A 2H solid-state NMR study of the effect of antimicrobial agents on intact Escherichia coli without mutating

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 2, 2013, Pages 614-622

  Tardy Laporte, Catherine ^a   Arnold, Alexandre A ^a   Genard, Bertrand ^b   Gastineau, Romain ^c   Morançais, Michèle ^d   Mouget, Jean Luc ^c   Tremblay, Réjean ^b   Marcotte, Isabelle ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^b INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

^c UNIVERSITÉ DU MAINE   (France)

^d UNIVERSITÉ DE NANTES   (France)

Author keywords

Cetyltrimethylammonium chloride; Marennine like pigment; Membrane interaction; Nuclear magnetic resonance; Polyhydroxylated fullerene nanoparticle; Polymyxin B

Indexed keywords

ANTIINFECTIVE AGENT; CETRIMONIUM CHLORIDE; DIPALMITOYLPHOSPHATIDYLCHOLINE; DIPALMITOYLPHOSPHATIDYLGLYCEROL; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; FATTY ACID; FULLERENOL; MARENNINE; MEMBRANE PHOSPHOLIPID; NANOPARTICLE; PALMITIC ACID; POLYMYXIN B; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; BACTERIAL MUTATION; CELL STRUCTURE; CELL VIABILITY; CHEMICAL REACTION; CONTROLLED STUDY; DEUTERON NUCLEAR MAGNETIC RESONANCE; DRUG INTERACTION; ESCHERICHIA COLI; IN VIVO STUDY; ISOTOPE LABELING; LIPID ANALYSIS; LIPOGENESIS; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROCESS DEVELOPMENT; SPECTROSCOPY; STRUCTURE ANALYSIS;

ANTI-INFECTIVE AGENTS; DETERGENTS; DIATOMS; ESCHERICHIA COLI; FULLERENES; LIPID BILAYERS; LIPIDS; MAGNETIC RESONANCE SPECTROSCOPY; MICROBIAL SENSITIVITY TESTS; MODELS, CHEMICAL; MODELS, STATISTICAL; NANOPARTICLES; PALMITIC ACID; PHOSPHOLIPIDS; TEMPERATURE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84870197216     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.09.011     Document Type: Article

References (64)

