213, USA.
Ahn J; Department of Structural Biology, University of Pittsburgh, Pittsburgh, PA 15213, USA.
Kagan VE; Department of Environmental and Occupational Health, University of Pittsburgh, Pittsburgh, PA 15213, USA; Center for Free Radical and Antioxidant Health, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Chemistry, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Pharmacology and Chemical Biology, University of Pittsburgh, Pittsburgh, PA 15213, USA; Institute for Regenerative Medicine, IM Sechenov, Moscow State Medical University, Moscow 119146, Russian Federation.
van der Wel PCA; Department of Structural Biology, University of Pittsburgh, Pittsburgh, PA 15213, USA; Zernike Institute for Advanced Materials, University of Groningen, Groningen, the Netherlands. Electronic address: .
Źródło:: Journal of molecular biology [J Mol Biol] 2021 Jul 23; Vol. 433 (15), pp. 167057. Date of Electronic Publication: 2021 May 24.
Typ publikacji:: Comparative Study; Journal Article; Research Support, N.I.H., Extramural
Język:: English
Imprint Name(s):: Publication: Amsterdam : Elsevier
Original Publication: 1959- : London : Academic Press
MeSH Terms:: Cardiolipins/*metabolism
Cytochrome-c Peroxidase/*chemistry
Cytochrome-c Peroxidase/*metabolism
Phosphatidylglycerols/*metabolism
Cytochromes c/metabolism ; Gene Expression Regulation ; Magnetic Resonance Spectroscopy ; Models, Molecular ; Nuclear Magnetic Resonance, Biomolecular ; Protein Conformation
References:: Nature. 2007 Dec 13;450(7172):964-72. (PMID: 18075575)
Mol Aspects Med. 2010 Feb;31(1):1-20. (PMID: 19698742)
J Mol Biol. 2020 Jul 24;432(16):4722-4744. (PMID: 32598938)
J Phys Chem B. 2019 Oct 24;123(42):8939-8953. (PMID: 31557440)
Proc Natl Acad Sci U S A. 2016 Apr 5;113(14):3809-14. (PMID: 26966231)
J Mol Biol. 2004 Oct 8;343(1):223-33. (PMID: 15381432)
J Biomol NMR. 2017 Mar;67(3):165-178. (PMID: 28229262)
Mitochondrion. 2019 Nov;49:305-313. (PMID: 31351921)
Biophys Rev. 2018 Aug;10(4):1151-1185. (PMID: 29574621)
Nat Rev Mol Cell Biol. 2008 Jul;9(7):532-42. (PMID: 18568041)
J Phys Chem B. 2020 Apr 9;124(14):2769-2777. (PMID: 32182433)
J Biol Chem. 2015 Dec 25;290(52):30879-87. (PMID: 26487716)
J Biol Chem. 2004 Jul 30;279(31):32294-300. (PMID: 15169766)
Annu Rev Biophys. 2018 May 20;47:201-222. (PMID: 29498890)
Biochemistry. 2000 May 23;39(20):6066-74. (PMID: 10821679)
Biochim Biophys Acta. 1982 Jul 28;689(2):337-45. (PMID: 6180764)
Nat Chem Biol. 2005 Sep;1(4):223-32. (PMID: 16408039)
Biophys J. 2014 Aug 19;107(4):879-90. (PMID: 25140423)
Sci Rep. 2018 Mar 20;8(1):4919. (PMID: 29559686)
J Phys Chem B. 2018 Jun 28;122(25):6471-6482. (PMID: 29693387)
Oxid Med Cell Longev. 2020 Apr 17;2020:6813405. (PMID: 32377304)
J Biol Inorg Chem. 2020 May;25(3):467-487. (PMID: 32189145)
Free Radic Biol Med. 2020 Feb 1;147:231-241. (PMID: 31883467)
Biochemistry. 1991 Jul 23;30(29):7219-24. (PMID: 1649625)
J Fluoresc. 2018 Jan;28(1):79-88. (PMID: 28879486)
Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14778-82. (PMID: 12407175)
Sci Rep. 2016 Jul 27;6:30447. (PMID: 27461282)
J Phys Chem B. 2015 Jan 29;119(4):1334-49. (PMID: 25469712)
Solid State Nucl Magn Reson. 2019 Apr;98:1-11. (PMID: 30641444)
