Assembly of Transmembrane b-Type Cytochromes and Cytochrome Complexes

  • Hans-Georg KochEmail author
  • Dirk SchneiderEmail author
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 41)


Cytochromes are involved in charge-transfer reactions, and many cytochromes contain a transmembrane domain and are part of membrane-localized electron transfer chains. Protoporphyrin IX (heme b) is the first heme product in the tetrapyrrole/heme biosynthesis pathway. In contrast to c-type cytochromes, there is no need for a specialized machinery catalyzing covalent attachment of the heme molecule to a b-type apo-cytochrome, nor is the cofactor further modified, as in a-, d- and o-type cytochromes. Thus, formation of a holo-cytochrome is relatively simple for b-type cytochromes, and this class of proteins probably represents the most ancient members of transmembrane cytochromes. However, assembly of individual transmembrane b-type cytochromes as well as of larger cytochrome complexes involves multiple steps, which have to be tightly controlled and aligned: the apo-protein as well as the heme cofactor needs to be synthesized, targeted to, and integrated into a membrane prior to holo-cytochrome formation. Spontaneous folding and assembly of individual transmembrane b-type cytochromes involves folding of the polypeptide chain and formation of a heme-binding cavity, which allows specific and tight binding of the cofactor. Additional biogenesis steps are eventually required for maturation of transmembrane b-type cytochrome complexes.


Signal Recognition Particle Heme Binding Heme Molecule Heme Cofactor Helical Hairpin 
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.



b-type heme with a reduced α-band peak at 559 nm


Guided entry of tail-anchored proteins


Ribosome-nascent-chain complex


Signal recognition particle






Translocase of the inner mitochondrial membrane


Translocase of the outer mitochondrial membrane



The authors thank all previous and current lab members. This work was funded by grants from the Deutsche Forschungsgemeinschaft.


  1. Abramson J, Riistama S, Larsson G, Jasaitis A, Svensson-Ek M, Laakkonen L, Puustinen A, … Wikstrom M (2000) The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. 7:910–917Google Scholar
  2. Akdogan Y, Anbazhagan V, Hinderberger D, Schneider D (2012) Heme binding constricts the conformational dynamics of the cytochrome b(559)’ heme binding cavity. Biochemistry 51:7149–7156PubMedCrossRefGoogle Scholar
  3. Alami M, Luke I, Deitermann S, Eisner G, Koch HG, Brunner J, Muller M (2003) Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol Cell 12:937–946PubMedCrossRefGoogle Scholar
  4. Angelini S, Deitermann S, Koch HG (2005) FtsY, the bacterial signal-recognition particle receptor, interacts functionally and physically with the SecYEG translocon. EMBO Rep 6:476–481PubMedPubMedCentralCrossRefGoogle Scholar
  5. Angelini S, Boy D, Schiltz E, Koch HG (2006) Membrane binding of the bacterial signal recognition particle receptor involves two distinct binding sites. J Cell Biol 174:715–724PubMedPubMedCentralCrossRefGoogle Scholar
  6. Aschtgen M-S, Zoued A, Lloubes R, Journet L, Cascales E (2012) The C-tail anchored TssL subunit, an essential protein of the enteroaggregative Escherichia coli Sci-1 Type VI secretion system, is inserted by YidC. MicrobiologyOpen 1:71–82PubMedPubMedCentralCrossRefGoogle Scholar
  7. Babcock GT, Widger WR, Cramer WA, Oertling WA, Metz JG (1985) Axial ligands of chloroplast cytochrome b-559: identification and requirement for a heme-crosslinked polypeptide structure. Biochemistry 24:3638–3645PubMedCrossRefGoogle Scholar
  8. Bange G, Sinning I (2013) SIMIBI twins in protein targeting and localization. Nat Struct Mol Biol 20:776–780PubMedCrossRefGoogle Scholar
  9. Barker PD, Ferguson SJ (1999) Still a puzzle: why is haem covalently attached in c-type cytochromes? Structure 7:R281–R290PubMedCrossRefGoogle Scholar
  10. Barrick D (1994) Replacement of the proximal ligand of sperm whale myoglobin with free imidazole in the mutant His-93 → Gly. Biochemistry 33:6546–6554PubMedCrossRefGoogle Scholar
