The lipid bilayer modulates the structure and function of an ATP-binding cassette exporter

Journal of Biological Chemistry

Volumn 291, Issue 9, 2016, Pages 4453-4461

  Zoghbi, Maria E ^a   Cooper, Rebecca S ^a   Altenberg, Guillermo A ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINETRIPHOSPHATE; BINS; BIOLOGICAL MEMBRANES; CONFORMATIONS; ENERGY TRANSFER; FACINGS; HYDROLYSIS; LIPID BILAYERS; NUCLEOTIDES; PROTEINS; TEMPERATURE;

ATP-BINDING CASSETTE; DOUBLE ELECTRON-ELECTRON RESONANCE; MEMBRANE PROTEINS; NUCLEOTIDE-BINDING DOMAIN; PHYSIOLOGICAL CONDITION; RESONANCE ENERGY TRANSFER; STRUCTURAL STUDIES; TRANSPORT SUBSTRATES;

BINDING ENERGY;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; MSBA PROTEIN; NANODISC; ABC TRANSPORTER; BACTERIAL PROTEIN; HYBRID PROTEIN; LIPID BILAYER; MEMBRANE PROTEIN; MSBA PROTEIN, BACTERIA; NANOMATERIAL;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; HYDROLYSIS; LIPID BILAYER; LUMINESCENCE RESONANCE ENERGY TRANSFER SPECTROSCOPY; MEMBRANE RECONSTITUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; SPECTROSCOPY; STRUCTURE ACTIVITY RELATION; TEMPERATURE; AMINO ACID SUBSTITUTION; BIOLOGICAL MODEL; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CELL MEMBRANE; CHEMISTRY; COMPARATIVE STUDY; ENZYME STABILITY; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MUTATION; PROTEIN UNFOLDING; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

ADENOSINE TRIPHOSPHATE; AMINO ACID SUBSTITUTION; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BINDING SITES; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER TECHNIQUES; ENZYME STABILITY; HYDROLYSIS; KINETICS; LIPID BILAYERS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MUTATION; NANOSTRUCTURES; PROTEIN CONFORMATION; PROTEIN UNFOLDING; RECOMBINANT FUSION PROTEINS; SALMONELLA TYPHIMURIUM;

EID: 84961862480     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.698498     Document Type: Article

References (43)

