Advertisement

The Maltose ABC Transporter: Where Structure Meets Function

  • Cédric Orelle
  • Michael L. Oldham
  • Amy L. Davidson
Chapter
Part of the Springer Series in Biophysics book series (BIOPHYSICS, volume 17)

Abstract

ATP-binding cassette (ABC) transporters mediate active transport of a variety of substrates across biological membranes. The long studied maltose importer from Escherichia coli has provided a wealth of biochemical and genetic information, making it an attractive target for structure determination. The maltose transporter is a complex composed of a heterodimer of transmembrane subunits and a nucleotide-binding subunit homodimer that together function in concert with a periplasmic-binding protein, responsible for delivery of maltose to the transporter. The complex has now been crystallized in multiple states along the translocation pathway. Functional studies were key for stabilizing the transporter in these conformational states, validating the structures and understanding the molecular mechanism of transport. ATP hydrolysis and substrate transport are coupled via concerted conformational changes spanning the bilayer that result in alternating access of the substrate-binding site to either side of the membrane. Although the detailed dynamics of the complex remain to be revealed, we illustrate here how the interplay between biochemical, biophysical, and structural studies established the maltose transporter as one of the best characterized proteins of the ABC family. While many of these molecular insights are relevant to the entire ABC transporter family, some mechanistic features may differ between subclasses, highlighting the extraordinary diversity of ABC proteins and the need for further structure/function analyses.

Keywords

ATP hydrolysis Electron Paramagnetic Resonance (EPR) Transition state Inducer exclusion Maltodextrin Allostery 

References

  1. Alvarez FJ, Orelle C, Davidson AL (2010) Functional reconstitution of an ABC transporter in nanodiscs for use in electron paramagnetic resonance spectroscopy. J Am Chem Soc 132(28):9513–9515PubMedCentralPubMedGoogle Scholar
  2. Austermuhle MI, Hall JA, Klug CS, Davidson AL (2004) Maltose-binding protein is open in the catalytic transition state for ATP hydrolysis during maltose transport. J Biol Chem 279(27):28243–28250PubMedGoogle Scholar
  3. Biemans-Oldehinkel E, Doeven MK, Poolman B (2006) ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett 580(4):1023–1035PubMedGoogle Scholar
  4. Bishop L, Agbayani R Jr, Ambudkar SV, Maloney PC, Ames GF (1989) Reconstitution of a bacterial periplasmic permease in proteoliposomes and demonstration of ATP hydrolysis concomitant with transport. Proc Natl Acad Sci U S A 86(18):6953–6957PubMedCentralPubMedGoogle Scholar
  5. Bluschke B, Volkmer-Engert R, Schneider E (2006) Topography of the surface of the signal-transducing protein EIIA(Glc) that interacts with the MalK subunits of the maltose ATP-binding cassette transporter (MalFGK2) of Salmonella typhimurium. J Biol Chem 281(18):12833–12840. doi: 10.1074/jbc.M512646200 PubMedGoogle Scholar
  6. Bohm S, Licht A, Wuttge S, Schneider E, Bordignon E (2013) Conformational plasticity of the type I maltose ABC importer. Proc Natl Acad Sci U S A 110(14):5492–5497. doi: 10.1073/pnas.1217745110 PubMedCentralPubMedGoogle Scholar
  7. Boos W, Shuman H (1998) Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol Mol Biol Rev 62(1):204–229PubMedCentralPubMedGoogle Scholar