  11. Bauerschmitt H, Mick DU, Deckers M, Vollmer C, Funes S, Kehrein K, Ott M, … Herrmann JM (2010) Ribosome-binding proteins Mdm38 and Mba1 display overlapping functions for regulation of mitochondrial translation. Mol Biol Cell 21:1937–1944Google Scholar
  12. Beck K, Eisner G, Trescher D, Dalbey RE, Brunner J, Muller M (2001) YidC, an assembly site for polytopic Escherichia coli membrane proteins located in immediate proximity to the SecYE translocon and lipids. EMBO Rep 2:709–714PubMedPubMedCentralCrossRefGoogle Scholar
  13. Becker T, Bottinger L, Pfanner N (2012) Mitochondrial protein import: from transport pathways to an integrated network. Trends Biochem Sci 37:85–91PubMedCrossRefGoogle Scholar
  14. Beha D, Deitermann S, Muller M, Koch HG (2003) Export of beta-lactamase is independent of the signal recognition particle. J Biol Chem 278:22161–22167PubMedCrossRefGoogle Scholar
  15. Beilharz T, Egan B, Silver PA, Hofmann K, Lithgow T (2003) Bipartite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae. J Biol Chem 278:8219–8223PubMedCrossRefGoogle Scholar
  16. Bibi E (2011) Early targeting events during membrane protein biogenesis in Escherichia coli. Biochim Biophys Acta 1808:841–850PubMedCrossRefGoogle Scholar
  17. Borgese N, Righi M (2010) Remote origins of tail-anchored proteins. Traffic 11:877–885PubMedCrossRefGoogle Scholar
  18. Borisov VB, Gennis RB, Hemp J, Verkhovsky MI (2011) The cytochrome bd respiratory oxygen reductases. Biochim Biophys Acta 1807:1398–1413PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bornemann T, Jockel J, Rodnina MV, Wintermeyer W (2008) Signal sequence-independent membrane targeting of ribosomes containing short nascent peptides within the exit tunnel. Nat Struct Mol Biol 15:494–499PubMedCrossRefGoogle Scholar
  20. Braig D, Bar C, Thumfart JO, Koch HG (2009) Two cooperating helices constitute the lipid-binding domain of the bacterial SRP receptor. J Mol Biol 390:401–413PubMedCrossRefGoogle Scholar
  21. Braig D, Mircheva M, Sachelaru I, van der Sluis EO, Sturm L, Beckmann R, Koch HG (2011) Signal sequence-independent SRP-SR complex formation at the membrane suggests an alternative targeting pathway within the SRP cycle. Mol Biol Cell 22:2309–2323PubMedPubMedCentralCrossRefGoogle Scholar
  22. Brasseur G, Brivet-Chevillotte P (1995) Characterization of mutations in the mitochondrial cytochrome b gene of Saccharomyces cerevisiae affecting the quinone reductase site (QN). Eur J Biochem 230:1118–1124PubMedCrossRefGoogle Scholar
  23. Brasseur G, Saribas AS, Daldal F (1996) A compilation of mutations located in the cytochrome b subunit of the bacterial and mitochondrial bc1 complex. Biochim Biophys Acta 1275:61–69PubMedCrossRefGoogle Scholar
  24. Breyton C, Tribet C, Olive J, Dubacq JP, Popot JL (1997) Dimer to monomer conversion of the cytochrome b6 f complex. Causes and consequences. J Biol Chem 272:21892–21900PubMedCrossRefGoogle Scholar
  25. Chen M, Xie K, Jiang F, Yi L, Dalbey RE (2002) YidC, a newly defined evolutionarily conserved protein, mediates membrane protein assembly in bacteria. Biol Chem 383:1565–1572PubMedCrossRefGoogle Scholar
  26. Cordova JM, Noack PL, Hilcove SA, Lear JD, Ghirlanda G (2007) Design of a functional membrane protein by engineering a heme-binding site in glycophorin A. J Am Chem Soc 129:512–518PubMedCrossRefGoogle Scholar
  27. Cramer WA, Yan J, Zhang H, Kurisu G, Smith JL (2005) Structure of the cytochrome b6f complex: new prosthetic groups, Q-space, and the ‘hors d’oeuvres hypothesis’ for assembly of the complex. Photosynth Res 85:133–143PubMedCrossRefGoogle Scholar
  28. Craney A, Tahlan K, Andrews D, Nodwell J (2011) Bacterial transmembrane proteins that lack N-terminal signal sequences. PLoS ONE 6:e19421PubMedPubMedCentralCrossRefGoogle Scholar
  29. Cristobal S, Scotti P, Luirink J, von Heijne G, de Gier JW (1999) The signal recognition particle-targeting pathway does not necessarily deliver proteins to the sec-translocase in Escherichia coli. J Biol Chem 274:20068–20070PubMedCrossRefGoogle Scholar
