Simulations of substrate transport in the multidrug transporter EmrD

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 6, 2012, Pages 1620-1632

  Baker, Joseph ^a   Wright, Stephen H ^b   Tama, Florence ^c  

^a The University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c University of Arizona   (United States)

Author keywords

Major facilitator superfamily; Membrane transporter; Steered molecular dynamics

Indexed keywords

CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CARRIER PROTEIN; MULTIDRUG RESISTANCE PROTEIN; PHOSPHOLIPID; PROTEIN EMRD; UNCLASSIFIED DRUG;

ARTICLE; CYTOPLASM; DIFFUSION; MEMBRANE TRANSPORT; MOLECULAR DYNAMICS; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TRANSPORT; SIMULATION; STANDARD;

CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; DRUG RESISTANCE, MULTIPLE; ESCHERICHIA COLI PROTEINS; LIPID BILAYERS; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR DYNAMICS SIMULATION; PERIPLASM;

ESCHERICHIA COLI;

EID: 84860631049     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24056     Document Type: Article

References (65)

1. Pao SS, Paulsen IT, Saier MH, Jr. Major facilitator superfamily. Microbiol Mol Biol R 1998; 62: 1-34.
2. Law CJ, Maloney PC, Wang DN. Ins and outs of major facilitator superfamily antiporters. Annu Rev Microbiol 2008; 62: 289-305.
3. Naroditskaya V, Schlosser MJ, Fang NY, Lewis K. An E. coli gene is involved in adaptation to low energy shock. Biochem Biophys Res Commun 1993; 196: 803-809.
4. Nishino K, Yamaguchi A. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol 2001; 183: 5803-5812.
5. Paulsen IT, Brown MH, Skurray RA. Proton-dependent multidrug efflux systems. Microbiol Rev 1996; 60: 575-608.
6. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S. Structure and mechanism of the lactose permease of Escherichia coli. Science 2003; 301: 610-615.
7. Huang Y, Lemieux MJ, Song J, Auer M, Wang DN. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 2003; 301: 616-620.
8. Yin Y, He X, Szewczyk P, Nguyen T, Chang G. Structure of the multidrug transporter EmrD from Escherichia coli. Science 2006; 312: 741-744.
9. Kaback HR, Dunten R, Frillingos S, Venkatesan P, Kwaw I, Zhang W, Ermolova N. Site-directed alkylation and the alternating access model for LacY. Proc Natl Acad Sci USA 2007; 104: 491-494.
10. Majumdar DS, Smirnova I, Kasho V, Nir E, Kong X, Weiss S, Kaback HR. Single-molecule FRET reveals sugar-induced conformational dynamics in LacY. Proc Natl Acad Sci USA 2007; 104: 12640-12645.
11. Smirnova I, Kasho V, Choe JY, Altenbach C, Hubbell WL, Kaback HR. Sugar binding induces an outward facing conformation of LacY. Proc Natl Acad Sci USA 2007; 104: 16504-16509.
12. Zhou Y, Guan L, Freites JA, Kaback HR. Opening and closing of the periplasmic gate in lactose permease. Proc Natl Acad Sci USA 2008; 105: 3774-3778.
13. Neyfakh AA. Mystery of multidrug transporters: the answer can be simple. Mol Microbiol 2002; 44: 1123-1130.
14. Lewinson O, Adler J, Sigal N, Bibi E. Promiscuity in multidrug recognition and transport: the bacterial MFS Mdr transporters. Mol Microbiol 2006; 61: 277-284.
15. Krulwich TA, Quirk PG, Guffanti AA. Uncoupler-resistant mutants of bacteria. Microbiol Rev 1990; 54: 52-65.
16. Fluman N, Bibi E. Bacterial multidrug transport through the lens of the major facilitator superfamily. Biochim Biophys Acta 2009; 1794: 738-747.
17. Higgins C. Multiple molecular mechanisms for multidrug resistance transporters. Nature 2007; 446: 749-757.
18. Bolhuis H, van Veen HW, Molenaar D, Poolman B, Driessen AJM, Konings WN. Multidrug resistances in Lactococcus lactis: evidence for ATP-dependent drug extrusion from the inner leaflet of the cytoplasmic membrane. EMBO J 1996; 15: 4239-4245.
