Receptor-transporter interactions of canonical ATP-binding cassette import systems in prokaryotes

European Journal of Cell Biology

Volumn 91, Issue 4, 2012, Pages 311-317

  Schneider, Erwin ^a   Eckey, Viola ^a,c   Weidlich, Daniela ^a   Wiesemann, Nicole ^a   Vahedi Faridi, Ardeshir ^b   Thaben, Paul ^b   Saenger, Wolfram ^b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c BAM FEDERAL INSTITUTE FOR MATERIALS RESEARCH AND TESTING   (Germany)

Author keywords

ABC transporters; Arginine transporter; Binding proteins; Crystal structures; Escherichia coli; Geobacillus stearothermophilus; Maltose transporter; Solute receptors; Transmembrane communication

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A1; ARGININE; GLUTAMIC ACID; GLUTAMINE; HISTIDINE; ISOLEUCINE; LYSINE; MALTOSE BINDING PROTEIN; TYROSINE;

BINDING AFFINITY; BINDING SITE; CROSS LINKING; CRYSTAL STRUCTURE; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GEOBACILLUS STEAROTHERMOPHILUS; HYDROLYSIS; LIGAND BINDING; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN BINDING; RECEPTOR BINDING; RECEPTOR TRANSPORTER INTERACTION; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; SHORT SURVEY; SURFACE CHARGE;

ATP-BINDING CASSETTE TRANSPORTERS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GEOBACILLUS STEAROTHERMOPHILUS; PROTEIN STRUCTURE, TERTIARY; SALMONELLA TYPHIMURIUM; WATER-ELECTROLYTE BALANCE;

ENTEROBACTERIACEAE; ESCHERICHIA COLI; GEOBACILLUS STEAROTHERMOPHILUS; PROKARYOTA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 84857374524     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2011.02.008     Document Type: Short Survey

References (63)

