The AcrB efflux pump: Conformational cycling and peristalsis lead to multidrug resistance

Current Drug Targets

Volumn 9, Issue 9, 2008, Pages 729-749

  Seeger, Markus A ^a,b,c   Diederichs, Kay ^d   Eicher, Thomas ^a   Brandstätter, Lorenz ^a   Schiefner, André ^d,e,f   Verrey, François ^a   Pos, Klaas M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF KONSTANZ   (Germany)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f GOETHE UNIVERSITY   (Germany)

Author keywords

AcrB Efflux Pump; Antibiotics; Antimicrobial resistance; Asymmetric structure; Conformational; Detergents; Gram negative bacteria; Human pathogenic bacteria; The periplasmic membrane fusion protein (MFP); Trimeric outer membrane factor (OMF)

Indexed keywords

ACRIFLAVINE; ACRIFLAVINE RESISTANCE PROTEIN A; ACRIFLAVINE RESISTANCE PROTEIN B; ANTIBIOTIC AGENT; BERBERINE; BETA LACTAM ANTIBIOTIC; CARRIER PROTEIN; CIPROFLOXACIN; DOXORUBICIN; ERYTHROMYCIN; ETHIDIUM; MACROLIDE; MEMBRANE FUSION PROTEIN; MEMBRANE PROTEIN; MINOCYCLINE; OUTER MEMBRANE PROTEIN; OXACILLIN; OXAZOLIDINONE DERIVATIVE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RESISTANCE NODULATION DIVISION PROTEIN; TAUROCHOLIC ACID; TETRACYCLINE DERIVATIVE; TOLC PROTEIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; BACTERIAL METABOLISM; BACTERIAL OUTER MEMBRANE; COMPLEX FORMATION; COMPUTER ANALYSIS; CONFORMATIONAL TRANSITION; CYTOPLASM; DRUG PROTEIN BINDING; DRUG STRUCTURE; DRUG TRANSPORT; ENERGY TRANSFER; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; HYDROPHOBICITY; MEMBRANE TRANSPORT; MOLECULAR RECOGNITION; MULTIDRUG RESISTANCE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; PROTON MOTIVE FORCE; PSEUDOMONAS AERUGINOSA; PUBLIC HEALTH; REVIEW; STOICHIOMETRY;

ANTI-BACTERIAL AGENTS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN KINASES; PROTON-TRANSLOCATING ATPASES;

EID: 52449109122     PISSN: 13894501     EISSN: None     Source Type: Journal    
DOI: 10.2174/138945008785747789     Document Type: Review

References (106)

