An allosteric transport mechanism for the AcrAB-TolC multidrug efflux pump

eLife

Volumn 6, Issue , 2017, Pages

  Wang, Zhao ^a   Fan, Guizhen ^b   Hryc, Corey F ^a   Blaza, James N ^c   Serysheva, Irina I ^b   Schmid, Michael F ^a   Chiu, Wah ^a   Luisi, Ben F ^d   Du, Dijun ^d  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AEROBIC RESPIRATION CONTROL PROTEIN A; MEMBRANE FUSION PROTEIN; PUROMYCIN; TOLC PROTEIN; ACRAB-TOLC PROTEIN, E COLI; ANTIINFECTIVE AGENT; CARRIER PROTEIN; ESCHERICHIA COLI PROTEIN;

ARTICLE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DRUG TRANSPORT; ENZYME ACTIVITY; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; IMAGE PROCESSING; IMAGE QUALITY; LIGAND BINDING; MOLECULAR DOCKING; MULTIDRUG RESISTANCE; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEOMICS; ALLOSTERISM; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; METABOLISM; PROTEIN CONFORMATION;

ALLOSTERIC REGULATION; ANTI-BACTERIAL AGENTS; CARRIER PROTEINS; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; PROTEIN CONFORMATION;

EID: 85018306842     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.24905     Document Type: Article

References (60)

