Copper transport and regulation in <i>Schizosaccharomyces pombe</i>

Beaudoin, Jude; Ekici, Seda; Daldal, Fevzi; Aı̈t-Mohand, Samia; Guérin, Brigitte; Labbé, Simon

doi:10.1042/bst2013089

Cited by 26 publications

(23 citation statements)

References 39 publications

(68 reference statements)

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“…Exogenous copper is transported across the plasma membrane by the Ctr4-Ctr5 heteromeric complex in dividing cells that grow mitotically (12,16,21,28). We next sought to determine the location of Ctr4 and Ctr5 during spore germination because steady-state levels of ctr4 ϩ and ctr5 ϩ transcripts were poorly expressed in early stages of spore germination.…”

Section: Ctr4-gfp and Ctr5-cherry First Co-localize At The Spore Contmentioning

confidence: 99%

Cell-surface copper transporters and superoxide dismutase 1 are essential for outgrowth during fungal spore germination

Plante

Normant

Ramos-Torres

et al. 2017

Journal of Biological Chemistry

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During fungal spore germination, a resting spore returns to a conventional mode of cell division and resumes vegetative growth, but the requirements for spore germination are incompletely understood. Here, we show that copper is essential for spore germination in Germinating spores develop a single germ tube that emerges from the outer spore wall in a process called outgrowth. Under low-copper conditions, the copper transporters Ctr4 and Ctr5 are maximally expressed at the onset of outgrowth. In the case of Ctr6, its expression is broader, taking place before and during outgrowth. Spores lacking Ctr4, Ctr5, and the copper sensor Cuf1 exhibit complete germination arrest at outgrowth. In contrast, deletion only partially interferes with formation of outgrowing spores. At outgrowth, Ctr4-GFP and Ctr5-Cherry first co-localize at the spore contour, followed by re-location to a middle peripheral spore region. Subsequently, they move away from the spore body to occupy the periphery of the nascent cell. After breaking of spore dormancy, Ctr6 localizes to the vacuole membranes that are enriched in the spore body relative to the germ tube. Using a copper-binding tracker, results showed that labile copper is preferentially localized to the spore body. Further analysis showed that Ctr4 and Ctr6 are required for copper-dependent activation of the superoxide dismutase 1 (SOD1) during spore germination. This activation is critical because the loss of SOD1 activity blocked spore germination at outgrowth. Taken together, these results indicate that cell-surface copper transporters and SOD1 are required for completion of the spore germination program.

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Section: Ctr4-gfp and Ctr5-cherry First Co-localize At The Spore Contmentioning

confidence: 99%

Cell-surface copper transporters and superoxide dismutase 1 are essential for outgrowth during fungal spore germination

Plante

Normant

Ramos-Torres

et al. 2017

Journal of Biological Chemistry

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“…In this species, a CcoA-deficient strain is defective in cbb 3 -Cox biogenesis, and compared with a wild-type strain, contains smaller amounts of cellular Cu (like a mutant lacking cbb 3 -Cox) ( 41 ). The inability of a mutant lacking CcoA to take up radioactive 64 Cu ( 14 ) and the heterologous complementation of a Ctr-less S. pompe mutant with R. capsulatus CcoA ( 43 ) showed unequivocally that CcoA is a cytoplasmic Cu importer required for cbb 3 -Cox production in R. capsulatus ( 41 ).…”

Section: Introductionmentioning

confidence: 99%

Uncovering the Transmembrane Metal Binding Site of the Novel Bacterial Major Facilitator Superfamily-Type Copper Importer CcoA

