Amazing structure of respirasome: unveiling the secrets of cell respiration
Runyu Guo, Jinke Gu, Meng Wu, Maojun Yang
Amazing structure of respirasome: unveiling the secrets of cell respiration
Respirasome, a huge molecular machine that carries out cellular respiration, has gained growing attention since its discovery, because respiration is the most indispensable biological process in almost all living creatures. The concept of respirasome has renewed our understanding of the respiratory chain organization, and most recently, the structure of respirasome solved by Yang’s group from Tsinghua University (Gu et al.Nature 237(7622):639–643, 2016) firstly presented the detailed interactions within this huge molecular machine, and provided important information for drug design and screening. However, the study of cellular respiration went through a long history. Here, we briefly showed the detoured history of respiratory chain investigation, and then described the amazing structure of respirasome.
respirasome structure / supercomplexes organization / cellular respiration / respiratory complexes / megacomplex
[1] |
Acin-Perez R, Enriquez JA (2014) The function of the respiratory supercomplexes: the plasticity model. Biochim Biophys Acta 1837:444–450. doi:10.1016/j.bbabio.2013.12.009
CrossRef
Google scholar
|
[2] |
Acin-Perez R
CrossRef
Google scholar
|
[3] |
Acin-Perez R, Fernandez-Silva P, Peleato ML, Perez-Martos A, Enriquez JA (2008) Respiratory active mitochondrial supercomplexes. Mol Cell 32:529–539. doi:10.1016/j.molcel.2008.10.021
CrossRef
Google scholar
|
[4] |
Allen RD, Schroeder CC, Fok AK (1989) An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J Cell Biol 108:2233–2240
CrossRef
Google scholar
|
[5] |
Althoff T, Mills DJ, Popot JL, Kuhlbrandt W (2011) Arrangement of electron transport chain components in bovine mitochondrial supercomplex I1III2IV1. EMBO J30:4652–4664. doi:10.1038/ emboj.2011.324
CrossRef
Google scholar
|
[6] |
Anderson CM
CrossRef
Google scholar
|
[7] |
Baradaran R, Berrisford JM, Minhas GS, Sazanov LA (2013) Crystal structure of the entire respiratory complex I. Nature 494:443–448. doi:10.1038/nature11871
CrossRef
Google scholar
|
[8] |
Baranova EA, Holt PJ, Sazanov LA (2007) Projection structure of the membrane domainof Escherichia coli respiratory complexI at8A resolution. J Mol Biol 366:140–154. doi:10.1016/j.jmb.2006.11.026
CrossRef
Google scholar
|
[9] |
Barcena C, Martinez MA, Ortega MP, Munoz HG, Sarraga GU (2010) Mitochondria with tubulovesicular cristae in renal oncocytomas. Ultrastruct Pathol 34:315–320. doi:10.3109/01913123. 2010.506021
|
[10] |
Benard G
|
[11] |
Berrisford JM, Sazanov LA (2009) Structural basis for the mechanism of respiratory complex I. J Biol Chem 284:29773–29783. doi:10.1074/jbc.M109.032144
CrossRef
Google scholar
|
[12] |
Blaza JN, Serreli R, Jones AJ, Mohammed K, Hirst J(2014) Kinetic evidence against partitioning of the ubiquinone pool and the catalytic relevance of respiratory-chain supercomplexes. Proc Natl Acad Sci U S A 111:15735–15740. doi:10.1073/pnas. 1413855111
|
[13] |
Bultema JB, Braun HP, Boekema EJ, Kouril R(2009) Megacomplex organization of the oxidative phosphorylation system by structural analysis of respiratory supercomplexes from potato. Biochim Biophys Acta 1787:60–67. doi:10.1016/j.bbabio.2008.10.010
