Multidrug resistance of a porin deletion mutant of Mycobacterium smegmatis

Antimicrobial Agents and Chemotherapy

Volumn 48, Issue 11, 2004, Pages 4163-4170

  Stephan, Joachim ^a   Mailaender, Claudia ^a   Etienne, Gilles ^b   Daffé, Mamadou ^b   Niederweis, Michael ^a,c  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^c University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; CEFALORIDINE; CEFALOTIN; CHENODEOXYCHOLIC ACID; CHLORAMPHENICOL; CYCLOSERINE; ERYTHROMYCIN; ETHAMBUTOL; ISONIAZID; KANAMYCIN A; NOVOBIOCIN; PORIN; PORIN MSPA; RIFAMPICIN; STEROID; TETRACYCLINE; UNCLASSIFIED DRUG; VANCOMYCIN;

ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIUM MUTANT; CELL MEMBRANE PERMEABILITY; DELETION MUTANT; DIFFUSION; DRUG DESIGN; DRUG PENETRATION; DRUG STRUCTURE; DRUG UPTAKE; GENE DELETION; HYDROPHILICITY; HYDROPHOBICITY; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL;

AMINOGLYCOSIDES; ANTI-BACTERIAL AGENTS; ANTITUBERCULAR AGENTS; BETA-LACTAMS; BIOLOGICAL TRANSPORT; CELL WALL; CHEMISTRY, PHYSICAL; CULTURE MEDIA; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE DELETION; LIPID METABOLISM; MICROBIAL SENSITIVITY TESTS; MYCOBACTERIUM SMEGMATIS; PORINS;

EID: 7244258919     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.48.11.4163-4170.2004     Document Type: Article

References (67)

