H
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
07 2019
07 2019
Historique:
received:
07
02
2018
accepted:
23
05
2019
entrez:
26
7
2019
pubmed:
26
7
2019
medline:
13
9
2019
Statut:
ppublish
Résumé
The mitochondrial ADP/ATP carrier (AAC) is a major transport protein of the inner mitochondrial membrane. It exchanges mitochondrial ATP for cytosolic ADP and controls cellular production of ATP. In addition, it has been proposed that AAC mediates mitochondrial uncoupling, but it has proven difficult to demonstrate this function or to elucidate its mechanisms. Here we record AAC currents directly from inner mitochondrial membranes from various mouse tissues and identify two distinct transport modes: ADP/ATP exchange and H
Identifiants
pubmed: 31341297
doi: 10.1038/s41586-019-1400-3
pii: 10.1038/s41586-019-1400-3
pmc: PMC6662629
mid: NIHMS1530212
doi:
Substances chimiques
Coenzymes
0
Fatty Acids
0
Protons
0
Adenosine Diphosphate
61D2G4IYVH
Adenosine Triphosphate
8L70Q75FXE
Mitochondrial ADP, ATP Translocases
9068-80-8
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
515-520Subventions
Organisme : NINDS NIH HHS
ID : R01 NS021328
Pays : United States
Organisme : NICHD NIH HHS
ID : U54 HD086984
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM107710
Pays : United States
Organisme : NIDDK NIH HHS
ID : K99 DK105203
Pays : United States
Organisme : NIDDK NIH HHS
ID : R00 DK105203
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM118939
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH108592
Pays : United States
Organisme : NIH HHS
ID : R01 OD010944
Pays : United States
Références
Klingenberg, M. The ADP and ATP transport in mitochondria and its carrier. Biochim. Biophys. Acta 1778, 1978–2021 (2008).
doi: 10.1016/j.bbamem.2008.04.011
Stepien, G., Torroni, A., Chung, A. B., Hodge, J. A. & Wallace, D. C. Differential expression of adenine nucleotide translocator isoforms in mammalian tissues and during muscle cell differentiation. J. Biol. Chem. 267, 14592–14597 (1992).
pubmed: 1378836
pmcid: 1378836
Rodić, N. et al. DNA methylation is required for silencing of ant4, an adenine nucleotide translocase selectively expressed in mouse embryonic stem cells and germ cells. Stem Cells 23, 1314–1323 (2005).
doi: 10.1634/stemcells.2005-0119
Levy, S. E., Chen, Y. S., Graham, B. H. & Wallace, D. C. Expression and sequence analysis of the mouse adenine nucleotide translocase 1 and 2 genes. Gene 254, 57–66 (2000).
doi: 10.1016/S0378-1119(00)00252-3
Graham, B. H. et al. A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nat. Genet. 16, 226–234 (1997).
doi: 10.1038/ng0797-226
Ruprecht, J. J. et al. The molecular mechanism of transport by the mitochondrial ADP/ATP carrier. Cell 176, 435–447.e15 (2019).
doi: 10.1016/j.cell.2018.11.025
Andreyev, A. Yu. et al. Carboxyatractylate inhibits the uncoupling effect of free fatty acids. FEBS Lett. 226, 265–269 (1988).
doi: 10.1016/0014-5793(88)81436-4
Skulachev, V. P. Uncoupling: new approaches to an old problem of bioenergetics. Biochim. Biophys. Acta Bioenerg. 1363, 100–124 (1998).
doi: 10.1016/S0005-2728(97)00091-1
Brustovetsky, N. & Klingenberg, M. The reconstituted ADP/ATP carrier can mediate H
pubmed: 7961643
pmcid: 7961643
Brand, M. D. et al. The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem. J. 392, 353–362 (2005).
doi: 10.1042/BJ20050890
Halestrap, A. P. & Richardson, A. P. The mitochondrial permeability transition: A current perspective on its identity and role in ischaemia/reperfusion injury. J. Mol. Cell. Cardiol. 78, 129–141 (2015).
doi: 10.1016/j.yjmcc.2014.08.018
Bernardi, P., Rasola, A., Forte, M. & Lippe, G. The mitochondrial permeability transition pore: channel formation by F-ATP synthase, integration in signal transduction, and role in pathophysiology. Physiol. Rev. 95, 1111–1155 (2015).
