Transport across the outer membrane porin of mycolic acid containing actinomycetales: Nocardia farcinica

Biochimica et Biophysica Acta - Biomembranes

Volumn 1848, Issue 2, 2015, Pages 654-661

  Singh, Pratik Raj ^a   Bajaj, Harsha ^a   Benz, Roland ^a   Winterhalter, Mathias ^a   Mahendran, Kozhinjampara R ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

Author keywords

Antibiotic resistance; Mycolata; Nocardia farcinica; Porin; Single channel electrophysiology

Indexed keywords

AMIKACIN; AMINO ACID; ERTAPENEM; KANAMYCIN; LIPOSOME; MYCOLIC ACID; PORIN; SUGAR; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BETA LACTAM; RECOMBINANT PROTEIN;

ARTICLE; BACTERIAL CELL WALL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG POTENTIATION; HYDROPHILICITY; MEMBRANE CHANNEL; MUTATIONAL ANALYSIS; NOCARDIA FARCINICA; NONHUMAN; RESIDUE ANALYSIS; CELL MEMBRANE; CELL WALL; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; METABOLISM; MUTATION; NOCARDIA; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY; STRUCTURAL HOMOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ACTINOMYCETALES; NOCARDIA FARCINICA; POSIBACTERIA;

AMIKACIN; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAMS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELL WALL; ESCHERICHIA COLI; GENE EXPRESSION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KANAMYCIN; LIPOSOMES; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; MYCOLIC ACIDS; NOCARDIA; PORINS; RECOMBINANT PROTEINS; STATIC ELECTRICITY; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84919338453     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.11.020     Document Type: Article

References (55)

