Skip to main content
SpringerLink
Log in

The Effect of N-Ethylmaleimide on Permeability Transition as Induced by Carboxyatractyloside, Agaric Acid, and Oleate

  • Original Paper
  • Published:
Cell Biochemistry and Biophysics Aims and scope Submit manuscript

Abstract

In this work, we studied the effect of N-ethylmaleimide on permeability transition. The findings indicate that the amine inhibited the effects of carboxyatractyloside and agaric acid. It is known that these reagents interact with the adenine nucleotide carrier through the cytosolic side. When oleate, which interacts through the matrix side, was used it was found that the amine amplified the effects of oleate on permeability transition. The results also show that N-ethylmaleimide strengthened the inhibition induced by carboxyatractyloside, agaric acid, and oleate on ADP exchange. Furthermore, it was also found that oleate improved the binding of eosin-5-maleimide on the adenine nucleotide translocase.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Zoratti, M., & Szabó, I. (1995). The mitochondrial permeability transition. Biochimica et Biophysica Acta, 1241, 139–176.

    PubMed  Google Scholar 

  2. Bernardi, P., Krauskopf, A., Basso, E., Petronilli, V., Blalchy-Dyson, E., Di Lisa, F., et al. (2006). The mitochondrial permeability transition from in vitro artifact to disease target. FEBS Journal, 273, 2077–2099.

    Article  PubMed  CAS  Google Scholar 

  3. LeQuoc, K., & LeQuoc, D. (1998). Involvement of the ADP/ATP carrier in calcium-induced perturbations of the mitochondrial inner membrane permeability: Importance of the orientation of the nucleotide binding site. Archives of Biochemistry and Biophysics, 265, 249–257.

    Article  Google Scholar 

  4. Haworth, R. A., & Hunter, D. R. (2000). Control of the mitochondrial permeability transition pore by high-affinity ADP binding at the ADP/ATP translocase in permeabilized mitochondria. Journal of Bioenergetics and Biomembranes, 32, 91–96.

    Article  PubMed  CAS  Google Scholar 

  5. McStay, G., Clarke, S. J., & Halestrap, A. P. (2002). Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore. Biochemical Journal, 367, 541–548.

    Article  PubMed  CAS  Google Scholar 

  6. Majima, E., Koike, H., Hong, Y.-M., Shinohara, Y., & Terada, H. (1993). Characterization of cysteine residues of mitochondrial ADP/ATP carrier with the SH-reagents eosin 5-maleimide and N-ethylmaleimide. Journal of Biological Chemistry, 268, 22181–22187.

    PubMed  CAS  Google Scholar 

  7. Aquila, H., Eiermann, W., & Klingenberg, M. (1982). Incorporation of N-ethylmaleimide into the membrane-bound ADP/ATP translocator. Isolation of the protein labeled with N-[3H] ethylmaleimide. European Journal of Biochemistry, 122, 133–139.

    Article  PubMed  CAS  Google Scholar 

  8. Majima, E., Shinohara, Y., Yamaguchi, N., Hong, Y. M., & Terada, H. (1994). Importance of loops of mitochondrial ADP/ATP carrier for its transport activity deduced from reactivities of its cysteine residues with the sulfhydryl reagent eosin-5-maleimide. Biochemistry, 33, 9530–9536.

    Article  PubMed  CAS  Google Scholar 

  9. García, N., Zazueta, C., Pavón, N., & Chávez, E. (2005). Agaric acid induces mitochondrial permeability transition through its interaction with the adenine nucleotide translocase. Its dependence on membrane fluidity. Mitochondrion, 5, 272–281.

    Article  PubMed  Google Scholar 

  10. Andreyev, A. Y., Bondareva, T. O., Dedukhova, V. I., Mokhova, E. N., Skulachev, V. P., & Volkov, N. I. (1988). Carboxyatractyloside inhibits the uncoupling effect of free fatty acids. FEBS Letters, 226, 265–269.

    Article  PubMed  Google Scholar 

  11. Andreyev, A. Y., Bondareva, T. O., Dedukhova, V. I., Mokhova, E. N., Skulachev, V. P., Tsofina, L. M., et al. (1989). The ATP/ADP-antiporter is involved in the uncoupling effect of fatty acids on mitochondria. European Journal of Biochemistry, 182, 585–592.

    Article  PubMed  Google Scholar 

  12. Skulachev, V. P. (1999). Anion carriers in fatty acid-mediated physiological uncoupling. Journal of Bioenergetics and Biomembranes, 31, 431–435.

    Article  PubMed  CAS  Google Scholar 

  13. Schönfeld, P., & Bohnensack, R. (1997). Fatty acid-promoted mitochondrial permeability transition by membrane depolarization and binding to the ADP/ATP carrier. FEBS Letters, 420, 167–170.

    Article  PubMed  Google Scholar 

  14. Wojtczak, L., Weickowski, M. R., & Schonfeld, P. (1998). Protonophoric activity of fatty acid analogs and derivatives in the inner mitochondrial membrane: A further argument for the fatty acid cycling model. Archives of Biochemistry and Biophysics, 357, 76–84.

    Article  PubMed  CAS  Google Scholar 

  15. Skulachev, V. P. (1998). Uncoupling: New approaches to an old problem of bioenergetics. Biochimica et Biophysica Acta, 1363, 100–124.