Khalfaoui-Hassani

Verissimo

Koch

et al. 2016

mBio

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Uptake and trafficking of metals and their delivery to their respective metalloproteins are important processes. Cells need precise control of each step to avoid exposure to excessive metal concentrations and their harmful consequences. Copper (Cu) is a required micronutrient used as a cofactor in proteins. However, in large amounts, it can induce oxidative damage; hence, Cu homeostasis is indispensable for cell survival. Biogenesis of respiratory heme-Cu oxygen (HCO) reductases includes insertion of Cu into their catalytic subunits to form heme-Cu binuclear centers. Previously, we had shown that CcoA is a major facilitator superfamily (MFS)-type bacterial Cu importer required for biogenesis of cbb3-type cytochrome c oxidase (cbb3-Cox). Here, using Rhodobacter capsulatus, we focused on the import and delivery of Cu to cbb3-Cox. By comparing the CcoA amino acid sequence with its homologues from other bacterial species, we located several well-conserved Met, His, and Tyr residues that might be important for Cu transport. We determined the topology of the transmembrane helices that carry these residues to establish that they are membrane embedded, and substituted for them amino acids that do not ligand metal atoms. Characterization of these mutants for their uptake of radioactive 64Cu and cbb3-Cox activities demonstrated that Met233 and His261 of CcoA are essential and Met237 and Met265 are important, whereas Tyr230 has no role for Cu uptake or cbb3-Cox biogenesis. These findings show for the first time that CcoA-mediated Cu import relies on conserved Met and His residues that could act as metal ligands at the membrane-embedded Cu binding domain of this transporter.

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“…At low Cu availability, the Cu chaperones SenC (in R. capsulatus [ 23 ]) and PrrC (in R. sphaeroides [ 24 ]), which are homologues of mitochondrial Sco1/Sco2, and their interacting partners PccA (of R. capsulatus [ 33 ]) and PCu A C (of R. sphaeroides [ 24 ]) are needed for cbb 3 -Cox biogenesis. Finally, a member of the major facilitator superfamily (MFS) of transporters, CcoA, is a Cu importer that is required for assembly of the Cu B center of cbb 3 -Cox ( 32 , 34 , 35 ). R. capsulatus mutants lacking CcoA are impaired for Cu uptake and contain a very small amount of cbb 3 -Cox ( 34 ).…”

Section: Introductionmentioning

confidence: 99%

Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome c Oxidases

Khalfaoui-Hassani

Blaby‐Haas

et al. 2018

mBio

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Cytochrome c oxidases are members of the heme-copper oxidase superfamily. These enzymes have different subunits, cofactors, and primary electron acceptors, yet they all contain identical heme-copper (CuB) binuclear centers within their catalytic subunits. The uptake and delivery pathways of the CuB atom incorporated into this active site, where oxygen is reduced to water, are not well understood. Our previous work with the facultative phototrophic bacterium Rhodobacter capsulatus indicated that the copper atom needed for the CuB site of cbb3-type cytochrome c oxidase (cbb3-Cox) is imported to the cytoplasm by a major facilitator superfamily-type transporter, CcoA. In this study, a comparative genomic analysis of CcoA orthologs in alphaproteobacterial genomes showed that CcoA is widespread among organisms and frequently co-occurs with cytochrome c oxidases. To define the specificity of CcoA activity, we investigated its function in Rhodobacter sphaeroides, a close relative of R. capsulatus that contains both cbb3- and aa3-Cox. Phenotypic, genetic, and biochemical characterization of mutants lacking CcoA showed that in its absence, or even in the presence of its bypass suppressors, only the production of cbb3-Cox and not that of aa3-Cox was affected. We therefore concluded that CcoA is dedicated solely to cbb3-Cox biogenesis, establishing that distinct copper uptake systems provide the CuB atoms to the catalytic sites of these two similar cytochrome c oxidases. These findings illustrate the large variety of strategies that organisms employ to ensure homeostasis and fine control of copper trafficking and delivery to the target cuproproteins under different physiological conditions.

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Copper transport and regulation in Schizosaccharomyces pombe

Cited by 26 publications

References 39 publications

Cell-surface copper transporters and superoxide dismutase 1 are essential for outgrowth during fungal spore germination

Cell-surface copper transporters and superoxide dismutase 1 are essential for outgrowth during fungal spore germination

Uncovering the Transmembrane Metal Binding Site of the Novel Bacterial Major Facilitator Superfamily-Type Copper Importer CcoA

Widespread Distribution and Functional Specificity of the Copper Importer CcoA: Distinct Cu Uptake Routes for Bacterial Cytochrome c Oxidases

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