Coarse-grained molecular dynamics simulation of interactions between cyclic lipopeptide Bacillomycin D and cell membranes

References

• Walsh C. Antibiotics : actions, origins, resistance. Washington (DC): ASM Press; 2003.10.1128/9781555817886
   Google Scholar
• Palumbi SR. Humans as the world’s greatest evolutionary force. Science. 2001 Sep 7;293(5536):1786–1790. DOI:10.1126/science.293.5536.1786. PubMed PMID: 11546863; eng.
   PubMed Web of Science ®Google Scholar
• von Nussbaum F, Brands M, Hinzen B, et al. Antibacterial natural products in medicinal chemistry – exodus or revival? Angew Chem Int Ed. 2006 Aug 4;45(31):5072–5129. DOI:10.1002/anie.200600350 . PubMed PMID: 16881035.
   PubMed Web of Science ®Google Scholar
• Arnusch CJ, Ulm H, Josten M, et al. Ultrashort peptide bioconjugates are exclusively antifungal agents and synergize with cyclodextrin and amphotericin B. Antimicrob Agents Chemother. 2012 Jan;56(1):1–9. DOI:10.1128/AAC.00468-11. PubMed PMID: 22006001; PubMed Central PMCID: PMCPMC3256016.
   PubMed Web of Science ®Google Scholar
• Cho S-J, Lee SK, Cha BJ, et al. Detection and characterization of the Gloeosporium gloeosporioides growth inhibitory compound iturin A from Bacillus subtilis strain KS03. FEMS Microbiol Lett. 2003;223(1):47–51.10.1016/S0378-1097(03)00329-X
   PubMed Web of Science ®Google Scholar
• Phister TG, O’Sullivan DJ, McKay LL. Identification of bacilysin, chlorotetaine, and iturin A produced by Bacillus sp. Strain CS93 isolated from pozol, a Mexican fermented maize dough. Appl Environ Microbiol. 2004;70(1):631–634.10.1128/AEM.70.1.631-634.2004
   PubMed Web of Science ®Google Scholar
• Yu G, Sinclair J, Hartman G, et al. Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem. 2002;34(7):955–963.10.1016/S0038-0717(02)00027-5
   Web of Science ®Google Scholar
• Bonmatin J-M, Laprévote O, Peypoux F. Diversity among microbial cyclic lipopeptides: iturins and surfactins. Activity-Structure Relationships to design new bioactive agents. Comb Chem High Throughput Screening. 2003;6(6):541–556.10.2174/138620703106298716
   PubMed Web of Science ®Google Scholar
• Seydlová G, Svobodová J. Review of surfactin chemical properties and the potential biomedical applications. Open Med. 2008;3(2):123–133.
   Google Scholar
• Shaligram NS, Singhal RS. Surfactin – a review on biosynthesis, fermentation, purification and applications. Food Technol Biotechnol. 2010;48(2):119–134.
   Web of Science ®Google Scholar
• Honma M, Tanaka K, Konno K, et al. Termination of the structural confusion between plipastatin A1 and fengycin IX. Bioorg Med Chem. 2012;20(12):3793–3798.10.1016/j.bmc.2012.04.040
   PubMed Web of Science ®Google Scholar
• Nishikiori T, Naganawa H, Muraoka Y, et al. Plipastatins: new inhibitors of phospholipase A2, produced by Bacillus cereus BMG302-fF67. III. Structural elucidation of plipastatins. J Antibiot. 1986;39(6):755–761.10.7164/antibiotics.39.755
   PubMed Web of Science ®Google Scholar
• Bie X, Lu Z, Lu F. Identification of fengycin homologues from Bacillus subtilis with ESI-MS/CID. J Microbiol Methods. 2009;79(3):272–278.10.1016/j.mimet.2009.09.013
   PubMed Web of Science ®Google Scholar
• Vanittanakom N, Loeffler W, Koch U, et al. Fengycin – a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J Antibiotics. 1986;39(7):888–901.10.7164/antibiotics.39.888
   PubMed Web of Science ®Google Scholar
• Villegas-Escobar V, Ceballos I, Mira JJ, et al. Fengycin C produced by Bacillus subtilis EA-CB0015. J Nat Prod. 2013;76(4):503–509.10.1021/np300574v
   PubMed Web of Science ®Google Scholar
• Peypoux F, Besson F, Michel G, et al. Structure of Bacillomycin D, a new antibiotic of the iturin group. FEBS J. 1981;118(2):323–327.
   Google Scholar
• Etchegaray A, Castro Bueno C, Melo IS, et al. Effect of a highly concentrated lipopeptide extract of Bacillus subtilis on fungal and bacterial cells. Arch Microbiol. 2008;190(6):611–622. DOI:10.1007/s00203-008-0409-z.
   PubMed Web of Science ®Google Scholar
• Tenoux I, Besson F, Michel G. Studies on Bacillomycin D biosynthesis by Bacillus subtilis. Microbios. 1993;74(298):29–37 . PubMed PMID: 8336553.
   PubMedGoogle Scholar
• Besson F, Peypoux F, Michel G. Action of mycosubtilin and of Bacillomycin L on Micrococcus luteus cells and protoplasts influence of the polarity of the antibiotics upon their action on the bacterial cytoplasmic membrane. FEBS Lett. 1978 Jun 1;90(1):36–40. PubMed PMID: 658439.10.1016/0014-5793(78)80292-0
   PubMed Web of Science ®Google Scholar
• Cochrane SA, Vederas JC. Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Med Res Rev. 2016 Jan;36(1):4–31. DOI:10.1002/med.21321. PubMed PMID: WOS:000366598600002.
   PubMed Web of Science ®Google Scholar
• Pastor RW, Feller SE. Time scales of lipid dynamics and molecular dynamics. In: Merz KM, Roux B, editors. Biological membranes: a molecular perspective from computation and experiment. Boston (MA): Birkhäuser Boston; 1996. p. 3–29.10.1007/978-1-4684-8580-6
   Google Scholar
• Bolintineanu DS, Kaznessis YN. Computational studies of protegrin antimicrobial peptides: a review. Peptides. 2011 Jan;32(1):188–201. DOI:10.1016/j.peptides.2010.10.006. PubMed PMID: 20946928; PubMed Central PMCID: PMCPMC3013618.
   PubMed Web of Science ®Google Scholar
• Li J, Koh J-J, Liu S, et al. Membrane active antimicrobial peptides: translating mechanistic insights to design. Front Neurosci. 2017;11.
   Web of Science ®Google Scholar
• Li ZL, Ding HM, Ma YQ. Interaction of peptides with cell membranes: insights from molecular modeling. J Phys: Condens Matter. 2016;28(8):083001.
   PubMed Web of Science ®Google Scholar
• Marín-Medina N, Ramírez DA, Trier S, et al. Mechanical properties that influence antimicrobial peptide activity in lipid membranes. Appl Microbiol Biotechnol. 2016;100(24):10251–10263.10.1007/s00253-016-7975-9
   PubMed Web of Science ®Google Scholar
• MacCallum JL, Bennett WD, Tieleman DP. Distribution of amino acids in a lipid bilayer from computer simulations. Biophys J. 2008;94(9):3393–3404.10.1529/biophysj.107.112805
   PubMed Web of Science ®Google Scholar
• Tieleman DP, Berendsen HJ, Sansom MS. An alamethicin channel in a lipid bilayer: molecular dynamics simulations. Biophys J. 1999;76(4):1757–1769.10.1016/S0006-3495(99)77337-6
   PubMed Web of Science ®Google Scholar
• Tieleman DP, Hess B, Sansom MS. Analysis and evaluation of channel models: simulations of alamethicin. Biophys J. 2002;83(5):2393–2407.10.1016/S0006-3495(02)75253-3
   PubMed Web of Science ®Google Scholar
• Cirac AD, Moiset G, Mika JT, et al. The molecular basis for antimicrobial activity of pore-forming cyclic peptides. Biophys J. 2011;100(10):2422–2431.10.1016/j.bpj.2011.03.057
   PubMed Web of Science ®Google Scholar
• Zasloff M. Antimicrobial peptides of multicellular organisms. Nature. 2002;415(6870):389–395.10.1038/415389a
   PubMed Web of Science ®Google Scholar
• Brogden KA. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol. 2005;3(3):238–250.10.1038/nrmicro1098
   PubMed Web of Science ®Google Scholar
• Groot RD, Warren PB. Dissipative particle dynamics: bridging the gap between atomistic and mesoscopic simulation. J Chem Phys. 1997;107(11):4423–4435. DOI:10.1063/1.474784.
   Web of Science ®Google Scholar
• Marrink SJ, Risselada HJ, Yefimov S, et al. The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B. 2007 Jul 12;111(27):7812–7824. DOI:10.1021/jp071097f. PubMed PMID: WOS:000247761600015.
   PubMed Web of Science ®Google Scholar
• Milano G, Kawakatsu T. Hybrid particle-field molecular dynamics simulations for dense polymer systems. J Chem Phys. 2009 Jun 7;130(21). DOI:Artn 214106 10.1063/1.3142103. PubMed PMID: WOS:000266674400007; English.
   PubMed Web of Science ®Google Scholar
• Rodgers JM, Sorensen J, de Meyer FJM, et al. Understanding the phase behavior of coarse-grained model lipid bilayers through computational calorimetry. J Phys Chem B. 2012 Feb 9;116(5):1551–1569. DOI:10.1021/jp207837v. PubMed PMID: WOS:000299985200010.
