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Volume 19   Issue 2   Year 2024
Kholina E.G., Kovalenko I.B., Strakhovskaya M.G.

Cationic Biocides Tend to Embed into the Inner Layer of the Model Outer Membrane Vesicles of Gram-negative Bacteria: Computational Insights

Mathematical Biology & Bioinformatics. 2024;19(2):261-275.

doi: 10.17537/2024.19.261.

References

  1. Tang K.W.K., Millar B.C., Moore J.E. Antimicrobial Resistance (AMR). Br. J. Biomed. Sci. 2023;80:11387. doi: 10.3389/bjbs.2023.11387
  2. Cox G., Wright G.D. Intrinsic Antibiotic Resistance: Mechanisms, Origins, Challenges and Solutions. Int. J. Med. Microbiol. 2013;303:287–292. doi: 10.1016/j.ijmm.2013.02.009
  3. Lee C.-R., Lee J.H., Park M., Park K.S., Bae I.K., Kim Y.B., Cha C.-J., Jeong B.C., Lee S.H. Biology of Acinetobacter Baumannii: Pathogenesis, Antibiotic Resistance Mechanisms, and Prospective Treatment Options. Front. Cell. Infect. Microbiol. 2017;7:55. doi: 10.3389/fcimb.2017.00055
  4. Olaitan A.O., Morand S., Rolain J.-M. Mechanisms of Polymyxin Resistance: Acquired and Intrinsic Resistance in Bacteria. Front. Microbiol. 2014;5:643. doi: 10.3389/fmicb.2014.00643
  5. Langsrud S., Sundheim G., Borgmann-Strahsen R. Intrinsic and Acquired Resistance to Quaternary Ammonium Compounds in Food-Related Pseudomonas Spp. J. Appl. Microbiol. 2003;95:874–882. doi: 10.1046/j.1365-2672.2003.02064.x
  6. Nikaido H. Molecular Basis of Bacterial Outer Membrane Permeability Revisited. Microbiol. Mol. Biol. Rev. 2003;67:593–656. doi: 10.1128/MMBR.67.4.593-656.2003
  7. Khalid S., Schroeder C., Bond P.J., Duncan A.L. What Have Molecular Simulations Contributed to Understanding of Gram-Negative Bacterial Cell Envelopes?: This Article Is Part of the Bacterial Cell Envelopes Collection. Microbiology. 2022;168. doi: 10.1099/mic.0.001165
  8. Kulp A., Kuehn M.J. Biological Functions and Biogenesis of Secreted Bacterial Outer Membrane Vesicles. Annu. Rev. Microbiol. 2010;64:163–184. doi: 10.1146/annurev.micro.091208.073413
  9. Kuehn M.J., Kesty N.C. Bacterial Outer Membrane Vesicles and the Host–Pathogen Interaction. Genes Dev. 2005;19:2645–2655. doi: 10.1101/gad.1299905
  10. Schwechheimer C., Kuehn M.J. Outer-Membrane Vesicles from Gram-Negative Bacteria: Biogenesis and Functions. Nat. Rev. Microbiol. 2015;13:605–619. doi: 10.1038/nrmicro3525
  11. Li N.; Wu M.; Wang L.; Tang M.; Xin H.; Deng K. Efficient Isolation of Outer Membrane Vesicles (OMVs) Secreted by Gram-Negative Bacteria via a Novel Gradient Filtration Method. Membranes. 2024;14:135. doi: 10.3390/membranes14060135
  12. Anand D., Chaudhuri A. Bacterial Outer Membrane Vesicles: New Insights and Applications. Mol. Membr. Biol. 2016;33:125–137. doi: 10.1080/09687688.2017.1400602
  13. Magaña G., Harvey C., Taggart C.C., Rodgers A.M. Bacterial Outer Membrane Vesicles: Role in Pathogenesis and Host-Cell Interactions. Antibiotics. 2023;13:32. doi: 10.3390/antibiotics13010032
  14. Kim J.Y., Suh J.W., Kang J.S., Kim S.B., Yoon Y.K., Sohn J.W. Gram-Negative Bacteria’s Outer Membrane Vesicles. Infect. Chemother. 2023;55:1. doi: 10.3947/ic.2022.0145
  15. Jan A.T. Outer Membrane Vesicles (OMVs) of Gram-Negative Bacteria: A Perspective Update. Front. Microbiol. 2017;8:1053. doi: 10.3389/fmicb.2017.01053
