1,126
Views
53
CrossRef citations to date
0
Altmetric
Review Article

Mechanism of the ABC transporter ATPase domains: catalytic models and the biochemical and biophysical record

&
Pages 39-50 | Received 12 Aug 2012, Accepted 27 Sep 2012, Published online: 06 Nov 2012

References

  • Aleksandrov L, Aleksandrov A, Riordan JR. 2008. Mg2+ -dependent ATP occlusion at the first nucleotide-binding domain (NBD1) of CFTR does not require the second (NBD2). Biochem J 416:129–136.
  • 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 323:1718–1722.
  • Ames GF, Mimura CS, Holbrook SR, Shyamala V. 1992. Traffic ATPases: a superfamily of transport proteins operating from Escherichia coli to humans. Adv Enzymol Relat Areas Mol Biol 65:1–47.
  • Artur L, Chaves P, Gadsby DC. 2011. Extent of nucleotide-binding domain (NBD) separation when a CFTR channel closes. Biophys J Suppl 100:265a–266a.
  • Basso C, Vergani P, Nairn AC, Gadsby DC. 2003. Prolonged nonhydrolytic interaction of nucleotide with CFTR’s NH2-terminal nucleotide binding domain and its role in channel gating. J Gen Physiol 122:333–348.
  • Borbat PP, Surendhran K, Bortolus M, Zou P, Freed JH, Mchaourab HS. 2007. Conformational motion of the ABC transporter MsbA induced by ATP hydrolysis. PLoS Biol 5:e271.
  • Bordignon E, Grote M, Schneider E. 2010. The maltose ATP-binding cassette transporter in the 21st century–towards a structural dynamic perspective on its mode of action. Mol Microbiol 77:1354–1366.
  • Buchaklian AH, Klug CS. 2005. Characterization of the Walker A motif of MsbA using site-directed spin labeling electron paramagnetic resonance spectroscopy. Biochemistry 44:5503–5509.
  • Buchaklian AH, Klug CS. 2006. Characterization of the LSGGQ and H motifs from the Escherichia coli lipid A transporter MsbA. Biochemistry 45:12539–12546.
  • 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 12:651–661.
  • Dalmas O, Orelle C, Foucher AE, Geourjon C, Crouzy S, Di Pietro A, Jault JM. 2005. The Q-loop disengages from the first intracellular loop during the catalytic cycle of the multidrug ABC transporter BmrA. J Biol Chem 280:36857–36864.
  • Davidson AL, Dassa E, Orelle C, Chen J. 2008. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317–64, table of contents.
  • Dawson RJ, Hollenstein K, Locher KP. 2007. Uptake or extrusion: crystal structures of full ABC transporters suggest a common mechanism. Mol Microbiol 65:250–257.
  • Dawson RJ, Locher KP. 2006. Structure of a bacterial multidrug ABC transporter. Nature 443:180–185.
  • Eckford PD, Sharom FJ. 2009. ABC efflux pump-based resistance to chemotherapy drugs. Chem Rev 109:2989–3011.
  • Ernst R, Kueppers P, Stindt J, Kuchler K, Schmitt L. 2010. Multidrug efflux pumps: substrate selection in ATP-binding cassette multidrug efflux pumps–first come, first served? FEBS J 277:540–549.
  • Fath MJ, Kolter R. 1993. ABC transporters: bacterial exporters. Microbiol Rev 57:995–1017.
  • Grote M, Bordignon E, Polyhach Y, Jeschke G, Steinhoff HJ, Schneider E. 2008. A comparative electron paramagnetic resonance study of the nucleotide-binding domains’ catalytic cycle in the assembled maltose ATP-binding cassette importer. Biophys J 95:2924–2938.
  • 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 284:17521–17526.
  • Gustot A, Smriti, Ruysschaert JM, McHaourab H, Govaerts C. 2010. Lipid composition regulates the orientation of transmembrane helices in HorA, an ABC multidrug transporter. J Biol Chem 285:14144–14151.
  • Haider AJ, Briggs D, Self TJ, Chilvers HL, Holliday ND, Kerr ID. 2011. Dimerization of ABCG2 analysed by bimolecular fluorescence complementation. PLoS ONE 6:e25818.
  • Higgins CF, Linton KJ. 2004. The ATP switch model for ABC transporters. Nat Struct Mol Biol 11:918–926.
  • Hollenstein K, Dawson RJ, Locher KP. 2007a. Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 17:412–418.
  • Hollenstein K, Frei DC, Locher KP. 2007b. Structure of an ABC transporter in complex with its binding protein. Nature 446:213–216.
  • 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 101:789–800.
  • Horn C, Bremer E, Schmitt L. 2003. Nucleotide dependent monomer/dimer equilibrium of OpuAA, the nucleotide-binding protein of the osmotically regulated ABC transporter OpuA from Bacillus subtilis. J Mol Biol 334:403–419.