  8. Borths EL, Poolman B, Hvorup RN, Locher KP, Rees DC (2005) In vitro functional characterization of BtuCD-F, the Escherichia coli ABC transporter for vitamin B12 uptake. Biochemistry 44(49):16301–16309PubMedGoogle Scholar
  9. Bouige P, Laurent D, Piloyan L, Dassa E (2002) Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr Protein Pept Sci 3(5):541–559PubMedGoogle Scholar
  10. Chen J, Sharma S, Quiocho FA, Davidson AL (2001) Trapping the transition state of an ATP-binding cassette transporter: evidence for a concerted mechanism of maltose transport. Proc Natl Acad Sci U S A 98(4):1525–1530PubMedCentralPubMedGoogle Scholar
  11. 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(3):651–661PubMedGoogle Scholar
  12. Chen S, Oldham ML, Davidson AL, Chen J (2013) Carbon catabolite repression of the maltose transporter revealed by X-ray crystallography. Nature 499(7458):364–368PubMedGoogle Scholar
  13. Cui J, Davidson AL (2011) ABC solute importers in bacteria. Essays Biochem 50(1):85–99PubMedGoogle Scholar
  14. Cui J, Qasim S, Davidson AL (2010) Uncoupling substrate transport from ATP hydrolysis in the Escherichia coli maltose transporter. J Biol Chem 285(51):39986–39993PubMedCentralPubMedGoogle Scholar
  15. Dassa E (2011) Natural history of ABC systems: not only transporters. Essays Biochem 50(1):19–42PubMedGoogle Scholar
  16. Dassa E, Bouige P (2001) The ABC of ABCS: a phylogenetic and functional classification of ABC systems in living organisms. Res Microbiol 152(3–4):211–229PubMedGoogle Scholar
  17. Dassa E, Hofnung M (1985) Sequence of gene malG in E. coli K12: homologies between integral membrane components from binding protein-dependent transport systems. EMBO J 4(9):2287–2293PubMedCentralPubMedGoogle Scholar
  18. Daus ML, Landmesser H, Schlosser A, Muller P, Herrmann A, Schneider E (2006) ATP induces conformational changes of periplasmic loop regions of the maltose ATP-binding cassette transporter. J Biol Chem 281(7):3856–3865PubMedGoogle Scholar
  19. Daus ML, Berendt S, Wuttge S, Schneider E (2007a) Maltose binding protein (MalE) interacts with periplasmic loops P2 and P1 respectively of the MalFG subunits of the maltose ATP binding cassette transporter (MalFGK(2)) from Escherichia coli/Salmonella during the transport cycle. Mol Microbiol 66(5):1107–1122PubMedGoogle Scholar
  20. Daus ML, Grote M, Muller P, Doebber M, Herrmann A, Steinhoff HJ, Dassa E, Schneider E (2007b) ATP-driven MalK dimer closure and reopening and conformational changes of the "EAA" motifs are crucial for function of the maltose ATP-binding cassette transporter (MalFGK2). J Biol Chem 282(31):22387–22396PubMedGoogle Scholar
  21. Daus ML, Grote M, Schneider E (2009) The MalF P2 loop of the ATP-binding cassette transporter MalFGK2 from Escherichia coli and Salmonella enterica serovar typhimurium interacts with maltose binding protein (MalE) throughout the catalytic cycle. J Bacteriol 191(3):754–761PubMedCentralPubMedGoogle Scholar
  22. Davidson AL, Nikaido H (1990) Overproduction, solubilization, and reconstitution of the maltose transport system from Escherichia coli. J Biol Chem 265(8):4254–4260PubMedGoogle Scholar
  23. 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(14):8946–8951PubMedGoogle Scholar
  24. Davidson AL, Sharma S (1997) Mutation of a single MalK subunit severely impairs maltose transport activity in Escherichia coli. J Bacteriol 179(17):5458–5464PubMedCentralPubMedGoogle Scholar
  25. Davidson AL, Shuman HA, Nikaido H (1992) Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins. Proc Natl Acad Sci U S A 89(6):2360–2364PubMedCentralPubMedGoogle Scholar
