Skip to main content
SpringerLink
Log in

Assembly of Transmembrane b-Type Cytochromes and Cytochrome Complexes

  • Chapter
  • First Online:
Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 41))

Summary

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

b559 :

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

GET:

Guided entry of tail-anchored proteins

RNC:

Ribosome-nascent-chain complex

SRP:

Signal recognition particle

SR:

SRP-receptor

TM:

Transmembrane

TIM:

Translocase of the inner mitochondrial membrane

TOM:

Translocase of the outer mitochondrial membrane

References

  • 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. 7:910–917

    Google Scholar 

  • Akdogan Y, Anbazhagan V, Hinderberger D, Schneider D (2012) Heme binding constricts the conformational dynamics of the cytochrome b(559)’ heme binding cavity. Biochemistry 51:7149–7156

    Article  CAS  PubMed  Google Scholar 

  • 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 12:937–946

    Article  CAS  PubMed  Google Scholar 

  • Angelini S, Deitermann S, Koch HG (2005) FtsY, the bacterial signal-recognition particle receptor, interacts functionally and physically with the SecYEG translocon. EMBO Rep 6:476–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 174:715–724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:71–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 24:3638–3645

    Article  CAS  PubMed  Google Scholar 

  • Bange G, Sinning I (2013) SIMIBI twins in protein targeting and localization. Nat Struct Mol Biol 20:776–780

    Article  CAS  PubMed  Google Scholar 

  • Barker PD, Ferguson SJ (1999) Still a puzzle: why is haem covalently attached in c-type cytochromes? Structure 7:R281–R290

    Article  CAS  PubMed  Google Scholar 

  • Barrick D (1994) Replacement of the proximal ligand of sperm whale myoglobin with free imidazole in the mutant His-93 → Gly. Biochemistry 33:6546–6554

    Article  CAS  PubMed  Google Scholar 

  • 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 21:1937–1944

    Google Scholar 

  • 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 2:709–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker T, Bottinger L, Pfanner N (2012) Mitochondrial protein import: from transport pathways to an integrated network. Trends Biochem Sci 37:85–91

    Article  CAS  PubMed  Google Scholar 

  • Beha D, Deitermann S, Muller M, Koch HG (2003) Export of beta-lactamase is independent of the signal recognition particle. J Biol Chem 278:22161–22167

    Article  CAS  PubMed  Google Scholar 

  • 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 278:8219–8223

    Article  CAS  PubMed  Google Scholar 

  • Bibi E (2011) Early targeting events during membrane protein biogenesis in Escherichia coli. Biochim Biophys Acta 1808:841–850

    Article  CAS  PubMed  Google Scholar 

  • Borgese N, Righi M (2010) Remote origins of tail-anchored proteins. Traffic 11:877–885

    Article  CAS  PubMed  Google Scholar 

  • Borisov VB, Gennis RB, Hemp J, Verkhovsky MI (2011) The cytochrome bd respiratory oxygen reductases. Biochim Biophys Acta 1807:1398–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 15:494–499

    Article  CAS  PubMed  Google Scholar 

  • 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 390:401–413

    Article  CAS  PubMed  Google Scholar 

  • 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 22:2309–2323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 230:1118–1124

    Article  CAS  PubMed  Google Scholar 

  • 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 1275:61–69

    Article  PubMed  Google Scholar 

  • 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 272:21892–21900

    Article  CAS  PubMed  Google Scholar 

  • 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 383:1565–1572

    Article  CAS  PubMed  Google Scholar 

  • 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 129:512–518

    Article  CAS  PubMed  Google Scholar 

  • 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 85:133–143

    Article  CAS  PubMed  Google Scholar 

  • Craney A, Tahlan K, Andrews D, Nodwell J (2011) Bacterial transmembrane proteins that lack N-terminal signal sequences. PLoS ONE 6:e19421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 274:20068–20070

    Article  CAS  PubMed  Google Scholar 

  • 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 195:1–12

    Article  CAS  PubMed  Google Scholar 

  • 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 31:3351–3358

    Article  CAS  PubMed  Google Scholar 

  • 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 280:39077–39085

    Article  CAS  PubMed  Google Scholar 

  • Discher BM, Koder RL, Moser CC, Dutton PL (2003) Hydrophilic to amphiphilic design in redox protein maquettes. Curr Opin Chem Biol 7:741–748

    Article  CAS  PubMed  Google Scholar 

  • 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 44:12329–12343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 581:2647–2651

    Article  CAS  PubMed  Google Scholar 

  • Dreher C, Prodöhl A, Hielscher R, Hellwig P, Schneider D (2008) Multiple step assembly of the transmembrane cytochrome b6. J Mol Biol 382:1057–1065

