• Marco Fioroni
  • Tamara Dworeck
  • Francisco Rodríguez-Ropero
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 794)


This chapter will be an introductory section on the biology of membrane proteins in general, with regard to the different structural as well as functional classes of these proteins (i.e. α-helix and β-barrel). It will furthermore give some basic information on biological membranes and the lipids they consist of. The focus will be on the characteristics and unique structural and functional features of β-barrel outer membrane proteins. This chapter will then introduce to the E. coli outer membrane iron transporter FhuA (Ferric hydroxamate uptake component A), which as a member of the TonB protein-dependent transporters belongs to the largest known β-barrels. The FhuA has been successfully employed as a model for the transformation of a β-barrel protein into a custom-made nano-channel. By means of the FhuA example this chapter will therefore look at β-barrel proteins not only within the biological context but it will already introduce to the relevance and use of proteins belonging to this class for the nano-material sciences and specifically for the design of biological nano-channels.


Outer Membrane Transmembrane Helix Polar Amino Acid Peripheral Protein Membrane Span Helix 
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.


  1. 1.
    Gorter E, Grendel F (1925) On bimolecular layers of lipoids on the chromocytes of the blood. J Exp Med 41:439–443PubMedGoogle Scholar
  2. 2.
    Danielli JF, Davson H (1935) A contribution to the theory of permeability of thin films. J Cell Comp Physiol 3:495–508Google Scholar
  3. 3.
    Singer SJ, Nicholson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731PubMedGoogle Scholar
  4. 4.
    Rietveld A, Simons K (1998) The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim Biophys Acta 1376:467–479PubMedGoogle Scholar
  5. 5.
    McElhaney RN, Tourtellotte ME (1971) The relationship between fatty acid structure and the positional distribution of esterified fatty acids in phosphatidylglycerol from Mycoplasma laidlawii B. Biochim Biophys Acta 202:120–128Google Scholar
  6. 6.
    van Meer G, Voelker D, Feigenson G (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124PubMedGoogle Scholar
  7. 7.
    Rothman JE, Lenard J (1977) Membrane asymmetry. Science 195:743–753PubMedGoogle Scholar
  8. 8.
    Muller P, Herrmann A (2002) Rapid transbilayer movement of spin-labeled steroids in human erythrocytes and in liposomes. Biophys J 82:1418–1428PubMedGoogle Scholar
  9. 9.
    Marr AG, Ingraham JL (1962) Effect of temperature on the composition of fatty acids in Escherichia coli. J Bacteriol 84:1260–1267PubMedGoogle Scholar
  10. 10.
    Silvius JR (1982) Thermotropic phase transitions of pure lipids in model membranes and their modifications by membrane proteins. In: Jost PC, Griffith OH (eds) Lipid-protein interactions. Wiley, New YorkGoogle Scholar
  11. 11.
    Dove SK, Cooke FT, Douglas MR, Sayers LG, Parker PJ, Michell RH (1997) Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature 390:187–192PubMedGoogle Scholar
  12. 12.
    Guidotti G (1972) Membrane proteins. Annu Rev Biochem 41:731–752PubMedGoogle Scholar
  13. 13.
    Daley DO, Rapp M, Granseth E, Melen K, Drew D, von Heijne G (2005) Global topology analysis of the Escherichia coli inner membrane proteome. Science 308:1321–1323PubMedGoogle Scholar
  14. 14.
    Miller JP, Lo RS, Ben-Hur A, Desmarais C, Stagljar I, Noble WS, Fields S (2005) Large-scale identification of yeast integral membrane protein interactions. Proc Natl Acad Sci USA 102:12123–12128PubMedGoogle Scholar
  15. 15.
    Arinaminpathy Y, Khurana E, Engelman DM, Gerstein MB (2009) Computational analysis of membrane proteins: the largest class of drug targets. Drug Discov Today 14:1130–1135PubMedGoogle Scholar
  16. 16.
    Luckey M (2008) Membrane structural biology – with biochemical and biophysical foundations. Cambridge University Press, New YorkGoogle Scholar
  17. 17.
    Hedin LE, Illergard K, Elofsson A (2011) An introduction to membrane proteins. J Proteome Res 10:3324–3331PubMedGoogle Scholar
  18. 18.
    Bijlmakers MJ, Marsh M (2003) The on-off story of protein palmitoylation. Trends Cell Biol 13:32–42PubMedGoogle Scholar
  19. 19.
    Magee AI, Gutierrez L, McKay IA, Marshall CJ, Hall A (1987) Dynamic fatty acylation of p21N-ras. EMBO J 6:3353–3357PubMedGoogle Scholar
  20. 20.
    Dowler S, Currie RA, Campbell DG, Deak M, Kular G, Downes CP, Alessi DR (2000) Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities. Biochem J 351:19–31PubMedGoogle Scholar
  21. 21.
    Ferguson KM, Lemmon MA, Schlessinger J, Sigler PB (1995) Structure of the high affinity complex of inositol trisphosphate with a phospholipase C pleckstrin homology domain. Cell 83:1037–1046PubMedGoogle Scholar
  22. 22.
    Kholodenko BN, Hancock JF, Kolch W (2010) Signalling ballet in space and time. Nat Rev Mol Cell Biol 11:414–426PubMedGoogle Scholar
  23. 23.
    Yeagle P (1992) The structure of biological membranes. CRC Press, Boca RatonGoogle Scholar
  24. 24.
    Ubarretxena-Belandia I, Engelman DM (2001) Helical membrane proteins: diversity of functions in the context of simple architecture. Curr Opin Struct Biol 11:370–376PubMedGoogle Scholar
  25. 25.
    Seddon AM, Curnow P, Booth PJ (2004) Membrane proteins, lipids and detergents: not just a soap opera. Biochim Biophys Acta 1666:105–117PubMedGoogle Scholar
  26. 26.
    Junge F, Schneider B, Reckel S, Schwarz D, Dötsch V, Bernhard F (2008) Large-scale production of functional membrane proteins. Cell Mol Life Sci 65:1729–1755PubMedGoogle Scholar
  27. 27.
