Identification of a Novel Transporter for Dicarboxylates and Tricarboxylates in Plant Mitochondria

Picault, Nathalie; Palmieri, Luigi; Pisano, Isabella; Hodges, Michael; Palmieri, Ferdinando

doi:10.1074/jbc.m202702200

Cited by 146 publications

(51 citation statements)

References 43 publications

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“…In Arabidopsis thaliana these proteins include three dicarboxylate carriers (DIC1–3) [13], a dicarboxylate/tricarboxylate carrier (DTC1) [14] and a specific succinate/fumarate carrier (SFC1) [15,16]. …”

Section: Introductionmentioning

confidence: 99%

Transport Pathways—Proton Motive Force Interrelationship in Durum Wheat Mitochondria

Trono¹,

Laus

Soccio

et al. 2014

IJMS

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In durum wheat mitochondria (DWM) the ATP-inhibited plant mitochondrial potassium channel (PmitoKATP) and the plant uncoupling protein (PUCP) are able to strongly reduce the proton motive force (pmf) to control mitochondrial production of reactive oxygen species; under these conditions, mitochondrial carriers lack the driving force for transport and should be inactive. However, unexpectedly, DWM uncoupling by PmitoKATP neither impairs the exchange of ADP for ATP nor blocks the inward transport of Pi and succinate. This uptake may occur via the plant inner membrane anion channel (PIMAC), which is physiologically inhibited by membrane potential, but unlocks its activity in de-energized mitochondria. Probably, cooperation between PIMAC and carriers may accomplish metabolite movement across the inner membrane under both energized and de-energized conditions. PIMAC may also cooperate with PmitoKATP to transport ammonium salts in DWM. Interestingly, this finding may trouble classical interpretation of in vitro mitochondrial swelling; instead of free passage of ammonia through the inner membrane and proton symport with Pi, that trigger metabolite movements via carriers, transport of ammonium via PmitoKATP and that of the counteranion via PIMAC may occur. Here, we review properties, modulation and function of the above reported DWM channels and carriers to shed new light on the control that they exert on pmf and vice-versa.

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Section: Introductionmentioning

confidence: 99%

Transport Pathways—Proton Motive Force Interrelationship in Durum Wheat Mitochondria

Trono¹,

Laus

Soccio

et al. 2014

IJMS

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“…Control cultures with the empty vector were processed in parallel. Inclusion bodies were isolated, and Ggc1p was purified by centrifugation and washing steps as described previously (13,15). The proteins were separated by SDS-PAGE in 17.5% gels and either stained with Coomassie Blue dye or transferred to nitrocellulose membranes for immunodetection with a rabbit antiserum raised against bacterially expressed Ggc1p.…”

Section: Methodsmentioning

confidence: 99%

Identification of the Mitochondrial GTP/GDP Transporter in Saccharomyces cerevisiae

