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Biogenesis of bacterial inner-membrane proteins

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Abstract

All cells must traffic proteins into and across their membranes. In bacteria, several pathways have evolved to enable protein transfer across the inner membrane, the periplasm, and the outer membrane. The major route of protein translocation in and across the cytoplasmic membrane is the general secretion pathway (Sec-pathway). The biogenesis of membrane proteins not only requires protein translocation but also coordinated targeting to the membrane beforehand and folding and assembly into their protein complexes afterwards to function properly in the cell. All these processes are responsible for the biogenesis of membrane proteins that mediate essential functions of the cell such as selective transport, energy conversion, cell division, extracellular signal sensing, and motility. This review will highlight the most recent developments on the structure and function of bacterial membrane proteins, focusing on the journey that integral membrane proteins take to find their final destination in the inner membrane.

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References

  1. Kramer G, Rauch T, Rist W, Vorderwülbecke S, Patzelt H, Schulze-Specking A, Ban N, Deuerling E, Bukau B (2002) L23 protein functions as a chaperone docking site on the ribosome. Nature 419:171–174

    CAS  PubMed  Google Scholar 

  2. Kaiser CM, Chang HC, Agashe VR, Lakshmipathy SK, Etchells SA, Hayer-Hartl M, Hartl FU, Barral JM (2006) Real-time observation of trigger factor function on translating ribosomes. Nature 444:455–460

    CAS  PubMed  Google Scholar 

  3. Rutkowska A, Mayer MP, Hoffmann A, Merz F, Zachmann-Brand B, Schaffitzel C, Ban N, Deuerling E, Bukau B (2008) Dynamics of trigger factor interaction with translating ribosomes. J Biol Chem 283:4124–4132

    CAS  PubMed  Google Scholar 

  4. Ferbitz L, Maier T, Patzelt H, Bukau B, Deuerling E, Ban N (2004) Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 431:590–596

    CAS  PubMed  Google Scholar 

  5. Bukau B, Deuerling E, Pfund C, Craig EA (2000) Getting newly synthesized proteins into shape. Cell 101:119–122

    CAS  PubMed  Google Scholar 

  6. Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603–647

    CAS  PubMed  Google Scholar 

  7. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858

    CAS  PubMed  Google Scholar 

  8. Vorderwülbecke S, Kramer G, Merz F, Kurz TA, Rauch T, Zachmann-Brand B, Bukau B, Deuerling E (2004) Low temperature or GroEL/ES overproduction permits growth of Escherichia coli cells lacking trigger factor and DnaK. FEBS Lett 559:181–187

    PubMed  Google Scholar 

  9. Lee HC, Bernstein HD (2002) Trigger factor retards protein export in Escherichia coli. J Biol Chem 277:43527–43535

    CAS  PubMed  Google Scholar 

  10. Wild J, Altman E, Yura T, Gross CA (1992) DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev 6:1165–1172

    CAS  PubMed  Google Scholar 

  11. Wild J, Rossmeissl P, Walter WA, Gross CA (1996) Involvement of the DnaK–DnaJ–GrpE chaperone team in protein secretion in Escherichia coli. J Bacteriol 178:3608–3613

    CAS  PubMed  Google Scholar 

  12. Wild J, Walter WA, Gross CA, Altman E (1993) Accumulation of secretory protein precursors in Escherichia coli induces the heat shock response. J Bacteriol 175:3992–3997

    CAS  PubMed  Google Scholar 

  13. Müller JP (1996) Influence of impaired chaperone or secretion function on SecB production in Escherichia coli. J Bacteriol 178:6097–6104

    PubMed  Google Scholar 

  14. 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

    CAS  PubMed  Google Scholar 

  15. Ullers RS, Houben EN, Raine A, ten Hagen-Jongman CM, Ehrenberg M, Brunner J, Oudega B, Harms N, Luirink J (2003) Interplay of signal recognition particle and trigger factor at L23 near the nascent chain exit site on the Escherichia coli ribosome. J Cell Biol 161:679–684

    CAS  PubMed  Google Scholar 

  16. Buskiewicz I, Deuerling E, Gu SQ, Jöckel J, Rodnina MV, Bukau B, Wintermeyer W (2004) Trigger factor binds to ribosome-signal-recognition particle (SRP) complexes and is excluded by binding of the SRP receptor. Proc Natl Acad Sci USA 101:7902–7906

    CAS  PubMed  Google Scholar 

  17. Raine A, Ivanova N, Wikberg JE, Ehrenberg M (2004) Simultaneous binding of trigger factor and signal recognition particle to the E. coli ribosome. Biochimie 86:495–500

    CAS  PubMed  Google Scholar 

  18. Randall LL, Hardy SJ, Topping TB, Smith VF, Bruce JE, Smith RD (1998) The interaction between the chaperone SecB and its ligands: evidence for multiple subsites for binding. Protein Sci 7:2384–2390

    CAS  PubMed  Google Scholar 

  19. Driessen AJ, Manting EH, van der Does C (2001) The structural basis of protein targeting and translocation in bacteria. Nat Struct Biol 8:492–498

    CAS  PubMed  Google Scholar 

  20. Fekkes P, de Wit JG, van der Wolk JP, Kimsey HH, Kumamoto CA, Driessen AJ (1998) Preprotein transfer to the Escherichia coli translocase requires the co-operative binding of SecB and the signal sequence to SecA. Mol Microbiol 29:1179–1190

    CAS  PubMed  Google Scholar 

  21. Zhou J, Xu Z (2003) Structural determinants of SecB recognition by SecA in bacterial protein translocation. Nat Struct Biol 10:942–947

    CAS  PubMed  Google Scholar 

  22. Fekkes P, van der Does C, Driessen AJM (1997) The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of precursor protein translocation. EMBO J 16:6105–6113

    CAS  PubMed  Google Scholar 

  23. Vrontou E, Economou A (2004) Structure and function of SecA, the preprotein translocase nanomotor. Biochim Biophys Acta 1694:67–80

    CAS  PubMed  Google Scholar 

  24. Papanikou E, Karamanou S, Economou A (2007) Bacterial protein secretion through the translocase nanomachine. Nat Rev Microbiol 5:839–851

    CAS  PubMed  Google Scholar 

  25. von Heijne G (1990) Protein targeting signals. Curr Opin Cell Biol 2:604–608

    Google Scholar 

  26. Herskovits AA, Bochkareva ES, Bibi E (2000) New prospects in studying the bacterial signal recognition particle pathway. Mol Microbiol 38:927–939

