1oxv › Citations

Crystal structures of the ATPase subunit of the glucose ABC transporter from Sulfolobus solfataricus: nucleotide-free and nucleotide-bound conformations.

Verdon G, Albers SV, Dijkstra BW, Driessen AJ, Thunnissen AM
J Mol Biol 330 343-58 (2003)
Related entries: 1oxs, 1oxt, 1oxu

Cited: 93 times
EuropePMC logo PMID: 12823973

Abstract

The ABC-ATPase GlcV energizes a binding protein-dependent ABC transporter that mediates glucose uptake in Sulfolobus solfataricus. Here, we report high-resolution crystal structures of GlcV in different states along its catalytic cycle: distinct monomeric nucleotide-free states and monomeric complexes with ADP-Mg(2+) as a product-bound state, and with AMPPNP-Mg(2+) as an ATP-like bound state. The structure of GlcV consists of a typical ABC-ATPase domain, comprising two subdomains, connected by a linker region to a C-terminal domain of unknown function. Comparisons of the nucleotide-free and nucleotide-bound structures of GlcV reveal re-orientations of the ABCalpha subdomain and the C-terminal domain relative to the ABCalpha/beta subdomain, and switch-like rearrangements in the P-loop and Q-loop regions. Additionally, large conformational differences are observed between the GlcV structures and those of other ABC-ATPases, further emphasizing the inherent flexibility of these proteins. Notably, a comparison of the monomeric AMPPNP-Mg(2+)-bound GlcV structure with that of the dimeric ATP-Na(+)-bound LolD-E171Q mutant reveals a +/-20 degrees rigid body re-orientation of the ABCalpha subdomain relative to the ABCalpha/beta subdomain, accompanied by a local conformational difference in the Q-loop. We propose that these differences represent conformational changes that may have a role in the mechanism of energy-transduction and/or allosteric control of the ABC-ATPase activity in bacterial importers.

Articles - 1oxv mentioned but not cited (2)

  1. In vivo phosphorylation of CFTR promotes formation of a nucleotide-binding domain heterodimer. Mense M, Vergani P, White DM, Altberg G, Nairn AC, Gadsby DC. EMBO J 25 4728-4739 (2006)
  2. Purification, crystallization and preliminary X-ray diffraction analysis of the putative ABC transporter ATP-binding protein from Thermotoga maritima. Ethayathulla AS, Bessho Y, Shinkai A, Padmanabhan B, Singh TP, Kaur P, Yokoyama S. Acta Crystallogr Sect F Struct Biol Cryst Commun 64 498-500 (2008)


Reviews citing this publication (33)

