Skip to main content
SpringerLink
Log in

In Saccharomyces cerevisiae, Cations Control the Fate of the Energy Derived from Oxidative Metabolism Through the Opening and Closing of the Yeast Mitochondrial Unselective Channel

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

The yeast mitochondrial unspecific channel (YMUC) sensitivity to inorganic (Ca2+ or Mg2+) or organic (hexyl or octyl-guanidine) cations was measured. The rate of oxygen consumption in State 3 and State 4, the transmembrane potential (Δψ), mitochondrial swelling, and the polyethylene-glycol mediated recontraction were used to follow opening of the YMUC. Addition of 0.4 mM PO4 did not close the YMUC, although it did enhance the sensitivity to Ca2+ (I50 decreased from 50 to 0.3 mM) and Mg2+ (I50 decreased from 5 to 0.83 mM Mg2+). The Ca2+ concentration needed to close the YMUC was higher than the concentrations usually observed in the cell. Nonetheless, Mg2+, Ca2+, and PO4 exhibited additive effects. These cations did not inhibit contraction of preswollen mitochondria, suggesting that the YMUC/cation interaction was labile. Octyl-guanidine (OG-I50 7.5 μM) was the only cation which inhibited mitochondrial recontraction, probably as a result of membrane binding stabilization through its hydrophobic tail. The PO4-dependent, Ca2+/Mg2+-mediated closure of the YMUC may be a means to control the proportion of oxidative energy producing ATP or being lost as heat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • åkerman, K. E. O., and Wikstrom, M. K. F. (1976). FEBS Lett. 68, 191–197.

    Google Scholar 

  • Anraku, Y., Ohya, Y., and Iida, H. (1991). Biochim. Biophys. Acta 1903, 169–177.

    Google Scholar 

  • Ballarin, C., and Sorgato, M. C. (1995). J. Biol. Chem. 270, 19262–19268.

    Google Scholar 

  • Beaty, G., Gutiérrez, C., López-Vancell, R., and Estrada, S. (1986). Acta Physiol. Pharmacol. Latinoam. 36, 217–232.

    Google Scholar 

  • Beauvoit, B., Rigoulet, M., Bunoust, O., Raffard, G., Canioni, P., and Guérin, B. (1993). Eur. J. Biochem. 214, 163–172.

    Google Scholar 

  • Bernardi, P. (1996). Biochim. Biophys. Acta 1275, 5–9.

    Google Scholar 

  • Bernardi, P., and Petronilli, B. (1996). J. Bioenerg. Biomembr. 28, 131–138.

    Google Scholar 

  • Bernardi, P., Veronese, P., and Petronilli, B. (1993). J. Biol. Chem. 268, 1005–1010.

    Google Scholar 

  • Bradshaw, P. C., Jung, D., and Pfeifer, D. R. (2001). J. Biol. Chem. 276, 40502–40609.

    Google Scholar 

  • Castrejón, V., Parra, C., Moreno, R., Peña, A., and Uribe, S. (1997). Arch. Biochem. Biophys. 346, 37–44.

    Google Scholar 

  • Chávez, E., Peña A., Zazueta, C., Ramírez, J., García, N., and Carrillo, R. (2000). J. Bioenerg. Biomembr. 32, 193–198.

    Google Scholar 

  • Corkey, B. E., Duszynsky, J., Rich, T. L., Mat-Schinsky, B., and Williamson, J. R. (1986). J. Biol. Chem. 261, 2567–2574.

    Google Scholar 

  • Cortés, P., Castrejón, V., Sampedro, J. G., and Uribe, S. (2000). Biochim. Biophys. Acta 1456, 67–76.

    Google Scholar 

  • Crompton, M. (1999). Biochem. J. 341, 233–249.

    Google Scholar 

  • Dejean, L., Beauvoit, B., Alonso, A., Bunoust, O., Guérin, B., and Rigoulet, M. (2002). Biochim. Biophys. Acta 1554, 159–169.

