Crystal structure of the periplasmic region of MacB, a noncanonic ABC transporter

Biochemistry

Volumn 48, Issue 23, 2009, Pages 5218-5225

  Xu, Yongbin ^a   Sim, Se Hoon ^b   Ki, Hyun Nam ^c   Xiao, Ling Jin ^a   Kim, Hong Man ^b   Kwang, Yeon Hwang ^c   Lee, Kangseok ^b   Ha, Nam Chul ^a  

^a Pusan National University   (South Korea)

^b Chung Ang University   (South Korea)

^c Korea University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; EFFLUX PUMPS; GAIN INSIGHT; GRAM-NEGATIVE BACTERIA; HEAT-STABLE ENTEROTOXIN; MACROLIDE ANTIBIOTICS; MEMBRANE FUSION; OUTER MEMBRANE; PERIPLASMIC REGIONS; SEQUENCE ANALYSIS; STRUCTURAL MOTIFS;

ANTIBIOTICS; BACTERIA; CELL MEMBRANES; ESCHERICHIA COLI;

CRYSTAL STRUCTURE;

ABC TRANSPORTER; MACROLIDE SPECIFIC ABC TYPE EFFLUX CARRIER B PROTEIN; PERIPLASMIC PROTEIN; UNCLASSIFIED DRUG;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; ESCHERICHIA COLI; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PASTEURELLACEAE; PERIPLASM; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ESCHERICHIA COLI; LEPIDIUM MEYENII; NEGIBACTERIA;

EID: 67049159916     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900415t     Document Type: Article

References (36)