  1. Structure, function, and evolution of bacterial ATP-binding cassette systems. Davidson AL, Dassa E, Orelle C, Chen J. Microbiol Mol Biol Rev 72 317-64, table of contents (2008)
  2. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Deeley RG, Westlake C, Cole SP. Physiol Rev 86 849-899 (2006)
  3. The ATP switch model for ABC transporters. Higgins CF, Linton KJ. Nat Struct Mol Biol 11 918-926 (2004)
  4. ATP-binding cassette transporters in bacteria. Davidson AL, Chen J. Annu Rev Biochem 73 241-268 (2004)
  5. Structural diversity of ABC transporters. ter Beek J, Guskov A, Slotboom DJ. J Gen Physiol 143 419-435 (2014)
  6. Structure and function of ABC transporters. Linton KJ. Physiology (Bethesda) 22 122-130 (2007)
  7. ABC transporter architecture and regulatory roles of accessory domains. Biemans-Oldehinkel E, Doeven MK, Poolman B. FEBS Lett 580 1023-1035 (2006)
  8. KATP Channels in the Cardiovascular System. Foster MN, Coetzee WA. Physiol Rev 96 177-252 (2016)
  9. Canonical and ECF-type ATP-binding cassette importers in prokaryotes: diversity in modular organization and cellular functions. Eitinger T, Rodionov DA, Grote M, Schneider E. FEMS Microbiol Rev 35 3-67 (2011)
  10. Structure and function of ABC transporters: the ATP switch provides flexible control. Linton KJ, Higgins CF. Pflugers Arch 453 555-567 (2007)
  11. The A-loop, a novel conserved aromatic acid subdomain upstream of the Walker A motif in ABC transporters, is critical for ATP binding. Ambudkar SV, Kim IW, Xia D, Sauna ZE. FEBS Lett 580 1049-1055 (2006)
  12. Multidrug resistance ABC transporters. Chang G. FEBS Lett 555 102-105 (2003)
  13. Structure and mechanism of ABC transporters. Locher KP. Curr Opin Struct Biol 14 426-431 (2004)
  14. ATP-binding cassette transporters in Escherichia coli. Moussatova A, Kandt C, O'Mara ML, Tieleman DP. Biochim Biophys Acta 1778 1757-1771 (2008)
  15. CLC-0 and CFTR: chloride channels evolved from transporters. Chen TY, Hwang TC. Physiol Rev 88 351-387 (2008)
  16. The motor domains of ABC-transporters. What can structures tell us? Oswald C, Holland IB, Schmitt L. Naunyn Schmiedebergs Arch Pharmacol 372 385-399 (2006)
  17. How can we best use structural information on P-glycoprotein to design inhibitors? McDevitt CA, Callaghan R. Pharmacol Ther 113 429-441 (2007)
  18. Insights into ABC transport in archaea. Albers SV, Koning SM, Konings WN, Driessen AJ. J Bioenerg Biomembr 36 5-15 (2004)
  19. How do ABC transporters drive transport? van der Does C, Tampé R. Biol Chem 385 927-933 (2004)
  20. Structure of ABC transporters. Zolnerciks JK, Andress EJ, Nicolaou M, Linton KJ. Essays Biochem 50 43-61 (2011)
  21. A molecular understanding of ATP-dependent solute transport by multidrug resistance-associated protein MRP1. Chang XB. Cancer Metastasis Rev 26 15-37 (2007)
  22. ABC transporters, mechanisms and biology: an overview. Holland IB. Essays Biochem 50 1-17 (2011)
  23. Structures and models of transporter proteins. Dahl SG, Sylte I, Ravna AW. J Pharmacol Exp Ther 309 853-860 (2004)
  24. Intracellular peptide transporters in human--compartmentalization of the "peptidome". Herget M, Tampé R. Pflugers Arch 453 591-600 (2007)
  25. Molecular insights into the mechanism of ATP-hydrolysis by the NBD of the ABC-transporter HlyB. Hanekop N, Zaitseva J, Jenewein S, Holland IB, Schmitt L. FEBS Lett 580 1036-1041 (2006)
  26. Gene regulation in prokaryotes by subcellular relocalization of transcription factors. Böhm A, Boos W. Curr Opin Microbiol 7 151-156 (2004)
  27. Review. ATP hydrolysis-driven gating in cystic fibrosis transmembrane conductance regulator. Muallem D, Vergani P. Philos Trans R Soc Lond B Biol Sci 364 247-255 (2009)
  28. The origin and early evolution of membrane channels. Pohorille A, Schweighofer K, Wilson MA. Astrobiology 5 1-17 (2005)
  29. ABC transporter architecture and mechanism: implications from the crystal structures of BtuCD and BtuF. Locher KP, Borths E. FEBS Lett 564 264-268 (2004)
  30. Molecular basis for the ATPase activity of CFTR. Cheung JC, Kim Chiaw P, Pasyk S, Bear CE. Arch Biochem Biophys 476 95-100 (2008)
  31. The structures of MsbA: Insight into ABC transporter-mediated multidrug efflux. Reyes CL, Ward A, Yu J, Chang G. FEBS Lett 580 1042-1048 (2006)
  32. The ABC of binding-protein-dependent transport in Archaea. Lee SJ, Böhm A, Krug M, Boos W. Trends Microbiol 15 389-397 (2007)
  33. Biochemical and structural analysis of the Bacillus subtilis ABC transporter OpuA and its isolated subunits. Horn C, Jenewein S, Sohn-Bösser L, Bremer E, Schmitt L. J Mol Microbiol Biotechnol 10 76-91 (2005)

Articles citing this publication (58)