    Article  CAS  PubMed  Google Scholar 

  • 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 42:517–526

    Article  CAS  PubMed  Google Scholar 

  • 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 281:12248–12252

    Article  PubMed  CAS  Google Scholar 

  • du Plessis DJ, Berrelkamp G, Nouwen N, Driessen AJ (2009) The lateral gate of SecYEG opens during protein translocation. J Biol Chem 284:15805–15814

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • du Plessis DJF, Nouwen N, Driessen AJM (2011) The sec translocase. Biochim Biophys Acta 1808:851–865

    Article  PubMed  CAS  Google Scholar 

  • Eitan A, Bibi E (2004) The core Escherichia coli signal recognition particle receptor contains only the N and G domains of FtsY. J Bacteriol 186:2492–2494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1817:898–910

    Article  CAS  PubMed  Google Scholar 

  • 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 1143:243–271

    Article  CAS  PubMed  Google Scholar 

  • 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 365:995–1004

    Article  CAS  PubMed  Google Scholar 

  • Ferguson SJ, Stevens JM, Allen JWA, Robertson IB (2008) Cytochrome c assembly: a tale of ever increasing variation and mystery? Biochim Biophys Acta - Bioenergetics 1777:980–984

    Article  CAS  Google Scholar 

  • Fontaine F, Fuchs RT, Storz G (2011) Membrane localization of small proteins in Escherichia coli. J Biol Chem 286:32464–32474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 442:75–78

    Article  CAS  PubMed  Google Scholar 

  • 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 18:614–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 392:13–19

    Article  CAS  PubMed  Google Scholar 

  • 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 280:904–915

    Google Scholar 

  • Garcia-Horsman JA, Barquera B, Rumbley J, Ma J, Gennis RB (1994) The superfamily of heme-copper respiratory oxidases. J Bacteriol 176:5587–5600

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 25:195–209

    Google Scholar 

  • 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 126:8141–8147

    Article  CAS  PubMed  Google Scholar 

  • Grudnik P, Bange G, Sinning I (2009) Protein targeting by the signal recognition particle. Biol Chem 390:775–782

    Article  CAS  PubMed  Google Scholar 

  • 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 193:1101–1114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 199:137–150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:566–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamza I, Dailey HA (2012) One ring to rule them all: trafficking of heme and heme synthesis intermediates in the metazoans. Biochim Biophys Acta 1823:1617–1632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan SS, Yamashita E, Cramer WA (2013) Transmembrane signaling and assembly of the cytochrome b6f-lipidic charge transfer complex. Biochim Biophys Acta - Bioenergetics 1827:1295–1308

    Article  CAS  Google Scholar 

  • Hell K, Neupert W, Stuart RA (2001) Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. Embo J 20:1281–1288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 176:239–244

    Article  CAS  Google Scholar 

  • 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 1:21–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 101:5536–5541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jormakka M, Byrne B, Iwata S (2003) Formate dehydrogenase–a versatile enzyme in changing environments. Curr Opin Struct Biol 13:418–423

    Article  CAS  PubMed  Google Scholar 

  • Kalbfleisch T, Cambon A, Wattenberg BW (2007) A bioinformatics approach to identifying tail-anchored proteins in the human genome. Traffic 8:1687–1694

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 47:223–233

    Article  CAS  PubMed  Google Scholar 

  • 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 92:4532–4536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim HJ, Khalimonchuk O, Smith PM, Winge DR (2012) Structure, function, and assembly of heme centers in mitochondrial respiratory complexes. Biochim Biophys Acta 1823:1604–1616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 368:777–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koch HG, Schneider D (2007) Assembly and stability of transmembrane cytochromes. Curr Chem Biol 1:59–74

    CAS  Google Scholar 

  • 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 10:2163–2173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koch HG, Moser M, Muller M (2003) Signal recognition particle-dependent protein targeting, universal to all kingdoms of life. Rev Physiol Biochem Pharmacol 146:55–94

    Article  CAS  PubMed  Google Scholar 

  • 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 132:15516–15518

    Google Scholar 

  • 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 164:505–534

    Article  CAS  PubMed  Google Scholar 

  • 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 12:563–578

    Article  CAS  PubMed  Google Scholar 

  • 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, Norfolk

    Google Scholar 

  • 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 270:27797–27803

    Article  CAS  PubMed  Google Scholar 

  • Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014

    Article  CAS  PubMed  Google Scholar 

  • 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 190:623–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1565:215–231