    CAS  PubMed  Google Scholar 

  27. Valent QA, Kendall DA, High S, Kusters R, Oudega B, Luirink J (1995) Early events in preprotein recognition in E. coli: interaction of SRP and trigger factor with nascent polypeptides. EMBO J 14:5494–5505

    CAS  PubMed  Google Scholar 

  28. Valent QA, de Gier J-WL, von Heijne G, Kendall DA, ten Hagen-Jongman CM, Oudega B, Luirink J (1997) Nascent membrane and presecretory proteins synthesized in Escherichia coli associate with signal recognition particle and trigger factor. Mol Microbiol 25:53–64

    CAS  PubMed  Google Scholar 

  29. Valent QA, Scotti PA, High S, de Gier J-WL, von Heijne G, Lentzen G, Wintermeyer W, Oudega B, Luirink J (1998) The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J 17:2504–2512

    CAS  PubMed  Google Scholar 

  30. Lee HC, Bernstein HD (2001) The targeting pathway of Escherichia coli presecretory and integral membrane proteins is specified by the hydrophobicity of the targeting signal. Proc Natl Acad Sci USA 98:3471–3476

    CAS  PubMed  Google Scholar 

  31. Peterson JH, Woolhead CA, Bernstein HD (2003) Basic amino acids in a distinct subset of signal peptides promote interaction with the signal recognition particle. J Biol Chem 278:46155–46162

    CAS  PubMed  Google Scholar 

  32. Maier KS, Hubich S, Liebhart H, Krauss S, Kuhn A, Facey SJ (2008) An amphiphilic region in the cytoplasmic domain of KdpD is recognized by the signal recognition particle and targeted to the Escherichia coli membrane. Mol Microbiol 68:1471–1484

    CAS  PubMed  Google Scholar 

  33. de Gier J-WL, Mansournia P, Valent QA, Phillips GJ, Luirink J, von Heijne G (1996) Assembly of a cytoplasmic membrane protein in Escherichia coli is dependent on the signal recognition particle. FEBS Lett 399:307–309

    PubMed  Google Scholar 

  34. van der Laan M, Nouwen N, Driessen AJM (2004) SecYEG proteoliposomes catalyze the Δψ-dependent membrane insertion of FtsQ. J Biol Chem 279:1659–1664

    PubMed  Google Scholar 

  35. Koch HG, Hengelage T, Neumann-Haefelin C, MacFarlane J, Hoffschulte HK, Schimz KL, Mechler B, Müller 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

    CAS  PubMed  Google Scholar 

  36. Seluanov A, Bibi E (1997) FtsY, the prokaryotic signal recognition particle receptor homologue, is essential for biogenesis of membrane proteins. J Biol Chem 272:2053–2055

    CAS  PubMed  Google Scholar 

  37. Wagner S, Pop O, Haan GJ, Baars L, Koningstein G, Klepsch MM, Genevaux P, Luirink J, de Gier J-W (2008) Biogenesis of MalF and the MalFGK2 maltose transport complex in Escherichia coli requires YidC. J Biol Chem 283:17881–17890

    CAS  PubMed  Google Scholar 

  38. Keenan RJ, Freymann DM, Stroud RM, Walter P (2001) The signal recognition particle. Annu Rev Biochem 70:755–775

    CAS  PubMed  Google Scholar 

  39. Luirink J, Sinning I (2004) SRP-mediated protein targeting: structure and function revisited. Biochim Biophys Acta 1694:17–35

    CAS  PubMed  Google Scholar 

  40. Wild K, Rosendal KR, Sinning I (2004) A structural step into the SRP cycle. Mol Microbiol 53:357–363

    CAS  PubMed  Google Scholar 

  41. Connolly T, Rapiejko P, Gilmore R (1991) Requirement of GTP hydrolysis for dissociation of the signal recognition particle from its receptor. Science 252:1171–1173

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  43. Bange G, Wild K, Sinning I (2007) Protein translocation: checkpoint role for SRP GTPase activation. Curr Biol 17:R980–R982

    CAS  PubMed  Google Scholar 

  44. Shan SO, Chandrasekar S, Walter P (2007) Conformational changes in the GTPase modules of the signal reception particle and its receptor drive initiation of protein translocation. J Cell Biol 178:611–620

    CAS  PubMed  Google Scholar 

  45. Luirink J, ten Hagen-Jongman CM, van der Weijden CC, Oudega B, High S, Dobberstein B, Kusters R (1994) An alternative protein targeting pathway in Escherichia coli: studies on the role of FtsY. EMBO J 13:2289–2296

    CAS  PubMed  Google Scholar 

  46. Bahari L, Parlitz R, Eitan A, Stjepanovic G, Bochkareva ES, Sinning I, Bibi E (2007) Membrane targeting of ribosomes and their release require distinct and separable functions of FtsY. J Biol Chem 282:32168–32175

    CAS  PubMed  Google Scholar 

  47. de Leeuw E, te Kaat K, Moser C, Menestrina G, Demel R, de Kruijff B, Oudega B, Luirink J, Sinning I (2000) Anionic phospholipids are involved in membrane association of FtsY and stimulate its GTPase activity. EMBO J 19:531–541

    PubMed  Google Scholar 

  48. Millman JS, Qi H-Y, Vulcu F, Bernstein HD, Andrews DW (2001) FtsY binds to the Escherichia coli inner membrane via interactions with phosphatidylethanolamine and membrane proteins. J Biol Chem 276:25982–25989

    CAS  PubMed  Google Scholar 

  49. 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

    CAS  PubMed  Google Scholar 

  50. Braig D, Bär C, Thumfart J-O, Koch H-G (2009) Two cooperating helices constitute the lipid-binding domain of the bacterial SRP receptor. J Mol Biol 390:401–413

    CAS  PubMed  Google Scholar 

  51. de Leeuw E, Poland D, Mol O, Sinning I, ten Hagen-Jongman CM, Oudega B, Luirink J (1997) Membrane association of FtsY, the E. coli SRP receptor. FEBS Lett 416:225–229

    PubMed  Google Scholar 

  52. 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

    CAS  PubMed  Google Scholar 

  53. 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

    CAS  PubMed  Google Scholar 

  54. 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

    CAS  PubMed  Google Scholar 

  55. Freymann DM, Keenan RJ, Stroud RM, Walter P (1997) Structure of the conserved GTPase domain of the signal recognition particle. Nature 385:361–364

    CAS  PubMed  Google Scholar 

  56. Montoya G, Svensson C, Luirink J, Sinning I (1997) Crystal structure of the NG domain from the signal-recognition particle receptor FtsY. Nature 385:365–368