Methods. 2018 Sep 15;148:123-135. (PMID: 29702226)
J Membr Biol. 2004 Mar 1;198(1):43-53. (PMID: 15209096)
J Biol Inorg Chem. 2017 Jan;22(1):19-29. (PMID: 27826772)
Biochim Biophys Acta. 2012 Sep;1818(9):2135-48. (PMID: 22583835)
Metallomics. 2011 Apr;3(4):319-22. (PMID: 21264390)
J Biol Chem. 1992 Nov 5;267(31):22243-8. (PMID: 1331048)
Biochemistry. 1991 Apr 23;30(16):3880-5. (PMID: 1850291)
J Phys Chem B. 2015 Oct 8;119(40):12846-59. (PMID: 26369421)
Proc Natl Acad Sci U S A. 2019 Oct 15;116(42):21031-21036. (PMID: 31570587)
Biochemistry. 1991 Apr 23;30(16):3871-9. (PMID: 1850290)
Biophys Physicobiol. 2019 Jan 31;16:18-27. (PMID: 30775200)
Biochemistry. 1994 Mar 8;33(9):2451-8. (PMID: 8117705)
FEBS Lett. 1995 Mar 6;360(3):255-60. (PMID: 7883043)
ACS Omega. 2019 Jan 16;4(1):1386-1400. (PMID: 31459406)
Biochemistry. 2017 Apr 4;56(13):1887-1898. (PMID: 28277678)
Biochemistry. 1992 Feb 18;31(6):1636-43. (PMID: 1310614)
J Am Chem Soc. 2020 Nov 18;142(46):19532-19539. (PMID: 33156621)
J Biomol NMR. 1995 Nov;6(3):277-93. (PMID: 8520220)
Biophys J. 1993 Dec;65(6):2408-17. (PMID: 8312479)
Front Cell Dev Biol. 2017 Sep 29;5:90. (PMID: 29034233)
Soft Matter. 2015 Jan 7;11(1):130-8. (PMID: 25369786)
Prog Lipid Res. 2000 May;39(3):257-88. (PMID: 10799718)
Free Radic Biol Med. 2009 Jun 1;46(11):1439-53. (PMID: 19285551)
Acc Chem Res. 2010 May 18;43(5):652-60. (PMID: 20143816)
J Phys Chem B. 2011 Nov 24;115(46):13723-30. (PMID: 22004429)
J Biol Chem. 1994 Jan 21;269(3):1770-4. (PMID: 8294426)
Proc Natl Acad Sci U S A. 2013 Apr 16;110(16):6269-74. (PMID: 23576757)
J Mol Biol. 1990 Jul 20;214(2):585-95. (PMID: 2166170)
Biochim Biophys Acta. 2016 Jan;1857(1):34-45. (PMID: 26482708)
Proteins. 2006 May 1;63(2):349-55. (PMID: 16287119)
Semin Cell Dev Biol. 2018 Apr;76:201-212. (PMID: 28754444)
Chem Rev. 2017 Nov 8;117(21):13382-13460. (PMID: 29027792)
J Biol Chem. 1995 Feb 17;270(7):3197-202. (PMID: 7852404)
Biochemistry. 2008 Dec 23;47(51):13699-710. (PMID: 19053260)
Biophys J. 2016 Nov 1;111(9):1965-1973. (PMID: 27806278)
J Biol Chem. 1998 Jun 12;273(24):14933-41. (PMID: 9614098)
Biochim Biophys Acta Biomembr. 2017 Jan;1859(1):61-68. (PMID: 27984017)
Proc Natl Acad Sci U S A. 2012 Jan 3;109(1):125-30. (PMID: 22190488)
Biochim Biophys Acta. 1983 Jul 27;732(2):473-8. (PMID: 6871211)
Nat Commun. 2017 May 24;8:15462. (PMID: 28537272)
Int J Radiat Oncol Biol Phys. 2007 Sep 1;69(1):176-86. (PMID: 17707271)
J Biol Inorg Chem. 2013 Mar;18(3):289-97. (PMID: 23334161)
Biophys J. 2008 Jun;94(12):4828-36. (PMID: 18326641)
Chem Phys Lipids. 2014 Apr;179:11-6. (PMID: 24144810)
Cell Death Differ. 2007 Mar;14(3):597-606. (PMID: 16888643)
Biochemistry. 2016 Jan 26;55(3):407-28. (PMID: 26720007)
J Am Chem Soc. 2012 Nov 14;134(45):18713-23. (PMID: 23066867)
Chem Phys Lipids. 2015 Dec;193:1-10. (PMID: 26415690)
Acc Chem Res. 2013 Sep 17;46(9):2028-36. (PMID: 23875699)
J Alzheimers Dis. 2014;42 Suppl 3:S125-52. (PMID: 25056458)
Cell Growth Differ. 2002 Sep;13(9):449-55. (PMID: 12354754)
Biochemistry. 2017 Sep 12;56(36):4830-4839. (PMID: 28813137)
Biochim Biophys Acta. 2006 May-Jun;1757(5-6):648-59. (PMID: 16740248)
Biophys J. 2015 Nov 3;109(9):1873-84. (PMID: 26536264)
Mol Pharmacol. 2006 Aug;70(2):706-17. (PMID: 16690782)