  26. Davidson AL, Laghaeian SS, Mannering DE (1996) The maltose transport system of Escherichia coli displays positive cooperativity in ATP hydrolysis. J Biol Chem 271(9):4858–4863PubMedGoogle Scholar
  27. Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72(2):317–364, table of contentsPubMedCentralPubMedGoogle Scholar
  28. Dawson RJ, Locher KP (2007) Structure of the multidrug ABC transporter Sav 1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett 581(5):935–938PubMedGoogle Scholar
  29. Dean M (2005) The genetics of ATP-binding cassette transporters. Methods Enzymol 400:409–429PubMedGoogle Scholar
  30. Dean DA, Davidson AL, Nikaido H (1989) Maltose transport in membrane vesicles of Escherichia coli is linked to ATP hydrolysis. Proc Natl Acad Sci U S A 86(23):9134–9138PubMedCentralPubMedGoogle Scholar
  31. 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(34):21005–21010PubMedGoogle Scholar
  32. Dietzel I, Kolb V, Boos W (1978) Pole cap formation in Escherichia coli following induction of the maltose-binding protein. Arch Microbiol 118(2):207–218PubMedGoogle Scholar
  33. Duplay P, Bedouelle H, Fowler A, Zabin I, Saurin W, Hofnung M (1984) Sequences of the malE gene and of its product, the maltose-binding protein of Escherichia coli K12. J Biol Chem 259(16):10606–10613PubMedGoogle Scholar
  34. Eitinger T, Rodionov DA, Grote M, Schneider E (2011) Canonical and ECF-type ATP-binding cassette importers in prokaryotes: diversity in modular organization and cellular functions. FEMS Microbiol Rev 35(1):3–67PubMedGoogle Scholar
  35. Erkens GB, Majsnerowska M, ter Beek J, Slotboom DJ (2012) Energy coupling factor-type ABC transporters for vitamin uptake in prokaryotes. Biochemistry 51(22):4390–4396PubMedGoogle Scholar
  36. Falke JJ, Hazelbauer GL (2001) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26(4):257–265PubMedCentralPubMedGoogle Scholar
  37. Fetsch EE, Davidson AL (2002) Vanadate-catalyzed photocleavage of the signature motif of an ATP-binding cassette (ABC) transporter. Proc Natl Acad Sci U S A 99(15):9685–9690PubMedCentralPubMedGoogle Scholar
  38. Froshauer S, Beckwith J (1984) The nucleotide sequence of the gene for malF protein, an inner membrane component of the maltose transport system of Escherichia coli. Repeated DNA sequences are found in the malE-malF intercistronic region. J Biol Chem 259(17):10896–10903PubMedGoogle Scholar
  39. George AM, Jones PM (2012) Perspectives on the structure-function of ABC transporters: the Switch and Constant Contact models. Prog Biophys Mol Biol 109(3):95–107PubMedGoogle Scholar
  40. Geourjon C, Orelle C, Steinfels E, Blanchet C, Deleage G, Di Pietro A, Jault JM (2001) A common mechanism for ATP hydrolysis in ABC transporter and helicase superfamilies. Trends Biochem Sci 26(9):539–544PubMedGoogle Scholar
  41. Gilson E, Nikaido H, Hofnung M (1982) Sequence of the malK gene in E.coli K12. Nucleic Acids Res 10(22):7449–7458PubMedCentralPubMedGoogle Scholar
  42. Gould AD, Shilton BH (2010) Studies of the maltose transport system reveal a mechanism for coupling ATP hydrolysis to substrate translocation without direct recognition of substrate. J Biol Chem 285(15):11290–11296PubMedCentralPubMedGoogle Scholar
  43. Gould AD, Telmer PG, Shilton BH (2009) Stimulation of the maltose transporter ATPase by unliganded maltose binding protein. Biochemistry 48(33):8051–8061PubMedCentralPubMedGoogle Scholar
  44. Grote M, Polyhach Y, Jeschke G, Steinhoff HJ, Schneider E, Bordignon E (2009) Transmembrane signaling in the maltose ABC transporter MalFGK2-E: periplasmic MalF-P2 loop communicates substrate availability to the ATP-bound MalK dimer. J Biol Chem 284(26):17521–17526PubMedCentralPubMedGoogle Scholar