  16. Muñoz-Echeverri L.M., Benavides-López S., Geiger O., Trujillo-Roldán M.A., Valdez-Cruz N.A. Bacterial Extracellular Vesicles: Biotechnological Perspective for Enhanced Productivity. World J. Microbiol. Biotechnol. 2024;40:174. doi: 10.1007/s11274-024-03963-7
  17. Combo S., Mendes S., Nielsen K.M., Da Silva G.J., Domingues S. The Discovery of the Role of Outer Membrane Vesicles against Bacteria. Biomedicines. 2022;10:2399. doi: 10.3390/biomedicines10102399
  18. Wai S.N., Takade A., Amako K. The Release of Outer Membrane Vesicles from the Strains of Enterotoxigenic Escherichia coli. Microbiol. Immunol. 1995;39:451–456. doi: 10.1111/j.1348-0421.1995.tb02228.x
  19. Kolling G.L.; Matthews K.R. Export of Virulence Genes and Shiga Toxin by Membrane Vesicles of Escherichia Coli O157:H7. Appl. Environ. Microbiol. 1999;65:1843–1848. doi: 10.1128/AEM.65.5.1843-1848.1999
  20. Chatterjee D., Chaudhuri K. Association of Cholera Toxin with Vibrio Cholerae Outer Membrane Vesicles Which Are Internalized by Human Intestinal Epithelial Cells. FEBS Lett. 2011;585:1357–1362. doi: 10.1016/j.febslet.2011.04.017
  21. Pérez A., Merino M., Rumbo-Feal S., Álvarez-Fraga L., Vallejo J.A., Beceiro A., Ohneck E.J., Mateos J., Fernández-Puente P., Actis L.A. et al. The FhaB/FhaC Two-Partner Secretion System Is Involved in Adhesion of Acinetobacter Baumannii AbH12O-A2 Strain. Virulence. 2017;8:959–974. doi: 10.1080/21505594.2016.1262313
  22. Bauman S.J., Kuehn M.J. Pseudomonas Aeruginosa Vesicles Associate with and Are Internalized by Human Lung Epithelial Cells. BMC Microbiol. 2009;9:26. doi: 10.1186/1471-2180-9-26
  23. Ellis T.N., Kuehn M.J. Virulence and Immunomodulatory Roles of Bacterial Outer Membrane Vesicles. Microbiol. Mol. Biol. Rev. 2010;74:81–94. doi: 10.1128/MMBR.00031-09
  24. Toledo A., Coleman J.L., Kuhlow C.J., Crowley J.T., Benach J.L. The Enolase of Borrelia Burgdorferi Is a Plasminogen Receptor Released in Outer Membrane Vesicles. Infect. Immun. 2012;80:359–368. doi: 10.1128/IAI.05836-11
  25. Lappann M., Otto A., Becher D., Vogel U. Comparative Proteome Analysis of Spontaneous Outer Membrane Vesicles and Purified Outer Membranes of Neisseria Meningitidis. J. Bacteriol. 2013;195:4425–4435. doi: 10.1128/JB.00625-13
  26. Nagakubo T., Nomura N., Toyofuku M. Cracking Open Bacterial Membrane Vesicles. Front. Microbiol. 2020;10:3026. doi: 10.3389/fmicb.2019.03026
  27. Yonezawa H., Osaki T., Kurata S., Fukuda M., Kawakami H., Ochiai K., Hanawa T., Kamiya S. Outer Membrane Vesicles of Helicobacter Pylori TK1402 Are Involved in Biofilm Formation. BMC Microbiol. 2009;9:197. doi: 10.1186/1471-2180-9-197
  28. Henriquez T., Falciani C. Extracellular Vesicles of Pseudomonas: Friends and Foes. Antibiotics. 2023;12:703. doi: 10.3390/antibiotics12040703
  29. Jiang B., Lai Y., Xiao W., Zhong T., Liu F., Gong J., Huang J. Microbial Extracellular Vesicles Contribute to Antimicrobial Resistance. PLOS Pathog. 2024;20:e1012143. doi: 10.1371/journal.ppat.1012143
  30. Medvedeva E.S., Baranova N.B., Mouzykantov A.A., Grigorieva T.Yu., Davydova M.N., Trushin M.V., Chernova O.A., Chernov V.M. Adaptation of Mycoplasmas to Antimicrobial Agents: Acholeplasma Laidlawii Extracellular Vesicles Mediate the Export of Ciprofloxacin and a Mutant Gene Related to the Antibiotic Target. Sci. World J. 2014;2014:1–7. doi: 10.1155/2014/150615
