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Research journey of respirasome |
Meng Wu1, Jinke Gu1, Shuai Zong1, Runyu Guo1, Tianya Liu1, Maojun Yang1,2( ) |
1. Ministry of Education Key Laboratory of Protein Science, Tsinghua-Peking Joint Center for Life Sciences, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, China 2. School of Pharmacy, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China |
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Abstract Respirasome, as a vital part of the oxidative phosphorylation system, undertakes the task of transferring electrons from the electron donors to oxygen and produces a proton concentration gradient across the inner mitochondrial membrane through the coupled translocation of protons. Copious research has been carried out on this lynchpin of respiration. From the discovery of individual respiratory complexes to the report of the high-resolution structure of mammalian respiratory supercomplex I1III2IV1, scientists have gradually uncovered the mysterious veil of the electron transport chain (ETC). With the discovery of the mammalian respiratory mega complex I2III2IV2, a new perspective emerges in the research field of the ETC. Behind these advances glitters the light of the revolution in both theory and technology. Here, we give a short review about how scientists ‘see’ the structure and the mechanism of respirasome from the macroscopic scale to the atomic scale during the past decades.
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| Keywords
electron transport chain
supercomplex organization
cellular respiration
structure of respirasome
cryo-EM
megacomplex
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Corresponding Author(s):
Maojun Yang
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Issue Date: 02 June 2020
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|
| 1 |
R, Acin-Perez MP Bayona-Bafaluy, P Fernandez-Silva, R Moreno-Loshuertos, A, Perez-Martos C, Bruno CT Moraes, JA Enriquez (2004) Respiratory complex III is required to maintain complex I in mammalian mitochondria. Mol Cell 13:805–815
https://doi.org/10.1016/S1097-2765(04)00124-8
|
| 2 |
R Acin-Perez, P Fernandez-Silva, ML Peleato, A Perez-Martos, JA Enriquez (2008) Respiratory active mitochondrial supercomplexes. Mol Cell 32:529–539
https://doi.org/10.1016/j.molcel.2008.10.021
|
| 3 |
PS Adiga, R Malladi, W Baxter, RM Glaeser (2004) A binary segmentation approach for boxing ribosome particles in cryo EM micrographs. J Struct Biol 145:142–151
https://doi.org/10.1016/j.jsb.2003.10.026
|
| 4 |
M Adrian, J Dubochet, J Lepault, AW McDowall (1984) Cryo-electron microscopy of viruses. Nature 308:32–36
https://doi.org/10.1038/308032a0
|
| 5 |
A-NA Agip, JN Blaza, HR Bridges, C Viscomi, S Rawson, SP Muench, J Hirst (2018) Cryo-EM structures of complex I from mouse heart mitochondria in two biochemically defined states. Nat Struct Mol Biol 25:548–556
https://doi.org/10.1038/s41594-018-0073-1
|
| 6 |
AA Agip, JN Blaza, JG Fedor, J Hirst(2019) Mammalian respiratory complex I through the lens of cryo-EM. Annu Rev Biophys 48:165–184
https://doi.org/10.1146/annurev-biophys-052118-115704
|
| 7 |
A Al-Azzawi, A Ouadou, JJ Tanner, J Cheng (2019a) AutoCryo-Picker: an unsupervised learning approach for fully automated single particle picking in Cryo-EM images. BMC Bioinform 20:326
https://doi.org/10.1186/s12859-019-2926-y
|
| 8 |
A Al-Azzawi, A Ouadou, JJ Tanner, J Cheng (2019b) A superclustering approach for fully automated single particle picking in Cryo-EM. Genes (Basel).
https://doi.org/10.3390/genes10090666
|
| 9 |
M Alcázar-Fabra, P Navas, G Brea-Calvo (2016) Coenzyme Q biosynthesis and its role in the respiratory chain structure. Biochim Biophys Acta (BBA) 1857:1073–1078
https://doi.org/10.1016/j.bbabio.2016.03.010
|
| 10 |
RD Allen, CC Schroeder, AK Fok (1989) An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J Cell Biol 108:2233–2240
https://doi.org/10.1083/jcb.108.6.2233
|
| 11 |
T Althoff, DJ Mills, JL Popot, W Kuhlbrandt (2011) Arrangement of electron transport chain components in bovine mitochondrial supercomplex I1III2IV1. EMBO J 30:4652–4664
https://doi.org/10.1038/emboj.2011.324
|
| 12 |
XC Bai, IS Fernandez, G McMullan, SH Scheres (2013) Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. Elife 2:e00461
https://doi.org/10.7554/eLife.00461.011
|
| 13 |
XC Bai, G McMullan, SH Scheres (2015) How cryo-EM is revolutionizing structural biology. Trends Biochem Sci 40:49–57
https://doi.org/10.1016/j.tibs.2014.10.005
|
| 14 |
E Balsa, R Marco, E Perales-Clemente, R Szklarczyk, E Calvo, MO Landazuri, JA Enriquez (2012) NDUFA4 is a subunit of complex IV of the mammalian electron transport chain. Cell Metab 16:378–386
https://doi.org/10.1016/j.cmet.2012.07.015
|
| 15 |
B Barquera (2014) The sodium pumping NADH:quinone oxidoreductase (Na(+)-NQR), a unique redox-driven ion pump. J Bioenerg Biomembr 46:289–298
https://doi.org/10.1007/s10863-014-9565-9
|
| 16 |
MGD Bates, JP Bourke, C Giordano, G d’Amati, DM Turnbull, RW Taylor (2012) Cardiac involvement in mitochondrial DNA disease: clinical spectrum, diagnosis, and management. Eur Heart J 33:3023–3033
https://doi.org/10.1093/eurheartj/ehs275
|
| 17 |
M Bentinger, M Tekle, G Dallner (2010) Coenzyme Q—biosynthesis and functions. Biochem Biophys Res Commun 396:74–79
https://doi.org/10.1016/j.bbrc.2010.02.147
|
| 18 |
A Bezawork-Geleta, J Rohlena, L Dong, K Pacak, J Neuzil (2017) Mitochondrial complex II: at the crossroads. Trends Biochem Sci 42:312–325
https://doi.org/10.1016/j.tibs.2017.01.003
|
| 19 |
GA Biagini, N Fisher, AE Shone, MA Mubaraki, A Srivastava, A Hill, T Antoine, AJ Warman, J Davies, C Pidathalaet al. (2012) Generation of quinolone antimalarials targeting the Plasmodium falciparum mitochondrial respiratory chain for the treatment and prophylaxis of malaria. Proc Natl Acad Sci USA 109:8298–8303
https://doi.org/10.1073/pnas.1205651109
|
| 20 |
C Bianchi, ML Genova, G Parenti Castelli, G Lenaz (2004) The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis. J Biol Chem 279:36562–36569
https://doi.org/10.1074/jbc.M405135200
|
| 21 |
PV Blair (1967) Preparation and properties of repeating units of mitochondrial electron transfer. Methods Enzymol 10:208–212
https://doi.org/10.1016/0076-6879(67)10041-4
|
| 22 |
JN Blaza, R Serreli, AJ Jones, K Mohammed, J Hirst (2014) Kinetic evidence against partitioning of the ubiquinone pool and the catalytic relevance of respiratory-chain supercomplexes. Proc Natl Acad Sci USA 111:15735–15740
https://doi.org/10.1073/pnas.1413855111
|
| 23 |
JN Blaza, KR Vinothkumar, J Hirst (2018) Structure of the deactive state of mammalian respiratory complex I. Structure 26:312–319. e313
https://doi.org/10.1016/j.str.2017.12.014
|
| 24 |
E Bottani, R Cerutti, ME Harbour, S Ravaglia, SA Dogan, C Giordano, IM Fearnley, G D’Amati, C Viscomi, E Fernandez-Vizarraet al. (2017) TTC19 plays a husbandry role on UQCRFS1 turnover in the biogenesis of mitochondrial respiratory complex III. Mol Cell 67:96–105.e104
https://doi.org/10.1016/j.molcel.2017.06.001
|
| 25 |
U Brandt (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75:69–92
https://doi.org/10.1146/annurev.biochem.75.103004.142539
|
| 26 |
U Brandt (2011) A two-state stabilization-change mechanism for proton-pumping complex I. Biochim Biophys Acta 1807:1364–1369