1. Alvarez F.J., Orelle C., Davidson A.L. Functional reconstitution of an ABC transporter in nanodiscs for use in electron paramagnetic resonance spectroscopy. J. Am. Chem. Soc. 2010, 132:9513-9515.
2. Ames G.F.-L. Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu. Rev. Biochem. 1986, 55:397-452.
3. Ames G.F.-L., Liu C.E., Joshi A.K., Nikaido K. Liganded and unliganded receptors interact with equal affinity with the membrane complex of periplasmic permeases, a subfamily of traffic ATPases. J. Biol. Chem. 1996, 271:14264-14270.
4. Ames G.F.-L., Nikaido K., Wang I.X., Liu P.-Q., Liu C.E., Hu C. Purification and characterization of the membrane-bound complex of an ABC transporter, the histidine permease. J. Bioenerg. Biomembr. 2001, 33:79-92.
5. Berntsson R.P., Smits S.H., Schmitt L., Slotboom D.J., Poolman B. A structural classification of substrate-binding proteins. FEBS Lett. 2010, 584:2606-2617.
6. Biemans-Oldehinkel E., Poolman B. On the role of the two extracytoplasmic substrate binding domains in the ABC transporter OpuA. EMBO J. 2003, 22:5983-5993.
7. Biemans-Oldehinkel E., Doeven M.K., Poolman B. ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett. 2006, 580:1023-1035.
8. Blüschke B., Eckey V., Kunert B., Berendt S., Landmesser H., Portwich M., Volkmer R., Schneider E. Mapping putative contact sites between subunits in a bacterial ATP binding cassette (ABC) transporter by synthetic peptide libraries. J. Mol. Biol. 2007, 369:386-399.
9. Bohl E., Shuman H.A., Boos W. Mathematical treatment of the kinetics of binding protein dependent transport systems reveals that both the substrate loaded and unloaded binding proteins interact with the membrane components. J. Theor. Biol. 1995, 172:83-94.
10. Boos W., Shuman H. Maltose/maltodextrin system of Escherichia coli: transport, metabolism and regulation. Microbiol. Mol. Biol. Rev. 1998, 62:204-229.
11. Bordignon E., Grote M., Schneider E. The maltose ABC transporter in the 21st century - towards a structural-dynamic perspective on its mode of action. Mol. Microbiol. 2010, 77:1354-1366.
12. Braun V., Herrmann C. Docking of the periplasmic FecB binding protein to the FecCD transmembrane proteins in the ferric citrate transport system of Escherichia coli. J. Bacteriol. 2007, 189:6913-6918.
13. Chen C., Malek A.A., Wargo M.J., Hogan D.A., Beattie G.A. The ATP-binding cassette transporter Cbc (choline/betaine/carnitine) recruits multiple substrate-binding proteins with strong specificity for distinct quaternary ammonium compounds. Mol. Microbiol. 2010, 75:29-45.
14. Chen J., Lu G., Lin J., Davidson A.L., Quiocho F.A. A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell 2003, 12:651-661.
15. Chen J., Sharma S., Quiocho F.A., Davidson A.L. 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. 2001, 98:1525-1530.
16. Covitz K.-M.Y., Panagiotidis C.H., Hor L.-I., Reyes M., Treptow N.A., Shuman H.A. Mutations that alter the transmembrane signalling pathway in an ATP binding cassette (ABC) transporter. EMBO J. 1994, 13:1752-1759.
17. Cui J., Qasim S., Davidson A.L. Uncoupling substrate transport from ATP hydrolysis in the Escherichia coli maltose transporter. J. Biol. Chem. 2011, 285:39986-39993.
18. Daus M.L., Grote M., Müller P., Doebber M., Herrmann A., Steinhoff H.-J., Dassa E., Schneider E. ATP-driven MalK dimer closure and re-opening and conformational changes of the 'EAA' motifs are crucial for function of the maltose ATP-binding cassette transporter (MalFGK2). J. Biol. Chem. 2007, 282:22369-22387.
19. 2 from Escherichia coli/Salmonella enterica serovar Typhimurium interacts with maltose binding protein (MalE) throughout the catalytic cycle. J. Bacteriol. 2009, 191:754-761.
20. 2) from Escherichia coli/Salmonella during the transport cycle. Mol. Microbiol. 2007, 66:1107-1122.
21. Daus M.L., Landmesser H., Schlosser A., Müller P., Herrmann A., Schneider E. ATP induces conformational changes of periplasmic loop regions of the maltose ATP binding cassette transporter. J. Biol. Chem. 2006, 281:3856-3865.
22. Davidson A.L., Dassa E., Orelle C., Chen J. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 2008, 72:317-364.
23. Doeven M.K., van den Bogaart G., Krasnikov V., Poolman B. Probing receptor translocator interactions in the oligopeptide ABC transporter by fluorescence correlation spectroscopy. Biophys. J. 2008, 94:3956-3965.
24. Dawson R.J.P., Locher K.P. Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett. 2007, 581:935-938.
25. Eckey V., Landmesser H., Schneider E. Studying subunit-subunit interactions in a bacterial ABC transporter by in vitro-assembly. Biochem. Biophys. Acta 2010, 1798:1250-1253.
26. Eckey V., Weidlich W., Landmesser H., Bergmann U., Schneider E. The second extracellular loop of pore-forming subunits of ATP-binding cassette transporters for basic amino acids plays a crucial role in interaction with the cognate solute binding protein(s). J. Bacteriol. 2010, 192:2150-2159.
27. Eitinger T., Rodionov D.A., Grote M., Schneider E. Canonical and ECF-type ATP binding cassette importers in prokaryotes: diversity in modular organisation and cellular functions. FEMS Microbiol. Rev. 2011, 35:3-67.
28. Fleischer R., Wengner A., Scheffel F., Landmesser H., Schneider E. Identification of a gene cluster encoding an arginine ATP-binding-cassette transporter in the genome of the thermophilic gram-positive bacterium Geobacillus stearothermophilus DSMZ 13240. Microbiology 2005, 151:835-840.
29. Gould A.D., Shilton B.H. Studies of the maltose transport system reveal a mechanism for coupling ATP hydrolysis to substrate translocation without direct recognition of substrate. J. Biol. Chem. 2010, 285:11290-11296.
30. Grote M., Bordignon E., Polyhach Y., Jeschke G., Steinhoff H.-J., Schneider E. A comparative EPR study of the nucleotide-binding domains' catalytic cycle in the assembled maltose ABC-importer. Biophys. J. 2008, 95:2924-2938.