    Von Heine G (2011) Introduction to theme “membrane protein folding and insertion”. Annu Rev Biochem 80:157–160Google Scholar
  28. 28.
    Haswell ES, Phillips R, Rees DC (2011) Mechanosensitive channels: what can they do and how do they do it? Structure 19:1356–1369PubMedGoogle Scholar
  29. 29.
    Granseth E, Daley D, Rapp M, Melen K, von Heijne G (2005) Experimentally constrained topology models for bacterial inner membrane proteins. J Mol Biol 352:489–494PubMedGoogle Scholar
  30. 30.
    Bowie JU (1997) Helix packing in membrane proteins. J Mol Biol 272:780–789PubMedGoogle Scholar
  31. 31.
    Arce J, Sturgis JN, Duneau JP (2009) Dissecting membrane protein architecture: an annotation of structural complexity. Biopolymers 91:815–829PubMedGoogle Scholar
  32. 32.
    Bocharov EV, Mineev KS, Volynsky PE, Ermolyuk YS, Tkach EN, Sobol AG, Chupin VV, Kirpichnikov MP, Efremov RG, Arseniev AS (2008) Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state. J Biol Chem 283:6950–6956PubMedGoogle Scholar
  33. 33.
    Smith SO, Bormann BJ (1995) Determination of helix-helix interactions in membranes by rotational resonance NMR. Proc Natl Acad Sci USA 92:488–491PubMedGoogle Scholar
  34. 34.
    Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77PubMedGoogle Scholar
  35. 35.
    Grigorieff N, Ceska TA, Downing KH, Baldwin JM, Henderson R (1996) Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol 259:393–421PubMedGoogle Scholar
  36. 36.
    Yohannan S, Faham S, Yang D, Whitelegge J, Bowie J (2004) The evolution of transmembrane helix kinks and the structural diversity of G protein-coupled receptors. Proc Natl Acad Sci USA 101:959–963PubMedGoogle Scholar
  37. 37.
    Fu D, Libson A, Miercke L, Weitzman C, Nollert P, Krucinski J, Stroud R (2000) Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290:481–486PubMedGoogle Scholar
  38. 38.
    Viklund H, Granseth E, Elofsson A (2006) Structural classification and prediction of reentrant regions in alpha-helical transmembrane proteins: application to complete genomes. J Mol Biol 361:591–603PubMedGoogle Scholar
  39. 39.
    Kauko A, Illergard K, Elofsson A (2008) Coils in the membrane core are conserved and functionally important. J Mol Biol 380:170–180PubMedGoogle Scholar
  40. 40.
    Elofsson A, von Heijne G (2007) Membrane protein structure: prediction versus reality. Annu Rev Biochem 76:125–140PubMedGoogle Scholar
  41. 41.
    Blobel G (1980) Intracellular protein topogenesis. Proc Natl Acad Sci USA 77:1496–1500PubMedGoogle Scholar
  42. 42.
    Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK (1999) Structure of bacteriorhodopsin at 1.55 A resolution. J Mol Biol 291:899–911PubMedGoogle Scholar
  43. 43.
    Verdon G, Boudker O (2012) Crystal structure of an asymmetric trimer of a bacterial glutamate transporter homolog. Nat Struct Mol Biol 19:355–357PubMedGoogle Scholar
  44. 44.
    Gromiha MM (1999) A simple method for predicting transmembrane a helices with better accuracy. Protein Eng 12:557–561PubMedGoogle Scholar
  45. 45.
    Barlow DJ, Thornton JM (1988) Helix geometry in proteins. J Mol Biol 201:601–619PubMedGoogle Scholar
  46. 46.
    Reiersen H, Rees AR (2001) The hunchback and its neighbours: proline as an environmental modulator. Trends Biochem Sci 26:679–684PubMedGoogle Scholar
  47. 47.
    Cordes FS, Bright JN, Sansom MSP (2002) Proline-induced distortions of transmembrane helices. J Mol Biol 323:951–960PubMedGoogle Scholar
  48. 48.
    Engelman DM, Steitz TA, Goldman A (1986) Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu Rev Biophys Biophys Chem 15:321–353PubMedGoogle Scholar
  49. 49.
    Koehler J, Woetzel N, Staritzbichler R, Sanders CR, Meiler J (2009) A unified hydrophobicity scale for multi-span membrane proteins. Proteins 76: 13–29PubMedGoogle Scholar
  50. 50.
    Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132PubMedGoogle Scholar
  51. 51.
    Wimely WC, White SH (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat Struct Biol 3:842–848Google Scholar
  52. 52.
    Hessa T, Kim H, Lundin C, Boekel J, Andersson H, Nilsson I, White SH, von Hejne G (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377–381PubMedGoogle Scholar
  53. 53.
    Brosig B, Langosch D (1998) The dimerization motif of the glycophorin A transmembrane segment in membranes: importance of glycine residues. Protein Sci 7:1052–1056PubMedGoogle Scholar
  54. 54.
    Russ WP, Engelman DM (2000) The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol 296:911–919PubMedGoogle Scholar
  55. 55.
    Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin-1. Nature 407:599–605PubMedGoogle Scholar
  56. 56.
    Walters RF, DeGrado WF (2006) Helix-packing motifs in membrane proteins. Proc Natl Acad Sci USA 103:13658–13663PubMedGoogle Scholar
  57. 57.
    Marsico A, Henschel A, Winter C, Tuukkanen A, Vassilev B, Scheubert K, Schroeder M (2010) Structural fragment clustering reveals novel structural and functional motifs in α-helical transmembrane proteins. BMC Bioinformatics 11:204–224PubMedGoogle Scholar
  58. 58.
    White SH, Ladokhin AS, Jayasinghe S, Hristova K (2001) How membranes shape protein structure. J Biol Chem 276:32395–32398PubMedGoogle Scholar
  59. 59.
    White SH, Wimley WC (1999) Membrane protein folding and stability: physical principles. Annu Rev Biophys Biomol Struct 28:319–365PubMedGoogle Scholar
  60. 60.