1. H. Nikaido, Prevention of drug access to bacterial targets: permeability barriers and active efflux, Science 264 (1994) 382-388, http://dx.doi.org/10.1126/science.8153625.
2. H. Nikaido, Molecular basis of bacterial outer membrane permeability revisited, Microbiol. Mol. Biol. Rev. 67 (2003) 593-656.
3. A.H. Delcour, Outer membrane permeability and antibiotic resistance, Biochim. Biophys. Acta 1794 (2009) 808-816, http://dx.doi.org/10.1016/j.bbapap.2008.11.005.
4. J.-M. Pagès, C.E. James, M. Winterhalter, The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria, Nat. Rev. Microbiol. 6 (2008) 893-903, http://dx.doi.org/10.1038/nrmicro1994.
5. K. Poole, Outer membranes and efflux: the path to multidrug resistance in Gram-negative bacteria, Curr. Pharm. Biotechnol. 3 (2002) 77-98.
6. H. Nikaido, Outer membrane barrier as a mechanism of antimicrobial resistance, Antimicrob. Agents Chemother. 33 (1989) 1831-1836, http://dx.doi.org/10.1128/AAC.33.11.1831.
7. T.J. Silhavy, D. Kahne, S. Walker, The bacterial cell envelope, Cold Spring Harb. Perspect. Biol. 2 (2010) a000414, http://dx.doi.org/10.1101/cshperspect.a000414.
8. V. Jarlier, H. Nikaido, Mycobacterial cell wall: structure and role in natural resistance to antibiotics, FEMS Microbiol. Lett. 123 (1994) 11-18.
9. V. Jarlier, L. Gutmann, H. Nikaido, Interplay of cell wall barrier and beta-lactamase activity determines high resistance to beta-lactam antibiotics in Mycobacterium chelonae, Antimicrob. Agents Chemother. 35 (1991) 1937-1939, http://dx.doi.org/10.1128/AAC.35.9.1937.
10. D.E. Minnikin, S.M. Minnikin, M. Goodfellow, J.L. Stanford, The mycolic acids of Mycobacterium chelonei, J. Gen. Microbiol. 128 (1982) 817-822, http://dx.doi.org/10.1099/00221287-131-9-2237.
11. D.E. Minnikin, Chemical principles in the organization of lipid components in the mycobacterial cell envelope, Res. Microbiol. 142 (1991) 423-427, http://dx.doi.org/10.1016/0923-2508(91)90114-P.
12. P.J. Brennan, H. Nikaido, The envelope of mycobacteria, Annu. Rev. Biochem. 64 (1995) 29-63, http://dx.doi.org/10.1146/annurev.biochem.64.1.29.
13. D.E. Minnikin, S.M. Minnikin, J.H. Parlett, M. Goodfellow, M. Magnusson, Mycolic acid patterns of some species of Mycobacterium, Arch. Microbiol. 139 (1984) 225-231, http://dx.doi.org/10.1007/BF00402005.
14. J. Trias, V. Jarlier, R. Benz, Porins in the cell wall ofmycobacteria, Science 258 (1992) 1479-1481, http://dx.doi.org/10.1126/science.1279810.
15. M. Niederweis, Mycobacterial porins - new channel proteins in unique outermembranes, Mol. Microbiol. 49 (2003) 1167-1177, http://dx.doi.org/10.1046/j.1365-2958.2003.03662.x.
16. T. Lichtinger, A. Burkovski, M. Niederweis, R. Krámer, R. Benz, Biochemical and biophysical characterization of the cell wall porin of Corynebacterium glutamicum: the channel is formed by a low molecular mass polypeptide, Biochemistry 37 (1998) 15024-15032, http://dx.doi.org/10.1021/bi980961e.
17. J. Trias, R. Benz, Permeability of the cell wall of Mycobacterium smegmatis, Mol. Microbiol. 14 (1994) 283-290, http://dx.doi.org/10.1111/j.1365-2958.1994.tb01289.x.
18. F.G. Riess, T. Lichtinger, R. Cseh, A.F. Yassin, K.P. Schaal, R. Benz, The cell wall porin of Nocardia farcinica: biochemical identification of the channel-forming protein and biophysical characterization of the channel properties, Mol. Microbiol. 29 (1998) 139-150, http://dx.doi.org/10.1046/j.1365-2958.1998.00914.x.
19. C.M. Jones, M. Niederweis, Role of porins in iron uptake by Mycobacterium smegmatis, J. Bacteriol. 192 (2010) 6411-6417.
20. O. Danilchanka, M. Pavlenok, M. Niederweis, Role of porins for uptake of antibiotics by Mycobacterium smegmatis, Antimicrob. Agents Chemother. 52 (2008) 3127-3134, http://dx.doi.org/10.1128/AAC. 00239-08.