    CAS  PubMed  Google Scholar 

  57. Zopf D, Bernstein HD, Johnson AE, Walter P (1990) The methionine-rich domain of the 54-kD protein subunit of the signal recognition particle contains an RNA-binding site and can be crosslinked to a signal sequence. EMBO J 9:4511–4517

    CAS  PubMed  Google Scholar 

  58. Batey RT, Rambo RP, Lucast L, Rha B, Doudna JA (2000) Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science 287:1232–1239

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  60. Halic M, Becker T, Pool MR, Spahn CM, Grassucci RA, Frank J, Beckmann R (2004) Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427:808–814

    CAS  PubMed  Google Scholar 

  61. Egea PF, Shan SO, Napetschnig J, Savage DF, Walter P, Stroud RM (2004) Substrate twinning activates the signal recognition particle and its receptor. Nature 427:215–221

    CAS  PubMed  Google Scholar 

  62. Focia PJ, Shepotinovskaya IV, Seidler JA, Freymann DM (2004) Heterodimeric GTPase core of the SRP targeting complex. Science 303:373–377

    CAS  PubMed  Google Scholar 

  63. Pohlschröder M, Prinz WA, Hartmann E, Beckwith J (1997) Protein translocation in the three domains of life: variations on a theme. Cell 91:563–566

    PubMed  Google Scholar 

  64. Kuhn A (1988) Alterations in the extracellular domain of M13 procoat protein make its membrane insertion dependent on secA and secY. Eur J Biochem 177:267–271

    CAS  PubMed  Google Scholar 

  65. Andersson H, von Heijne G (1993) Sec dependent and sec independent assembly of E. coli inner-membrane proteins: the topological rules depend on chain length. EMBO J 12:683–691

    CAS  PubMed  Google Scholar 

  66. Breukink E, Demel RA, de Korte-Kool G, de Kruijff B (1992) SecA insertion into phospholipids is stimulated by negatively charged lipids and inhibited by ATP: a monolayer study. Biochemistry 31:1119–1124

    CAS  PubMed  Google Scholar 

  67. Karamanou S, Bariami V, Papanikou E, Kalodimos CG, Economou A (2008) Assembly of the translocase motor onto the preprotein-conducting channel. Mol Microbiol 70:311–322

    CAS  PubMed  Google Scholar 

  68. Breukink E, Nouwen N, van Raalte A, Mizushima S, Tommassen J, de Kruijff B (1995) The C terminus of SecA is involved in both lipid binding and SecB binding. J Biol Chem 270:7902–7907

    CAS  PubMed  Google Scholar 

  69. Hunt JF, Weinkauf S, Henry L, Fak JJ, McNicholas P, Oliver DB, Deisenhofer J (2002) Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science 297:2018–2026

    CAS  PubMed  Google Scholar 

  70. Zimmer J, Nam Y, Rapoport TA (2008) Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455:936–943

    CAS  PubMed  Google Scholar 

  71. Erlandson KJ, Miller SBM, Nam Y, Osborne AR, Zimmer J, Rapoport TA (2008) A role for the two-helix finger of the SecA ATPase in protein translocation. Nature 455:984–987

    CAS  PubMed  Google Scholar 

  72. Economou A, Wickner W (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78:835–843

    CAS  PubMed  Google Scholar 

  73. Erlandson KJ, Or E, Osborne AR, Rapoport TA (2008) Analysis of polypeptide movement in the SecY channel during SecA-mediated protein translocation. J Biol Chem 283:15709–15715

    CAS  PubMed  Google Scholar 

  74. van der Wolk JP, de Wit JG, Driessen AJ (1997) The catalytic cycle of the Escherichia coli SecA ATPase comprises two distinct preprotein translocation events. EMBO J 16:7297–7304

    PubMed  Google Scholar 

  75. Schiebel E, Driessen AJ, Hartl FU, Wickner W (1991) \( \Updelta \mu _{{\text {H}^{ + }}} \) and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell 64:927–939

    CAS  PubMed  Google Scholar 

  76. Bessonneau P, Besson V, Collinson I, Duong F (2002) The SecYEG preprotein translocation channel is a conformationally dynamic and dimeric structure. EMBO J 21:995–1003

    CAS  PubMed  Google Scholar 

  77. Duong F (2003) Binding, activation and dissociation of the dimeric SecA ATPase at the dimeric SecYEG translocase. EMBO J 22:4375–4384

    CAS  PubMed  Google Scholar 

  78. Tziatzios C, Schubert D, Lotz M, Gundogan D, Betz H, Schägger H, Haase W, Duong F, Collinson I (2004) The bacterial protein-translocation complex: SecYEG dimers associate with one or two SecA molecules. J Mol Biol 340:513–524

    CAS  PubMed  Google Scholar 

  79. Meyer TH, Ménétret JF, Breitling R, Miller KR, Akey CW, Rapoport TA (1999) The bacterial SecY/E translocation complex forms channel-like structures similar to those of the eukaryotic Sec61p complex. J Mol Biol 285:1789–1800

    CAS  PubMed  Google Scholar 

  80. Manting EH, van der Does C, Remigy H, Engel A, Driessen AJ (2000) SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J 19:852–861

    CAS  PubMed  Google Scholar 

  81. Scheuring J, Braun N, Nothdurft L, Stumpf M, Veenendaal AK, Kol S, van der Does C, Driessen AJ, Weinkauf S (2005) The oligomeric distribution of SecYEG is altered by SecA and translocation ligands. J Mol Biol 354:258–271

    CAS  PubMed  Google Scholar 

  82. Hanein D, Matlack KE, Jungnickel B, Plath K, Kalies KU, Miller KR, Rapoport TA, Akey CW (1996) Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell 87:721–732

    CAS  PubMed  Google Scholar 

  83. Yahr TL, Wickner WT (2000) Evaluating the oligomeric state of SecYEG in preprotein translocase. EMBO J 19:4393–4401

    CAS  PubMed  Google Scholar 

  84. Mori H, Tsukazaki T, Masui R, Kuramitsu S, Yokoyama S, Johnson AE, Kimura Y, Akiyama Y, Ito K (2003) Fluorescence resonance energy transfer analysis of protein translocase. SecYE from Thermus thermophilus HB8 forms a constitutive oligomer in membranes. J Biol Chem 278:14257–14264

    CAS  PubMed  Google Scholar 

  85. Osborne AR, Rapoport TA (2007) Protein translocation is mediated by oligomers of the SecY complex with one SecY copy forming the channel. Cell 129:97–110