  31. Kadurugamuwa J.L., Beveridge T.J. Bacteriolytic Effect of Membrane Vesicles from Pseudomonas Aeruginosa on Other Bacteria Including Pathogens: Conceptually New Antibiotics. J. Bacteriol. 1996;178:2767–2774. doi: 10.1128/jb.178.10.2767-2774.1996
  32. Manning A.J., Kuehn M.J. Contribution of Bacterial Outer Membrane Vesicles to Innate Bacterial Defense. BMC Microbiol. 2011;11:258. doi: 10.1186/1471-2180-11-258
  33. Balhuizen M.D., Van Dijk A., Jansen J.W.A., Van De Lest C.H.A., Veldhuizen E.J.A., Haagsman H.P. Outer Membrane Vesicles Protect Gram-Negative Bacteria against Host Defense Peptides. mSphere. 2021;6:e00523-21. doi: 10.1128/mSphere.00523-21
  34. Park J., Kim M., Shin B., Kang M., Yang J., Lee T.K., Park W. A Novel Decoy Strategy for Polymyxin Resistance in Acinetobacter Baumannii. eLife. 2021;10:e66988. doi: 10.7554/eLife.66988
  35. Grenier D., Bertrand J., Mayrand D. Porphyromonas Gingivalis Outer Membrane Vesicles Promote Bacterial Resistance to Chlorhexidine. Oral Microbiol. Immunol. 1995;10:319–320. doi: 10.1111/j.1399-302X.1995.tb00161.x
  36. Kim S.W., Park S.B., Im S.P., Lee J.S., Jung J.W., Gong T.W., Lazarte J.M.S., Kim J., Seo J.-S., Kim J.-H. et al. Outer Membrane Vesicles from β-Lactam-Resistant Escherichia Coli Enable the Survival of β-Lactam-Susceptible E. Coli in the Presence of β-Lactam Antibiotics. Sci. Rep. 2018;8:5402. doi: 10.1038/s41598-018-23656-0
  37. Stentz R., Horn N., Cross K., Salt L., Brearley C., Livermore D.M., Carding S.R. Cephalosporinases Associated with Outer Membrane Vesicles Released by Bacteroides Spp. Protect Gut Pathogens and Commensals against β-Lactam Antibiotics. J. Antimicrob. Chemother. 2015;70:701–709. doi: 10.1093/jac/dku466
  38. Marrink S.J., Risselada H.J., Yefimov S., Tieleman D.P., De Vries A.H. The MARTINI Force Field: Coarse Grained Model for Biomolecular Simulations. J. Phys. Chem. B. 2007;111:7812–7824. doi: 10.1021/jp071097f
  39. Hsu P., Bruininks B.M.H., Jefferies D., Cesar Telles De Souza P., Lee J., Patel D.S., Marrink S.J., Qi Y., Khalid S., Im W. CHARMM‐GUI Martini Maker for Modeling and Simulation of Complex Bacterial Membranes with Lipopolysaccharides. J. Comput. Chem. 2017;38:2354–2363. doi: 10.1002/jcc.24895
  40. Jefferies D., Shearer J., Khalid S. Role of O-Antigen in Response to Mechanical Stress of the E. Coli Outer Membrane: Insights from Coarse-Grained MD Simulations. J. Phys. Chem. B. 2019;123:3567–3575. doi: 10.1021/acs.jpcb.8b12168
  41. Im W., Khalid S. Molecular Simulations of Gram-Negative Bacterial Membranes Come of Age. Annu. Rev. Phys. Chem. 2020;71:171–188. doi: 10.1146/annurev-physchem-103019-033434
  42. Rzepiela A.J., Sengupta D., Goga N., Marrink S.J. Membrane Poration by Antimicrobial Peptides Combining Atomistic and Coarse-Grained Descriptions. Faraday Discuss. 2010;144:431–443. doi: 10.1039/B901615E
  43. Balatti G., Ambroggio E., Fidelio G., Martini M., Pickholz M. Differential Interaction of Antimicrobial Peptides with Lipid Structures Studied by Coarse-Grained Molecular Dynamics Simulations. Molecules. 2017;22:1775. doi: 10.3390/molecules22101775
  44. Talandashti R., Mehrnejad F., Rostamipour K., Doustdar F., Lavasanifar A. Molecular Insights into Pore Formation Mechanism, Membrane Perturbation, and Water Permeation by the Antimicrobial Peptide Pleurocidin: A Combined All-Atom and Coarse-Grained Molecular Dynamics Simulation Study. J. Phys. Chem. B. 2021;125:7163–7176. doi: 10.1021/acs.jpcb.1c01954
