Advertisement

Introduction to Mitochondrial Oxidative Phosphorylation

  • Bernhard KadenbachEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (volume 748)

Abstract

The basic mechanism of ATP synthesis in the mitochondria by oxidative phosphorylation (OxPhos) was revealed in the second half of the twentieth century. The OxPhos complexes I–V have been analyzed concerning their subunit composition, genes, and X-ray structures. This book presents new developments regarding the morphology, biogenesis, gene evolution, heat, and reactive oxygen species (ROS) generation in mitochondria, as well as the structure and supercomplex formation of OxPhos complexes. In addition, multiple mitochondrial diseases based on mutations of nuclear-encoded genes have been identified. Little is known, however, of the regulation of OxPhos according to the variable cellular demands of ATP. In particular, the functions of the supernumerary (nuclear-encoded) subunits of mitochondrial OxPhos complexes, which are mostly absent in bacteria, remain largely unknown, although the corresponding and conserved core subunits exhibit the same catalytic activity. Identification of regulatory pathways modulating OxPhos activity, by subunit isoform expression, by allosteric interaction with ATP/ADP, by reversible phosphorylation of protein subunits, or by supercomplex formation, will help to understand the role of mitochondria in the many degenerative diseases, mostly based on ROS formation in mitochondria and/or insufficient energy production.

Keywords

Mitochondrial Disease Bovine Heart Paracoccus Denitrificans Mitochondrial Carrier OxPhos Complex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgement

I would really like to thank Rabia Ramzan for preparing Fig. 1.1.

References

  1. Abrahams JP, Leslie AG, Lutter R, Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370(6491):621–628PubMedGoogle Scholar
  2. Anthony G, Stroh A, Lottspeich F, Kadenbach B (1990) Different isozymes of cytochrome c oxidase are expressed in bovine smooth muscle and skeletal or heart muscle. FEBS Lett 277:97–100PubMedGoogle Scholar
  3. Arnold S, Kadenbach B (1997) Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome c oxidase. Eur J Biochem 249:350–354PubMedGoogle Scholar
  4. Arnold S, Goglia F, Kadenbach B (1998) 3,5-diiodothyronine binds to subunit Va of cytochrome c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur J Biochem 252:325–330PubMedGoogle Scholar
  5. Bamber L, Harding M, Monne M, Slotboom DJ, Kunji ERS (2007) The yeast mitochondrial ADP/ATP carrier functions as a monomer in mitochondrial membranes. Proc Natl Acad Sci USA 104:10830–10834PubMedGoogle Scholar
  6. Bonne G, Seibel P, Possekel S, Marsac C, Kadenbach B (1993) Expression of humen cytochrome c oxidase subunits during fetal development. Eur J Biochem 217:1099–1107PubMedGoogle Scholar
  7. Bowler MW, Montgomery MG, Leslie AGW, Walker JE (2007) Ground state structure of F1-ATPase from bovine heart mitochondria at 1.9 Å resolution. J Biol Chem 282:14238–14242PubMedGoogle Scholar
  8. Boyer PD, Chance B, Ernster L, Mitchell P, Racker E, Slater EC (1977) Oxidative phosphorylation and photophosphorylation. Annu Rev Biochem 46:955–966PubMedGoogle Scholar
  9. Brenner D, Mak TW (2009) Mitochondrial cell death effectors. Curr Opin Cell Biol 21:871–877PubMedGoogle Scholar