  1. A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Chen J, Lu G, Lin J, Davidson AL, Quiocho FA. Mol Cell 12 651-661 (2003)
  2. CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Vergani P, Lockless SW, Nairn AC, Gadsby DC. Nature 433 876-880 (2005)
  3. Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. 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. EMBO J 23 282-293 (2004)
  4. H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. Zaitseva J, Jenewein S, Jumpertz T, Holland IB, Schmitt L. EMBO J 24 1901-1910 (2005)
  5. Crystal structure of the maltose transporter in a pretranslocation intermediate state. Oldham ML, Chen J. Science 332 1202-1205 (2011)
  6. ABCA4 disease progression and a proposed strategy for gene therapy. Cideciyan AV, Swider M, Aleman TS, Tsybovsky Y, Schwartz SB, Windsor EA, Roman AJ, Sumaroka A, Steinberg JD, Jacobson SG, Stone EM, Palczewski K. Hum Mol Genet 18 931-941 (2009)
  7. Molecular models of the open and closed states of the whole human CFTR protein. Mornon JP, Lehn P, Callebaut I. Cell Mol Life Sci 66 3469-3486 (2009)
  8. A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer. Zaitseva J, Oswald C, Jumpertz T, Jenewein S, Wiedenmann A, Holland IB, Schmitt L. EMBO J 25 3432-3443 (2006)
  9. ATP hydrolysis is required to reset the ATP-binding cassette dimer into the resting-state conformation. Lu G, Westbrooks JM, Davidson AL, Chen J. Proc Natl Acad Sci U S A 102 17969-17974 (2005)
  10. Evidence for a Sav1866-like architecture for the human multidrug transporter P-glycoprotein. Zolnerciks JK, Wooding C, Linton KJ. FASEB J 21 3937-3948 (2007)
  11. The CFTR ion channel: gating, regulation, and anion permeation. Hwang TC, Kirk KL. Cold Spring Harb Perspect Med 3 a009498 (2013)
  12. Functional analysis of cytoplasmic dynein heavy chain in Caenorhabditis elegans with fast-acting temperature-sensitive mutations. Schmidt DJ, Rose DJ, Saxton WM, Strome S. Mol Biol Cell 16 1200-1212 (2005)
  13. Development of EGFR-targeted polymer blend nanocarriers for combination paclitaxel/lonidamine delivery to treat multi-drug resistance in human breast and ovarian tumor cells. Milane L, Duan Z, Amiji M. Mol Pharm 8 185-203 (2011)
  14. 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. Jones PM, George AM. Proteins 75 387-396 (2009)
  15. Structure of the human multidrug resistance protein 1 nucleotide binding domain 1 bound to Mg2+/ATP reveals a non-productive catalytic site. Ramaen O, Leulliot N, Sizun C, Ulryck N, Pamlard O, Lallemand JY, Tilbeurgh Hv, Jacquet E. J Mol Biol 359 940-949 (2006)
  16. Formation of the productive ATP-Mg2+-bound dimer of GlcV, an ABC-ATPase from Sulfolobus solfataricus. Verdon G, Albers SV, van Oosterwijk N, Dijkstra BW, Driessen AJ, Thunnissen AM. J Mol Biol 334 255-267 (2003)
  17. Full-open and closed CFTR channels, with lateral tunnels from the cytoplasm and an alternative position of the F508 region, as revealed by molecular dynamics. Mornon JP, Hoffmann B, Jonic S, Lehn P, Callebaut I. Cell Mol Life Sci 72 1377-1403 (2015)
  18. Dynamics of ATP-binding cassette contribute to allosteric control, nucleotide binding and energy transduction in ABC transporters. Wang C, Karpowich N, Hunt JF, Rance M, Palmer AG. J Mol Biol 342 525-537 (2004)
  19. Nucleotide-dependent allostery within the ABC transporter ATP-binding cassette: a computational study of the MJ0796 dimer. Jones PM, George AM. J Biol Chem 282 22793-22803 (2007)
  20. X-ray structure of RLI, an essential twin cassette ABC ATPase involved in ribosome biogenesis and HIV capsid assembly. Karcher A, Büttner K, Märtens B, Jansen RP, Hopfner KP. Structure 13 649-659 (2005)
  21. Dimer opening of the nucleotide binding domains of ABC transporters after ATP hydrolysis. Wen PC, Tajkhorshid E. Biophys J 95 5100-5110 (2008)
  22. CFTR gating II: Effects of nucleotide binding on the stability of open states. Bompadre SG, Cho JH, Wang X, Zou X, Sohma Y, Li M, Hwang TC. J Gen Physiol 125 377-394 (2005)