21. R. Benz, Bacterial Cell Wall, Elsevier, 1994., http://dx.doi.org/10.1016/S0167-7306(08)60422-6.
22. World Health Organization, Global Tuberculosis Control 2011,, 2011, ISBN 978 92 9061 522 4.
23. B.R. Bloom, Vaccines for the Third World, Nature 342 (1989) 115-120.
24. C. Kläckta, P. Knörzer, F. Riess, R. Benz, Hetero-oligomeric cell wall channels (porins) of Nocardia farcinica, Biochim. Biophys. Acta Biomembr. 1808 (2011) 1601-1610, http://dx.doi.org/10.1016/j.bbamem.2010.11.011.
25. P.R. Singh, I. Bárcena-Uribarri, N. Modi, U. Kleinekathöfer, R. Benz, M. Winterhalter, et al., Pulling peptides across nanochannels: resolving peptide binding and translocation through the hetero-oligomeric channel from Nocardia farcinica, ACS Nano 6 (2012) 10699-10707, http://dx.doi.org/10.1021/nn303900y.
26. H. Nikaido, E.Y. Rosenberg, Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins, J. Bacteriol. 153 (1983) 241-252.
27. F. Yoshimura, H. Nikaido, Diffusion of beta-lactam antibiotics through the porin channels of Escherichia coli K-12, Antimicrob. Agents Chemother. 27 (1985) 84-92.
28. M. Montal, P. Mueller, Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties, Proc. Natl. Acad. Sci. U. S. A. 69 (1972) 3561-3566, http://dx.doi.org/10.1073/pnas.69.12.3561.
29. E.M. Nestorovich, C. Danelon, M. Winterhalter, S.M. Bezrukov, Designed to penetrate: time-resolved interaction of single antibiotic molecules with bacterial pores, Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 9789-9794, http://dx.doi.org/10.1073/pnas.152206799.
30. A.L. Hodgkin, B. Katz, The effect of sodium ions on the electrical activity of the giant axon of the squid, J. Physiol. 108 (1949) 37-77.
31. C. Danelon, A. Suenaga, M. Winterhalter, I. Yamato, Molecular origin of the cation selectivity in OmpF porin: single channel conductances vs. free energy calculation, Biophys. Chem. 104 (2003) 591-603, http://dx.doi.org/10.1016/S0301-4622(03)00062-0.
32. J. Trias, R. Benz, Characterization of the channel formed by the mycobacterial porin in lipid bilayer membranes. Demonstration of voltage gating and of negative point charges at the channel mouth, J. Biol. Chem. 268 (1993) 6234-6240.
33. H. Bajaj, Q.T. Tran, K.R. Mahendran, C. Nasrallah, J.P. Colletier, A. Davin-Regli, et al., Antibiotic uptake through membrane channels: role of Providencia stuartii omppst1 porin in carbapenem resistance, Biochemistry 51 (2012) 10244-10249, http://dx.doi.org/10.1021/bi301398j.
34. K.R. Mahendran, M. Kreir, H. Weingart, N. Fertig, M. Winterhalter, Permeation of antibiotics through Escherichia coli OmpF and OmpC porins: screening for influx on a single-molecule level, J. Biomol. Screen. 15 (2010) 302-307, http://dx.doi.org/10.1177/1087057109357791.
35. B.K. Ziervogel, B. Roux, The binding of antibiotics in OmpF porin, Structure 21 (2013) 76-87, http://dx.doi.org/10.1016/j.str.2012.10.014.
36. P.R. Singh, M. Ceccarelli, M. Lovelle, M. Winterhalter, K.R. Mahendran, Antibiotic permeation across the OmpF channel: modulation of the affinity site in the presence of magnesium, J. Phys. Chem. B 116 (2012) 4433-4438, http://dx.doi.org/10.1021/jp2123136.
37. D. Fologea, J. Uplinger, B. Thomas, D.S. McNabb, J. Li, Slowing DNA translocation in a solid-state nanopore, Nano Lett. 5 (2005) 1734-1737, http://dx.doi.org/10.1021/nl051063o.
38. K.R. Mahendran, M. Romero-Ruiz, A. Schlösinger, M. Winterhalter, S. Nussberger, Protein translocation through Tom40: kinetics of peptide release, Biophys. J. 102 (2012) 39-47, http://dx.doi.org/10.1016/j.bpj.2011.11.4003.
39. R.S. Kane, P.T. Glink, R.G. Chapman, J.C. McDonald, P.K. Jensen, H. Gao, et al., Basicity of the amino groups of the aminoglycoside amikacin using capillary electrophoresis and coupled CE-MS-MS techniques, Anal. Chem. 73 (2001) 4028-4036, http://dx.doi.org/10.1021/ac010173m.
