Cellular and Molecular Life Sciences

, Volume 66, Issue 19, pp 3111–3126

The ATP-binding cassette family: a structural perspective

Review

Abstract

The ATP-binding cassette family is one of the largest groupings of membrane proteins, moving allocrites across lipid membranes, using energy from ATP. In bacteria, they reside in the inner membrane and are involved in both uptake and export. In eukaryotes, these transporters reside in the cell’s internal membranes as well as in the plasma membrane and are unidirectional—out of the cytoplasm. The range of substances that these proteins can transport is huge, which makes them interesting for structure–function studies. Moreover, their abundance in nature has made them targets for structural proteomics consortia. There are eight independent structures for ATP-binding cassette transporters, making this one of the best characterised membrane protein families. Our understanding of the mechanism of transport across membranes and membrane protein structure in general has been enhanced by recent developments for this family.

Keywords

ATP-binding cassette Membrane protein Structure Transporter Lipid bilayer 

References

  1. 1.
    Fuellen G, Spitzer M, Cullen P, Lorkowski S (2005) Correspondence of function and phylogeny of ABC proteins based on an automated analysis of 20 model protein data sets. Proteins 61:888–899PubMedCrossRefGoogle Scholar
  2. 2.
    Chen CJ, Chin JE, Ueda K, Clark DP, Pastan I, Gottesman MM, Roninson IB (1986) Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47:381–389PubMedCrossRefGoogle Scholar
  3. 3.
    Gros P, Croop J, Housman D (1986) Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell 47:371–380PubMedCrossRefGoogle Scholar
  4. 4.
    Dean M, Hamon Y, Chimini G (2001) The human ATP-binding cassette (ABC) transporter superfamily. J Lipid Res 42:1007–1017PubMedGoogle Scholar
  5. 5.
    Rees DC, Johnson E, Lewinson O (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10:218–227PubMedCrossRefGoogle Scholar
  6. 6.
    Linton KJ, Higgins CF (1998) The Escherichia coli ATP-binding cassette (ABC) proteins. Mol Microbiol 28:5–13PubMedCrossRefGoogle Scholar
  7. 7.
    Dassa E, Bouige P (2001) The ABC of ABCS: a phylogenetic and functional classification of ABC systems in living organisms. Res Microbiol 152:211–229PubMedCrossRefGoogle Scholar
  8. 8.
    Bouige P, Laurent D, Piloyan L, Dassa E (2002) Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr Protein Pept Sci 3:541–559PubMedCrossRefGoogle Scholar
  9. 9.
    Cogdell RJ, Gardiner AT, Hashimoto H, Brotosudarmo TH (2008) A comparative look at the first few milliseconds of the light reactions of photosynthesis. Photochem Photobiol Sci 7:1150–1158PubMedCrossRefGoogle Scholar
  10. 10.
    Oldham ML, Khare D, Quiocho FA, Davidson AL, Chen J (2007) Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450:515–521PubMedCrossRefGoogle Scholar
  11. 11.
    Locher KP, Lee AT, Rees DC (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296:1091–1098PubMedCrossRefGoogle Scholar
  12. 12.
    Pinkett HW, Lee AT, Lum P, Locher KP, Rees DC (2007) An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science 315:373–377PubMedCrossRefGoogle Scholar
  13. 13.
    Mourez M, Hofnung M, Dassa E (1997) Subunit interactions in ABC transporters: a conserved sequence in hydrophobic membrane proteins of periplasmic permeases defines an important site of interaction with the ATPase subunits. EMBO J 16:3066–3077PubMedCrossRefGoogle Scholar
  14. 14.
    Story RM, Steitz TA (1992) Structure of the recA protein-ADP complex. Nature 355:374–376PubMedCrossRefGoogle Scholar
  15. 15.
    Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113PubMedCrossRefGoogle Scholar
  16. 16.
    Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases, and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1:945–951PubMedGoogle Scholar
  17. 17.