  23. Functional roles of nonconserved structural segments in CFTR's NH2-terminal nucleotide binding domain. Csanády L, Chan KW, Nairn AC, Gadsby DC. J Gen Physiol 125 43-55 (2005)
  24. Regulation of expression of the arabinose and glucose transporter genes in the thermophilic archaeon Sulfolobus solfataricus. Lubelska JM, Jonuscheit M, Schleper C, Albers SV, Driessen AJ. Extremophiles 10 383-391 (2006)
  25. Nucleotide dependent monomer/dimer equilibrium of OpuAA, the nucleotide-binding protein of the osmotically regulated ABC transporter OpuA from Bacillus subtilis. Horn C, Bremer E, Schmitt L. J Mol Biol 334 403-419 (2003)
  26. A novel ligand bound ABC transporter, LolCDE, provides insights into the molecular mechanisms underlying membrane detachment of bacterial lipoproteins. Ito Y, Kanamaru K, Taniguchi N, Miyamoto S, Tokuda H. Mol Microbiol 62 1064-1075 (2006)
  27. The Q loops of the human multidrug resistance transporter ABCB1 are necessary to couple drug binding to the ATP catalytic cycle. Zolnerciks JK, Akkaya BG, Snippe M, Chiba P, Seelig A, Linton KJ. FASEB J 28 4335-4346 (2014)
  28. cAMP-dependent protein kinase phosphorylation produces interdomain movement in SUR2B leading to activation of the vascular KATP channel. Shi Y, Chen X, Wu Z, Shi W, Yang Y, Yang Y, Cui N, Jiang C, Harrison RW. J Biol Chem 283 7523-7530 (2008)
  29. Structure of the ATPase subunit CysA of the putative sulfate ATP-binding cassette (ABC) transporter from Alicyclobacillus acidocaldarius. Scheffel F, Demmer U, Warkentin E, Hülsmann A, Schneider E, Ermler U. FEBS Lett 579 2953-2958 (2005)
  30. Control of the CFTR channel's gates. Vergani P, Basso C, Mense M, Nairn AC, Gadsby DC. Biochem Soc Trans 33 1003-1007 (2005)
  31. Structure of MlaFB uncovers novel mechanisms of ABC transporter regulation. Kolich LR, Chang YT, Coudray N, Giacometti SI, MacRae MR, Isom GL, Teran EM, Bhabha G, Ekiert DC. Elife 9 e60030 (2020)
  32. Functionally important ATP binding and hydrolysis sites in Escherichia coli MsbA. Westfahl KM, Merten JA, Buchaklian AH, Klug CS. Biochemistry 47 13878-13886 (2008)
  33. Kinetics of the association/dissociation cycle of an ATP-binding cassette nucleotide-binding domain. Zoghbi ME, Fuson KL, Sutton RB, Altenberg GA. J Biol Chem 287 4157-4164 (2012)
  34. The conformational coupling and translocation mechanism of vitamin B12 ATP-binding cassette transporter BtuCD. Weng J, Ma J, Fan K, Wang W. Biophys J 94 612-621 (2008)
  35. Crystal structure of the ATP-binding cassette of multisugar transporter from Pyrococcus horikoshii OT3. Ose T, Fujie T, Yao M, Watanabe N, Tanaka I. Proteins 57 635-638 (2004)
  36. Effects of putative catalytic base mutation E211Q on ABCG2-mediated methotrexate transport. Hou YX, Li CZ, Palaniyandi K, Magtibay PM, Homolya L, Sarkadi B, Chang XB. Biochemistry 48 9122-9131 (2009)
  37. Genetic analysis of the mode of interplay between an ATPase subunit and membrane subunits of the lipoprotein-releasing ATP-binding cassette transporter LolCDE. Ito Y, Matsuzawa H, Matsuyama S, Narita S, Tokuda H. J Bacteriol 188 2856-2864 (2006)
  38. Crystal structure of atypical cytoplasmic ABC-ATPase SufC from Thermus thermophilus HB8. Watanabe S, Kita A, Miki K. J Mol Biol 353 1043-1054 (2005)
  39. Functional characterization of the Saccharomyces cerevisiae ABC-transporter Yor1p overexpressed in plasma membranes. Grigoras I, Lazard M, Plateau P, Blanquet S. Biochim Biophys Acta 1778 68-78 (2008)
  40. Investigating the role of the invariant carboxylate residues E552 and E1197 in the catalytic activity of Abcb1a (mouse Mdr3). Carrier I, Gros P. FEBS J 275 3312-3324 (2008)
  41. Structures of the nucleotide-binding domain of the human ABCB6 transporter and its complexes with nucleotides. Haffke M, Menzel A, Carius Y, Jahn D, Heinz DW. Acta Crystallogr D Biol Crystallogr 66 979-987 (2010)