  30. Daldal F, Davidson E, Cheng S (1987) Isolation of the structural genes for the Rieske Fe-S protein, cytochrome b and cytochrome c1 all components of the ubiquinol: cytochrome c2 oxidoreductase complex of Rhodopseudomonas capsulata. J Mol Biol 195:1–12PubMedCrossRefGoogle Scholar
  31. Davidson E, Ohnishi T, Tokito M, Daldal F (1992) Rhodobacter capsulatus mutants lacking the Rieske FeS protein form a stable cytochrome bc1 subcomplex with an intact quinone reduction site. Biochemistry 31:3351–3358PubMedCrossRefGoogle Scholar
  32. Deitermann S, Sprie GS, Koch HG (2005) A dual function for SecA in the assembly of single spanning membrane proteins in Escherichia coli. J Biol Chem 280:39077–39085PubMedCrossRefGoogle Scholar
  33. Discher BM, Koder RL, Moser CC, Dutton PL (2003) Hydrophilic to amphiphilic design in redox protein maquettes. Curr Opin Chem Biol 7:741–748PubMedCrossRefGoogle Scholar
  34. Discher BM, Noy D, Strzalka J, Ye S, Moser CC, Lear JD, Blasie JK, Dutton PL (2005) Design of amphiphilic protein maquettes: controlling assembly, membrane insertion, and cofactor interactions. Biochemistry 44:12329–12343PubMedPubMedCentralCrossRefGoogle Scholar
  35. Dreher C, Prodöhl A, Weber M, Schneider D (2007) Heme binding properties of heterologously expressed spinach cytochrome b(6): implications for transmembrane b-type cytochrome formation. FEBS Lett 581:2647–2651PubMedCrossRefGoogle Scholar
  36. Dreher C, Prodöhl A, Hielscher R, Hellwig P, Schneider D (2008) Multiple step assembly of the transmembrane cytochrome b6. J Mol Biol 382:1057–1065PubMedCrossRefGoogle Scholar
  37. Dreher C, Hielscher R, Prodohl A, Hellwig P, Schneider D (2010) Characterization of two cytochrome b6 proteins from the cyanobacterium Gloeobacter violaceus PCC 7421. J Bioenerg Biomembr 42:517–526PubMedCrossRefGoogle Scholar
  38. du Plessis DJF, Nouwen N, Driessen AJM (2006) Subunit a of cytochrome o oxidase requires both YidC and SecYEG for membrane insertion. J Biol Chem 281:12248–12252PubMedCrossRefGoogle Scholar
  39. du Plessis DJ, Berrelkamp G, Nouwen N, Driessen AJ (2009) The lateral gate of SecYEG opens during protein translocation. J Biol Chem 284:15805–15814PubMedPubMedCentralCrossRefGoogle Scholar
  40. du Plessis DJF, Nouwen N, Driessen AJM (2011) The sec translocase. Biochim Biophys Acta 1808:851–865PubMedCrossRefGoogle Scholar
  41. Eitan A, Bibi E (2004) The core Escherichia coli signal recognition particle receptor contains only the N and G domains of FtsY. J Bacteriol 186:2492–2494PubMedPubMedCentralCrossRefGoogle Scholar
  42. Ekici S, Pawlik G, Lohmeyer E, Koch HG, Daldal F (2012) Biogenesis of cbb(3)-type cytochrome c oxidase in Rhodobacter capsulatus. Biochim Biophys Acta 1817:898–910PubMedCrossRefGoogle Scholar
  43. Esposti MD, De Vries S, Crimi M, Ghelli A, Patarnello T, Meyer A (1993) Mitochondrial cytochrome b: evolution and structure of the protein. Biochim Biophys Acta 1143:243–271PubMedCrossRefGoogle Scholar
  44. Facey SJ, Neugebauer SA, Krauss S, Kuhn A (2007) The mechanosensitive channel protein MscL is targeted by the SRP to the novel YidC membrane insertion pathway of Escherichia coli. J Mol Biol 365:995–1004PubMedCrossRefGoogle Scholar
  45. Ferguson SJ, Stevens JM, Allen JWA, Robertson IB (2008) Cytochrome c assembly: a tale of ever increasing variation and mystery? Biochim Biophys Acta - Bioenergetics 1777:980–984CrossRefGoogle Scholar
  46. Fontaine F, Fuchs RT, Storz G (2011) Membrane localization of small proteins in Escherichia coli. J Biol Chem 286:32464–32474PubMedPubMedCentralCrossRefGoogle Scholar
  47. Francke C, Loyal R, Ohad I, Haehnel W (1999) In vitro assembly of a beta2 cytochrome b559-like complex from the chemically synthesised beta-subunit encoded by the Synechocystis sp. 6803 psbF gene. FEBS Lett 442:75–78PubMedCrossRefGoogle Scholar
  48. Frauenfeld J, Gumbart J, van der Sluis EO, Funes S, Gartmann M, Beatrix B, Mielke T, Berninghaus O, Becker T, Schulten K, Beckmann R (2011) Cryo EM structure of the ribosome-SecYE complex in the membrane environment. Nat Struct Mol Biol 18:614–621PubMedPubMedCentralCrossRefGoogle Scholar
  49. Funes S, Kauff F, van der Sluis EO, Ott M, Herrmann JM (2011) Evolution of YidC/Oxa1/Alb3 insertases: three independent gene duplications followed by functional specialization in bacteria, mitochondria and chloroplasts. Biol Chem 392:13–19PubMedCrossRefGoogle Scholar