https://doi.org/10.1016/j.bbabio.2011.04.006
|
| 27 |
AF Brilot, JZ Chen, A Cheng, J Pan, SC Harrison, CS Potter, B Carragher, R Henderson, N Grigorieff (2012) Beam-induced motion of vitrified specimen on holey carbon film. J Struct Biol 177:630–637
https://doi.org/10.1016/j.jsb.2012.02.003
|
| 28 |
P Brzezinski, P Adelroth (1998) Pathways of proton transfer in cytochrome c oxidase. J Bioenerg Biomembr 30:99–107
https://doi.org/10.1023/A:1020567729941
|
| 29 |
JB Bultema, HP Braun, EJ Boekema, R Kouril (2009) Megacomplex organization of the oxidative phosphorylation system by structural analysis of respiratory supercomplexes from potato. Biochim Biophys Acta 1787:60–67
https://doi.org/10.1016/j.bbabio.2008.10.010
|
| 30 |
G Cecchini (2003) Function and structure of complex II of the respiratory chain. Annu Rev Biochem 72:77–109
https://doi.org/10.1146/annurev.biochem.72.121801.161700
|
| 31 |
B Chance, RW Estabrook, CP Lee (1963) Electron transport in the oxysome. Science 140:379–380
https://doi.org/10.1126/science.140.3565.379-c
|
| 32 |
B Chance, GR Williams (1955) A method for the localization of sites for oxidative phosphorylation. Nature 176:250
https://doi.org/10.1038/176250a0
|
| 33 |
Y Cheng (2015) Single-particle cryo-EM at crystallographic resolution. Cell 161:450–457
https://doi.org/10.1016/j.cell.2015.03.049
|
| 34 |
S Cogliati, E Calvo, M Loureiro, AM Guaras, R Nieto-Arellano, C Garcia-Poyatos, I Ezkurdia, N Mercader, J Vazquez, JA Enriquez (2016) Mechanism of super-assembly of respiratory complexes III and IV. Nature 539:579–582
https://doi.org/10.1038/nature20157
|
| 35 |
FL Crane, Y Hatefi, RL Lester, C Widmer (1957) Isolation of a quinone from beef heart mitochondria. Biochim Biophys Acta 25:220–221
https://doi.org/10.1016/0006-3002(57)90457-2
|
| 36 |
AR Crofts, SW Meinhardt, KR Jones, M Snozzi (1983) The role of the quinone pool in the cyclic electron-transfer chain of rhodopseudomonas sphaeroides: a modified Q-cycle mechanism. Biochim Biophys Acta 723:202–218
https://doi.org/10.1016/0005-2728(83)90120-2
|
| 37 |
KM Davies, TB Blum, W Kuhlbrandt (2018) Conserved in situ arrangement of complex I and III2 in mitochondrial respiratory chain supercomplexes of mammals, yeast, and plants. Proc Natl Acad Sci USA 115:3024–3029
https://doi.org/10.1073/pnas.1720702115
|
| 38 |
KM Davies, M Strauss, B Daum, JH Kief, HD Osiewacz, A Rycovska, V Zickermann, W Kuhlbrandt (2011) Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc Natl Acad Sci USA 108:14121–14126
https://doi.org/10.1073/pnas.1103621108
|
| 39 |
DJ De Rosier, A Klug (1968) Reconstruction of three dimensional structures from electron micrographs. Nature 217:130–134
https://doi.org/10.1038/217130a0
|
| 40 |
J Dubochet, M Adrian, JJ Chang, JC Homo, J Lepault, AW McDowall, P Schultz (1988) Cryo-electron microscopy of vitrified specimens. Q Rev Biophys 21:129–228
https://doi.org/10.1017/S0033583500004297
|
| 41 |
J Dubochet, FP Booy, R Freeman, AV Jones, CA Walter (1981) Low temperature electron microscopy. Annu Rev Biophys Bioeng 10:133–149
https://doi.org/10.1146/annurev.bb.10.060181.001025
|
| 42 |
MR Duchen, G Szabadkai (2010) Roles of mitochondria in human disease. Essays Biochem 47:115–137
https://doi.org/10.1042/bse0470115
|
| 43 |
NV Dudkina, M Kudryashev, H Stahlberg, EJ Boekema(2011) Interaction of complexes I, III, and IV within the bovine respirasome by single particle cryoelectron tomography. Proc Natl Acad Sci USA 108:15196–15200
https://doi.org/10.1073/pnas.1107819108
|
| 44 |
RG Efremov, LA Sazanov (2012) The coupling mechanism of respiratory complex I- a structural and evolutionary perspective . Biochim Biophys Acta 1817:1785– 1795
https://doi.org/10.1016/j.bbabio.2012.02.015
|
| 45 |
JA Enríquez (2016) Supramolecular organization of respiratory complexes. Annu Rev Physiol 78:533–561
https://doi.org/10.1146/annurev-physiol-021115-105031
|
| 46 |
H, Eubel J, Heinemeyer S Sunderhaus, HP Braun (2004) Respiratory chain supercomplexes in plant mitochondria. Plant Physiol Biochem 42:937–942
https://doi.org/10.1016/j.plaphy.2004.09.010
|
| 47 |
DR Evans, HI Guy (2004) Mammalian pyrimidine biosynthesis: fresh insights into an ancient pathway. J Biol Chem 279:33035–33038
https://doi.org/10.1074/jbc.R400007200
|
| 48 |
X Fan, J Wang, X Zhang, Z Yang, JC Zhang, L Zhao, HL Peng, J Lei, HW Wang (2019) Single particle cryo-EM reconstruction of 52 kDa streptavidin at 3.2 Angstrom resolution. Nat Commun 10:2386
https://doi.org/10.1038/s41467-019-10368-w
|
| 49 |
JG Fedor, J Hirst (2018) Mitochondrial supercomplexes do not enhance catalysis by quinone channeling. Cell Metab 28:525–531.e524
https://doi.org/10.1016/j.cmet.2018.05.024
|
| 50 |
X Feng, Z, Fu S Kaledhonkar, Y Jia, B Shah, A Jin, Z Liu, M Sun, B Chen, RA Grassucciet al. (2017) A fast and effective microfluidic spraying-plunging method for high-resolution singleparticle cryo-EM. Structure 25:663–670.e663
https://doi.org/10.1016/j.str.2017.02.005
|
| 51 |
Y Feng, WF Li, J, Li JW Wang, JP Ge, D Xu, YJ Liu, KQ Wu, QY Zeng, JW Wuet al. (2012) Structural insight into the type-II mitochondrial NADH dehydrogenases. Nature 491:478–482
https://doi.org/10.1038/nature11541
|
| 52 |
K Fiedorczuk, JA Letts, G Degliesposti, K Kaszuba, M Skehel, LA Sazanov (2016) Atomic structure of the entire mammalian mitochondrial complex I. Nature 538:406
https://doi.org/10.1038/nature19794
|
| 53 |
J Frank (2017a) Advances in the field of single-particle cryo-electron microscopy over the last decade. Nat Protoc 12:209–212
https://doi.org/10.1038/nprot.2017.004
|
| 54 |
J Frank (2017b) Time-resolved cryo-electron microscopy: Recent progress. J Struct Biol 200:303–306
https://doi.org/10.1016/j.jsb.2017.06.005
|
| 55 |
J, Frank B Shimkin, H Dowse (1981) Spider—a modular software system for electron image processing. Ultramicroscopy 6:343–357
https://doi.org/10.1016/S0304-3991(81)80236-7
|
| 56 |
M Frenzel, H Rommelspacher, MD Sugawa, NA Dencher (2010) Ageing alters the supramolecular architecture of OxPhos complexes in rat brain cortex. Exp Gerontol 45:563–572
https://doi.org/10.1016/j.exger.2010.02.003
|
| 57 |
T Friedrich (2014) On the mechanism of respiratory complex I. J Bioenerg Biomembr 46:255–268
https://doi.org/10.1007/s10863-014-9566-8
|
| 58 |
Z Fu, S Kaledhonkar, A Borg, M Sun, B Chen, RA Grassucci, M Ehrenberg, J Frank (2016) Key intermediates in ribosome recycling visualized by time-resolved cryoelectron microscopy. Structure 24:2092–2101
https://doi.org/10.1016/j.str.2016.09.014
|
| 59 |
ML Genova, G Lenaz (2011) New developments on the functions of coenzyme Q in mitochondria. BioFactors 37:330–354
https://doi.org/10.1002/biof.168
|
| 60 |
ML Genova, G Lenaz (2014) Functional role of mitochondrial respiratory supercomplexes. Biochim Biophys Acta 1837:427–443
https://doi.org/10.1016/j.bbabio.2013.11.002
|
| 61 |
LA Gomez, JS Monette, JD Chavez, CS Maier, TM Hagen (2009) Supercomplexes of the mitochondrial electron transport chain decline in the aging rat heart. Arch Biochem Biophys 490:30–35
https://doi.org/10.1016/j.abb.2009.08.002
|
| 62 |
H Gong, J Li, A Xu, Y Tang, W Ji, R Gao, S Wang, L Yu, C Tian, J Liet al. (2018) An electron transfer path connects subunits of a mycobacterial respiratory supercomplex. Science.