  45. Gutmann DA, Ward A, Urbatsch IL, Chang G, van Veen HW (2010) Understanding polyspecificity of multidrug ABC transporters: closing in on the gaps in ABCB1. Trends Biochem Sci 35(1):36–42PubMedGoogle Scholar
  46. Hall JA, Ganesan AK, Chen J, Nikaido H (1997) Two modes of ligand binding in maltose-binding protein of Escherichia coli. Functional significance in active transport. J Biol Chem 272(28):17615–17622PubMedGoogle Scholar
  47. Hazelbauer GL (1975) Maltose chemoreceptor of Escherichia coli. J Bacteriol 122(1):206–214PubMedCentralPubMedGoogle Scholar
  48. Higgins CF (2001) ABC transporters: physiology, structure and mechanism–an overview. Res Microbiol 152(3–4):205–210PubMedGoogle Scholar
  49. Hinz A, Tampe R (2012) ABC transporters and immunity: mechanism of self-defense. Biochemistry 51(25):4981–4989PubMedGoogle Scholar
  50. Hohl M, Briand C, Grutter MG, Seeger MA (2012) Crystal structure of a heterodimeric ABC transporter in its inward-facing conformation. Nat Struct Mol Biol 19(4):395–402PubMedGoogle Scholar
  51. Hollenstein K, Frei DC, Locher KP (2007) Structure of an ABC transporter in complex with its binding protein. Nature 446(7132):213–216PubMedGoogle Scholar
  52. 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(7):789–800PubMedGoogle Scholar
  53. Hunke S, Dose S, Schneider E (1995) Vanadate and bafilomycin A1 are potent inhibitors of the ATPase activity of the reconstituted bacterial ATP-binding cassette transporter for maltose (MalFGK2). Biochem Biophys Res Commun 216(2):589–594PubMedGoogle Scholar
  54. Hunke S, Mourez M, Jehanno M, Dassa E, Schneider E (2000) ATP modulates subunit-subunit interactions in an ATP-binding cassette transporter (MalFGK2) determined by site-directed chemical cross-linking. J Biol Chem 275(20):15526–15534PubMedGoogle Scholar
  55. Isenbarger TA, Carr CE, Johnson SS, Finney M, Church GM, Gilbert W, Zuber MT, Ruvkun G (2008) The most conserved genome segments for life detection on Earth and other planets. Orig Life Evol Biosph 38(6):517–533PubMedGoogle Scholar
  56. Jacso T, Grote M, Daus ML, Schmieder P, Keller S, Schneider E, Reif B (2009) Periplasmic loop P2 of the MalF subunit of the maltose ATP binding cassette transporter is sufficient to bind the maltose binding protein MalE. Biochemistry 48(10):2216–2225PubMedGoogle Scholar
  57. Jardetzky O (1966) Simple allosteric model for membrane pumps. Nature 211(5052):969–970PubMedGoogle Scholar
  58. Jones PM, George AM (1999) Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol Lett 179(2):187–202PubMedGoogle Scholar
  59. Jones PM, George AM (2012) Mechanism of the ABC transporter ATPase domains: catalytic models and the biochemical and biophysical record. Crit Rev Biochem Mol Biol 48(1):39–50PubMedGoogle Scholar
  60. Joseph B, Jeschke G, Goetz BA, Locher KP, Bordignon E (2011) Transmembrane gate movements in the type II ATP-binding cassette (ABC) importer BtuCD-F during nucleotide cycle. J Biol Chem 286(47):41008–41017PubMedCentralPubMedGoogle Scholar
  61. Kellermann O, Szmelcman S (1974) Active transport of maltose in Escherichia coli K12. Involvement of a "periplasmic" maltose binding protein. Eur J Biochem 47(1):139–149PubMedGoogle Scholar
  62. Khare D, Oldham ML, Orelle C, Davidson AL, Chen J (2009) Alternating access in maltose transporter mediated by rigid-body rotations. Mol Cell 33(4):528–536PubMedCentralPubMedGoogle Scholar