    Article  PubMed  CAS  Google Scholar 

  16. Brustovetsky, N., & Klingenberg, M. (1994). The reconstituted ADP/ATP carrier can mediate H+ transport by free fatty acids, which is further stimulated by mersalyl. Journal of Biological Chemistry, 269, 27329–27336.

    PubMed  CAS  Google Scholar 

  17. Mironova, G. D., Gateau-Roesch, O., Levrat, C., Gritsenko, E., Pavlov, E., Lazareva, A. V., et al. (2002). Palmitic and stearic acids bind Ca2+ with high affinity and form nonspecific channels in black-lipid membranes. Possible relation to Ca2+-activated mitochondrial pores. Journal of Bioenergetics and Biomembranes, 33, 319–331.

    Article  Google Scholar 

  18. Chávez, E., Zazueta, C., & García, N. (1999). Carboxyatractyloside increases the effect of oleate on mitochondrial permeability transition. FEBS Letters, 445, 189–191.

    Article  PubMed  Google Scholar 

  19. Lowry, O. H., Rosebrough, N., Farr, A. L., & Randal, R. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193, 262–275.

    Google Scholar 

  20. Brustovetsky, N. N., Dedukhova, V. I., Egorova, M. V., Mokhova, E. N., & Skulachev, V. P. (1990). Inhibitors of the ATP/ADP antiporter suppress stimulation of mitochondrial respiration and H+ permeability transition by palmitate and anionic detergents. FEBS Letters, 272, 187–189.

    Article  PubMed  CAS  Google Scholar 

  21. Schönfeld, P., & Wojtczak, L. (2007). Fatty acids decrease mitochondrial generation of reactive oxygen species at the reverse electron transport but increase it at the forward transport. Biochimica et Biophysica Acta, 1767, 1032–1040.

    Article  PubMed  Google Scholar 

  22. García, N., Martínez-Abundis, E., Pavón, N., & Chávez, E. (2007). On the opening of an insensitive cyclosporin A non-specific pore by phenylarsine plus mersalyl. Cell Biochemistry and Biophysics, 49, 84–90.

    Article  PubMed  Google Scholar 

  23. Kowaltowski, A. J., Vercesi, A. E., & Castilho, R. F. (1997). Mitochondrial membrane protein thiol reactivity with N-ethylmaleimide or mersalyl is modified by Ca2+: Correlation with mitochondrial permeability transition. Biochimica et Biophysica Acta, 1318, 395–402.

    Article  PubMed  CAS  Google Scholar 

  24. Halestrap, A. P., McStay, G. P., & Clarke, S. J. (2002). The permeability transition pore complex: Another view. Biochimie, 84, 153–166.

    Article  PubMed  CAS  Google Scholar 

  25. Costantini, P., Colonna, R., & Bernardi, P. (1998). Induction of the mitochondrial permeability transition by N-ethylmaleimide depends on secondary oxidation of critical thiol groups. Potentiation by copper-orthophenanthroline without dimerization of the adenine nucleotide translocase. Biochimica et Biophysica Acta, 1365, 385–392.

    Article  PubMed  CAS  Google Scholar 

  26. Atlante, A., Bobba, A., de Bari, L., Fontana, F., Calissano, P., Marra, E., et al. (2006). Caspase-dependent alteration of the ADP/ATP translocator triggers the mitochondrial permeability transition which is not required for the low-potassium-dependent apoptosis of cerebellar granule cells. Journal of Neurochemistry, 97, 11661–11681.

    Article  Google Scholar 

  27. Zazueta, C., Reyes-Vivas, H., Zafra, G., Sánchez, C. A., Vera, G., & Chávez, E. (1998). Mitochondrial permeability transition as induced by cross-linking of the adenine nucleotide translocase. International Journal of Biochemistry and Cell Biology, 30, 517–527.

    Article  PubMed  CAS  Google Scholar 

  28. Kokoszka, J. E., Waymire, K. G., Levy, S. E., Sligh, J. E., Cai, J., Jones, D. P., et al. (2004). The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature, 430, 461–465.

    Article  Google Scholar 

  29. Coty, W., & Pedersen, P. L. (1975). Phosphate transport in rat liver mitochondria. Membrane components labeled by N-ethylmaleimide during inhibition transport. Journal of Biological Chemistry, 250, 3515–3521.

    PubMed  CAS  Google Scholar 

  30. Lapidus, R. G., & Sokolove, P. M. (1994). The mitochondrial permeability transition. Interactions of spermine, ADP, and inorganic phosphate. Journal of Biological Chemistry, 269, 18931–18936.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors recognize the technical assistance of Mr. Fernando Ibarra.

Author information

Authors and Affiliations

  1. Departamento de Bioquímica, Instituto Nacional de Cardiología, Ignacio Chávez, Mexico, D.F., 01480, Mexico

    Noemí García, Natalia Pavón & Edmundo Chávez

Authors
  1. Noemí García
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Natalia Pavón
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edmundo Chávez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edmundo Chávez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

García, N., Pavón, N. & Chávez, E. The Effect of N-Ethylmaleimide on Permeability Transition as Induced by Carboxyatractyloside, Agaric Acid, and Oleate. Cell Biochem Biophys 51, 81–87 (2008). https://doi.org/10.1007/s12013-008-9016-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12013-008-9016-5

Keywords

Search

Navigation