Multidrug transport protein NorM from Vibrio cholerae simultaneously couples to sodium- and proton-motive force

Journal of Biological Chemistry

Volumn 289, Issue 21, 2014, Pages 14624-14632

  Jin, Yoonhee ^a   Nair, Asha ^a   Van Veen, Hendrik W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EXTRUSION; PROTONS; SODIUM;

HIGH RESOLUTION CRYSTAL STRUCTURE; MECHANISTIC MODELS; PROTEOLIPOSOMES; PROTON-MOTIVE FORCES; TOXIC COMPOUNDS; TRANSPORT PROTEINS; VIBRIO CHOLERAE;

PROTEINS;

MULTIDRUG RESISTANCE PROTEIN; PROTEIN NORM; PROTEOLIPOSOME; PROTON; SODIUM ION; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL METABOLISM; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTON MOTIVE FORCE; PROTON TRANSPORT; SIGNAL TRANSDUCTION; SODIUM MOTIVE FORCE; SODIUM TRANSPORT; VIBRIO CHOLERAE;

BIOENERGETICS; ENZYME MECHANISMS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT; MULTIDRUG TRANSPORTERS;

ANTIPORTERS; ASPARTIC ACID; BACTERIAL PROTEINS; BINDING SITES; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELL MEMBRANE; DNA; ETHIDIUM; GLUTAMIC ACID; LACTOCOCCUS LACTIS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEOLIPIDS; PROTON-MOTIVE FORCE; PROTONS; SODIUM; VIBRIO CHOLERAE;

EID: 84901443477     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.546770     Document Type: Article

References (34)

