Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1995 May 1;307(Pt 3):657–661. doi: 10.1042/bj3070657

The mechanism for the ATP-induced uncoupling of respiration in mitochondria of the yeast Saccharomyces cerevisiae.

S Prieto 1, F Bouillaud 1, E Rial 1
PMCID: PMC1136701  PMID: 7741693

Abstract

We have recently reported that ATP induces an uncoupling pathway in Saccharomyces cerevisiae mitochondria [Prieto, Bouillaud, Ricquier and Rial (1992) Eur. J. Biochem. 208, 487-491]. The presence of this pathway would explain the reported low efficiency of oxidative phosphorylation in S. cerevisiae, and may represent one of the postulated energy-dissipating mechanisms present in these yeasts. In this paper we demonstrate that ATP exerts its action in two steps: first, at low ATP/Pi ratios, it increases the respiratory-chain activity, probably by altering the kinetic properties of cytochrome c oxidase. Second, at higher ATP/Pi ratios, an increase in membrane permeability leads to a collapse in membrane potential. The ATP effect on cytochrome c oxidase corroborates a recent report showing that ATP interacts specifically with yeast cytochrome oxidase, stimulating its activity [Taanman and Capaldi (1993) J. Biol. Chem. 268, 18754-18761].

Full text

PDF
657

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arechaga I., Raimbault S., Prieto S., Levi-Meyrueis C., Zaragoza P., Miroux B., Ricquier D., Bouillaud F., Rial E. Cysteine residues are not essential for uncoupling protein function. Biochem J. 1993 Dec 15;296(Pt 3):693–700. doi: 10.1042/bj2960693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balcavage W. X., Mattoon J. R. Properties of Saccharomyces cerevisiae mitochondria prepared by a mechanical method. Biochim Biophys Acta. 1968 Apr 2;153(3):521–530. doi: 10.1016/0005-2728(68)90182-5. [DOI] [PubMed] [Google Scholar]
  3. Beauvoit B., Rigoulet M., Bunoust O., Raffard G., Canioni P., Guérin B. Interactions between glucose metabolism and oxidative phosphorylations on respiratory-competent Saccharomyces cerevisiae cells. Eur J Biochem. 1993 May 15;214(1):163–172. doi: 10.1111/j.1432-1033.1993.tb17909.x. [DOI] [PubMed] [Google Scholar]
  4. Bisson R., Schiavo G., Montecucco C. ATP induces conformational changes in mitochondrial cytochrome c oxidase. Effect on the cytochrome c binding site. J Biol Chem. 1987 May 5;262(13):5992–5998. [PubMed] [Google Scholar]
  5. Ferguson-Miller S., Brautigan D. L., Margoliash E. Correlation of the kinetics of electron transfer activity of various eukaryotic cytochromes c with binding to mitochondrial cytochrome c oxidase. J Biol Chem. 1976 Feb 25;251(4):1104–1115. [PubMed] [Google Scholar]
  6. Fitton V., Rigoulet M., Ouhabi R., Guérin B. Mechanistic stoichiometry of yeast mitochondrial oxidative phosphorylation. Biochemistry. 1994 Aug 16;33(32):9692–9698. doi: 10.1021/bi00198a039. [DOI] [PubMed] [Google Scholar]
  7. Guérin B., Bunoust O., Rouqueys V., Rigoulet M. ATP-induced unspecific channel in yeast mitochondria. J Biol Chem. 1994 Oct 14;269(41):25406–25410. [PubMed] [Google Scholar]
  8. Guérin B., Labbe P., Somlo M. Preparation of yeast mitochondria (Saccharomyces cerevisiae) with good P/O and respiratory control ratios. Methods Enzymol. 1979;55:149–159. doi: 10.1016/0076-6879(79)55021-6. [DOI] [PubMed] [Google Scholar]
  9. Hüther F. J., Kadenbach B. Specific effects of ATP on the kinetics of reconstituted bovine heart cytochrome-c oxidase. FEBS Lett. 1986 Oct 20;207(1):89–94. doi: 10.1016/0014-5793(86)80018-7. [DOI] [PubMed] [Google Scholar]
  10. Lagunas R. Energy metabolism of Saccharomyces cerevisiae discrepancy between ATP balance and known metabolic functions. Biochim Biophys Acta. 1976 Sep 13;440(3):661–674. doi: 10.1016/0005-2728(76)90049-9. [DOI] [PubMed] [Google Scholar]
  11. Lagunas R., Gancedo C. Role of phosphate in the regulation of the Pasteur effect in Saccharomyces cerevisiae. Eur J Biochem. 1983 Dec 15;137(3):479–483. doi: 10.1111/j.1432-1033.1983.tb07851.x. [DOI] [PubMed] [Google Scholar]
  12. Manon S., Guerin M. Modifications of oxidative phosphorylations in mitochondria isolated from a mutant of Saccharomyces cerevisiae. Possible alterations of the phosphate transport. Eur J Biochem. 1988 Feb 15;172(1):205–211. doi: 10.1111/j.1432-1033.1988.tb13874.x. [DOI] [PubMed] [Google Scholar]
  13. Ohnishi T., Kawaguchi K., Hagihara B. Preparation and some properties of yeast mitochondria. J Biol Chem. 1966 Apr 25;241(8):1797–1806. [PubMed] [Google Scholar]
  14. Onishi T. Induction of the site I phosphorylation in vivo in Saccharomyces carlsbergensis. Biochem Biophys Res Commun. 1970 Oct 23;41(2):344–352. doi: 10.1016/0006-291x(70)90510-3. [DOI] [PubMed] [Google Scholar]
  15. Prieto S., Bouillaud F., Ricquier D., Rial E. Activation by ATP of a proton-conducting pathway in yeast mitochondria. Eur J Biochem. 1992 Sep 1;208(2):487–491. doi: 10.1111/j.1432-1033.1992.tb17212.x. [DOI] [PubMed] [Google Scholar]
  16. Rigoulet M., Guerin B., Denis M. Modification of flow-force relationships by external ATP in yeast mitochondria. Eur J Biochem. 1987 Oct 15;168(2):275–279. doi: 10.1111/j.1432-1033.1987.tb13417.x. [DOI] [PubMed] [Google Scholar]
  17. Rothman L. B., Cabib E. Regulation of glycogen synthesis in the intact yeast cell. Biochemistry. 1969 Aug;8(8):3332–3341. doi: 10.1021/bi00836a030. [DOI] [PubMed] [Google Scholar]
  18. Rottenberg H. The measurement of membrane potential and deltapH in cells, organelles, and vesicles. Methods Enzymol. 1979;55:547–569. doi: 10.1016/0076-6879(79)55066-6. [DOI] [PubMed] [Google Scholar]
  19. Taanman J. W., Capaldi R. A. Subunit VIa of yeast cytochrome c oxidase is not necessary for assembly of the enzyme complex but modulates the enzyme activity. Isolation and characterization of the nuclear-coded gene. J Biol Chem. 1993 Sep 5;268(25):18754–18761. [PubMed] [Google Scholar]
  20. Velours J., Rigoulet M., Guerin B. Protection of yeast mitochondrial structure by phosphate and other H+-donating anions. FEBS Lett. 1977 Sep 1;81(1):18–22. doi: 10.1016/0014-5793(77)80918-6. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES