Interaction of the Antimicrobial Peptide Polymyxin B1 with Both Membranes of E. coli: A Molecular Dynamics Study

PLoS Computational Biology

Volumn 11, Issue 4, 2015, Pages

  Berglund, Nils A ^a,b   Piggot, Thomas J ^a   Jefferies, Damien ^a   Sessions, Richard B ^c   Bond, Peter J ^b,d   Khalid, Syma ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b BIOINFORMATICS INSTITUTE   (Singapore)

^c School of Biochemistry   (United Kingdom)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; ESCHERICHIA COLI; MOLECULAR DYNAMICS; PEPTIDES;

ANTIMICROBIAL PEPTIDE; BACTERIAL CELLS; CATIONIC PROTEINS; CELL LYSIS; DIFFERENT MECHANISMS; DYNAMIC STUDIES; E. COLI; INNER MEMBRANES; LIPOPEPTIDES; OUTER MEMBRANE;

MEMBRANES;

LIPID A; LIPOPOLYSACCHARIDE; POLYMYXIN DERIVATIVE; POLYMYXIN; POLYMYXIN B(1);

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; ESCHERICHIA COLI; HYDRATION; INNER MEMBRANE; MEMBRANE STABILIZATION; MOLECULAR DYNAMICS; NONHUMAN; OUTER MEMBRANE; PROTEIN AGGREGATION; PROTEIN INTERACTION; ANALOGS AND DERIVATIVES; BIOLOGY; CELL MEMBRANE; CHEMISTRY; METABOLISM;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

CELL MEMBRANE; COMPUTATIONAL BIOLOGY; ESCHERICHIA COLI; LIPOPOLYSACCHARIDES; MOLECULAR DYNAMICS SIMULATION; POLYMYXINS;

EID: 84929493561     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004180     Document Type: Article

References (72)

1. Kraemer BF, Campbell RA, Schwertz H, Cody MJ, Franks Z, Tolley ND, et al. Novel Anti-bacterial Activities of beta-defensin 1 in Human Platelets: Suppression of Pathogen Growth and Signaling of Neutrophil Extracellular Trap Formation. Plos Pathogens. 2011;7(11).
2. Kimura Y, Matsunaga H, Vaara M, Polymyxin B-Octapeptide and Polymyxin B-Heptapeptide Are Potent Outer-Membrane Permeability-Increasing Agents. Journal of Antibiotics. 1992;45(5):742–9. 1624376
3. Izadpanah A, Gallo RL, Antimicrobial peptides. Journal of the American Academy of Dermatology. 2005;52(3):381–92. 15761415
4. Storm DR, Rosenthal KS, Swanson PE, Polymyxin and Related Peptide Antibiotics. Annual Review of Biochemistry. 1977;46:723–63. 197881
5. Rosenthal KS, Storm DR, Disruption of Escherichia-Coli Outer Membrane-Permeability Barrier by Immobilized Polymyxin-B. Journal of Antibiotics. 1977;30(12):1087–92. 202585
6. Velkov T, Thompson PE, Nation RL, Li J, Structure-Activity Relationships of Polymyxin Antibiotics. Journal of Medicinal Chemistry. 2010;53(5):1898–916. doi: 10.1021/jm900999h 19874036
7. Sud IJ, Feingold DS, Mechanism of polymyxin B resistance in Proteus mirabilis. J Bacteriol. 1970;104(1):289–94. 4319722
8. Falagas ME, Kasiakou SK, Toxicity of polymyxins: a systematic review of the evidence from old and recent studies. Critical care. 2006;10(1).
9. Abdelraouf K, Braggs KH, Yin T, Truong LD, Hu M, Tam VH, Characterization of polymyxin B-induced nephrotoxicity: implications for dosing regimen design. Antimicrobial agents and chemotherapy. 2012;56(9):4625–9. doi: 10.1128/AAC.00280-12 22687519
10. Landman D, Georgescu C, Don Antonio M, Quale J, Polymyxins Revisited. Clin Microb Rev. 2008;21(3):449–65. doi: 10.1128/CMR.00006-08 18625681
11. Falagas ME, Kasiakou SK, Colistin: The revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clinical Infectious Diseases. 2005;40(9):1333–41. 15825037
12. Kanazawa K, Sato Y, Ohki K, Okimura K, Uchida Y, Shindo M, et al. Contribution of each amino acid residue in polymyxin B(3) to antimicrobial and lipopolysaccharide binding activity. Chemical & pharmaceutical bulletin. 2009;57(3):240–4.
13. Morrison DC, Jacobs DM, Binding of polymyxin B to the lipid A portion of bacterial lipopolysaccharides. Immunochemistry. 1976;13(10):813–8. 187544
14. Bond PJ, Khalid S, Antimicrobial and Cell-Penetrating Peptides: Structure, Assembly and Mechanisms of Membrane Lysis via Atomistic and Coarse-Grained Molecular Dynamic Simulations. Protein Peptide Lett. 2010;17(11):1313–27. 20673230
15. Bond PJ, Parton DL, Clark JF, Sansom MS, Coarse-grained simulations of the membrane-active antimicrobial Peptide maculatin 1.1. Biophys J. 2008;95(8):3802–15. doi: 10.1529/biophysj.108.128686 18641064
16. Ravi HK, Stach M, Soares TA, Darbre T, Reymond JL, Cascella M, Electrostatics and flexibility drive membrane recognition and early penetration by the antimicrobial peptide dendrimer bH1. Chemical communications. 2013;49(78):8821–3. doi: 10.1039/c3cc44912b 23959139
17. La Rocca P, Biggin PC, Tieleman DP, Sansom MSP, Simulation studies of the interaction of antimicrobial peptides and lipid bilayers. Bba-Biomembranes. 1999;1462(1–2):185–200. 10590310
18. Leontiadou H, Mark AE, Marrink SJ, Antimicrobial peptides in action. Journal of the American Chemical Society. 2006;128(37):12156–61. 16967965
19. Shepherd CM, Vogel HJ, Tieleman DP, Interactions of the designed antimicrobial peptide MB21 and truncated dermaseptin S3 with lipid bilayers: molecular-dynamics simulations. The Biochemical journal. 2003;370(Pt 1):233–43. 12423203
20. Lins RD, Straatsma TP, Computer simulation of the rough lipopolysaccharide membrane of Pseudomonas aeruginosa. Biophys J. 2001;81(2):1037–46. 11463645
21. Lins RD, Vorpagel ER, Guglielmi M, Straatsma TP, Computer simulation of uranyl uptake by the rough lipopolysaccharide membrane of Pseudomonas aeruginosa. Biomacromolecules. 2008;9(1):29–35. 18067253
22. Obst S, Kastowsky M, Bradaczek H, Molecular dynamics simulations of six different fully hydrated monomeric conformers of Escherichia coli re-lipopolysaccharide in the presence and absence of Ca2+. Biophys J. 1997;72(3):1031–46. 9138554
23. Soares TA, Straatsma TP, Assessment of the convergence of molecular dynamics simulations of lipopolysaccharide membranes. Molecular Simulations. 2008;34(3):295–307.
24. Lad MD, Birembaut F, Clifton LA, Frazier RA, Webster JR, Green RJ, Antimicrobial peptide-lipid binding interactions and binding selectivity. Biophys J. 2007;92(10):3575–86. 17325007
25. Moore RA, Bates NC, Hancock RE, Interaction of polycationic antibiotics with Pseudomonas aeruginosa lipopolysaccharide and lipid A studied by using dansyl-polymyxin. Antimicrobial agents and chemotherapy. 1986;29(3):496–500. 3013085
26. Mares J, Kumaran S, Gobbo M, Zerbe O, Interactions of Lipopolysaccharide and Polymyxin Studied by NMR Spectroscopy. J Biol Chem. 2009;284(17):11498–506. doi: 10.1074/jbc.M806587200 19244241
27. Piggot TJ, Holdbrook DA, Khalid S, Electroporation of the E. coli and S. aureus Membranes: Molecular Dynamics Simulations of Complex Bacterial Membranes. J Phys Chem B. 2011;115(45):13381–8. doi: 10.1021/jp207013v 21970408
28. Koldso H, Shorthouse D, Helie J, Sansom MS, Lipid clustering correlates with membrane curvature as revealed by molecular simulations of complex lipid bilayers. PLoS computational biology. 2014;10(10):e1003911. doi: 10.1371/journal.pcbi.1003911 25340788
29. Boggs JM, Wang HY, Rangaraj G, Tummler B, Interdigitation of phosphatidylcholine and phosphatidylethanolamine mixed with complexes of acidic lipids and polymyxin B or polymyxin B nonapeptide. Biochimica et biophysica acta. 1989;985(2):199–210. 2553118
30. Theretz A, Ranck JL, Tocanne JF, Polymyxin B-induced phase separation and acyl chain interdigitation in phosphatidylcholine/phosphatidylglycerol mixtures. Biochim Biophys Acta. 1983;732(3):499–508. 6307373
31. Schindler M, Osborn MJ, Interaction of divalent cations and polymyxin B with lipopolysaccharide. Biochemistry-Us. 1979;18(20):4425–30. 226126
32. Velkov T, Roberts KD, Nation RL, Thompson PE, Li J, Pharmacology of polymyxins: new insights into an 'old' class of antibiotics. Future microbiology. 2013;8(6):711–24. doi: 10.2217/fmb.13.39 23701329
33. Domingues MM, Inacio RG, Raimundo JM, Martins M, Castanho MA, Santos NC, Biophysical characterization of polymyxin B interaction with LPS aggregates and membrane model systems. Biopolymers. 2012;98(4):338–44. 23193598
34. Mecke A, Lee DK, Ramamoorthy A, Orr BG, Banaszak Holl MM, Membrane thinning due to antimicrobial peptide binding: an atomic force microscopy study of MSI-78 in lipid bilayers. Biophysical journal. 2005;89(6):4043–50. 16183881
35. Neale C, Bennett WFD, Tieleman DP, Pomes R, Statistical Convergence of Equilibrium Properties in Simulations of Molecular Solutes Embedded in Lipid Bilayers. Journal of Chemical Theory and Computation. 2011;7(12):4175–88.
36. Wang Y, Zhao T, Wei D, Strandberg E, Ulrich AS, Ulmschneider JP, How reliable are molecular dynamics simulations of membrane active antimicrobial peptides? Biochim Biophys Acta. 2014;1838(9):2280–8. doi: 10.1016/j.bbamem.2014.04.009 24747526
37. Rzepiela AJ, Sengupta D, Goga N, Marrink SJ, Membrane poration by antimicrobial peptides combining atomistic and coarse-grained descriptions. Faraday Discuss. 2010;144:431–43; discussion 45–81. 20158042
38. Horn JN, Sengillo JD, Lin D, Romo TD, Grossfield A, Characterization of a potent antimicrobial lipopeptide via coarse-grained molecular dynamics. Biochim Biophys Acta. 2012;1818(2):212–8. doi: 10.1016/j.bbamem.2011.07.025 21819964
39. Raetz CRH, Biochemistry of Endotoxins. Annu Rev Biochem. 1990;59(1):129–70.
40. Raetz CRH, Whitfield C, Lipolysaccharide Endotoxins. Annu Rev Biochem. 2002;71(1):635–700.
41. Holdbrook DA, Piggot TJ, Sansom MSP, Khalid S, Stability and membrane interactions of an autotransport protein: MD simulations of the Hia translocator domain in a complex membrane environment. BBA—Biomembranes. 2013;1828(2):715–23.
42. Lugtenberg EJJ, Peters R, Distribution of lipids in cytoplasmic and outer membranes of Escherichia coli K12. BBA—Lipid Lipid Met. 1976;441(1):38–47.
43. Aibara S, Kato M, Ishinaga M, Kito M, Changes in positional distribution of fatty acids in the phospholipids of Escherichia coli after shift-down in temperature. BBA—Lipid Lipid Met. 1972;270(3):301–6.
44. Kito M, Ishinaga M, Nishihara M, Kato M, Hata T, Sawada S, Metabolism of the Phosphatidylglycerol Molecular Species in Escherichia coli. Eur J Biochem. 1975;54(1):55–63. 1097251
45. Yokota K, Kanamoto R, Kito M, Composition of cardiolipin molecular species in Escherichia coli. J Bacteriol. 1980;141(3):1047–51. 6988400
46. Marrink SJ, de Vries AH, Mark AE, Coarse Grained Model for Semiquantitative Lipid Simulations. J Phys Chem B. 2003;108(2):750–60.