https://doi.org/10.1126/science.aat8923
|
| 63 |
DE Green, A Tzagoloff (1966) The mitochondrial electron transfer chain. Arch Biochem Biophys 116:293–304
https://doi.org/10.1016/0003-9861(66)90036-1
|
| 64 |
C Greggio, P Jha, SS Kulkarni, S Lagarrigue, NT Broskey, M Boutant, X, Wang S Conde Alonso, E Ofori, J Auwerxet al. (2017) Enhanced respiratory chain supercomplex formation in response to exercise in human skeletal muscle. Cell Metab 25:301–311
https://doi.org/10.1016/j.cmet.2016.11.004
|
| 65 |
N Grigorieff (1998) Three-dimensional structure of bovine NADH: ubiquinone oxidoreductase (complex I) at 22 A in ice. J Mol Biol 277:1033–1046
https://doi.org/10.1006/jmbi.1998.1668
|
| 66 |
J Gu, M, Wu R, Guo K Yan, J Lei, N Gao, M Yang (2016) The architecture of the mammalian respirasome. Nature 537:639
https://doi.org/10.1038/nature19359
|
| 67 |
J Gu, L Zhang, S Zong, R Guo, T Liu, J, Yi P Wang, W Zhuo, M Yang (2019) Cryo-EM structure of the mammalian ATP synthase tetramer bound with inhibitory protein IF1. Science 364:1068–1075
https://doi.org/10.1126/science.aaw4852
|
| 68 |
R Guo, J Gu, S Zong, M Wu, M Yang (2018) Structure and mechanism of mitochondrial electron transport chain. Biomed J 41:9–20
https://doi.org/10.1016/j.bj.2017.12.001
|
| 69 |
R Guo, S Zong, M Wu, J Gu, M Yang (2017) Architecture of human mitochondrial respiratory megacomplex I2III2IV2. Cell 170:1247–1257.e1212
https://doi.org/10.1016/j.cell.2017.07.050
|
| 70 |
SS Gupte, CR Hackenbrock (1988) The role of cytochrome c diffusion in mitochondrial electron transport. J Biol Chem 263:5248–5253
|
| 71 |
CR Hackenbrock (1977) Molecular organization and the fluid nature of the mitochondrial energy transducing membrane. In: Abrahamsson S, Pascher I (eds) Structure of biological membranes. Springer, Boston, MA,pp 199–234
https://doi.org/10.1007/978-1-4684-8127-3_12
|
| 72 |
JW Jr Harding, EA Pyeritz, ES Copeland, HB 3rd White (1975) Role of glycerol 3-phosphate dehydrogenase in glyceride metabolism. Effect of diet on enzyme activities in chicken liver. Biochemical Journal 146:223–229
https://doi.org/10.1042/bj1460223
|
| 73 |
AM Hartley, N Lukoyanova, Y Zhang, A Cabrera-Orefice, S Arnold, B Meunier, N Pinotsis, A Marechal (2019) Structure of yeast cytochrome c oxidase in a supercomplex with cytochrome bc1. Nat Struct Mol Biol 26:78–83
https://doi.org/10.1038/s41594-018-0172-z
|
| 74 |
Y Hatefi (1985) The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 54:1015–1069
https://doi.org/10.1146/annurev.bi.54.070185.005055
|
| 75 |
Y Hatefi, AG Haavik, LR Fowler, DE Griffiths (1962) Studies on the electron transfer system. XLII. Reconstitution of the electron transfer system. J Biol Chem 237:2661–2669
|
| 76 |
SB Hayward, RM Glaeser (1979) Radiation damage of purple membrane at low temperature. Ultramicroscopy 04:201–210
https://doi.org/10.1016/S0304-3991(79)90211-0
|
| 77 |
R Henderson, JM Baldwin, TA Ceska, F Zemlin, E Beckmann, KH Downing (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol 213:899–929
https://doi.org/10.1016/S0022-2836(05)80271-2
|
| 78 |
R Henderson, PN Unwin (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257:28–32
https://doi.org/10.1038/257028a0
|
| 79 |
C Heron, CI Ragan, BL Trumpower (1978) The interaction between mitochondrial NADH-ubiquinone oxidoreductase and ubiquinolcytochrome c oxidoreductase. Restoration of ubiquinone-pool behaviour. Biochem J 174:791–800
https://doi.org/10.1042/bj1740791
|
| 80 |
R Hill, D Keilin (1930) The porphyrin of component c of cytochrome and its relationship to other porphyrins. Proc R Soc Lond B Biol Sci 107:286–292
https://doi.org/10.1098/rspb.1930.0071
|
| 81 |
J Hirst (2013) Mitochondrial complex I. Annu Rev Biochem 82:551–575
https://doi.org/10.1146/annurev-biochem-070511-103700
|
| 82 |
J Hirst (2018) Open questions: respiratory chain supercomplexes—why are they there and what do they do? BMC Biol 16:111
https://doi.org/10.1186/s12915-018-0577-5
|
| 83 |
M Hochli, CR Hackenbrock (1976) Fluidity in mitochondrial membranes: thermotropic lateral translational motion of intramembrane particles. Proc Natl Acad Sci USA 73:1636–1640
https://doi.org/10.1073/pnas.73.5.1636
|
| 84 |
M Hochli, L Hochli, CR Hackenbrock (1985) Independent lateral diffusion of cytochrome bc1 complex and cytochrome oxidase in the mitochondrial inner membrane. Eur J Cell Biol 38:1–5
|
| 85 |
G Hofhaus, H Weiss, K Leonard (1991) Electron microscopic analysis of the peripheral and membrane parts of mitochondrial NADH dehydrogenase (complex I) . J Mol Biol 221:1027–1043
https://doi.org/10.1016/0022-2836(91)80190-6
|
| 86 |
AD Hofmann, M Beyer, U Krause-Buchholz, M Wobus, M Bornhauser, G Rodel (2012) OXPHOS supercomplexes as a hallmark of the mitochondrial phenotype of adipogenic differentiated human MSCs. PLoS ONE 7:e35160
https://doi.org/10.1371/journal.pone.0035160
|
| 87 |
M Hu, H Yu, K Gu, Z Wang, H, Ruan K Wang, S Ren, B Li, L Gan, S Xuet al. (2018) A particle-filter framework for robust cryo-EM 3D reconstruction. Nat Methods 15:1083–1089
https://doi.org/10.1038/s41592-018-0223-8
|
| 88 |
C Hunte, V Zickermann, U Brandt (2010) Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science 329:448–451
https://doi.org/10.1126/science.1191046
|
| 89 |
K Ikeda, S Shiba, K Horie-Inoue, K Shimokata, S Inoue (2013) A stabilizing factor for mitochondrial respiratory supercomplex assembly regulates energy metabolism in muscle. Nat Commun 4:2147
https://doi.org/10.1038/ncomms3147
|
| 90 |
TM Iverson, C, Luna-Chavez G Cecchini, DC Rees (1999) Structure of the Escherichia coli fumarate reductase respiratory complex. Science 284:1961–1966
https://doi.org/10.1126/science.284.5422.1961
|
| 91 |
S Iwata, JW Lee, K Okada, JK Lee, M Iwata, B Rasmussen, TA Link, S Ramaswamy, BK Jap (1998) Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281:64–71
https://doi.org/10.1126/science.281.5373.64
|
| 92 |
S Iwata, C Ostermeier, B Ludwig, H Michel (1995) Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376:660–669
https://doi.org/10.1038/376660a0
|