1. Saier, M. H., Jr. (2000) Microbiol. Mol. Biol. Rev., 64, 354-411.
2. Saier, M. H., Jr. and Paulsen, I. T. (2001) Semin. Cell Dev. Biol., 12, 205-13.
3. Bolhuis, H.; van Veen, H. W.; Molenaar, D.; Poolman, B.; Driessen, A. J. and Konings, W. N. (1996) EMBO J., 15, 4239-45.
4. Dawson, R. J. and Locher, K. P. (2006) Nature, 443, 180-5.
5. Edgar, R. and Bibi, E. (1997) J. Bacteriol., 179, 2274-80.
6. Yin, Y.; He, X.; Szewczyk, P.; Nguyen, T. and Chang, G. (2006) Science, 312, 741-4.
7. Abramson, J.; Smirnova, I.; Kasho, V.; Verner, G.; Kaback, H. R. and Iwata, S. (2003) Science, 301, 610-5.
8. Huang,, Y.; Lemieux, M. J.; Song, J.; Auer, M. and Wang, D. N. (2003) Science, 301, 616-20.
9. Schuldiner, S.; Granot, D.; Mordoch, S. S.; Ninio, S.; Rotem, D.; Soskin, M.; Tate, C. G. and Yerushalmi, H. (2001) News Physiol. Sci., 16, 130-4.
10. Tate, C. G.; Ubarretxena-Belandia, I. and Baldwin, J. M. (2003) J. Mol. Biol., 332, 229-42.
11. Otsuka, M.; Yasuda, M.; Morita, Y.; Otsuka, C.; Tsuchiya, T.; Omote, H. and Moriyama, Y. (2005) J. Bacteriol., 187, 1552-8.
12. Goldberg, M.; Pribyl, T.; Juhnke, S. and Nies, D. H. (1999) J. Biol. Chem., 274, 26065-70.
13. Murakami, S. and Yamaguchi, A. (2003) Curr. Opin. Struct. Biol., 13, 443-52.
14. Poole, K. (2001) J. Mol. Microbiol. Biotechnol., 3, 255-64.
15. Ohgami, N.; Ko, D. C.; Thomas, M.; Scott, M. P.; Chang, C. C. and Chang, T. Y. (2004) Proc. Natl. Acad. Sci. USA, 101, 12473-8.
16. Fralick, J. A. (1996) J. Bacteriol., 178, 5803-5.
17. Hirakawa, H.; Nishino, K.; Yamada, J.; Hirata, T. and Yamaguchi, A. (2003) J. Antimicrob. Chemother., 52, 576-82.
18. Sulavik, M. C.; Houseweart, C.; Cramer, C.; Jiwani, N.; Murgolo, N.; Greene, J.; DiDomenico, B.; Shaw, K. J.; Miller, G. H.; Hare, R. and Shimer, G. (2001) Antimicrob. Agents Chemother., 45, 1126-36.
19. Kobayashi, N.; Nishino, K. and Yamaguchi, A. (2001) J. Bacteriol., 183, 5639-44.
20. Nakamura, H. (1965) J. Bacteriol., 90, 8-14.
21. Ma, D.; Cook, D. N.; Alberti, M.; Pon, N. G.; Nikaido, H. and Hearst, J. E. (1993) J. Bacteriol., 175, 6299-313.
22. Elkins, C. A.and Nikaido, H. (2003) J. Bacteriol., 185, 5349-56.
23. Baranova, N. and Nikaido, H. (2002) J. Bacteriol., 184, 4168-76.
24. Nagakubo, S.; Nishino, K.; Hirata, T. and Yamaguchi, A. (2002) J. Bacteriol., 184, 4161-7.
25. Kobayashi, K.; Tsukagoshi, N. and Aono, R. (2001) J. Bacteriol., 183, 2646-53.
26. Doole, K.; Krebes, K.; McNally, C. and Neshat, S. (1993) J. Bacteriol., 175, 7363-72.
27. Poole, K. (2004) Clin. Microbiol. Infect., 10, 12-26.
28. Nikaido, H. (1996) J. Bacteriol., 178, 5853-9.
29. Nikaido, H.; Basina, M.; Nguyen, V. and Rosenberg, E. Y. (1998) J. Bacteriol, 180, 4686-92.
30. Li, X. Z.; Zhang, L. and Poole, K. (1998) J. Bacteriol., 180, 2987-91.
31. Thanassi, D. G.; Cheng, L. W. and Nikaido, H. (1997) J. Bacteriol., 179, 2512-8.
32. Kawamura-Sato, K.; Shibayama, K.; Horii, T.; Iimuma, Y.; Arakawa, Y. and Ohta, M. (1999) FEMS Microbiol. Lett., 179, 345-52.
33. Lau, S. Y. and Zgurskaya, H. I. (2005) J. Bacteriol., 187, 7815-25.
34. Rahmati, S.;. Yang, S.; Davidson, A. L. and Zechiedrich, E. L. (2002) Mol. Microbiol., 43, 677-85.
35. Lomovskaya, O.; Warren, M. S.; Lee, A.; Galazzo, J.; Fronko, R.; Lee, M.; Blais, J.; Cho, D.; Chamberland, S.; Renau, T.; Leger, R.; Hecker, S.; Watkins, W.; Hoshino, K.; Ishida, H. and Lee, V. J. (2001) Antimicrob. Agents Chemother., 45, 105-16.
36. Bohnert, J. A. and Kern, W. V. (2005) Antimicrob. Agents Chemother., 49, 849-52.