    Article  CAS  PubMed  Google Scholar 

  • 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 26:511–521

    Article  CAS  PubMed  Google Scholar 

  • 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 91:12847–12851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mick DU, Fox TD, Rehling P (2011) Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation. Nat Rev Mol Cell Biol 12:14–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 15:488–498

    Article  CAS  PubMed  Google Scholar 

  • Moulin M, Smith AG (2005) Regulation of tetrapyrrole biosynthesis in higher plants. Biochem Soc Trans 33:737–742

    Article  CAS  PubMed  Google Scholar 

  • 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 66:107–157

    Article  CAS  PubMed  Google Scholar 

  • 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 265:11193–11197

    CAS  PubMed  Google Scholar 

  • NCotIUoB (NC-IUB) (1992) Nomenclature of electron-transfer proteins. Recommendations 1989. J Biol Chem 267:665–677

    Google Scholar 

  • Negron C, Fufezan C, Koder RL (2009) Geometric constraints for porphyrin binding in helical protein binding sites. Proteins 74:400–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nevo-Dinur K, Nussbaum-Shochat A, Ben-Yehuda S, Amster-Choder O (2011) Translation-independent localization of mRNA in E. coli. Science 331:1081–1084

    Article  CAS  PubMed  Google Scholar 

  • Nikkila H, Gennis RB, Sligar SG (1991) Cloning and expression of the gene encoding the soluble cytochrome b562 of Escherichia coli. Eur J Biochem 202:309–313

    Article  CAS  PubMed  Google Scholar 

  • Ott M, Herrmann JM (2010) Co-translational membrane insertion of mitochondrially encoded proteins. Biochim Biophys Acta 1803:767–775

    Article  CAS  PubMed  Google Scholar 

  • Ott M, Prestele M, Bauerschmitt H, Funes S, Bonnefoy N, Herrmann JM (2006) Mba1, a membrane-associated ribosome receptor in mitochondria. Embo J 25:1603–1610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer T, Berks BC (2012) The twin-arginine translocation (Tat) protein export pathway. Nat Rev Microbiol 10:483–496

    CAS  PubMed  Google Scholar 

  • 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 158:1702–1712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palombo I, Daley DO (2012) Heme incorporation into the cytochrome bo3 occurs at a late stage of assembly. FEBS Lett 586:4197–4202

    Article  CAS  PubMed  Google Scholar 

  • Park E, Rapoport TA (2012) Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu Rev Biophys 41:21–40

    Article  CAS  PubMed  Google Scholar 

  • 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 506:102–106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 282:32176–32184

    Article  CAS  PubMed  Google Scholar 

  • 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 192:6378–6389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira MM, Santana M, Teixeira M (2001) A novel scenario for the evolution of haem-copper oxygen reductases. Biochim Biophys Acta 1505:185–208

    Article  CAS  PubMed  Google Scholar 

  • Pohlschroder M, Hartmann E, Hand NJ, Dilks K, Haddad A (2005) Diversity and evolution of protein translocation. Annu Rev Microbiol 59:91–111

    Article  CAS  PubMed  Google Scholar 

  • Popot JL, Engelman DM (1990) Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29:4031–4037

    Article  CAS  PubMed  Google Scholar 

  • 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 285:3575–3581

    Article  CAS  PubMed  Google Scholar 

  • Prodöhl A, Volkmer T, Finger C, Schneider D (2005) Defining the structural basis for assembly of a transmembrane cytochrome. J Mol Biol 350:744–756

    Article  PubMed  CAS  Google Scholar 

  • Prodöhl A, Weber M, Dreher C, Schneider D (2007) A mutational study of transmembrane helix-helix interactions. Biochimie 89:1433–1437

    Article  PubMed  CAS  Google Scholar 

  • Rabu C, Schmid V, Schwappach B, High S (2009) Biogenesis of tail-anchored proteins: the beginning for the end? J Cell Sci 122:3605–3612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rapoport TA, Jungnickel B, Kutay U (1996) Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu Rev Biochem 65:271–303

    Article  CAS  PubMed  Google Scholar 

  • Rau HK, Haehnel W (1998) Design, synthesis, and properties of a novel cytochrome b model. J Am Chem Soc 120:468–476

    Article  CAS  Google Scholar 

  • Reedy CJ, Gibney BR (2004) Heme protein assemblies. Chem Rev 104:617–649

    Article  CAS  PubMed  Google Scholar 

  • Renthal R (2010) Helix insertion into bilayers and the evolution of membrane proteins. Cell Mol Life Sci 67:1077–1088