  10. Buschmann S, Warkentin E, Xie H, Langer JD, Ermler U, Michel H (2010) The structure of cbb3 cytochrome oxidase provides insights into proton pumping. Science 329(5989):327–330PubMedGoogle Scholar
  11. Carroll J, Fearnley IM, Wang Q, Walker JE (2009) Measurement of the molecular masses of hydrophilic and hydrophobic subunits of ATP synthase and complex I in a single experiment. Anal Biochem 395:249–255PubMedGoogle Scholar
  12. Chen R, Fearnley IM, Peak-Chew SY, Walker JE (2004) The phosphorylation of subunits of complex I from bovine heart mitochondria. J Biol Chem 279:26036–26045PubMedGoogle Scholar
  13. Collinson IR, Runswick MJ, Buchanan SK, Fearnley IM, Skehel JM, van Raaij MJ, Griffiths DE, Walker JE (1994) Fo membrane domain of ATP synthase from bovine heart mitochondria: purification, subunit composition, and reconstitution with F1-ATPase. Biochemistry 33: 7971–7978PubMedGoogle Scholar
  14. Dalmonte ME, Forte E, Genova ML, Giuffrè A, Sarti P, Lenaz G (2009) Control of respiration by cytochrome c oxidase in intact cells: role of the membrane potential. J Biol Chem 284: 32331–32335PubMedGoogle Scholar
  15. Das J, Miller ST, Stern DL (2004) Comparison of diverse protein sequences of the nuclear-encoded subunits of cytochrome c oxidase suggests conservation of structure underlies evolving functional sites. Mol Biol Evol 21:1572–1582PubMedGoogle Scholar
  16. De Rasmo D, Panelli D, Sardanelli AM, Papa S (2008) cAMP-dependent protein kinase regulates the mitochondrial import of the nuclear encoded NDUFS4 subunit of complex I. Cell Signal 20:989–997PubMedGoogle Scholar
  17. Dickson VK, Silvester JA, Fearnley IM, Leslie AG, Walker JE (2006) On the structure of the stator of the mitochondrial ATP synthase. EMBO J 25:2911–2918PubMedGoogle Scholar
  18. DiMauro S, Schon EA (2008) Mitochondrial disorders in the nervous system. Annu Rev Neurosci 31:91–123PubMedGoogle Scholar
  19. Efremov RG, Sazanov LA (2011) Structure of the membrane domain of respiratory complex I. Nature 476(7361):414–420PubMedGoogle Scholar
  20. Ferguson-Miller S, Hiser C, Liu J (2012) Gating and regulation of the cytochrome c oxidase proton pump. Biochim Biophys Acta 1817:489–494Google Scholar
  21. Frank V, Kadenbach B (1996) Regulation of the H+/e–stoichiometry of cytochrome c oxidase from bovine heart by intraliposomal ATP/ADP ratios. FEBS Lett 382:121–124PubMedGoogle Scholar
  22. Groen AK, Wanders RJA, Westerhoff HV, van der Meer R, Tager JM (1982) Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257:2754–2757PubMedGoogle Scholar
  23. Helling S, Hüttemann H, Ramzan R, Kim SH, Lee I, Müller T, Langenfeld E, Meyer HE, Kadenbach B, Vogt S, Marcus K (2012) Multiple phosphorylations of cytochrome c oxidase and their functions. Proteomics 12:950–959Google Scholar
  24. Hunte C, Zickermann V, Brandt U (2010) Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science 329(5990):448–451PubMedGoogle Scholar
  25. Hüttemann M, Kadenbach B, Grossman LI (2001) Mammalian subunit IV isoforms of cytochrome c oxidase. Gene 267:111–123PubMedGoogle Scholar
  26. Hüttemann M, Jaradat S, Grossman LI (2003a) Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb – the counterpart to testes-specific cytochrome c? Mol Reprod Dev 66:8–16PubMedGoogle Scholar
  27. Hüttemann M, Schmidt TR, Grossman LI (2003b) A third isoform of cytochrome c oxidase subunit VIII is present in mammals. Gene 312:95–102PubMedGoogle Scholar