CrossRef
Google scholar
|
[14] |
Chance B (1950) Oxidase activity–light absorption relationships in cytochrome system of heart muscle preparations. Biol Bull 99:318
|
[15] |
Chance B, Estabrook RW, Lee CP (1963) ElectronTransportin the Oxysome. Science 140:379–380. doi:10.1126/science.140.3565. 379-c
|
[16] |
Chazotte B, Hackenbrock CR (1991) Lateral diffusion of redox components in the mitochondrial inner membrane is unaffected by inner membrane folding and matrix density. J Biol Chem 266:5973–5979
|
[17] |
Chen C, Chen Y, Guan MX (2015) A peep into mitochondrial disorder: multifaceted from mitochondrial DNA mutations to nuclear gene modulation. Protein Cell 6:862–870. doi:10.1007/ s13238-015-0175-z
|
[18] |
Cogliati S
CrossRef
Google scholar
|
[19] |
Cogliati S, Enriquez JA, Scorrano L (2016) Mitochondrial Cristae: Where Beauty Meets Functionality. Trends Biochem Sci 41:261–273. doi:10.1016/j.tibs.2016.01.001
CrossRef
Google scholar
|
[20] |
Daoud R, Forget L, Lang BF (2012) Yeast mitochondrial RNase P, RNaseZ and the RNA degradosome are partofa stable super-complex. Nucleic Acids Res 40:1728–1736. doi:10.1093/nar/ gkr941
|
[21] |
Davies KM
CrossRef
Google scholar
|
[22] |
Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39. doi:10.1016/j.bbabio.2004.09.009
CrossRef
Google scholar
|
[23] |
Diaz F, Fukui H, Garcia S, Moraes CT (2006) Cytochromec oxidase is required for the assembly/stability of respiratory complex I in mouse fibroblasts. Mol Cell Biol 26:4872–4881. doi:10.1128/ MCB.01767-05
|
[24] |
Dudkina NV, Eubel H, Keegstra W, Boekema EJ, Braun HP (2005) Structure of a mitochondrial supercomplex formed by respiratory-chain complexes I and III. Proc Natl Acad Sci USA 102:3225–3229. doi:10.1073/pnas.0408870102
CrossRef
Google scholar
|
[25] |
Dudkina NV, Heinemeyer J, Sunderhaus S, Boekema EJ, Braun HP (2006) Respiratory chain supercomplexes in the plant mitochondrial membrane. Trends Plant Sci 11:232–240. doi:10.1016/j. tplants.2006.03.007
|
[26] |
Dudkina NV, Kudryashev M, Stahlberg H, Boekema EJ (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. doi:10.1073/pnas.1107819108
CrossRef
Google scholar
|
[27] |
Dudkina NV, Folea IM, Boekema EJ (2015) Towards structural and functional characterization of photosynthetic and mitochondrial supercomplexes. Micron 72:39–51. doi:10.1016/j.micron.2015.03.002
CrossRef
Google scholar
|
[28] |
Efremov RG, Sazanov LA (2011) Structure ofthe membrane domain of respiratory complex I. Nature 476:414–420. doi:10.1038/ nature10330
|
[29] |
Efremov RG, Baradaran R, Sazanov LA (2010) The architecture of respiratory complex I. Nature 465:441–445. doi:10.1038/ nature09066
CrossRef
Google scholar
|
[30] |
Enriquez JA (2016) Supramolecular organization of respiratory complexes. Annu Rev Physiol 78:533–561. doi:10.1146/ annurev-physiol-021115-105031
CrossRef
Google scholar
|
[31] |
Enriquez JA, Lenaz G(2014) Coenzymeqand the respiratory chain: coenzyme q pool and mitochondrial supercomplexes. Mol Syndromol 5:119–140. doi:10.1159/000363364
|
[32] |
Ernster L, Schatz G (1981) Mitochondria:a historical review. J Cell Biol 91:227s–255s
CrossRef
Google scholar
|