19. Mazurkiewicz P, Konings WN, Poelarends GJ. Acidic residues in the lactococcal multidrug efflux pump LmrP play critical roles in transport of lipophilic cationic compounds. J Biol Chem 2002; 277: 26081-26088.
20. Bolhuis H, van Veen HW, Brands JR, Putman M, Poolman B, Driessen AJM, Konings WN. Energetics and mechanism of drug transport mediated by the lactococcal multidrug transporter LmrP. J Biol Chem 1996; 271: 24123-24128.
21. Mitchell BA, Paulsen IT, Brown MH, Skurray RA. Bioenergetics of the staphylococcal multidrug export protein QacA. J Biol Chem 1999; 274: 3541-3548.
22. Schumacher MA, Miller MC, Brennan RG. Structural mechanism of the simultaneous binding of two drugs to a multidrug-binding protein. EMBO J 2004; 23: 2923-2930.
23. Klyachko KA, Schuldiner S, Neyfakh AA. Mutations affecting substrate specificity of the Bacillus subtilis multidrug transporter Bmr. J Bacteriol 1997; 179: 2189-2193.
24. Zheleznova EE, Markham PN, Neyfakh AA, Brennan RG. Structural basis of multidrug recognition by BmrR, a transcription activator of a multidrug transporter. Cell 1999; 96: 353-362.
25. Murray DS, Schumacher MA, Brennan RG. Crystal structures of QacR-diamidine complexes reveal additional multidrug-binding modes and a novel mechanism of drug charge neutralization. J Biol Chem 2004; 279: 14365-14371.
26. Adler J, Bibi E. Determinants of substrate recognition by the Escherichia coli multidrug transporter MdfA identified on both sides of the membrane. J Biol Chem 2004; 279: 8957-8965.
27. Adler J, Bibi E. Promiscuity in the geometry of electrostatic interactions between the Escherichia coli multidrug resistance transporter MdfA and cationic substrates. J Biol Chem 2005; 280: 2721-2729.
28. Lewinson O, Bibi E. Evidence for simultaneous binding of dissimilar substrates by the Escherichia coli multidrug transporter MdfA. Biochemistry 2001; 40: 12612-12618.
29. Putman M, Koole LA, van Veen HW, Konings WN. The secondary multidrug transporter LmrP contains multiple drug interaction sites. Biochemistry 1999; 38: 13900-13905.
30. Borst P, Zelcer N, van de Wetering K, Poolman B. On the putative co-transport of drugs by multidrug resistance proteins. FEBS Lett 2005; 580: 1085-1093.
31. Roux B, Schulten K. Computational studies of membrane channels. Structure 2004; 12: 1343-1351.
32. Bennett M, D'Rozario R, Sansom MSP, Yeagle PL. Asymmetric stability among the transmembrane helices of lactose permease. Biochemistry 2006; 45: 8088-8095.
33. D'Rozario R, Sansom MSP. Helix dynamics in a membrane transport protein: comparative simulations of the glycerol-3-phosphate transporter and its constituent helices. Mol Membr Biol 2008; 25: 571-583.
34. Enkavi G, Tajkhorshid E. Simulation of spontaneous substrate binding revealing the binding pathway and mechanism and initial conformational response of GlpT. Biochemistry 2010; 49: 1105-1114.
35. Yin Y, Jensen M, Tajkhorshid E, Schulten K. Sugar binding and protein conformational changes in lactose permease. Biophys J 2006; 91: 3972-3985.
36. Holyoake J, Sansom MSP. Conformational change in an MFS protein: MD simulations of LacY. Structure 2007; 15: 873-884.
37. Law CJ, Almqvist J, Bernstein A, Goetz RM, Huang Y, Soudant C, Laaksonen A, Hovmöller S, Wang DN. Salt-bridge dynamics control substrate-induced conformational change in the membrane transporter GlpT. J Mol Biol 2008; 378: 828-839.
38. Law CJ, Enkavi G, Wang DN, Tajkhorshid E. Structural basis of substrate selectivity in the glycerol-3-phosphate antiporter GlpT. Biophys J 2009; 97: 1346-1353.
39. Sotomayor M, Schulten K. Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophys J 2004; 87: 3050-3065.
40. Yu J, Yool AJ, Schulten K, Tajkhorshid E. Mechanism of gating and ion conductivity of a possible tetrameric pore in aquaporin-1. Structure 2006; 14: 1411-1423.