1. Andersen C, Koronakis E, Bokma E, Eswaran J, Humphreys D, Hughes C, Koronakis V. 2002. Transition to the open state of the TolC periplasmic tunnel entrance. PNAS 99:11103–11108. doi: 10.1073/pnas.162039399, PMID: 12163644
2. Augustus AM, Celaya T, Husain F, Humbard M, Misra R. 2004. Antibiotic-sensitive TolC mutants and their suppressors. Journal of Bacteriology 186:1851–1860. doi: 10.1128/JB.186.6.1851-1860.2004, PMID: 14996816
3. Bai XC, Rajendra E, Yang G, Shi Y, Scheres SH. 2015. Sampling the conformational space of the catalytic subunit of human g-secretase. eLife 4:e11182. doi: 10.7554/eLife.11182, PMID: 26623517
4. Baker MR, Fan G, Serysheva II. 2015. Single-particle cryo-EM of the ryanodine receptor channel in an aqueous environment. European Journal of Translational Myology 25:35–48. doi: 10.4081/ejtm.2015.4803, PMID: 25 844145
5. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG. 2011. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallographica Section D Biological Crystallography 67: 271–281. doi: 10.1107/S0907444910048675, PMID: 21460445
6. Bavro VN, Pietras Z, Furnham N, Pérez-Cano L, Fernández-Recio J, Pei XY, Misra R, Luisi B. 2008. Assembly and channel opening in a bacterial drug efflux machine. Molecular Cell 30:114–121. doi: 10.1016/j.molcel.2008.02. 015, PMID: 18406332
7. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D Biological Crystallography 66:12–21. doi: 10.1107/S0907444909042073, PMID: 20057044
8. Daury L, Orange F, Taveau JC, Verchère A, Monlezun L, Gounou C, Marreddy RK, Picard M, Broutin I, Pos KM, Lambert O. 2016. Tripartite assembly of RND multidrug efflux pumps. Nature Communications 7:10731. doi: 10.1038/ncomms10731, PMID: 26867482
9. Du D, van Veen HW, Luisi BF. 2015b. Assembly and operation of bacterial tripartite multidrug efflux pumps. Trends in Microbiology 23:311–319. doi: 10.1016/j.tim.2015.01.010, PMID: 25728476
10. Du D, van Veen HW, Murakami S, Pos KM, Luisi BF. 2015a. Structure, mechanism and cooperation of bacterial multidrug transporters. Current Opinion in Structural Biology 33:76–91. doi: 10.1016/j.sbi.2015.07.015, PMID: 26282926
11. Du D, Wang Z, James NR, Voss JE, Klimont E, Ohene-Agyei T, Venter H, Chiu W, Luisi BF. 2014. Structure of the AcrAB-TolC multidrug efflux pump. Nature 509:512–515. doi: 10.1038/nature13205, PMID: 24747401
12. Eicher T, Cha HJ, Seeger MA, Brandstätter L, El-Delik J, Bohnert JA, Kern WV, Verrey F, Grütter MG, Diederichs K, Pos KM. 2012. Transport of drugs by the multidrug transporter AcrB involves an access and a deep binding pocket that are separated by a switch-loop. PNAS 109:5687–5692. doi: 10.1073/pnas.1114944109, PMID: 22451937
13. Eicher T, Seeger MA, Anselmi C, Zhou W, Brandstätter L, Verrey F, Diederichs K, Faraldo-Gómez JD, Pos KM. 2014. Coupling of remote alternating-access transport mechanisms for protons and substrates in the multidrug efflux pump AcrB. eLife 3:e03145. doi: 10.7554/eLife.03145, PMID: 25248080
14. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of coot. Acta Crystallographica Section D Biological Crystallography 66:486–501. doi: 10.1107/S0907444910007493, PMID: 20383002
15. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallographica Section D Biological Crystallography 62:72–82. doi: 10.1107/S0907444905036693, PMID: 16369096
16. Federici L, Du D, Walas F, Matsumura H, Fernandez-Recio J, McKeegan KS, Borges-Walmsley MI, Luisi BF, Walmsley AR. 2005. The crystal structure of the outer membrane protein VceC from the bacterial pathogen Vibrio cholerae at 1.8 A resolution. Journal of Biological Chemistry 280:15307–15314. doi: 10.1074/jbc. M500401200, PMID: 15684414
17. Fischer N, Kandt C. 2013. Porter domain opening and closing motions in the multi-drug efflux transporter AcrB. Biochimica Et Biophysica Acta (BBA) - Biomembranes 1828:632–641. doi: 10.1016/j.bbamem.2012.10.016, PMID: 23088914
18. Harley KT, Saier MH. 2000. A novel ubiquitous family of putative efflux transporters. Journal of Molecular Microbiology and Biotechnology 2:195–198. PMID: 10939244
19. Henderson R, Sali A, Baker ML, Carragher B, Devkota B, Downing KH, Egelman EH, Feng Z, Frank J, Grigorieff N, Jiang W, Ludtke SJ, Medalia O, Penczek PA, Rosenthal PB, Rossmann MG, Schmid MF, Schröder GF, Steven AC, Stokes DL, et al. 2012. Outcome of the first Electron microscopy validation task force meeting. Structure 20:205–214. doi: 10.1016/j.str.2011.12.014, PMID: 22325770
