Two independent respiratory chains adapt OXPHOS performance to glycolytic switch

Cell Metabolism - Tập 34 - Trang 1792-1808.e6 - 2022
Erika Fernández-Vizarra1,2,3, Sandra López-Calcerrada4, Ana Sierra-Magro4, Rafael Pérez-Pérez4, Luke E. Formosa5, Daniella H. Hock6, María Illescas4, Ana Peñas4, Michele Brischigliaro3, Shujing Ding1, Ian M. Fearnley1, Charalampos Tzoulis7, Robert D.S. Pitceathly8, Joaquín Arenas4,9, Miguel A. Martín4,9, David A. Stroud6, Massimo Zeviani1,2,10, Michael T. Ryan5, Cristina Ugalde4,9
1Medical Research Council Mitochondrial Biology Unit, University of Cambridge, Cambridge, CB2 0XY, UK
2Veneto Institute of Molecular Medicine, 35129 Padova, Italy
3Department of Biomedical Sciences, University of Padova, 35131 Padova, Italy
4Instituto de Investigación Hospital 12 de Octubre, Madrid 28041, Spain
5Department of Biochemistry and Molecular Biology, Monash Biomedicine Discovery Institute, Monash University, 3800 Melbourne, Australia
6Department of Biochemistry and Pharmacology, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, 3052 Melbourne, Australia
7Neuro-SysMed Center of Excellence for Clinical Research in Neurological Diseases, Department of Neurology, Haukeland University Hospital and Department of Clinical Medicine, University of Bergen, Pb 7804, 5020 Bergen, Norway
8Department of Neuromuscular Diseases, UCL Queen Square Institute of Neurology and The National Hospital for Neurology and Neurosurgery, London WC1N 3BG, UK
9Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), U723, Madrid, Spain
10Department of Neurosciences, University of Padova, 35128 Padova, Italy

Tài liệu tham khảo

Acín-Pérez, 2008, Respiratory active mitochondrial supercomplexes, Mol. Cell, 32, 529, 10.1016/j.molcel.2008.10.021 Anwar, 2021, Targeting pyruvate dehydrogenase kinase signaling in the development of effective cancer therapy, Biochim. Biophys. Acta Rev. Cancer, 1876, 188568, 10.1016/j.bbcan.2021.188568 Balsa, 2019, ER and nutrient stress promote assembly of respiratory chain supercomplexes through the PERK-eIF2alpha axis, Mol. Cell, 74, 877, 10.1016/j.molcel.2019.03.031 Bayona-Bafaluy, 2021, Oxidative phosphorylation system and cell culture media, Trends Cell Biol., 31, 618, 10.1016/j.tcb.2021.05.003 Berndtsson, 2020, Respiratory supercomplexes enhance electron transport by decreasing cytochrome c diffusion distance, EMBO Rep., 21, e51015, 10.15252/embr.202051015 Bianchi, 2004, The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis, J. Biol. Chem., 279, 36562, 10.1074/jbc.M405135200 Blaza, 2014, Kinetic evidence against partitioning of the ubiquinone pool and the catalytic relevance of respiratory-chain supercomplexes, Proc. Natl. Acad. Sci. USA, 111, 15735, 10.1073/pnas.1413855111 Calvo, 2016, MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins, Nucleic Acids Res., 44, D1251, 10.1093/nar/gkv1003 Calvo, 2020, Functional role of respiratory supercomplexes in mice: SCAF1 relevance and segmentation of the Q pool, Sci. Adv., 6, eaba7509, 10.1126/sciadv.aba7509 Cogliati, 2016, Mechanism of super-assembly of respiratory complexes III and IV, Nature, 539, 579, 10.1038/nature20157 Cogliati, 2021, Regulation and functional role of the electron transport chain supercomplexes, Biochem. Soc. Trans., 49, 2655, 10.1042/BST20210460 Cox, 2008, MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification, Nat. Biotechnol., 26, 1367, 10.1038/nbt.1511 Cruciat, 2000, The cytochrome bc1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria, J. Biol. Chem., 275, 18093, 10.1074/jbc.M001901200 Doerrier, 2018, High-resolution FluoRespirometry