1. Li, X. Z., and Nikaido, H. (2009) Efflux-mediated drug resistance in bacteria: an update. Drugs 69, 1555-1623
2. McAleese, F., Petersen, P., Ruzin, A., Dunman, P. M., Murphy, E., Projan, S. J., and Bradford, P. A. (2005) A novel MATE family efflux pump contributes to the reduced susceptibility of laboratory-derived Staphylococcus aureus mutants to tigecycline. Antimicrob. Agents Chemother. 49, 1865-1871 (Pubitemid 40631601)
3. Kaatz, G. W., and McAleese, F., and Seo, S. M. (2005) Multidrug resistance in Staphylococcus aureus due to overexpression of a novel multidrug and toxin extrusion (MATE) transport protein. Antimicrob. Agents Chemother. 49, 1857-1864 (Pubitemid 40631600)
4. Omote, H., Hiasa, M., Matsumoto, T., Otsuka, M., and Moriyama, Y. (2006) The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol. Sci. 27, 587-593 (Pubitemid 44572392)
5. Kuroda, T., and Tsuchiya, T. (2009) Multidrug efflux transporters in the MATE family. Biochim. Biophys. Acta 1794, 763-768
6. Becker, M. L., Visser, L. E., van Schaik, R. H., Hofman, A., Uitterlinden, A. G., and Stricker, B. H. (2010) Interaction between polymorphisms in the OCT1 and MATE1 transporter and metformin response. Pharmacogenet. Genomics 20, 38-44
7. Tsuda, M., Terada, T., Mizuno, T., Katsura, T., Shimakura, J., and Inui, K. (2009) Targeted disruption of the multidrug and toxin extrusion 1 (mate1) gene in mice reduces renal secretion of metformin. Mol. Pharmacol. 75, 1280-1286
8. +-organic cation antiporters. Biochem. Pharmacol. 74, 359-371 (Pubitemid 46890818)
9. Matsushima, S., Maeda, K., Inoue, K., Ohta, K. Y., Yuasa, H., Kondo, T., Nakayama, H., Horita, S., Kusuhara, H., and Sugiyama, Y. (2009) The inhibition of human multidrug and toxin extrusion 1 is involved in the drug-drug interaction caused by cimetidine. Drug Metab. Dispos. 37, 555-559
10. Nakamura, T., Yonezawa, A., Hashimoto, S., Katsura, T., and Inui, K. (2010) Disruption of multidrug and toxin extrusion MATE1 potentiates cisplatin-induced nephrotoxicity. Biochem. Pharmacol. 80, 1762-1767
11. Brown, M. H., Paulsen, I. T., and Skurray, R. A. (1999) The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol. Microbiol. 31, 394-395 (Pubitemid 29012178)
12. van Veen, H. W. (2010) Structural biology: last of the multidrug transporters. Nature 467, 926-927
13. +/multidrug antiporter in Vibrio parahaemolyticus. J. Bacteriol. 187, 1552-1558 (Pubitemid 40289355)
14. He, X., Szewczyk, P., Karyakin, A., Evin, M., Hong, W. X., Zhang, Q., and Chang, G. (2010) Structure of a cation-bound multidrug and toxic compound extrusion transporter. Nature 467, 991-994
15. +-coupled, substrate-bound MATE multidrug transporter. Proc. Natl. Acad. Sci. U.S.A. 110, 2099-2104
16. + coupled multidrug efflux pump. PLoS One 8, e59525
17. +-coupled multidrug efflux pump, PmpM, a member of the MATE family of transporters, from Pseudomonas aeruginosa. J. Bacteriol. 186, 262-265 (Pubitemid 38020311)
18. Tanaka, Y., Hipolito, C. J., Maturana, A. D., Ito, K., Kuroda, T., Higuchi, T., Katoh, T., Kato, H. E., Hattori, M., Kumazaki, K., Tsukazaki, T., Ishitani, R., Suga, H., and Nureki, O. (2013) Structural basis for the drug extrusion mechanism by a MATE multidrug transporter. Nature 496, 247-251
19. +-coupled multidrug extrusion by a MATE transporter. Nat. Struct. Mol. Biol. 20, 1310-1317
20. Vanni, S., Campomanes, P., Marcia, M., and Rothlisberger, U. (2012) Ion binding and internal hydration in the multidrug resistance secondary active transporter NorM investigated by molecular dynamics simulations. Biochemistry 51, 1281-1287
21. de Ruyter, P. G., Kuipers, O. P., Beerthuyzen, M. M., van Alen-Boerrigter, I., and de Vos, W. M. (1996) Functional analysis of promoters in the nisin gene cluster of Lactococcus lactis. J. Bacteriol. 178, 3434-3439 (Pubitemid 26179045)
22. Putman, M., van Veen, H. W., Poolman, B., and Konings, W. N. (1999) Restrictive use of detergents in the functional reconstitution of the secondary multidrug transporter LmrP. Biochemistry 38, 1002-1008
23. Venter, H., Velamakanni, S., Balakrishnan, L., and van Veen, H. W. (2008) On the energy-dependence of Hoechst 33342 transport by the ABC transporter LmrA. Biochem. Pharmacol. 75, 866-874 (Pubitemid 351174118)
24. Woebking, B., Velamakanni, S., Federici, L., Seeger, M. A., Murakami, S., and van Veen, H. W. (2008) Functional role of transmembrane helix 6 in drug binding and transport by the ABC transporter MsbA. Biochemistry 47, 10904-10914
25. Schaedler, T. A., and van Veen, H. W. (2010) A flexible cation binding site in the multidrug major facilitator superfamily transporter LmrP is associated with variable proton coupling. FASEB J. 24, 3653-3661
26. Ambudkar, S. V., Zlotnick, G. W., and Rosen, B. P. (1984) Calcium efflux from Escherichia coli: evidence for two systems. J. Biol. Chem. 259, 6142-6146 (Pubitemid 14106321)
27. Schaedler, T. A., Tong, Z., and van Veen, H. W. (2012) The multidrug transporter LmrP protein mediates selective calcium efflux. J. Biol. Chem. 287, 27682-27690
28. Venter, H., Shilling, R. A., Velamakanni, S., Balakrishnan, L., and Van Veen, H. W. (2003) An ABC transporter with a secondary-active multidrug translocator domain. Nature 426, 866-870 (Pubitemid 38056875)
29. Wang, W., and van Veen, H. W. (2012) Basic residues R260 and K357 affect the conformational dynamics of the major facilitator superfamily multidrug transporter LmrP. PLoS One 7, e38715
30. Fluman, N., Ryan, C. M., Whitelegge, J. P., and Bibi, E. (2012) Dissection of mechanistic principles of a secondary multidrug efflux protein. Mol. Cell 47, 777-787
31. Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V., Polouchine, N., Shakhova, V., Grigoriev, I., Lou, Y., Rohksar, D., Lucas, S., Huang, K., Goodstein, D. M., Hawkins, T., Plengvidhya, V., Welker, D., Hughes, J., Goh, Y., Benson, A., Baldwin, K., Lee, J. H., Díaz-Muñiz, I., Dosti, B., Smeianov, V., Wechter, W., Barabote, R., Lorca, G., Altermann, E., Barrangou, R., Ganesan, B., Xie, Y., Rawsthorne, H., Tamir, D., Parker, C., Breidt, F., Broadbent, J., Hutkins, R., O'Sullivan, D., Steele, J., Unlu, G., Saier, M., Klaenhammer, T., Richardson, P., Kozyavkin, S., Weimer, B., and Mills, D. (2006) Comparative genomics of the lactic acid bacteria. Proc. Natl. Acad. Sci. U.S.A. 103, 15611-15616 (Pubitemid 44625640)
32. Gouaux, E., and Mackinnon, R. (2005) Principles of selective ion transport in channels and pumps. Science 310, 1461-1465 (Pubitemid 41746336)
33. --dependent neurotransmitter transporters. Nature 437, 215-223 (Pubitemid 41294479)
34. +-substrate coupling in the multidrug antiporter NorM probed with a spin-labeled substrate. Biochemistry 52, 5790-5799