| 93 |
B Kadenbach (2017) Regulation of mammalian 13-subunit cytochrome c oxidase and binding of other proteins: role of NDUFA4. Trends Endocrinol Metab 28:761–770
https://doi.org/10.1016/j.tem.2017.09.003
|
| 94 |
HM Kalckar (1974) Origins of the concept oxidative phosphorylation. Mol Cell Biochem 5:55–62
https://doi.org/10.1007/BF01874172
|
| 95 |
HM Kalckar (1991) 50 years of biological research—from oxidative phosphorylation to energy requiring transport regulation. Annu Rev Biochem 60:1–38
https://doi.org/10.1146/annurev.bi.60.070191.000245
|
| 96 |
D Keilin, EF Hartree (1947) Activity of the cytochrome system in heart muscle preparations. Biochem J 41:500–502
https://doi.org/10.1042/bj0410500
|
| 97 |
S Kerscher, S Drose, V Zickermann, U Brandt (2008) The three families of respiratory NADH dehydrogenases. Results Probl Cell Differ 45:185–222
https://doi.org/10.1007/400_2007_028
|
| 98 |
SJ Kerscher (2000) Diversity and origin of alternative NADH: ubiquinone oxidoreductases. Biochim Biophys Acta 1459:274–283
https://doi.org/10.1016/S0005-2728(00)00162-6
|
| 99 |
AA Konstantinov, S Siletsky, D Mitchell, A Kaulen, RB Gennis (1997) The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directed mutations on time-resolved electrogenic intraprotein proton transfer. Proc Natl Acad Sci USA 94:9085–9090
https://doi.org/10.1073/pnas.94.17.9085
|
| 100 |
F Krause (2006) Detection and analysis of protein-protein interactions in organellar and prokaryotic proteomes by native gel electrophoresis: (Membrane) protein complexes and supercomplexes. Electrophoresis 27:2759–2781
https://doi.org/10.1002/elps.200600049
|
| 101 |
F Krause, NH Reifschneider, D Vocke, H Seelert, S Rexroth, NA Dencher (2004a) “Respirasome”-like supercomplexes in green leaf mitochondria of spinach. J Biol Chem 279:48369–48375
https://doi.org/10.1074/jbc.M406085200
|
| 102 |
F Krause, CQ Scheckhuber, A Werner, S Rexroth, NH Reifschneider, NA Dencher, HD Osiewacz (2004b) Supramolecular organization of cytochrome c oxidase- and alternative oxidasedependent respiratory chains in the filamentous fungus Podospora anserina. J Biol Chem 279:26453–26461
https://doi.org/10.1074/jbc.M402756200
|
| 103 |
A Kroger, M Klingenberg (1973) The kinetics of the redox reactions of ubiquinone related to the electron-transport activity in the respiratory chain. Eur J Biochem 34:358–368
https://doi.org/10.1111/j.1432-1033.1973.tb02767.x
|
| 104 |
M Kuijper, G van Hoften, B Janssen, R, Geurink S De Carlo, M Vos, G, van Duinen B van Haeringen, M Storms (2015) FEI’s direct electron detector developments: embarking on a revolution in cryo-TEM. J Struct Biol 192:179–187
https://doi.org/10.1016/j.jsb.2015.09.014
|
| 105 |
E Lamantea, F, Carrara C Mariotti, L Morandi, V Tiranti, M Zeviani (2002) A novel nonsense mutation (Q352X) in the mitochondrial cytochrome b gene associated with a combined deficiency of complexes I and III. Neuromuscul Disord 12:49–52
https://doi.org/10.1016/S0960-8966(01)00244-9
|
| 106 |
R Langlois, J Pallesen, JT Ash, Ho D Nam, JL Rubinstein, J Frank (2014) Automated particle picking for low-contrast macromolecules in cryo-electron microscopy. J Struct Biol 186:1–7
https://doi.org/10.1016/j.jsb.2014.03.001
|
| 107 |
E Lapuente-Brun, R Moreno-Loshuertos, R Acin-Perez, A Latorre-Pellicer, C, Colas E Balsa, E Perales-Clemente, PM Quiros, E Calvo, MA Rodriguez-Hernandezet al. (2013) Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340:1567–1570
https://doi.org/10.1126/science.1230381
|
| 108 |
NZ Lax, DM Turnbull, AK Reeve (2011) Mitochondrial mutations: newly discovered players in neuronal degeneration. Neuroscientist 17:645–658
https://doi.org/10.1177/1073858410385469
|
| 109 |
KE Leigh, PP Navarro, S Scaramuzza, W Chen, Y Zhang, D Castano-Diez, M Kudryashev (2019) Subtomogram averaging from cryo-electron tomograms. Methods Cell Biol 152:217–259
https://doi.org/10.1016/bs.mcb.2019.04.003
|
| 110 |
G Lenaz, ML Genova (2007) Kinetics of integrated electron transfer in the mitochondrial respiratory chain: random collisions vs. solid state electron channeling. Am J Physiol Cell Physiol 292:C1221–1239
https://doi.org/10.1152/ajpcell.00263.2006
|
| 111 |
G Lenaz, ML Genova (2012) Supramolecular organisation of the mitochondrial respiratory chain: a new challenge for the mechanism and control of oxidative phosphorylation. Adv Exp Med Biol 748:107–144
https://doi.org/10.1007/978-1-4614-3573-0_5
|
| 112 |
G, Lenaz G, Tioli AI Falasca, ML Genova (2016) Complex I function in mitochondrial supercomplexes. Biochim Biophys Acta 1857:991–1000
https://doi.org/10.1016/j.bbabio.2016.01.013
|
| 113 |
K Leonard, H Haiker, H Weiss (1987) Three-dimensional structure of NADH: ubiquinone reductase (complex I) from Neurospora mitochondria determined by electron microscopy of membrane crystals. J Mol Biol 194:277–286
https://doi.org/10.1016/0022-2836(87)90375-5
|
| 114 |
J Lepault, J Dubochet, W Baschong, E Kellenberger (1987) Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. EMBO J 6:1507–1512
https://doi.org/10.1002/j.1460-2075.1987.tb02393.x
|
| 115 |
JA Letts, K Fiedorczuk, G Degliesposti, M Skehel, LA Sazanov (2019) Structures of respiratory supercomplex I+III2 reveal functional and conformational crosstalk. Mol Cell 75:1131–1146
https://doi.org/10.1016/j.molcel.2019.07.022
|
| 116 |
JA Letts, K Fiedorczuk, LA Sazanov (2016) The architecture of respiratory supercomplexes. Nature 537:644–648
https://doi.org/10.1038/nature19774
|
| 117 |
JA Letts, LA Sazanov (2017) Clarifying the supercomplex: the higher-order organization of the mitochondrial electron transport chain. Nat Struct Mol Biol 24:800–808
https://doi.org/10.1038/nsmb.3460
|
| 118 |
X Li, P Mooney, S Zheng, CR Booth, MB Braunfeld, S Gubbens, DA Agard, Y Cheng (2013) Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Methods 10:584–590
https://doi.org/10.1038/nmeth.2472
|
| 119 |
M Liao, E Cao, D Julius, Y Cheng (2013) Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504:107–112
https://doi.org/10.1038/nature12822
|
| 120 |