    Rees DC, DeAntonio L, Eisenberg D (1989) Hydrophobic organization of membrane proteins. Science 245:510–513PubMedGoogle Scholar
  61. 61.
    Beuming T, Weinstein H (2004) A knowledge-based scale for the analysis and prediction of buried and exposed faces of transmembrane domain proteins. Bioinformatics 20:1822–1835PubMedGoogle Scholar
  62. 62.
    Von Heijne G (2006) Membrane-protein topology. Nat Rev Mol Cell Biol 7:909–918Google Scholar
  63. 63.
    Langosch D, Heringa J (1998) Interaction of transmembrane helices by a knobs-into-holes packing characteristic of soluble coiled coils. Proteins 31:150–159PubMedGoogle Scholar
  64. 64.
    Chantalat L, Jones ND, Korber F, Navaza J, Pavlovsky AG (1995) The crystal-structure of wild-type growth-hormone at 2.5 Angstrom resolution. Protein Pept Lett 2:333–340Google Scholar
  65. 65.
    Dobbs AJ, Anderson BF, Faber HR, Baker EN (1996) Three-dimensional structure of cytochrome c′ from two Alcaligenes species and the implications for four-helix bundle structures. Acta Crystallogr D Biol Crystallogr 52:356–368PubMedGoogle Scholar
  66. 66.
    Chang DK, Cheng SF, Trivedi VD, Lin KL (1999) Proline affects oligomerization of a coiled coil by inducing a kink in a long helix. J Struct Biol 128:270–279PubMedGoogle Scholar
  67. 67.
    Woolfson DN, Williams DH (1990) The influence of proline residues on alpha-helical structure. FEBS Lett 277:185–188PubMedGoogle Scholar
  68. 68.
    Von Heijne G (1987) The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J 5:3021–3027Google Scholar
  69. 69.
    Johansson M, Nilsson I, Von Heijne G (1993) Positively charged amino acids placed next to a signal sequence block protein translocation more efficiently in Escherichia coli than in mammalian microsomes. Mol Gen Genet 239:251–256PubMedGoogle Scholar
  70. 70.
    Miyazawa A, Fujiyoshi Y, Unwin N (2003) Structure and gating mechanism of the acetylcholine receptor pore. Nature 423:949–955PubMedGoogle Scholar
  71. 71.
    Amunts A, Drory O, Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447:58–63PubMedGoogle Scholar
  72. 72.
    Brunisholz RA, Zuber H (1992) Structure, function and organization of antenna polypeptides and antenna complexes from the three families of Rhodospirillaneae. J Photochem Photobiol B 15:113–140PubMedGoogle Scholar
  73. 73.
    Davidson AL, Maloney PC (2007) ABC transporters: how small machines do a big job. Trends Microbiol 15:448–455PubMedGoogle Scholar
  74. 74.
    Akopian AN, Sivilotti L, Wood JN (1996) A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379:257–262PubMedGoogle Scholar
  75. 75.
    Andrade SL, Einsle O (2007) The Amt/Mep/Rh family of ammonium transport proteins. Mol Membr Biol 24:357–365PubMedGoogle Scholar
  76. 76.
    Minocha R, Studley K, Saier MH Jr (2003) The urea transporter (UT) family: bioinformatic analyses leading to structural, functional, and evolutionary predictions. Receptors Channels 9:345–352PubMedGoogle Scholar
  77. 77.
    Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS (2003) Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chem 278:41148–41159PubMedGoogle Scholar
  78. 78.
    Schrempf H, Schmidt O, Kümmerlen R, Hinnah S, Müller D, Betzler M, Steinkamp T, Wagner R (1995) A prokaryotic potassium ion channel with two predicted transmembrane segments from Streptomyces lividans. EMBO J 14:5170–5178PubMedGoogle Scholar
  79. 79.
    Agre P, Bonhivers M, Borgnia MJ (1998) The aquaporins, blueprints for cellular plumbing systems. J Biol Chem 273:14659–14662PubMedGoogle Scholar
  80. 80.
    Agre P, Preston GM, Smith BL, Jung JS, Raina S, Moon C, Guggino WB, Nielsen S (1993) Aquaporin CHIP: the archetypal molecular water channel. Am J Physiol 265:463–476Google Scholar
  81. 81.
    Kaldenhoff R, Bertl A, Otto B, Moshelion M, Uehlein N (2007) Characterization of plant aquaporins. Methods Enzymol 428:505–531PubMedGoogle Scholar
  82. 82.
    Gonen T, Walz T (2006) The structure of aquaporins. Q Rev Biophys 39:361–396PubMedGoogle Scholar
  83. 83.
    Driessen AJM, Manting EH, van der Does C (2001) The structural basis of protein targeting and translocation in bacteria. Nat Struct Biol 8:492–498PubMedGoogle Scholar
  84. 84.
    Hedin L, Ojemalm K, Bernsel A, Hennerdal A, Illergard K, Enquist K, Kauko A, Cristobal S, Von Heijne G, Lerch-Bader M, Nilsson I, Elofsson A (2009) Membrane insertion of marginally hydrophobic transmembrane helices depends on sequence context. J Mol Biol 1:221–229Google Scholar
  85. 85.
    Goder V, Spiess M (2001) Topogenesis of membrane proteins: determinants and dynamics. FEBS Lett 504:87–93PubMedGoogle Scholar
  86. 86.
    Lee P, Tullman-Ercek D, Georgiou G (2006) The bacterial twin-arginine translocation pathway. Annu Rev Microbiol 60:373–395PubMedGoogle Scholar
  87. 87.
    Rehling P, Brandner K, Pfanner N (2004) Mitochondrial import and the twin-pore translocase. Nat Rev Mol Cell Biol 5:519–530PubMedGoogle Scholar
  88. 88.
    Emanuelsson O, Elofsson A, Von Heijne G, Cristobal S (2003) In silico prediction of the peroxisomal proteome in fungi, plants and animals. J Mol Biol 330:443–456PubMedGoogle Scholar
  89. 89.
    Popot JL, Engelman DM (1990) Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29:4031–4037PubMedGoogle Scholar
  90. 90.
