Elastic network model-based normal mode analysis reveals the conformational couplings in the tripartite AcrAB-TolC multidrug efflux complex

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 10, 2011, Pages 2936-2945

  Wang, Beibei ^a   Weng, Jingwei ^a   Fan, Kangnian ^a   Wang, Wenning ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

Allostery; Cross correlation; Docking; Membrane protein; Transporter

Indexed keywords

ADAPTOR PROTEIN; MEMBRANE PROTEIN; PROTEIN ACRA; PROTEIN ACRB; TOLC PROTEIN; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DRUG TRANSPORT; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI PROTEINS; LIPOPROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR DYNAMICS SIMULATION; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY;

EID: 80052566971     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23143     Document Type: Article

References (43)

1. Higgins CF. Multiple molecular mechanisms for multidrug resistance transporters. Nature 2007; 446: 749-757.
2. Nikaido H. Multidrug efflux pumps of gram-negative bacteria. J Bacteriol 1996; 178: 5853-5859.
3. Zgurskaya HI, Nikaido H. Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proc Natl Acad Sci USA 1999; 96: 7190-7195.
4. Tikhonova EB, Zgurskaya HI. AcrA, AcrB, and TolC of Escherichia coli form a stable intermembrane multidrug efflux complex. J Biol Chem 2004; 279: 32116-32124.
5. Zgurskaya HI, Yamada Y, Tikhonova EB, Ge Q, Krishnamoorthy G. Structural and functional diversity of bacterial membrane fusion proteins. Biochim Biophys Acta 2009; 1794: 794-807.
6. Murakami S, Nakashima R, Yamashita E, Yamaguchi A. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 2002; 419: 587-593.
7. Murakami S, Nakashima R, Yamashita E, Matsumoto T, Yamaguchi A. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 2006; 443: 173-179.
8. Seeger MA, Schiefner A, Eicher T, Verrey F, Diederichs K, Pos KM. Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 2006; 313: 1295-1298.
9. Sennhauser G, Amstutz P, Briand C, Storchenegger O, Grutter MG. Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors. PLoS Biol 2007; 5: 106-113.
10. Tornroth-Horsefield S, Gourdon P, Horsefield R, Brive L, Yamamoto N, Mori H, Snijder A, Neutze R. Crystal structure of AcrB in complex with a single transmembrane subunit reveals another twist. Structure 2007; 15: 1663-1673.
11. Yu EW, McDermott G, Zgurskaya HI, Nikaido H, Koshland DE. Structural basis of multiple drug-binding capacity of the AcrB multidrug efflux pump. Science 2003; 300: 976-980.
12. Mikolosko J, Bobyk K, Zgurskaya HI, Ghosh P. Conformational flexibility in the multidrug efflux system protein AcrA. Structure 2006; 14: 577-587.
13. Zgurskaya HI, Nikaido H. AcrA is a highly asymmetric protein capable of spanning the periplasm. J Mol Biol 1999; 285: 409-420.
14. Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C. Crystal structure of the bacterial membrane protein ToOC central to multidrug efflux and protein export. Nature 2000; 405: 914-919.
15. Takatsuka Y, Chen C, Nikaido H. Mechanism of recognition of compounds of diverse structures by the multidrug efflux pump AcrB of Escherichia coli. Proc Natl Acad Sci USA 2010; 107: 6559-6565.
16. Takatsuka Y, Nikaido H. Covalently linked trimer of the acrb multidrug efflux pump provides support for the functional rotating mechanism. J Bacteriol 2009; 191: 1729-1737.
17. Schulz R, Vargiu AV, Collu F, Kleinekathofer U, Ruggerone P. Functional rotation of the transporter AcrB: insights into drug extrusion from simulations. PLoS Comput Biol 2010; 6:e1000806.
18. Yao X-Q, Kenzaki H, Murakami S, Takada S. Drug export and allosteric coupling in a multidrug transporter revealed by molecular simulations. Nat Commun 2010; 1: 117 doi:10.1038/ncomms1116.