and OXPHOS protocols for human cells, permeabilized fibers from small biopsies of muscle, and isolated mitochondria, Methods Mol. Biol., 1782, 31, 10.1007/978-1-4939-7831-1_3 Echeverri Ruiz, 2021, Dynamic regulation of mitochondrial pyruvate metabolism is necessary for orthotopic pancreatic tumor growth, Cancer Metab., 9, 39, 10.1186/s40170-021-00275-4 Fang, 2021, A membrane arm of mitochondrial complex I sufficient to promote respirasome formation, Cell Rep., 35, 108963, 10.1016/j.celrep.2021.108963 Fedor, 2018, Mitochondrial supercomplexes do not enhance catalysis by quinone channeling, Cell Metab., 28, 525, 10.1016/j.cmet.2018.05.024 Fernández-Vizarra, 2022, Cooperative assembly of the mitochondrial respiratory chain, Trends Biochem. Sci., 10.1016/j.tibs.2022.07.005 Fernández-Vizarra, 2021, SILAC-based complexome profiling dissects the structural organization of the human respiratory supercomplexes in SCAFIKO cells, Biochim. Biophys. Acta Bioenerg., 1862, 148414, 10.1016/j.bbabio.2021.148414 García-Poyatos, 2020, Scaf1 promotes respiratory supercomplexes and metabolic efficiency in zebrafish, EMBO Rep., 21, e50287, 10.15252/embr.202050287 Gray, 2014, Regulation of pyruvate metabolism and human disease, Cell. Mol. Life Sci., 71, 2577, 10.1007/s00018-013-1539-2 Gu, 2016, The architecture of the mammalian respirasome, Nature, 537, 639, 10.1038/nature19359 Guo, 2017, Architecture of human mitochondrial respiratory megacomplex I2III2IV2, Cell, 170, 1247, 10.1016/j.cell.2017.07.050 Hirst, 2018, Open questions: respiratory chain supercomplexes-why are they there and what do they do?, BMC Biol., 16, 111, 10.1186/s12915-018-0577-5 Hock, 2020, HIGD2A is required for assembly of the COX3 module of human mitochondrial complex IV, Mol. Cell. Proteomics, 19, 1145, 10.1074/mcp.RA120.002076 Hofhaus, 1996, Use of polarography to detect respiration defects in cell cultures, Methods Enzymol., 264, 476, 10.1016/S0076-6879(96)64043-9 Hollinshead, 2020, Respiratory supercomplexes promote mitochondrial efficiency and growth in severely hypoxic pancreatic cancer, Cell Rep., 33, 108231, 10.1016/j.celrep.2020.108231 Ikeda, 2013, A stabilizing factor for mitochondrial respiratory supercomplex assembly regulates energy metabolism in muscle, Nat. Commun., 4, 2147, 10.1038/ncomms3147 Ikeda, 2019, Mitochondrial supercomplex assembly promotes breast and endometrial tumorigenesis by metabolic alterations and enhanced hypoxia tolerance, Nat. Commun., 10, 4108, 10.1038/s41467-019-12124-6 Javadov, 2021, Mitochondrial respiratory supercomplexes in mammalian cells: structural versus functional role, J. Mol. Med. (Berl), 99, 57, 10.1007/s00109-020-02004-8 Labun, 2016, CHOPCHOP v2: a web tool for the next generation of CRISPR genome engineering, Nucleic Acids Res., 44, W272, 10.1093/nar/gkw398 Lapuente-Brun, 2013, Supercomplex assembly determines electron flux in the mitochondrial electron transport chain, Science, 340, 1567, 10.1126/science.1230381 Lenaz, 2007, Kinetics of integrated electron transfer in the mitochondrial respiratory chain: random collisions vs. solid state electron channeling, Am. J. Physiol. Cell Physiol., 292, C1221, 10.1152/ajpcell.00263.2006 Lenaz, 2009, Mobility and function of coenzyme Q (ubiquinone) in the mitochondrial respiratory chain, Biochim. Biophys. Acta, 1787, 563, 10.1016/j.bbabio.2009.02.019 Letts, 2017, Clarifying the supercomplex: the higher-order organization of the mitochondrial electron transport chain, Nat. Struct. Mol. Biol., 24, 800, 10.1038/nsmb.3460 Letts, 2016, The architecture of respiratory supercomplexes, Nature, 537, 644, 