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Plant VDAC Permeability: Molecular Basis and Role in Oxidative Stress

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Molecular Basis for Mitochondrial Signaling

Part of the book series: Biological and Medical Physics, Biomedical Engineering ((BIOMEDICAL))

Abstract

The mitochondrial voltage-dependent anion-selective channel (VDAC) is highly abundant in the mitochondrial outer membrane. It is permeable to molecules with a size up to about 5 kDa and is the main pathway for the exchange of metabolites and ions between the mitochondrial intermembrane space and the cytosol. Experimental studies performed for plant VDAC have shown that the channel displays properties reported for VDACs of other eukaryotic organisms. Firstly, it transports compounds as diverse as inorganic ions (e.g., K+ and Cl−), adenylates (e.g., ATP and AMP), and large macromolecules (tRNA and DNA). Secondly, despite its wide pore, the channel displays selectivity toward these compounds, i.e., it distinguishes between K+ and Cl− but also between ATP and AMP. The question of how VDAC can selectively transport these different compounds is addressed in this chapter based on data obtained for plant VDAC. It is well known that all organisms have at least one canonical VDAC isoform that shares similar electrophysiological properties and secondary structure with cognate VDAC of other organisms. For instance, this is the case of the mammalian VDAC1, the yeast Saccharomyces cerevisiae VDAC1 and the PcVDAC purified from the bean Phaseolus coccineus seeds. Consequently, Brownian dynamic simulations of monatomic ion permeation through the experimental three-dimensional structure of the mammalian VDAC1 and the PcVDAC modeled structure predict fairly well conductance and selectivity of both proteins. In addition, the data of molecular simulation studies performed on the mammalian VDAC1 agree with the experimental data obtained for PcVDAC, which suggests a similar permeation process for these VDAC proteins. Accordingly, both the experimental and theoretical studies indicate that the selectivity for inorganic ions is a consequence of the excess of positive charges and their distribution inside the pore and the absence of defined pathways for the permeation. In contrast, the permeation of metabolites involves a major binding site located at the N-terminal helix which folded into the pore lumen and occurs through a preferential pathway. The key residues forming the binding site are conserved in the PcVDAC pointing to the conserved permeation process. The process might be affected by VDAC interaction with other proteins. For example, it is suggested that plant VDAC is involved in the oxidative stress response which includes cytosolic hexokinase and thioredoxin binding to VDAC. This in turn may influence the exchange of molecules between the mitochondria and the cytosol.

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Notes

  1. 1.

    Within the chapter, we will follow the proposition of the Nomenclature Committee on Cell Death (Galluzzi et al. 2015).

  2. 2.

    The affinity for glucose is one to three orders of magnitude higher than that of other sugars.

Abbreviations

BiFC:

Bimolecular fluorescence complementation

HK and HXK:

Hexokinase

Trx:

Thioredoxin

VDAC:

Voltage-dependent anion channel

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Acknowledgments

FH is a research director at the F.R.S.-FNRS (Belgium).

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Authors and Affiliations

  1. Structure et Fonction des Membranes Biologiques, Université Libre de Bruxelles (ULB), Boulevard du Triomphe CP 206/2, 1050, Brussels, Belgium

    Fabrice Homblé & Hayet Saidani

  2. Laboratory of Bioenergetics, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614, Poznan, Poland

    Hana Kmita

  3. I.R.P.H.E, Aix-Marseille Université, CNRS, Technopôle de Château-Gombert, 13384, Marseille Cedex 13, France

    Marc Léonetti

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  1. Fabrice Homblé
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Correspondence to Fabrice Homblé .

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  1. Section on Molecular Transport, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, USA

    Tatiana K. Rostovtseva

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Homblé, F., Kmita, H., Saidani, H., Léonetti, M. (2017). Plant VDAC Permeability: Molecular Basis and Role in Oxidative Stress. In: Rostovtseva, T. (eds) Molecular Basis for Mitochondrial Signaling. Biological and Medical Physics, Biomedical Engineering. Springer, Cham. https://doi.org/10.1007/978-3-319-55539-3_7

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