  50. Funes S, Westerburg H, Jaimes-Miranda F, Woellhaf MW, Aguilar-Lopez JL, Janssen L, Bonnefoy N, … Herrmann JM (2013) Partial suppression of Oxa1 mutants by mitochondria-targeted signal recognition particle provides insights into the evolution of the cotranslational insertion systems. Febs J 280:904–915Google Scholar
  51. Garcia-Horsman JA, Barquera B, Rumbley J, Ma J, Gennis RB (1994) The superfamily of heme-copper respiratory oxidases. J Bacteriol 176:5587–5600PubMedPubMedCentralGoogle Scholar
  52. Gennis RB, Barquera B, Hacker B, Van Doren SR, Arnaud S, Crofts AR, Davidson E, … Daldal F (1993) The bc1 complexes of Rhodobacter sphaeroides and Rhodobacter capsulatus. J Bioenerg Biomembr 25:195–209Google Scholar
  53. Ghirlanda G, Osyczka A, Liu W, Antolovich M, Smith KM, Dutton PL, Wand AJ, DeGrado WF (2004) De novo design of a D2-symmetrical protein that reproduces the diheme four-helix bundle in cytochrome bc1. J Am Chem Soc 126:8141–8147PubMedCrossRefGoogle Scholar
  54. Grudnik P, Bange G, Sinning I (2009) Protein targeting by the signal recognition particle. Biol Chem 390:775–782PubMedCrossRefGoogle Scholar
  55. Gruschke S, Kehrein K, Rompler K, Grone K, Israel L, Imhof A, Herrmann JM, Ott M (2011) Cbp3-Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly. J Cell Biol 193:1101–1114PubMedPubMedCentralCrossRefGoogle Scholar
  56. Gruschke S, Rompler K, Hildenbeutel M, Kehrein K, Kuhl I, Bonnefoy N, Ott M (2012) The Cbp3-Cbp6 complex coordinates cytochrome b synthesis with bc(1) complex assembly in yeast mitochondria. J Cell Biol 199:137–150PubMedPubMedCentralCrossRefGoogle Scholar
  57. Gu SQ, Peske F, Wieden HJ, Rodnina MV, Wintermeyer W (2003) The signal recognition particle binds to protein L23 at the peptide exit of the Escherichia coli ribosome. RNA 9:566–573PubMedPubMedCentralCrossRefGoogle Scholar
  58. Hamza I, Dailey HA (2012) One ring to rule them all: trafficking of heme and heme synthesis intermediates in the metazoans. Biochim Biophys Acta 1823:1617–1632PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hasan SS, Yamashita E, Cramer WA (2013) Transmembrane signaling and assembly of the cytochrome b6f-lipidic charge transfer complex. Biochim Biophys Acta - Bioenergetics 1827:1295–1308CrossRefGoogle Scholar
  60. Hell K, Neupert W, Stuart RA (2001) Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. Embo J 20:1281–1288PubMedPubMedCentralCrossRefGoogle Scholar
  61. Herrmann RG, Alt J, Schiller B, Widger WR, Cramer WA (1984) Nucleotide sequence of the gene for apocytochrome b-559 on the spinach plastid chromosome: implications for the structure of the membrane protein. FEBS Lett 176:239–244CrossRefGoogle Scholar
  62. Hizlan D, Robson A, Whitehouse S, Gold VA, Vonck J, Mills D, Kuhlbrandt W, Collinson I (2012) Structure of the SecY complex unlocked by a preprotein mimic. Cell Rep 1:21–28PubMedPubMedCentralCrossRefGoogle Scholar
  63. Huang SS, Koder RL, Lewis M, Wand AJ, Dutton PL (2004) The HP-1 maquette: from an apoprotein structure to a structured hemoprotein designed to promote redox-coupled proton exchange. Proc Natl Acad Sci USA 101:5536–5541PubMedPubMedCentralCrossRefGoogle Scholar
  64. Jormakka M, Byrne B, Iwata S (2003) Formate dehydrogenase–a versatile enzyme in changing environments. Curr Opin Struct Biol 13:418–423PubMedCrossRefGoogle Scholar
  65. Kalbfleisch T, Cambon A, Wattenberg BW (2007) A bioinformatics approach to identifying tail-anchored proteins in the human genome. Traffic 8:1687–1694PubMedCrossRefGoogle Scholar
  66. Keilin DD (1925) On cytochrome, a respiratory pigment, common to animals, yeast, and higher plants. In: Proceedings of the royal society of London Series B, containing papers of a biological character 98:312–339 (CR - Copyright © 1925 The Royal Society)Google Scholar
  67. Khalimonchuk O, Ostermann K, Rodel G (2005) Evidence for the association of yeast mitochondrial ribosomes with Cox11p, a protein required for the Cu(B) site formation of cytochrome c oxidase. Curr Genet 47:223–233PubMedCrossRefGoogle Scholar