Vozza

Blanco

Palmieri

et al. 2004

Journal of Biological Chemistry

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110

128

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The genome of Saccharomyces cerevisiae contains 35 members of a family of transport proteins that, with a single exception, are found in the inner membranes of mitochondria. The transport functions of the 16 biochemically identified mitochondrial carriers are concerned with shuttling substrates, biosynthetic intermediates, and cofactors across the inner membrane. Here the identification and functional characterization of the mitochondrial GTP/GDP carrier (Ggc1p) is described. The ggc1 gene was overexpressed in bacteria. The purified protein was reconstituted into liposomes, and its transport properties and kinetic parameters were characterized. It transported GTP and GDP and, to a lesser extent, the corresponding deoxynucleotides and the structurally related ITP and IDP by a counter-exchange mechanism. Transport was saturable with an apparent K m of 1 M for GTP and 5 M for GDP. It was strongly inhibited by pyridoxal 5-phosphate, bathophenanthroline, tannic acid, and bromcresol purple but little affected by the inhibitors of the ADP/ATP carrier carboxyatractyloside and bongkrekate. Furthermore, in contrast to the ADP/ATP carrier, the Ggc1p-mediated GTP/GDP heteroexchange is H ؉ -compensated and thus electroneutral. Cells lacking the ggc1 gene had reduced levels of GTP and increased levels of GDP in their mitochondria. Furthermore, the knock-out of ggc1 results in lack of growth on nonfermentable carbon sources and complete loss of mitochondrial DNA. The physiological role of Ggc1p in S. cerevisiae is probably to transport GTP into mitochondria, where it is required for important processes such as nucleic acid and protein synthesis, in exchange for intramitochondrially generated GDP.In the mitochondrial matrix, GTP is required as an energy source for protein synthesis; as a substrate for the synthesis of tRNA, mRNA, rRNA, and RNA primers; and as a phosphate group donor for the activity of GTP-AMP phosphotransferase (1) and G proteins (2, 3). In several organisms, GTP is synthesized in the mitochondria by succinyl-CoA ligase, which catalyzes the conversion of succinyl-CoA to succinate with the generation of GTP, and by nucleoside diphosphate kinase, which catalyzes the transfer of the ␥ phosphate from ATP to a nucleoside diphosphate to yield nucleotide triphosphates. In Saccharomyces cerevisiae, however, succinyl-CoA ligase produces ATP instead of GTP (4), and the mitochondrial nucleoside diphosphate kinase is localized in the intermembrane space and absent in the matrix (5). These observations imply that in S. cerevisiae GTP has to be imported into the mitochondria probably via a carrier system embedded in the inner mitochondrial membrane.Despite the importance of GTP in mitochondrial metabolism, the transport of guanine nucleotides has not been characterized in yeast mitochondria, nor has any mitochondrial protein responsible for this transport been identified. There are only two indirect observations that suggest that GTP is transported across the inner mitochondrial membrane of S. cerevisiae. First, mitochondri...

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“…It is important to identify for each putative homolog the substrates transported as well as their kinetic properties. The overexpression of plant carrier proteins in E. coli and the subsequent reconstitution of the purified proteins into liposomes offer a possibility for successful analysis (55,56), but the low expression levels obtained for many heterologously synthesized carrier proteins can be a major drawback to this approach. However, we showed previously that heterologous synthesis of plastidic ATP/ADP transporters in E. coli leads to their functional integration into the bacterial cytoplasmic membrane with transport properties similar to carriers in their authentic membranes (20,57).…”

Section: And E)mentioning

confidence: 99%

Identification and Characterization of a Novel Plastidic Adenine Nucleotide Uniporter from Solanum tuberosum

Leroch

Kirchberger

Haferkamp

et al. 2005

Journal of Biological Chemistry

121

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Homologs of BT1 (the Brittle1 protein) are found to be phylogenetically related to the mitochondrial carrier family and appear to occur in both mono-and dicotyledonous plants. Whereas BT1 from cereals is probably involved in the transport of ADP-glucose, which is essential for starch metabolism in endosperm plastids, BT1 from a noncereal plant, Solanum tuberosum (StBT1), catalyzes an adenine nucleotide uniport when functionally integrated into the bacterial cytoplasmic membrane. Import studies into intact Escherichia coli cells harboring StBT1 revealed a narrow substrate spectrum with similar affinities for AMP, ADP, and ATP of about 300 -400 M. Transiently expressed StBT1-green fluorescent protein fusion protein in tobacco leaf protoplasts showed a plastidic localization of the StBT1. In vitro synthesized radioactively labeled StBT1 was targeted to the envelope membranes of isolated spinach chloroplasts. Furthermore, we showed by real time reverse transcription-PCR a ubiquitous expression pattern of the StBT1 in autotrophic and heterotrophic potato tissues. We therefore propose that StBT1 is a plastidic adenine nucleotide uniporter used to provide the cytosol and other compartments with adenine nucleotides exclusively synthesized inside plastids.

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Identification of a Novel Transporter for Dicarboxylates and Tricarboxylates in Plant Mitochondria

Cited by 146 publications

References 43 publications

Transport Pathways—Proton Motive Force Interrelationship in Durum Wheat Mitochondria

Transport Pathways—Proton Motive Force Interrelationship in Durum Wheat Mitochondria

Identification of the Mitochondrial GTP/GDP Transporter in Saccharomyces cerevisiae

Identification and Characterization of a Novel Plastidic Adenine Nucleotide Uniporter from Solanum tuberosum

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