    Hunt JF, Earnest TN, Bousche O, Kalshathi K, Reilly K, Horvath C, Rothschild KJ, Engelman DM (1997) A biophysical study of integral membrane protein folding. Biochemistry 36:15156–15176PubMedGoogle Scholar
  91. 91.
    White SH (2009) Biophysical dissection of membrane proteins. Nature 459:344–346PubMedGoogle Scholar
  92. 92.
    Kauko A, Hedin L, Thebaud E, Cristobal S, Elofsson A, Von Heijne G (2010) Repositioning of transmembrane alpha-helices during membrane protein folding. J Mol Biol 397:190–201PubMedGoogle Scholar
  93. 93.
    Booth PJ, Curran AR (1999) Membrane protein folding. Curr Opin Struct Biol 9:115–121PubMedGoogle Scholar
  94. 94.
    Waxman SG (2007) Channel, neuronal and clinical function in sodium channelopathies: from genotype to phenotype. Nat Neurosci 10:405–409PubMedGoogle Scholar
  95. 95.
    Turner APF (1997) Switching channels makes sense. Nature 387:555–557PubMedGoogle Scholar
  96. 96.
    Hucho F, Weise C (2001) Ligand-gated ion channels. Angew Chem Int Ed 40:3100–3116Google Scholar
  97. 97.
    Neher E, Sakmann B (1992) The patch clamp technique. Sci Am 266:44–51PubMedGoogle Scholar
  98. 98.
    Cuello LG, Jogini V, Marien Cortes DM, Somporpisut A, Purdy MD, Wiener MC, Perozo E (2010) Design and characterization of a constitutively open KcsA. FEBS Lett 584:1133–1138PubMedGoogle Scholar
  99. 99.
    Beacham DW, Blackmer T, O’Grady M, Hanson GT (2010) Cell-based potassium ion channel screening using the FluxOR assay. J Biomol Screen 15:441–446PubMedGoogle Scholar
  100. 100.
    Galietta LV, Jayaraman S, Verkman AS (2001) Cell-based assay for high-throughput quantitative screening of CFTR chloride transport agonists. Am J Physiol Cell Physiol 281:C1734–C1742PubMedGoogle Scholar
  101. 101.
    Peitz I, Voelker M, Fromherz P (2007) Recombinant serotonin receptor on a transistor as a prototype for cell-based biosensors. Angew Chem Int Ed 46:5787–5790Google Scholar
  102. 102.
    Mach T, Chimerel C, Fritz J, Fertig N, Winterhalter M, Futterer C (2008) Miniaturized planar lipid bilayer: increased stability, low electric noise and fast fluid perfusion. Anal Bioanal Chem 390:841–846PubMedGoogle Scholar
  103. 103.
    Savage DF, Stroud RM (2007) Structural basis of aquaporin inhibition by mercury. J Mol Biol 368:607–617PubMedGoogle Scholar
  104. 104.
    Kumar M, Grzelakowski M, Zilles J, Clark M, Meier W (2007) Highly permeable polymeric membranes based on the incorporation of the functional water channel protein aquaporin Z. Proc Natl Acad Sci 104:20719–20724PubMedGoogle Scholar
  105. 105.
    Hill TR, Taylor BW (2012) Use of aquaporins to achieve needed water purity on the International Space Station for the Extravehicular Mobility Unit Space Suit System. Conference proceedings, conference on environmental systems (ICES), American Institute of Aeronautics and Astronautics, San Diego, 15–19 July 2011Google Scholar
  106. 106.
    Bishop RE (2008) Structural biology of membrane-intrinsic β-barrel enzymes: sentinels of the bacterial outer membrane. Biochim Biophys Acta 1778:1881–1896PubMedGoogle Scholar
  107. 107.
    Montoya M, Gouaux E (2003) Beta-barrel membrane protein folding and structure viewed through the lens of alpha-hemolysin. Biochim Biophys Acta 1666:250–263Google Scholar
  108. 108.
    Saier MH Jr (2000) Families of proteins forming transmembrane channels. J Membr Biol 175:165–180PubMedGoogle Scholar
  109. 109.
    Schulz GE (2002) The structure of bacterial outer membrane proteins. Biochim Biophys Acta 1565:308–317PubMedGoogle Scholar
  110. 110.
    Koebnik R, Locher KP, Van Gelder P (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37:239–253PubMedGoogle Scholar
  111. 111.
    Newcomer ME, Jones TA, Aqvist J, Sundelin J, Eriksson U, Rask L, Peterson PA (1984) The three-dimensional structure of retinol-binding protein. EMBO J 3:1451–1454PubMedGoogle Scholar
  112. 112.
    Galdiero S, Galdiero M, Pedone C (2007) β-barrel membrane bacterial proteins: structure, function, assembly and interaction with lipids. Curr Protein Pept Sci 8:63–82PubMedGoogle Scholar
  113. 113.
    Vogt J, Schulz GE (1999) The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence. Structure 7:1301–1309PubMedGoogle Scholar
  114. 114.
    Clavel T, Germon P, Vianney A, Portalier R, Lazzaroni JC (1998) TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA. Mol Microbiol 29:359–367PubMedGoogle Scholar
  115. 115.
    Prince SM, Achtman M, Derrick JP (2002) Crystal structure of the OpcA integral membrane adhesin from Neisseria meningitidis. Proc Natl Acad Sci USA 99:3417–3421PubMedGoogle Scholar
  116. 116.
    Ye J, Van den Berg B (2004) Crystal structure of the bacterial nucleoside transporter Tsx. EMBO J 23:3187–3195PubMedGoogle Scholar
  117. 117.
    Locher KP, Rees B, Koebnik R, Mitschler A, Moulinier L, Rosenbusch JP, Moras D (1998) Transmembrane signaling across the ligand-gated FhuA receptor: Crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95:771–778PubMedGoogle Scholar
  118. 118.
    Huang Y, Smith BS, Chen LX, Baxter RH, Deisenhofer J (2009) Insights into pilus assembly and secretion from the structure and functional characterization of usher PapC. Proc Natl Acad Sci USA 106:7403–7407PubMedGoogle Scholar
  119. 119.
    Krewinkel M, Dworeck T, Fioroni M (2012) Engineering of an E. coli outer membrane protein FhuA with increased channel diameter. J Nanobiotechnol 9:33Google Scholar
  120. 120.
    Schirmer T, Keller TA, Wang YF, Rosenbusch JP (1995) Structural basis for sugar translocation through maltoporin channels at 3.1 A resolution. Science 267:512–514PubMedGoogle Scholar
  121. 121.
    Buchanan SK (1999) Beta-barrel proteins from bacterial outer membranes: structure, function and refolding. Curr Opin Struct Biol 9:455–461PubMedGoogle Scholar
  122. 122.
    Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274:1859–1866PubMedGoogle Scholar
  123. 123.
    Sakai N, Mareda J, Matile S (2008) Artificial β-barrels. Acc Chem Res 41:1354–1365PubMedGoogle Scholar
  124. 124.
    Lim Y, Lee M (2011) Toroidal β-barrels from self-assembling β-sheet peptides. J Mater Chem 21:11680–11685Google Scholar
  125. 125.
    Gromiha MM, Majumdar R, Ponnuswamy PK (1997) Identification of membrane spanning β strands in bacterial porins. Protein Eng 10:497–500PubMedGoogle Scholar
  126. 126.
    Tamm LK, Hong H, Liang B (2004) Folding and assembly of β-barrel membrane proteins. Biochim Biophys Acta 1666:250–263PubMedGoogle Scholar
  127. 127.
    Seshadri K, Garemyr R, Wallin E, Von Heijne G, Elofsson A (1998) Architecture of β-barrel membrane proteins: analysis of trimeric porins. Protein Sci 7:2026–2032PubMedGoogle Scholar
  128. 128.
    Chou PY, Fasman GD (1977) Beta-turns in proteins. J Mol Biol 115:135–175PubMedGoogle Scholar
  129. 129.
    Sibanda BL, Thornton JM (1986) β-Hairpin families in globular proteins. Nature 316:170–174Google Scholar
  130. 130.
    Chothia C (1973) Conformation of twisted β-pleated sheets in proteins. J Mol Biol 75:295–302PubMedGoogle Scholar
  131. 131.
    Gellmann SH (1998) Minimal model systems for β-sheet secondary structure in proteins. Curr Opin Chem Biol 2:717–725Google Scholar
  132. 132.
    Petsko GA, Ringe D (2004) Protein structure and function. Sinauer Associates, SunderlandGoogle Scholar
  133. 133.
    Stickle DF, Presta LG, Dill KA, Rose GD (1992) Hydrogen bonding in globular proteins. J Mol Biol 226:1143–1159PubMedGoogle Scholar
  134. 134.
    Schulz GE (2000) β-Barrel membrane proteins. Curr Opin Struct Biol 10:443–447PubMedGoogle Scholar
  135. 135.
    Wimley WC (2002) Toward genomic identification of β-barrel membrane proteins: composition and architecture of known structures. Protein Sci 11:301–312PubMedGoogle Scholar
  136. 136.
    Kleinschmidt JH (2006) Folding and stability of monomeric β-barrel membrane proteins. In: Tamm LK (ed) Protein-lipid interactions. Wiley VCH, WeinheimGoogle Scholar
  137. 137.
    Rosenbusch JP (2001) Stability of membrane proteins: relevance for the selection of appropriate methods for high-resolution structure determinations. J Struct Biol 136:144–157PubMedGoogle Scholar
  138. 138.
    Arora A, Abildgaard F, Bushweller JH, Tamm LK (2001) Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat Struct Biol 8:334–338PubMedGoogle Scholar
  139. 139.
    Wimley WC (2003) The versatile β-barrel membrane protein. Curr Opin Struct Biol 13:404–411PubMedGoogle Scholar
  140. 140.
    Naveed H, Jackups R, Liang J (2009) Predicting weakly stable regions, oligomerization state, and protein-protein interfaces in transmembrane domains of outer membrane proteins. Proc Natl Acad Sci 106:12735–12740PubMedGoogle Scholar
  141. 141.
    Evanics F, Hwang P, Cheng Y, Kay L, Prosser R (2006) Topology of an outer-membrane enzyme: measuring oxygen and water contacts in solution NMR studies of PagP. J Am Chem Soc 128:8256–8264PubMedGoogle Scholar
  142. 142.
    Huysmans G, Radford S, Brockwell D, Baldwin S (2007) The N-terminal helix is a post-assembly clamp in the bacterial outer membrane protein PagP. J Mol Biol 373:529–540PubMedGoogle Scholar
  143. 143.
    Koebnik R (1995) Proposal for a peptidoglycan-associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins. Mol Microbiol 16:1269–1270PubMedGoogle Scholar
  144. 144.
    Cowan SW, Garavito RM, Jansonius JN, Jenkins JA, Karlsson R, Konig N, Pai EF, Pauptit RA, Rizkallah PJ, Rosenbach JP (1995) The structure of OmpF porin in a tetragonal crystal form. Structure 3:1041–1050PubMedGoogle Scholar
  145. 145.
    Hill K, Model K, Ryan MT, Dietmeier K, Martin F, Wagner R, Pfanner N (1998) Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature 395:516–521PubMedGoogle Scholar
  146. 146.
    Schleiff E, Soll J, Kuchler M, Kuhlbrandt W, Harrer R (2003) Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol 160:541–551PubMedGoogle Scholar
  147. 147.
    Kleinschmidt JH, Tamm LK (2002) Secondary and tertiary structure formation of the b-barrel membrane protein OmpA is synchronized and depends on membrane thickness. J Mol Biol 324:319–330PubMedGoogle Scholar
  148. 148.
    Wimley WC, Hristova K, Ladokhin AS, Silvestro L, Axelsen PH, White SH (1998) Folding of b-sheet membrane proteins: a hydrophobic hexapeptide model. J Mol Biol 277:1091–1110PubMedGoogle Scholar
  149. 149.
    Ramachandran R, Heuck AP, Tweten RK, Johnson AE (2002) Structural insights into the membrane-anchoring mechanism of a cholesterol-dependent cytolysin. Nat Struct Biol 9:823–827PubMedGoogle Scholar
  150. 150.
    Bayley H (1997) Toxin structure: part of a hole? Curr Biol 7:R763–R767PubMedGoogle Scholar
  151. 151.
    Misra R (2012) Assembly of the β-barrel outer membrane proteins in Gram-negative bacteria, mitochondria, and chloroplasts. ISRN Mol Biol 2012:1–15Google Scholar
  152. 152.
    Holtje JV (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203PubMedGoogle Scholar
  153. 153.
    Beveridge TJ (1999) Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181:4725–4733PubMedGoogle Scholar
  154. 154.
    Tamm LK, Arora A, Kleinschmidt JH (2001) Structure and assembly of beta-barrel membrane proteins. J Biol Chem 276:32399–32402PubMedGoogle Scholar
  155. 155.
    Walther DM, Rapaport D, Tommassen J (2009) Biogenesis of β-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell Mol Life Sci 66:2789–2804PubMedGoogle Scholar
  156. 156.
    Paetzel M, Strynadka NCJ (2001) Signal peptide cleavage in the E. coli membrane. CSBMCB/SCBBMC Bull 2001:60–65Google Scholar
  157. 157.
    Bannwarth M, Schulz GE (2003) The expression of outer membrane proteins for crystallization. Biochim Biophys Acta 1610:37–45PubMedGoogle Scholar
  158. 158.
    Dworeck T, Petri AK, Muhammad N, Fioroni M, Schwaneberg U (2011) FhuA deletion variant Δ1-159 overexpression in inclusion bodies and refolding with Polyethylene-Poly(ethylene glycol) diblock copolymer. Protein Expr Purif 77:75–79PubMedGoogle Scholar
  159. 159.
    Bechtluft P, Nouwen N, Tans SJ, Driessen AJ (2010) SecB – a chaperone dedicated to protein translocation. Mol Biosyst 6:620–627PubMedGoogle Scholar
  160. 160.
    du Plessis DJF, Nouwen N, Driessen AJM (2011) The Sec translocase. Biochim Biophys Acta 1808:851–865PubMedGoogle Scholar
  161. 161.
    Kusters I, Driessen AJ (2011) SecA, a remarkable nanomachine. Cell Mol Life Sci 68:2053–2066PubMedGoogle Scholar
  162. 162.
    Ricci DP, Silhavy TJ (2012) The Bam machine: a molecular cooper. Biochim Biophys Acta 1818:1067–1084PubMedGoogle Scholar
  163. 163.
    Vertommen D, Ruiz N, Leverrier P, Silhavy TJ, Collet JF (2009) Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics. Proteomics 9:2432–2443PubMedGoogle Scholar
  164. 164.
    Rigel NW, Silhavy TJ (2012) Making a beta-barrel: assembly of outer membrane proteins in gram-negative bacteria. Curr Opin Microbiol 15:189–193PubMedGoogle Scholar
  165. 165.
    Schäfer U, Beck K, Müller M (1999) Skp, a molecular chaperone of gram-negative bacteria, is required for the formation of soluble periplasmic intermediates of outer membrane proteins. J Biol Chem 274:24567–24574PubMedGoogle Scholar
  166. 166.
    Booth PJ, Templer RH, Meijberg W, Allen SJ, Curran AR, Lorch M (2001) In vitro studies of membrane protein folding. Crit Rev Biochem Mol Biol 36:501–603PubMedGoogle Scholar
  167. 167.
    Wu T, Malinverni J, Ruiz N, Kim S, Silhavy TJ, Kahne D (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121:235–245PubMedGoogle Scholar
  168. 168.
    Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299:262–265PubMedGoogle Scholar
  169. 169.
    Robert V, Volokhina EB, Senf F, Bos MP, Van Gelder P, Tommassen J (2006) Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol 4:1984–1995Google Scholar
  170. 170.
    Struyve M, Moons M, Tommassen J (1991) Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 218:141–148PubMedGoogle Scholar
  171. 171.
    Kim S, Malinverni JC, Sliz P, Silhavy TJ, Harrison SC, Kahne D (2007) Structure and function of an essential component of the outer membrane protein assembly machine. Science 317:961–964PubMedGoogle Scholar
  172. 172.
    Bullmann L, Haarmann R, Mirus O, Bredemeier R, Hempel F, Maier UG, Schleiff E (2010) Filling the gap, evolutionarily conserved Omp85 in plastids of chromalveolates. J Biol Chem 285:6848–6856PubMedGoogle Scholar
  173. 173.
    Malinverni JC, Werner J, Kim S, Sklar JG, Kahne D, Misra R, Silhavy TJ (2006) YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol Microbiol 61:151–164PubMedGoogle Scholar
  174. 174.
    Hagan CL, Kim S, Kahne D (2010) Reconstitution of outer membrane protein assembly from purified components. Science 14:890–892Google Scholar
  175. 175.
    Hagan CL, Kahne D (2011) The reconstituted Escherichia coli Bam complex catalyzes multiple rounds of β-barrel assembly. Biochemistry 50:7444–7446PubMedGoogle Scholar
  176. 176.
    Kim KH, Aulakh S, Paetzel M (2011) Crystal structure of β-barrel assembly machinery BamCD protein complex. J Biol Chem 286:39116–39121PubMedGoogle Scholar
  177. 177.
    Kim KH, Paetzel M (2011) Crystal structure of Escherichia coli BamB, a lipoprotein component of the β-barrel assembly machinery complex. J Mol Biol 406:667–678PubMedGoogle Scholar
  178. 178.
    Kim KH, Kang HS, Okon M, Escobar-Cabrera E, McIntosh LP, Paetzel M (2011) Structural characterization of Escherichia coli BamE, a lipoprotein component of the β-barrel assembly machinery complex. Biochemistry 50:1081–1090PubMedGoogle Scholar
  179. 179.
    Güven A, Fioroni M, Hauer B, Schwaneberg U (2010) Molecular understanding of sterically controlled compound release through an engineered channel protein (FhuA). J Nanobiotechnol 8:14Google Scholar
  180. 180.