   PubMed Web of Science ®Google Scholar
• Baoukina S, Tieleman DP. Direct simulation of protein-mediated vesicle fusion: lung surfactant protein B. Biophys J. 2010 Oct 6;99(7):2134–2142. DOI:10.1016/j.bpj.2010.07.049. PubMed PMID: WOS:000282850600018.
   PubMed Web of Science ®Google Scholar
• Rosetti C, Pastorino C. Comparison of ternary bilayer mixtures with asymmetric or symmetric unsaturated phosphatidylcholine lipids by coarse grained molecular dynamics simulations. J Phys Chem B. 2012 Mar 22;116(11):3525–3537. DOI:10.1021/jp212406u. PubMed PMID: WOS:000301766700006.
   PubMed Web of Science ®Google Scholar
• Khalfa A, Tarek M. On the antibacterial action of cyclic peptides: insights from coarse-grained MD simulations. J Phys Chem B. 2010 Mar 4;114(8):2676–2684. DOI:10.1021/jp9064196. PubMed PMID: WOS:000274842600016.
   PubMed Web of Science ®Google Scholar
• de Jong DH, Singh G, Bennett WFD, et al. Improved parameters for the MARTINI coarse-grained protein force field. J Chem Theory Comput. 2013 Jan;9(1):687–697. DOI:10.1021/ct300646 g. PubMed PMID: WOS:000313378700069.
   PubMed Web of Science ®Google Scholar
• Horn JN, Sengillo JD, Lin D, et al. Characterization of a potent antimicrobial lipopeptide via coarse-grained molecular dynamics. Biochim Biophys Acta (BBA) – Biomembr. 2012 Feb;1818(2):212–218. DOI:10.1016/j.bbamem.2011.07.025. PubMed PMID: WOS:000300380000012.
   PubMed Web of Science ®Google Scholar
• Woo H-J, Wallqvist A. Spontaneous buckling of lipid bilayer and vesicle budding induced by antimicrobial peptide magainin 2: a coarse-grained simulation study. J Phys Chem B. 2011 Jun 30;115(25):8122–8129. DOI:10.1021/jp2023023. PubMed PMID: WOS:000291896200009.
   PubMed Web of Science ®Google Scholar
• Gkeka P, Sarkisov L. Spontaneous formation of a barrel-stave pore in a coarse-grained model of the synthetic LS3 peptide and a DPPC lipid bilayer. J Phys Chem B. 2009;113(1):6–8.10.1021/jp808417a
   PubMed Web of Science ®Google Scholar
• Polyansky AA, Ramaswamy R, Volynsky PE, et al. Antimicrobial peptides induce growth of phosphatidylglycerol domains in a model bacterial membrane. J Phys Chem Lett. 2010;1(20):3108–3111.10.1021/jz101163e
   Web of Science ®Google Scholar
• de Jong DH, Singh G, Bennett WD, et al. Improved parameters for the MARTINI coarse-grained protein force field. J Chem Theory Comput. 2012;9(1):687–697.
   PubMed Web of Science ®Google Scholar
• Monticelli L, Kandasamy SK, Periole X, et al. The MARTINI coarse-grained force field: extension to proteins. J Chem Theory Comput. 2008;4(5):819–834.10.1021/ct700324x
   PubMed Web of Science ®Google Scholar
• Yang J, Wang Y, Chen Y. GPU accelerated molecular dynamics simulation of thermal conductivities. J Comput Phys. 2007 Feb 10;221(2):799–804. DOI:10.1016/j.jcp.2006.06.039. PubMed PMID: WOS:000244463800018.
   Web of Science ®Google Scholar
• Stone JE, Phillips JC, Freddolino PL, et al. Accelerating molecular modeling applications with graphics processors. J Comput Chem. 2007 Dec;28(16):2618–2640. DOI:10.1002/jcc.20829. PubMed PMID: WOS:000250972500013.
   PubMed Web of Science ®Google Scholar
• Anderson JA, Lorenz CD, Travesset A. General purpose molecular dynamics simulations fully implemented on graphics processing units. J Comput Phys. 2008 May 1;227(10):5342–5359. DOI:10.1016/j.jcp.2008.01.047. PubMed PMID: WOS:000255447000027.
   Web of Science ®Google Scholar
• van Meel JA, Arnold A, Frenkel D, et al. Harvesting graphics power for MD simulations. Mol Simulat. 2008;34(3):259–266. DOI:10.1080/08927020701744295. PubMed PMID: WOS:000255991700003.
   Web of Science ®Google Scholar
• Periole X, Marrink SJ. The MARTINI coarse-grained force field. Methods Mol Biol. 2013;924:533–565. DOI:10.1007/978-1-62703-017-5_20 . PubMed PMID: 23034762.