    CAS  PubMed  Google Scholar 

  86. Veenendaal AKJ, van der Does C, Driessen AJM (2004) The protein-conducting channel SecYEG. Biochim Biophys Acta 1694:81–95

    CAS  PubMed  Google Scholar 

  87. Joly JC, Leonard MR, Wickner WT (1994) Subunit dynamics in Escherichia coli preprotein translocase. Proc Natl Acad Sci USA 91:4703–4707

    CAS  PubMed  Google Scholar 

  88. 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

    CAS  PubMed  Google Scholar 

  89. 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

    PubMed  Google Scholar 

  90. Cannon KS, Or E, Clemons WM Jr, Shibata Y, Rapoport TA (2005) Disulfide bridge formation between SecY and a translocating polypeptide localizes the translocation pore to the center of SecY. J Cell Biol 169:219–225

    CAS  PubMed  Google Scholar 

  91. Tsukazaki T, Mori H, Fukai S, Ishitani R, Mori T, Dohmae N, Perederina A, Sugita Y, Vassylyev DG, Ito K, Nureki O (2008) Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455:988–991

    CAS  PubMed  Google Scholar 

  92. Duong F, Wickner W (1997) Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J 16:2756–2768

    CAS  PubMed  Google Scholar 

  93. Gardel C, Johnson K, Jacq A, Beckwith J (1990) The secD locus of E. coli codes for two membrane proteins required for protein export. EMBO J 9:3209–3216

    CAS  PubMed  Google Scholar 

  94. Törnroth-Horsefield S, Gourdon P, Horsefield R, Brive L, Yamamoto N, Mori H, Snijder A, Neutze R (2007) Crystal structure of AcrB in complex with a single transmembrane subunit reveals another twist. Structure 15:1663–1673

    PubMed  Google Scholar 

  95. Pogliano JA, Beckwith J (1994) SecD and SecF facilitate protein export in Escherichia coli. EMBO J 13:554–561

    CAS  PubMed  Google Scholar 

  96. Chen M, Xie K, Yuan J, Yi L, Facey SJ, Pradel N, Wu L-F, Kuhn A, Dalbey RE (2005) Involvement of SecDF and YidC in the membrane insertion of M13 procoat mutants. Biochemistry 44:10741–10749

    CAS  PubMed  Google Scholar 

  97. Samuelson JC, Chen M, Jiang F, Möller I, Wiedmann M, Kuhn A, Phillips GJ, Dalbey RE (2000) YidC mediates membrane protein insertion in bacteria. Nature 406:637–641

    CAS  PubMed  Google Scholar 

  98. Chen M, Samuelson JC, Jiang F, Müller M, Kuhn A, Dalbey RE (2002) Direct interaction of YidC with the Sec-independent Pf3 coat protein during its membrane protein insertion. J Biol Chem 277:7670–7675

    CAS  PubMed  Google Scholar 

  99. van der Laan M, Bechtluft P, Kol S, Nouwen N, Driessen AJM (2004) F1Fo ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis. J Cell Biol 165:213–222

    PubMed  Google Scholar 

  100. 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

    CAS  PubMed  Google Scholar 

  101. Nouwen N, Driessen AJ (2002) SecDFyajC forms a heterotetrameric complex with YidC. Mol Microbiol 44:1397–1405

    CAS  PubMed  Google Scholar 

  102. Xie K, Kiefer D, Nagler G, Dalbey RE, Kuhn A (2006) Different regions of the nonconserved large periplasmic domain of Escherichia coli YidC are involved in the SecF interaction and membrane insertase activity. Biochemistry 45:13401–13408

    CAS  PubMed  Google Scholar 

  103. Scotti PA, Urbanus ML, Brunner J, de Gier JW, von Heijne G, van der Does C, Driessen AJM, Oudega B, Luirink J (2000) YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J 19:542–549

    CAS  PubMed  Google Scholar 

  104. Beck K, Eisner G, Trescher D, Dalbey RE, Brunner J, Müller 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

    CAS  PubMed  Google Scholar 

  105. Urbanus ML, Scotti PA, Fröderberg L, Sääf A, de Gier J-WL, Brunner J, Samuelson JC, Dalbey RE, Oudega B, Luirink J (2001) Sec-dependent membrane protein insertion: sequential interaction of nascent FtsQ with SecY and YidC. EMBO Rep 2:524–529

    CAS  PubMed  Google Scholar 

  106. Celebi N, Yi L, Facey SJ, Kuhn A, Dalbey RE (2006) Membrane biogenesis of subunit II of cytochrome bo oxidase: contrasting requirements for insertion of the N-terminal and C-terminal domains. J Mol Biol 357:1428–1436

    CAS  PubMed  Google Scholar 

  107. van Bloois E, Haan GJ, de Gier JW, Oudega B, Luirink J (2006) Distinct requirements for translocation of the N-tail and C-tail of the Escherichia coli inner membrane protein CyoA. J Biol Chem 281:10002–10009

    PubMed  Google Scholar 

  108. Dalbey RE, Kuhn A (2000) Evolutionarily related insertion pathways of bacterial, mitochondrial, and thylakoid membrane proteins. Annu Rev Cell Dev Biol 16:51–87

    CAS  PubMed  Google Scholar 

  109. Bonnefoy N, Chalvet F, Hamel P, Slonimski PP, Dujardin G (1994) OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis. J Mol Biol 239:201–212

    CAS  PubMed  Google Scholar 

  110. Funes S, Nargang FE, Neupert W, Herrmann JM (2004) The Oxa2 protein of Neurospora crassa plays a critical role in the biogenesis of cytochrome oxidase and defines a ubiquitous subbranch of the Oxa1/YidC/Alb3 protein family. Mol Biol Cell 15:1853–1861

    CAS  PubMed  Google Scholar 

  111. Moore M, Harrison MS, Peterson EC, Henry R (2000) Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 275:1529–1532

    CAS  PubMed  Google Scholar 

  112. Gerdes L, Bals T, Klostermann E, Karl M, Philippar K, Hünken M, Soll J, Schünemann D (2006) A second thylakoid membrane-localized Alb3/Oxa1/YidC homologue is involved in proper chloroplast biogenesis in Arabidopsis thaliana. J Biol Chem 281:16632–16642

    CAS  PubMed  Google Scholar 

  113. Jiang F, Yi L, Moore M, Chen M, Rohl T, van Wijk K-J, de Gier J-WL, Henry R, Dalbey RE (2002) Chloroplast YidC homolog Albino3 can functionally complement the bacterial YidC depletion strain and promote membrane insertion of both bacterial and chloroplast thylakoid proteins. J Biol Chem 277:19281–19288