10.1038/nature19774 Letts, 2019, Structures of respiratory supercomplex I+III2 reveal functional and conformational crosstalk, Mol. Cell, 75, 1131, 10.1016/j.molcel.2019.07.022 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method, Methods, 25, 402, 10.1006/meth.2001.1262 Lobo-Jarne, 2018, Respiratory chain supercomplexes: structures, function and biogenesis, Semin. Cell Dev. Biol., 76, 179, 10.1016/j.semcdb.2017.07.021 Lobo-Jarne, 2018, Human COX7A2L regulates complex III biogenesis and promotes supercomplex organization remodeling without affecting mitochondrial bioenergetics, Cell Rep., 25, 1786, 10.1016/j.celrep.2018.10.058 Lobo-Jarne, 2020, Multiple pathways coordinate assembly of human mitochondrial complex IV and stabilization of respiratory supercomplexes, EMBO J., 39, e103912, 10.15252/embj.2019103912 Lopez-Fabuel, 2016, Complex I assembly into supercomplexes determines differential mitochondrial ROS production in neurons and astrocytes, Proc. Natl. Acad. Sci. USA, 113, 13063, 10.1073/pnas.1613701113 Milenkovic, 2017, The enigma of the respiratory chain supercomplex, Cell Metab., 25, 765, 10.1016/j.cmet.2017.03.009 Molinié, 2022, MDH2 produced OAA is a metabolic switch rewiring the fuelling of respiratory chain and TCA cycle, Biochim. Biophys. Acta Bioenerg., 1863, 148532, 10.1016/j.bbabio.2022.148532 Moreno-Lastres, 2012, Mitochondrial complex I plays an essential role in human respirasome assembly, Cell Metab., 15, 324, 10.1016/j.cmet.2012.01.015 Mourier, 2014, The respiratory chain supercomplex organization is independent of COX7a2l isoforms, Cell Metab., 20, 1069, 10.1016/j.cmet.2014.11.005 Nijtmans, 2002, Blue Native electrophoresis to study mitochondrial and other protein complexes, Methods, 26, 327, 10.1016/S1046-2023(02)00038-5 Ogunjimi, 2000, Evidence for a conformational change in subunit III of bovine heart mitochondrial cytochrome c oxidase, J. Bioenerg. Biomembr., 32, 617, 10.1023/A:1005678729157 Páleníková, 2021, Quantitative density gradient analysis by mass spectrometry (qDGMS) and complexome profiling analysis (ComPrAn) R package for the study of macromolecular complexes, Biochim. Biophys. Acta Bioenerg., 1862, 148399, 10.1016/j.bbabio.2021.148399 Páleníková, 2021, Duplexing complexome profiling with SILAC to study human respiratory chain assembly defects, Biochim. Biophys. Acta Bioenerg., 1862, 148395, 10.1016/j.bbabio.2021.148395 Pérez-Pérez, 2016, COX7A2L is a mitochondrial complex III binding protein that stabilizes the III2+IV supercomplex without affecting respirasome formation, Cell Rep., 16, 2387, 10.1016/j.celrep.2016.07.081 Pesta, 2012, High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle, Methods Mol. Biol., 810, 25, 10.1007/978-1-61779-382-0_3 Protasoni, 2020, Respiratory supercomplexes act as a platform for complex III-mediated maturation of human mitochondrial complexes I and IV, EMBO J., 39, e102817, 10.15252/embj.2019102817 Ran, 2013, Genome engineering using the CRISPR-Cas9 system, Nat. Protoc., 8, 2281, 10.1038/nprot.2013.143 Robinson, 1992, Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts, Biochem. Med. Metab. Biol., 48, 122, 10.1016/0885-4505(92)90056-5 Schägger, 2000, Supercomplexes in the respiratory chains of yeast and mammalian mitochondria, EMBO J., 19, 1777, 10.1093/emboj/19.8.1777 Schell, 2014, A role for the mitochondrial pyruvate carrier as a repressor of the Warburg effect and colon cancer cell growth, Mol. Cell, 56, 400, 10.1016/j.molcel.2014.09.026 Schell, 2017, Control of intestinal stem cell function and proliferation by mitochondrial pyruvate metabolism, Nat. Cell Biol., 