Y-A Lim, V Rhein, G Baysang, F Meier, AJ Poljak, M Raftery, M Guilhaus, LM Ittner, A Eckert, J Götz (2010) Aβ and human amylin share a common toxicity pathway via mitochondrial dysfunction. Proteomics 10:1621–1633
https://doi.org/10.1002/pmic.200900651
|
| 121 |
T Lobo-Jarne, C Ugalde (2018) Respiratory chain supercomplexes: structures, function and biogenesis. Semin Cell Dev Biol 76:179–190
https://doi.org/10.1016/j.semcdb.2017.07.021
|
| 122 |
F Luo, X Gui, H Zhou, J Gu, Y Li, X Liu, M Zhao, D Li, X Li, C Liu (2018) Atomic structures of FUS LC domain segments reveal bases for reversible amyloid fibril formation. Nat Struct Mol Biol 25:341–346
https://doi.org/10.1038/s41594-018-0050-8
|
| 123 |
E Maranzana, G Barbero, AI Falasca, G Lenaz, ML Genova (2013) Mitochondrial respiratory supercomplex association limits production of reactive oxygen species from complex I. Antioxid Redox Signal 19:1469–1480
https://doi.org/10.1089/ars.2012.4845
|
| 124 |
I, Marques NA Dencher, A Videira, F Krause (2007) Supramolecular organization of the respiratory chain in Neurospora crassamitochondria. Eukaryot Cell 6:2391–2405
https://doi.org/10.1128/EC.00149-07
|
| 125 |
G McMullan, AR Faruqi, D Clare, R Henderson (2014) Comparison of optimal performance at 300 keV of three direct electron detectors for use in low dose electron microscopy. Ultramicroscopy 147:156–163
https://doi.org/10.1016/j.ultramic.2014.08.002
|
| 126 |
G McMullan, AR Faruqi, R Henderson (2016) Direct electron detectors. Methods Enzymol 579:1–17
https://doi.org/10.1016/bs.mie.2016.05.056
|
| 127 |
AM Melo, TM Bandeiras, M Teixeira (2004) New insights into type II NAD(P)H: quinone oxidoreductases. Microbiol Mol Biol Rev 68:603–616
https://doi.org/10.1128/MMBR.68.4.603-616.2004
|
| 128 |
A Merk, A Bartesaghi, S Banerjee, V Falconieri, P Rao, MI Davis, R Pragani, MB Boxer, LA Earl, JLS Milneet al. (2016) Breaking cryo-EM resolution barriers to facilitate drug discovery. Cell 165:1698–1707
https://doi.org/10.1016/j.cell.2016.05.040
|
| 129 |
D Milenkovic, JN Blaza, N-G Larsson, J Hirst (2017) The enigma of the respiratory chain supercomplex. Cell Metab 25:765–776
https://doi.org/10.1016/j.cmet.2017.03.009
|
| 130 |
E Mileykovskaya, PA Penczek, J Fang, VK Mallampalli, GC Sparagna, W Dowhan (2012) Arrangement of the respiratory chain complexes in Saccharomyces cerevisiae supercomplex III2IV2 revealed by single particle cryo-electron microscopy. J Biol Chem 287:23095–23103
https://doi.org/10.1074/jbc.M112.367888
|
| 131 |
P Mitchell(1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144
https://doi.org/10.1038/191144a0
|
| 132 |
P Mitchell (1975a) The protonmotive Q cycle: a general formulation. FEBS Lett 59:137–139
https://doi.org/10.1016/0014-5793(75)80359-0
|
| 133 |
P Mitchell (1975b) Protonmotive redox mechanism of the cytochrome b-c1 complex in the respiratory chain: protonmotive ubiquinone cycle. FEBS Lett 56:1–6
https://doi.org/10.1016/0014-5793(75)80098-6
|
| 134 |
P Mitchell (2011) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biochim Biophys Acta (BBA) 1807:1507–1538
https://doi.org/10.1016/j.bbabio.2011.09.018
|
| 135 |
A Mourier, S Matic, B Ruzzenente, NG Larsson, D Milenkovic (2014) The respiratory chain supercomplex organization is independent of COX7a2l isoforms. Cell Metab 20:1069–1075
https://doi.org/10.1016/j.cmet.2014.11.005
|
| 136 |
F Muller, AR Crofts, DM Kramer (2002) Multiple Q-cycle bypass reactions at the Qo site of the cytochrome bc1 complex. Biochemistry 41:7866–7874
https://doi.org/10.1021/bi025581e
|
| 137 |
WV Nicholson, RM Glaeser (2001) Review: automatic particle detection in electron microscopy. J Struct Biol 133:90–101
https://doi.org/10.1006/jsbi.2001.4348
|
| 138 |
E, Nogales SH Scheres (2015) Cryo-EM: a unique tool for the visualization of macromolecular complexity. Mol Cell 58:677–689
https://doi.org/10.1016/j.molcel.2015.02.019
|
| 139 |
E Nubel, I Wittig, S Kerscher, U Brandt, H Schagger (2009) Twodimensional native electrophoretic analysis of respiratory supercomplexes from Yarrowia lipolytica. Proteomics 9:2408–2418
https://doi.org/10.1002/pmic.200800632
|
| 140 |
T Ogura, C Sato (2004) Automatic particle pickup method using a neural network has high accuracy by applying an initial weight derived from eigenimages: a new reference free method for single-particle analysis. J Struct Biol 145:63–75
https://doi.org/10.1016/S1047-8477(03)00139-4
|
| 141 |
T Ohnishi, K Kawaguchi, B Hagihara (1966) Preparation and some properties of yeast mitochondria. J Biol Chem 241:1797–1806
|
| 142 |
T, Ohnishi ST Ohnishi, K Shinzawa-Itoh, S Yoshikawa, RT Weber (2012) EPR detection of two protein-associated ubiquinone components (SQ(Nf) and SQ(Ns)) in the membrane in situ and in proteoliposomes of isolated bovine heart complex I. Biochim Biophys Acta 1817:1803–1809
https://doi.org/10.1016/j.bbabio.2012.03.032
|
| 143 |
Y Osuda, K Shinzawa-Itoh, K Tani, S Maeda, S Yoshikawa, T Tsukihara, C Gerle (2016) Two-dimensional crystallization of monomeric bovine cytochrome c oxidase with bound cytochrome c in reconstituted lipid membranes. Microscopy (Oxf) 65:263–267
https://doi.org/10.1093/jmicro/dfv381
|
| 144 |
A Osyczka, CC Moser, F Daldal, PL Dutton (2004) Reversible redox energy coupling in electron transfer chains. Nature 427:607–612
https://doi.org/10.1038/nature02242
|
| 145 |
A Osyczka, CC Moser, PL Dutton (2005) Fixing the Q cycle. Trends Biochem Sci 30:176–182
https://doi.org/10.1016/j.tibs.2005.02.001
|
| 146 |
S Papa, G Capitanio, F Papa (2018) The mechanism of coupling between oxido-reduction and proton translocation in respiratory chain enzymes. Biol Rev 93:322–349
https://doi.org/10.1111/brv.12347
|
| 147 |
S Papa, PL Martino, G, Capitanio A Gaballo, D De Rasmo, A Signorile, V Petruzzella (2012) The oxidative phosphorylation system in mammalian mitochondria. In: Scatena R, Bottoni P, Giardina B (eds) Advances in mitochondrial medicine. Springer, Dordrecht, pp 3–37
https://doi.org/10.1007/978-94-007-2869-1_1
|
| 148 |
