Caught in the Act: ATP hydrolysis of an ABC-multidrug transporter followed by real-time magic angle spinning NMR

FEBS Letters

Volumn 582, Issue 23-24, 2008, Pages 3557-3562

  Hellmich, Ute A ^a   Haase, Winfried ^b   Velamakanni, Saroj ^c   van Veen, Hendrik W ^c   Glaubitz, Clemens ^a  

^a Centre for Biomolecular Magnetic Resonance   (Germany)

^b MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

31P NMR; ABC transporter; ATP hydrolysis; Real time NMR; Solid state NMR

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; PROTEIN LMRA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROLYSIS; KINETICS; LACTOCOCCUS LACTIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; HYDROLYSIS; KINETICS; MICROSCOPY, ELECTRON; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHORUS ISOTOPES; TIME FACTORS;

LACTOCOCCUS LACTIS;

EID: 53049103551     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2008.09.033     Document Type: Article

References (34)

1. van Veen H.W., Callaghan R., Soceneantu L., Sardini A., Konings W.N., and Higgins C.F. A bacterial antibiotic-resistance gene that complements the human multidrug-resistance P-glycoprotein gene. Nature 391 (1998) 291-295
2. van Veen H.W., Müller M., Hioggins C.F., and Konings W.N. The homodimeric ATP-binding cassette transporter LmrA mediates multidrug transport by an alternating two-site (two-cylinder engine) mechanism. EMBO J. 19 11 (2000) 1514-2503
3. Schneider E., and Hunke S. ATP-binding cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains. FEMS Microbiol. Rev. 22 (1998) 1-20
4. Locher K.P., Lee A.T., and Rees C.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296 5570 (2002) 1091-1098
5. Dawson R.JP., and Locher K.P. Structure of a bacterial multidrug ABC transporter. Nature 443 (2006) 180-185
6. Dawson R.JP., and Locher K.P. Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett. 581 (2007) 935-938
7. Hollenstein K., Frei D.C., and Locher K.P. Structure of an ABC transporter in complex with its binding protein. Nature 446 (2007) 213-216
8. Gerber S., Comellas-Bigler M., Goetz B.A., and Locher K.P. Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science 321 (2008) 246-250
9. Pinkett H.W., Lee A.T., Lum P., Locher K.P., and Rees D.C. An inward facing conformation of a putative metal-chelate-type ABC transporter. Science 315 (2007) 373-377
10. Ward A., Reyes C.L., Yu J., Roth C.B., and Chang G. Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc. Natl. Acad. Sci. USA 104 48 (2007) 19005-19010
11. Oldham M.L., Khare D., Quiocho F.A., Davidson A., and Chen J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450 (2007) 515-522
12. Kadaba N.S., Kaiser J.T., Johnson E., Lee A., and Rees D.C. The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 321 (2008) 250-253
13. Oswald C., Holland B.I., and Schmitt L. The motor domains of ABC transporters - what can structures tell us?. Naunyn-Schmiedeberg's Arch. Pharmacol. 372 (2006) 385-399
14. Siarheyeva A., Lopez J.J., Lehner I., Hellmich U.A., van Veen H.W., and Glaubitz C. Probing the molecular dynamics of the ABC multidrug transporter LmrA by deuterium solid-state nuclear magnetic resonance. Biochemistry 46 (2007) 3075-3083
15. Lehner I., Basting D., Meyer B., Haase W., Manolikas T., Kaiser C., Karas M., and Glaubitz C. The key residue for substrate transport (Glu 14) in the EmrE dimer is asymmetric. J. Biol. Chem. 283 6 (2008) 3281-3288
16. Patching S.G., Henderson P.J.F., Herbert R.B., and Middleton D.A. Solid-state NMR Spectroscopy detects interactions between tryptophan residues of the E. coli sugar transporter GalP and the alpha-anomer of the d-glucose substrate. J. Am. Chem. Soc. 130 (2008) 1236-1244
17. Placzek W.J., Almeida M.S., and Wüthrich K. NMR structure and functional characterization of a human cancer-related nucleoside triphosphatase. J. Mol. Biol. 367 (2007) 788-801
18. Ugurbil K., Rottenberg H., Glynn P., and Shulman R.G. 31P nuclear magnetic resonance studies of bioenergetics and glycolysis in anaerobic Escherichia coli cells. Proc. Natl. Acad. Sci. USA 55 (1978) 2244-2248
19. 31P MRS: a quantitative review. NMR Biomed. 20 (2007) 555-565
20. Brown T.R., Ugurbil K., and Shulman R.G. 31P nuclear magnetic resonance measurements of ATPase kinetics in aerobic Escherichia coli cells. Proc. Natl. Acad. Sci. USA 74 (1977) 5551-5553
21. Brune M., Hunter J.L., Corrie J.E.T., and Webb M.R. Direct, Real-Time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment 1 ATPase. Biochemistry 33 (1994) 8262-8271
22. He Z.-H., Chillingworth R.K., Brune M., Corrie J.E.T., Trentham D.R., Webb M.R., and Ferenczi M.A. ATPase kinetics on activation of rabbit and frog permeabilized isometric muscle fibers: a real time phosphate assay. J. Physiol. 501 (1997) 125-148
23. 2+-stimulated ATPase activity. Anal. Biochem. 157 (1986) 375-380
24. Janvilisri T., Venter H., Shahi S., Reuter G., Balakrishnan L., and van Veen H.W. Sterol transport by the human breast cancer resistance protein (ABCG2) expressed in Lactococcus lactis. J. Biol. Chem. 278 23 (2003) 20645-20651
25. 32Pi onto filter papers. Application to ATPase and cyclic AMP phosphodiesterase determination. Biochim. Biophys. Acta 523 2 (1978) :516-521
26. Badola P., and Sanders II C.R. Escherichia coli diacylglycerol kinase is an evolutionary optimized membrane enzyme and catalyzes direct phosphoryl transfer. J. Biol. Chem. 272 39 (1997) 24176-24182
27. Venter H., Velamakanni s., Balakrishnan L., and van Veen H.W. On the energy-dependence of Hoechst 33342 transport by the ABC-transporter LmrA. Biochem. Pharmacol. 75 4 (2007) 866-874
28. Venter H., Shilling R.A., Velamakanni S., Balakrishnan L., and van Veen H.W. An ABC-transporter with a secondary-active multidrug translocator domain. Nature 426 (2003) 866-870
29. Margolles A., Putmann M., van Veen H.W., and Konings W.N. The purified and functionally reconstituted multidrug transporter LmrA of Lactococcus lactis mediates the transbilayer movement of specific fluorescent phospholipds. Biochemistry 38 (1999) 16298-16306
30. Fung B.M., Khitrin A.K., and Ermolaev K. An improved broadband decoupling sequence for liquid crystals and solids. J. Magn. Reson. 142 (2000) 97-101
31. Mason J., Siarheyeva A., Haase W., Lorch M., van Veen H.W., and Glaubitz C. Amino acid type selective isotope labeling of the multidrug ABC transporter LmrA for solid-state NMR studies. FEBS Lett. 568 (2004) 117-121
32. 13C cross-polarization magic-angle spinning NMR spectroscopy. FEBS Lett. 580 (2006) 6685-6689
33. Cohn M., and Hughes T.R. Nuclear magnetic resonance spectra of adenosine di- and tri-phosphate - II: effect of complexing with divalent metal ions. J. Biol. Chem. 237 1 (1962) 176-181
34. 2+ in intact frog skeletal muscle. J. Biol. Chem. 255 9 (1980) 3987-3993