Conserved small protein associates with the multidrug efflux pump AcrB and differentially affects antibiotic resistance

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 41, 2012, Pages 16696-16701

  Hobbs, Errett C ^a,c   Yin, Xuefeng ^a,b   Paul, Brian J ^a,d   Astarita, Jillian L ^a,e   Storz, Gisela ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^d DUPONT COMPANY   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Multidrug resistance; Resistance nodulation division; RND superfamily

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; BETA GALACTOSIDASE; CHLORAMPHENICOL; ERYTHROMYCIN; FUSIDIC ACID; KANAMYCIN; MEMBRANE PROTEIN; PROTEIN ACRB; PROTEIN ACRZ; PUROMYCIN; RIFAMPICIN; TETRACYCLINE; TOLC PROTEIN; UNCLASSIFIED DRUG;

ACRZ GENE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIUM CULTURE; BACTERIUM MUTANT; CULTURE MEDIUM; ENZYME ACTIVITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE MUTATION; MINIMUM INHIBITORY CONCENTRATION; MIXED CELL CULTURE; MULTIDRUG RESISTANCE; NONHUMAN; PARTITION COEFFICIENT; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIAL OUTER MEMBRANE PROTEINS; CARRIER PROTEINS; CONSERVED SEQUENCE; DNA-BINDING PROTEINS; DRUG RESISTANCE, MICROBIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; IMMUNOBLOTTING; LIPOPROTEINS; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTATION; PERIPLASM; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-ACTIVATORS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84867374260     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1210093109     Document Type: Article

References (38)

1. Otto M (2010) Looking toward basic science for potential drug discovery targets against community-associated MRSA. Med Res Rev 30:1-22.
2. Nikaido H, Pagès JM (2012) Broad-specificity efflux pumps and their role in multidrug resistance of Gram-negative bacteria. FEMS Microbiol Rev 36:340-363.
3. Grkovic S, Brown MH, Skurray RA (2002) Regulation of bacterial drug export systems. Microbiol Mol Biol Rev 66:671-701. (Pubitemid 35425113)
4. Randall LP, Woodward MJ (2002) The multiple antibiotic resistance (mar) locus and its significance. Res Vet Sci 72:87-93. (Pubitemid 34679286)
5. Blair JM, Piddock LJ (2009) Structure, function and inhibition of RND efflux pumps in Gram-negative bacteria: An update. Curr Opin Microbiol 12:512-519.
6. 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. (Pubitemid 44387601)
7. Seeger MA, et al. (2006) Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 313:1295-1298. (Pubitemid 44330954)
8. Lomovskaya O, Zgurskaya HI, Totrov M, Watkins WJ (2007) Waltzing transporters and 'the dance macabre' between humans and bacteria. Nat Rev Drug Discov 6:56-65. (Pubitemid 46020286)
9. Piddock LJ (2006) Multidrug-resistance efflux pumps - not just for resistance. Nat Rev Microbiol 4:629-636.
10. Hobbs EC, Fontaine F, Yin X, Storz G (2011) An expanding universe of small proteins. Curr Opin Microbiol 14:167-173.
11. Hemm MR, Paul BJ, Schneider TD, Storz G, Rudd KE (2008) Small membrane proteins found by comparative genomics and ribosome binding site models. Mol Microbiol 70: 1487-1501.
12. Hemm MR, et al. (2010) Small stress response proteins in Escherichia coli: Proteins missed by classical proteomic studies. J Bacteriol 192:46-58.
13. Fontaine F, Fuchs RT, Storz G (2011) Membrane localization of small proteins in Escherichia coli. J Biol Chem 286:32464-32474.
14. Zeghouf M, et al. (2004) Sequential Peptide Affinity (SPA) system for the identification of mammalian and bacterial protein complexes. J Proteome Res 3:463-468. (Pubitemid 39207350)
15. Hobbs EC, Astarita JL, Storz G (2010) Small RNAs and small proteins involved in resistance to cell envelope stress and acid shock in Escherichia coli: Analysis of a barcoded mutant collection. J Bacteriol 192:59-67.
16. Törnroth-Horsefield S, et al. (2007) Crystal structure of AcrB in complex with a single transmembrane subunit reveals another twist. Structure 15:1663-1673. (Pubitemid 350213410)
17. Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121-4130.
18. Karimova G, Pidoux J, Ullmann A, Ladant D (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756. (Pubitemid 28224168)
19. Mendel RR, Bittner F (2006) Cell biology of molybdenum. Biochim Biophys Acta 1763: 621-635. (Pubitemid 44189541)
20. Martin RG, Gillette WK, Rosner JL (2000) Promoter discrimination by the related transcriptional activators MarA and SoxS: Differential regulation by differential binding. Mol Microbiol 35:623-634. (Pubitemid 30085279)
21. Martin RG, Gillette WK, Martin NI, Rosner JL (2002) Complex formation between activator and RNA polymerase as the basis for transcriptional activation by MarA and SoxS in Escherichia coli. Mol Microbiol 43:355-370. (Pubitemid 34146727)
22. Sulavik MC, et al. (2001) Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob Agents Chemother 45:1126-1136. (Pubitemid 32230993)
23. Nichols RJ, et al. (2011) Phenotypic landscape of a bacterial cell. Cell 144:143-156.
24. Alix E, Blanc-Potard AB (2009) Hydrophobic peptides: Novel regulators within bacterial membrane. Mol Microbiol 72:5-11.
25. Eguchi Y, et al. (2007) B1500, a small membrane protein, connects the two-component systems EvgS/EvgA and PhoQ/PhoP in Escherichia coli. Proc Natl Acad Sci USA 104:18712-18717. (Pubitemid 350210762)
26. Lippa AM, Goulian M (2009) Feedback inhibition in the PhoQ/PhoP signaling system by a membrane peptide. PLoS Genet 5:e1000788.
27. Modell JW, Hopkins AC, Laub MT (2011) A DNA damage checkpoint in Caulobacter crescentus inhibits cell division through a direct interaction with FtsW. Genes Dev 25: 1328-1343.
28. 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: 565-569.
29. Takatsuka Y, Chen C, Nikaido H (2010) Mechanism of recognition of compounds of diverse structures by the multidrug efflux pump AcrB of Escherichia coli. Proc Natl Acad Sci USA 107:6559-6565.
30. Eicher T, et al. (2012) Transport of drugs by the multidrug transporter AcrB involves an access and a deep binding pocket that are separated by a switch-loop. Proc Natl Acad Sci USA 109:5687-5692.
31. Husain F, Bikhchandani M, Nikaido H (2011) Vestibules are part of the substrate path in the multidrug efflux transporter AcrB of Escherichia coli. J Bacteriol 193:5847-5849.
32. Husain F, Nikaido H (2010) Substrate path in the AcrB multidrug efflux pump of Escherichia coli. Mol Microbiol 78:320-330.
33. Tal N, Schuldiner S (2009) A coordinated network of transporters with overlapping speci ficities provides a robust survival strategy. Proc Natl Acad Sci USA 106: 9051-9056.
34. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645. (Pubitemid 30412767)
35. Yu D, et al. (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97:5978-5983. (Pubitemid 30367509)
36. Miller JH (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria (Cold Spring Harbor Laboratory Press, Plainview, NY).
37. Massé E, Escorcia FE, Gottesman S (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17:2374-2383. (Pubitemid 37214786)
38. Opdyke JA, Kang JG, Storz G (2004) GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186:6698-6705. (Pubitemid 39332106)