    Google Scholar 

  • Dejean, L., Beauvoit, B., Guérin, B., and Rigoulet, M. (2000). Biochim. Biophys. Acta 1457, 45–56.

    Google Scholar 

  • De-kloet, S. R., Van Wermeskerken, R. K. A., and Konigsberger, V. V. (1961). Biochim. Biophys. Acta 47, 138–143.

    Google Scholar 

  • Denton, R. M., and McCormack, J. G. (1980). FEBS Lett. 119, 1–8.

    Google Scholar 

  • Estabrook, R. W. (1967). Methods Enzymol. 10, 41–47.

    Google Scholar 

  • Garlid, K. D. (1988). In Integration of Mitochondria Function (Lemasters, J. J., Hackenbrock, C. R., Thurman, R. G., and Westerhoff, H. V., eds.), Plenum, New York, pp. 259–278.

    Google Scholar 

  • Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., Galibert, F., Hoheisel, J. D., Jacq, C., Johnston, M., Louis, E. J., Mewes, H. W., Murakami, Y., Philippsen, P., Tettelin, H., and Oliver S. G. (1996). Science 274, 546–567.

    Google Scholar 

  • Gómez-Puyou, A., and Tuena, M. (1977). J. Bioenerg. Biomembr. 9, 91–102.

    Google Scholar 

  • Gornal, A. G., Bardavill, C. J., and David, M. M. (1949). J. Biol. Chem. 177, 751–760.

    Google Scholar 

  • Gunter, T. E., and Pfeiffer, D. R. (1990). Am. J. Physiol. 258, C755-C786.

    Google Scholar 

  • Halestrap, A. P., and Davidson A. M. (1990). Biochem. J. 268, 153–160.

    Google Scholar 

  • Haworth, R. A., and Hunter, D. R. (1979). Arch. Biochem. Biophys. 195, 460–467.

    Google Scholar 

  • Ichaz, F., Jouaville, L. S., and Mazat, J. P. (1997). Cell 89, 1145–1153.

    Google Scholar 

  • Jung, D. W., Bradshaw, P. C., and Pfeiffer, D. R. (1997). J. Biol. Chem. 272, 21104–21112.

    Google Scholar 

  • Jung, D. W., and Brierley, G. P. (1986). J. Biol. Chem. 261, 6408–6415.

    Google Scholar 

  • Lemasters, J. J., Nieminen, A. L., Quian, T., Trost, L. C., Elmore, S. P., Nishimura, Y., Crowe, R. A., Cascio, W. E., Bradham, C. A., Brenner, D. A., and Herman, B. (1998). Biochim. Biophys. Acta 1366, 177–196.

    Google Scholar 

  • Lohret, T. A., and Kinnally, K. W. (1995). J. Biol. Chem. 270, 15950–15953.

    Google Scholar 

  • Madeo, F., Frohlich, E., Ligr, M., Grey, M., Sigrist, S. J., Wolf, D. H., and Frohlich, K. U. (1999). J. Cell. Biol. 145, 757–767.

    Google Scholar 

  • Manon, S., and Guérin, M. (1992). Biochim. Biophys. Acta 1108, 169–176.

    Google Scholar 

  • Manon, S., Roucou, X., Guerin, M., Rigoulet, M., and Guerin, B. (1998). J. Bioenerg. Biomembr. 30, 419–429.

    Google Scholar 

  • Masiacos, P. T., Williams, D. G., Berkich, D. A., Smith, M. B., and LaNoue, K. F. (1991). Biochemistry 30, 8351–8357.

    Google Scholar 

  • Matsuyama, S., Nouraini, S., and Reed, J. C. (1999). Curr. Opin. Microbiol. 2, 618–623.

    Google Scholar 

  • Nakajima-Shimada, J., Iida, H., Tsuji, F. L., and Anraku, Y. (1991). Proc. Natl. Acad. Sci. U.S.A. 88, 6878–6882.

    Google Scholar 

  • Nichols, B. J., Rigoulet, M., and Denton, R. M. (1994). Biochem. J. 303, 461–465.

