Cytosolic GAPDH as a redox-dependent regulator of energy metabolism

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Abstract

Background

Plant cytosolic NAD-dependent glyceraldehyde-3-phosphate dehydrogenase (GapC) displays redox-dependent changes in its subcellular localizations and activity. Apart from its fundamental role in glycolysis, it also exhibits moonlighting properties. Since the exceptional redox-sensitivity of GapC has been suggested to play a crucial role in its various functions, we here studied its redox-dependent subcellular localization and the influence of the redox-state on GapC protein interactions.

Results

In mesophyll protoplasts from Arabidopsis thaliana, colocalization of GapC with mitochondria was more pronounced under reducing conditions than upon oxidative stress. In accordance, reduced GapC showed an increased affinity to the mitochondrial voltage-dependent anion-selective channel (VDAC) compared to the oxidized one . On the other hand, nuclear localization of GapC was increased under oxidizing conditions. The essential role of the catalytic cysteine for nuclear translocation was shown by using the corresponding cysteine mutants. Furthermore, interaction of GapC with the thioredoxin Trx- h3 as a candidate to revert the redox-modifications, occurred in the nucleus of oxidized protoplasts. In a yeast complementation assay, we could demonstrate that the plant-specific non-phosphorylating glyceraldehyde 3-P dehydrogenase (GapN) can substitute for glucose 6-P dehydrogenase to generate NADPH for re-reduction of the Trx system and ROS defense.

Conclusions

The preferred association of reduced, glycolytically active GapC with VDAC suggests a substrate-channeling metabolon at the mitochondrial surface for efficient energy generation. Increased occurrence of oxidized GapC in the nucleus points to a function in signal transduction and gene expression. Furthermore, the interaction of GapC with Trx- h3 in the nucleus indicates reversal of the oxidative cysteine modification after re-establishment of cellular homeostasis. Both, energy metabolism and signal transfer for long-term adjustment and protection from redox-imbalances are mediated by the various functions of GapC. The molecular properties of GapC as a redox-switch are key to its multiple roles in orchestrating energy metabolism.

Electronic supplementary material

The online version of this article (10.1186/s12870-018-1390-6) contains supplementary material, which is available to authorized users.

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A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast.

U Gueldener (2002)

Heterologous markers are important tools required for the molecular dissection of gene function in many organisms, including Saccharomyces cerevisiae. Moreover, the presence of gene families and isoenzymes often makes it necessary to delete more than one gene. We recently introduced a new and efficient gene disruption cassette for repeated use in budding yeast, which combines the heterologous dominant kan(r) resistance marker with a Cre/loxP-mediated marker removal procedure. Here we describe an additional set of four completely heterologous loxP-flanked marker cassettes carrying the genes URA3 and LEU2 from Kluyveromyces lactis, his5(+) from Schizosaccharomyces pombe and the dominant resistance marker ble(r) from the bacterial transposon Tn5, which confers resistance to the antibiotic phleomycin. All five loxP--marker gene--loxP gene disruption cassettes can be generated using the same pair of oligonucleotides and all can be used for gene disruption with high efficiency. For marker rescue we have created three additional Cre expression vectors carrying HIS3, TRP1 or ble(r) as the yeast selection marker. The set of disruption cassettes and Cre expression plasmids described here represents a significant further development of the marker rescue system, which is ideally suited to functional analysis of the yeast genome.

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Protein S-glutathionylation: a regulatory device from bacteria to humans.

Isabella Dalle-Donne, Ranieri Rossi, Graziano Colombo … (2009)

S-Glutathionylation is the specific post-translational modification of protein cysteine residues by the addition of the tripeptide glutathione, the most abundant and important low-molecular-mass thiol within most cell types. Protein S-glutathionylation is promoted by oxidative or nitrosative stress but also occurs in unstressed cells. It can serve to regulate a variety of cellular processes by modulating protein function and to prevent irreversible oxidation of protein thiols. Recent findings support an essential role for S-glutathionylation in the control of cell-signalling pathways associated with viral infections and with tumour necrosis factor-(-induced apoptosis. Glyceraldehyde-3-phosphate dehydrogenase has recently been implicated in the regulation of endothelin-1 synthesis by a novel, S-glutathionylation-based mechanism involving messenger RNA stability. Moreover, recent studies have identified S-glutathionylation as a redox signalling mechanism in plants.