    Ambudkar SV, Kim IW, Xia D, Sauna ZE (2006) The A-loop, a novel conserved aromatic acid subdomain upstream of the Walker A motif in ABC transporters, is critical for ATP binding. FEBS Lett 580:1049–1055PubMedCrossRefGoogle Scholar
  18. 18.
    Kim IW, Peng XH, Sauna ZE, FitzGerald PC, Xia D, Muller M, Nandigama K, Ambudkar SV (2006) The conserved tyrosine residues 401 and 1044 in ATP sites of human P-glycoprotein are critical for ATP binding and hydrolysis: evidence for a conserved subdomain, the A-loop in the ATP-binding cassette. Biochemistry 45:7605–7616PubMedCrossRefGoogle Scholar
  19. 19.
    Moody JE, Millen L, Binns D, Hunt JF, Thomas PJ (2002) Cooperative, ATP-dependent association of the nucleotide binding cassettes during the catalytic cycle of ATP-binding cassette transporters. J Biol Chem 277:21111–21114PubMedCrossRefGoogle Scholar
  20. 20.
    Zaitseva J, Jenewein S, Jumpertz T, Holland IB, Schmitt L (2005) H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J 24:1901–1910PubMedCrossRefGoogle Scholar
  21. 21.
    Chen J, Lu G, Lin J, Davidson AL, Quiocho FA (2003) A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol Cell 12:651–661PubMedCrossRefGoogle Scholar
  22. 22.
    Smith PC, Karpowich N, Millen L, Moody JE, Rosen J, Thomas PJ, Hunt JF (2002) ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol Cell 10:139–149PubMedCrossRefGoogle Scholar
  23. 23.
    Hopfner KP, Karcher A, Shin DS, Craig L, Arthur LM, Carney JP, Tainer JA (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101:789–800PubMedCrossRefGoogle Scholar
  24. 24.
    Hopfner KP, Tainer JA (2003) Rad50/SMC proteins and ABC transporters: unifying concepts from high-resolution structures. Curr Opin Struct Biol 13:249–255PubMedCrossRefGoogle Scholar
  25. 25.
    Schmitt L, Benabdelhak H, Blight MA, Holland IB, Stubbs MT (2003) Crystal structure of the nucleotide-binding domain of the ABC-transporter haemolysin B: identification of a variable region within ABC helical domains. J Mol Biol 330:333–342PubMedCrossRefGoogle Scholar
  26. 26.
    Hollenstein K, Dawson RJ, Locher KP (2007) Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 17:412–418PubMedCrossRefGoogle Scholar
  27. 27.
    Dawson RJ, Locher KP (2006) Structure of a bacterial multidrug ABC transporter. Nature 443:180–185PubMedCrossRefGoogle Scholar
  28. 28.
    Hollenstein K, Frei DC, Locher KP (2007) Structure of an ABC transporter in complex with its binding protein. Nature 446:213–216PubMedCrossRefGoogle Scholar
  29. 29.
    Kadaba NS, Kaiser JT, Johnson E, Lee A, Rees DC (2008) The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 321:250–253PubMedCrossRefGoogle Scholar
  30. 30.
    Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, Harrell PM, Trinh YT, Zhang Q, Urbatsch IL, Chang G (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323:1718–1722PubMedCrossRefGoogle Scholar
  31. 31.
    Hung LW, Wang IX, Nikaido K, Liu PQ, Ames GF, Kim SH (1998) Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396:703–707PubMedCrossRefGoogle Scholar
  32. 32.
    Jones PM, George AM (1999) Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol Lett 179:187–202PubMedCrossRefGoogle Scholar
  33. 33.
    Diederichs K, Diez J, Greller G, Muller C, Breed J, Schnell C, Vonrhein C, Boos W, Welte W (2000) Crystal structure of MalK, the ATPase subunit of the trehalose/maltose ABC transporter of the archaeon Thermococcus litoralis. EMBO J 19:5951–5961PubMedCrossRefGoogle Scholar
  34. 34.