    Google Scholar 

  • Papa, S., Tuena de Gómez-Puyou, M., and Gómez-Puyou, A. (1975). Eur. J. Biochem. 55, 1–8.

    Google Scholar 

  • Peña, A., Piña, M. Z., Escamilla, E., and Piña, E. (1977). FEBS Lett. 80, 209–213.

    Google Scholar 

  • Pérez-Vázquez, V., Ramírez, J., Aguilera-Aguirre, L., González-Hernández, J. C., Clemente-Guerrero, M., Manzo-ávalos, S., Uribe S., and Saavedra-Molina, A. (2002). Amino Acids 22, 405–416.

    Google Scholar 

  • Pfeiffer, D. R., Gudz, T. I., Novgorodov, S. A., and Erdahl, W. L. (1995). J. Biol. Chem. 270, 4923–4932.

    Google Scholar 

  • Pressman (1963). J. Biol. Chem. 238, 401–409.

    Google Scholar 

  • Prieto, S., Bouillaud, F., Ricquier, D., and Rial, E. (1992). Eur. J. Biochem. 208, 487–491.

    Google Scholar 

  • Romani, A., Marfella, C., and Scarpa, A. (1993). J. Biol. Chem. 268, 15489–15495.

    Google Scholar 

  • Romani, A., and Scarpa, A. (1992). Arch. Biochem. Biophys. 298, 1–12.

    Google Scholar 

  • Romani, A., and Scarpa, A. (2000). Front. Biosci. 5, D720–D734.

    Google Scholar 

  • Roucou, X., Manon, S., and Guérin, M. (1997). Biochem. Mol. Biol. Int. 43, 53–61.

    Google Scholar 

  • Shikama, K. (1971). Arch. Biochem. Biophys. 147, 311–317.

    Google Scholar 

  • Szabo, I., Bathori, G., Wolf, D., Stare, T., Cola, C., and Zoratti, M. (1995). Biochim. Biophys. Acta 1235, 115–125.

    Google Scholar 

  • Szabo, I., Bernardi, P., and Zoratti, M. (1992). J. Biol. Chem. 267, 2940–2946.

    Google Scholar 

  • Uribe, S., Ramirez, J., and Peña, A. (1985). J. Bacteriol. 161, 1195–2000.

    Google Scholar 

  • Uribe, S., Rangel, P., and Pardo, J. P. (1992). Cell Calcium 13, 211–217.

    Google Scholar 

  • Uribe, S., Rangel, P., Pardo, J. P., and Pereira-da-Silva L. (1993). Eur. J. Biochem. 258, 817–821.

    Google Scholar 

  • Velours, J., Rigoulet, M., and Guéran, B. (1977). FEBS Lett. 81, 18–22.

    Google Scholar 

  • Welihinda, A. A., Trumbly, R. J., Garlid, K. D., and Beavis, A. D. (1993). Biochim. Biophys. Acta 1144, 367–373.

    Google Scholar 

  • Zhu, B., Wan, C. M., Liu, R. T., Sun, A. M., Huang, S., and Wang, Z. R. (2002). Space Med. Eng. 15, 355–358.

    Google Scholar 

  • Zoratti, M., and Szabo, I. (1995). Biochim. Biophys. Acta 1241, 139–176.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Instituto de Fisiología Celular, UNAM, México, DF, México

    Victoriano Pérez-Vázquez & Salvador Uribe

  2. Instituto de Investigaciones Químico-Biológicas UMSNH, México, DF, México

    Alfredo Saavedra-Molina

Authors
  1. Victoriano Pérez-Vázquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alfredo Saavedra-Molina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Salvador Uribe
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pérez-Vázquez, V., Saavedra-Molina, A. & Uribe, S. In Saccharomyces cerevisiae, Cations Control the Fate of the Energy Derived from Oxidative Metabolism Through the Opening and Closing of the Yeast Mitochondrial Unselective Channel. J Bioenerg Biomembr 35, 231–241 (2003). https://doi.org/10.1023/A:1024659615022

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024659615022

Search

Navigation