    CAS  PubMed  Google Scholar 

  114. van Bloois E, Nagamori S, Koningstein G, Ullers RS, Preuss M, Oudega B, Harms N, Kaback HR, Herrmann JM, Luirink J (2005) The Sec-independent function of Escherichia coli YidC is evolutionary-conserved and essential. J Biol Chem 280:12996–13003

    PubMed  Google Scholar 

  115. van Bloois E, Koningstein G, Bauerschmitt H, Herrmann JM, Luirink J (2007) Saccharomyces cerevisiae Cox18 complements the essential Sec-independent function of Escherichia coli YidC. FEBS J 274:5704–5713

    PubMed  Google Scholar 

  116. Benz M, Bals T, Gügel IL, Piotrowski M, Kuhn A, Schünemann D, Soll J, Ankele E (2009) Alb4 of Arabidopsis promotes assembly and stabilization of a non chlorophyll-binding photosynthetic complex, the CF1CFo-ATP synthase. Mol Plant 2:1410–1424

    CAS  PubMed  Google Scholar 

  117. Yen MR, Harley KT, Tseng YH, Saier MH Jr (2001) Phylogenetic and structural analyses of the oxa1 family of protein translocases. FEMS Microbiol Lett 204:223–231

    CAS  PubMed  Google Scholar 

  118. Yu Z, Koningstein G, Pop A, Luirink J (2008) The conserved third transmembrane segment of YidC contacts nascent Escherichia coli inner-membrane proteins. J Biol Chem 283:34635–34642

    CAS  PubMed  Google Scholar 

  119. Klenner C, Yuan J, Dalbey RE, Kuhn A (2008) The Pf3 coat protein contacts TM1 and TM3 of YidC during membrane biogenesis. FEBS Lett 582:3967–3972

    CAS  PubMed  Google Scholar 

  120. Serek J, Bauer-Manz G, Struhalla G, van den Berg L, Kiefer D, Dalbey RE, Kuhn A (2004) Escherichia coli YidC is a membrane insertase for Sec-independent proteins. EMBO J 23:294–301

    CAS  PubMed  Google Scholar 

  121. Dalbey RE, Kuhn A (2004) YidC family members are involved in the membrane insertion, lateral integration, folding, and assembly of membrane proteins. J Cell Biol 166:769–774

    CAS  PubMed  Google Scholar 

  122. Nagamori S, Smirnova IN, Kaback HR (2004) Role of YidC in folding polytopic membrane proteins. J Cell Biol 165:53–62

    CAS  PubMed  Google Scholar 

  123. Shimohata N, Nagamori S, Akiyama Y, Kaback HR, Ito K (2007) SecY alterations that impair membrane protein folding and generate a membrane stress. J Cell Biol 176:307–317

    CAS  PubMed  Google Scholar 

  124. Wang P, Kuhn A, Dalbey RE (2010) Global change of gene regulation and cell physiology in YidC-depleted E. coli. J Bacteriol. doi:10.1128/JB.00484-09

  125. van der Laan M, Urbanus ML, ten Hagen-Jongman CM, Nouwen N, Oudega B, Harms N, Driessen AJ, Luirink J (2003) A conserved function of YidC in the biogenesis of respiratory chain complexes. Proc Natl Acad Sci USA 100:5801–5806

    PubMed  Google Scholar 

  126. Koch HG, Moser M, Schimz KL, Müller M (2002) The integration of YidC into the cytoplasmic membrane of Escherichia coli requires the signal recognition particle, SecA and SecYEG. J Biol Chem 277:5715–5718

    CAS  PubMed  Google Scholar 

  127. Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211–231

    CAS  PubMed  Google Scholar 

  128. Ami D, Natalello A, Schultz T, Gatti-Lafranconi P, Lotti M, Doglia SM, de Marco A (2009) Effects of recombinant protein misfolding and aggregation on bacterial membranes. Biochim Biophys Acta 1794:263–269

    CAS  PubMed  Google Scholar 

  129. Hong H, Tamm LK (2004) Elastic coupling of integral membrane protein stability to lipid bilayer forces. Proc Natl Acad Sci USA 101:4065–4070

    CAS  PubMed  Google Scholar 

  130. Perozo E, Cortes DM, Sompornpisut P, Kloda A, Martinac B (2002) Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature 418:942–948

    CAS  PubMed  Google Scholar 

  131. Moe P, Blount P (2005) Assessment of potential stimuli for mechano-dependent gating of MscL: effects of pressure, tension, and lipid headgroups. Biochemistry 44:12239–12244

    CAS  PubMed  Google Scholar 

  132. Akiyama Y, Kihara A, Ito K (1996) Subunit a of proton ATPase Fo sector is a substrate of the FtsH protease in Escherichia coli. FEBS Lett 399:26–28

    CAS  PubMed  Google Scholar 

  133. Kihara A, Akiyama Y, Ito K (1998) Different pathways for protein degradation by the FtsH/HflKC membrane-embedded protease complex: an implication from the interference by a mutant form of a new substrate protein YccA. J Mol Biol 279:175–188

    CAS  PubMed  Google Scholar 

  134. Chiba S, Akiyama Y, Mori H, Matsuo E, Ito K (2000) Length recognition at the N-terminal tail for the initiation of FtsH-mediated proteolysis. EMBO Rep 1:47–52

    CAS  PubMed  Google Scholar 

  135. Chiba S, Akiyama Y, Ito K (2002) Membrane protein degradation by FtsH can be initiated from either end. J Bacteriol 184:4775–4782

    CAS  PubMed  Google Scholar 

  136. Bogdanov M, Heacock PN, Dowhan W (2002) A polytopic membrane protein displays a reversible topology dependent on membrane lipid composition. EMBO J 21:2107–2116

    CAS  PubMed  Google Scholar 

  137. Zhang W, Bogdanov M, Pi J, Pittard AJ, Dowhan W (2003) Reversible topological organization within a polytopic membrane protein is governed by a change in membrane phospholipids composition. J Biol Chem 278:50128–50135

    CAS  PubMed  Google Scholar 

  138. Zhang W, Campbell HA, King SC, Dowhan W (2005) Phospholipids as determinants of membrane protein topology. Phosphatidylethanolamine is required for the proper topological organization of the γ-aminobutyric acid permease (GabP) of Escherichia coli. J Biol Chem 280:26032–26038

    CAS  PubMed  Google Scholar 

  139. Xie J, Bogdanov M, Heacock P, Dowhan W (2006) Phosphatidylethanolamine and monoglucosyldiacylglycerol are interchangeable in supporting topogenesis and function of the polytopic membrane protein lactose permease. J Biol Chem 281:19172–19178