  28. Indran IR, Tufo G, Pervaiz S, Brenner C (2011) Recent advances in apoptosis, mitochondria and drug resistance in cancer cells. Biochim Biophys Acta 1807:735–745, ReviewPubMedGoogle Scholar
  29. Inoue Y, Shingyoji C (2007) The roles of noncatalytic ATP binding and ADP binding in the regulation of dynein motile activity in flagella. Cell Motil Cytoskeleton 64:690–704PubMedGoogle Scholar
  30. Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376:660–669PubMedGoogle Scholar
  31. Iwata S, Lee JW, Okada K, Lee JK, Iwata M, Rasmussen B, Link TA, Ramaswamy S, Jap BK (1998) Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281(5373):64–71PubMedGoogle Scholar
  32. Jastroch M, Divakaruni AS, Mookerjee S, Treberg JR, Brand MD (2010) Mitochondrial proton and electron leaks. Essays Biochem 47:53–67PubMedGoogle Scholar
  33. Kadenbach B, Ramzan R, Wen L, Vogt S (2010) New extension of the Mitchell Theory for oxidative phosphorylation in mitochondria of living organisms. Biochim Biophys Acta 1800: 205–212PubMedGoogle Scholar
  34. Klingenberg M (2008) The ADP and ATP transport in mitochondria and its carrier. Biochim Biophys Acta 1778:1978–2021PubMedGoogle Scholar
  35. Koepke J, Olkhova E, Angerer H, Müller H, Peng G, Michel H (2009) High resolution crystal structure of Paracoccus denitrificans cytochrome c oxidase: new insights into the active site and the proton transfer pathways. Biochim Biophys Acta 1787:635–645PubMedGoogle Scholar
  36. Krishnan KJ, Reeve AK, Samuels DC, Chinnery PF, Blackwood JK, Taylor RW, Wanrooij S, Spelbrink JN, Lightowlers RN, Turnbull DM (2008) What causes mitochondrial DNA deletions in human cells? Nat Genet 40:275–279PubMedGoogle Scholar
  37. Kunji ER, Robinson AJ (2010) Coupling of proton and substrate translocation in the transport cycle of mitochondrial carriers. Curr Opin Struct Biol 20:440–447PubMedGoogle Scholar
  38. Lee I, Kadenbach B (2001) Palmitate decreases proton pumping of liver-type cytochrome c oxidase. Eur J Biochem 268:6329–6334PubMedGoogle Scholar
  39. Lee I, Bender E, Arnold S, Kadenbach B (2001) New control of mitochondrial membrane potential and ROS-formation. Biol Chem 382:1629–1633PubMedGoogle Scholar
  40. Lee I, Bender E, Kadenbach B (2002) Control of mitochondrial membrane potential and ROS formation by reversible phosphorylation of cytochrome c oxidase. Mol Cell Biochem 234(235):63–70PubMedGoogle Scholar
  41. Lee I, Salomon AR, Ficarro S, Mathes I, Lottspeich F, Grossman LI, Hüttemann M (2005) cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J Biol Chem 280:6094–6100PubMedGoogle Scholar
  42. Lehninger AL (1970) Biochemistry. Worth Publishers, New YorkGoogle Scholar
  43. Lill R (2009) Function and biogenesis of iron-sulphur proteins. Nature 460(7257):831–838PubMedGoogle Scholar
  44. Linder D, Freund R, Kadenbach B (1995) Species-specific expression of cytochrome c oxidase isozymes. Comp Biochem Physiol 112B:461–469Google Scholar
  45. Linn TC, Pettit FH, Reed LJ (1969) Alpha-keto acid dehydrogenase complexes. X. Regulation of the activity of the pyruvate dehydrogenase complex from beef kidney mitochondria by phosphorylation and dephosphorylation. Proc Natl Acad Sci USA 62:234–241PubMedGoogle Scholar
  46. Liu J, Qin L, Ferguson-Miller S (2011) Crystallographic and online spectral evidence for role of conformational change and conserved water in cytochrome oxidase proton pump. Proc Natl Acad Sci USA 108(4):1284–1289PubMedGoogle Scholar
