SLC25A39 is necessary for mitochondrial glutathione import in mammalian cells.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
received:
26
03
2021
accepted:
09
09
2021
pubmed:
29
10
2021
medline:
8
1
2022
entrez:
28
10
2021
Statut:
ppublish
Résumé
Glutathione (GSH) is a small-molecule thiol that is abundant in all eukaryotes and has key roles in oxidative metabolism
Identifiants
pubmed: 34707288
doi: 10.1038/s41586-021-04025-w
pii: 10.1038/s41586-021-04025-w
doi:
Substances chimiques
Iron-Sulfur Proteins
0
Mitochondrial Membrane Transport Proteins
0
Proteome
0
SLC25A39 protein, human
0
SLC25A40 protein, human
0
Slc25a39 protein, mouse
0
Glutathione
GAN16C9B8O
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
136-140Subventions
Organisme : NIH HHS
ID : 1R01 CA193842-06A1
Pays : United States
Organisme : NIH HHS
ID : R01-DK101989-06A1
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK101989
Pays : United States
Organisme : NIH HHS
ID : R01 DK101989-01A1
Pays : United States
Organisme : NIH HHS
ID : DP2 OD024174-01
Pays : United States
Organisme : NIH HHS
ID : 1R01 CA193842-01
Pays : United States
Organisme : NIH HHS
ID : 5R01 CA186702-07
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001866
Pays : United States
Organisme : NIH HHS
ID : R01 CA225231-01
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007739
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL135564
Pays : United States
Organisme : NIH HHS
ID : K99 DK128602-01
Pays : United States
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Meister, A. & Anderson, M. E. Glutathione. Annu. Rev. Biochem. 52, 711–760 (1983).
pubmed: 6137189
doi: 10.1146/annurev.bi.52.070183.003431
Mårtensson, J., Lai, J. C. & Meister, A. High-affinity transport of glutathione is part of a multicomponent system essential for mitochondrial function. Proc. Natl Acad. Sci. USA 87, 7185–7189 (1990).
pubmed: 2402500
pmcid: 54708
doi: 10.1073/pnas.87.18.7185
Deponte, M. The incomplete glutathione puzzle: just guessing at numbers and figures? Antioxid. Redox Signal. 27, 1130–1161 (2017).
pubmed: 28540740
pmcid: 5661824
doi: 10.1089/ars.2017.7123
Griffith, O. W. & Meister, A. Origin and turnover of mitochondrial glutathione. Proc. Natl Acad. Sci. USA 82, 4668–4672 (1985).
pubmed: 3860816
pmcid: 390447
doi: 10.1073/pnas.82.14.4668
Hwang, C., Sinskey, A. J. & Lodish, H. F. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257, 1496–1502 (1992).
pubmed: 1523409
doi: 10.1126/science.1523409
Meredith, M. J. & Reed, D. J. Status of the mitochondrial pool of glutathione in the isolated hepatocyte. J. Biol. Chem. 257, 3747–3753 (1982).
pubmed: 7061508
doi: 10.1016/S0021-9258(18)34844-0
Deneke, S. M. & Fanburg, B. L. Regulation of cellular glutathione. Am. J. Physiol. Lung Cell. Mol. Physiol. 257, L163–L173 (1989).
doi: 10.1152/ajplung.1989.257.4.L163
Jones, D. P. Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol. 348, 93–112 (2002).
pubmed: 11885298
doi: 10.1016/S0076-6879(02)48630-2
Kurosawa, K., Hayashi, N., Sato, N., Kamada, T. & Tagawa, K. Transport of glutathione across the mitochondrial membranes. Biochem. Biophys. Res. Commun. 167, 367–372 (1990).
pubmed: 2310399
doi: 10.1016/0006-291X(90)91774-M
Griffith, O. W. & Meister, A. Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J. Biol. Chem. 254, 7558–7560 (1979).
pubmed: 38242
doi: 10.1016/S0021-9258(18)35980-5
Münch, C. & Harper, J. W. Mitochondrial unfolded protein response controls matrix pre-RNA processing and translation. Nature 534, 710–713 (2016).
pubmed: 27350246
pmcid: 4939261
doi: 10.1038/nature18302
Lee, H.-R. et al. Adaptive response to GSH depletion and resistance to l-buthionine-(S,R)-sulfoximine: involvement of Nrf2 activation. Mol. Cell. Biochem. 318, 23–31 (2008).
pubmed: 18587629
doi: 10.1007/s11010-008-9853-y
Sun, X. et al. Activation of the p62–Keap1–NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology 63, 173–184 (2016).
pubmed: 26403645
doi: 10.1002/hep.28251
Booty, L. M. et al. Selective disruption of mitochondrial thiol redox state in cells and in vivo. Cell Chem. Biol. 26, 449-461.e8 (2019).