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Stress-triggered redox signalling: what's in pROSpect?

Christine Foyer, Graham Noctor (2016)

Reactive oxygen species (ROS) have a profound influence on almost every aspect of plant biology. Here, we emphasize the fundamental, intimate relationships between light-driven reductant formation, ROS, and oxidative stress, together with compartment-specific differences in redox buffering and the perspectives for their analysis. Calculations of approximate H2 O2 concentrations in the peroxisomes are provided, and based on the likely values in other locations such as chloroplasts, we conclude that much of the H2 O2 detected in conventional in vitro assays is likely to be extracellular. Within the context of scant information on ROS perception mechanisms, we consider current knowledge, including possible parallels with emerging information on oxygen sensing. Although ROS can sometimes be signals for cell death, we consider that an equally important role is to transmit information from metabolism to allow appropriate cellular responses to developmental and environmental changes. Our discussion speculates on novel sensing mechanisms by which this could happen and how ROS could be counted by the cell, possibly as a means of monitoring metabolic flux. Throughout, we place emphasis on the positive effects of ROS, predicting that in the coming decades they will increasingly be defined as hallmarks of viability within a changing and challenging environment.

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Author and article information

Contributors

Markus Schneider: schneider@biologie.uni-osnabrueck.de

Johannes Knuesting: knuesting@biologie.uni-osnabrueck.de

Oliver Birkholz: birkholz@biologie.uni-osnabrueck.de

Jürgen J. Heinisch: heinisch@biologie.uni-osnabrueck.de

Renate Scheibe:

ORCID: http://orcid.org/0000-0002-6140-6181

scheibe@biologie.uni-osnabrueck.de

Journal

Journal ID (nlm-ta): BMC Plant Biol

Journal ID (iso-abbrev): BMC Plant Biol

Title: BMC Plant Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2229

Publication date (Electronic): 6 September 2018

Publication date PMC-release: 6 September 2018

Publication date Collection: 2018

Volume: 18

Electronic Location Identifier: 184

Affiliations

[1 ]ISNI 0000 0001 0672 4366, GRID grid.10854.38, Division of Plant Physiology, Department of Biology and Chemistry, , Osnabrück University, ; Barbarastr. 11, 49076 Osnabrück, Germany

[2 ]ISNI 0000 0001 0672 4366, GRID grid.10854.38, Division of Biophysics, Department of Biology and Chemistry, , Osnabrück University, ; Barbarastr. 11, 49076 Osnabrück, Germany

[3 ]ISNI 0000 0001 0672 4366, GRID grid.10854.38, Division of Genetics, Department of Biology and Chemistry, , Osnabrück University, ; Barbarastr. 11, 49076 Osnabrück, Germany

Author information

Renate Scheibe http://orcid.org/0000-0002-6140-6181

Article

Publisher ID: 1390

DOI: 10.1186/s12870-018-1390-6

PMC ID: 6127989

PubMed ID: 30189844

SO-VID: 9aab15b0-e09a-4532-9120-197d2553b358

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 18 October 2017

Date accepted : 22 August 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;

Award ID: SFB 944

Award Recipient : Renate Scheibe

Custom metadata

ScienceOpen disciplines: Plant science & Botany

Keywords: redox,metabolism,gapdh,vdac,thioredoxin,mitochondria,nucleus,glycolysis,metabolon,gapn

Data availability:

ScienceOpen disciplines: Plant science & Botany

Keywords: redox, metabolism, gapdh, vdac, thioredoxin, mitochondria, nucleus, glycolysis, metabolon, gapn

Cytosolic GAPDH as a redox-dependent regulator of energy metabolism

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Cancer Metabolism

Most cited references 50

A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast.

Protein S-glutathionylation: a regulatory device from bacteria to humans.

Stress-triggered redox signalling: what's in pROSpect?

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