31. 2-E. Periplasmic MalFP2 loop communicates substrate availability to the ATP-bound MalK dimer. J. Biol. Chem. 2009, 284:17521-17526.
32. ABC Proteins: From Bacteria to Man 2003, Elsevier, Amsterdam. I.B. Holland, S.P.C. Cole, K. Kuchler, C.F. Higgins (Eds.).
33. Hollenstein K., Frei D.C., Locher K.P. Structure of an ABC transporter in complex with its binding protein. Nature 2007, 446:213-216.
34. Hvorup R.N., Goetz B.A., Niederer M., Hollenstein K., Perozo E., Locher K.P. Asymmetry in the structure of the ABC transporter-binding protein complex BtuCD-BtuF. Science 2007, 317:1387-1390.
35. Jacso T., Grote M., Daus M.L., Schmieder P., Keller S., Schneider E., Reif B. The periplasmic loop P2 of the MalF subunit of the maltose ATP binding cassette transporter is sufficient to bind the maltose binding protein MalE. Biochemistry 2009, 48:2216-2225.
36. Khare D., Oldham M., Orelle C., Davidson A.L., Chen J. Alternating access in maltose transporter mediated by rigid-body rotations. Mol. Cell 2009, 33:528-536.
37. Koyanagi T., Katayama T., Suzuki H., Kumagai H. Identification of the LIV-I/LS system as the third phenylalanine transporter in Escherichia coli K-12. J. Bacteriol. 2004, 186:343-350.
38. Lange V., Becker-Baldus J., Kunert B., van Rossum B.-J., Casagrande F., Engel A., Roske Y., Scheffel F.M., Schneider E., Oschkinat H. A MAS NMR study of the bacterial ABC transporter ArtMP. Chem. BioChem. 2010, 11:547-555.
39. Lecher J., Pittelkow M., Zobel S., Bursy J., Bönig T., Smits S.H.J., Schmitt L., Bremer E. The crystal structure of UehA in complex with ectoine - A comparison with other TRAP-T binding proteins. J. Mol. Biol. 2009, 389:58-73.
40. Lewinson O., Lee A.T., Locher K.P., Rees D.C. A distinct mechanism for the ABC transporter BtuCD-BtuF revealed by the dynamics of complex formation. Nature Struct. Mol. Biol. 2010, 17:332-338.
41. Liu C.E., Liu P.-Q., Wolf A., Lin E., Ames G.F.-L. Both lobes of the soluble receptor of the periplasmic histidine permease, an ABC transporter (traffic ATPase) interact with the membrane-bound complex. J. Biol. Chem. 1999, 274:739-747.
42. Locher K. Structure and mechanism of ATP-binding cassette transporters. Phil. Trans. R. Soc. B 2009, 364:239-245.
43. Lu G., Westbrooks J.M., Davidson A.L., Chen J. ATP hydrolysis is required to reset the ATP-binding cassette dimer into the resting-state conformation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17969-17974.
44. Mourez M., Hofnung M., Dassa E. 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. 1997, 16:3066-3077.
45. Mulligan C., Fischer M., Thomas G.H. Tripartite ATP-independent periplasmic (TRAP) transporters in bacteria and archaea. FEMS Microbiol. Rev. 2011, 35:68-86.
46. Nikaido K., Ames G.F.-L. Purification and characterization of the periplasmic lysine-arginine-ornithine-binding protein (LAO) from Salmonella typhimurium. J. Biol. Chem. 1992, 267:20706-20712.
47. Noll K.M., Lapierre P., Gogarten J.P., Nanavati D.M. Evolution of mal ABC transporter operons in the Thermococcales and Thermotogales. BMC Evol. Biol. 2008, 8:7.
48. Oh B.-H., Kang C.H., De Bondt H., Kim S.-H., Nikaido K., Joshi A.K., Ames G.F.-L. The bacterial periplasmic histidine-binding protein. Structure/function analysis of the ligand-binding site and comparison with related proteins. J. Biol. Chem. 1994, 269:4135-4143.
49. Oldham M.L., Khare D., Quiocho F.A., Davidson A.L., Chen J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature 2007, 450:515-522.
50. Orelle C., Ayvaz T., Everly R.M., Klug C.S., Davidson A.L. 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. 2008, 105:12837-12842.
51. Oswald C., Holland I.B., Schmitt L. The motor domains of ABC-transporters. What can structures tell us?. Naunyn-Schmiedeberg's Arch. Pharmacol. 2006, 372:385-399.
52. Quiocho F.A., Ledvina P.S. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol. Microbiol. 1996, 20:17-25.
53. Rees D.C., Johnson E., Lewinson O. ABC transporters: the power to change. Nature Rev. Mol. Cell Biol. 2009, 10:218-227.
54. Saurin W., Köster W., Dassa E. Bacterial binding protein dependent permeases: characterization of distinctive signatures for functionally related integral cytoplasmic membrane proteins. Mol. Microbiol. 1994, 12:993-1004.
55. Schneider E. Import of solutes by ABC transporters-the maltose and other systems. ABC Proteins: From Bacteria to Man 2003, 157-185. Elsevier, Amsterdam. E.B. Holland, S. Cole, K. Kuchler, C. Higgins (Eds.).
56. Schneider E., Hunke S. ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains. FEMS Microbiol. Rev. 1998, 22:1-20.
57. Shilton B.H. The dynamics of the MBP-MalFGK(2) interaction: a prototype for binding protein dependent ABC-transporter systems. Biochim. Biophys. Acta 2008, 1778:1772-1780.
58. Sutcliffe I.C., Russell R.R. Lipoproteins of gram-positive bacteria. J. Bacteriol. 1995, 177:1123-1128.
59. 2. J. Mol. Biol. 2008, 375:448-459.
60. van der Heide T., Poolman B. ABC transporters: one, two or four extracytoplasmic substrate-binding sites?. EMBO Rep. 2002, 3:938-943.
61. Wilkinson A.J., Verschueren K.H.G. Crystal structures of periplasmic solute-binding proteins in ABC transport complexes illuminate their function. ABC Proteins: From Bacteria to Man 2003, 187-207. Elsevier, Amsterdam. E.B. Holland, S. Cole, K. Kuchler, C. Higgins (Eds.).
62. Zhang P., Wang J., Shi Y. Structure and mechanism of the S component of a bacterial ECF transporter. Nature 2010, 468:717-720.
63. Zou P., Mchaourab H.S. Increased sensitivity and extended range of distance measurements in spin-labeled membrane proteins: Q-band double electron-electron resonance and nanoscale bilayers. Biophys. J. 2010, 98:L18-L20.