   PubMedGoogle Scholar
• Zhao PC, Quan CS, Jin LM, et al. Effects of critical medium components on the production of antifungal lipopeptides from Bacillus amyloliquefaciens Q-426 exhibiting excellent biosurfactant properties. World J Microbiol Biotechnol. 2013 Mar;29(3):401–409. DOI:10.1007/s11274-012-1180-5. PubMed PMID: WOS:000314534200002; English.
   PubMed Web of Science ®Google Scholar
• Studio D. version 2.5; San Diego (CA): Accelrys.; 2009. 92121.
   Google Scholar
• Thimon L, Peyoux F, Maget-Dana R, et al. Surface-active properties of antifungal lipopeptides produced by Bacillus subtilis. J Am Oil Chem Soc. 1992;69(1):92–93.10.1007/BF02635884
   Web of Science ®Google Scholar
• Hamley IW. Lipopeptides: from self-assembly to bioactivity. Chem Commun. 2015;51(41):8574–8583.10.1039/C5CC01535A
   PubMed Web of Science ®Google Scholar
• Kirkham S, Castelletto V, Hamley IW, et al. Self-assembly of the cyclic lipopeptide daptomycin: spherical micelle formation does not depend on the presence of calcium chloride. ChemPhysChem. 2016;17(14):2118–2122.10.1002/cphc.v17.14
   PubMed Web of Science ®Google Scholar
• Wassenaar TA, Ingolfsson HI, Bockmann RA, et al. Computational lipidomics with insane: a versatile tool for generating custom membranes for molecular simulations. J Chem Theor Comput. 2015 May 12;11(5):2144–2155. DOI:10.1021/acs.jctc.5b00209 . PubMed PMID: 26574417.
   PubMed Web of Science ®Google Scholar
• Phillips JC, Braun R, Wang W, et al. Scalable molecular dynamics with NAMD. J Comput Chem. 2005 Dec;26(16):1781–1802. DOI:10.1002/jcc.20289. PubMed PMID: 16222654; PubMed Central PMCID: PMCPMC2486339.
   PubMed Web of Science ®Google Scholar
• Martyna GJ, Tobias DJ, Klein ML. Constant pressure molecular dynamics algorithms. J Chem Phys. 1994;101(5):4177–4189.10.1063/1.467468
   Web of Science ®Google Scholar
• Patel H, Tscheka C, Edwards K, et al. All-or-none membrane permeabilization by fengycin-type lipopeptides from Bacillus subtilis QST713. Biochim Biophys Acta (BBA) – Biomembr. 2011 Aug;1808(8):2000–2008. DOI:10.1016/j.bbamem.2011.04.008 . PubMed PMID: 21545788.
   PubMed Web of Science ®Google Scholar
• Horn JN, Cravens A, Grossfield A. Interactions between fengycin and model bilayers quantified by coarse-grained molecular dynamics. Biophys J. 2013 Oct 1;105(7):1612–1623. DOI:10.1016/j.bpj.2013.08.034. PubMed PMID: WOS:000325383000010; English.
   PubMed Web of Science ®Google Scholar
• Gao LH, Fang WH. Effects of induced tension and electrostatic interactions on the mechanisms of antimicrobial peptide translocation across lipid bilayer. Soft Matter. 2009;5(17):3312–3318. DOI:10.1039/b902971k. PubMed PMID: WOS:000269062900018; English.
   Web of Science ®Google Scholar
• Romo TD, Grossfield A. LOOS: an extensible platform for the structural analysis of simulations. Conf Proc IEEE Eng Med Biol Soc. 2009;2009:2332–2335. DOI:10.1109/IEMBS.2009.5335065 . PubMed PMID: 19965179.
   PubMedGoogle Scholar
• Dunkin CM, Pokorny A, Almeida PF, et al. Molecular dynamics studies of transportan 10 (Tp10) interacting with a POPC lipid bilayer. J Phys Chem B. 2010;115(5):1188–1198.
   PubMed Web of Science ®Google Scholar
• Lin D, Grossfield A. Thermodynamics of antimicrobial lipopeptide binding to membranes: origins of affinity and selectivity. Biophys J. 2014;107(8):1862–1872.10.1016/j.bpj.2014.08.026
   PubMed Web of Science ®Google Scholar
• Horn JN, Sengillo JD, Lin D, et al. Characterization of a potent antimicrobial lipopeptide via coarse-grained molecular dynamics. Biochim Biophys Acta (BBA) – Biomembr. 2012;1818(2):212–218.
   PubMed Web of Science ®Google Scholar
• Horn JN, Romo TD, Grossfield A. Simulating the mechanism of antimicrobial lipopeptides with all-atom molecular dynamics. Biochemistry. 2013;52(33):5604–5610.10.1021/bi400773q
   PubMed Web of Science ®Google Scholar