    Article  CAS  PubMed  Google Scholar 

  • 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 368:425–432

    Google Scholar 

  • 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 273:30415–30418

    Article  CAS  PubMed  Google Scholar 

  • 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 288:16295–16307

    Google Scholar 

  • Saint-Marcoux D, Wollman F-A, de Vitry C (2009) Biogenesis of cytochrome b6 in photosynthetic membranes. J Cell Biol 185:1195–1207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 406:637–641

    Article  CAS  PubMed  Google Scholar 

  • Saraste M, Castresana J (1994) Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett 341:1–4

    Article  CAS  PubMed  Google Scholar 

  • 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 24:621–630

    Article  CAS  PubMed  Google Scholar 

  • Shepherd M, Heath MD, Poole RK (2007) NikA binds heme: a new role for an Escherichia coli periplasmic nickel-binding protein. Biochemistry 46:5030–5037

    Article  CAS  PubMed  Google Scholar 

  • Shinde S, Cordova JM, Woodrum BW, Ghirlanda G (2012) Modulation of function in a minimalist heme-binding membrane protein. J Biol Inorg Chem 17:557–564

    Article  CAS  PubMed  Google Scholar 

  • Shinopoulos KE, Brudvig GW (2012) Cytochrome b559 and cyclic electron transfer within photosystem II. Biochim Biophys Acta 1817:66–75

    Article  CAS  PubMed  Google Scholar 

  • Sinning I, Bange G, Wild K (2011) It takes two to Get3. Structure 19:1353–1355

    Article  CAS  PubMed  Google Scholar 

  • Smith LJ, Kahraman A, Thornton JM (2010) Heme proteins—diversity in structural characteristics, function, and folding. Proteins 78:2349–2368

    Article  CAS  PubMed  Google Scholar 

  • Stenberg F, von Heijne G, Daley DO (2007) Assembly of the cytochrome bo3 complex. J Mol Biol 371:765–773

    Article  CAS  PubMed  Google Scholar 

  • 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 286:23489–23497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426:413–418

    Article  CAS  PubMed  Google Scholar 

  • 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 281:13972–13978

    Article  CAS  PubMed  Google Scholar 

  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346

    Article  CAS  PubMed  Google Scholar 

  • Thöny-Meyer L (1997) Biogenesis of respiratory cytochromes in bacteria. Microbiol Mol Biol Rev 61:337–376

    PubMed  PubMed Central  Google Scholar 

  • 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 31:37–45

    Article  PubMed  CAS  Google Scholar 

  • 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 455:1138–1142

    Google Scholar 

  • 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 24:4819–4836

    Google Scholar 

  • 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 37:16242–16251

    Article  CAS  PubMed  Google Scholar 

  • 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 427:36–44

    Article  PubMed  CAS  Google Scholar 

  • 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 1758:1815–1822

    Article  CAS  PubMed  Google Scholar 

  • 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 407:594–606

    Google Scholar 

  • 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 1818:2103–2107

    Article  CAS  Google Scholar 

  • 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 377:761–773

    Article  CAS  PubMed  Google Scholar 

  • 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 23:464–479

    Google Scholar 

  • 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 81:674–678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Widger WR, Cramer WA, Hermodson M, Herrmann RG (1985) Evidence for a hetero-oligomeric structure of the chloroplast cytochrome b-559. FEBS Lett 191:186–190

    Article  CAS  Google Scholar 

  • 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 5:1658–1667

    Google Scholar 

  • 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 42:10537–10544

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Shan SO (2012) Translation elongation regulates substrate selection by the signal recognition particle. J Biol Chem 287:7652–7660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 288:7704–7716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 584:2516–2525

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann R, Eyrisch S, Ahmad M, Helms V (2011) Protein translocation across the ER membrane. Biochim Biophys Acta 1808:912–924

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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

Author information

Authors and Affiliations

  1. Institut für Biochemie und Molekularbiologie, ZBMZ, Albert-Ludwigs-Universität Freiburg, 79104, Freiburg, Germany

    Hans-Georg Koch

  2. Institut für Pharmazie und Biochemie, Johannes Gutenberg-Universität Mainz, 55128, Mainz, Germany

    Dirk Schneider

Authors
  1. Hans-Georg Koch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dirk Schneider
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hans-Georg Koch or Dirk Schneider .

Editor information

Editors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, Indiana, USA

    William A. Cramer

  2. Department of Biology, University of Wisconsin-Oshkosh, Oshkosh, Wisconsin, USA

    Toivo Kallas

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Koch, HG., Schneider, D. (2016). Assembly of Transmembrane b-Type Cytochromes and Cytochrome Complexes. In: Cramer, W., Kallas, T. (eds) Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling. Advances in Photosynthesis and Respiration, vol 41. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7481-9_28

Download citation

Publish with us

Policies and ethics

Search

Navigation