1. E. Di Pasquale, C. Salmi-Smail, J.-M. Brunel, P. Sanchez, J. Fantini, and M. Maresca Biophysical studies of the interaction of squalamine and other cationic amphiphilic molecules with bacterial and eukaryotic membranes: importance of the distribution coefficient in membrane selectivity Chem. Phys. Lipids 163 2010 131 140
2. C.T. Barrett, and J.F. Barrett Antibacterials: are the new entries enough to deal with the emerging resistance problems? Curr. Opin. Biotechnol. 14 2003 621 626
3. World Health Organization Medical impact of use of antimicrobial drugs in food animals http://www.who.int/csr/don/1997-03-28/en/ 1997
4. C. Walsh Molecular mechanisms that confer antibacterial drug resistance Nature 406 2000 775 781
5. K.M. Overbye, and J.F. Barrett Antibiotics: where did we go wrong? Drug Discov. Today 10 2005 45 52
6. K. Matsuzaki Why and how are peptide-lipid interactions utilized for self defence? Biochem. Soc. Trans. 29 2001 598 601
7. D.E. Warschawski, A.A. Arnold, M. Beaugrand, A. Gravel, É. Chartrand, and I. Marcotte Choosing membrane mimetics for NMR structural studies of transmembrane proteins Biochim. Biophys. Acta 1808 2011 1957 1974
8. H. Jenssen, P. Hamill, and R.E.W. Hancock Peptide antimicrobial agents Clin. Microbiol. Rev. 19 2006 491 511
9. A. Arouri, M. Dathe, and A. Blume Peptide induced demixing in PG/PE lipid mixtures: a mechanism for the specificity of antimicrobial peptides towards bacterial membranes? Biochim. Biophys. Acta 1788 2009 650 659
10. J.H. Davis, C.P. Nichol, G. Weeks, and M. Bloom Study of the cytoplasmic and outer membranes of Escherichia coli by deuterium magnetic resonance Biochemistry 18 1979 2103 2112
11. 2H NMR as a method to study structure, dynamics, and interactions Acc. Chem. Res. 20 1987 221 228
12. E. Strandberg, and A.S. Ulrich NMR methods for studying membrane-active antimicrobial peptides Concepts Magn. Reson. 23 2004 89 120
13. I. Marcotte, K.L. Wegener, Y.-H. Lam, B.C.S. Chia, M.R.R. de Planque, J.H. Bowie, M. Auger, and F. Separovic Interaction of antimicrobial peptides from Australian amphibians with lipid membranes Chem. Phys. Lipids 122 2003 107 120
14. B. Bechinger, and E.S. Salnikov The membrane interactions of antimicrobial peptides revealed by solid-state NMR spectroscopy Chem. Phys. Lipids 165 2012 282 301
15. W. Dowhan, M. Bogdanov, and E. Mileykovskaya Functional roles of lipids in membranes D.E. Vance, J.E. Vance, Biochemistry of Lipids, Lipoproteins and Membranes 2008 Elsevier Amsterdam 1 37
16. M. Esfahani, E.M. Barnes, and S.J. Wakil Control of fatty acid composition in phospholipids of Escherichia coli: response to fatty acid supplements in a fatty acid auxotroph Proc. Natl. Acad. Sci. U. S. A. 64 1969 1057 1064
17. 2H-NMR study of Acholeplasma laidlawii membranes highly enriched in myristic acid Biochim. Biophys. Acta 688 1982 622 636
18. C.P. Nichol, J.H. Davis, G. Weeks, and M. Bloom Quantitative study of the fluidity of Escherichia coli membranes using deuterium magnetic resonance Biochemistry 19 1980 451 457
19. 2H solid-state NMR investigation of whole Escherichia coli interacting with antimicrobial peptide MSI-78 Biochemistry 51 2012 118 125
20. M. Sinensky Temperature control of phospholipid biosynthesis in Escherichia coli J. Bacteriol. 106 1971 449 455
21. J.-B. Pouvreau, M. Morançais, F. Fleury, P. Rosa, L. Thio, B. Cahingt, F. Zal, J. Fleurence, and P. Pondaven Preliminary characterisation of the blue-green pigment "marennine" from the marine 108 tychopelagic diatom Haslea ostrearia (Gaillon/Bory) Simonsen J. Appl. Phycol. 18 2006 757 767
22. J.-L. Mouget, P. Rosa, C. Vachoux, and G. Tremblin Enhancement of marennine production by blue light in the diatom Haslea ostrearia J. Appl. Phycol. 17 2005 437 445