  63. Korkhov VM, Mireku SA, Locher KP (2012) Structure of AMP-PNP-bound vitamin B12 transporter BtuCD-F. Nature 490(7420):367–372PubMedGoogle Scholar
  64. Kuhnau S, Reyes M, Sievertsen A, Shuman HA, Boos W (1991) The activities of the Escherichia coli MalK protein in maltose transport, regulation, and inducer exclusion can be separated by mutations. J Bacteriol 173(7):2180–2186PubMedCentralPubMedGoogle Scholar
  65. Lewinson O, Lee AT, Locher KP, Rees DC (2010) A distinct mechanism for the ABC transporter BtuCD-BtuF revealed by the dynamics of complex formation. Nat Struct Mol Biol 17(3):332–338PubMedCentralPubMedGoogle Scholar
  66. Linton KJ, Holland IB (2011) The ABC transporters of human physiology and disease, 1st edn. World Scientific, SingaporeGoogle Scholar
  67. Locher KP (2009) Review. Structure and mechanism of ATP-binding cassette transporters. Philos Trans R Soc Lond B Biol Sci 364(1514):239–245PubMedCentralPubMedGoogle Scholar
  68. Locher KP, Lee AT, Rees DC (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296(5570):1091–1098PubMedGoogle Scholar
  69. Loo TW, Clarke DM (1995) Covalent modification of human P-glycoprotein mutants containing a single cysteine in either nucleotide-binding fold abolishes drug-stimulated ATPase activity. J Biol Chem 270(39):22957–22961PubMedGoogle Scholar
  70. Loo TW, Bartlett MC, Clarke DM (2003) Drug binding in human P-glycoprotein causes conformational changes in both nucleotide-binding domains. J Biol Chem 278(3):1575–1578PubMedGoogle Scholar
  71. Lu G, Westbrooks JM, Davidson AL, Chen J (2005) ATP hydrolysis is required to reset the ATP-binding cassette dimer into the resting-state conformation. Proc Natl Acad Sci U S A 102(50):17969–17974PubMedCentralPubMedGoogle Scholar
  72. Luckey M, Nikaido H (1980) Specificity of diffusion channels produced by lambda phage receptor protein of Escherichia coli. Proc Natl Acad Sci U S A 77(1):167–171PubMedCentralPubMedGoogle Scholar
  73. Magasanik B (1970) Glucose effects: inducer exclusion and repression. In: The Lactose operon, vol 1. Cold Spring Harbor Monograph Archive, pp. 189–219Google Scholar
  74. Mannering DE, Sharma S, Davidson AL (2001) Demonstration of conformational changes associated with activation of the maltose transport complex. J Biol Chem 276(15):12362–12368PubMedGoogle Scholar
  75. Manson MD, Boos W, Bassford PJ Jr, Rasmussen BA (1985) Dependence of maltose transport and chemotaxis on the amount of maltose-binding protein. J Biol Chem 260(17):9727–9733PubMedGoogle Scholar
  76. 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(24):21111–21114PubMedCentralPubMedGoogle Scholar
  77. Morbach S, Tebbe S, Schneider E (1993) The ATP-binding cassette (ABC) transporter for maltose/maltodextrins of Salmonella typhimurium. Characterization of the ATPase activity associated with the purified MalK subunit. J Biol Chem 268(25):18617–18621PubMedGoogle Scholar
  78. 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(11):3066–3077PubMedCentralPubMedGoogle Scholar
  79. Mourez M, Jehanno M, Schneider E, Dassa E (1998) In vitro interaction between components of the inner membrane complex of the maltose ABC transporter of Escherichia coli: modulation by ATP. Mol Microbiol 30(2):353–363PubMedGoogle Scholar
  80. Oldham ML, Chen J (2011a) Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science 332(6034):1202–1205PubMedGoogle Scholar
  81. Oldham ML, Chen J (2011b) Snapshots of the maltose transporter during ATP hydrolysis. Proc Natl Acad Sci U S A 108(37):15152–15156PubMedCentralPubMedGoogle Scholar