    Güven A, Dworeck T, Fioroni M, Schwaneberg U (2011) Residue K556-A light triggerable gatekeeper to sterically control translocation in FhuA. Adv Eng Mater 13:B324–B329Google Scholar
  181. 181.
    Muhammad N, Dworeck T, Fioroni M, Schwaneberg U (2011) Engineering of the E. coli outer membrane protein FhuA to overcome the hydrophobic mismatch in thick polymeric membranes. J Nanobiotechnol 9:8Google Scholar
  182. 182.
    Nardin C, Meier W (2002) Hybrid materials from amphiphilic block copolymers and membrane proteins. Rev Mol Biotechnol 90:17–26Google Scholar
  183. 183.
    Mohammad M, Iyer R, Howard KR, McPike M, Borer PN, Movileanu L (2012) Engineering a rigid protein tunnel for biomolecular detection. J Am Chem Soc 134:9521–9531PubMedGoogle Scholar
  184. 184.
    Howorka S, Siwy Z (2009) Nanopore analytics: sensing of single molecules. Chem Soc Rev 38:2360–2384PubMedGoogle Scholar
  185. 185.
    Chen M, Khalid S, Sansom MSP, Bayley H (2008) Outer membrane protein G: engineering a quiet pore for biosensing. Proc Natl Acad Sci 105:6272–6277PubMedGoogle Scholar
  186. 186.
    Branton D, Deamer DW, Marziali A, Bayley H, Benner SA, Butler T, Di Ventra M, Garaj S, Hibbs A, Huang X, Jovanovich SB, Krstic PS, Lindsay S, Sean Ling X, Mastrangelo CH, Meller A, Oliver JS, Pershin YV, Ramsey JM, Riehn R, Soni GV, Tabard-Cossa V, Wanunu M, Wiggin M, Schloss JA (2008) The potential and challenges of nanopore sequencing. Nat Biotechnol 26:1146–1153PubMedGoogle Scholar
  187. 187.
    Onoda A, Fukumoto K, Arlt M, Bocola M, Schwaneberg U, Hayashi T (2012) A rhodium complex-linked β-barrel protein as a hybrid biocatalyst for phenylacetylene polymerization. Chem Commun 48:9756–9758Google Scholar
  188. 188.
    Surrey T, Jähnig FJ (1992) Refolding and oriented insertion of a membrane protein into a lipid bilayer. Proc Natl Acad Sci USA 89:7457–7461PubMedGoogle Scholar
  189. 189.
    Surrey T, Schmid A, Jähnig F (1996) Folding and membrane insertion of the trimeric β-barrel protein OmpF. Biochemistry 35:2283–2288PubMedGoogle Scholar
  190. 190.
    Klug CS, Feix JB (1998) Guanidine hydrochloride unfolding of a transmembrane h-strand in FepA using site-directed spin labeling. Protein Sci 7:1469–1476PubMedGoogle Scholar
  191. 191.
    Banerjee S, Huber T, Sakmar T (2008) Rapid incorporation of functional rhodopsin into nanoscale apolipoprotein bound bilayer (NABB) particles. J Mol Biol 377:1067–1081PubMedGoogle Scholar
  192. 192.
    Mohammad M, Howard KR, Movileanu L (2011) Redesign of a plugged β-barrel membrane protein. J Biol Chem 286:8000–8013PubMedGoogle Scholar
  193. 193.
    Onaca O, Sarkar P, Roccatano D, Friedrich T, Hauer B, Grzelakowski M, Güven A, Fioroni M, Schwaneberg U (2008) Functionalized nanocompartments (synthosomes) with a reduction-triggered release system. Angew Chem Int Ed 47:7029–7031Google Scholar
  194. 194.
    Létoffé S, Wecker K, Delepierre M, Delepelaire P, Wandersman C (2005) Activities of the Serratia marcescens heme receptor HasR and isolated plug and β-barrel domains: the β-barrel forms a heme-specific channel. J Bacteriol 187:4637–4645PubMedGoogle Scholar
  195. 195.
    Koebnik R (1999) Membrane assembly of the Escherichia coli outer membrane protein OmpA: exploring sequence constraints on trans-membrane b-strands. J Mol Biol 285:1801–1810PubMedGoogle Scholar
  196. 196.
    Bonhivers M, Desmadril M, Moeck GS, Boulanger P, Colomer-Pallas A, Letellier L (2001) Stability studies of FhuA, a two-domain outer membrane protein from Escherichia coli. Biochemistry 40:2606–2613PubMedGoogle Scholar
  197. 197.
    Klammt C, Schwarz D, Fendler K, Haase W, Dötsch V, Bernhard F (2005) Evaluation of detergents for the soluble expression of a-helical and b-barrel-type integral membrane proteins by a preparative scale individual cell-free expression system. FEBS J 272:6024–6038PubMedGoogle Scholar
  198. 198.
    Briat JF (1992) Iron assimilation and storage in prokaryotes. J Gen Microbiol 138:2475–2483PubMedGoogle Scholar
  199. 199.
    Alfonso-Prieto M, Biarnés X, Vidossich P, Rovira C (2009) The molecular mechanism of the catalase reaction. J Am Chem Soc 131:11751–11761PubMedGoogle Scholar
  200. 200.
    Ratledge C, Dover LG (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881–941PubMedGoogle Scholar
  201. 201.
    Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726PubMedGoogle Scholar
  202. 202.
    Ferguson AD, Deisenhofer J (2002) TonB-dependent receptors – structural perspectives. Biochim Biophys Acta 1565:318–332PubMedGoogle Scholar
  203. 203.
    Lundrigan ML, Kadner RJ (1986) Nucleotide sequence of the gene for the ferrienterochelin receptor FepA in Escherichia coli. Homology among outer membrane receptors that interact with TonB. J Biol Chem 261:10797–10801PubMedGoogle Scholar
  204. 204.
    Pressler U, Staudenmaier H, Zimmermann L, Braun V (1988) Genetics of the iron dicitrate transport system of Escherichia coli. J Bacteriol 170:2716–2724PubMedGoogle Scholar
  205. 205.