doi: 10.1152/physrev.00001.2015
Korshunov, S. S., Skulachev, V. P. & Starkov, A. A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 416, 15–18 (1997).
doi: 10.1016/S0014-5793(97)01159-9
Wojtczak, L. & Schönfeld, P. Effect of fatty acids on energy coupling processes in mitochondria. Biochim. Biophys. Acta 1183, 41–57 (1993).
doi: 10.1016/0005-2728(93)90004-Y
Bouillaud, F., Weissenbach, J. & Ricquier, D. Complete cDNA-derived amino acid sequence of rat brown fat uncoupling protein. J. Biol. Chem. 261, 1487–1490 (1986).
pubmed: 3753702
pmcid: 3753702
Aquila, H., Link, T. A. & Klingenberg, M. The uncoupling protein from brown fat mitochondria is related to the mitochondrial ADP/ATP carrier. Analysis of sequence homologies and of folding of the protein in the membrane. EMBO J. 4, 2369–2376 (1985).
doi: 10.1002/j.1460-2075.1985.tb03941.x
Fedorenko, A., Lishko, P. V. & Kirichok, Y. Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell 151, 400–413 (2012).
doi: 10.1016/j.cell.2012.09.010
Bertholet, A. M. et al. Mitochondrial patch clamp of beige adipocytes reveals UCP1-positive and UCP1-negative cells both exhibiting futile creatine cycling. Cell Metab. 25, 811–822.e814 (2017).
doi: 10.1016/j.cmet.2017.03.002
Roussel, D., Harding, M., Runswick, M. J., Walker, J. E. & Brand, M. D. Does any yeast mitochondrial carrier have a native uncoupling protein function? J. Bioenerg. Biomembr. 34, 165–176 (2002).
doi: 10.1023/A:1016027302232
Echtay, K. S., Winkler, E., Frischmuth, K. & Klingenberg, M. Uncoupling proteins 2 and 3 are highly active H
doi: 10.1073/pnas.98.4.1416
Jabůrek, M. et al. Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J. Biol. Chem. 274, 26003–26007 (1999).
doi: 10.1074/jbc.274.37.26003
Krauss, S., Zhang, C. Y. & Lowell, B. B. The mitochondrial uncoupling-protein homologues. Nat. Rev. Mol. Cell Biol. 6, 248–261 (2005).
doi: 10.1038/nrm1592
Samartsev, V. N. et al. Involvement of aspartate/glutamate antiporter in fatty acid-induced uncoupling of liver mitochondria. Biochim. Biophys. Acta Bioenerg. 1319, 251–257 (1997).
doi: 10.1016/S0005-2728(96)00166-1
Wieckowski, M. R. & Wojtczak, L. Involvement of the dicarboxylate carrier in the protonophoric action of long-chain fatty acids in mitochondria. Biochem. Biophys. Res. Commun. 232, 414–417 (1997).
doi: 10.1006/bbrc.1997.6298
Zácková, M., Krämer, R. & Jezek, P. Interaction of mitochondrial phosphate carrier with fatty acids and hydrophobic phosphate analogs. Int. J. Biochem. Cell Biol. 32, 499–508 (2000).
doi: 10.1016/S1357-2725(00)00006-6
Engstová, H. et al. Natural and azido fatty acids inhibit phosphate transport and activate fatty acid anion uniport mediated by the mitochondrial phosphate carrier. J. Biol. Chem. 276, 4683–4691 (2001).
doi: 10.1074/jbc.M009409200
Gutknecht, J. Proton conductance caused by long-chain fatty acids in phospholipid bilayer membranes. J. Membr. Biol. 106, 83–93 (1988).
doi: 10.1007/BF01871769
Kokoszka, J. E. et al. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427, 461–465 (2004).
doi: 10.1038/nature02229
Penzo, D., Tagliapietra, C., Colonna, R., Petronilli, V. & Bernardi, P. Effects of fatty acids on mitochondria: implications for cell death. Biochim. Biophys. Acta Bioenerg. 1555, 160–165 (2002).
doi: 10.1016/S0005-2728(02)00272-4
Wieckowski, M. R. & Wojtczak, L. Fatty acid-induced uncoupling of oxidative phosphorylation is partly due to opening of the mitochondrial permeability transition pore. FEBS Lett. 423, 339–342 (1998).