    Fetsch EE, Davidson AL (2002) Vanadate-catalyzed photocleavage of the signature motif of an ATP-binding cassette (ABC) transporter. Proc Natl Acad Sci USA 99:9685–9690PubMedCrossRefGoogle Scholar
  35. 35.
    Cremo CR, Loo JA, Edmonds CG, Hatlelid KM (1992) Vanadate catalyzes photocleavage of adenylate kinase at proline-17 in the phosphate-binding loop. Biochemistry 31:491–497PubMedCrossRefGoogle Scholar
  36. 36.
    Grammer JC, Loo JA, Edmonds CG, Cremo CR, Yount RG (1996) Chemistry and mechanism of vanadate-promoted photooxidative cleavage of myosin. Biochemistry 35:15582–15592PubMedCrossRefGoogle Scholar
  37. 37.
    Ko YH, Bianchet M, Amzel LM, Pedersen PL (1997) Novel insights into the chemical mechanism of ATP synthase. Evidence that in the transition state the gamma-phosphate of ATP is near the conserved alanine within the P-loop of the beta-subunit. J Biol Chem 272:18875–18881PubMedCrossRefGoogle Scholar
  38. 38.
    Loo TW, Clarke DM (2002) Vanadate trapping of nucleotide at the ATP-binding sites of human multidrug resistance P-glycoprotein exposes different residues to the drug-binding site. Proc Natl Acad Sci USA 99:3511–3516PubMedCrossRefGoogle Scholar
  39. 39.
    Zaitseva J, Oswald C, Jumpertz T, Jenewein S, Wiedenmann A, Holland IB, Schmitt L (2006) A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer. EMBO J 25:3432–3443PubMedCrossRefGoogle Scholar
  40. 40.
    Linton KJ, Higgins CF (2007) Structure and function of ABC transporters: the ATP switch provides flexible control. Pflugers Arch 453:555–567PubMedCrossRefGoogle Scholar
  41. 41.
    Dawson RJ, Hollenstein K, Locher KP (2007) Uptake or extrusion: crystal structures of full ABC transporters suggest a common mechanism. Mol Microbiol 65:250–257PubMedCrossRefGoogle Scholar
  42. 42.
    Hvorup RN, Goetz BA, Niederer M, Hollenstein K, Perozo E, Locher KP (2007) Asymmetry in the structure of the ABC transporter-binding protein complex BtuCD-BtuF. Science 317:1387–1390PubMedCrossRefGoogle Scholar
  43. 43.
    Ward A, Reyes CL, Yu J, Roth CB, Chang G (2007) Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc Natl Acad Sci USA 104:19005–19010PubMedCrossRefGoogle Scholar
  44. 44.
    Gerber S, Comellas-Bigler M, Goetz BA, Locher KP (2008) Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science 321:246–250PubMedCrossRefGoogle Scholar
  45. 45.
    Rosenberg MF, Callaghan R, Ford RC, Higgins CF (1997) Structure of the multidrug resistance P-glycoprotein to 2.5 nm resolution determined by electron microscopy and image analysis. J Biol Chem 272:10685–10694PubMedCrossRefGoogle Scholar
  46. 46.
    Rosenberg MF, Velarde G, Ford RC, Martin C, Berridge G, Kerr ID, Callaghan R, Schmidlin A, Wooding C, Linton KJ, Higgins CF (2001) Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle. EMBO J 20:5615–5625PubMedCrossRefGoogle Scholar
  47. 47.
    Rosenberg MF, Mao Q, Holzenburg A, Ford RC, Deeley RG, Cole SP (2001) The structure of the multidrug resistance protein 1 (MRP1/ABCC1). Crystallization and single-particle analysis. J Biol Chem 276:16076–16082PubMedCrossRefGoogle Scholar
  48. 48.
    Rosenberg MF, Kamis AB, Callaghan R, Higgins CF, Ford RC (2003) Three-dimensional structures of the mammalian multidrug resistance P-glycoprotein demonstrate major conformational changes in the transmembrane domains upon nucleotide binding. J Biol Chem 278:8294–8299PubMedCrossRefGoogle Scholar
  49. 49.