    CAS  PubMed  Google Scholar 

  140. Bogdanov M, Dowhan W (1995) Phosphatidylethanolamine is required for in vivo function of the membrane-associated lactose permease of Escherichia coli. J Biol Chem 270:732–739

    CAS  PubMed  Google Scholar 

  141. Allen SJ, Curran AR, Templer RH, Meijberg W, Booth PJ (2004) Controlling the folding efficiency of an integral membrane protein. J Mol Biol 342:1293–1304

    CAS  PubMed  Google Scholar 

  142. Miller D, Charalambous K, Rotem D, Schuldiner S, Curnow P, Booth PJ (2009) In vitro unfolding and refolding of the small multidrug transporter EmrE. J Mol Biol 393:815–832

    CAS  PubMed  Google Scholar 

  143. Lill R, Dowhan W, Wickner W (1990) The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell 60:271–280

    CAS  PubMed  Google Scholar 

  144. Hendrick JP, Wickner W (1991) SecA protein needs both acidic phospholipids and SecY/E protein for functional high-affinity binding to the Escherichia coli plasma membrane. J Biol Chem 266:24596–24600

    CAS  PubMed  Google Scholar 

  145. Weidner U, Geier S, Ptock A, Friedrich T, Leif H, Weiss H (1993) The gene locus of the proton-translocating NADH: ubiquinone oxidoreductase in Escherichia coli. Organization of the 14 genes and relationship between the derived proteins and subunits of mitochondrial complex I. J Mol Biol 233:109–122

    CAS  PubMed  Google Scholar 

  146. Guénebaut V, Schlitt A, Weiss H, Leonard K, Friedrich T (1998) Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 276:105–112

    PubMed  Google Scholar 

  147. Peng G, Fritzsch G, Zickermann V, Schägger H, Mentele R, Lottspeich F, Bostina M, Radermacher M, Huber R, Stetter KO, Michel H (2003) Isolation, characterization and electron microscopic single particle analysis of the NADH:ubiquinone oxidoreductase (complex I) from the hyperthermophilic eubacterium Aquifex aeolicus. Biochemistry 42:3032–3039

    CAS  PubMed  Google Scholar 

  148. Sazanov LA, Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430–1436

    CAS  PubMed  Google Scholar 

  149. Price CE, Driessen AJ (2008) YidC is involved in the biogenesis of anaerobic respiratory complexes in the inner membrane of Escherichia coli. J Biol Chem 283:26921–26927

    CAS  PubMed  Google Scholar 

  150. Rapisarda VA, Chehín RN, De Las Rivas J, Rodríguez-Montelongo L, Farías RN, Massa EM (2002) Evidence for Cu(I)-thiolate ligation and prediction of a putative copper-binding site in the Escherichia coli NADH dehydrogenase-2. Arch Biochem Biophys 405:87–94

    CAS  PubMed  Google Scholar 

  151. Abramson J, Riistama S, Larsson G, Jasaitis A, Svensson-Ek M, Laakkonen L, Puustinen A, Iwata S, Wikstöm M (2000) The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat Struct Biol 7:910–917

    CAS  PubMed  Google Scholar 

  152. Ma J, Katsonouri A, Gennis RB (1997) Subunit II of the cytochrome bo 3 ubiquinol oxidase from Escherichia coli is a lipoprotein. Biochemistry 36:11298–11303

    CAS  PubMed  Google Scholar 

  153. Stenberg F, von Heijne G, Daley DO (2007) Assembly of the cytochrome bo 3 complex. J Mol Biol 371:765–773

    CAS  PubMed  Google Scholar 

  154. Tran QH, Bongaerts J, Vlad D, Unden G (1997) Requirement for the proton-pumping NADH dehydrogenase I of Escherichia coli in respiration of NADH to fumarate and its bioenergetic implications. Eur J Biochem 244:155–160

    CAS  PubMed  Google Scholar 

  155. Iverson TM, Luna-Chavez C, Cecchini G, Rees DC (1999) Structure of the Escherichia coli fumarate reductase respiratory complex. Science 284:1961–1966

    CAS  PubMed  Google Scholar 

  156. Bertero MG, Rothery RA, Palak M, Hou C, Lim D, Blasco F, Weiner JH, Strynadka NC (2003) Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A. Nat Struct Biol 10:681–687

    CAS  PubMed  Google Scholar 

  157. Deisenhofer J, Michel H (1989) The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. Science 245:1463–1473

    CAS  PubMed  Google Scholar 

  158. Ermler U, Fritzsch G, Buchanan SK, Michel H (1994) Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 Å resolution: cofactors and protein-cofactor interactions. Structure 2:925–936

    CAS  PubMed  Google Scholar 

  159. Fotiadis D, Qian P, Philippsen A, Bullough PA, Engel A, Hunter CN (2004) Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy. J Biol Chem 279:2063–2068

    CAS  PubMed  Google Scholar 

  160. Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565

    CAS  PubMed  Google Scholar 

  161. Woolhead CA, Thompson SJ, Moore M, Tissier C, Mant A, Rodger A, Henry R, Robinson C (2001) Distinct Albino3-dependent and -independent pathways for thylakoid membrane protein insertion. J Biol Chem 276:40841–40846

    CAS  PubMed  Google Scholar 

  162. Spence E, Bailey S, Nenninger A, Møller SG, Robinson C (2004) A homolog of Albino3/OxaI is essential for thylakoid biogenesis in the cyanobacterium Synechocystis sp. PCC6803. J Biol Chem 279:55792–55800

    CAS  PubMed  Google Scholar 

  163. Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370:621–628

    CAS  PubMed  Google Scholar 

  164. Meier T, Polzer P, Diederichs K, Welte W, Dimroth P (2005) Structure of the rotor ring of F-type Na+-ATPase from Ilyobacter tartaricus. Science 308:659–662

    CAS  PubMed  Google Scholar 

  165. Pogoryelov D, Yildiz O, Faraldo-Gómez JD, Meier T (2009) High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat Struct Mol Biol 16:1068–1073

    CAS  PubMed  Google Scholar 

  166. Junge W, Sielaff H, Engelbrecht S (2009) Torque generation and elastic power transmission in the rotary FoF1-ATPase. Nature 459:364–370

    CAS  PubMed  Google Scholar 

  167. 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 F1Fo ATP synthase and SecE of the SecYEG translocase. Biochemistry 42:10537–10544