Structure. 2019 May 7;27(5):806-815.e4. (PMID: 30879887)
Proc Natl Acad Sci U S A. 2005 Mar 29;102(13):4741-6. (PMID: 15774579)
Biochemistry. 2006 Apr 18;45(15):4998-5009. (PMID: 16605268)
Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1259-63. (PMID: 11818574)
Biochemistry. 2007 Dec 11;46(49):14232-44. (PMID: 18004876)
J Phys Chem B. 2013 Oct 24;117(42):12878-86. (PMID: 23713573)
J Inorg Biochem. 2020 Feb;203:110924. (PMID: 31760234)
Biophys Chem. 1995 May;54(3):271-8. (PMID: 7749061)
Eur Biophys J. 1991;20(3):183-91. (PMID: 1660398)
Grant Information:: P01 HL114453 United States HL NHLBI NIH HHS; R01 GM113908 United States GM NIGMS NIH HHS; S10 OD012213 United States OD NIH HHS; U19 AI068021 United States AI NIAID NIH HHS
Contributed Indexing:: Keywords: lipid peroxidation; lipidomics; mitochondrial apoptosis; peripheral membrane proteins; solid-state NMR spectroscopy
Substance Nomenclature:: 0 (Cardiolipins)
0 (Phosphatidylglycerols)
9007-43-6 (Cytochromes c)
EC 1.11.1.5 (Cytochrome-c Peroxidase)
Entry Date(s):: Date Created: 20210525 Date Completed: 20210920 Latest Revision: 20220724
Update Code:: 20240105
PubMed Central ID:: PMC8380053
DOI:: 10.1016/j.jmb.2021.167057
PMID:: 34033821
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Cardiolipin (CL) is a mitochondrial anionic lipid that plays important roles in the regulation and signaling of mitochondrial apoptosis. CL peroxidation catalyzed by the assembly of CL-cytochrome c (cyt c) complexes at the inner mitochondrial membrane is a critical checkpoint. The structural changes in the protein, associated with peroxidase activation by CL and different anionic lipids, are not known at a molecular level. To better understand these peripheral protein-lipid interactions, we compare how phosphatidylglycerol (PG) and CL lipids trigger cyt c peroxidase activation, and correlate functional differences to structural and motional changes in membrane-associated cyt c. Structural and motional studies of the bound protein are enabled by magic angle spinning solid state NMR spectroscopy, while lipid peroxidase activity is assayed by mass spectrometry. PG binding results in a surface-bound state that preserves a nativelike fold, which nonetheless allows for significant peroxidase activity, though at a lower level than binding its native substrate CL. Lipid-specific differences in peroxidase activation are found to correlate to corresponding differences in lipid-induced protein mobility, affecting specific protein segments. The dynamics of omega loops C and D are upregulated by CL binding, in a way that is remarkably controlled by the protein:lipid stoichiometry. In contrast to complete chemical denaturation, membrane-induced protein destabilization reflects a destabilization of select cyt c foldons, while the energetically most stable helices are preserved. Our studies illuminate the interplay of protein and lipid dynamics in the creation of lipid peroxidase-active proteolipid complexes implicated in early stages of mitochondrial apoptosis.
Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
(Copyright © 2021 The Author(s). Published by Elsevier Ltd.. All rights reserved.)

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