pubmed: 30713096
pmcid: 6436940
doi: 10.1016/j.chembiol.2018.12.002
Ruprecht, J. J. & Kunji, E. R. S. The SLC25 mitochondrial carrier family: structure and mechanism. Trends Biochem. Sci. 45, 244–258 (2020).
pubmed: 31787485
doi: 10.1016/j.tibs.2019.11.001
Pebay-Peyroula, E. et al. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39–44 (2003).
pubmed: 14603310
doi: 10.1038/nature02056
Zhu, X. G. et al. CHP1 regulates compartmentalized glycerolipid synthesis by activating GPAT4. Mol. Cell 74, 45–58.e7 (2019).
pubmed: 30846317
pmcid: 6450717
doi: 10.1016/j.molcel.2019.01.037
Zhang, H., Go, Y.-M. & Jones, D. P. Mitochondrial thioredoxin-2/peroxiredoxin-3 system functions in parallel with mitochondrial GSH system in protection against oxidative stress. Arch. Biochem. Biophys. 465, 119–126 (2007).
pubmed: 17548047
doi: 10.1016/j.abb.2007.05.001
Seelig, G. F., Simondsen, R. P. & Meister, A. Reversible dissociation of gamma-glutamylcysteine synthetase into two subunits. J. Biol. Chem. 259, 9345–9347 (1984).
pubmed: 6146611
doi: 10.1016/S0021-9258(17)42703-7
Li, W., Li, Z., Yang, J. & Ye, Q. Production of glutathione using a bifunctional enzyme encoded by gshF from Streptococcus thermophilus expressed in Escherichia coli. J. Biotechnol. 154, 261–268 (2011).
pubmed: 21683099
doi: 10.1016/j.jbiotec.2011.06.001
Chen, W. W., Freinkman, E., Wang, T., Birsoy, K. & Sabatini, D. M. Absolute quantification of matrix metabolites reveals the dynamics of mitochondrial metabolism. Cell 166, 1324–1337.e11 (2016).
pubmed: 27565352
pmcid: 5030821
doi: 10.1016/j.cell.2016.07.040
Slabbaert, J. R. et al. Shawn, the Drosophila homolog of SLC25A39/40, is a mitochondrial carrier that promotes neuronal survival. J. Neurosci. 36, 1914–1929 (2016).
pubmed: 26865615
pmcid: 6602013
doi: 10.1523/JNEUROSCI.3432-15.2016
Usaj, M. et al. TheCellMap.org: a web-accessible database for visualizing and mining the global yeast genetic interaction network. Genes Genomes Genet. 7, 1539–1549 (2017).
Luk, E., Carroll, M., Baker, M. & Culotta, V. C. Manganese activation of superoxide dismutase 2 in Saccharomyces cerevisiae requires MTM1, a member of the mitochondrial carrier family. Proc. Natl Acad. Sci. USA 100, 10353–10357 (2003).
pubmed: 12890866
pmcid: 193565
doi: 10.1073/pnas.1632471100
Nilsson, R. et al. Discovery of genes essential for heme biosynthesis through large-scale gene expression analysis. Cell Metab. 10, 119–130 (2009).
pubmed: 19656490
pmcid: 2745341
doi: 10.1016/j.cmet.2009.06.012
Biederbick, A. et al. Role of human mitochondrial Nfs1 in cytosolic iron–sulfur protein biogenesis and iron regulation. Mol. Cell. Biol. 26, 5675–5687 (2006).
pubmed: 16847322
pmcid: 1592756
doi: 10.1128/MCB.00112-06
Mayr, J. A., Feichtinger, R. G., Tort, F., Ribes, A. & Sperl, W. Lipoic acid biosynthesis defects. J. Inherit. Metab. Dis. 37, 553–563 (2014).
pubmed: 24777537
doi: 10.1007/s10545-014-9705-8
Chen, Z. & Lash, L. H. Evidence for mitochondrial uptake of glutathione by dicarboxylate and 2-oxoglutarate carriers. J. Pharmacol. Exp. Ther. 285, 608–618 (1998).
pubmed: 9580605
Booty, L. M. et al. The mitochondrial dicarboxylate and 2-oxoglutarate carriers do not transport glutathione. FEBS Lett. 589, 621–628 (2015).
pubmed: 25637873
pmcid: 4332691
doi: 10.1016/j.febslet.2015.01.027
Kumar, C. et al. Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control. EMBO J. 30, 2044–2056 (2011).
pubmed: 21478822
pmcid: 3098478
doi: 10.1038/emboj.2011.105
Rodríguez-Manzaneque, M. T., Tamarit, J., Bellí, G., Ros, J. & Herrero, E. Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol. Biol. Cell 13, 1109–1121 (2002).
