Threonine-978 in the transmembrane segment of the multidrug efflux pump AcrB of Escherichia coli is crucial for drug transport as a probable component of the proton relay network

Journal of Bacteriology

Volumn 188, Issue 20, 2006, Pages 7284-7289

  Takatsuka, Yumiko ^a   Nikaido, Hiroshi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTIPORTER; ARGININE; ASPARTIC ACID; BACTERIAL PROTEIN; LYSINE; MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN ACRB; THREONINE; TOXIC SUBSTANCE; UNCLASSIFIED DRUG;

ALANINE SCANNING MUTAGENESIS; AMINO ACID SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; DRUG TRANSPORT; ESCHERICHIA COLI; HYDROGEN BOND; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTON TRANSPORT;

AMINO ACID SUBSTITUTION; ANTIPORTERS; CONSERVED SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROGEN BONDING; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTONS; THREONINE;

ESCHERICHIA COLI;

EID: 33749630424     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00683-06     Document Type: Article

References (32)

1. Abramson, J., I. Smirnova, V. Kasho, G. Verner, H. R. Kaback, and S. Iwata. 2003. Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610-615.
2. Bryson, V., and W. Szybalzski. 1952. Microbial selection. Science 116:45-51.
3. Elkins, C. A., and H. Nikaido. 2002. Substrate specificity of the RND-type multidrug efflux pumps AcrB and AcrD of Escherichia coli is determined predominately by two large periplasmic loops. J. Bacteriol. 184:6490-6498.
4. Fralick, J. A. 1996. Evidence that TolC is required for functioning of the Mar/AcrAB efflux pump of Escherichia coli. J. Bacteriol. 178:5803-5805.
5. Frillingos, S., M. Sahin-Tóth, J. Wu, and H. R. Kaback. 1998. Cys-scanning mutagenesis: a novel approach to structure-function relationships in polytopic membrane proteins. FASEB J. 12:1281-1299.
6. Goldberg, M., T. Pribyl, S. Juhnke, and D. H. Nies. 1999. Energetics and topology of CzcA, a cation/proton antiporter of the resistance-Nodulation-cell division protein family. J. Biol. Chem. 274:26065-26070.
7. Guan, L., and T. Nakae. 2001. Identification of essential charged residues in transmembrane segments of the multidrug transporter MexB of Pseudomonas aeruginosa. J. Bacteriol. 183:1734-1739.
8. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
9. Koronakis, V., A. Sharff, E. Koronakis, B. Luisi, and C. Hughes. 2000. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914-919.
10. Ma, D., D. A. Cook, M. Alberti, N. G. Pen, H. Nikaido, and J. E. Hearst. 1993. Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. J. Bacteriol. 175:6299-6313.
11. Ma, D., D. A. Cook, M. Alberti, N. G. Pon, H. Nikaido, and J. E. Hearst. 1995. Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol. Microbiol. 16:45-55.
12. Murakami, S., R. Nakashima, E. Yamashita, and A. Yamaguchi. 2002. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419:587-593.
13. Murakami, S., and A. Yamaguchi. 2003. Multidrug-exporting secondary transporters. Curr. Opin. Struct. Biol. 13:443-452.
14. Nikaido, H. 1998. Antibiotic resistance caused by gram-negative multidrug efflux pumps. Clin. Infect. Dis. 27(Suppl. 1):S32-S41.
15. Nishino, K., and A. Yamaguchi. 2001. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J. Bacteriol. 183:5803-5812.
16. Paulsen, I. T., M. H. Brown, and R. A. Skurray. 1996. Proton-dependent multidrug efflux systems. Microbiol. Rev. 60:575-608.
17. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
18. Shukla, S., S. V. Ambudkar, and R. Prasad. 2004. Substitution of threonine-1351 in the multidrug transporter Cdr1p of Candida albicans results in hypersusceptibility to antifungal agents and threonine-1351 is essential for synergic effects of calcineurin inhibitor FK520. J. Antimicrob. Chemother. 54:38-45.
19. Soskine, M., Y. Adam, and S. Schuldiner. 2004. Direct evidence for substrate-induced proton release in detergent-solubilized EmrE, a multidrug transporter. J. Biol. Chem. 279:9951-9955.
20. Stewart, C., J. Bailey, and C. Manoil. 1998. Mutant membrane protein toxicity. J. Biol. Chem. 273:28078-28084.
21. Su, C.-C., M. Li, R. Gu, Y. Takatsuka, G. McDermott, H. Nikaido, and E. W. Yu. 2006. Conformation of the AcrB multidrug efflux pump in mutants of the putative proton relay pathway. J. Bacteriol. 188:7290-7296.
22. Sulavik, M. C., C. Houseweart, C. Cramer, N. Jiwani, N. Murgolo, J. Greene, B. DiDomenico, K. J. Shaw, G. H. Miller, R. Hare, and G. Shimer. 2001. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob. Agents Chemother. 45:1126-1136.
23. Tate, C. G., I. Ubarretxena-Belandia, and J. M. Baldwin. 2003. Conformational changes in the multidrug transporter EmrE associated with substrate binding. J. Mol. Biol. 332:229-242.
24. Tikhonova, E. B., and H. I. Zgurskaya. 2004. AcrA, AcrB, and TolC of Escherichia coli form a stable intermembrane multidrug efflux complex. J. Biol. Chem. 279:32116-32124.
25. Touzé, T., J. Eswaran, E. Bokma, E. Koronakis, C. Hughes, and V. Koronakis. 2004. Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Mol. Microbiol. 53:697-706.
26. Tseng, T. T., K. S. Gratwick, J. Kollman, D. Park, D. H. Nies, A. Goffeau, and M. H. Saier, Jr. 1999. The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J. Mol. Microbiol. Biotechnol. 1:107-125.
27. Venter, H., R. A. Shilling, S. Velamakanni, L. Balakrishnan, and H. W. Veen. 2003. An ABC transporter with a secondary-active multidrug translocator domain. Nature 426:866-870.
28. + and substrate fluxes based on "time-sharing" of a common binding site. Biochemistry 39:14711-14719.
29. Yu, E. W., J. R. Aires, G. McDermott, and H. Nikaido. 2005. A periplasmic drug-binding site of the AcrB multidrug efflux pump: a crystallographic and site-directed mutagenesis study. J. Bacteriol. 187:6804-6815.
30. Zgurskaya, H. I., and H. Nikaido. 1999. AcrA is a highly asymmetric protein capable of spanning the periplasm. J. Mol. Biol. 285:409-420.
31. Zgurskaya, H. I., and H. Nikaido. 1999. Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proc. Natl. Acad. Sci. USA 96:7190-7195.
32. Zgurskaya, H. I., and H. Nikaido. 2000. Cross-linked complex between oligomeric periplasmic lipoprotein AcrA and the inner-membrane-associated multidrug efflux pump AcrB from Escherichia coli. J. Bacteriol. 182:4264-4267.