19, 1027, 10.1038/ncb3593 Schneider, 2012, NIH Image to ImageJ: 25 years of image analysis, Nat. Methods, 9, 671, 10.1038/nmeth.2089 Shiba, 2017, Deficiency of COX7RP, a mitochondrial supercomplex assembly promoting factor, lowers blood glucose level in mice, Sci. Rep., 7, 7606, 10.1038/s41598-017-08081-z Sinkler, 2017, Tissue- and condition-specific isoforms of mammalian cytochrome c oxidase subunits: From function to human disease, Oxid. Med. Cell. Longev., 2017, 1534056, 10.1155/2017/1534056 Smith, 2019, MitoMiner v4.0: an updated database of mitochondrial localization evidence, phenotypes and diseases, Nucleic Acids Res., 47, D1225, 10.1093/nar/gky1072 Sorge, 2020, ATF4-induced Warburg metabolism drives over-proliferation in Drosophila, Cell Rep., 31, 107659, 10.1016/j.celrep.2020.107659 Sousa, 2016, Functional asymmetry and electron flow in the bovine respirasome, eLife, 5, e21290, 10.7554/eLife.21290 Stacpoole, 2017, Therapeutic targeting of the pyruvate dehydrogenase complex/pyruvate dehydrogenase kinase (PDC/PDK) axis in cancer, J. Natl. Cancer Inst., 109, djx071, 10.1093/jnci/djx071 Stroud, 2016, Accessory subunits are integral for assembly and function of human mitochondrial complex I, Nature, 538, 123, 10.1038/nature19754 Stuchebrukhov, 2020, Kinetic advantage of forming respiratory supercomplexes, Biochim. Biophys. Acta Bioenerg., 1861, 148193, 10.1016/j.bbabio.2020.148193 Szibor, 2020, Bioenergetic consequences from xenotopic expression of a tunicate AOX in mouse mitochondria: switch from RET and ROS to FET, Biochim. Biophys. Acta Bioenerg., 1861, 148137, 10.1016/j.bbabio.2019.148137 Tataranni, 2019, Dichloroacetate affects mitochondrial function and stemness-associated properties in pancreatic cancer cell lines, Cells, 8, 478, 10.3390/cells8050478 Timón-Gómez, 2020, Distinct roles of mitochondrial HIGD1A and HIGD2A in respiratory complex and supercomplex biogenesis, Cell Rep., 31, 107607, 10.1016/j.celrep.2020.107607 Trouillard, 2011, Questioning the functional relevance of mitochondrial supercomplexes by time-resolved analysis of the respiratory chain, Proc. Natl. Acad. Sci. USA, 108, E1027, 10.1073/pnas.1109510108 Tyanova, 2016, The Perseus computational platform for comprehensive analysis of (prote)omics data, Nat. Methods, 13, 731, 10.1038/nmeth.3901 van Strien, 2021, CEDAR, an online resource for the reporting and exploration of complexome profiling data, Biochim. Biophys. Acta Bioenerg., 1862, 148411, 10.1016/j.bbabio.2021.148411 Vercellino, 2021, Structure and assembly of the mammalian mitochondrial supercomplex CIII2CIV, Nature, 598, 364, 10.1038/s41586-021-03927-z Vercellino, 2022, The assembly, regulation and function of the mitochondrial respiratory chain, Nat. Rev. Mol. Cell Biol., 23, 141, 10.1038/s41580-021-00415-0 Vidoni, 2017, MR-1S interacts with PET100 and PET117 in module-based assembly of human cytochrome c oxidase, Cell Rep., 18, 1727, 10.1016/j.celrep.2017.01.044 Villani, 2000, In vivo control of respiration by cytochrome c oxidase in human cells, Free Radic. Biol. Med., 29, 202, 10.1016/S0891-5849(00)00303-8 Villani, 1998, Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types, J. Biol. Chem., 273, 31829, 10.1074/jbc.273.48.31829 Wu, 2016, Structure of mammalian respiratory supercomplex I1III2IV1, Cell, 167, 1598, 10.1016/j.cell.2016.11.012 Zhang, 2016, COX7AR is a stress-inducible mitochondrial COX subunit that promotes breast cancer malignancy, Sci. Rep., 6, 31742, 10.1038/srep31742 Zong, 2018, Structure of the intact 14-subunit human cytochrome c oxidase, Cell Res., 28, 1026, 10.1038/s41422-018-0071-1