pubmed: 11950925
pmcid: 102255
doi: 10.1091/mbc.01-10-0517
Almusafri, F. et al. Clinical and molecular characterization of 6 children with glutamate–cysteine ligase deficiency causing hemolytic anemia. Blood Cells. Mol. Dis. 65, 73–77 (2017).
pubmed: 28571779
doi: 10.1016/j.bcmd.2017.05.011
Wessel, D. & Flügge, U. I. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141–143 (1984).
pubmed: 6731838
doi: 10.1016/0003-2697(84)90782-6
McAlister, G. C. et al. MultiNotch MS3 enables accurate, sensitive, and multiplexed detection of differential expression across cancer cell line proteomes. Anal. Chem. 86, 7150–7158 (2014).
pubmed: 24927332
pmcid: 4215866
doi: 10.1021/ac502040v
Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).
doi: 10.1038/nmeth.3901
pubmed: 27348712
Birsoy, K. et al. An essential role of the mitochondrial electron transport chain in cell proliferation is to enable aspartate synthesis. Cell 162, 540–551 (2015).
pubmed: 26232224
pmcid: 4522279
doi: 10.1016/j.cell.2015.07.016
Concordet, J.-P. & Haeussler, M. CRISPOR: intuitive guide selection for CRISPR/Cas9 genome editing experiments and screens. Nucleic Acids Res. 46, W242–W245 (2018).
pubmed: 29762716
pmcid: 6030908
doi: 10.1093/nar/gky354
Shola, D. T. N., Yang, C., Han, C., Norinsky, R. & Peraza, R. D. in Mouse Genetics: Methods and Protocols (eds. Singh, S. R., Hoffman, R. M. & Singh, A.) 1–27 (Springer US, 2021).
Murgha, Y. E., Rouillard, J.-M. & Gulari, E. Methods for the preparation of large quantities of complex single-stranded oligonucleotide libraries. PLoS ONE 9, e94752 (2014).
pubmed: 24733454
pmcid: 3986247
doi: 10.1371/journal.pone.0094752
Sadreyev, I. R., Ji, F., Cohen, E., Ruvkun, G. & Tabach, Y. PhyloGene server for identification and visualization of co-evolving proteins using normalized phylogenetic profiles. Nucleic Acids Res. 43, W154–W159 (2015).
pubmed: 25958392
pmcid: 4489270
doi: 10.1093/nar/gkv452
Ruan, J. et al. TreeFam: 2008 update. Nucleic Acids Res. 36, D735–D740 (2008).
pubmed: 18056084
doi: 10.1093/nar/gkm1005
Thomas, P. D. et al. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res. 13, 2129–2141 (2003).
pubmed: 12952881
pmcid: 403709
doi: 10.1101/gr.772403
Studer, G. et al. ProMod3—a versatile homology modelling toolbox. PLOS Comput. Biol. 17, e1008667 (2021).
pubmed: 33507980
pmcid: 7872268
doi: 10.1371/journal.pcbi.1008667
Pebay-Peyroula, E. et al. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39–44 (2003).
pubmed: 14603310
doi: 10.1038/nature02056
Robinson, A. J. & Kunji, E. R. S. Mitochondrial carriers in the cytoplasmic state have a common substrate binding site. Proc. Natl. Acad. Sci. 103, 2617–2622 (2006).
pubmed: 16469842
pmcid: 1413793
doi: 10.1073/pnas.0509994103
Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
doi: 10.1002/jcc.20084
pubmed: 15264254
Bycroft, C. et al. The UK Biobank resource with deep phenotyping and genomic data. Nature 562, 203–209 (2018).
pubmed: 30305743
pmcid: 6786975
doi: 10.1038/s41586-018-0579-z
Barbeira, A. N. et al. Integrating predicted transcriptome from multiple tissues improves association detection. PLoS Genet. 15, e1007889 (2019).
pubmed: 30668570
pmcid: 6358100
doi: 10.1371/journal.pgen.1007889
Zhou, D. et al. A unified framework for joint-tissue transcriptome-wide association and Mendelian randomization analysis. Nat. Genet. 52, 1239–1246 (2020).
pubmed: 33020666
pmcid: 7606598
doi: 10.1038/s41588-020-0706-2
Unlu, G. et al. Phenome-based approach identifies RIC1-linked Mendelian syndrome through zebrafish models, biobank associations and clinical studies. Nat. Med. 26, 98–109 (2020).
pubmed: 31932796
pmcid: 7147997
doi: 10.1038/s41591-019-0705-y
Aguet, F. et al. Genetic effects on gene expression across human tissues. Nature 550, 204–213 (2017).
doi: 10.1038/nature24277