20. Hobbs EC, Yin X, Paul BJ, Astarita JL, Storz G. 2012. Conserved small protein associates with the multidrug efflux pump AcrB and differentially affects antibiotic resistance. PNAS 109:16696–16701. doi: 10.1073/pnas. 1210093109, PMID: 23010927
21. Jeong H, Kim JS, Song S, Shigematsu H, Yokoyama T, Hyun J, Ha NC. 2016. Pseudoatomic structure of the Tripartite Multidrug Efflux pump AcrAB-TolC reveals the intermeshing Cogwheel-like interaction between AcrA and TolC. Structure 24:272–276. doi: 10.1016/j.str.2015.12.007, PMID: 26777412
22. Kim JS, Jeong H, Song S, Kim HY, Lee K, Hyun J, Ha NC. 2015. Structure of the tripartite multidrug efflux pump AcrAB-TolC suggests an alternative assembly mode. Molecules and Cells 38:180–186. doi: 10.14348/molcells.2015.2277, PMID: 26013259
23. Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C. 2000. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914–919. doi: 10.1038/35016007, PMID: 1087 9525
24. Kucukelbir A, Sigworth FJ, Tagare HD. 2014. Quantifying the local resolution of cryo-EM density maps. Nature Methods 11:63–65. doi: 10.1038/nmeth.2727, PMID: 24213166
25. Lee M, Jun SY, Yoon BY, Song S, Lee K, Ha NC. 2012. Membrane fusion proteins of type I secretion system and tripartite efflux pumps share a binding motif for TolC in gram-negative bacteria. PLoS One 7:e40460. doi: 10. 1371/journal.pone.0040460, PMID: 22792337
26. Li X, Mooney P, Zheng S, Booth CR, Braunfeld MB, Gubbens S, Agard DA, Cheng Y. 2013. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nature Methods 10:584–590. doi: 10.1038/nmeth.2472, PMID: 23644547
27. Liao M, Cao E, Julius D, Cheng Y. 2013. Structure of the TRPV1 ion channel determined by Electron cryomicroscopy. Nature 504:107–112. doi: 10.1038/nature12822, PMID: 24305160
28. Mikolosko J, Bobyk K, Zgurskaya HI, Ghosh P. 2006. Conformational flexibility in the multidrug efflux system protein AcrA. Structure 14:577–587. doi: 10.1016/j.str.2005.11.015, PMID: 16531241
29. Mindell JA, Grigorieff N. 2003. Accurate determination of local defocus and specimen tilt in Electron microscopy. Journal of Structural Biology 142:334–347. doi: 10.1016/S1047-8477(03)00069-8, PMID: 12781660
30. Murakami S, Nakashima R, Yamashita E, Matsumoto T, Yamaguchi A. 2006. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443:173–179. doi: 10.1038/nature05076, PMID: 16 915237
31. Murakami S, Nakashima R, Yamashita E, Yamaguchi A. 2002. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419:587–593. doi: 10.1038/nature01050, PMID: 12374972
32. Murshudov GN, Vagin AA, Lebedev A, Wilson KS, Dodson EJ. 1999. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallographica Section D Biological Crystallography 55:247–255. doi: 10.1107/S090744499801405X, PMID: 10089417
33. Müller RT, Pos KM. 2015. The assembly and disassembly of the AcrAB-TolC three-component multidrug efflux pump. Biological Chemistry 396:1083–1089. doi: 10.1515/hsz-2015-0150, PMID: 26061621
34. Nakashima R, Sakurai K, Yamasaki S, Nishino K, Yamaguchi A. 2011. Structures of the multidrug exporter AcrB reveal a proximal multisite drug-binding pocket. Nature 480:565. doi: 10.1038/nature10641, PMID: 22121023
35. Ntreh AT, Weeks JW, Nickels LM, Zgurskaya HI. 2016. Opening the Channel: the two functional interfaces of Pseudomonas aeruginosa OpmH with the Triclosan Efflux pump TriABC. Journal of Bacteriology 198:3176– 3185. doi: 10.1128/JB.00535-16, PMID: 27645384
36. Opperman TJ, Nguyen ST. 2015. Recent advances toward a molecular mechanism of efflux pump inhibition. Frontiers in Microbiology 6:421. doi: 10.3389/fmicb.2015.00421, PMID: 25999939
37. Ovchinnikov S, Kamisetty H, Baker D. 2014. Robust and accurate prediction of residue-residue interactions across protein interfaces using evolutionary information. eLife 3:e02030. doi: 10.7554/eLife.02030, PMID: 24 842992
38. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera–a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25:1605–1612. doi: 10.1002/jcc.20084, PMID: 15264254
39. Popot JL. 2010. Amphipols, nanodiscs, and fluorinated surfactants: three nonconventional approaches to studying membrane proteins in aqueous solutions. Annual Review of Biochemistry 79:737–775. doi: 10.1146/annurev.biochem.052208.114057, PMID: 20307193
40. Pu Y, Zhao Z, Li Y, Zou J, Ma Q, Zhao Y, Ke Y, Zhu Y, Chen H, Baker MA, Ge H, Sun Y, Xie XS, Bai F. 2016. Enhanced Efflux Activity facilitates drug tolerance in dormant bacterial cells. Molecular Cell 62:284–294. doi: 10.1016/j.molcel.2016.03.035, PMID: 27105118