  68. Kihara A, Akiyama Y, Ito K (1995) FtsH is required for proteolytic elimination of uncomplexed forms of SecY, an essential protein translocase subunit. Proc Natl Acad Sci USA 92:4532–4536PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kim HJ, Khalimonchuk O, Smith PM, Winge DR (2012) Structure, function, and assembly of heme centers in mitochondrial respiratory complexes. Biochim Biophys Acta 1823:1604–1616PubMedPubMedCentralCrossRefGoogle Scholar
  70. Klostermann E, Droste Gen Helling I, Carde JP, Schunemann D (2002) The thylakoid membrane protein ALB3 associates with the cpSecY-translocase in Arabidopsis thaliana. Biochem J 368:777–781PubMedPubMedCentralCrossRefGoogle Scholar
  71. Koch HG, Schneider D (2007) Assembly and stability of transmembrane cytochromes. Curr Chem Biol 1:59–74Google Scholar
  72. Koch HG, Hengelage T, Neumann-Haefelin C, MacFarlane J, Hoffschulte HK, Schimz KL, Mechler B, Muller M (1999) In vitro studies with purified components reveal signal recognition particle (SRP) and SecA/SecB as constituents of two independent protein-targeting pathways of Escherichia coli. Mol Biol Cell 10:2163–2173PubMedPubMedCentralCrossRefGoogle Scholar
  73. Koch HG, Moser M, Muller M (2003) Signal recognition particle-dependent protein targeting, universal to all kingdoms of life. Rev Physiol Biochem Pharmacol 146:55–94PubMedCrossRefGoogle Scholar
  74. Korendovych IV, Senes A, Kim YH, Lear JD, Fry HC, Therien MJ, Blasie JK, … Degrado WF (2010) De novo design and molecular assembly of a transmembrane diporphyrin-binding protein complex. J Am Chem Soc 132:15516–15518Google Scholar
  75. Kudva R, Denks K, Kuhn P, Vogt A, Muller M, Koch HG (2013) Protein translocation across the inner membrane of Gram-negative bacteria: the Sec and Tat dependent protein transport pathways. Res Microbiol 164:505–534PubMedCrossRefGoogle Scholar
  76. Kuhn P, Weiche B, Sturm L, Sommer E, Drepper F, Warscheid B, Sourjik V, Koch HG (2011) The bacterial SRP receptor, SecA and the ribosome use overlapping binding sites on the SecY translocon. Traffic 12:563–578PubMedCrossRefGoogle Scholar
  77. Kuhn P, Kudva R, Welte T, Sturm L, Koch H-G (2014) Targeting and integration of bacterial membrane proteins. In: Remaut H, Fronzes R (eds) Bacterial Membranes: Structural and Molecular Biology. Caister Academic Press, NorfolkGoogle Scholar
  78. Kuras R, Buschlen S, Wollman FA (1995) Maturation of pre-apocytochrome f in vivo. A site-directed mutagenesis study in Chlamydomonas reinhardtii. J Biol Chem 270:27797–27803PubMedCrossRefGoogle Scholar
  79. Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014PubMedCrossRefGoogle Scholar
  80. Lam VQ, Akopian D, Rome M, Henningsen D, Shan SO (2010) Lipid activation of the signal recognition particle receptor provides spatial coordination of protein targeting. J Cell Biol 190:623–635PubMedPubMedCentralCrossRefGoogle Scholar
  81. Lancaster CR (2002) Wolinella succinogenes quinol: fumarate reductase-2.2-A resolution crystal structure and the E-pathway hypothesis of coupled transmembrane proton and electron transfer. Biochim Biophys Acta 1565:215–231PubMedCrossRefGoogle Scholar
  82. Li W, Schulman S, Boyd D, Erlandson K, Beckwith J, Rapoport TA (2007) The plug domain of the SecY protein stabilizes the closed state of the translocation channel and maintains a membrane seal. Mol Cell 26:511–521PubMedCrossRefGoogle Scholar
  83. McRee DE, Jensen GM, Fitzgerald MM, Siegel HA, Goodin DB (1994) Construction of a bisaquo heme enzyme and binding by exogenous ligands. Proc Natl Acad Sci USA 91:12847–12851PubMedPubMedCentralCrossRefGoogle Scholar
  84. Mick DU, Fox TD, Rehling P (2011) Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation. Nat Rev Mol Cell Biol 12:14–20PubMedPubMedCentralCrossRefGoogle Scholar
  85. Mochizuki N, Tanaka R, Grimm B, Masuda T, Moulin M, Smith AG, Tanaka A, Terry MJ (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 15:488–498PubMedCrossRefGoogle Scholar
  86. Moulin M, Smith AG (2005) Regulation of tetrapyrrole biosynthesis in higher plants. Biochem Soc Trans 33:737–742PubMedCrossRefGoogle Scholar
