Structural basis of mitochondrial membrane bending by the I-II-III
Cryoelectron Microscopy
Electron Transport
Electron Transport Complex III
/ chemistry
Electron Transport Complex IV
/ chemistry
Mitochondria
/ chemistry
Mitochondrial Membranes
/ chemistry
Electron Transport Complex II
/ chemistry
Electron Transport Complex I
/ chemistry
Protein Multimerization
Protein Subunits
/ chemistry
Molecular Dynamics Simulation
Binding Sites
Evolution, Molecular
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
received:
28
06
2022
accepted:
09
02
2023
medline:
31
3
2023
pubmed:
24
3
2023
entrez:
23
3
2023
Statut:
ppublish
Résumé
Mitochondrial energy conversion requires an intricate architecture of the inner mitochondrial membrane
Identifiants
pubmed: 36949187
doi: 10.1038/s41586-023-05817-y
pii: 10.1038/s41586-023-05817-y
pmc: PMC10060162
doi:
Substances chimiques
Electron Transport Complex III
EC 7.1.1.8
Electron Transport Complex IV
EC 1.9.3.1
Electron Transport Complex II
EC 1.3.5.1
Electron Transport Complex I
EC 7.1.1.2
Protein Subunits
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
934-938Subventions
Organisme : Medical Research Council
ID : MR/M00936X/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/T032154/1
Pays : United Kingdom
Informations de copyright
© 2023. The Author(s).
Références
Schägger, H. & Pfeiffer, K. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19, 1777–1783 (2000).
pubmed: 10775262
pmcid: 302020
doi: 10.1093/emboj/19.8.1777
Caruana, N. J. & Stroud, D. A. The road to the structure of the mitochondrial respiratory chain supercomplex. Biochem. Soc. Trans. 48, 621–629 (2020).
pubmed: 32311046
pmcid: 7200630
doi: 10.1042/BST20190930
Bezawork-Geleta, A., Rohlena, J., Dong, L., Pacak, K. & Neuzil, J. Mitochondrial complex II: at the crossroads. Trends Biochem. Sci. 42, 312–325 (2017).
pubmed: 28185716
pmcid: 7441821
doi: 10.1016/j.tibs.2017.01.003
Acin-Perez, R., Fernandez-Silva, P., Peleato, M. L., Perez-Martos, A. & Enriquez, J. A. Respiratory active mitochondrial supercomplexes. Mol. Cell 32, 529–539 (2008).
pubmed: 19026783
doi: 10.1016/j.molcel.2008.10.021
Jiang, C. et al. Regulation of mitochondrial respiratory chain complex levels, organization, and function by arginyltransferase 1. Front. Cell Dev. Biol. 8, 603688 (2020).
pubmed: 33409279
pmcid: 7779560
doi: 10.3389/fcell.2020.603688
Lapuente-Brun, E. et al. Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340, 1567–1570 (2013).
pubmed: 23812712
doi: 10.1126/science.1230381
Schon, E. A. & Dencher, N. A. Heavy breathing: energy conversion by mitochondrial respiratory supercomplexes. Cell Metab. 9, 1–3 (2009).
pubmed: 19117538
doi: 10.1016/j.cmet.2008.12.011
Zhou, L., Maldonado, M., Padavannil, A., Guo, F. & Letts, J. A. Structures of Tetrahymena’s respiratory chain reveal the diversity of eukaryotic core metabolism. Science 376, 831–839 (2022).
pubmed: 35357889
doi: 10.1126/science.abn7747
Colina-Tenorio, L., Horten, P., Pfanner, N. & Rampelt, H. Shaping the mitochondrial inner membrane in health and disease. J. Intern. Med. 287, 645–664 (2020).
pubmed: 32012363
doi: 10.1111/joim.13031
Blum, T. B., Hahn, A., Meier, T., Davies, K. M. & Kühlbrandt, W. Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows. Proc. Natl Acad. Sci. USA 116, 4250–4255 (2019).
pubmed: 30760595
pmcid: 6410833
doi: 10.1073/pnas.1816556116
Mühleip, A., McComas, S. E. & Amunts, A. Structure of a mitochondrial ATP synthase with bound native cardiolipin. eLife 8, e51179 (2019).
pubmed: 31738165
pmcid: 6930080
doi: 10.7554/eLife.51179
Kock Flygaard, R., Mühleip, A., Tobiasson, V. & Amunts, A. Type III ATP synthase is a symmetry-deviated dimer that induces membrane curvature through tetramerization. Nat. Commun. 11, 5342 (2020).