41. Rohou A, Grigorieff N. 2015. CTFFIND4: fast and accurate defocus estimation from Electron micrographs. Journal of Structural Biology 192:216–221. doi: 10.1016/j.jsb.2015.08.008, PMID: 26278980
42. Rosenthal PB, Henderson R. 2003. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle Electron cryomicroscopy. Journal of Molecular Biology 333:721–745. doi: 10.1016/j.jmb. 2003.07.013, PMID: 14568533
43. Scheres SH. 2012. RELION: implementation of a bayesian approach to cryo-EM structure determination. Journal of Structural Biology 180:519–530. doi: 10.1016/j.jsb.2012.09.006, PMID: 23000701
44. Scheres SH. 2016. Processing of structurally Heterogeneous Cryo-EM Data in RELION. Methods in Enzymology 579:125–157. doi: 10.1016/bs.mie.2016.04.012, PMID: 27572726
45. Seeger MA, Schiefner A, Eicher T, Verrey F, Diederichs K, Pos KM. 2006. Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science. 313:1295–1298. doi: 10.1126/science.1131542, PMID: 16 946072
46. Sjuts H, Vargiu AV, Kwasny SM, Nguyen ST, Kim HS, Ding X, Ornik AR, Ruggerone P, Bowlin TL, Nikaido H, Pos KM, Opperman TJ. 2016. Molecular basis for inhibition of AcrB multidrug efflux pump by novel and powerful pyranopyridine derivatives. PNAS 113:3509–3514. doi: 10.1073/pnas.1602472113, PMID: 26976576
47. Song S, Hwang S, Lee S, Ha NC, Lee K. 2014. Interaction mediated by the putative tip regions of MdsA and MdsC in the formation of a Salmonella-specific tripartite efflux pump. PLoS One 9:e100881. doi: 10.1371/journal.pone.0100881, PMID: 24960027
48. Su CC, Long F, Zimmermann MT, Rajashankar KR, Jernigan RL, Yu EW. 2011. Crystal structure of the CusBA heavy-metal efflux complex of Escherichia coli. Nature 470:558–562. doi: 10.1038/nature09743, PMID: 213504 90
49. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ. 2007. EMAN2: an extensible image processing suite for Electron microscopy. Journal of Structural Biology 157:38–46. doi: 10.1016/j.jsb.2006.05. 009, PMID: 16859925
50. Tribet C, Audebert R, Popot JL. 1996. Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. PNAS 93:15047–15050. doi: 10.1073/pnas.93.26.15047, PMID: 8986761
51. Wang Z, Hryc CF, Bammes B, Afonine PV, Jakana J, Chen DH, Liu X, Baker ML, Kao C, Ludtke SJ, Schmid MF, Adams PD, Chiu W. 2014. An atomic model of brome mosaic virus using direct Electron detection and realspace optimization. Nature Communications 5:4808. doi: 10.1038/ncomms5808, PMID: 25185801
52. Weeks JW, Bavro VN, Misra R. 2014. Genetic assessment of the role of AcrB b-hairpins in the assembly of the TolC-AcrAB multidrug efflux pump of Escherichia coli. Molecular Microbiology 91:965–975. doi: 10.1111/mmi. 12508, PMID: 24386963
53. Xu Y, Lee M, Moeller A, Song S, Yoon BY, Kim HM, Jun SY, Lee K, Ha NC. 2011. Funnel-like hexameric assembly of the periplasmic adapter protein in the tripartite multidrug efflux pump in gram-negative bacteria. Journal of Biological Chemistry 286:17910–17920. doi: 10.1074/jbc.M111.238535, PMID: 21454662
54. Xu Y, Sim SH, Song S, Piao S, Kim HM, Jin XL, Lee K, Ha NC. 2010. The tip region of the MacA alpha-hairpin is important for the binding to TolC to the Escherichia coli MacAB-TolC pump. Biochemical and Biophysical Research Communications 394:962–965. doi: 10.1016/j.bbrc.2010.03.097, PMID: 20307498
55. Yum S, Xu Y, Piao S, Sim SH, Kim HM, Jo WS, Kim KJ, Kweon HS, Jeong MH, Jeon H, Lee K, Ha NC. 2009. Crystal structure of the periplasmic component of a tripartite macrolide-specific efflux pump. Journal of Molecular Biology 387:1286–1297. doi: 10.1016/j.jmb.2009.02.048, PMID: 19254725
56. Zgurskaya HI, Nikaido H. 1999. Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. PNAS 96:7190–7195. doi: 10.1073/pnas.96.13.7190, PMID: 10377390
57. Zgurskaya HI, Weeks JW, Ntreh AT, Nickels LM, Wolloscheck D. 2015. Mechanism of coupling drug transport reactions located in two different membranes. Frontiers in Microbiology 6:100. doi: 10.3389/fmicb.2015.00100, PMID: 25759685
58. Zhang K. 2016. Gctf: real-time CTF determination and correction. Journal of Structural Biology 193:1–12. doi: 10.1016/j.jsb.2015.11.003, PMID: 26592709
59. Zheng SQ, Palovcak E, Armache JP, Agard D, Cheng Y. 2016. Anisotropic correction of beam-induced motion for improved single-particle Electron cryo-microscopy. Nature Methods. doi: 10.1101/061960
60. Zoonens M, Popot JL. 2014. Amphipols for each season. The Journal of Membrane Biology 247:759–796. doi: 10.1007/s00232-014-9666-8, PMID: 24969706