40. C. Danelon, E.M. Nestorovich, M. Winterhalter, M. Ceccarelli, S.M. Bezrukov, Interaction of zwitterionic penicillins with the OmpF channel facilitates their translocation, Biophys. J. 90 (2006) 1617-1627, http://dx.doi.org/10.1529/biophysj.105.075192.
41. K.R. Mahendran, E. Hajjar, T. Mac H, M. Lovelle, A. Kumar, I. Sousa, et al., Molecular basis of enrofloxacin translocation through OmpF, an outer membrane channel of Escherichia coli - when binding does not imply translocation, J. Phys. Chem. B 114 (2010) 5170-5179, http://dx.doi.org/10.1021/jp911485k.
42. E. Hajjar, K.R. Mahendran, A. Kumar, A. Bessonov, M. Petrescu, H. Weingart, et al., Bridging timescales and length scales: from macroscopic flux to the molecular mechanism of antibiotic diffusion through porins, Biophys. J. 98 (2010) 569-575, http://dx.doi.org/10.1016/j.bpj.2009.10.045.
43. S. Vidal, J. Bredin, J.M. Pagès, J. Barbe, β-Lactam screening by specific residues of the OmpF eyelet, J. Med. Chem. 48 (2005) 1395-1400, http://dx.doi.org/10.1021/jm049652e.
44. S.A. Benson, J.L. Occi, B.A. Sampson, Mutations that alter the pore function of the OmpF porin of Escherichia coli K12, J. Mol. Biol. 203 (1988) 961-970, http://dx.doi.org/10.1016/0022-2836(88)90121-0.
45. R. Misra, S.A. Benson, Isolation and characterization of OmpC porin mutants with altered pore properties, J. Bacteriol. 170 (1988) 528-533.
46. A. Thiolas, C. Bornet, A. Davin-Régli, J.M. Pagès, C. Bollet, Resistance to imipenem, cefepime, and cefpirome associated with mutation in Omp36 osmoporin of Enterobacter aerogenes, Biochem. Biophys. Res. Commun. 317 (2004) 851-856, http://dx.doi.org/10.1016/j.bbrc.2004.03.130.
47. J. Ishikawa, A. Yamashita, Y. Mikami, Y. Hoshino, H. Kurita, K. Hotta, et al., The complete genomic sequence of Nocardia farcinica IFM10152, Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 14925-14930, http://dx.doi.org/10.1073/pnas.0406410101.
48. E. Cercenado, M. Marín, M. Sánchez-Martínez, O. Cuevas, J. Martínez-Alarcón, E. Bouza, In vitro activities of tigecycline and eight other antimicrobials against different Nocardia species identified by molecular methods, Antimicrob. Agents Chemother. 51 (2007) 1102-1104, http://dx.doi.org/10.1128/AAC. 01102-06.
49. L. Movileanu, J.P. Schmittschmitt, J.M. Scholtz, H. Bayley, Interactions of peptides with a protein pore, Biophys. J. 89 (2005) 1030-1045, http://dx.doi.org/10.1529/biophysj.104.057406.
50. J. Stephan, C. Mailaender, G. Etienne, M. Daffé, M. Niederweis, Multidrug resistance of a porin deletion mutant of Mycobacterium smegmatis, Antimicrob. Agents Chemother. 48 (2004) 4163-4170, http://dx.doi.org/10.1128/AAC. 48.11.4163-4170.2004.
51. O.H. Torres, P. Domingo, R. Pericas, P. Boiron, J.A. Montiel, G. Vázquez, Infection Caused by Nocardia farcinica: Case Report and Review, 2000., http://dx.doi.org/10.1007/s100960050460.
52. V. Jarlier, H. Nikaido, Permeability barrier to hydrophilic solutes in Mycobacterium chelonei, J. Bacteriol. 172 (1990) 1418-1423.
53. H. Gebhardt, X. Meniche, M. Tropis, R. Krämer, M. Daffé, S. Morbach, The key role of the mycolic acid content in the functionality of the cell wall permeability barrier in Corynebacterineae, Microbiology 153 (2007) 1424-1434, http://dx.doi.org/10.1099/mic.0.2006/003541-0.
54. C.E. Barry, R.E. Lee, K. Mdluli, A.E. Sampson, B.G. Schroeder, R.A. Slayden, et al., Mycolic acids: structure, biosynthesis and physiological functions, Prog. Lipid Res. 37 (1998) 143-179, http://dx.doi.org/10.1016/S0163-7827(98)00008-3.
55. K.W. Langford, B. Penkov, I.M. Derrington, J.H. Gundlach, Unsupported planar lipid membranes formed from mycolic acids of Mycobacterium tuberculosis, J. Lipid Res. 52 (2011) 272-277, http://dx.doi.org/10.1194/jlr.M012013.