doi: 10.1016/S0014-5793(98)00118-5
Schönfeld, P. & Bohnensack, R. Fatty acid-promoted mitochondrial permeability transition by membrane depolarization and binding to the ADP/ATP carrier. FEBS Lett. 420, 167–170 (1997).
doi: 10.1016/S0014-5793(97)01511-1
Nedergaard, J. & Cannon, B. The ‘novel’ ‘uncoupling’ proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions. Exp. Physiol. 88, 65–84 (2003).
doi: 10.1113/eph8802502
Bouillaud, F. UCP2, not a physiologically relevant uncoupler but a glucose sparing switch impacting ROS production and glucose sensing. Biochim. Biophys. Acta 1787, 377–383 (2009).
doi: 10.1016/j.bbabio.2009.01.003
Vozza, A. et al. UCP2 transports C4 metabolites out of mitochondria, regulating glucose and glutamine oxidation. Proc. Natl Acad. Sci. USA 111, 960–965 (2014).
doi: 10.1073/pnas.1317400111
Echtay, K. S. et al. Superoxide activates mitochondrial uncoupling proteins. Nature 415, 96–99 (2002).
doi: 10.1038/415096a
Echtay, K. S. et al. A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 22, 4103–4110 (2003).
doi: 10.1093/emboj/cdg412
Parker, N., Affourtit, C., Vidal-Puig, A. & Brand, M. D. Energization-dependent endogenous activation of proton conductance in skeletal muscle mitochondria. Biochem J. 412, 131–139 (2008).
doi: 10.1042/BJ20080006
Nishikimi, A. et al. Tributyltin interacts with mitochondria and induces cytochrome c release. Biochem. J. 356, 621–626 (2001).
doi: 10.1042/bj3560621
Vieira, H. L. et al. The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene 20, 4305–4316 (2001).
doi: 10.1038/sj.onc.1204575
Cunningham, S. A., Wiesinger, H. & Nicholls, D. G. Quantification of fatty acid activation of the uncoupling protein in brown adipocytes and mitochondria from the guinea-pig. Eur. J. Biochem. 157, 415–420 (1986).
doi: 10.1111/j.1432-1033.1986.tb09683.x
Klingenberg, M. & Huang, S. G. Structure and function of the uncoupling protein from brown adipose tissue. Biochim. Biophys. Acta 1415, 271–296 (1999).
doi: 10.1016/S0005-2736(98)00232-6
Cho, J. et al. Mitochondrial ATP transporter Ant2 depletion impairs erythropoiesis and B lymphopoiesis. Cell Death Differ. 22, 1437–1450 (2015).
doi: 10.1038/cdd.2014.230
Morrow, R. M. et al. Mitochondrial energy deficiency leads to hyperproliferation of skeletal muscle mitochondria and enhanced insulin sensitivity. Proc. Natl Acad. Sci. USA 114, 2705–2710 (2017).
doi: 10.1073/pnas.1700997114
Bertholet, A. M. & Kirichok, Y. UCP1: A transporter for H
doi: 10.1016/j.biochi.2016.10.013
Garlid, K. D., Orosz, D. E., Modrianský, M., Vassanelli, S. & Jezek, P. On the mechanism of fatty acid-induced proton transport by mitochondrial uncoupling protein. J. Biol. Chem. 271, 2615–2620 (1996).
doi: 10.1074/jbc.271.5.2615
Pebay-Peyroula, E. et al. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39–44 (2003).
doi: 10.1038/nature02056
Esposito, L. A., Melov, S., Panov, A., Cottrell, B. A. & Wallace, D. C. Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl Acad. Sci. USA 96, 4820–4825 (1999).
doi: 10.1073/pnas.96.9.4820
Gadd, M. E. et al. Mitochondrial iPLA2 activity modulates the release of cytochrome c from mitochondria and influences the permeability transition. J Biol Chem 281, 6931–6939 (2006).
doi: 10.1074/jbc.M510845200
Kinsey, G. R., McHowat, J., Beckett, C. S. & Schnellmann, R. G. Identification of calcium-independent phospholipase A
doi: 10.1152/ajprenal.00318.2006
Burke, J. E. & Dennis, E. A. Phospholipase A2 structure/function, mechanism, and signaling. J. Lipid Res. 50, S237–S242 (2009).
doi: 10.1194/jlr.R800033-JLR200