  47. Ludwig B, Bender E, Arnold S, Hüttemann M, Lee I, Kadenbach B (2001) Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chembiochem 2:392–403PubMedGoogle Scholar
  48. Margulis L (1975) Symbiotic theory of the origin of eukaryotic organelles; criteria for proof. Symp Soc Exp Biol 29:21–38PubMedGoogle Scholar
  49. Martinou JC, Youle RJ (2011) Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell 21:92–101PubMedGoogle Scholar
  50. McKenzie M, Lazarou M, Ryan MT (2009) Analysis of respiratory chain complex assembly with radiolabeled nuclear- and mitochondrial-encoded subunits. Methods Enzymol 456:321–339PubMedGoogle Scholar
  51. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature 191:144–148PubMedGoogle Scholar
  52. Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev 41:445–502PubMedGoogle Scholar
  53. Müller-Höcker J, Schneiderbanger K, Stefani FH, Kadenbach B (1992) Progressive loss of cytochrome-c-oxidase in the human extraocular muscles in ageing—a cytochemical-immunohistochemical study. Mutat Res 275:115–124PubMedGoogle Scholar
  54. Müller-Höcker J, Seibel P, Schneiderbanger K, Kadenbach B (1993) Different in situ hybridisation patterns of mitochondrial DNA in cytochrome c oxidase- deficient extraocular muscle fibres in the elderly. Virchows Arch A Pathol Anat Histopathol 422:7–15PubMedGoogle Scholar
  55. Napiwotzki J, Kadenbach B (1998) Extramitochondrial ATP/ADP-ratios regulate cytochrome c oxidase activity via binding to the cytosolic domain of subunit IV. Biol Chem 379:335–339PubMedGoogle Scholar
  56. Nyola A, Hunte C (2008) A structural analysis of the transient interaction between the cytochrome bc1 complex and its substrate cytochrome c. Biochem Soc Trans 36:981–985PubMedGoogle Scholar
  57. Pacelli C, Latorre D, Cocco T, Capuano F, Kukat C, Seibel P, Villani G (2011) Tight control of mitochondrial membrane potential by cytochrome c oxidase. Mitochondrion 11:334–341PubMedGoogle Scholar
  58. Pagliarini DJ, Dixon JE (2006) Mitochondrial modulation: reversible phosphorylation takes center stage? Trends Biochem Sci 31:26–34PubMedGoogle Scholar
  59. Palmieri F (2008) Diseases caused by defects of mitochondrial carriers: a review. Biochim Biophys Acta 1777:564–578PubMedGoogle Scholar
  60. Palmieri F, Pierri CL (2010) Mitochondrial metabolite transport. Essays Biochem 47:37–52PubMedGoogle Scholar
  61. Palmieri F, Pierri CL, De Grassi A, Nunes-Nesi A, Fernie AR (2011) Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant J 66:161–181PubMedGoogle Scholar
  62. Parsons WJ, Williams RS, Shelton JM, Luo Y, Kessler DJ, Richardson JA (1996) Developmental regulation of cytochrome oxidase subunit VIa isoforms in cardiac and skeletal muscle. Am J Physiol 270:H567–H574PubMedGoogle Scholar
  63. Paumard P, Vaillier J, Coulary B, Schaeffer J, Soubannier V, Mueller DM, Brèthes D, di Rago JP, Velours J (2002) The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J 21:221–230PubMedGoogle Scholar
  64. Pebay-Peyroula E, Dahout-Gonzalez C, Kahn R, Trezeguet V, Lauquin GJ, Brandolin G (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426:39–44PubMedGoogle Scholar
  65. Piccoli C, Scrima R, Boffoli D, Capitanio N (2006) Control by cytochrome c oxidase of the callular oxidative phosphorylation system depends on the mitochondrial energy state. Biochem J 396:573–583PubMedGoogle Scholar