    Rosenberg MF, Kamis AB, Aleksandrov LA, Ford RC, Riordan JR (2004) Purification and crystallization of the cystic fibrosis transmembrane conductance regulator (CFTR). J Biol Chem 279:39051–39057PubMedCrossRefGoogle Scholar
  50. 50.
    Rosenberg MF, Callaghan R, Modok S, Higgins CF, Ford RC (2005) Three-dimensional structure of P-glycoprotein: the transmembrane regions adopt an asymmetric configuration in the nucleotide-bound state. J Biol Chem 280:2857–2862PubMedCrossRefGoogle Scholar
  51. 51.
    Ward A, Mulligan S, Carragher B, Chang G, Milligan RA (2009) Nucleotide dependent packing differences in helical crystals of the ABC transporter MsbA. J Struct Biol 165:169–175PubMedCrossRefGoogle Scholar
  52. 52.
    Chami M, Steinfels E, Orelle C, Jault JM, Di Pietro A, Rigaud JL, Marco S (2002) Three-dimensional structure by cryo-electron microscopy of YvcC, an homodimeric ATP-binding cassette transporter from Bacillus subtilis. J Mol Biol 315:1075–1085PubMedCrossRefGoogle Scholar
  53. 53.
    Ferreira-Pereira A, Marco S, Decottignies A, Nader J, Goffeau A, Rigaud JL (2003) Three-dimensional reconstruction of the Saccharomyces cerevisiae multidrug resistance protein Pdr5p. J Biol Chem 278:11995–11999PubMedCrossRefGoogle Scholar
  54. 54.
    Lee JY, Urbatsch IL, Senior AE, Wilkens S (2002) Projection structure of P-glycoprotein by electron microscopy. Evidence for a closed conformation of the nucleotide binding domains. J Biol Chem 277:40125–40131PubMedCrossRefGoogle Scholar
  55. 55.
    McDevitt CA, Shintre CA, Grossmann JG, Pollock NL, Prince SM, Callaghan R, Ford RC (2008) Structural insights into P-glycoprotein (ABCB1) by small angle X-ray scattering and electron crystallography. FEBS Lett 582:2950–2956PubMedCrossRefGoogle Scholar
  56. 56.
    Procko E, Gaudet R (2008) Functionally important interactions between the nucleotide-binding domains of an antigenic peptide transporter. Biochemistry 47:5699–5708PubMedCrossRefGoogle Scholar
  57. 57.
    Oldham ML, Davidson AL, Chen J (2008) Structural insights into ABC transporter mechanism. Curr Opin Struct Biol 18:726–733PubMedCrossRefGoogle Scholar
  58. 58.
    Khare D, Oldham ML, Orelle C, Davidson AL, Chen J (2009) Alternating access in maltose transporter mediated by rigid-body rotations. Mol Cell 33:528–536PubMedCrossRefGoogle Scholar
  59. 59.
    Callaghan R, Ford RC, Kerr ID (2006) The translocation mechanism of P-glycoprotein. FEBS Lett 580:1056–1063PubMedCrossRefGoogle Scholar
  60. 60.
    Higgins CF, Linton KJ (2004) The ATP switch model for ABC transporters. Nat Struct Mol Biol 11:918–926PubMedCrossRefGoogle Scholar
  61. 61.
    Senior AE, al-Shawi MK, Urbatsch IL (1995) The catalytic cycle of P-glycoprotein. FEBS Lett 377:285–289PubMedCrossRefGoogle Scholar
  62. 62.
    Lugo MR, Sharom FJ (2005) Interaction of LDS-751 with P-glycoprotein and mapping of the location of the R drug binding site. Biochemistry 44:643–655PubMedCrossRefGoogle Scholar
  63. 63.
    Qu Q, Sharom FJ (2002) Proximity of bound Hoechst 33342 to the ATPase catalytic sites places the drug binding site of P-glycoprotein within the cytoplasmic membrane leaflet. Biochemistry 41:4744–4752PubMedCrossRefGoogle Scholar
  64. 64.