  87. Muller M, Koch HG, Beck K, Schafer U (2001) Protein traffic in bacteria: multiple routes from the ribosome to and across the membrane. Prog Nucleic Acid Res Mol Biol 66:107–157PubMedCrossRefGoogle Scholar
  88. Nakamura H, Yamato I, Anraku Y, Lemieux L, Gennis RB (1990) Expression of cyoA and cyoB demonstrates that the CO-binding heme component of the Escherichia coli cytochrome o complex is in subunit I. J Biol Chem 265:11193–11197PubMedGoogle Scholar
  89. NCotIUoB (NC-IUB) (1992) Nomenclature of electron-transfer proteins. Recommendations 1989. J Biol Chem 267:665–677Google Scholar
  90. Negron C, Fufezan C, Koder RL (2009) Geometric constraints for porphyrin binding in helical protein binding sites. Proteins 74:400–416PubMedPubMedCentralCrossRefGoogle Scholar
  91. Nevo-Dinur K, Nussbaum-Shochat A, Ben-Yehuda S, Amster-Choder O (2011) Translation-independent localization of mRNA in E. coli. Science 331:1081–1084PubMedCrossRefGoogle Scholar
  92. Nikkila H, Gennis RB, Sligar SG (1991) Cloning and expression of the gene encoding the soluble cytochrome b562 of Escherichia coli. Eur J Biochem 202:309–313PubMedCrossRefGoogle Scholar
  93. Ott M, Herrmann JM (2010) Co-translational membrane insertion of mitochondrially encoded proteins. Biochim Biophys Acta 1803:767–775PubMedCrossRefGoogle Scholar
  94. Ott M, Prestele M, Bauerschmitt H, Funes S, Bonnefoy N, Herrmann JM (2006) Mba1, a membrane-associated ribosome receptor in mitochondria. Embo J 25:1603–1610PubMedPubMedCentralCrossRefGoogle Scholar
  95. Palmer T, Berks BC (2012) The twin-arginine translocation (Tat) protein export pathway. Nat Rev Microbiol 10:483–496PubMedGoogle Scholar
  96. Palmer SR, Crowley PJ, Oli MW, Ruelf MA, Michalek SM, Brady LJ (2012) YidC1 and YidC2 are functionally distinct proteins involved in protein secretion, biofilm formation and cariogenicity of Streptococcus mutans. Microbiology 158:1702–1712PubMedPubMedCentralCrossRefGoogle Scholar
  97. Palombo I, Daley DO (2012) Heme incorporation into the cytochrome bo3 occurs at a late stage of assembly. FEBS Lett 586:4197–4202PubMedCrossRefGoogle Scholar
  98. Park E, Rapoport TA (2012) Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu Rev Biophys 41:21–40PubMedCrossRefGoogle Scholar
  99. Park E, Menetret JF, Gumbart JC, Ludtke SJ, Li W, Whynot A, Rapoport TA, Akey CW (2013) Structure of the SecY channel during initiation of protein translocation. Nature 506:102–106PubMedPubMedCentralCrossRefGoogle Scholar
  100. Parlitz R, Eitan A, Stjepanovic G, Bahari L, Bange G, Bibi E, Sinning I (2007) Escherichia coli signal recognition particle receptor FtsY contains an essential and autonomous membrane-binding amphipathic helix. J Biol Chem 282:32176–32184PubMedCrossRefGoogle Scholar
  101. Pawlik G, Kulajta C, Sachelaru I, Schroder S, Waidner B, Hellwig P, Daldal F, Koch HG (2010) The putative assembly factor CcoH is stably associated with the cbb3-type cytochrome oxidase. J Bacteriol 192:6378–6389PubMedPubMedCentralCrossRefGoogle Scholar
  102. Pereira MM, Santana M, Teixeira M (2001) A novel scenario for the evolution of haem-copper oxygen reductases. Biochim Biophys Acta 1505:185–208PubMedCrossRefGoogle Scholar
  103. Pohlschroder M, Hartmann E, Hand NJ, Dilks K, Haddad A (2005) Diversity and evolution of protein translocation. Annu Rev Microbiol 59:91–111PubMedCrossRefGoogle Scholar
  104. Popot JL, Engelman DM (1990) Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29:4031–4037PubMedCrossRefGoogle Scholar
  105. Price CE, Driessen AJ (2010) Conserved negative charges in the transmembrane segments of subunit K of the NADH: ubiquinone oxidoreductase determine its dependence on YidC for membrane insertion. J Biol Chem 285:3575–3581PubMedCrossRefGoogle Scholar
  106. Prodöhl A, Volkmer T, Finger C, Schneider D (2005) Defining the structural basis for assembly of a transmembrane cytochrome. J Mol Biol 350:744–756PubMedCrossRefGoogle Scholar
  107. Prodöhl A, Weber M, Dreher C, Schneider D (2007) A mutational study of transmembrane helix-helix interactions. Biochimie 89:1433–1437PubMedCrossRefGoogle Scholar