  82. Oldham ML, Khare D, Quiocho FA, Davidson AL, Chen J (2007) Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450(7169):515–521PubMedGoogle Scholar
  83. Oldham ML, Davidson AL, Chen J (2008) Structural insights into ABC transporter mechanism. Curr Opin Struct Biol 18(6):726–733PubMedCentralPubMedGoogle Scholar
  84. Oloo EO, Fung EY, Tieleman DP (2006) The dynamics of the MgATP-driven closure of MalK, the energy-transducing subunit of the maltose ABC transporter. J Biol Chem 281(38):28397–28407. doi: 10.1074/jbc.M513614200 PubMedGoogle Scholar
  85. Orelle C, Dalmas O, Gros P, Di Pietro A, Jault JM (2003) The conserved glutamate residue adjacent to the Walker-B motif is the catalytic base for ATP hydrolysis in the ATP-binding cassette transporter BmrA. J Biol Chem 278(47):47002–47008PubMedGoogle Scholar
  86. 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 U S A 105(35):12837–12842PubMedCentralPubMedGoogle Scholar
  87. Orelle C, Alvarez FJ, Oldham ML, Orelle A, Wiley TE, Chen J, Davidson AL (2010) Dynamics of alpha-helical subdomain rotation in the intact maltose ATP-binding cassette transporter. Proc Natl Acad Sci U S A 107(47):20293–20298PubMedCentralPubMedGoogle Scholar
  88. Procko E, O'Mara ML, Bennett WF, Tieleman DP, Gaudet R (2009) The mechanism of ABC transporters: general lessons from structural and functional studies of an antigenic peptide transporter. FASEB J 23(5):1287–1302PubMedGoogle Scholar
  89. Rees DC, Johnson E, Lewinson O (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10(3):218–227PubMedCentralPubMedGoogle Scholar
  90. Richet E, Davidson AL, Joly N (2012) The ABC transporter MalFGK(2) sequesters the MalT transcription factor at the membrane in the absence of cognate substrate. Mol Microbiol 85(4):632–647PubMedGoogle Scholar
  91. Rodionov DA, Hebbeln P, Eudes A, ter Beek J, Rodionova IA, Erkens GB, Slotboom DJ, Gelfand MS, Osterman AL, Hanson AD, Eitinger T (2009) A novel class of modular transporters for vitamins in prokaryotes. J Bacteriol 191(1):42–51PubMedCentralPubMedGoogle Scholar
  92. 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(37):35265–35271PubMedGoogle Scholar
  93. Saurin W, Koster W, Dassa E (1994) Bacterial binding protein-dependent permeases: characterization of distinctive signatures for functionally related integral cytoplasmic membrane proteins. Mol Microbiol 12(6):993–1004PubMedGoogle Scholar
  94. Schirmer T, Keller TA, Wang YF, Rosenbusch JP (1995) Structural basis for sugar translocation through maltoporin channels at 3.1 A resolution. Science 267(5197):512–514PubMedGoogle Scholar
  95. Sharma S, Davidson AL (2000) Vanadate-induced trapping of nucleotides by purified maltose transport complex requires ATP hydrolysis. J Bacteriol 182(23):6570–6576PubMedCentralPubMedGoogle Scholar
  96. Sharom FJ (2008) ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 9(1):105–127PubMedGoogle Scholar
  97. Shuman HA (1982) Active transport of maltose in Escherichia coli K12. Role of the periplasmic maltose-binding protein and evidence for a substrate recognition site in the cytoplasmic membrane. J Biol Chem 257(10):5455–5461PubMedGoogle Scholar
  98. Smith CA, Rayment I (1996) X-ray structure of the magnesium(II).ADP.vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 A resolution. Biochemistry 35(17):5404–5417PubMedGoogle Scholar
  99. 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(1):139–149PubMedCentralPubMedGoogle Scholar
  100. Spurlino JC, Lu GY, Quiocho FA (1991) The 2.3-A resolution structure of the maltose- or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis. J Biol Chem 266(8):5202–5219PubMedGoogle Scholar