[33] |
Eubel H, Jansch L, Braun HP (2003) New insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of complex II. Plant Physiol 133:274–286
CrossRef
Google scholar
|
[34] |
Eubel H, Heinemeyer J, Sunderhaus S, Braun HP (2004) Respiratory chain supercomplexes in plant mitochondria. Plant Physiol Biochem 42:937–942. doi:10.1016/j.plaphy.2004.09.010
CrossRef
Google scholar
|
[35] |
Feng J, Lu S, Ding Y, Zheng M, Wang X (2016) Homocysteine activates Tcells by enhancing endoplasmic reticulum-mitochondria coupling and increasing mitochondrial respiration. Protein Cell 7:391–402. doi:10.1007/s13238-016-0245-x
CrossRef
Google scholar
|
[36] |
Fiedorczuk K
CrossRef
Google scholar
|
[37] |
Frenzel M, Rommelspacher H, Sugawa MD, Dencher NA (2010) Ageing alters the supramolecular architecture of OxPhos complexes in rat brain cortex. Exp Gerontol 45:563–572. doi:10.1016/ j.exger.2010.02.003
CrossRef
Google scholar
|
[38] |
Gao X
CrossRef
Google scholar
|
[39] |
Gao X
CrossRef
Google scholar
|
[40] |
Genova ML (2014) Electron Transport in the Mitochondrial Respiratory Chain. Struct Basis Biol Energy Gener 39:401–417. doi:10. 1007/978-94-017-8742-0_21
CrossRef
Google scholar
|
[41] |
Genova ML, Lenaz G (2014) Functional role of mitochondrial respiratory supercomplexes. Biochim Biophys Acta 1837:427–443. doi:10.1016/j.bbabio.2013.11.002
CrossRef
Google scholar
|
[42] |
Gomez LA, Monette JS, Chavez JD, Maier CS, Hagen TM (2009) Supercomplexes of the mitochondrial electron transport chain decline in the aging rat heart. Arch Biochem Biophys 490:30–35. doi:10.1016/j.abb.2009.08.002
CrossRef
Google scholar
|
[43] |
Green DE, Tzagoloff A (1966) The mitochondrial electron transfer chain. Arch Biochem Biophys 116:293–304
CrossRef
Google scholar
|
[44] |
Gu J
CrossRef
Google scholar
|
[45] |
Gupte S
CrossRef
Google scholar
|
[46] |
Hackenbrock CR, Schneider H, Lemasters JJ, Hochli M (1980) Relationships between bilayer lipid, motional freedom of oxidoreductase components, and electron transfer in the mitochondrial inner membrane. Adv Exp Med Biol 132:245–263
CrossRef
Google scholar
|
[47] |
Hackenbrock CR, Gupte S, Wu ES, Jacobson K (1984) Lateral diffusion, collision and efficiency of oxidation-reduction components in mitochondrial electron transport. Biochem Soc Trans 12:402–403
CrossRef
Google scholar
|
[48] |
Hackenbrock CR, Chazotte B, Gupte SS (1986) The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport. J Bioenerg Biomembr 18:331–368
CrossRef
Google scholar
|
[49] |
Hatefi Y, Haavik AG, Fowler LR, Griffiths DE (1962) Studies on the electron transfer system. XLII. Reconstitution of the electron transfer system. J Biol Chem 237:2661–2669
|
[50] |
Heinemeyer J, Braun HP, Boekema EJ, Kouril R (2007) A structural model of the cytochrome C reductase/oxidase supercomplex from yeast mitochondria. JBiol Chem 282:12240–12248. doi:10. 1074/jbc.M610545200
CrossRef
Google scholar
|
[51] |
Hochli M, Hackenbrock CR (1976) Fluidity in mitochondrial membranes: thermotropic lateral translational motion of intramembrane particles. Proc Natl Acad Sci USA 73:1636–1640
CrossRef
Google scholar
|
[52] |
Hochli M, Hackenbrock CR (1979) Lateral translational diffusion of cytochrome c oxidase in the mitochondrial energy-transducing membrane. Proc Natl Acad Sci USA 76:1236–1240