  42. ATP Binding and Hydrolysis Properties of ABCB10 and Their Regulation by Glutathione. Qiu W, Liesa M, Carpenter EP, Shirihai OS. PLoS One 10 e0129772 (2015)
  43. Beyond Toxin Transport: Novel Role of ABC Transporter for Enzymatic Machinery of Cereulide NRPS Assembly Line. Gacek-Matthews A, Chromiková Z, Sulyok M, Lücking G, Barák I, Ehling-Schulz M. mBio 11 e01577-20 (2020)
  44. Glutamine residues in Q-loops of multidrug resistance protein MRP1 contribute to ATP binding via interaction with metal cofactor. Yang R, Hou YX, Campbell CA, Palaniyandi K, Zhao Q, Bordner AJ, Chang XB. Biochim Biophys Acta 1808 1790-1796 (2011)
  45. Mutational analysis of conserved aromatic residues in the A-loop of the ABC transporter ABCB1A (mouse Mdr3). Carrier I, Urbatsch IL, Senior AE, Gros P. FEBS Lett 581 301-308 (2007)
  46. Nucleotide-dependent dimerization of the C-terminal domain of the ABC transporter CvaB in colicin V secretion. Guo X, Harrison RW, Tai PC. J Bacteriol 188 2383-2391 (2006)
  47. Molecular basis for differential nucleotide binding of the nucleotide-binding domain of ABC-transporter CvaB. Guo X, Chen X, Weber IT, Harrison RW, Tai PC. Biochemistry 45 14473-14480 (2006)
  48. The hydroxyl group of S685 in Walker A motif and the carboxyl group of D792 in Walker B motif of NBD1 play a crucial role for multidrug resistance protein folding and function. Yang R, Scavetta R, Chang XB. Biochim Biophys Acta 1778 454-465 (2008)
  49. Interaction between the bound Mg.ATP and the Walker A serine residue in NBD2 of multidrug resistance-associated protein MRP1 plays a crucial role for the ATP-dependent leukotriene C4 transport. Yang R, Scavetta R, Chang XB. Biochemistry 47 8456-8464 (2008)
  50. Structural basis for a homodimeric ATPase subunit of an ECF transporter. Chai C, Yu Y, Zhuo W, Zhao H, Li X, Wang N, Chai J, Yang M. Protein Cell 4 793-801 (2013)
  51. Successful development and use of a thermodynamic stability screen for optimizing the yield of nucleotide binding domains. de Araujo ED, Kanelis V. Protein Expr Purif 103 38-47 (2014)
  52. Dual nucleotide specificity determinants of an infection aborting anticodon nuclease. Krutkina E, Klaiman D, Margalit T, Jerabeck-Willemsen M, Kaufmann G. Virology 487 260-272 (2016)
  53. Replacement of the positively charged Walker A lysine residue with a hydrophobic leucine residue and conformational alterations caused by this mutation in MRP1 impair ATP binding and hydrolysis. Buyse F, Hou YX, Vigano C, Zhao Q, Ruysschaert JM, Chang XB. Biochem J 397 121-130 (2006)
  54. Solution NMR studies of periplasmic binding proteins and their interaction partners. Pistolesi S, Tjandra N, Bermejo GA. Biomol Concepts 2 53-64 (2011)
  55. Microseeding - a powerful tool for crystallizing proteins complexed with hydrolyzable substrates. Oswald C, Smits SHJ, Bremer E, Schmitt L. Int J Mol Sci 9 1131-1141 (2008)
  56. Hepatitis B Virus Oncoprotein HBx Is Not an ATPase. Langton M, Pandelia ME. ACS Omega 5 16772-16778 (2020)
  57. Structural and functional characterization of an orphan ATP-binding cassette ATPase involved in manganese utilization and tolerance in Leptospira spp. Benaroudj N, Saul F, Bellalou J, Miras I, Weber P, Bondet V, Murray GL, Adler B, Ristow P, Louvel H, Haouz A, Picardeau M. J Bacteriol 195 5583-5591 (2013)
  58. Structural assessment of glycyl mutations in invariantly conserved motifs. Prakash T, Sandhu KS, Singh NK, Bhasin Y, Ramakrishnan C, Brahmachari SK. Proteins 69 617-632 (2007)


Related citations provided by authors (2)

  1. Purification, crystallization and preliminary X-ray diffraction analysis of an archaeal ABC-ATPase. Verdon G, Albers SV, Dijkstra BW, Driessen AJ, Thunnissen AM Acta Crystallogr. D Biol. Crystallogr. 58 362-365 (2002)
  2. Glucose transport in the extremely thermoacidophilic Sulfolobus solfataricus involves a high-affinity membrane-integrated binding protein. Albers SV, Elferink MG, Charlebois RL, Sensen CW, Driessen AJ, Konings WN J. Bacteriol. 181 4285-4291 (1999)

Quick links