K Parey, U Brandt, H Xie, DJ Mills, K Siegmund, J Vonck, W Kuhlbrandt, V Zickermann (2018) Cryo-EM structure of respiratory complex I at work. Elife 7:e39213
https://doi.org/10.7554/eLife.39213
|
| 149 |
PA Penczek, RA Grassucci, J Frank (1994) The ribosome at improved resolution: new techniques for merging and orientation refinement in 3D cryo-electron microscopy of biological particles. Ultramicroscopy 53:251–270
https://doi.org/10.1016/0304-3991(94)90038-8
|
| 150 |
G Peng, G Fritzsch, V Zickermann, H Schagger, R Mentele, F Lottspeich, M Bostina, M Radermacher, R Huber, KO Stetteret al. (2003) Isolation, characterization and electron microscopic single particle analysis of the NADH:ubiquinone oxidoreductase (complex I) from the hyperthermophilic eubacterium Aquifex aeolicus. Biochemistry 42:3032–3039
https://doi.org/10.1021/bi026876v
|
| 151 |
R Perez-Perez, T Lobo-Jarne, D Milenkovic, A Mourier, A Bratic, A Garcia-Bartolome, E Fernandez-Vizarra, S Cadenas, A Delmiro, I Garcia-Consuegraet al. (2016) COX7A2L is a mitochondrial complex III binding protein that stabilizes the III2+IV supercomplex without affecting respirasome formation. Cell Rep 16:2387–2398
https://doi.org/10.1016/j.celrep.2016.07.081
|
| 152 |
SR Pieczenik, J Neustadt (2007) Mitochondrial dysfunction and molecular pathways of disease. Exp Mol Pathol 83:84–92
https://doi.org/10.1016/j.yexmp.2006.09.008
|
| 153 |
R Pietras, M Sarewicz, A Osyczka (2016) Distinct properties of semiquinone species detected at the ubiquinol oxidation Qo site of cytochrome bc1 and their mechanistic implications. J R Soc Interface.
https://doi.org/10.1098/rsif.2016.0133
|
| 154 |
RDS Pitceathly, J-W Taanman (2018) NDUFA4 (Renamed COXFA4) is a cytochrome-c oxidase subunit. Trends Endocrinol Metab 29:452–454
https://doi.org/10.1016/j.tem.2018.03.009
|
| 155 |
HR Powell (2017) X-ray data processing. Biosci Rep.
https://doi.org/10.1042/BSR20170227
|
| 156 |
A Punjani, JL Rubinstein, DJ Fleet, MA Brubaker (2017) cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat Methods 14:290–296
https://doi.org/10.1038/nmeth.4169
|
| 157 |
M Radermacher, T Ruiz, T Clason, S Benjamin, U Brandt, V Zickermann (2006) The three-dimensional structure of complex I from Yarrowia lipolytica: a highly dynamic enzyme. J Struct Biol 154:269–279
https://doi.org/10.1016/j.jsb.2006.02.011
|
| 158 |
M Radermacher, T Wagenknecht, A Verschoor, J Frank (1987) Three-dimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli . J Microsc 146:113–136
https://doi.org/10.1111/j.1365-2818.1987.tb01333.x
|
| 159 |
CI Ragan, C Heron (1978) The interaction between mitochondrial NADH-ubiquinone oxidoreductase and ubiquinol-cytochrome c oxidoreductase. Evidence for stoicheiometric association. Biochem J 174:783–790
https://doi.org/10.1042/bj1740783
|
| 160 |
SJ Ramirez-Aguilar , M Keuthe, M Rocha, VV Fedyaev, K Kramp, KJ Gupta, AG Rasmusson, WX Schulze, JT van Dongen (2011) The composition of plant mitochondrial supercomplexes changes with oxygen availability. J Biol Chem 286:43045–43053
https://doi.org/10.1074/jbc.M111.252544
|
| 161 |
S Rathore, J Berndtsson, L Marin-Buera, J Conrad, M Carroni, P Brzezinski, M Ott (2019) Cryo-EM structure of the yeast respiratory supercomplex. Nat Struct Mol Biol 26:50–57
https://doi.org/10.1038/s41594-018-0169-7
|
| 162 |
I, Razinkov V Dandey, H, Wei Z Zhang, D Melnekoff, WJ Rice, C Wigge, CS Potter, B Carragher (2016) A new method for vitrifying samples for cryoEM. J Struct Biol 195:190–198
https://doi.org/10.1016/j.jsb.2016.06.001
|
| 163 |
NH Reifschneider, S Goto, H Nakamoto, R Takahashi, M Sugawa, NA Dencher, F Krause (2006) Defining the mitochondrial proteomes from five rat organs in a physiologically significant context using 2D blue-native/SDS-PAGE. J Proteome Res 5:1117–1132
https://doi.org/10.1021/pr0504440
|
| 164 |
AL Robinson (1986) Electron microscope inventors share nobel physics prize. Science 234:821–822
https://doi.org/10.1126/science.234.4778.821
|
| 165 |
JL Rubinstein, MA Brubaker (2015) Alignment of cryo-EM movies of individual particles by optimization of image translations. J Struct Biol 192:188–195
https://doi.org/10.1016/j.jsb.2015.08.007
|
| 166 |
CJ Russo, LA Passmore (2016) Progress towards an optimal specimen support for electron cryomicroscopy. Curr Opin Struct Biol 37:81–89
https://doi.org/10.1016/j.sbi.2015.12.007
|
| 167 |
LA Sazanov (2015) A giant molecular proton pump: structure and mechanism of respiratory complex I. Nat Rev Mol Cell Biol 16:375–388
https://doi.org/10.1038/nrm3997
|
| 168 |
LA Sazanov, R, Baradaran RG Efremov, JM Berrisford, G Minhas (2013) A long road towards the structure of respiratory complex I, a giant molecular proton pump. Biochem Soc Trans 41:1265–1271
https://doi.org/10.1042/BST20130193
|
| 169 |
H Schägger, K Pfeiffer (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19:1777–1783
https://doi.org/10.1093/emboj/19.8.1777
|
| 170 |
E Schafer, NA Dencher, J Vonck, DN Parcej (2007) Threedimensional structure of the respiratory chain supercomplex I1III2IV1 from bovine heart mitochondria. Biochemistry 46:12579–12585
https://doi.org/10.1021/bi700983h
|
| 171 |
E Schafer, H Seelert, NH Reifschneider, F Krause, NA Dencher, J Vonck (2006) Architecture of active mammalian respiratory chain supercomplexes. J Biol Chem 281:15370–15375
https://doi.org/10.1074/jbc.M513525200
|
| 172 |
H Schagger, R de Coo, MF Bauer, S Hofmann, C Godinot, U Brandt (2004) Significance of respirasomes for the assembly/stability of human respiratory chain complex I. J Biol Chem 279:36349–36353
https://doi.org/10.1074/jbc.M404033200
|
| 173 |
H Schagger, K Pfeiffer (2001) The ratio of oxidative phosphorylation complexes I-V in bovine heart mitochondria and the composition of respiratory chain supercomplexes. J Biol Chem 276:37861–37867
|
| 174 |
AHV Schapira (2006) Mitochondrial disease. The Lancet 368:70–82
https://doi.org/10.1016/S0140-6736(06)68970-8
|
| 175 |
C Scharfe, HH-S Lu, JK Neuenburg, EA Allen, G-C Li, T Klopstock, TM Cowan, GM Enns, RW Davis (2009) Mapping Gene Associations in human mitochondria using clinical disease phenotypes. PLoS Comput Biol 5:e1000374