  66. Pierron D, Wildman DE, Hüttemann M, Markondapatnaikuni GC, Aras S, Grossman LI (2012) Cytochrome c oxidase: evolution of control via nuclear subunit addition. Biochim Biophys Acta 1817:590–597Google Scholar
  67. Pivovarova NB, Andrews SB (2010) Calcium-dependent mitochondrial function and dysfunction in neurons. FEBS J 277:3622–3636PubMedGoogle Scholar
  68. Rajagopalan K, Watt DS, Haley BE (1999) Orientation of GTP and ADP within their respective binding sites in glutamate dehydrogenase. Eur J Biochem 265:564–571PubMedGoogle Scholar
  69. Rees DM, Leslie AG, Walker JE (2009) The structure of the membrane extrinsic region of bovine ATP synthase. Proc Natl Acad Sci USA 106:21597–21601PubMedGoogle Scholar
  70. Richards TA, Archibald JM (2011) Cell evolution: gene transfer agents and the origin of mitochondria. Curr Biol 21:R112–R114PubMedGoogle Scholar
  71. Robblee JP, Cao W, Henn A, Hannemann DE, De La Cruz EM (2005) Thermodynamics of nucleotide binding to actomyosin V and VI: a positive heat capacity change accompanies strong ADP binding. Biochemistry 44:10238–10249PubMedGoogle Scholar
  72. Salje J, Ludwig B, Richter OM (2005) Is a third proton-conducting pathway operative in bacterial cytochrome c oxidase? Biochem Soc Trans 33:829–831PubMedGoogle Scholar
  73. Samavati L, Lee I, Mathes I, Lottspeich F, Hüttemann M (2008) Tumor necrosis factor alpha inhibits oxidative phosphorylation through tyrosine phosphorylation at subunit I of cytochrome c oxidase. J Biol Chem 283:21134–21144PubMedGoogle Scholar
  74. Sazanov LA, Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311(5766):1430–1433PubMedGoogle Scholar
  75. Scacco S, Vergari R, Scarpulla RC, Technikova-Dobrova Z, Sardanelli A, Lambo R, Lorusso V, Papa S (2000) cAMP-dependent phosphorylation of the nuclear encoded 18-kDa (IP) subunit of respiratory complex I and activation of the complex in serum-starved mouse fibroblast cultures. J Biol Chem 275:17578–17582PubMedGoogle Scholar
  76. Schägger H (2002) Respiratory chain supercomplexes of mitochondria and bacteria. Biochim Biophys Acta 1555:154–159PubMedGoogle Scholar
  77. Schmidt O, Pfanner N, Meisinger C (2010) Mitochondrial protein import: from proteomics to functional mechanisms. Nat Rev Mol Cell Biol 11:655–667PubMedGoogle Scholar
  78. Schultz IJ, Chen C, Paw BH, Hamza I (2010) Iron and porphyrin trafficking in heme biogenesis. J Biol Chem 285:26753–26759PubMedGoogle Scholar
  79. Sheftel A, Stehling O, Lill R (2010) Iron-sulfur proteins in health and disease. Trends Endocrinol Metab 21:302–314PubMedGoogle Scholar
  80. Shimokata K, Katayama Y, Murayama H, Suematsu M, Tsukihara T, Muramoto K, Aoyama H, Yoshikawa S, Shimada H (2007) The proton pumping pathway of bovine heart cytochrome c oxidase. Proc Natl Acad Sci USA 104:4200–4205PubMedGoogle Scholar
  81. Shinzawa-Itoh K, Aoyama H, Muramoto K, Terada H, Kurauchi T, Tadehara Y, Yamasaki A, Sugimura T, Kurono S, Tsujimoto K, Mizushima T, Yamashita E, Tsukihara T, Yoshikawa S (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J 26:1713–1725PubMedGoogle Scholar
  82. Shoubridge EA (2001) Cytochrome c oxidase deficiency. Am J Med Genet 106:46–52PubMedGoogle Scholar
  83. Stock D, Leslie AG, Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286(5445):1700–1705PubMedGoogle Scholar
  84. Sun F, Huo X, Zhai Y, Wang A, Xu J, Su D, Bartlam M, Rao Z (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121:1043–1057PubMedGoogle Scholar