1. Lewis, K. (2000) Translocases: a bacterial tunnel for drugs and proteins. Curr. Biol. 10, R678-681.
2. Zgurskaya, H. I., and Nikaido, H. (1999) Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 96, 7190-7195.
3. Dinh, T., Paulsen, I. T., and Saier, M. H.Jr. (1994) A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J. Bacteriol. 176, 3825-3831. (Pubitemid 24191264)
4. Ma, D., Cook, D. N., Alberti, M., Pon, N. G., Nikaido, H., and Hearst, J. E. (1993) Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. J. Bacteriol. 175, 6299-6313. (Pubitemid 23292446)
5. Nikaido, H. (1994) Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264, 382-388. (Pubitemid 24178901)
6. Ma, D., Cook, D. N., Alberti, M., Pon, N. G., Nikaido, H., and Hearst, J. E. (1995) Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol. Microbiol. 16, 45-55.
7. Okusu, H., Ma, D., and Nikaido, H. (1996) AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J. Bacteriol. 178, 306-308. (Pubitemid 26006095)
8. Murakami, S., Nakashima, R., Yamashita, E., and Yamaguchi, A. (2002) Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419, 587-593.
9. Seeger, M. A., Schiefner, A., Eicher, T., Verrey, F., Diederichs, K., and Pos, K. M. (2006) Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 313, 1295-1298. (Pubitemid 44330954)
10. Murakami, S., Nakashima, R., Yamashita, E., Matsumoto, T., and Yamaguchi, A. (2006) Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443, 173-179. (Pubitemid 44387601)
11. 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. (Pubitemid 26327687)
12. Koronakis, V., Sharff, A., Koronakis, E., Luisi, B., and Hughes, C. (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405, 914-919. (Pubitemid 30435040)
13. Zgurskaya, H. I., and Nikaido, H. (1999) AcrA is a highly asymmetric protein capable of spanning the periplasm. J. Mol. Biol. 285, 409-420.
14. Zgurskaya, H. I., Yamada, Y., Tikhonova, E. B., Ge, Q., and Krishnamoorthy, G. (2009) Structural and functional diversity of bacterial membrane fusion proteins. Biochim. Biophys. Acta 1798, 794-807.
15. Kobayashi, N., Nishino, K., and Yamaguchi, A. (2001) Novel macrolide-specific ABC-type efflux transporter in Escherichia coli. J. Bacteriol. 183, 5639-5644. (Pubitemid 32898610)
16. Kobayashi, N., Nishino, K., Hirata, T., and Yamaguchi, A. (2003) Membrane topology of ABC-type macrolide antibiotic exporter MacB in Escherichia coli. FEBS Lett. 546, 241-246. (Pubitemid 36782419)
17. Rouquette-Loughlin, C. E., Balthazar, J. T., and Shafer, W. M. (2005) Characterization of the MacA-MacB efflux system in Neisseria gonorrhoeae. J. Antimicrob. Chemother. 56, 856-860.
18. Crosby, J. A., and Kachlany, S. C. (2007) TdeA, a TolC-like protein required for toxin and drug export in Aggregatibacter (Actinobacillus) actinomycetemcomitans. Gene 388, 83-92. (Pubitemid 46019845)
19. Yamanaka, H., Kobayashi, H., Takahashi, E., and Okamoto, K. (2008) MacAB Is Involved in the Secretion of Escherichia coli Heat-Stable Enterotoxin II. J. Bacteriol. 190, 7693-7698.
20. Davidson, A. L., Dassa, E., Orelle, C., and Chen, J. (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364.
21. Lin, H. T., Bavro, V. N., Barrera, N. P., Frankish, H. M., Velamakanni, S., van Veen, H. W., Robinson, C. V., Borges-Walmsley, M. I., and Walmsley, A. R. (2008) The MacB ABC transporter is a dimer whose ATPase activity and macrolide-binding capacity are regulated by the membrane fusion protein MacA. J. Biol. Chem. 284, 1145-1154.
22. Tikhonova, E. B., Devroy, V. K., Lau, S. Y., and Zgurskaya, H. I. (2007) Reconstitution of the Escherichia coli macrolide transporter: the periplasmic membrane fusion protein MacA stimulates the ATPase activity of MacB. Mol. Microbiol. 63, 895-910.
23. Yum, S., Xu, Y., Piao, S., Sim, S. H., Kim, H. M., Jo, W. S., Kim, K. J., Kweon, H. S., Jeong, M. H., Jeon, H., Lee, K., and Ha, N. C. (2009) Crystal structure of the periplasmic component of a tripartite macrolide-specific efflux pump. J. Mol. Biol. 387, 1286-1297.
24. Otwinosky, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326. (Pubitemid 27085611)
25. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55, 849-861.
26. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.
27. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921.
28. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 58, 1948-1954.
29. DeLano, W. (2002) The PyMOL User's Manual , DeLano Scientific, Palo Alto.
30. Kim, S., Yum, S., Jo, W. S., Lee, B. L., Jeong, M. H., and Ha, N. C. (2008) Expression and biochemical characterization of the periplasmic domain of bacterial outer membrane porin TdeA. J. Microbiol. Biotechnol. 18, 845-851.
31. Piao, S., Xu, Y., and Ha, N. C. (2008) Crystallization and preliminary X-ray crystallographic analysis of MacA from Actinobacillus actinomycetemcomitans. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64, 391-393.
32. Holm, L., and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
33. Tamura, N., Murakami, S., Oyama, Y., Ishiguro, M., and Yamaguchi, A. (2005) Direct interaction of multidrug efflux transporter AcrB and outer membrane channel TolC detected via site-directed disulfide cross-linking. Biochemistry 44, 11115-11121. (Pubitemid 41209047)
34. Hollenstein, K., Frei, D. C., and Locher, K. P. (2007) Structure of an ABC transporter in complex with its binding protein. Nature 446, 213-216. (Pubitemid 46398672)
35. Ward, A., Reyes, C. L., Yu, J., Roth, C. B., and Chang, G. (2007) Flexibility in the ABC transporter MsbA: Alternating access with a twist. Proc. Natl. Acad. Sci. U. S. A. 104, 19005-19010.
36. Bavro, V. N., Pietras, Z., Furnham, N., Perez-Cano, L., Fernandez-Recio, J., Pei, X. Y., Misra, R., and Luisi, B. (2008) Assembly and channel opening in a bacterial drug efflux machine. Mol. Cell 30, 114-121.