    CAS  PubMed  Google Scholar 

  168. Kol S, Turrell BR, de Keyzer J, van der Laan M, Nouwen N, Driessen AJM (2006) YidC-mediated membrane insertion of assembly mutants of subunit c of the F1Fo ATPase. J Biol Chem 281:29762–29768

    CAS  PubMed  Google Scholar 

  169. Yi L, Celebi N, Chen M, Dalbey RE (2004) Sec/SRP requirements and energetics of membrane insertion of subunits a, b, and c of the Escherichia coli F1Fo ATP synthase. J Biol Chem 279:39260–39267

    CAS  PubMed  Google Scholar 

  170. Kol S, Majczak W, Heerlien R, van der Berg JP, Nouwen N, Driessen AJM (2009) Subunit a of the F1Fo ATP synthase requires YidC and SecYEG for membrane insertion. J Mol Biol 390:893–901

    CAS  PubMed  Google Scholar 

  171. Hermolin J, Fillingame RH (1995) Assembly of Fo sector of Escherichia coli H+ ATP synthase. Interdependence of subunit insertion into the membrane. J Biol Chem 270:2815–2817

    CAS  PubMed  Google Scholar 

  172. Kol S, Nouwen N, Driessen AJM (2008) The charge distribution in the cytoplasmic loop of subunit c of the F1Fo ATPase is a determinant for YidC targeting. J Biol Chem 283:9871–9877

    CAS  PubMed  Google Scholar 

  173. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610–615

    CAS  PubMed  Google Scholar 

  174. Guan L, Kaback HR (2006) Lessons from lactose permease. Annu Rev Biophys Biomol Struct 35:67–91

    CAS  PubMed  Google Scholar 

  175. Smirnova I, Kasho V, Choe JY, Altenbach C, Hubbell WL, Kaback HR (2007) Sugar binding induces an outward facing conformation of LacY. Proc Natl Acad Sci USA 104:16504–16509

    CAS  PubMed  Google Scholar 

  176. Saier MH Jr (2000) Families of transmembrane sugar transport proteins. Mol Microbiol 35:699–710

    CAS  PubMed  Google Scholar 

  177. Murakami S, Nakashima R, Yamashita E, Yamaguchi A (2002) Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419:587–593

    CAS  PubMed  Google Scholar 

  178. Yin Y, He X, Szewczyk P, Nguyen T, Chang G (2006) Structure of the multidrug transporter EmrD from Escherichia coli. Science 312:741–744

    CAS  PubMed  Google Scholar 

  179. Yousef MS, Guan L (2009) A 3D structure model of the melibiose permease of Escherichia coli represents a distinctive fold for Na+ symporters. Proc Natl Acad Sci USA 106:15291–15296

    CAS  PubMed  Google Scholar 

  180. Huang Y, Lemieux MJ, Song J, Auer M, Wang DN (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301:616–620

    CAS  PubMed  Google Scholar 

  181. Yamashita A, Singh SK, Kawate T, Jin Y, Gouaux E (2005) Crystal structure of a bacterial homologue of Na+/Cl−dependent neurotransmitter transporters. Nature 437:215–223

    CAS  PubMed  Google Scholar 

  182. Ressl S, Terwisscha van Scheltinga AC, Vonrhein C, Ott V, Ziegler C (2009) Molecular basis of transport and regulation in the Na+/betaine symporter BetP. Nature 458:47–52

    CAS  PubMed  Google Scholar 

  183. Faham S, Watanabe A, Besserer GM, Cascio D, Specht A, Hirayama BA, Wright EM, Abramson J (2008) The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na+/sugar symport. Science 321:810–814

    CAS  PubMed  Google Scholar 

  184. Weyand S, Shimamura T, Yajima S, Suzuki S, Mirza O, Krusong K, Carpenter EP, Rutherford NG, Hadden JM, O’Reilly J, Ma P, Saidijam M, Patching SG, Hope RJ, Norbertczak HT, Roach PC, Iwata S, Henderson PJ, Cameron AD (2008) Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322:709–713

    CAS  PubMed  Google Scholar 

  185. Higgens CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113

    Google Scholar 

  186. Davidson AL, Maloney PC (2007) ABC transporters: how small machines do a big job. Trends Microbiol 15:448–455

    CAS  PubMed  Google Scholar 

  187. Paulsen IT, Beness AM, Saier MH Jr (1997) Computer-based analyses of the protein constituents of transport systems catalyzing export of complex carbohydrates in bacteria. Microbiology 143:2685–2699

    CAS  PubMed  Google Scholar 

  188. Davidson AL, Nikaido H (1991) Purification and characterization of the membrane-associated components of the maltose transport system from Escherichia coli. J Biol Chem 266:8946–8951

    CAS  PubMed  Google Scholar 

  189. Davidson AL, Shuman HA, Nikaido H (1992) Mechanism of maltose transport in Escherichia coli: transmembrane signalling by periplasmic binding proteins. Proc Natl Acad Sci USA 89:2360–2364

    CAS  PubMed  Google Scholar 

  190. Oldham ML, Khare D, Quiocho FA, Davidson AL, Chen J (2007) Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450:515–521

    CAS  PubMed  Google Scholar 

  191. Khare D, Oldham ML, Orelle C, Davidson AL, Chen J (2009) Alternating access in maltose transporter mediated by rigid-body rotations. Mol Cell 33:528–536

    CAS  PubMed  Google Scholar 

  192. Froshauer S, Green GN, Boyd D, McGovern K, Beckwith J (1988) Genetic analysis of the membrane insertion and topology of MalF, a cytoplasmic membrane protein of Escherichia coli. J Mol Biol 200:501–511

    CAS  PubMed  Google Scholar 

  193. Deutscher J, Francke C, Postma PW (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70:939–1031

    CAS  PubMed  Google Scholar 

  194. Cai M, Williams DC Jr, Wang G, Lee BR, Peterkofsky A, Clore GM (2003) Solution structure of the phosphoryl transfer complex between the signal-transducing protein IIAGlucose and the cytoplasmic domain of the glucose transporter IICBGlucose of the Escherichia coli glucose phosphotransferase system. J Biol Chem 278:25191–25206

    CAS  PubMed  Google Scholar 

  195. Huber F, Erni B (1996) Membrane topology of the mannose transporter of Escherichia coli K12. Eur J Biochem 239:810–817

    CAS  PubMed  Google Scholar 

  196. Oberholzer AE, Schneider P, Siebold C, Baumann U, Erni B (2009) Crystal structure of enzyme I of the phosphoenolpyruvate: sugar phosphotransferase system in the dephosphorylated state. J Biol Chem 284:33169–33176

