Quantitative measurement of the outer membrane permeability in Escherichia coli lpp and tol-pal mutants defines the significance of Tol-Pal function for maintaining drug resistance

Journal of Antibiotics

Volumn 69, Issue 12, 2016, Pages 863-870

  Kowata, Hikaru ^a   Tochigi, Saeko ^a   Kusano, Tomonobu ^a   Kojima, Seiji ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

6 AMINOPENICILLANIC ACID; ACRAB PROTEIN; BACTERIAL PROTEIN; BETA LACTAMASE AMPC; LIPOPOLYSACCHARIDE; LIPOSOME; LPP PROTEIN; MAGNESIUM ION; OUTER MEMBRANE PROTEIN C; OUTER MEMBRANE PROTEIN F; PAL PROTEIN; PROTEOLIPOSOME; TOL PROTEIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; ESCHERICHIA COLI PROTEIN; OUTER MEMBRANE PROTEIN; PENICILLIN G;

ANTIBIOTIC RESISTANCE; ARTICLE; ASSAY; BACTERIAL CELL; CELL GROWTH; DELETION MUTANT; DIFFUSION; ESCHERICHIA COLI; GENE DELETION; HYDROLYSIS; HYDROPHOBICITY; MEMBRANE PERMEABILITY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OUTER MEMBRANE; PERIPLASM; PHENOTYPE; PHOSPHOLIPID BILAYER; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; CELL MEMBRANE PERMEABILITY; DRUG EFFECTS; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST; MULTIDRUG RESISTANCE;

ANTI-BACTERIAL AGENTS; BACTERIAL OUTER MEMBRANE PROTEINS; CELL MEMBRANE PERMEABILITY; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; MICROBIAL SENSITIVITY TESTS; PENICILLIN G;

EID: 85006736282     PISSN: 00218820     EISSN: 18811469     Source Type: Journal    
DOI: 10.1038/ja.2016.50     Document Type: Article

References (43)