37. Levy, S. B. and McMurry, L. (1978) Nature, 276, 90-2.
38. de Cristobal, R. E.; Vincent, P. A. and Salomon, R. A. (2006) J. Antimicrob. Chemother., 58, 31-6.
39. Piddock, L. J. (2006) Nat. Rev. Microbiol., 4, 629-36.
40. Piddock, L. J. (2006) Clin. Microbiol. Rev., 19, 382-402.
41. Poole, K. (2000) Antimicrob. Agents Chemother., 44, 2595-9.
42. Grkovic, S.; Brown, M. H. and Skurray, R. A. (2002) Microbiol. Mol. Biol. Rev., 66, 671-701, table of contents.
43. Nagel de Zwaig, R. and Luria, S. E. (1967) J. Bacteriol., 94, 1112-23.
44. Zakharov, S. D.; Eroukova, V. Y.; Rokitskaya, T. I.; Zhalnina, M. V.; Sharma, O.; Loll, P. J.; Zgurskaya, H. I.; Antonenko, Y. N. and Cramer, W. A. (2004) Biophys. J., 87, 3901-11.
45. Thanabalu, T.; Koronakis, E.; Hughes, C. and Koronakis, V. (1998) EMBO J., 17, 6487-96.
46. Koronakis, V.; Sharff, A.; Koronakis, E.; Luisi, B. and Hughes, C. (2000) Nature, 405, 914-9.
47. Akama, H.; Matsuura, T.; Kashiwagi, S.; Yoneyama, H.; Narita, S.; Tsukihara, T.; Nakagawa, A. and Nakae, T. (2004) J. Biol. Chem., 279, 25939-42.
48. Federici, L.; Du, D.; Walas, F.; Matsumura, H.; Fernandez-Recio, J.; McKeegan, K. S.; Borges-Walmsley, M. I.; Luisi, B. F. and Walmsley, A. R. (2005) J. Biol. Chem., 280, 15307-14.
49. Andersen, C.; Koronakis, E.; Bokma, E.; Eswaran, J.; Humphreys, D.; Hughes, C. and Koronakis, V. (2002) Proc. Natl. Acad. Sci. USA, 99, 11103-8.
50. Eswaran, J.; Hughes, C. and Koronakis, V. (2003) J. Mol. Biol., 327, 309-15.
51. Augustus, A. M.; Celaya, T.; Husain, F.; Humbard, M. and Misra, R. (2004) J. Bacteriol., 186, 1851-60.
52. Dinh, T.; Paulsen, I. T.; Saier, M. H., Jr. (1994) J. Bacteriol, 176, 3825-31.
53. Tikhonova, E. B.; Devroy, V. K.; Lau, S. Y. and Zgurskaya, H. I. (2007) Mol. Microbiol., 63, 895-910.
54. Higgins, M. K.; Bokma, E.; Koronakis, E.; Hughes, C. and Koronakis, V. (2004) Proc. Natl. Acad. Sc.i U. S. A., 101, 9994-9.
55. Mikolosko, J.; Bobyk, K.; Zgurskaya, H. I. and Ghosh, P. (2006) Structure, 14, 577-87.
56. Touze, T.; Eswaran, J.; Bokma, E.; Koronakis, E.; Hughes, C. and Koronakis, V. (2004) Mol. Microbiol., 53, 697-706.
57. Zgurskaya, H. I. and Nikaido, H. (1999) J. Mol. Biol., 285, 409-20.
58. Yoneyama, H.; Maseda, H.; Kamiguchi, H. and Nakao, T. (2000) J. Biol. Chem., 275, 4628-34.
59. Zgurskaya, H. I. and Nikaido, H. (2000) J. Bacteriol., 182, 4264-7.
60. Stenberg, F.; Chovanec, P.; Maslen, S. L.; Robinson, C. V.; Ilag, L. L.; von Heijne, G. and Daley, D. O. (2005) J. Biol. Chem., 280, 34409-19.
61. Murakami, S.; Nakashima, R.; Yamashita, E. and Yamaguchi, A. (2002) Nature, 419, 587-93.
62. Pos, K. M. and Diederichs, K. (2002) Acta. Crystallogr. Biol. Crystallogr., D58, 1865-7.
63. Pos, K. M.; Schiefner, A.; Seeger, M. A. and Diederichs, K. (2004) FEBS Lett., 564, 333-9.
64. Eda, S.; Yoneyama, H. and Nakae, T. (2003) Biochemistry, 42, 7238-44.
65. Guan, L. and Nakae, T. (2001) J. Bacteriol., 183, 1734-9.
66. Takatsuka, Y. and Nikaido, H. (2006) J. Bacteriol., 188, 7284-9.
67. Seeger, M. A.; Schiefner, A.; Eicher, T.; Verrey, F.; Diederichs, K. and Pos, K. M.(2006) Science, 313, 1295-8.
68. Murakami, S.; Nakashima, R.; Yamashita, E.; Matsumoto, T. and Yamaguchi, A. (2006) Nature, 443, 173-9.
69. Sennhauser, G.; Amstutz, P.; Briand, C; Storchenegger, O. and Grutter, M. G. (2007) PLoS Biol., 5, e7.
70. Yu, E. W.; McDermott, G.; Zgurskaya, H. I.; Nikaido, H. and Koshland, D. E., Jr. (2003) Science, 300, 976-80.