  • Horn C, Jenewein S, Tschapek B, Bouschen W, Metzger S, Bremer E, Schmitt L. 2008. Monitoring conformational changes during the catalytic cycle of OpuAA, the ATPase subunit of the ABC transporter OpuA from Bacillus subtilis. Biochem J 412:233–244.
  • 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 396:703–707.
  • Hyde SC, Emsley P, Hartshorn MJ, Mimmack MM, Gileadi U, Pearce SR, Gallagher MP, Gill DR, Hubbard RE, Higgins CF. 1990. Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 346:362–365.
  • Janas E, Hofacker M, Chen M, Gompf S, van der Does C, Tampé R. 2003. The ATP hydrolysis cycle of the nucleotide-binding domain of the mitochondrial ATP-binding cassette transporter Mdl1p. J Biol Chem 278:26862–26869.
  • Jones PM, George AM. 1999. Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol Lett 179:187–202.
  • Jones PM, George AM. 2002. Mechanism of ABC transporters: a molecular dynamics simulation of a well characterized nucleotide-binding subunit. Proc Natl Acad Sci USA 99:12639–12644.
  • Jones PM, George AM. 2004. The ABC transporter structure and mechanism: perspectives on recent research. Cell Mol Life Sci 61:682–699.
  • Jones PM, George AM. 2007. Nucleotide-dependent allostery within the ABC transporter ATP-binding cassette: a computational study of the MJ0796 dimer. J Biol Chem 282:22793–22803.
  • Jones PM, George AM. 2009. Opening of the ADP-bound active site in the ABC transporter ATPase dimer: evidence for a constant contact, alternating sites model for the catalytic cycle. Proteins 75:387–396.
  • Jones PM, George AM. 2011. Molecular-dynamics simulations of the ATP/apo state of a multidrug ATP-binding cassette transporter provide a structural and mechanistic basis for the asymmetric occluded state. Biophys J 100:3025–3034.
  • Jones PM, George AM. 2012. Role of the D-loops in allosteric control of ATP hydrolysis in an ABC transporter. J Phys Chem A 116:3004–3013.
  • Jones PM, O’Mara ML, George AM. 2009. ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem Sci 34:520–531.
  • Kadaba NS, Kaiser JT, Johnson E, Lee A, Rees DC. 2008. The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 321:250–253.
  • Kerr ID, Jones PM, George AM. 2010. Multidrug efflux pumps: the structures of prokaryotic ATP-binding cassette transporter efflux pumps and implications for our understanding of eukaryotic P-glycoproteins and homologues. FEBS J 277:550–563.
  • Khare D, Oldham ML, Orelle C, Davidson AL, Chen J. 2009. Alternating access in maltose transporter mediated by rigid-body rotations. Mol Cell 33:528–536.
  • Kos V, Ford RC. 2009. The ATP-binding cassette family: a structural perspective. Cell Mol Life Sci 66:3111–3126.
  • Kreimer DI, Malak H, Lakowicz JR, Trakhanov S, Villar E, Shnyrov VL. 2000. Thermodynamics and dynamics of histidine-binding protein, the water-soluble receptor of histidine permease. Implications for the transport of high and low affinity ligands. Eur J Biochem 267:4242–4252.
  • 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 23:282–293.
  • Loo TW, Bartlett MC, Clarke DM. 2010. Human P-glycoprotein is active when the two halves are clamped together in the closed conformation. Biochem Biophys Res Commun 395:436–440.
  • Loo TW, Bartlett MC, Clarke DM. 2002. The ‘‘LSGGQ’’ motif in each nucleotide-binding domain in human P-glycoprotein is adjacent to the opposing walker A sequence. J Biol Chem 277:41303–41306.
  • Malde AK, Mark AE. 2011. Challenges in the determination of the binding modes of non-standard ligands in X-ray crystal complexes. J Comput Aided Mol Des 25:1–12.
  • Nair PC, Malde AK, Drinkwater N, Mark AE. 2012. Missing fragments: detecting cooperative binding in fragment-based drug design. ACS Med Chem Lett 3:322–326.
  • Oancea G, O’Mara ML, Bennett WF, Tieleman DP, Abele R, Tampé R. 2009. Structural arrangement of the transmission interface in the antigen ABC transport complex TAP. Proc Natl Acad Sci USA 106:5551–5556.
  • Oldham ML, Chen J. 2011. Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science 332:1202–1205.
  • 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 USA 107:20293–20298.
  • Procko E, Ferrin-O’Connell I, Ng SL, Gaudet R. 2006. Distinct structural and functional properties of the ATPase sites in an asymmetric ABC transporter. Mol Cell 24:51–62.