1. Nikaido, H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656 (2003).
2. Tokuda, H. Biogenesis of outer membranes in Gram-negative bacteria. Biosci. Biotechnol. Biochem. 73, 465-473 (2009).
3. Bos, M. P., Robert, V. & Tommassen, J. Biogenesis of the gram-negative bacterial outer membrane. Annu. Rev. Microbiol. 61, 191-214 (2007).
4. Hirota, Y., Suzuki, H., Nishimura, Y. & Yasuda, S. On the process of cellular division in Escherichia coli: a mutant of E. coli lacking a murein-lipoprotein. Proc. Natl Acad. Sci. USA 74, 1417-1420 (1977).
5. Braun, V. Covalent lipoprotein from the outer membrane of Escherichia coli. Biochim. Biophys. Acta. 415, 335-377 (1975).
6. Lazzaroni, J. C. & Portalier, R. C. Isolation and preliminary characterization of periplasmic-leaky mutants of Escherichia coli K-12. FEMS Microbiol. Lett. 5, 411-416 (1979).
7. Suzuki, H. et al. Murein-lipoprotein of Escherichia coli: a protein involved in the stabilization of bacterial cell envelope. Mol. Gen. Genet. 167, 1-9 (1978).
8. Bernadac, A., Gavioli, M., Lazzaroni, J. C., Raina, S. & Lloubes, R. Escherichia coli tol-pal mutants form outer membrane vesicles. J. Bacteriol. 180, 4872-4878 (1998).
9. Inouye, M., Shaw, J. & Shen, C. The assembly of a structural lipoprotein in the envelope of Escherichia coli. J. Biol. Chem. 247, 8154-8159 (1972).
10. Godlewska, R., Wisniewska, K., Pietras, Z. & Jagusztyn-Krynicka, E. K. Peptidoglycanassociated lipoprotein (Pal) of Gram-negative bacteria: function, structure, role in pathogenesis and potential application in immunoprophylaxis. FEMS Microbiol. Lett. 298, 1-11 (2009).
11. Lazzaroni, J. C., Dubuisson, J. F. & Vianney, A. The Tol proteins of Escherichia coli and their involvement in the translocation of group A colicins. Biochimie 84, 391-397 (2002).
12. Lloubes, R. et al. The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res. Microbiol. 152, 523-529 (2001).
13. Yem, D. W. & Wu, H. C. Physiological characterization of an Escherichia coli mutant altered in the structure of murein lipoprotein. J. Bacteriol. 133, 1419-1426 (1978).
14. Jaurin, B., Grundstrom, T., Edlund, T. & Normark, S. The E. coli beta-lactamase attenuator mediates growth rate-dependent regulation. Nature 290, 221-225 (1981).
15. Kojima, S. & Nikaido, H. Permeation rates of penicillins indicate that Escherichia coli porins function principally as nonspecific channels. Proc. Natl Acad. Sci. USA 110, E2629-E2634 (2013).
16. Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006.0008 (2006).
17. Kim, H. S., Nagore, D. & Nikaido, H. Multidrug efflux pump MdtBC of Escherichia coli is active only as a B2C heterotrimer. J. Bacteriol. 192, 1377-1386 (2010).
18. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640-6645 (2000).
19. Millar, J. H. Experiments in Molecular Genetics (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 1972).
20. Kojima, S. & Nikaido, H. High salt concentrations increase permeability through OmpC channels of Escherichia coli. J. Biol. Chem. 289, 26464-26473 (2014).
21. Novick, R. P. Micro-iodometric assay for penicillinase. Biochem. J. 83, 236-240 (1962).
22. Smit, J., Kamio, Y. & Nikaido, H. Outer membrane of Salmonella typhimurium: chemical analysis and freeze-fracture studies with lipopolysaccharide mutants. J. Bacteriol. 124, 942-958 (1975).
23. Nikaido, H., Nikaido, K. & Harayama, S. Identification and characterization of porins in Pseudomonas aeruginosa. J. Biol. Chem. 266, 770-779 (1991).
24. Fung, J., MacAlister, T. J. & Rothfield, L. I. Role of murein lipoprotein in morphogenesis of the bacterial division septum: phenotypic similarity of lkyD and lpo mutants. J. Bacteriol. 133, 1467-1471 (1978).
25. Nikaido, H., Bavoil, P. & Hirota, Y. Outer membranes of gram-negative bacteria. XV. Transmembrane diffusion rates in lipoprotein-deficient mutants of Escherichia coli. J. Bacteriol. 132, 1045-1047 (1977).
26. Cascales, E., Bernadac, A., Gavioli, M., Lazzaroni, J. C. & Lloubes, R. Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J. Bacteriol. 184, 754-759 (2002).
27. Nichols, R. J. et al. Phenotypic landscape of a bacterial cell. Cell 144, 143-156 (2011).
28. Gerding, M. A., Ogata, Y., Pecora, N. D., Niki, H. & de Boer, P. A. The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol. Microbiol. 63, 1008-1025 (2007).
29. Lazzaroni, J. C. & Portalier, R. C. Genetic and biochemical characterization of periplasmic-leaky mutants of Escherichia coli K-12. J. Bacteriol. 145, 1351-1358 (1981).
30. Nikaido, H. & Normark, S. Sensitivity of Escherichia coli to various beta-lactams is determined by the interplay of outer membrane permeability and degradation by periplasmic beta-lactamases: a quantitative predictive treatment. Mol. Microbiol. 1, 29-36 (1987).
31. Li, X. Z., Ma, D., Livermore, D. M. & Nikaido, H. Role of efflux pump(s) in intrinsic resistance of Pseudomonas aeruginosa: active efflux as a contributing factor to beta-lactam resistance. Antimicrob. Agents Chemother. 38, 1742-1752 (1994).
32. Li, X. Z., Plesiat, P. & Nikaido, H. The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria. Clin. Microbiol. Rev. 28, 337-418 (2015).
33. Nagano, K. & Nikaido, H. Kinetic behavior of the major multidrug efflux pump AcrB of Escherichia coli. Proc. Natl Acad. Sci. USA 106, 5854-5858 (2009).
34. Gray, A. N. et al. Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division. eLife 4, e07118 (2015)
35. Vaara, M. Agents that increase the permeability of the outer-membrane. Microbiol. Rev. 56, 395-411 (1992).
36. Vaara, M. Antibiotic-supersusceptible mutants of Escherichia coli and Salmonella typhimurium. Antimicrob. Agents Chemother. 37, 2255-2260 (1993).
37. Nikaido, H. & Rosenberg, E. Y. Effect on solute size on diffusion rates through the transmembrane pores of the outer membrane of Escherichia coli. J. Gen. Physiol. 77, 121-135 (1981).
38. Lazzaroni, J. C., Fogninilefebvre, N. & Portalier, R. C. Effects of Lkyb-mutations on the expression of Ompf, Ompc and Lamb Porin structural genes in Escherichia coli K-12. FEMS Microbiol. Lett. 33, 235-239 (1986).
39. Meury, J. & Devilliers, G. Impairment of cell division in tolA mutants of Escherichia coli at low and high medium osmolarities. Biol. Cell 91, 67-75 (1999).
40. Hiemstra, H., Nanninga, N., Woldringh, C. L., Inouye, M. & Witholt, B. Distribution of newly synthesized lipoprotein over the outer membrane and the peptidoglycan sacculus of an Escherichia coli lac-lpp strain. J. Bacteriol. 169, 5434-5444 (1987).
41. Lim, S. P. & Nikaido, H. Kinetic parameters of efflux of penicillins by the multidrug efflux transporter AcrAB-TolC of Escherichia coli. Antimicrob. Agents Chemother. 54, 1800-1806 (2010).
42. Mazzariol, A., Cornaglia, G. & Nikaido, H. Contributions of the AmpC beta-lactamase and the AcrAB multidrug efflux system in intrinsic resistance of Escherichia coli K-12 to beta-lactams. Antimicrob. Agents Chemother. 44, 1387-1390 (2000).
43. Curtis, N. A., Orr, D., Ross, G. W. & Boulton, M. G. Affinities of penicillins and cephalosporins for the penicillin-binding proteins of Escherichia coli K-12 and their antibacterial activity. Antimicrob. Agents Chemother. 16, 533-539 (1979).