1. Ames, G. F., E. N. Spudich, and H. Nikaido. 1974. Protein composition of the outer membrane of Salmonella typhimurium: effect of lipopolysaccharide mutations. J. Bacteriol. 117:406-416.
2. Araoz, R., E. Anhalt, L. Rene, M. A. Badet-Denisot, P. Courvalin, and B. Badet. 2000. Mechanism-based inactivation of VanX, a D-alanyl-D-alanine dipeptidase necessary for vancomycin resistance. Biochemistry 39:15971-15979.
3. Bardou, F., C. Raynaud, C. Ramos, M. A. Laneelle, and G. Laneelle. 1998. Mechanism of isoniazid uptake in Mycobacterium tuberculosis. Microbiology 144:2539-2544.
4. Brennan, P. J., and H. Nikaido. 1995. The envelope of mycobacteria. Annu. Rev. Biochem. 64:29-63.
5. Brown-Elliott, B. A., and R. J. Wallace, Jr. 2002. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin. Microbiol. Rev. 15:716-746.
6. Chopra, I., and S. J. Eccles. 1978. Diffusion of tetracycline across the outer membrane of Escherichia coli K-12: involvement of protein Ia. Biochem. Biophys. Res. Commun. 83:550-557.
7. Coates, A., Y. Hu, R. Bax, and C. Page. 2002. The future challenges facing the development of new antimicrobial drugs. Nat. Rev. Drug Discov. 1:895-910.
8. Cui, L., X. Ma, K. Sato, K. Okuma, F. C. Tenover, E. M. Mamizuka, C. G. Gemmell, M. N. Kim, M. C. Ploy, N. El-Solh, V. Ferraz, and K. Hiramatsu. 2003. Cell wall thickening is a common feature of vancomycin resistance in Staphylococcus aureus. J. Clin. Microbiol. 41:5-14.
9. Dittmer, J. C. F., and R. L. Lester. 1964. A simple specific spray for the detection of phospholipids on thin layer chromatography. J. Lipid Res. 5:126-127.
10. Donadio, S., L. Carrano, L. Brandi, S. Serina, A. Soffientini, E. Raimondi, N. Montanini, M. Sosio, and C. O. Gualerzi. 2002. Targets and assays for discovering novel antibacterial agents. J. Biotechnol. 99:175-185.
11. Dubnau, E., J. Chan, C. Raynaud, V. P. Mohan, M. A. Laneelle, K. Yu, A. Quemard, I. Smith, and M. Daffé. 2000. Oxygenated mycolic acids are necessary for virulence of Mycobacterium tuberculosis in mice. Mol. Microbiol. 36:630-637.
12. Engelhardt, H., C. Heinz, and M. Niederweis. 2002. A tetrameric porin limits the cell wall permeability of Mycobacterium smegmatis. J. Biol. Chem. 277:37567-37572.
13. Etienne, G., C. Villeneuve, H. Billman-Jacobe, C. Astarie-Dequeker, M. A. Dupont, and M. Daffe. 2002. The impact of the absence of glycopeptidolipids on the ultrastructure, cell surface and cell wall properties, and phagocytosis of Mycobacterium smegmatis. Microbiology 148:3089-3100.
14. Faller, M., M. Niederweis, and G. E. Schulz. 2004. The structure of a mycobacterial outer-membrane channel. Science 303:1189-1192.
15. Gutmann, L., R. Williamson, N. Moreau, M. D. Kitzis, E. Collatz, J. F. Acar, and F. W. Goldstein. 1985. Cross-resistance to nalidixic acid, trimethoprim, and chloramphenicol associated with alterations in outer membrane proteins of Klebsiella, Enterobacter, and Serratia. J. Infect. Dis. 151:501-507.
16. Hancock, R. E. 1997. The bacterial outer membrane as a drug barrier. Trends Microbiol. 5:37-42.
17. Hancock, R. E., and F. S. Brinkman. 2002. Functions of Pseudomonas porins in uptake and efflux. Annu. Rev. Microbiol. 56:17-38.
18. Hancock, R. E., S. W. Farmer, Z. S. Li, and K. Poole. 1991. Interaction of aminoglycosides with the outer membranes and purified lipopolysaccharide and OmpF porin of Escherichia coli. Antimicrob. Agents Chemother. 35:1309-1314.
19. Hancock, R. E., and P. G. Wong. 1984. Compounds which increase the permeability of the Pseudomonas aeruginosa outer membrane. Antimicrob. Agents Chemother. 26:48-52.
20. Hansch, C., A. Leo, and D. H. Hoekman. 1995. Exploring QSAR. II. Hydrophobic, electronic, and steric constants. American Chemical Society, Washington, D.C.
