Home LiteratureArticle Details
PMID: 15972817 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria.

The Journal of biological chemistry ·Vol. 280 ·No. 33 ·2005-08-19 ·Pages 29403-8

Zhang M, Mileykovskaya E, Dowhan W

Abstract

Digitonin extracts of mitochondria from cardiolipin-containing (wild type) and cardiolipin-lacking (crd1Delta mutant) Saccharomyces cerevisiae subjected to colorless native polyacrylamide gel electrophoresis in the presence of 0.003% digitonin displayed a supercomplex composed of homodimers of complexes III and IV in the former case but only the individual homodimers in the latter case. To avoid treatment with any detergent or dye, we compared organization of the respiratory chain in intact mitochondria from wild type and cardiolipin-lacking cells by using a functional analysis developed previously for the study of the organization of the respiratory chain of S. cerevisiae (Boumans, H., Grivell, L. A., and Berden, J. A. (1998) J. Biol. Chem. 273, 4872-4877). Dependence of the kinetics of NADH oxidation via complexes III, IV, and cytochrome c on the concentration of the complex III-specific inhibitor antimycin A was studied. A linear relationship between respiratory activity and saturation of complex III with antimycin A was obtained for wild type mitochondria consistent with single functional unit kinetics of the respiratory chain. Under the same conditions, cardiolipin-lacking mitochondria displayed a hyperbolic relationship indicating cytochrome c pool behavior. No release of cytochrome c from cardiolipin-lacking mitochondria or mitoplasts under our standard experimental conditions was detected. Identical cytochrome c pool behavior was observed for both wild type and cardiolipin-lacking mitochondria in the presence of a chaotropic agent, which disrupts the interaction between respiratory complexes. The results demonstrate that cardiolipin is essential for association of complexes III and IV into a supercomplex in intact yeast mitochondria.