CrossRef
Google scholar
|
[53] |
Hofmann AD
|
[54] |
Huang LS
|
[55] |
Ikeda K, Shiba S, Horie-Inoue K, Shimokata K, Inoue S (2013) A stabilizing factor for mitochondrial respiratory supercomplex assembly regulates energy metabolism in muscle. Nat Commun 4:2147. doi:10.1038/ncomms3147
CrossRef
Google scholar
|
[56] |
Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structureat2.8A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376:660–669. doi:10.1038/376660a0
CrossRef
Google scholar
|
[57] |
Iwata S
CrossRef
Google scholar
|
[58] |
Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389. doi:10.1016/ j.bbabio.2010.11.009
CrossRef
Google scholar
|
[59] |
Kaila VR, Sharma V, Wikstrom M (2011) The identity of the transient proton loading site of the proton-pumping mechanism of cytochrome c oxidase. Biochim Biophys Acta 1807:80–84. doi:10.1016/j.bbabio.2010.08.014
CrossRef
Google scholar
|
[60] |
Kannt A, Lancaster CR, Michel H (1998) The coupling of electron transfer and proton translocation: electrostatic calculations on Paracoccus denitrificans cytochrome c oxidase. Biophys J74:708–721. doi:10.1016/S0006-3495(98)73996-7
CrossRef
Google scholar
|
[61] |
Keilin D, Hartree EF (1947) Activity of the cytochrome system in heart muscle preparations. Biochem J41:500–502
CrossRef
Google scholar
|
[62] |
Kouril R, Dekker JP, Boekema EJ (2012) Supramolecular organization of photosystem II in green plants. Biochim Biophys Acta 1817:2–12. doi:10.1016/j.bbabio.2011.05.024
CrossRef
Google scholar
|
[63] |
Lamantea E
CrossRef
Google scholar
|
[64] |
Lange C, Hunte C (2002) Crystal structure of the yeast cytochrome bc1 complex with its bound substrate cytochrome c. Proc Natl Acad Sci USA 99:2800–2805. doi:10.1073/pnas.052704699
CrossRef
Google scholar
|
[65] |
Lapuente-Brun E
CrossRef
Google scholar
|
[66] |
Lass A, Sohal RS (1999) Comparisons of coenzyme Q bound to mitochondrial membrane proteins among different mammalian species. Free Radic Biol Med 27:220–226
CrossRef
Google scholar
|
[67] |
Lass A, Kwong L, Sohal RS (1999a) Mitochondrial coenzyme Q content and aging. Biofactors 9:199–205
CrossRef
Google scholar
|
[68] |
Lass A, Forster MJ, Sohal RS (1999b) Effects of coenzyme Q10 and alpha-tocopherol administration on their tissue levels in the mouse: elevation of mitochondrial alpha-tocopherol by coenzyme Q10. Free Radic Biol Med 26:1375–1382
CrossRef
Google scholar
|
[69] |
Lenaz G, Genova ML (2010) Structure and organization of mitochondrial respiratory complexes: a new understanding of an old subject. Antioxid Redox Signal 12:961–1008. doi:10.1089/ ars.2009.2704
CrossRef
Google scholar
|
[70] |
Liao Y
CrossRef
Google scholar
|
[71] |
Liesa M, Shirihai OS (2013) Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab 17:491–506. doi:10.1016/j.cmet.2013.03.002
CrossRef
Google scholar
|
[72] |
Livingston AK, Cruz JA, Kohzuma K, Dhingra A, Kramer DM (2010) An Arabidopsis mutant with high cyclic electron flow around photosystem I (hcef) involving the NADPH dehydrogenase complex. Plant Cell 22:221–233. doi:10.1105/tpc.109. 071084
|
[73] |