    Siarheyeva A, Sharom FJ (2009) The ABC transporter MsbA interacts with lipid A and amphipathic drugs at different sites. Biochem J 419:317–328PubMedCrossRefGoogle Scholar
  65. 65.
    Smriti Zou P, McHaourab HS (2009) Mapping daunorubicin binding sites in the ABC transporter MsbA using site-specific quenching by spin labels. J Biol Chem 284:13904–13913CrossRefGoogle Scholar
  66. 66.
    Biemans-Oldehinkel E, Doeven MK, Poolman B (2006) ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett 580:1023–1035PubMedCrossRefGoogle Scholar
  67. 67.
    Orelle C, Ayvaz T, Everly RM, Klug CS, Davidson AL (2008) Both maltose-binding protein and ATP are required for nucleotide-binding domain closure in the intact maltose ABC transporter. Proc Natl Acad Sci USA 105:12837–12842PubMedCrossRefGoogle Scholar
  68. 68.
    Shilton BH (2008) The dynamics of the MBP–MalFGK(2) interaction: a prototype for binding protein dependent ABC-transporter systems. Biochim Biophys Acta 1778:1772–1780PubMedCrossRefGoogle Scholar
  69. 69.
    Ivetac A, Campbell JD, Sansom MS (2007) Dynamics and function in a bacterial ABC transporter: simulation studies of the BtuCDF system and its components. Biochemistry 46:2767–2778PubMedCrossRefGoogle Scholar
  70. 70.
    Panagiotidis CH, Boos W, Shuman HA (1998) The ATP-binding cassette subunit of the maltose transporter MalK antagonizes MalT, the activator of the Escherichia coli mal regulon. Mol Microbiol 30:535–546PubMedCrossRefGoogle Scholar
  71. 71.
    Bohm A, Boos W (2004) Gene regulation in prokaryotes by subcellular relocalization of transcription factors. Curr Opin Microbiol 7:151–156PubMedCrossRefGoogle Scholar
  72. 72.
    Richet E, Joly N, Danot O (2005) Two domains of MalT, the activator of the Escherichia coli maltose regulon, bear determinants essential for anti-activation by MalK. J Mol Biol 347:1–10PubMedCrossRefGoogle Scholar
  73. 73.
    Bohm A, Diez J, Diederichs K, Welte W, Boos W (2002) Structural model of MalK, the ABC subunit of the maltose transporter of Escherichia coli: implications for mal gene regulation, inducer exclusion, and subunit assembly. J Biol Chem 277:3708–3717PubMedCrossRefGoogle Scholar
  74. 74.
    Samanta S, Ayvaz T, Reyes M, Shuman HA, Chen J, Davidson AL (2003) Disulfide cross-linking reveals a site of stable interaction between C-terminal regulatory domains of the two MalK subunits in the maltose transport complex. J Biol Chem 278:35265–35271PubMedCrossRefGoogle Scholar
  75. 75.
    Dean DA, Reizer J, Nikaido H, Saier MH Jr (1990) Regulation of the maltose transport system of Escherichia coli by the glucose-specific enzyme III of the phosphoenolpyruvate-sugar phosphotransferase system. Characterization of inducer exclusion-resistant mutants and reconstitution of inducer exclusion in proteoliposomes. J Biol Chem 265:21005–21010PubMedGoogle Scholar
  76. 76.
    Stein A, Seifert M, Volkmer-Engert R, Siepelmeyer J, Jahreis K, Schneider E (2002) Functional characterization of the maltose ATP-binding-cassette transporter of Salmonella typhimurium by means of monoclonal antibodies directed against the MalK subunit. Eur J Biochem 269:4074–4085PubMedCrossRefGoogle Scholar
  77. 77.
    Benabdelhak H, Kiontke S, Horn C, Ernst R, Blight MA, Holland IB, Schmitt L (2003) A specific interaction between the NBD of the ABC-transporter HlyB and a C-terminal fragment of its transport substrate haemolysin A. J Mol Biol 327:1169–1179PubMedCrossRefGoogle Scholar
  78. 78.