doi: 10.1038/s41467-020-18993-6
Pinke, G., Zhou, L. & Sazanov, L. A. Cryo-EM structure of the entire mammalian F-type ATP synthase. Nat. Struct. Mol. Biol. 27, 1077–1085 (2020).
pubmed: 32929284
doi: 10.1038/s41594-020-0503-8
Mühleip, A. et al. ATP synthase hexamer assemblies shape cristae of Toxoplasma mitochondria. Nat. Commun. 12, 120 (2021).
pubmed: 33402698
pmcid: 7785744
doi: 10.1038/s41467-020-20381-z
Mühleip, A. W. et al. Helical arrays of U-shaped ATP synthase dimers form tubular cristae in ciliate mitochondria. Proc. Natl Acad. Sci. USA 113, 8442–8447 (2016).
pubmed: 27402755
pmcid: 4968746
doi: 10.1073/pnas.1525430113
Allen, R. D., Schroeder, C. C. & Fok, A. K. An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J. Cell Biol. 108, 2233–2240 (1989).
pubmed: 2525561
doi: 10.1083/jcb.108.6.2233
Gu, J. et al. The architecture of the mammalian respirasome. Nature 537, 639–643 (2016).
pubmed: 27654917
doi: 10.1038/nature19359
Guo, R., Zong, S., Wu, M., Gu, J. & Yang, M. Architecture of human mitochondrial respiratory megacomplex I
pubmed: 28844695
doi: 10.1016/j.cell.2017.07.050
Klusch, N., Senkler, J., Yildiz, O., Kuhlbrandt, W. & Braun, H. P. A ferredoxin bridge connects the two arms of plant mitochondrial complex I. Plant Cell 33, 2072–2091 (2021).
pubmed: 33768254
pmcid: 8290278
doi: 10.1093/plcell/koab092
Tobiasson, V. & Amunts, A. Ciliate mitoribosome illuminates evolutionary steps of mitochondrial translation. eLife 9, e59264 (2020).
pubmed: 32553108
pmcid: 7326499
doi: 10.7554/eLife.59264
Tobiasson, V., Berzina, I. & Amunts, A. Structure of a mitochondrial ribosome with fragmented rRNA in complex with membrane-targeting elements. Nat. Comm. 13, 6132 (2022).
Hagerhall, C. Succinate: quinone oxidoreductases. Variations on a conserved theme. Biochim. Biophys. Acta 1320, 107–141 (1997).
pubmed: 9210286
doi: 10.1016/S0005-2728(97)00019-4
Sun, F. et al. Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121, 1043–1057 (2005).
pubmed: 15989954
doi: 10.1016/j.cell.2005.05.025
Balabaskaran Nina, P. et al. Highly divergent mitochondrial ATP synthase complexes in Tetrahymena thermophila. PLoS Biol. 8, e1000418 (2010).
pubmed: 20644710
pmcid: 2903591
doi: 10.1371/journal.pbio.1000418
Berndtsson, J. et al. Respiratory supercomplexes enhance electron transport by decreasing cytochrome c diffusion distance. EMBO Rep. 21, e51015 (2020).
pubmed: 33016568
pmcid: 7726804
doi: 10.15252/embr.202051015
Tremmel, I. G., Kirchhoff, H., Weis, E. & Farquhar, G. D. Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins. Biochim. Biophys. Acta 1607, 97–109 (2003).
pubmed: 14670600
doi: 10.1016/j.bbabio.2003.09.004
Kirchhoff, H. Diffusion of molecules and macromolecules in thylakoid membranes. Biochim. Biophys. Acta 1837, 495–502 (2014).
pubmed: 24246635
doi: 10.1016/j.bbabio.2013.11.003
Letts, J. A., Fiedorczuk, K. & Sazanov, L. A. The architecture of respiratory supercomplexes. Nature 537, 644–648 (2016).
pubmed: 27654913
doi: 10.1038/nature19774
Althoff, T., Mills, D. J., Popot, J. L. & Kuhlbrandt, W. Arrangement of electron transport chain components in bovine mitochondrial supercomplex I
pubmed: 21909073
pmcid: 3243592
doi: 10.1038/emboj.2011.324
Wu, M., Gu, J., Guo, R., Huang, Y. & Yang, M. Structure of mammalian respiratory supercomplex I
pubmed: 27912063
doi: 10.1016/j.cell.2016.11.012
Gao, X. et al. Structural basis for the quinone reduction in the bc
pubmed: 12885240
doi: 10.1021/bi0341814
Zhang, Z. et al. Electron transfer by domain movement in cytochrome bc
pubmed: 9565029
doi: 10.1038/33612
Rajagukguk, S. et al. Effect of mutations in the cytochrome b ef loop on the electron-transfer reactions of the Rieske iron–sulfur protein in the cytochrome bc
pubmed: 17253777
doi: 10.1021/bi062094g
Chen, M. et al. Distinct structural modulation of photosystem I and lipid environment stabilizes its tetrameric assembly. Nat. Plants 6, 314–320 (2020).