    Coulton JW, Mason P, DuBow MS (1983) Molecular cloning of the ferrichrome-iron receptor of Escherichia coli K-12. J Bacteriol 156:1315–1321PubMedGoogle Scholar
  206. 206.
    Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W (1998) Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215–2220PubMedGoogle Scholar
  207. 207.
    Buchanan SK, Smith BS, Venkatramani L, Xia D, Esser L, Palnitkar M, Chakraborty R, van der Helm D, Deisenhofer J (1999) Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat Struct Biol 6:56–62PubMedGoogle Scholar
  208. 208.
    Ferguson AD, Chakraborty R, Smith BS, Esser L, van der Helm D, Deisenhofer J (2002) Structural basis of gating by the outer membrane transporter FecA. Science 295:1658–1659Google Scholar
  209. 209.
    Chakraborty R, Storey E, van der Helm D (2007) Molecular mechanism of ferricsiderophore passage through the outer membrane receptor proteins of Escherichia coli. Biometals 20:263–274PubMedGoogle Scholar
  210. 210.
    Braun V, Schaller K, Wolff H (1973) A common receptor protein for phage T5 and colicin M in the outer membrane of Escherichia coli B. Biochim Biophys Acta 323:87–97PubMedGoogle Scholar
  211. 211.
    Luria SE, Delbrück M (1943) Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28:491–511PubMedGoogle Scholar
  212. 212.
    Hantke K, Braun V (1975) Membrane receptor-dependent iron transport in Escherichia coli. FEBS Lett 49:301–305PubMedGoogle Scholar
  213. 213.
    Kadner RJ, Heller K, Coulton JW, Braun V (1980) Genetic control of hydroxamate-mediated iron uptake in Escherichia coli. J Bacteriol 143:256–264PubMedGoogle Scholar
  214. 214.
    Bonhivers M, Ghazi A, Boulanger P, Letellier L (1996) FhuA, a transporter of the Escherichia coli outer membrane, is converted into a channel upon binding of bacteriophage T5. EMBO J 15:1850–1856PubMedGoogle Scholar
  215. 215.
    Braun M, Killmann H, Maier E, Benz R, Braun V (2002) Diffusion through channel derivatives of the Escherichia coli FhuA transport protein. Eur J Biochem 269:4948–4959PubMedGoogle Scholar
  216. 216.
    Braun M, Killmann H, Braun V (1999) The beta-barrel domain of FhuADelta5-160 is sufficient for TonB-dependent FhuA activities of Escherichia coli. Mol Microbiol 33:1037–1049PubMedGoogle Scholar
  217. 217.
    Killmann H, Herrmann C, Torun A, Jung G, Braun V (2002) TonB of Escherichia coli activates FhuA through interaction with the β-barrel. Microbiology 148:3497–3509PubMedGoogle Scholar
  218. 218.
    Pawelek PD, Croteau N, Ng-Thow-Hing C, Khursigara CM, Moiseeva N, Allaire M, Coulton JW (2006) Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312:1399–1402PubMedGoogle Scholar
  219. 219.
    Braun V, Braun M (2002) Iron transport and signaling in E. coli. FEBS Lett 529:78–85PubMedGoogle Scholar
  220. 220.
    Eisenhauer HA, Shames S, Pawelek PD, Coulton JW (2005) Siderophore transport through Escherichia coli outer membrane receptor FhuA with disulfide-tethered cork and barrel domains. J Biol Chem 280:30574–30580PubMedGoogle Scholar
  221. 221.
    Ma L, Kaserer W, Annamalai R, Scott DC, Jin B, Jiang X, Xiao Q, Maymani H, Massis LM, Ferreira LC, Newton SM, Klebba PE (2007) Evidence of ball-and-chain transport of ferric enterobactin through FepA. J Biol Chem 282:397–406PubMedGoogle Scholar
  222. 222.
    Udho E, Jakes KS, Finkelstein A (2012) TonB-dependent transporter FhuA in planar lipid bilayers: partial exit of its plug from the barrel. Biochemistry 51:6753–6759PubMedGoogle Scholar
  223. 223.
    Bertin A, de Frutos M, Letellier L (2011) Bacteriophage-host interactions leading to genome internalization. Curr Opin Microbiol 14:492–496PubMedGoogle Scholar
  224. 224.
    Böhm J, Lambert O, Frangakis AS, Letellier L, Baumeister W, Rigaud JL (2001) FhuA-mediated phage genome transfer into liposomes: a cryo-electron tomography study. Curr Biol 11:1168–1175PubMedGoogle Scholar
  225. 225.
    Faraldo-Gómez JD, Smith GR, Sansom MSP (2003) Molecular dynamics simulations of the bacterial outer membrane protein FhuA: a comparative study of the ferrichrome-free and bound states. Biophys J 85:1406–1420PubMedGoogle Scholar
  226. 226.
    Locher KP, Rosenbusch JP (1997) Oligomeric states and siderophore binding of the ligand-gated FhuA protein that forms channels across Escherichia coli outer membranes. Eur J Biochem 247:770–775PubMedGoogle Scholar
  227. 227.
    Ferguson AD, Breed J, Diederichs K, Welte W, Coulton JW (1998) An internal affinity-tag for purification and crystallization of the siderophore receptor FhuA, integral outer membrane protein from Escherichia coli K-12. Protein Sci 7:1636–1638PubMedGoogle Scholar
  228. 228.
    Plancon L, Chami M, Letellier L (1997) Reconstitution of FhuA, an Escherichia coli outer membrane protein, into liposomes. Binding of phage T5 to Fhua triggers the transfer of DNA into the proteoliposomes. J Biol Chem 272:16868–16872PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Marco Fioroni
    • 1
  • Tamara Dworeck
    • 2
  • Francisco Rodríguez-Ropero
    • 3
  1. 1.Sustainable MomentumAachenGermany
  2. 2.Department of BiologyRWTH Aachen UniversityAachenGermany
  3. 3.Center of Smart InterfacesTechnische Universität DarmstadtDarmstadtGermany

Personalised recommendations