  108. Rabu C, Schmid V, Schwappach B, High S (2009) Biogenesis of tail-anchored proteins: the beginning for the end? J Cell Sci 122:3605–3612PubMedPubMedCentralCrossRefGoogle Scholar
  109. Rapoport TA, Jungnickel B, Kutay U (1996) Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu Rev Biochem 65:271–303PubMedCrossRefGoogle Scholar
  110. Rau HK, Haehnel W (1998) Design, synthesis, and properties of a novel cytochrome b model. J Am Chem Soc 120:468–476CrossRefGoogle Scholar
  111. Reedy CJ, Gibney BR (2004) Heme protein assemblies. Chem Rev 104:617–649PubMedCrossRefGoogle Scholar
  112. Renthal R (2010) Helix insertion into bilayers and the evolution of membrane proteins. Cell Mol Life Sci 67:1077–1088PubMedCrossRefGoogle Scholar
  113. Robertson DE, Farid RS, Moser CC, Urbauer JL, Mulholland SE, Pidikiti R, Lear JD, … Dutton PL (1994) Design and synthesis of multi-haem proteins. Nature 368:425–432Google Scholar
  114. Saaf A, Monne M, de Gier JW, von Heijne G (1998) Membrane topology of the 60-kDa Oxa1p homologue from Escherichia coli. J Biol Chem 273:30415–30418PubMedCrossRefGoogle Scholar
  115. Sachelaru I, Petriman NA, Kudva R, Kuhn P, Welte T, Knapp B, Drepper F, … Koch HG (2013) YidC occupies the lateral gate of the SecYEG translocon and is sequentially displaced by a nascent membrane protein. J Biol Chem 288:16295–16307Google Scholar
  116. Saint-Marcoux D, Wollman F-A, de Vitry C (2009) Biogenesis of cytochrome b6 in photosynthetic membranes. J Cell Biol 185:1195–1207PubMedPubMedCentralCrossRefGoogle Scholar
  117. Samuelson JC, Chen M, Jiang F, Moller I, Wiedmann M, Kuhn A, Phillips GJ, Dalbey RE (2000) YidC mediates membrane protein insertion in bacteria. Nature 406:637–641PubMedCrossRefGoogle Scholar
  118. Saraste M, Castresana J (1994) Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett 341:1–4PubMedCrossRefGoogle Scholar
  119. Schneider S, Marles-Wright J, Sharp KH, Paoli M (2007) Diversity and conservation of interactions for binding heme in b-type heme proteins. Nat Prod Rep 24:621–630PubMedCrossRefGoogle Scholar
  120. Shepherd M, Heath MD, Poole RK (2007) NikA binds heme: a new role for an Escherichia coli periplasmic nickel-binding protein. Biochemistry 46:5030–5037PubMedCrossRefGoogle Scholar
  121. Shinde S, Cordova JM, Woodrum BW, Ghirlanda G (2012) Modulation of function in a minimalist heme-binding membrane protein. J Biol Inorg Chem 17:557–564PubMedCrossRefGoogle Scholar
  122. Shinopoulos KE, Brudvig GW (2012) Cytochrome b559 and cyclic electron transfer within photosystem II. Biochim Biophys Acta 1817:66–75PubMedCrossRefGoogle Scholar
  123. Sinning I, Bange G, Wild K (2011) It takes two to Get3. Structure 19:1353–1355PubMedCrossRefGoogle Scholar
  124. Smith LJ, Kahraman A, Thornton JM (2010) Heme proteins—diversity in structural characteristics, function, and folding. Proteins 78:2349–2368PubMedCrossRefGoogle Scholar
  125. Stenberg F, von Heijne G, Daley DO (2007) Assembly of the cytochrome bo3 complex. J Mol Biol 371:765–773PubMedCrossRefGoogle Scholar
  126. Stjepanovic G, Kapp K, Bange G, Graf C, Parlitz R, Wild K, Mayer MP, Sinning I (2011) Lipids trigger a conformational switch that regulates signal recognition particle (SRP)-mediated protein targeting. J Biol Chem 286:23489–23497PubMedPubMedCentralCrossRefGoogle Scholar
  127. Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426:413–418PubMedCrossRefGoogle Scholar
  128. Sturm A, Schierhorn A, Lindenstrauss U, Lilie H, Bruser T (2006) YcdB from Escherichia coli reveals a novel class of Tat-dependently translocated hemoproteins. J Biol Chem 281:13972–13978PubMedCrossRefGoogle Scholar
  129. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346PubMedCrossRefGoogle Scholar
  130. Thöny-Meyer L (1997) Biogenesis of respiratory cytochromes in bacteria. Microbiol Mol Biol Rev 61:337–376PubMedPubMedCentralGoogle Scholar
  131. Tome L, Schaetzel C, Dreher C, Schneider D (2013) Fe- but not Mg-protophorphyrin IX binds to a transmembrane b-type cytochrome. Mol Membr Biol 31:37–45PubMedCrossRefGoogle Scholar
  132. Tottey S, Waldron KJ, Firbank SJ, Reale B, Bessant C, Sato K, Cheek TR, … Robinson NJ (2008) Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature 455:1138–1142Google Scholar