21. Harder, K. J., H. Nikaido, and M. Matsuhashi. 1981. Mutants of Escherichia coli that are resistant to certain beta-lactam compounds lack the OmpF porin. Antimicrob. Agents Chemother. 20:549-552.
22. Heifets, L. B. 1982. Synergistic effect of rifampin, streptomycin, ethionamide, and ethambutol on Mycobacterium intracellulare. Am. Rev. Respir. Dis. 125:43-48.
23. Heinz, C., S. Karosi, and M. Niederweis. 2003. High level expression of the mycobacterial porin MspA in Escherichia coli and purification of the recombinant protein. J. Chromatogr. B 790:337-348.
24. Heinz, C., and M. Niederweis. 2000. Selective extraction and purification of a mycobacterial outer membrane protein. Anal. Biochem. 285:113-120.
25. Hirai, K., H. Aoyama, T. Irikura, S. Iyobe, and S. Mitsuhashi. 1986. Differences in susceptibility to quinolones of outer membrane mutants of Salmonella typhimurium and Escherichia coli. Antimicrob. Agents Chemother. 29:535-538.
26. Hughes, D. 2003. Exploiting genomics, genetics and chemistry to combat antibiotic resistance. Nat. Rev. Genet. 4:432-441.
27. Im, W., and B. Roux. 2002. Ions and counterions in a biological channel: a molecular dynamics simulation of OmpF porin from Escherichia coli in an explicit membrane with 1 M KCl aqueous salt solution. J. Mol. Biol. 319:1177-1197.
28. Jackson, M., C. Raynaud, M. A. Laneelle, C. Guilhot, C. Laurent-Winter, D. Ensergueix, B. Gicquel, and M. Daffé. 1999. Inactivation of the antigen 85C gene profoundly affects the mycolate content and alters the permeability of the Mycobacterium tuberculosis cell envelope. Mol. Microbiol. 31:1573-1587.
29. Jaffe, A., Y. A. Chabbert, and O. Semonin. 1982. Role of porin proteins OmpF and OmpC in the permeation of beta-lactams. Antimicrob. Agents Chemother. 22:942-948.
30. Jarlier, V., L. Gutmann, and H. Nikaido. 1991. Interplay of cell wall barrier and β-lactamase activity determines high resistance to β-lactam antibiotics in Mycobacterium chelonae. Antimicrob. Agents Chemother. 35:1937-1939.
31. Jarlier, V., and H. Nikaido. 1994. Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol. Lett. 123:11-18.
32. Jarlier, V., and H. Nikaido. 1990. Permeability barrier to hydrophilic solutes in Mycobacterium chelonei. J. Bacteriol. 172:1418-1423.
33. 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.
34. Kremer, L. S., and G. S. Besra. 2002. Current status and future development of antitubercular chemotherapy. Expert Opin. Investig. Drugs 11:1033-1049.
35. Lambert, P. A. 2002. Cellular impermeability and uptake of biocides and antibiotics in gram-positive bacteria and mycobacteria. J. Appl. Microbiol. 92(Suppl.):46S-54S.
36. Liu, J., C. E. Barry III, G. S. Besra, and H. Nikaido. 1996. Mycolic acid structure determines the fluidity of the mycobacterial cell wall. J. Biol. Chem. 271:29545-29551.
37. Mailaender, C., N. Reiling, H. Engelhardt, S. Bossmann, S. Ehlers, and M. Niederweis. 2004. The MspA porin promotes growth and increases antibiotic susceptibility of both Mycobacterium bovis BCG and Mycobacterium tuberculosis. Microbiology 150:853-864.
38. Marciano, D. K., M. Russel, and S. M. Simon. 1999. An aqueous channel for filamentous phage export. Science 284:1516-1519.
39. Nakae, R., and T. Nakae. 1982. Diffusion of aminoglycoside antibiotics across the outer membrane of Escherichia coli. Antimicrob. Agents Chemother. 22:554-559.
40. Niederweis, M. 2003. Mycobacterial porins-new channel proteins in unique outer membranes. Mol. Microbiol. 49:1167-1177.
41. Niederweis, M., S. Ehrt, C. Heinz, U. Klocker, S. Karosi, K. M. Swiderek, L. W. Riley, and R. Benz. 1999. Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis. Mol. Microbiol. 33:933-945.
42. Nikaido, H. 1976. Outer membrane of Salmonella typhimurium. Transmembrane diffusion of some hydrophobic substances. Biochim. Biophys. Acta 433:118-132.
43. Nikaido, H. 1994. Porins and specific diffusion channels in bacterial outer membranes. J. Biol. Chem. 269:3905-3908.
