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The Saccharomyces cerevisiae mitochondrial unselective channel behaves as a physiological uncoupling system regulated by Ca2+, Mg2+, phosphate and ATP

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Abstract

It is proposed that the Saccharomyces cerevisiae the Mitochondrial Unselective Channel ( Sc MUC) is tightly regulated constituting a physiological uncoupling system that prevents overproduction of reactive oxygen species (ROS). Mg2+, Ca2+ or phosphate (Pi) close Sc MUC, while ATP or a high rate of oxygen consumption open it. We assessed Sc MUC activity by measuring in isolated mitochondria the respiratory control, transmembrane potential (ΔΨ), swelling and production of ROS. At increasing [Pi], less [Ca2+] and/or [Mg2+] were needed to close Sc MUC or increase ATP synthesis. The Ca2+-mediated closure of Sc MUC was prevented by high [ATP] while the Mg2+ or Pi effect was not. When Ca2+ and Mg2+ were alternatively added or chelated, Sc MUC opened and closed reversibly. Different effects of Ca2+ vs Mg2+ effects were probably due to mitochondrial Mg2+ uptake. Our results suggest that Sc MUC activity is dynamically controlled by both the ATP/Pi ratio and divalent cation fluctuations. It is proposed that the reversible opening/closing of Sc MUC leads to physiological uncoupling and a consequent decrease in ROS production.

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Abbreviations

PT:

permeability transition

Sc MUC:

Saccharomyces cerevisiae Mitochondrial Unselective Channel

PTP:

Permeability Transition Pore

ANC:

Adenine Nucleotide Carrier

VDAC:

Voltage Dependent Anion Channel

PiC:

Phosphate Carrier

CCCP:

carbonyl cyanide 3-chlorophenylhydrazone

ΔΨ:

Transmembrane Potential

ROS:

Reactive Oxygen Species

EDTA:

Ethylene-diamine-tetra-acetic acid

EGTA:

ethylene-glycol-tetra-acetic acid

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Acknowledgments

The authors thank Natalia Chiquete-Félix and Ramón Méndez for technical assistance. Partially funded by CONACYT grant 239487 and PAPIIT-UNAM IN204015. ACO is a CONACYT fellow enrolled in the Biochemistry PhD program at UNAM. LALM is supported by a postdoctoral fellowship from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), process number 2013/04919-9.

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Authors and Affiliations

  1. Departamento de Genética Molecular, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Mexico City, Mexico

    Alfredo Cabrera-Orefice, Rodrigo Ibarra-García-Padilla, Rocío Maldonado-Guzmán & Salvador Uribe-Carvajal

  2. Nijmegen Center for Mitochondrial Disorders, 6500, HB, Nijmegen, The Netherlands

    Sergio Guerrero-Castillo

  3. Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, São Paulo, SP, Brazil

    Luis A. Luévano-Martínez

  4. Departamento de Ciencias Médicas, Universidad de Guanajuato, 37320, Guanajuato, León, Mexico

    Victoriano Pérez-Vázquez

  5. Center for Human Nutrition, Washington University School of Medicine, St. Louis, MO, 63110, USA

    Manuel Gutiérrez-Aguilar

  6. Salvador Uribe-Carvajal, Department of Molecular Genetics, Instituto de Fisiología Celular, UNAM, Apdo. postal 70-242, 04510, Mexico City, Mexico

    Salvador Uribe-Carvajal

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  1. Alfredo Cabrera-Orefice
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  2. Rodrigo Ibarra-García-Padilla
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  4. Sergio Guerrero-Castillo
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  8. Salvador Uribe-Carvajal
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Correspondence to Salvador Uribe-Carvajal.

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Cabrera-Orefice, A., Ibarra-García-Padilla, R., Maldonado-Guzmán, R. et al. The Saccharomyces cerevisiae mitochondrial unselective channel behaves as a physiological uncoupling system regulated by Ca2+, Mg2+, phosphate and ATP. J Bioenerg Biomembr 47, 477–491 (2015). https://doi.org/10.1007/s10863-015-9632-x

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