  133. Trager C, Rosenblad MA, Ziehe D, Garcia-Petit C, Schrader L, Kock K, Richter CV, … Schunemann D (2012) Evolution from the prokaryotic to the higher plant chloroplast signal recognition particle: the signal recognition particle RNA is conserved in plastids of a wide range of photosynthetic organisms. Plant Cell 24:4819–4836Google Scholar
  134. Valkova-Valchanova MB, Saribas AS, Gibney BR, Dutton PL, Daldal F (1998) Isolation and characterization of a two-subunit cytochrome b-c1 subcomplex from Rhodobacter capsulatus and reconstitution of its ubihydroquinone oxidation (Qo) site with purified Fe-S protein subunit. Biochemistry 37:16242–16251PubMedCrossRefGoogle Scholar
  135. Van den Berg B, Clemons WM Jr, Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA (2004) X-ray structure of a protein-conducting channel. Nature 427:36–44PubMedCrossRefGoogle Scholar
  136. Volkmer T, Becker C, Prodöhl A, Finger C, Schneider D (2006) Assembly of a transmembrane b-type cytochrome is mainly driven by transmembrane helix interactions. Biochim Biophys Acta 1758:1815–1822PubMedCrossRefGoogle Scholar
  137. Weber M, Prodohl A, Dreher C, Becker C, Underhaug J, Svane AS, Malmendal A, … Schneider D (2011) SDS-facilitated in vitro formation of a transmembrane b-type cytochrome is mediated by changes in local pH. J Mol Biol 407:594–606Google Scholar
  138. Weber M, Tome L, Otzen D, Schneider D (2012) A Ser residue influences the structure and stability of a Pro-kinked transmembrane helix dimer. Biochim Biophys Acta - Biomembr 1818:2103–2107CrossRefGoogle Scholar
  139. Weiche B, Bürk J, Angelini S, Schiltz E, Thumfart JO, Koch H-G (2008) A cleavable N-terminal membrane anchor is involved in membrane binding of the Escherichia coli SRP receptor. J Mol Biol 377:761–773PubMedCrossRefGoogle Scholar
  140. Welte T, Kudva R, Kuhn P, Sturm L, Braig D, Müller M, Warscheid B, … Koch H-G (2012) Promiscuous targeting of polytopic membrane proteins to SecYEG or YidC by the Escherichia coli signal recognition particle. Mol Biol Cell 23:464–479Google Scholar
  141. Widger WR, Cramer WA, Herrmann RG, Trebst A (1984) Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b6-f complex: position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci USA 81:674–678PubMedPubMedCentralCrossRefGoogle Scholar
  142. Widger WR, Cramer WA, Hermodson M, Herrmann RG (1985) Evidence for a hetero-oligomeric structure of the chloroplast cytochrome b-559. FEBS Lett 191:186–190CrossRefGoogle Scholar
  143. Ye S, Discher BM, Strzalka J, Xu T, Wu SP, Noy D, Kuzmenko I, … Blasie JK (2005) Amphiphilic four-helix bundle peptides designed for light-induced electron transfer across a soft interface. Nano Lett 5:1658–1667Google Scholar
  144. Yi L, Jiang F, Chen M, Cain B, Bolhuis A, Dalbey RE (2003) YidC is strictly required for membrane insertion of subunits a and c of the F1F0 ATP synthase and SecE of the SecYEG translocase. Biochemistry 42:10537–10544PubMedCrossRefGoogle Scholar
  145. Zhang D, Shan SO (2012) Translation elongation regulates substrate selection by the signal recognition particle. J Biol Chem 287:7652–7660PubMedPubMedCentralCrossRefGoogle Scholar
  146. Zhu L, Wasey A, White SH, Dalbey RE (2013) Charge composition features of model single-span membrane proteins that determine selection of YidC and SecYEG translocase pathways in Escherichia coli. J Biol Chem 288:7704–7716PubMedPubMedCentralCrossRefGoogle Scholar
  147. Zickermann V, Angerer H, Ding MG, Nubel E, Brandt U (2010) Small single transmembrane domain (STMD) proteins organize the hydrophobic subunits of large membrane protein complexes. FEBS Lett 584:2516–2525PubMedCrossRefGoogle Scholar
  148. Zimmermann R, Eyrisch S, Ahmad M, Helms V (2011) Protein translocation across the ER membrane. Biochim Biophys Acta 1808:912–924PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Institut für Biochemie und MolekularbiologieZBMZ, Albert-Ludwigs-Universität FreiburgFreiburgGermany
  2. 2.Institut für Pharmazie und BiochemieJohannes Gutenberg-Universität MainzMainzGermany

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