41. Gumbart J, Schulten K. Molecular dynamics studies of the archaeal translocon. Biophys J 2006; 90: 2356-2367.
42. Jensen M, Yin Y, Tajkhorshid E, Schulten K. Sugar transport across lactose permease probed by steered molecular dynamics. Biophys J 2007; 93: 92-102.
43. Celik L, Schiott B, Tajkhorshid E. Substrate binding and formation of an occluded state in the leucine transporter. Biophys J 2008; 94: 1600-1612.
44. +-galactose transporter. Biochim Biophys Acta 2012; 1818: 263-271.
45. Shan J, Javitch JA, Shi L, Weinstein H. The substrate-driven transition to an inward-facing conformation in the functional mechanism of the dopamine transporter. PLoS ONE 2011; 6: e16350.
46. Capener CE, Shrivastava IH, Ranatunga KM, Forrest LR, Smith GR, Sansom MSP. Homology modeling and molecular dynamics simulation studies of an inward rectifier potassium channel. Biophys J 2000; 78: 2929-2942.
47. Gabrielsen M, Ravna A, Kristiansen K, Sylte I. Substrate binding and translocation of the serotonin transporter studied by docking and molecular dynamics simulations. J Mol Model 2011;doi: 10.1007/s00894-011-1133-1.
48. + antiporter. Biophys J 2009; 97: 121-131.
49. Guan L, Kaback HR. Lessons from lactose permease. Annu Rev Biophys Biomol Struct 2006; 35: 67-91.
50. Li H, Robertson AD, Jensen JH. Very fast empirical prediction and interpretation of protein pKa values. Proteins 2005; 61: 704-721.
51. Bas DC, Rogers DM, Jensen JH. Very fast prediction and rationalization of pKa values for protein-ligand complexes. Proteins 2008; 73: 765-783.
52. Olsson MHM, Søndergaard CR, Rostkowski M, Jensen JH. PROPKA3: consistent treatment of internal and surface residues in empirical pKa predictions. J Chem Theory Comput 2011; 7: 525-537.
53. Søndergaard CR, Olsson MHM, Rostkowski M, Jensen JH. Improved treatment of ligands and coupling effects in empirical calculation and rationalization of pKa values. J Chem Theory Comput 2011; 7: 2284-2295.
54. Jo S, Kim T, Im W. Automated builder and database of protein/membrane complexes for molecular dynamics simulations. PloS ONE 2007; 2: e880.
55. Dalke HW, Schulten K. VMD-visual molecular dynamics. J Mol Graph 1996; 14: 33-38.
56. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K. Scalable molecular dynamics with NAMD. J Comput Chem 2005; 26: 1781-1802.
57. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. Comparison of multiple amber force fields and development of improved protein backbone parameters. Proteins 2006; 65: 712-725.
58. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA. Development and testing of a general amber force field. J Comput Chem 2004; 25: 1157-1174.
59. Rosso L, Gould IR. Structure and dynamics of phospholipid bilayers using recently developed general all-atom force fields. J Comput Chem 2008; 29: 24-37.
60. Wang J, Wang W, Kollman PA, Case DA. Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model 2006; 25: 247-260.
61. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA, Jr, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA. Gaussian 03, Revision C.02. Wallingford, CT: Gaussian, Inc.; 2004.
62. Dupradeau FY, Cezard C, Lelong R, Stanislawiak E, Pecher J, Delepine JC, Cieplak P. R.E.DD.B.: a database for RESP and ESP atomic charges, and force field libraries. Nucleic Acids Res 2008; 36: D360-D367.
63. Pastor RW, Brooks BR, Szabo A. An analysis of the accuracy of Langevin and molecular dynamics algorithms. Mol Phys 1998; 65: 1409-1419.
64. Darden T, York D, Pedersen L. Particle mesh Ewald: an N-log(N) method for Ewald sums in large systems. J Chem Phys 1993; 98: 10089-10092.
65. Smart O, Goodfellow J, Wallace B. The pore dimensions of Gramicidin A. Biophys J 1993; 65: 2455-2460.