71. Yu, E. W.; Aires, J. R.; McDermott, G. and Nikaido, H. (2005) J. Bacteriol., 187, 6804-15.
72. Tornroth-Horsefield, S.; Gourdon, P.; Horsefield, R.; Brive, L.; Yamamoto, N.; Mori, H.; Snijder, A. and Neutze, R. (2007) Structure, 15, 1663-73.
73. Elkin, C. A. and Nikaido, H. (2002) J. Bacteriol., 184, 6490-8.
74. Eda, S.; Maseda, H. and Nakae, T. (2003) J. Biol. Chem., 278, 2085-8.
75. Tikhonova, E. B.; Wang, Q. and Zgurskaya, H. I. (2002) J. Bacteriol. 184, 6499-507.
76. Mao, W.; Warren, M. S.; Black, D. S.; Satou, T.; Murata, T.; Nishino, T.; Gotoh, N. and Lomovskaya, O. (2002) Mol. Microbiol., 46, 889-901.
77. Murakami, S.; Tamura, N.; Saito, A.; Hirata, T. and Yamaguchi, A. (2004) J. Biol. Chem., 279, 3743-8.
78. Seeger, M. A.; von Ballmoos, C.; Eicher, T.; Brandstatter, L.; Verrey, F.; Diederichs, K. and Pos, K. M. (2008) Nat. Struct. Mol. Biol., 15, 199-205.
79. Zgurskaya, H. I. and Nikaido, H. (1999) Proc. Natl. Acad. Sci. USA, 96, 7190-5.
80. Aires, J. R. and Nikaido, H. (2005) J. Bacteriol., 187, 1923-9.
81. Tikhonova, E. B. and Zgurskaya, H. I. (2004) J. Biol. Chem., 279, 32116-24.
82. Nehme, D.; Li, X. Z.; Elliot, R. and Poole, K. (2004) J. Bacteriol., 186, 2973-83.
83. Tamura, N.; Murakami, S.; Oyama, Y.; Ishiguro, M. and amaguchi, A. (2005) Biochemistry, 44, 11115-21.
84. Lobedanz, S.; Bokma, E.; Symmons, M. F.; Koronakis, E.; Hughes, C. and Koronakis, V (2007) Proc. Natl. Acad. Sci. USA, 104, 4612-7.
85. Mokhonov, V. V.; Mokhonova, E. I; Akama, H.; and Nakae,T.; (2004) Biochem. Biophys. Res. Commun., 322, 483-9.
86. Gerken, H.; Misra, R. (2004) Mol. Microbiol., 54, 620-31.
87. Eda, S.; Maseda, H.; Yoshihara, E. and Nakae, T. (2006} FEMS Microbiol. Lett., 254, 101-7.
88. Stegmeier, J. F.; Polleichtner, G.; Brandes, N.; Hotz, C. and Andersen, C. (2006) Biochemistry, 45, 10303-12.
89. Bokma, E.; Koronakis, E.; Lobedanz, S.; Hughes, C. and Koronakis, V. (2006) FEBS Lett., 580, 5339-43.
90. Vediyappan, G.; Borisova, T. and Fralick, J. A. (2006) J. Bacteriol., 188, 3757-62.
91. Nehme, D.; Poole, K. (2005) Antimicrob. Agents Chemother., 49, 4375-8.
92. Krishnamoorthy, G.; Tikhonova, E. B. and Zgurskaya, H. I. (2008) J. Bacteriol., 190, 691-8.
93. Vaccaro, L.; Koronakis, V. and Sansom, M. S. (2006) Biophys. J., 91, 558-64.
94. Su, C. C.; Li, M.; Gu, R.; Takatsuka, Y.; McDermott, G.; Nikaido, H. and Yu, E. W. (2006) J. Bacteriol., 188, 7290-6.
95. Das, D.; Xu, Q. S.; Lee, J. Y.; Ankoudinova, I.; Huang, C.; Lou, Y.; DeGiovanni, A.; Kim, R. and Kim, S. H. (2007) J. Struct. Biol., 158, 494-502.
96. Abrahams, J. P.; Leslie, A. G.; Lutter, R. and Walker, J. E. (1994) Nature, 370, 621-8.
97. Hackney, D. D.; Rosen, G. and Boyer, P. D. (1979) Proc. Natl. Acad. Sci. USA, 76, 3646-50.
98. Hutton, R. L. and Boyer, P. D. (1979) J. Biol. Chem., 254, 9990-3.
99. Boyer, P. D. (1997) Annu. Rev. Biochem., 66, 717-49.
100. Petrek M., O. M., Banas P., Kom J. and Damborsky J. (2006).
101. Petrek, M.; Kosinova, P.; Koca, J. and Otyepka, M. (2007) Structure, 15, 1357-63.
102. Su, C. C; Nikaido, H. and Yu, E. W. (2007) FEBS Lett., 581, 4972-6.
103. Lewinson, O. and Bibi, E. (2001) Biochemistry, 40, 12612-8.
104. Muth, T. R. and Schuldiner, S. (2000) EMBOJ., 19, 234-40.
105. Lewinson, O.; Adler, J.; Poelarends, G. J.; Mazurkiewicz, P.; Driessen, A. J. and Bibi, E. (2003) Proc. Natl. Acad. Sci. USA, 100, 1667-72.
106. Li, X. Z.; Ma, D.; Livermore, D. M. and Nikaido, H. (1994) Antimicrob. Agents Chemother., 38, 1742-52.