Maranzana E, Barbero G, Falasca AI, Lenaz G, Genova ML (2013) Mitochondrial respiratory supercomplex association limits production of reactive oxygen species from complex I. Antioxid Redox Signal 19:1469–1480. doi:10.1089/ars.2012.4845
CrossRef
Google scholar
|
[74] |
Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transferbya chemi-osmotic typeof mechanism. Nature 191:144–148
CrossRef
Google scholar
|
[75] |
Moreno-Lastres D
CrossRef
Google scholar
|
[76] |
Moreno-Loshuertos R, Enriquez JA (2016) Respiratory supercomplexes and the functional segmentation of the CoQ pool. Free Radic Biol Med. doi:10.1016/j.freeradbiomed.2016.04.018
CrossRef
Google scholar
|
[77] |
Morgan DJ, Sazanov LA (2008) Three-dimensional structure of respiratory complexIfrom Escherichia coli in ice in the presence of nucleotides. Biochim Biophys Acta 1777:711–718. doi:10. 1016/j.bbabio.2008.03.023
|
[78] |
Muhleip AW
CrossRef
Google scholar
|
[79] |
Nicastro D, Frangakis AS, Typke D, Baumeister W (2000) Cryoelectron tomography of neurospora mitochondria. J Struct Biol 129:48–56. doi:10.1006/jsbi.1999.4204
CrossRef
Google scholar
|
[80] |
Nubel E, Wittig I, Kerscher S, Brandt U, Schagger H (2009) Two-dimensional native electrophoretic analysis of respiratory super-complexes from Yarrowia lipolytica. Proteomics 9:2408–2418. doi:10.1002/pmic.200800632
CrossRef
Google scholar
|
[81] |
Ostermeier C, Harrenga A, Ermler U, Michel H (1997) Structure at 2.7 A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment. Proc Natl Acad SciUSA 94:10547–10553
CrossRef
Google scholar
|
[82] |
Palsdottir H, Lojero CG, Trumpower BL, Hunte C(2003) Structureof the yeast cytochrome bc1 complex with a hydroxyquinone anion Qo site inhibitor bound. J Biol Chem 278:31303–31311. doi:10. 1074/jbc.M302195200
|
[83] |
Perkins G
|
[84] |
Pfeiffer K
CrossRef
Google scholar
|
[85] |
Ramirez-Aguilar SJ
CrossRef
Google scholar
|
[86] |
Riva A, Loffredo F, Uccheddu A, Riva FT, Tandler B (2003) Mitochondria of human adrenal cortex have tubular cristae with bulbous tips. J Clin Endocrinol Metab 88:1903–1906. doi:10. 1210/jc.2002-030013
CrossRef
Google scholar
|
[87] |
Riva A
|
[88] |
Rochaix JD (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65:287–309. doi:10.1146/annurevarplant-050213-040226
|
[89] |
Sazanov LA (2007) Respiratory complex I: mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. Biochemistry 46:2275–2288. doi:10.1021/bi602508x
CrossRef
Google scholar
|
[90] |
Sazanov LA (2015) A giant molecular proton pump: structure and mechanism of respiratory complex I. Nat Rev Mol Cell Biol 16:375–388. doi:10.1038/nrm3997
CrossRef
Google scholar
|
[91] |
Sazanov LA, Hinchliffe P(2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430–1436. doi:10.1126/science.1123809
CrossRef
Google scholar
|
[92] |
Schafer E
|
[93] |
Schagger H (2001) Respiratory chain supercomplexes. IUBMB Life 52:119–128. doi:10.1080/15216540152845911
CrossRef
Google scholar
|
[94] |
Schagger H(2002) Respiratory chain supercomplexes of mitochondria and bacteria. Biochim Biophys Acta 1555:154–159
CrossRef
Google scholar
|
[95] |
Schagger H, Pfeiffer K (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J19:1777–1783. doi:10.1093/emboj/19.8.1777
CrossRef
Google scholar
|
[96] |
Schagger H, Pfeiffer K (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. doi:10.1074/jbc.M106474200