23. R. Gastineau, J.-B. Pouvreau, C. Hellio, M. Morançais, J. Fleurence, P. Gaudin, N. Bourgougnon, and J.-L. Mouget Biological activities of purified marennine, the blue pigment responsible for the greening of oysters J. Agric. Food Chem. 60 2012 3599 3605
24. R. Gastineau, Biodiversité, reproduction et phylogénie des diatomées bleues du genre Haslea et valorisation de leurs pigments de type marennine, in: Département de Biologie, vol. PhD, Université du Maine, Le Mans, 2011, pp. 328.
25. A. Clausell, M. Pujol, M.A. Alsina, and Y. Cajal Influence of polymyxins on the structural dynamics of Escherichia coli lipid membranes Talanta 60 2003 225 234
26. 2H-NMR study on the structural perturbations induced by charged detergents in the headgroup region of phosphatidylcholine bilayers Biochim. Biophys. Acta 855 1986 365 374
27. P.P. Brisebois, A.A. Arnold, Y.M. Chabre, R. Roy, and I. Marcotte Comparative study of the interaction of fullerenol nanoparticles with eukaryotic and bacterial model membranes using solid-state NMR and FTIR spectroscopy Eur. Biophys. J. 41 2012 535 544
28. F. Pernet, and R. Tremblay Effect of ultrasonication and grinding on the determination of lipid class content of microalgae harvested on filters Lipids 38 2003 1191 1195
29. Y. Marty, F. Delaunay, J. Moal, and J.-F. Samain Changes in the fatty acid composition of Pecten maximus (L.) during larval development J. Exp. Mar. Biol. Ecol. 163 1992 221 234
30. H. Wang, H. Cheng, F. Wang, D. Wei, and X. Wang An improved 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) reduction assay for evaluating the viability of Escherichia coli cells J. Microbiol. Methods 82 2010 330 333
31. J.H. Davis, K.R. Jeffrey, M. Bloom, M.I. Valic, and T.P. Higgs Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains Chem. Phys. Lett. 42 1976 390 394
32. J.D. van Beek matNMR: a flexible toolbox for processing, analyzing and visualizing magnetic resonance data in Matlab® J. Magn. Reson. 187 2007 19 26
33. J.H. Davis Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine Biophys. J. 27 1979 339 358
34. 2H-NMR Biochim. Biophys. Acta 737 1983 117 171
35. J. Seelig, and A. Seelig Lipid conformation in model membranes and biological membranes Q. Rev. Biophys. 13 1980 19 61
36. M.L. Nelson, M.C. Grier, S.E. Barbaro, and M.Y. Ismail Polyfunctional antibiotics affecting bacterial membrane dynamics Anti-Infect. Agents Med. Chem. 8 2009 3 16
37. D.F. Silbert, F. Ruch, and P.R. Vagelos Fatty acid replacements in a fatty acid auxotroph of Escherichia coli J. Bacteriol. 95 1968 1658 1665
38. R.D. Mavis, and P.R. Vagelos The effect of phospholipid fatty acid composition on membranous enzymes in Escherichia coli J. Biol. Chem. 247 1972 652 659
39. S. Morein, A.-S. Andersson, L. Rilfors, and G. Lindblom Wild-type Escherichia coli cells regulate the membrane lipid composition in a window between gel and non-lamellar structures J. Biol. Chem. 271 1996 6801 6809
40. D.M. Byers, and Z. Shen Biochemical evidence against protein-mediated uptake of myristic acid in the bioluminescent marine bacterium Vibrio harveyi Can. J. Microbiol. 48 2002 933 939
41. Y.-M. Zhang, and C.O. Rock Membrane lipid homeostasis in bacteria Nat. Rev. 6 2008 222 233
42. Y. Jiang, R.M. Morgan-Kiss, J.W. Campbell, C.H. Chan, and J.E. Cronan Expression of Vibrio harveyi Acyl-ACP synthetase allows efficient entry of exogenous fatty acids into the Escherichia coli fatty acid and lipid A synthetic pathways Biochemistry 49 2010 718 726
43. M.K. Shaw, and J.L. Ingraham Fatty acid composition of Escherichia coli as a possible controlling factor of the minimal growth temperature J. Bacteriol. 90 1965 141 146