https://doi.org/10.1371/journal.pcbi.1000374
|
| 176 |
SH Scheres (2012a) A Bayesian view on cryo-EM structure determination. J Mol Biol 415:406–418
https://doi.org/10.1016/j.jmb.2011.11.010
|
| 177 |
SH Scheres (2012b) RELION: implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 180:519–530
https://doi.org/10.1016/j.jsb.2012.09.006
|
| 178 |
SH Scheres (2014) Beam-induced motion correction for submegadalton cryo-EM particles. Elife 3:e03665
https://doi.org/10.7554/eLife.03665
|
| 179 |
SH Scheres (2016) Processing of structurally heterogeneous cryo- EM data in RELION. Methods Enzymol 579:125–157
https://doi.org/10.1016/bs.mie.2016.04.012
|
| 180 |
SH Scheres, S Chen (2012) Prevention of overfitting in cryo-EM structure determination. Nat Methods 9:853–854
https://doi.org/10.1038/nmeth.2115
|
| 181 |
FK Schur (2019) Toward high-resolution in situ structural biology with cryo-electron tomography and subtomogram averaging. Curr Opin Struct Biol 58:1–9
https://doi.org/10.1016/j.sbi.2019.03.018
|
| 182 |
TB Sherer, R Betarbet, JT Greenamyre (2002) Environment, mitochondria, and Parkinson’s disease. Neuroscientist 8:192–197
https://doi.org/10.1177/1073858402008003004
|
| 183 |
Y Shi (2014) A glimpse of structural biology through X-ray crystallography. Cell 159:995–1014
https://doi.org/10.1016/j.cell.2014.10.051
|
| 184 |
FJ Sigworth (1998) A maximum-likelihood approach to singleparticle image refinement. J Struct Biol 122:328–339
https://doi.org/10.1006/jsbi.1998.4014
|
| 185 |
JS Sousa, E D’Imprima, J Vonck (2018) Mitochondrial respiratory chain complexes. In: Harris JR, Boekema EJ (eds) Membrane protein complexes: structure and function. Springer, Singapore,pp 167–227
https://doi.org/10.1007/978-981-10-7757-9_7
|
| 186 |
JS Sousa, DJ Mills, J Vonck, W Kuhlbrandt (2016) Functional asymmetry and electron flow in the bovine respirasome. Elife.
https://doi.org/10.7554/eLife.21290
|
| 187 |
J Standfuss (2019) Membrane protein dynamics studied by X-ray lasers- or why only time will tell. Curr Opin Struct Biol 57:63–71
https://doi.org/10.1016/j.sbi.2019.02.001
|
| 188 |
AA Starkov, G Fiskum (2001) Myxothiazol induces H2O2 production from mitochondrial respiratory chain. Biochem Biophys Res Commun 281:645–650
https://doi.org/10.1006/bbrc.2001.4409
|
| 189 |
M Strauss, G Hofhaus, RR Schroder, W Kuhlbrandt (2008) Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J 27:1154–1160
https://doi.org/10.1038/emboj.2008.35
|
| 190 |
V Strecker, Z Wumaier, I Wittig, H Schagger (2010) Large pore gels to separate mega protein complexes larger than 10 MDa by blue native electrophoresis: isolation of putative respiratory strings or patches. Proteomics 10:3379–3387
https://doi.org/10.1002/pmic.201000343
|
| 191 |
A Stroh, O Anderka, K Pfeiffer, T Yagi, M Finel, B Ludwig, H Schagger (2004) Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans. J Biol Chem 279:5000–5007
https://doi.org/10.1074/jbc.M309505200
|
| 192 |
F Sun, X Huo, Y Zhai, A Wang, J Xu, D Su, M Bartlam, Z Rao (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121:1043–1057
https://doi.org/10.1016/j.cell.2005.05.025
|
| 193 |
KA Taylor, RM Glaeser (1974) Electron diffraction of frozen, hydrated protein crystals. Science 186:1036–1037
https://doi.org/10.1126/science.186.4168.1036
|
| 194 |
M Trouillard, B Meunier, F Rappaport (2011) Questioning the functional relevance of mitochondrial supercomplexes by timeresolved analysis of the respiratory chain. Proc Natl Acad Sci USA 108:E1027–1034
https://doi.org/10.1073/pnas.1109510108
|
| 195 |
T Tsukihara, H Aoyama, E Yamashita, T Tomizaki, H Yamaguchi, K Shinzawa-Itoh, R Nakashima, R Yaono, S Yoshikawa (1995) Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 A. Science 269:1069–1074
https://doi.org/10.1126/science.7652554
|
| 196 |
T Tsukihara, H Aoyama, E Yamashita, T Tomizaki, H Yamaguchi, K Shinzawa-Itoh, R Nakashima, R Yaono, S Yoshikawa (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272:1136–1144
https://doi.org/10.1126/science.272.5265.1136
|
| 197 |
B Turonova, FKM Schur, W Wan, JAG Briggs (2017) Efficient 3DCTF correction for cryo-electron tomography using NovaCTF improves subtomogram averaging resolution to 3.4A. J Struct Biol 199:187–195
https://doi.org/10.1016/j.jsb.2017.07.007
|
| 198 |
M van Heel, J Frank (1981) Use of multivariate statistics in analysing the images of biological macromolecules. Ultramicroscopy 6:187–194
https://doi.org/10.1016/0304-3991(81)90059-0
|
| 199 |
M van Heel, W Keegstra (1981) IMAGIC: a fast, flexible and friendly image analysis software system. Ultramicroscopy 7:113–129
https://doi.org/10.1016/0304-3991(81)90001-2
|
| 200 |
R Vartak, CA-M Porras, Y Bai (2013) Respiratory supercomplexes: structure, function and assembly. Protein Cell 4:582–590
https://doi.org/10.1007/s13238-013-3032-y
|
| 201 |
UD Vempati, X Han, CT Moraes (2009) Lack of cytochrome c in mouse fibroblasts disrupts assembly/stability of respiratory complexes I and IV. J Biol Chem 284:4383–4391
https://doi.org/10.1074/jbc.M805972200
|
| 202 |
Z Verner, I Skodova, S Polakova, V Durisova-Benkovicova, A Horvath, J Lukes (2013) Alternative NADH dehydrogenase (NDH2): intermembrane-space-facing counterpart of mitochondrial complex I in the procyclic Trypanosoma brucei. Parasitology 140:328–337
https://doi.org/10.1017/S003118201200162X
|
| 203 |
KR Vinothkumar, J Zhu, J Hirst (2014) Architecture of mammalian respiratory complex I. Nature 515:80
https://doi.org/10.1038/nature13686
|
| 204 |
J Vonck (2012) Supramolecular organization of the respiratory chain
https://doi.org/10.1007/978-94-007-4138-6_12
|
| 205 |
T Wagner, F Merino, M Stabrin, T Moriya, C Antoni, A Apelbaum, P Hagel, O Sitsel, T Raisch, D Prumbaumet al. (2019) SPHIREcrYOLO is a fast and accurate fully automated particle picker for cryo-EM. Commun Biol 2:218
https://doi.org/10.1038/s42003-019-0437-z
|
| 206 |
W Wan, JA Briggs (2016) Cryo-electron tomography and subtomogram averaging. Methods Enzymol 579:329–367