|
[97] |
Schneider H, Lemasters JJ, Hochli M, Hackenbrock CR (1980) Liposome-mitochondrial inner membrane fusion. Lateral diffusion of integral electron transfer components. J Biol Chem 255:3748–3756
|
[98] |
Schneider H, Lemasters JJ, Hackenbrock CR (1982a) Lateral diffusion of ubiquinone during electron transfer in phospholipidand ubiquinone-enriched mitochondrial membranes. JBiol Chem 257:10789–10793
|
[99] |
Schneider H, Hochli M, Hackenbrock CR (1982b) Relationship between the density distribution of intramembrane particles and electron transfer in the mitochondrial inner membrane as revealedby cholesterol incorporation. J Cell Biol 94:387–393
CrossRef
Google scholar
|
[100] |
Sousa PM
CrossRef
Google scholar
|
[101] |
Strauss M, Hofhaus G, Schroder RR, Kuhlbrandt W (2008) Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J27:1154–1160. doi:10.1038/emboj.2008.35
CrossRef
Google scholar
|
[102] |
Stroh A
|
[103] |
Stroud DA, Ryan MT (2013) Mitochondria: organization of respiratory chain complexes becomes cristae-lized. Curr Biol 23:R969–R971. doi:10.1016/j.cub.2013.09.035
CrossRef
Google scholar
|
[104] |
Stuart RA (2008) Supercomplex organization of the oxidative phosphorylation enzymes in yeast mitochondria. J Bioenerg Biomembr 40:411–417. doi:10.1007/s10863-008-9168-4
CrossRef
Google scholar
|
[105] |
Sun F
CrossRef
Google scholar
|
[106] |
Sun D, Li B, Qiu R, Fang H, Lyu J (2016) Cell Type-Specific Modulation of Respiratory Chain Supercomplex Organization. Int J Mol Sci. doi:10.3390/ijms17060926
CrossRef
Google scholar
|
[107] |
Tsukihara T
CrossRef
Google scholar
|
[108] |
Tsukihara T
CrossRef
Google scholar
|
[109] |
Tsukihara T
CrossRef
Google scholar
|
[110] |
Vartak R, Porras CA, Bai Y (2013) Respiratory supercomplexes: structure, function and assembly. Protein Cell 4:582–590. doi:10.1007/s13238-013-3032-y
CrossRef
Google scholar
|
[111] |
Vempati UD, Han X, Moraes CT (2009) Lack of cytochrome c in mouse fibroblasts disrupts assembly/stability of respiratory complexes I and IV. J Biol Chem 284:4383–4391. doi:10.1074/jbc.M805972200
CrossRef
Google scholar
|
[112] |
Vinothkumar KR, Zhu J, Hirst J (2014) Architecture of mammalian respiratory complex I. Nature 515:80–84. doi:10.1038/nature13686
CrossRef
Google scholar
|
[113] |
Wang X
CrossRef
Google scholar
|
[114] |
Wenz T
CrossRef
Google scholar
|
[115] |
Wittig I, Braun HP, Schagger H (2006a) Blue native PAGE. Nat Protoc 1:418–428. doi:10.1038/nprot.2006.62
CrossRef
Google scholar
|
[116] |
Wittig I, Carrozzo R, Santorelli FM, Schagger H (2006b) Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim Biophys Acta 1757:1066–1072. doi:10.1016/j.bbabio.2006.05.006
CrossRef
Google scholar
|
[117] |
Xia D
CrossRef
Google scholar
|
[118] |
Yankovskaya V
CrossRef
Google scholar
|
[119] |
Yoshikawa S
CrossRef
Google scholar
|
[120] |
Zhang Z
CrossRef
Google scholar
|
[121] |
Zhang M, Mileykovskaya E, Dowhan W (2005) Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J Biol Chem 280:29403–29408. doi:10.1074/jbc.M504955200
CrossRef
Google scholar
|
[122] |
Zhu J, Vinothkumar KR, Hirst J (2016) Structure ofmammalian respiratory complex I. Nature 536:354–358. doi:10.1038/nature19095
CrossRef
Google scholar
|
/
〈 | 〉 |