44. T. Kobayashi, M. Nishijima, Y. Tamori, S. Nojima, Y. Seyama, and T. Yamakawa Acyl phosphatidylglycerol of Escherichia coli Biochim. Biophys. Acta 620 1980 356 363
45. A.G. Rietveld, J.A. Killian, W. Dowhan, and B. de Kruijff Polymorphic regulation of membrane phospholipid composition in Escherichia coli J. Biol. Chem. 268 1993 12427 12433
46. P.B.W. Smith, A.P. Snyder, and C.S. Harden Characterization of bacterial phospholipids by electrospray ionization tandem mass spectrometry Anal. Chem. 67 1995 1824 1830
47. T. Ivancic, M. Vodovnik, R. Marinsek-Logar, and D. Stopar Conditioning of the membrane fatty acid profile of Escherichia coli during periodic temperature cycling Microbiology 155 2009 3461 3463
48. M.C. Mansilla, L.E. Cybulski, D. Albanesi, and D. de Mendoza Control of membrane lipid fluidity by molecular thermosensors J. Bacteriol. 186 2004 6681 6688
49. D.M. Byers Elongation of exogenous fatty acids by the bioluminescent bacterium Vibrio harveyi J. Bacteriol. 171 1989 59 64
50. M.H.W. Weber, W. Klein, L. Muller, and U.M. NiesMarahiel Role of Bacillus subtilis fatty acid desaturase in membrane adaptation during cold shock Mol. Microbiol. 39 2001 1321 1329
51. M. Esfahani, T. Ioneda, and S.J. Wakil Studies on the control of fatty acid metabolism III. Incorporation of fatty acids into phospholipids and regulation of fatty acid synthetase of Escherichia coli J. Biol. Chem. 246 1971 50 56
52. H.H. Mantsch, P.W. Yang, A. Martin, and D.G. Cameron Infrared spectroscopic studies of Acholeplasma laidlawii B membranes Eur. J. Biochem. 178 1988 335 341
53. 31P NMR study of the interaction of amphibian antimicrobial peptides with the membranes of live bacteria Lett. Pept. Sci. 7 2000 151 156
54. A.H. Delcour Outer membrane permeability and antibiotic resistance Biochim. Biophys. Acta 1724 2009 808 819
55. 24 induced tissue factor and ICAM-1 membrane expression and apoptosis in vitro Int. J. Nanomedicine 3 2008 59 68
56. H. Aoshima, K.E.N. Kokubo, S. Shirakawa, M. Ito, S. Yamana, and T. Oshima Antimicrobial activity of fullerenes and their hydroxylated derivatives Biocontrol Sci. 14 2009 69 72
57. B. Ahlström, M. Chelminska-Bertilsson, R.A. Thompson, and L. Edebo Submicellar complexes may initiate the fungicidal effects of cationic amphiphilic compounds on Candida albicans Antimicrob. Agents Chemother. 41 1997 544 550
58. W.G. Salt, and D. Wiseman The relation between the uptake of cetyltrimethylammonium bromide by Escherichia coli and its effects on cell growth J. Pharm. Pharmacol. 22 1970 261 264
59. R.E. Glover, R.R. Smith, M.V. Jones, S.K. Jackson, and C.C. Rowlands An EPR investigation of surfactant action on bacterial membranes FEMS Microbiol. Lett. 177 1999 57 62
60. L. Marcotte, J. Barbeau, and M. Lafleur Permeability and thermodynamics study of quaternary ammonium surfactants - phosphocholine vesicle system J. Colloid Interface Sci. 292 2005 219 227
61. M. Almgren Mixed micelles and other structures in the solubilization of bilayer lipid membranes by surfactants Biochim. Biophys. Acta 1508 2000 146 163
62. R.M. Epand, and R.F. Epand Bacterial membrane lipids in the action of antimicrobial agents J. Pept. Sci. 17 2011 298 305
63. P.J. Sherman, R.J. Jackway, J.D. Gehman, S. Praporski, G.A. McCubbin, A. Mechler, L.L. Martin, F. Separovic, and J.H. Bowie Solution structure and membrane interactions of the antimicrobial peptide fallaxidin 4.1a: an NMR and QCM study Biochemistry 48 2009 11892 11901
64. S. Vanounou, A.H. Parola, and I. Fishov Phosphatidylethanolamine and phosphatidylglycerol are segregated into different domains in bacterial membrane. A study with pyrene-labelled phospholipids Mol. Microbiol. 49 2003 1067 1079