19. Cui Q, Li GH, Ma JP, Karplus M. A normal mode analysis of structural plasticity in the biomolecular motor F-1-ATPase. J Mol Biol 2004; 340: 345-372.
20. Ma JP. New advances in normal mode analysis of supermolecular complexes and applications to structural refinement. Curr Protein Peptide Sci 2004; 5: 119-123.
21. Bahar I, Rader AJ. Coarse-grained normal mode analysis in structural biology. Curr Opin Struct Biol 2005; 15: 586-592.
22. Ma JP. Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes. Structure 2005; 13: 373-380.
23. Weng JW, Ma JP, Fan KN, Wang WN. The conformational coupling and translocation mechanism of vitamin B-12 ATP-binding cassette transporter BtuCD. Biophys J 2008; 94: 612-621.
24. Weng JW, Ma JP, Fan KN, Wang WN. Asymmetric conformational flexibility in the ATP-binding cassette transporter HI1470/1. Biophys J 2009; 96: 1918-1930.
25. Bahar I, Lezon TR, Bakan A, Shrivastava IH. Normal mode analysis of biomolecular structures: functional mechanisms of membrane proteins. Chem Rev 2010; 110: 1463-1497.
26. Bahar I, Lezon TR, Yang LW, Eyal E. Global dynamics of proteins: bridging between structure and function. Annu Rev Biophys 2010; 39: 23-42.
27. Bahar I, Atilgan AR, Erman B. Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Folding Des 1997; 2: 173-181.
28. Tirion MM. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 1996; 77: 1905-1908.
29. Atilgan AR, Durell SR, Jernigan RL, Demirel MC, Keskin O, Bahar I. Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys J 2001; 80: 505-515.
30. Lu MY, Poon B, Ma JP. A new method for coarse-grained elastic normal-mode analysis. J Chem Theory Comput 2006; 2: 464-471.
31. Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006; 22: 195-201.
32. Symmons MF, Bokma E, Koronakis E, Hughes C, Koronakis V. The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc Natl Acad Sci USA 2009; 106: 7173-7178.
33. De Vries SJ, van Dijk ADJ, Krzeminski M, van Dijk M, Thureau A, Hsu V, Wassenaar T, Bonvin A. HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets. Apr 20-21, 2007; Toronto, Canada, pp 726-733.
34. Dominguez C, Boelens R, Bonvin A. HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 2003; 125: 1731-1737.
35. Tamura N, Murakami S, Oyama Y, Ishiguro M, Yamaguchi A. Direct interaction of multidrug efflux transporter AcrB and outer membrane channel TolC detected via site-directed disulfide cross-linking. Biochemistry 2005; 44: 11115-11121.
36. Lobedanz S, Bokma E, Symmons MF, Koronakis E, Hughes C, Koronakis V. A periplasmic coiled-coil interface underlying ToIC recruitment and the assembly of bacterial drug eff lux pumps. Proc Natl Acad Sci USA 2007; 104: 4612-4617.
37. Bavro VN, Pietras Z, Furnham N, Perez-Cano L, Fernandez-Recio J, Pei XY, Misra R, Luisi B. Assembly and channel opening in a bacterial drug efflux machine. Mol Cell 2008; 30: 114-121.
38. Schulz R, Kleinekathofer U. Transitions between closed and open conformations of ToIC: the effects of ions in simulations. Biophys J 2009; 96: 3116-3125.
39. Vaccaro L, Scott KA, Sansom MSP. Gating at both ends and breathing in the middle: conformational dynamics of TolC. Biophys J 2008; 95: 5681-5691.
40. Fernandez-Recio J, Walas F, Federici L, Pratap JV, Bavro VN, Miguel RN, Mizuguchi K, Luisi B. A model of a transmembrane drug-efflux pump from Gram-negative bacteria. FEBS Lett 2004; 578: 5-9.
41. Husain F, Humbard M, Misra R. Interaction between the TolC and AcrA proteins of a multidrug efflux system of Escherichia coli. J Bacteriol 2004; 186: 8533-8536.
42. Touze T, Eswaran J, Bokma E, Koronakis E, Hughes C, Koronakis V. Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Mol Microbiol 2004; 53: 697-706.
43. Tikhonova EB, Yamada Y, Zgurskaya HI. Sequential mechanism of assembly of multidrug efflux pump AcrAB-ToIC. Chem Biol 2011; 18: 454-463.