Wolf, D. M. et al. Individual cristae within the same mitochondrion display different membrane potentials and are functionally independent. EMBO J. 38, e101056 (2019).
pubmed: 31609012
pmcid: 6856616
doi: 10.15252/embj.2018101056
Davies, K. M. et al. Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc. Natl Acad. Sci. USA 108, 14121–14126 (2011).
pubmed: 21836051
pmcid: 3161574
doi: 10.1073/pnas.1103621108
Paumard, P. et al. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21, 221–230 (2002).
pubmed: 11823415
pmcid: 125827
doi: 10.1093/emboj/21.3.221
Jha, P., Wang, X. & Auwerx, J. Analysis of mitochondrial respiratory chain supercomplexes using blue native polyacrylamide gel electrophoresis (BN-PAGE). Curr. Protoc. Mouse Biol. 6, 1–14 (2016).
pubmed: 26928661
pmcid: 4823378
doi: 10.1002/9780470942390.mo150182
Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. eLife 7, e42166 (2018).
pubmed: 30412051
pmcid: 6250425
doi: 10.7554/eLife.42166
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
pubmed: 28165473
doi: 10.1038/nmeth.4169
Hagen, W. J. H., Wan, W. & Briggs, J. A. G. Implementation of a cryo-electron tomography tilt-scheme optimized for high resolution subtomogram averaging. J. Struct. Biol. 197, 191–198 (2017).
pubmed: 27313000
pmcid: 5287356
doi: 10.1016/j.jsb.2016.06.007
Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71–76 (1996).
pubmed: 8742726
doi: 10.1006/jsbi.1996.0013
Nicastro, D. et al. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313, 944–948 (2006).
pubmed: 16917055
doi: 10.1126/science.1128618
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).
pubmed: 15572765
doi: 10.1107/S0907444904019158
Afonine, P. V. et al. Real-space refinement in PHENIX for cryo-EM and crystallography. Acta Crystallogr. D 74, 531–544 (2018).
doi: 10.1107/S2059798318006551
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).
pubmed: 20057044
doi: 10.1107/S0907444909042073
Souza, P. C. T. et al. Martini 3: a general purpose force field for coarse-grained molecular dynamics. Nat. Methods 18, 382–388 (2021).
pubmed: 33782607
doi: 10.1038/s41592-021-01098-3
de Jong, D. H. et al. Improved parameters for the Martini coarse-grained protein force field. J. Chem. Theory Comput. 9, 687–697 (2013).
pubmed: 26589065
doi: 10.1021/ct300646g
Wassenaar, T. A., Ingolfsson, H. I., Bockmann, R. A., Tieleman, D. P. & Marrink, S. J. Computational lipidomics with insane: a versatile tool for generating custom membranes for molecular simulations. J. Chem. Theory Comput. 11, 2144–2155 (2015).
pubmed: 26574417
doi: 10.1021/acs.jctc.5b00209
Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101 (2007).
pubmed: 17212484
doi: 10.1063/1.2408420
Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A. & Haak, J. R. Molecular-dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684–3690 (1984).
doi: 10.1063/1.448118
Parrinello, M. & Rahman, A. Polymorphic transitions in single-crystals—a new molecular-dynamics method. J. Appl. Phys. 52, 7182–7190 (1981).
doi: 10.1063/1.328693
Tironi, I. G., Sperb, R., Smith, P. E. & Vangunsteren, W. F. A generalized reaction field method for molecular-dynamics simulations. J. Chem. Phys. 102, 5451–5459 (1995).
doi: 10.1063/1.469273
Grubmuller, H., Heller, H., Windemuth, A. & Schulten, K. Generalized Verlet algorithm for efficient molecular dynamics simulations with long-range interactions. Mol. Simul. 6, 121–142 (1991).
doi: 10.1080/08927029108022142
Abraham, M. J. et al. GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2, 19–25 (2015).
doi: 10.1016/j.softx.2015.06.001
Goddard, T. D. et al. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci. 27, 14–25 (2018).
pubmed: 28710774
doi: 10.1002/pro.3235
Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graphics 14, 33–38 (1996).
doi: 10.1016/0263-7855(96)00018-5
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2