    CAS  PubMed  Google Scholar 

  197. Koning RI, Keegstra W, Oostergetel GT, Schuurman-Wolters G, Robillard GT, Brisson A (1999) The 5 Å projection structure of the transmembrane domain of the mannitol transporter enzyme II. J Mol Biol 287:845–851

    CAS  PubMed  Google Scholar 

  198. Veldhuis G, Broos J, Poolman B, Scheek RM (2005) Stoichiometry and substrate affinity of the mannitol transporter, EnzymeIImtl, from Escherichia coli. Biophys J 89:201–210

    CAS  PubMed  Google Scholar 

  199. Beutler R, Ruggiero F, Erni B (2000) Folding and activity of circularly permuted forms of a polytopic membrane protein. Proc Natl Acad Sci USA 97:1477–1482

    CAS  PubMed  Google Scholar 

  200. Agre P (2006) The aquaporin water channels. Proc Am Thorac Soc 3:5–13

    CAS  PubMed  Google Scholar 

  201. Hedfalk K, Törnroth-Horsefield S, Nyblom M, Johanson U, Kjellbom P, Neutze R (2006) Aquaporin gating. Curr Opin Struct Biol 16:447–456

    CAS  PubMed  Google Scholar 

  202. Pao GM, Wu LF, Johnson KD, Höfte H, Chrispeels MJ, Sweet G, Sandal NN, Saier MH Jr (1991) Evolution of the MIP family of integral membrane transport proteins. Mol Microbiol 5:33–37

    CAS  PubMed  Google Scholar 

  203. Wistow GJ, Pisano MM, Chepelinsky AB (1991) Tandem sequence repeats in transmembrane channel proteins. Trends Biochem Sci 16:170–171

    CAS  PubMed  Google Scholar 

  204. Viadiu H, Gonen T, Walz T (2007) Projection map of aquaporin-9 at 7 Å resolution. J Mol Biol 367:80–88

    CAS  PubMed  Google Scholar 

  205. Smolin N, Li B, Beck DA, Daggett V (2008) Side-chain dynamics are critical for water permeation through aquaporin-1. Biophys J 95:1089–1098

    CAS  PubMed  Google Scholar 

  206. Hovijitra NT, Wuu JJ, Peaker B, Swartz JR (2009) Cell-free synthesis of functional aquaporin Z in synthetic liposomes. Biotechnol Bioeng 104:40–49

    CAS  PubMed  Google Scholar 

  207. Booth IR, Louis P (1999) Managing hypoosmotic stress: aquaporins and mechanosensitive channels in Escherichia coli. Curr Opin Microbiol 2:166–169

    CAS  PubMed  Google Scholar 

  208. Chang G, Spencer RH, Lee AT, Barclay MT, Rees DC (1998) Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282:2220–2226

    CAS  PubMed  Google Scholar 

  209. Liu Z, Gandhi CS, Rees DC (2009) Structure of a tetrameric MscL in an expanded intermediate state. Nature 461:120–124

    CAS  PubMed  Google Scholar 

  210. Bass RB, Strop P, Barclay M, Rees DC (2002) Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298:1582–1587

    CAS  PubMed  Google Scholar 

  211. Szurmant H, Ordal GW (2004) Diversity in chemotaxis mechanisms among the Bacteria and Archaea. Microbiol Mol Biol Rev 68:301–319

    CAS  PubMed  Google Scholar 

  212. Hazelbauer GL, Falke JJ, Parkinson JS (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33:9–19

    CAS  PubMed  Google Scholar 

  213. Yeh JI, Biemann HP, Privé GG, Pandit J, Koshland DE Jr, Kim SH (1996) High-resolution structures of the ligand binding domain of the wild-type bacterial aspartate receptor. J Mol Biol 262:186–201

    CAS  PubMed  Google Scholar 

  214. Kim KK, Yokota H, Kim SH (1999) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400:787–792

    CAS  PubMed  Google Scholar 

  215. Gebert JF, Overhoff B, Manson MD, Boos W (1988) The Tsr chemosensory transducer of Escherichia coli assembles into the cytoplasmic membrane via a SecA-dependent process. J Biol Chem 263:16652–16660

    CAS  PubMed  Google Scholar 

  216. Shiomi D, Yoshimoto M, Homma M, Kawagishi I (2006) Helical distribution of the bacterial chemoreceptor via colocalization with the Sec protein translocation machinery. Mol Microbiol 60:894–906

    CAS  PubMed  Google Scholar 

  217. Facey SJ, Kuhn A (2003) The sensor protein KdpD inserts into the Escherichia coli membrane independent of the Sec translocase and YidC. Eur J Biochem 270:1724–1734

    CAS  PubMed  Google Scholar 

  218. Suzuki H, Yonekura K, Namba K (2004) Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. J Mol Biol 337:105–113

    CAS  PubMed  Google Scholar 

  219. Zhou J, Sharp LL, Tang HL, Lloyd SA, Billings S, Braun TF, Blair DF (1998) Function of protonatable residues in the flagellar motor of Escherichia coli: a critical role for Asp 32 of MotB. J Bacteriol 180:2729–2735

    CAS  PubMed  Google Scholar 

  220. Kubori T, Shimamoto N, Yamaguchi S, Namba K, Aizawa S (1992) Morphological pathway of flagellar assembly in Salmonella typhimurium. J Mol Biol 226:433–446

    CAS  PubMed  Google Scholar 

  221. Pradel N, Decorps A, Ye C, Santini CL, Wu LF (2005) YidC-dependent translocation of green fluorescence protein fused to the FliP cleavable signal peptide. Biochimie 87:191–196

    CAS  PubMed  Google Scholar 

  222. Macnab RM (2004) Type III flagellar protein export and flagellar assembly. Biochim Biophys Acta 1694:207–217

    CAS  PubMed  Google Scholar 

  223. Fan F, Macnab RM (1996) Enzymatic characterization of FliI. An ATPase involved in flagellar assembly in Salmonella typhimurium. J Biol Chem 271:31981–31988

    CAS  PubMed  Google Scholar 

  224. Minamino T, Macnab RM (2000) Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol Microbiol 35:1052–1064

    CAS  PubMed  Google Scholar 

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Acknowledgments

We apologize to the authors whose work we were unable to cite because of space limitations. We thank the Deutsche Forschungsgemeinschaft (DFG) for the long-standing support of our research.

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    Sandra J. Facey & Andreas Kuhn

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Facey, S.J., Kuhn, A. Biogenesis of bacterial inner-membrane proteins. Cell. Mol. Life Sci. 67, 2343–2362 (2010). https://doi.org/10.1007/s00018-010-0303-0

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