    Cuthbertson L, Kimber MS, Whitfield C (2007) Substrate binding by a bacterial ABC transporter involved in polysaccharide export. Proc Natl Acad Sci USA 104:19529–19534PubMedCrossRefGoogle Scholar
  79. 79.
    Patzlaff JS, van der Heide T, Poolman B (2003) The ATP/substrate stoichiometry of the ATP-binding cassette (ABC) transporter OpuA. J Biol Chem 278:29546–29551PubMedCrossRefGoogle Scholar
  80. 80.
    Linton KJ (2007) Structure and function of ABC transporters. Physiology (Bethesda) 22:122–130Google Scholar
  81. 81.
    Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774–797PubMedCrossRefGoogle Scholar
  82. 82.
    Pakotiprapha D, Inuzuka Y, Bowman BR, Moolenaar GF, Goosen N, Jeruzalmi D, Verdine GL (2008) Crystal structure of Bacillus stearothermophilus UvrA provides insight into ATP-modulated dimerization, UvrB interaction, and DNA binding. Mol Cell 29:122–133PubMedCrossRefGoogle Scholar
  83. 83.
    Dean M, Annilo T (2005) Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 6:123–142PubMedCrossRefGoogle Scholar
  84. 84.
    Ramaen O, Leulliot N, Sizun C, Ulryck N, Pamlard O, Lallemand JY, Tilbeurgh H, Jacquet E (2006) Structure of the human multidrug resistance protein 1 nucleotide binding domain 1 bound to Mg2+/ATP reveals a non-productive catalytic site. J Mol Biol 359:940–949PubMedCrossRefGoogle Scholar
  85. 85.
    Gaudet R, Wiley DC (2001) Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J 20:4964–4972PubMedCrossRefGoogle Scholar
  86. 86.
    Lewis HA, Buchanan SG, Burley SK, Conners K, Dickey M, Dorwart M, Fowler R, Gao X, Guggino WB, Hendrickson WA, Hunt JF, Kearins MC, Lorimer D, Maloney PC, Post KW, Rajashankar KR, Rutter ME, Sauder JM, Shriver S, Thibodeau PH, Thomas PJ, Zhang M, Zhao X, Emtage S (2004) Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J 23:282–293PubMedCrossRefGoogle Scholar
  87. 87.
    Gonen T, Cheng Y, Sliz P, Hiroaki Y, Fujiyoshi Y, Harrison SC, Walz T (2005) Lipid–protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438:633–638PubMedCrossRefGoogle Scholar
  88. 88.
    Harries WE, Akhavan D, Miercke LJ, Khademi S, Stroud RM (2004) The channel architecture of aquaporin 0 at a 2.2-A resolution. Proc Natl Acad Sci USA 101:14045–14050PubMedCrossRefGoogle Scholar
  89. 89.
    de Groot BL, Engel A, Grubmuller H (2003) The structure of the aquaporin-1 water channel: a comparison between cryo-electron microscopy and X-ray crystallography. J Mol Biol 325:485–493PubMedCrossRefGoogle Scholar
  90. 90.
    Lee JY, Urbatsch IL, Senior AE, Wilkens S (2008) Nucleotide-induced structural changes in P-glycoprotein observed by electron microscopy. J Biol Chem 283:5769–5779PubMedCrossRefGoogle Scholar
  91. 91.
    Eskandari S, Wright EM, Kreman M, Starace DM, Zampighi GA (1998) Structural analysis of cloned plasma membrane proteins by freeze-fracture electron microscopy. Proc Natl Acad Sci USA 95:11235–11240PubMedCrossRefGoogle Scholar
  92. 92.
    Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317–364PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  1. 1.Department of Molecular and Cellular Biology, College of Biological SciencesUniversity of GuelphGuelphCanada
  2. 2.Faculty of Life Sciences, Manchester Interdisplinary BiocentreThe University of ManchesterManchesterUK

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