47. Dahlberg M, Maliniak A, Mechanical Properties of Coarse-Grained Bilayers Formed by Cardiolipin and Zwitterionic Lipids. J Chem Theory Comput. 2010;6(5):1638–49.
48. Brocos P, Mendoza-Espinosa P, Castillo R, Mas-Oliva J, Pineiro A, Multiscale molecular dynamics simulations of micelles: coarse-grain for self-assembly and atomic resolution for finer details. Soft Matter. 2012;8(34):9005–14.
49. Hausmann W, Craig LC, Polymyxin B1.1 Fractionation, Molecular Weight Determination, Amino Acid and Fatty Acid Composition. J Am Chem Soc. 1954;76(19):4892–6.
50. Wilkinson S, Lowe LA, Structure of Polymyxin B1. Nature. 1964;202(4938):1211-.
51. Hanwell M, Curtis D, Lonie D, Vandermeersch T, Zurek E, Hutchison G, Avogadro: an advanced semantic chemical editor, visualization, and analysis platform. Journal of Cheminformatics. 2012;4(1):17. doi: 10.1186/1758-2946-4-17 22889332
52. Humphrey W, Dalke A, Schulten K, VMD: Visual molecular dynamics. J Mol Graphics. 1996;14(1):33–8. 8744570
53. Berendsen HJC, van der Spoel D, van Drunen R, GROMACS: A message-passing parallel molecular dynamics implementation. Comput Phys Commun. 1995;91(1–3):43–56.
54. van der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJC, GROMACS: Fast, flexible, and free. J Comput Chem. 2005;26(16):1701–18. 16211538
55. Pronk S, Páll S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, et al. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics. 2013;29(7):845–54. doi: 10.1093/bioinformatics/btt055 23407358
56. Oostenbrink C, Villa A, Mark AE, van Gunsteren WF, A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6. J Comput Chem. 2004;25(13):1656–76. 15264259
57. Piggot TJ, Holdbrook DA, Khalid S, Conformational dynamics and membrane interactions of the E. coli outer membrane protein FecA: A molecular dynamics simulation study. BBA—Biomembranes. 2013;1828(2):284–93.
58. Chandrasekhar I, Kastenholz M, Lins RD, Oostenbrink C, Schuler LD, Tieleman DP, et al. A consistent potential energy parameter set for lipids: dipalmitoylphosphatidylcholine as a benchmark of the GROMOS96 45A3 force field. Eur Biophys J. 2003;32(1):67–77. 12632209
59. Kukol A, Lipid Models for United-Atom Molecular Dynamics Simulations of Proteins. J Chem Theory Comput. 2009;5(3):615–26.
60. Piggot TJ, Piñeiro Á, Khalid S, Molecular Dynamics Simulations of Phosphatidylcholine Membranes: A Comparative Force Field Study. J Chem Theory Comput. 2012;8(11):4593–609.
61. Berendsen H, Postma J, van Gunsteren W, Hermans J, Pullman B, Interaction Models for Water in Relation to Protein Hydration. In: Intermolecular Forces: D. Reidel Publishing Company; 1981. p. 331–42.
62. Nosé S, A molecular dynamics method for simulations in the canonical ensemble. Mol Phys. 1984;52(2):255–68.
63. Hoover WG, Canonical dynamics: Equilibrium phase-space distributions. Phys Rev A. 1985;31(3):1695–7. 9895674
64. Emmerling G, Henning U, Gulik-Krzywicki T, Order-Disorder Conformational Transition of Hydrocarbon Chains in Lipopolysaccharide from Escherichia coli. Eur J Biochem. 1977;78(2):503–9. 21082
65. Van Alphen L, Lugtenberg B, Rietschel ET, Mombers C, Architecture of the Outer Membrane of Escherichia coli K12. Eur J Biochem. 1979;101(2):571–9. 391560
66. Brandenburg K, Seydel U, Physical aspects of structure and function of membranes made from lipopolysaccharides and free lipid A. BBA—Biomembranes. 1984;775(2):225–38.
67. Brandenburg K, Funari SS, Koch MHJ, Seydel U, Investigation into the Acyl Chain Packing of Endotoxins and Phospholipids under Near Physiological Conditions by WAXS and FTIR Spectroscopy. J Struct Biol. 1999;128(2):175–86. 10600571
68. Overath P, Traeuble H, Phase transitions in cells, membranes, and lipids of Escherichia coli. Detection by fluorescent probes, light scattering, and dilatometry. Biochemistry. 1973;12(14):2625–34. 4576094
69. Parrinello M, Rahman A, Polymorphic transitions in single crystals: A new molecular dynamics method. J Appl Phys. 1981;52(12):7182–90.
70. Nosé S, Klein ML, Constant pressure molecular dynamics for molecular systems. Mol Phys. 1983;50(5):1055–76.
71. Essmann U, Perera L, Berkowitz M, Darden T, Lee H, Pedersen L, A smooth particle mesh Ewald method. J Chem Phys. 1995;103(19):8577–93.
72. Hess B, P-LINCS: A Parallel Linear Constraint Solver for Molecular Simulation. J Chem Theory Comput. 2007;4(1):116–22.