https://doi.org/10.1016/bs.mie.2016.04.014
|
| 207 |
F Wang, H Gong, G Liu, M, Li C Yan, T Xia, X Li, J Zeng (2016) DeepPicker: a deep learning approach for fully automated particle picking in cryo-EM. J Struct Biol 195:325–336
https://doi.org/10.1016/j.jsb.2016.07.006
|
| 208 |
HW Wang, JW Wang (2017) How cryo-electron microscopy and X-ray crystallography complement each other. Protein Sci 26:32–39
https://doi.org/10.1002/pro.3022
|
| 209 |
Y Wang, SXL Zhang, D Gozal (2010) Reactive oxygen species and the brain in sleep apnea. Respir Physiol Neurobiol 174:307–316
https://doi.org/10.1016/j.resp.2010.09.001
|
| 210 |
DC Wharton, A Tzagoloff (1962) Studies on the electron transfer system. J Biol Chem 237:2051–2061
|
| 211 |
HD White, K Thirumurugan, ML Walker, J Trinick (2003) A second generation apparatus for time-resolved electron cryo-microscopy using stepper motors and electrospray. J Struct Biol 144:246–252
https://doi.org/10.1016/j.jsb.2003.09.027
|
| 212 |
M Wikstrom, V Sharma, VR Kaila, JP Hosler, G Hummer (2015) New perspectives on proton pumping in cellular respiration. Chem Rev 115:2196–2221
https://doi.org/10.1021/cr500448t
|
| 213 |
EG Williams, Y Wu, P, Jha S Dubuis, P Blattmann, CA Argmann, SM Houten, T Amariuta, W Wolski, N Zamboniet al. (2016) Systems proteomics of liver mitochondria function. Science 352: aad0189
https://doi.org/10.1126/science.aad0189
|
| 214 |
B Wiseman, RG Nitharwal, O Fedotovskaya, J Schafer, H Guo, Q Kuang, S Benlekbir, D Sjostrand, P Adelroth, JL Rubinsteinet al. (2018) Structure of a functional obligate complex III2IV2 respiratory supercomplex from Mycobacterium smegmatis. Nat Struct Mol Biol 25:1128–1136
https://doi.org/10.1038/s41594-018-0160-3
|
| 215 |
I Wittig, HP Braun, H Schagger (2006a) Blue native PAGE. Nat Protoc 1:418–428
https://doi.org/10.1038/nprot.2006.62
|
| 216 |
I Wittig, R Carrozzo, FM Santorelli, H Schagger (2006b) Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim Biophys Acta 1757:1066–1072
https://doi.org/10.1016/j.bbabio.2006.05.006
|
| 217 |
I Wittig, H Schagger (2009) Supramolecular organization of ATP synthase and respiratory chain in mitochondrial membranes. Biochim Biophys Acta 1787:672–680
https://doi.org/10.1016/j.bbabio.2008.12.016
|
| 218 |
HC Wong, J, Chen F Mouche, I Rouiller, M Bern (2004) Model-based particle picking for cryo-electron microscopy. J Struct Biol 145:157–167
https://doi.org/10.1016/j.jsb.2003.05.001
|
| 219 |
JJ Wright, E Salvadori, HR Bridges, J Hirst, MM Roessler (2016) Small-volume potentiometric titrations: EPR investigations of Fe-S cluster N2 in mitochondrial complex I. J Inorg Biochem 162:201–206
https://doi.org/10.1016/j.jinorgbio.2016.04.025
|
| 220 |
M Wu, J, Gu R Guo, Y Huang, M Yang (2016) Structure of mammalian respiratory supercomplex I1III2IV1. Cell 167:1598–1609.e1510
https://doi.org/10.1016/j.cell.2016.11.012
|
| 221 |
D Xia, CA Yu, H Kim, JZ Xia, AM Kachurin, L Zhang, L Yu, J Deisenhofer (1997) Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science 277:60–66
https://doi.org/10.1126/science.277.5322.60
|
| 222 |
XH Yang, BL Trumpower (1986) Purification of a three-subunit ubiquinol-cytochrome c oxidoreductase complex from Paracoccus denitrificans. J Biol Chem 261:12282–12289
|
| 223 |
YQ Yang, Y Yu, XL Li, J Li, Y Wu, J Yu, JP Ge, ZH Huang, LB Jiang, Y Raoet al. (2017) Target elucidation by cocrystal structures of NADH-ubiquinone oxidoreductase of Plasmodium falciparum (PfNDH2) with small molecule to eliminate drug-resistant malaria. J Med Chem 60:1994–2005
https://doi.org/10.1021/acs.jmedchem.6b01733
|
| 224 |
V Yankovskaya, R Horsefield, S Tornroth, C Luna-Chavez, H Miyoshi, C, Leger B Byrne, G, Cecchini S Iwata (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299:700–704
https://doi.org/10.1126/science.1079605
|
| 225 |
T, Yano M Rahimian, KK Aneja, NM Schechter, H Rubin, CP Scott (2014) Mycobacterium tuberculosis type II NADH-menaquinone oxidoreductase catalyzes electron transfer through a two-site ping-pong mechanism and has two quinone-binding sites. Biochemistry 53:1179–1190
https://doi.org/10.1021/bi4013897
|
| 226 |
S Yoshikawa, A Shimada (2015) Reaction mechanism of cytochrome c oxidase. Chem Rev 115:1936–1989
https://doi.org/10.1021/cr500266a
|
| 227 |
S Yoshikawa, K Shinzawa-Itoh, R Nakashima, R Yaono, E Yamashita, N Inoue, M Yao, MJ Fei, CP Libeu, T Mizushimaet al. (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280:1723
https://doi.org/10.1126/science.280.5370.1723
|
| 228 |
M Zeviani, S Di Donato (2004) Mitochondrial disorders. Brain 127:2153–2172
https://doi.org/10.1093/brain/awh259
|
| 229 |
M Zhang, E Mileykovskaya, W Dowhan(2002) Gluing the respiratory chain together: cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J Biol Chem 277:43553–43556
https://doi.org/10.1074/jbc.C200551200
|
| 230 |
Z Zhang, L Huang, VM Shulmeister, YI Chi, KK Kim, LW Hung, AR Crofts, EA Berry, SH Kim (1998) Electron transfer by domain movement in cytochrome bc1. Nature 392:677–684
https://doi.org/10.1038/33612
|
| 231 |
SQ Zheng, E Palovcak, JP Armache, KA Verba, Y Cheng, DA Agard (2017) MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat Methods 14:331–332
https://doi.org/10.1038/nmeth.4193
|
| 232 |
J, Zhu KR Vinothkumar, J Hirst (2016) Structure of mammalian respiratory complex I. Nature 536:354
https://doi.org/10.1038/nature19095
|
| 233 |
J Zivanov, T, Nakane SHW Scheres (2019) A Bayesian approach to beam-induced motion correction in cryo-EM single-particle analysis. IUCrJ 6:5–17
https://doi.org/10.1107/S205225251801463X
|
| 234 |
S Zong, J Gu, T Liu, R Guo, M Wu, M Yang (2018a) UQCRFS1N assembles mitochondrial respiratory complex-III into an asymmetric 21-subunit dimer. Protein Cell 9:586–591
https://doi.org/10.1007/s13238-018-0515-x
|
| 235 |
S Zong, M, Wu J Gu, T Liu, R Guo, M Yang (2018b) Structure of the intact 14-subunit human cytochrome c oxidase. Cell Res 28:1026–1034
https://doi.org/10.1038/s41422-018-0071-1
|
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