MeSH Terms
Antimycin A/pharmacology Cardiolipins/physiology Cytochromes c/metabolism Electron Transport Electron Transport Complex III/chemistry Electron Transport Complex IV/chemistry Mitochondria/enzymology Saccharomyces cerevisiae/enzymology Saccharomyces cerevisiae Proteins/chemistry
Chemicals
Cardiolipins Saccharomyces cerevisiae Proteins Antimycin A Cytochromes c Electron Transport Complex IV Electron Transport Complex III
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zhang Mei
Department of Biochemistry and Molecular Biology, University of Texas-Houston Medical School, 77225, USA.
Mileykovskaya Eugenia
Dowhan William
References (30)
30 references, click to expand
  1. Cytochromes c1 and b2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism.
    Cell. 1992 May 29;69(5):809-22 PMID: 1350514
  2. Cardiolipin in energy transducing membranes.
    Biochemistry (Mosc). 2005 Feb;70(2):154-8 PMID: 15807653
  3. Structural organization of the mitochondrial respiratory chain.
    Ital J Biochem. 2003 Mar;52(1):58-61 PMID: 12833641
  4. The cytochrome bc1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria.
    J Biol Chem. 2000 Jun 16;275(24):18093-8 PMID: 10764779
  5. The reaction of antimycin with a cytochrome b preparation active in reconstitution of the respiratory chain.
    Biochim Biophys Acta. 1970 Sep 1;216(2):237-49 PMID: 5504626
  6. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria.
    EMBO J. 2000 Apr 17;19(8):1777-83 PMID: 10775262
  7. The biosynthesis and functional role of cardiolipin.
    Prog Lipid Res. 2000 May;39(3):257-88 PMID: 10799718
  8. The respiratory chain in yeast behaves as a single functional unit.
    J Biol Chem. 1998 Feb 27;273(9):4872-7 PMID: 9478928
  9. Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane.
    J Biol Chem. 2002 Nov 15;277(46):43553-6 PMID: 12364341
  10. "Respirasome"-like supercomplexes in green leaf mitochondria of spinach.
    J Biol Chem. 2004 Nov 12;279(46):48369-75 PMID: 15342644
  11. Diversity and versatility of lipid-protein interactions revealed by molecular genetic approaches.
    Biochim Biophys Acta. 2004 Nov 3;1666(1-2):19-39 PMID: 15519306
  12. Pathways and energetics of mitochondrial protein import in Saccharomyces cerevisiae.
    Methods Enzymol. 1995;260:224-31 PMID: 8592447
  13. Cardiolipin is not required for Bax-mediated cytochrome c release from yeast mitochondria.
    J Biol Chem. 2004 Jan 9;279(2):1100-7 PMID: 14551208
  14. The ratio of oxidative phosphorylation complexes I-V in bovine heart mitochondria and the composition of respiratory chain supercomplexes.
    J Biol Chem. 2001 Oct 12;276(41):37861-7 PMID: 11483615
  15. Kinetic mechanism of beef heart ubiquinol:cytochrome c oxidoreductase.
    J Biochem. 1992 Jan;111(1):91-8 PMID: 1318882
  16. Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure.
    EMBO J. 2001 Dec 3;20(23):6591-600 PMID: 11726495
  17. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form.
    Anal Biochem. 1991 Dec;199(2):223-31 PMID: 1812789
  18. Respiratory chain supercomplexes of mitochondria and bacteria.
    Biochim Biophys Acta. 2002 Sep 10;1555(1-3):154-9 PMID: 12206908
  19. Lipids in membrane protein structures.
    Biochim Biophys Acta. 2004 Nov 3;1666(1-2):2-18 PMID: 15519305
  20. Purification and characterization of highly purified cytochrome b from complex III of baker's yeast.
    Biochim Biophys Acta. 1982 Sep 15;681(3):484-95 PMID: 6289886
  21. Further evidence for the pool function of ubiquinone as derived from the inhibition of the electron transport by antimycin.
    Eur J Biochem. 1973 Nov 15;39(2):313-23 PMID: 4359626
  22. Phospholipase A(2) digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure.
    Biochemistry. 1999 Nov 9;38(45):14966-72 PMID: 10555978
  23. The mitochondrial respiratory chain of yeast. Structure and biosynthesis and the role in cellular metabolism.
    Biochim Biophys Acta. 1987;895(3):205-39 PMID: 2849479
  24. Cardiolipin stabilizes respiratory chain supercomplexes.
    J Biol Chem. 2003 Dec 26;278(52):52873-80 PMID: 14561769
  25. Isolation of highly purified mitochondria from Saccharomyces cerevisiae.
    Methods Enzymol. 1995;260:213-23 PMID: 8592446
  26. Cardiolipin is not required to maintain mitochondrial DNA stability or cell viability for Saccharomyces cerevisiae grown at elevated temperatures.
    J Biol Chem. 2003 Sep 12;278(37):35204-10 PMID: 12840009
  27. Isolation and inactivation of the nuclear gene encoding the rotenone-insensitive internal NADH: ubiquinone oxidoreductase of mitochondria from Saccharomyces cerevisiae.
    Eur J Biochem. 1991 Feb 14;195(3):857-62 PMID: 1900238
  28. A method for the localization of sites for oxidative phosphorylation.
    Nature. 1955 Aug 6;176(4475):250-4 PMID: 13244669
  29. The role of phospholipids in the binding of antimycin to yeast Complex III.
    Biochim Biophys Acta. 1986 Nov 5;852(1):100-5 PMID: 3021213
  30. Phospholipase digestion of bound cardiolipin reversibly inactivates bovine cytochrome bc1.
    Biochemistry. 1999 Jul 13;38(28):9031-8 PMID: 10413476
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2005-08-19
Epub
2005-00-22
Pages
29403-8
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC4113954
Subset
IM
Grants
NIGMS NIH HHS · R01 GM056389 · United States
NIGMS NIH HHS · GM56389 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com