  85. Tiefenbrunn T, Liu W, Chen Y, Katritch V, Stout CD, Fee JA, Cherezov V (2011) High resolution structure of the ba3 cytochrome c oxidase from Thermus thermophilus in a lipidic environment. PLoS One 6(7):e22348PubMedGoogle Scholar
  86. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Shinzawa-Itoh H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1995) Structures of metal sites of oxidized bovine heart cytochrome coxidase at 2.8 Å. Science 269:1069–1074PubMedGoogle Scholar
  87. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272:1136–1144PubMedGoogle Scholar
  88. Van den Bogert C, Dekker HL, Cornelissen JC, Van Kuilenburg AB, Bolhuis PA, Muijsers AO (1992) Isoforms of cytochrome c oxidase in tissues and cell lines of the mouse. Biochim Biophys Acta 1099:118–122PubMedGoogle Scholar
  89. Villani G, Attardi G (1997) In vivo control of respiration by cytochrome c oxidase in wild-type and mitochondrial DNA mutation-carrying human cells. Proc Natl Acad Sci USA 94:1166–1171PubMedGoogle Scholar
  90. Villani G, Attardi G (2001) In vivo measurements of respiration control by cytochrome c oxidase and in situ analysis of oxidative phosphorylation. Methods Cell Biol 65:119–131PubMedGoogle Scholar
  91. Vogt S, Rhiel A, Koch V, Kadenbach B (2007) Regulation of oxidative phosphorylation by inhibition of its enzyme complexes via reversible phosphorylation. Curr Enzyme Inhib 3:189–206Google Scholar
  92. von Ballmoos C, Gennis RB, Ädelroth P, Brzezinski P (2011) Kinetic design of the respiratory oxidases. Proc Natl Acad Sci USA 108:11057–11062Google Scholar
  93. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a ­common nucleotide binding fold. EMBO J 1:945–951PubMedGoogle Scholar
  94. Wallace DC (2010) Mitochondrial DNA mutations in disease and aging. Environ Mol Mutagen 51:440–450PubMedGoogle Scholar
  95. Wallin IE (1923) The mitochondria problem. Am Nat 57(650):255–261Google Scholar
  96. Watt IN, Montgomery MG, Runswick MJ, Leslie AG, Walker JE (2010) Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc Natl Acad Sci USA 107:16823–16827PubMedGoogle Scholar
  97. Wierenga RK, Terpstra P, Hol WG (1986) Prediction of the occurrence of the ADP-binding beta alpha beta-fold in proteins, using an amino acid sequence fingerprint. J Mol Biol 187: 101–107PubMedGoogle Scholar
  98. Yoshikawa S, Shinzawa-Itoh K, Nakashima R, Yaono R, Yamashita E, Inoue N, Yao M, Fei MJ, Libeu CP, Mizushima T, Yamaguchi H, Tomizaki T, Tsukihara T (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280(5370):1723–1729PubMedGoogle Scholar
  99. Yoshikawa S, Muramoto K, Shinzawa-Itoh K, Aoyama H, Tsukihara T, Shimokata K, Katayama Y, Shimada H (2006) Proton pumping mechanism of bovine heart cytochrome c oxidase. Biochim Biophys Acta 1757:1110–1116PubMedGoogle Scholar
  100. Yu MA, Egawa T, Shinzawa-Itoh K, Yoshikawa S, Yeh SR, Rousseau DL, Gerfen GJ (2011) Radical formation in cytochrome c oxidase. Biochim Biophys Acta 1807:1295–1304PubMedGoogle Scholar
  101. Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts AR, Berry EA, Kim SH (1998) Electron transfer by domain movement in cytochrome bc1. Nature 392(6677): 677–684PubMedGoogle Scholar
  102. Zimmer C (2009) Origins. On the origin of eukaryotes. Science 325:666–668PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Fachbereich ChemiePhilipps-University MarburgMarburgGermany

Personalised recommendations