  101. 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(16):4074–4085PubMedGoogle Scholar
  102. Szmelcman S, Hofnung M (1975) Maltose transport in Escherichia coli K-12: involvement of the bacteriophage lambda receptor. J Bacteriol 124(1):112–118PubMedCentralPubMedGoogle Scholar
  103. Szmelcman S, Schwartz M, Silhavy TJ, Boos W (1976) Maltose transport in Escherichia coli K12. Eur J Biochem 65(1):13–19PubMedGoogle Scholar
  104. Tombline G, Senior AE (2005) The occluded nucleotide conformation of p-glycoprotein. J Bioenerg Biomembr 37(6):497–500PubMedGoogle Scholar
  105. Treptow NA, Shuman HA (1985) Genetic evidence for substrate and periplasmic-binding-protein recognition by the MalF and MalG proteins, cytoplasmic membrane components of the Escherichia coli maltose transport system. J Bacteriol 163(2):654–660PubMedCentralPubMedGoogle Scholar
  106. Urbatsch IL, Sankaran B, Weber J, Senior AE (1995) P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J Biol Chem 270(33):19383–19390PubMedGoogle Scholar
  107. Urbatsch IL, Beaudet L, Carrier I, Gros P (1998) Mutations in either nucleotide-binding site of P-glycoprotein (Mdr3) prevent vanadate trapping of nucleotide at both sites. Biochemistry 37(13):4592–4602PubMedGoogle Scholar
  108. van der Heide T, Poolman B (2002) ABC transporters: one, two or four extracytoplasmic substrate-binding sites? EMBO Rep 3(10):938–943PubMedCentralPubMedGoogle Scholar
  109. Vigonsky E, Ovcharenko E, Lewinson O (2013) Two molybdate/tungstate ABC transporters that interact very differently with their substrate binding proteins. Proc Natl Acad Sci U S A 110(14):5440–5445. doi: 10.1073/pnas.1213598110 PubMedCentralPubMedGoogle Scholar
  110. Wang T, Fu G, Pan X, Wu J, Gong X, Wang J, Shi Y (2013) Structure of a bacterial energy-coupling factor transporter. Nature. doi: 10.1038/nature12045 Google Scholar
  111. Wen PC, Tajkhorshid E (2008) Dimer opening of the nucleotide binding domains of ABC transporters after ATP hydrolysis. Biophys J 95(11):5100–5110PubMedCentralPubMedGoogle Scholar
  112. Wen PC, Tajkhorshid E (2011) Conformational coupling of the nucleotide-binding and the transmembrane domains in ABC transporters. Biophys J 101(3):680–690PubMedCentralPubMedGoogle Scholar
  113. Xu K, Zhang M, Zhao Q, Yu F, Guo H, Wang C, He F, Ding J, Zhang P (2013) Crystal structure of a folate energy-coupling factor transporter from Lactobacillus brevis. Nature. doi: 10.1038/nature12046 Google Scholar
  114. Ye J, Osborne AR, Groll M, Rapoport TA (2004) RecA-like motor ATPases–lessons from structures. Biochim Biophys Acta 1659(1):1–18PubMedGoogle Scholar
  115. Yuan YR, Blecker S, Martsinkevich O, Millen L, Thomas PJ, Hunt JF (2001) The crystal structure of the MJ0796 ATP-binding cassette. Implications for the structural consequences of ATP hydrolysis in the active site of an ABC transporter. J Biol Chem 276(34):32313–32321PubMedGoogle Scholar
  116. Zhang Y, Mannering DE, Davidson AL, Yao N, Manson MD (1996) Maltose-binding protein containing an interdomain disulfide bridge confers a dominant-negative phenotype for transport and chemotaxis. J Biol Chem 271(30):17881–17889PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Cédric Orelle
    • 1
    • 2
  • Michael L. Oldham
    • 3
  • Amy L. Davidson
    • 1
  1. 1.Department of ChemistryPurdue UniversityWest LafayetteUSA
  2. 2.Center for Pharmaceutical BiotechnologyUniversity of IllinoisChicagoUSA
  3. 3.Department of Biological SciencesPurdue University, Howard Hughes Medical InstituteWest LafayetteUSA

Personalised recommendations