1. Al-Shawi, M. K. (2011) Catalytic and transport cycles of ABC exporters. Essays Biochem. 50, 63-83
2. Bouige, P., Laurent, D., Piloyan, L., and Dassa, E. (2002) Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr. Protein Pept. Sci. 3, 541-559
3. Sharom, F. J. (2008) ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 9, 105-127
4. Hopfner, K. P., Karcher, A., Shin, D. S., Craig, L., and Arthur, L. M., Carney, J. P., and Tainer, J. A. (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
5. Smith, P. C., Karpowich, N., Millen, L., Moody, J. E., Rosen, J., and Thomas, P. J., and Hunt, J.F. (2002) ATP bindingtothe motor domain froman ABC transporter drives formation of anucleotide sandwich dimer. Mol. Cell 10, 139-149
6. Zoghbi, M. E., and Altenberg, G. A. (2014) ATP binding to two sites is necessary for dimerization of nucleotide-binding domains of ABC proteins. Biochem. Biophys. Res. Commun. 443, 97-102
7. Zoghbi, M. E., and Altenberg, G. A. (2013) Hydrolysis at one of the two nucleotide-binding sites drives the dissociation of ATP-binding cassette nucleotide-binding domain dimers. J. Biol. Chem. 288, 34259-34265
8. King, G., and Sharom, F. J. (2012) Proteins that bind and move lipids: MsbA and NPC1. Crit. Rev. Biochem. Mol. Biol. 47, 75-95
9. Doerrler, W. T., and Gibbons, H. S., and Raetz, C. R. (2004) MsbA-dependent translocation of lipids across the inner membrane of Escherichia coli. J. Biol. Chem. 279, 45102-45109
10. Doerrler, W. T., and Raetz, C. R. (2002) ATPase activity of the MsbA lipid flippase of Escherichia coli. J. Biol. Chem. 277, 36697-36705
11. Ward, A., and Reyes, C. L., Yu, J., Roth, C. B., and Chang, G. (2007) Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc. Natl. Acad. Sci. U.S.A. 104, 19005-19010
12. Mishra, S., Verhalen, B., Stein, R. A., and Wen, P. C., Tajkhorshid, E., and McHaourab, H. S. (2014) Conformational dynamics of the nucleotide binding domains and the power stroke of a heterodimeric ABC transporter. eLife 3, e02740
13. Zou, P., and McHaourab, H. S. (2010) Increased sensitivity and extended range of distance measurements in spin-labeled membrane proteins: Q-band double electron-electron resonance and nanoscale bilayers. Biophys. J. 98, L18-L20
14. Zou, P., and McHaourab, H. S. (2009) Alternating access of the putative substrate-binding chamber in the ABC transporter Msb A. J. Mol. Biol. 393, 574-585
15. Buchaklian, A. H., and Klug, C. S. (2005) Characterization of the Walker A motif of MsbA using site-directed spin labeling electron paramagnetic resonance spectroscopy. Biochemistry 44, 5503-5509
16. Schultz, K. M., and Merten, J. A., and Klug, C. S. (2011) Characterization of the E506Q and H537A dysfunctional mutants in the E. coli ABC transporter Msb A. Biochemistry 50, 3599-3608
17. Eckford, P. D., and Sharom, F. J. (2008) Functional characterization of Escherichia coli MsbA: interaction with nucleotides and substrates. J. Biol. Chem. 283, 12840-12850
18. Cooper, R. S., and Altenberg, G. A. (2013) Association/dissociation of the nucleotide-binding domains of the ATP-binding cassette protein MsbA measured during continuous hydrolysis. J. Biol. Chem. 288, 20785-20796
19. George, A. M., and Jones, P. M. (2013) An asymmetric post-hydrolysis state of the ABC transporter ATPase dimer. PLoS One 8, e59854
20. Jones, P. M., O'Mara, M. L., and George, A. M. (2009) ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem. Sci. 34, 520-531
21. Jones, P. M., and George, A. M. (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
22. Verhalen, B., Ernst, S., Börsch, M., and 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
23. Borbat, P. P., Surendhran, K., Bortolus, M., Zou, P., and Freed, J. H., and McHaourab, H. S. (2007) Conformational motion of the ABC transporter MsbA induced by ATP hydrolysis. PLoS Biol. 5, e271
24. Aller, S. G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R., Harrell, P. M., and Trinh, Y. T., Zhang, Q., Urbatsch, I. L., and Chang, G. (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722
25. Li, J., and Jaimes, K. F., and Aller, S. G. (2014) Refined structures of mouse P-glycoprotein. Protein Sci. 23, 34-46
26. Wen, P. C, Verhalen, B., Wilkens, S., McHaourab, H. S., and Tajkhorshid, E. (2013) On the origin of large flexibility of P-glycoprotein in the inwardfacing state. J. Biol. Chem. 288, 19211-19220
27. Ritchie, T. K., and Grinkova, Y. V., Bayburt, T. H., Denisov, I. G., and Zolnerciks, J. K., Atkins, W. M., and Sligar, S. G. (2009) Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Methods Enzymol. 464, 211-231
28. Zoghbi, M. E., Krishnan, S., and Altenberg, G. A. (2012) Dissociation of ATP-binding cassette nucleotide-binding domain dimers into monomers during the hydrolysis cycle. J. Biol. Chem. 287, 14994-15000
29. Zoghbi, M. E., and Fuson, K. L., Sutton, R. B., and Altenberg, G. A. (2012) Kinetics of the association/dissociation cycle of an ATP-binding cassette nucleotide-binding domain. J. Biol. Chem. 287, 4157-4164
30. + channel voltage sensor measured with luminescence energy transfer. Nature 436, 848-851
31. Selvin, P. R. (2002) Principles and biophysical applications of lanthanide-based probes. Annu. Rev. Biophys. Biomol. Struct. 31, 275-302
32. Urbatsch, I. L., Sankaran, B., Weber, J., and Senior, A. E. (1995) P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J. Biol. Chem. 270, 19383-19390
33. Heyduk, T., and Heyduk, E. (2001) Luminescence energy transfer with lanthanide chelates: interpretation of sensitized acceptor decay amplitudes. Anal. Biochem. 289, 60-67
34. James, D.R., and Ware, W. R. (1986) Recovery of underlying distributions of lifetimes from fluorescence decay data. Chem. Physics Lett. 126, 7-11
35. Siemiarczuk, A., Wagner, B.D., and Ware, W. R. (1990) Comparison of the maximum entropy and exponential series methods for the recovery of distributions of lifetimes from fluorescence lifetime data. J. Phys. Chem. 94, 1661-1666
36. + channels. Neuron 59, 98-109
37. Kawai, T., and Caaveiro, J. M., Abe, R., Katagiri, T., and Tsumoto, K. (2011) Catalytic activity of MsbA reconstituted in nanodisc particles is modulated by remote interactions with the bilayer. FEBS Lett. 585, 3533-3537
38. Cha, A., and Snyder, G. E., Selvin, P. R., and Bezanilla, F. (1999) Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy. Nature 402, 809-813
39. Lee, J. Y., and Urbatsch, I. L., Senior, A. E., and Wilkens, S. (2002) Projection structure of P-glycoprotein by electron microscopy: evidence for a closed conformation of the nucleotide binding domains. J. Biol. Chem. 277, 40125-40131
40. Zou, P., Bortolus, M., and McHaourab, H. S. (2009) Conformational cycle of the ABC transporter MsbA in liposomes: detailed analysis using double electron-electron resonance spectroscopy. J. Mol. Biol. 393, 586-597
41. Fribourg, P. F., Chami, M., Sorzano, C. O., Gubellini, F., Marabini, R., Marco, S., Jault, J.M., and Lévy, D. (2014) 3D cryo-electron reconstruction of Bmr A, a bacterial multidrug ABC transporter in an inward-facing conformation and in a lipidic environment. J. Mol. Biol. 426, 2059-2069
42. Lee, J. Y., and Urbatsch, I. L., Senior, A. E., and Wilkens, S. (2008) Nucleotide-induced structural changes in P-glycoprotein observed by electron microscopy. J. Biol. Chem. 283, 5769-5779
43. Mehmood, S., Domene, C, Forest, E., and Jault, J. M. (2012) Dynamics of a bacterial multidrug ABC transporter in the inward- and outward-facing conformations. Proc. Natl. Acad. Sci. U.S.A. 109, 10832-10836