Molecular mechanism of the Escherichia coli maltose transporter

Current Opinion in Structural Biology

Volumn 23, Issue 4, 2013, Pages 492-498

  Chen, Jue ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; MALTOSE TRANSPORTER; UNCLASSIFIED DRUG;

BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; HYDROLYSIS KINETICS; IMAGE ANALYSIS; MOLECULAR DYNAMICS; MOLECULAR IMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN LOCALIZATION; REVIEW; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ESCHERICHIA COLI;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MALTOSE; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84881106990     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.03.011     Document Type: Review

References (37)

1. Higgins C.F. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 1992, 8:67-113.
2. Monod J., Torriani A.M. Amylomaltase of Escherichia coli. Ann Inst Pasteur (Paris) 1950, 78:65-77.
3. Boos W., Shuman H. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol Mol Biol Rev 1998, 62:204-229.
4. Davidson A.L., Nikaido H. Overproduction, solubilization, and reconstitution of the maltose transport system from Escherichia coli. J Biol Chem 1990, 265:4254-4260.
5. 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.
6. Mannering D.E., Sharma S., Davidson A.L. Demonstration of conformational changes associated with activation of the maltose transport complex. J Biol Chem 2001, 276:12362-12368.
7. Austermuhle M.I., Hall J.A., Klug C.S., Davidson A.L. Maltose-binding protein is open in the catalytic transition state for ATP hydrolysis during maltose transport. J Biol Chem 2004, 279:28243-28250.
8. Grote M., Polyhach Y., Jeschke G., Steinhoff H.J., Schneider E., Bordignon E. 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 2009, 284:17521-17526.
9. Oldham M.L., Khare D., Quiocho Q.A., Davidson A.L., Chen J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature 2007, 450:515-521.
10. Khare D., Oldham M.L., Orelle C., Davidson A.L., Chen J. Alternating access in maltose transporter mediated by rigid-body rotations. Mol Cell 2009, 33:528-536.
11. Oldham M.L., Chen J. Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science 2011, 332:1202-1205.
12. Davidson A.L., Shuman H.A., Nikaido H. Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins. Proc Natl Acad Sci U S A 1992, 89:2360-2364.
13. Samanta S., Ayvaz T., Reyes M., Shuman H.A., Chen J., Davidson A.L. Disulfide crosslinking reveals a site of stable interaction between C-terminal regulatory domains of the two MalK subunits in the maltose transport complex. Journal of Biological Chemistry 2003, 278:35265-35271.
14. Long S.B., Tao X., Campbell E.B., MacKinnon R. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 2007, 450:376-382.
15. Oldham M.L., Chen J. Snapshots of the maltose transporter during ATP hydrolysis. Proc Natl Acad Sci U S A 2011, 108:15152-15156.
16. 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.
17. Shuman H.A. 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 1982, 257:5455-5461.
18. Merino G., Shuman H.A. Unliganded maltose-binding protein triggers lactose transport in an Escherichia coli mutant with an alteration in the maltose transport system. J Bacteriol 1997, 179:7687-7694.
19. Cui J., Qasim S., Davidson A.L. Uncoupling substrate transport from ATP hydrolysis in the Escherichia coli maltose transporter. J Biol Chem 2010, 285:39986-39993.
20. Quiocho F.A., Spurlino J.C., Rodseth L.E. Extensive features of tight oligosaccharide binding revealed in high-resolution structures of the maltodextrin transport/chemosensory receptor. Structure 1997, 5:997-1015.
21. Treptow N.A., Shuman H.A. 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 1985, 163:654-660.
22. Duan X., Quiocho F.A. Structural evidence for a dominant role of nonpolar interactions in the binding of a transport/chemosensory receptor to its highly polar ligands. Biochemistry 2002, 41:706-712.
23. 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.
24. Orelle C., Alvarez F.J., Oldham M.L., Orelle A., Wiley T.E., Chen J., Davidson A.L. Dynamics of alpha-helical subdomain rotation in the intact maltose ATP-binding cassette transporter. Proc Natl Acad Sci U S A 2010, 107:20293-20298.
25. Grote M., Bordignon E., Polyhach Y., Jeschke G., Steinhoff H.J., Schneider E. A comparative electron paramagnetic resonance study of the nucleotide-binding domains' catalytic cycle in the assembled maltose ATP-binding cassette importer. Biophys J 2008, 95:2924-2938.
26. 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.
27. Wang B., Dukarevich M., Sun E.I., Yen M.R., Saier M.H. Membrane porters of ATP-binding cassette transport systems are polyphyletic. J Membr Biol 2009, 231:1-10.
28. Kadaba N.S., Kaiser J.T., Johnson E., Lee A., Rees D.C. The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 2008, 321:250-253.
29. 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. Nat Struct Mol Biol 2010, 17:332-338.
30. Joseph B., Jeschke G., Goetz B.A., Locher K.P., Bordignon E. Transmembrane gate movements in the type II ATP-binding cassette (ABC) importer BtuCD-F during nucleotide cycle. J Biol Chem 2011, 286:41008-41017.
31. Korkhov V.M., Mireku S.A., Hvorup R.N., Locher K.P. Asymmetric states of vitamin B(1)(2) transporter BtuCD are not discriminated by its cognate substrate binding protein BtuF. FEBS Lett 2012, 586:972-976.
32. Korkhov V.M., Mireku S.A., Locher K.P. Structure of AMP-PNP-bound vitamin B12 transporter BtuCD-F. Nature 2012, 490:367-372.
33. Dawson R.J., Locher K.P. Structure of a bacterial multidrug ABC transporter. Nature 2006, 443:180-185.
34. Ward A., Reyes C.L., Yu J., Roth C.B., Chang G. Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc Natl Acad Sci U S A 2007, 104:19005-19010.
35. Aller S.G., Yu J., Ward A., Weng Y., Chittaboina S., Zhuo R., Harrell P.M., Trinh Y.T., Zhang Q., Urbatsch I.L., et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 2009, 323:1718-1722.
36. Jin M.S., Oldham M.L., Zhang Q., Chen J. Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans. Nature 2012, 490:566-569.
37. Hohl M., Briand C., Grutter M.G., Seeger M.A. Crystal structure of a heterodimeric ABC transporter in its inward-facing conformation. Nat Struct Mol Biol 2012, 19:395-402.