  • Sauna ZE, Kim IW, Nandigama K, Kopp S, Chiba P, Ambudkar SV. 2007. Catalytic cycle of ATP hydrolysis by P-glycoprotein: evidence for formation of the E.S reaction intermediate with ATP-gamma-S, a nonhydrolyzable analogue of ATP. Biochemistry 46:13787–13799.
  • Sauna ZE, Müller M, Peng XH, Ambudkar SV. 2002. Importance of the conserved Walker B glutamate residues, 556 and 1201, for the completion of the catalytic cycle of ATP hydrolysis by human P-glycoprotein (ABCB1). Biochemistry 41:13989–14000.
  • Senior AE, Bhagat S. 1998. P-glycoprotein shows strong catalytic cooperativity between the two nucleotide sites. Biochemistry 37:831–836.
  • Shyamala V, Baichwal V, Beall E, Ames GF. 1991. Structure-function analysis of the histidine permease and comparison with cystic fibrosis mutations. J Biol Chem 266:18714–18719.
  • Siarheyeva A, Liu R, Sharom FJ. 2010. Characterization of an asymmetric occluded state of P-glycoprotein with two bound nucleotides: implications for catalysis. J Biol Chem 285:7575–7586.
  • 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 10:139–149.
  • Syberg F, Suveyzdis Y, Kötting C, Gerwert K, Hofmann E. 2012. Time-resolved Fourier transform infrared spectroscopy of the nucleotide-binding domain from the ATP-binding Cassette transporter MsbA: ATP hydrolysis is the rate-limiting step in the catalytic cycle. J Biol Chem 287:23923–23931.
  • Szollosi A, Muallem DR, Csanády L, Vergani P. 2011. Mutant cycles at CFTR’s non-canonical ATP-binding site support little interface separation during gating. J Gen Physiol 137:549–562.
  • Tombline G, Bartholomew LA, Urbatsch IL, Senior AE. 2004. Combined mutation of catalytic glutamate residues in the two nucleotide binding domains of P-glycoprotein generates a conformation that binds ATP and ADP tightly. J Biol Chem 279:31212–31220.
  • Tsai MF, Li M, Hwang TC. 2010. Stable ATP binding mediated by a partial NBD dimer of the CFTR chloride channel. J Gen Physiol 135:399–414.
  • Tsai MF, Shimizu H, Sohma Y, Li M, Hwang TC. 2009. State-dependent modulation of CFTR gating by pyrophosphate. J Gen Physiol 133:405–419.
  • van der Heide T, Poolman B. 2002. ABC transporters: one, two or four extracytoplasmic substrate-binding sites? EMBO Rep 3:938–943.
  • van Veen HW, Margolles A, Müller M, Higgins CF, Konings WN. 2000. The homodimeric ATP-binding cassette transporter LmrA mediates multidrug transport by an alternating two-site (two-cylinder engine) mechanism. EMBO J 19:2503–2514.
  • Verdon G, Albers SV, van Oosterwijk N, Dijkstra BW, Driessen AJ, Thunnissen AM. 2003. Formation of the productive ATP-Mg2+-bound dimer of GlcV, an ABC-ATPase from Sulfolobus solfataricus. J Mol Biol 334:255–267.
  • Vergani P, Lockless SW, Nairn AC, Gadsby DC. 2005. CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Nature 433:876–880.
  • Verhalen B, Ernst S, Börsch M, Wilkens S. 2012. Dynamic ligand-induced conformational rearrangements in P-glycoprotein as probed by fluorescence resonance energy transfer spectroscopy. J Biol Chem 287:1112–1127.
  • Verhalen B, Wilkens S. 2011. P-glycoprotein retains drug-stimulated ATPase activity upon covalent linkage of the two nucleotide binding domains at their C-terminal ends. J Biol Chem 286:10476–10482.
  • Walter C, Wilken S, Schneider E. 1992. Characterization of site-directed mutations in conserved domains of MalK, a bacterial member of the ATP-binding cassette (ABC) family [corrected]. FEBS Lett 303:41–44.
  • 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 104:19005–19010.
  • Wen PC, Tajkhorshid E. 2011. Conformational coupling of the nucleotide-binding and the transmembrane domains in ABC transporters. Biophys J 101:680–690.
  • 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 276:32313–32321.
  • 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 25:3432–3443.
  • Zoghbi ME, Fuson KL, Sutton RB, Altenberg GA. 2012. Kinetics of the association/dissociation cycle of an ATP-binding cassette nucleotide-binding domain. J Biol Chem 287:4157–4164.
  • Zou P, Bortolus M, McHaourab HS. 2009. Conformational cycle of the ABC transporter MsbA in liposomes: detailed analysis using double electron-electron resonance spectroscopy. J Mol Biol 393:586–597.
  • Zou P, McHaourab HS. 2009. Alternating access of the putative substrate-binding chamber in the ABC transporter MsbA. J Mol Biol 393:574–585.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.