44. Nikaido, H. 2001. Preventing drug access to targets: cell surface permeability barriers and active efflux in bacteria. Semin. Cell Dev. Biol. 12:215-223.
45. Nikaido, H. 1994. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264:382-388.
46. Nikaido, H. 1985. Role of permeability barriers in resistance to beta-lactam antibiotics. Pharmacol. Ther. 27:197-231.
47. Nikaido, H., and S. Normark. 1987. 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.
48. Nikaido, H., E. Y. Rosenberg, and J. Foulds. 1983. Porin channels in Escherichia coli: studies with beta-lactams in intact cells. J. Bacteriol. 153:232-240.
49. Nikaido, H., and M. Vaara. 1985. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 49:1-32.
50. Paul, T. R., and T. J. Beveridge. 1992. Reevaluation of envelope profiles and cytoplasmic ultrastructure of mycobacteria processed by conventional embedding and freeze-substitution protocols. J. Bacteriol. 174:6508-6517.
51. Poole, K. 2002. Outer membranes and efflux: the path to multidrug resistance in gram-negative bacteria. Curr. Pharm. Biotechnol. 3:77-98.
52. Pugsley, A. P., and C. A. Schnaitman. 1978. Outer membrane proteins of Escherichia coli. VII. Evidence that bacteriophage-directed protein 2 functions as a pore. J. Bacteriol. 133:1181-1189.
53. Ramaswamy, S., and J. M. Musser. 1998. Molecular genetic basis of antimicrobial agent resistance in Mycobacterium tuberculosis: 1998 update. Tuber. Lung Dis. 79:3-29.
54. Riess, F. G., U. Dorner, B. Schiffier, and R. Benz. 2001. Study of the properties of a channel-forming protein of the cell wall of the gram-positive bacterium Mycobacterium phlei. J. Membr. Biol. 182:147-157.
55. +: a dominant selectable marker for gene replacement in mycobacteria. Mol. Microbiol. 16:991-1000.
56. Sawai, T., R. Hiruma, N. Kawana, M. Kaneko, F. Taniyasu, and A. Inami. 1982. Outer membrane permeation of beta-lactam antibiotics in Escherichia coli, Proteus mirabilis, and Enterobacter cloacae. Antimicrob. Agents Chemother. 22:585-592.
57. Schäfer, M., T. R. Schneider, and G. M. Sheldrick. 1996. Crystal structure of vancomycin. Structure 4:1509-1515.
58. Schulz, G. E. 1993. Bacterial porins: structure and function. Curr. Opin. Cell Biol. 5:701-707.
59. Schulze-Röbbecke, R., B. Janning, and R. Fischeder. 1992. Occurrence of mycobacteria in biofilm samples. Tuber. Lung Dis. 73:141-144.
60. Srinivasan, A., J. D. Dick, and T. M. Perl. 2002. Vancomycin resistance in staphylococci. Clin. Microbiol. Rev. 15:430-438.
61. Stahl, C., S. Kubetzko, I. Kaps, S. Seeber, H. Engelhardt, and M. Niederweis. 2001. MspA provides the main hydrophilic pathway through the cell wall of Mycobacterium smegmatis. Mol. Microbiol. 40:451-464.
62. Takayama, K., E. L. Armstrong, K. A. Kunugi, and J. O. Kilburn. 1979. Inhibition by ethambutol of mycolic acid transfer into the cell wall of Mycobacterium smegmatis. Antimicrob. Agents Chemother. 16:240-242.
63. Trias, J., and R. Benz. 1994. Permeability of the cell wall of Mycobacterium smegmatis. Mol. Microbiol. 14:283-290.
64. van Horn, K. G., C. A. Gedris, and K. M. Rodney. 1996. Selective isolation of vancomycin-resistant enterococci. J. Clin. Microbiol. 34:924-927.
65. Winder, F. G., and P. B. Collins. 1970. Inhibition by isoniazid of synthesis of mycolic acids in Mycobacterium tuberculosis. J. Gen. Microbiol. 63:41-48.
66. Zhang, Y., S. Dhandayuthapani, and V. Deretic. 1996. Molecular basis for the exquisite sensitivity of Mycobacterium tuberculosis to isoniazid. Proc. Natl. Acad. Sci. USA 93:13212-13216.
67. Zimmer, B. L., D. R. DeYoung, and G. D. Roberts. 1982. In vitro synergistic activity of ethambutol, isoniazid, kanamycin, rifampin, and streptomycin against Mycobacterium avium-intracellulare complex. Antimicrob. Agents Chemother. 22:148-150.