  45. Lee H. Heterodimer and Pore Formation of Magainin 2 and PGLa: The Anchoring and Tilting of Peptides in Lipid Bilayers. Biochim. Biophys. Acta BBA - Biomembr. 2020;1862:183305. doi: 10.1016/j.bbamem.2020.183305
  46. Balatti G.E., Martini M.F., Pickholz M. A Coarse-Grained Approach to Studying the Interactions of the Antimicrobial Peptides Aurein 1.2 and Maculatin 1.1 with POPG/POPE Lipid Mixtures. J. Mol. Model. 2018;24:208. doi: 10.1007/s00894-018-3747-z
  47. Catte A., Wilson M.R., Walker M., Oganesyan V.S. Antimicrobial Action of the Cationic Peptide, Chrysophsin-3: A Coarse-Grained Molecular Dynamics Study. Soft Matter. 2018;14:2796–2807. doi: 10.1039/C7SM02152F
  48. Li Q., Zhong X., Sun L., Dai L. Enhancement of Cell Membrane Poration by the Antimicrobial Peptide Melp5. arXiv:2310.11156 [physics.bio-ph]. doi: Cite to nonCR doi: 10.48550/arXiv.2310.11156
  49. Melcrová A., Maity S., Melcr J., De Kok N.A.W., Gabler M., Van Der Eyden J., Stensen W., Svendsen J.S.M., Driessen A.J.M., Marrink S.J. et al. Lateral Membrane Organization as Target of an Antimicrobial Peptidomimetic Compound. Nat. Commun. 2023;14:4038. doi: 10.1038/s41467-023-39726-5
  50. Hsu P.-C., Jefferies D., Khalid S. Molecular Dynamics Simulations Predict the Pathways via Which Pristine Fullerenes Penetrate Bacterial Membranes. J. Phys. Chem. B. 2016;120:11170–11179. doi: 10.1021/acs.jpcb.6b06615
  51. Rietschel E.T., Kirikae T., Schade F.U., Mamat U., Schmidt G., Loppnow H., Ulmer A.J., Zähringer U., Seydel U., Di Padova F. et al. Bacterial Endotoxin: Molecular Relationships of Structure to Activity and Function. FASEB J. 1994;8:217–225. doi: 10.1096/fasebj.8.2.8119492
  52. Van Oosten B., Marquardt D., Harroun T.A. Testing High Concentrations of Membrane Active Antibiotic Chlorhexidine Via Computational Titration and Calorimetry. J. Phys. Chem. B. 2017;121:4657–4668. doi: 10.1021/acs.jpcb.6b12510
  53. Yesylevskyy S.O., Schäfer L.V., Sengupta D., Marrink S.J. Polarizable Water Model for the Coarse-Grained MARTINI Force Field. PLoS Comput. Biol. 2010;6:e1000810. doi: 10.1371/journal.pcbi.1000810
  54. Abraham M.J., Murtola T., Schulz R., Páll S., Smith J.C., Hess B., Lindahl E. GROMACS: High Performance Molecular Simulations through Multi-Level Parallelism from Laptops to Supercomputers. SoftwareX. 2015;1(2):19–25. doi: 10.1016/j.softx.2015.06.001
  55. Kovalenko I.B., Knyazeva O.S., Antal T.K., Ponomarev V.Y., Riznichenko G.Y., Rubin A.B. Multiparticle Brownian Dynamics Simulation of Experimental Kinetics of Cytochrome Bf Oxidation and Photosystem I Reduction by Plastocyanin. Physiol. Plant. 2017;161:88–96. doi: 10.1111/ppl.12570
  56. Fedorov V.A., Kovalenko I.B., Khruschev S.S., Ustinin D.M., Antal T.K., Riznichenko G.Y., Rubin A.B. Comparative Analysis of Plastocyanin–Cytochrome f Complex Formation in Higher Plants, Green Algae and Cyanobacteria. Physiol. Plant. 2019;166:320–335. doi: 10.1111/ppl.12940
  57. The PyMOL Molecular Graphics System, Version 2.4 Schrödinger, LLC.
  58. Orekhov P.S., Kholina E.G., Bozdaganyan M.E., Nesterenko A.M., Kovalenko I.B., Strakhovskaya M.G. Molecular Mechanism of Uptake of Cationic Photoantimicrobial Phthalocyanine across Bacterial Membranes Revealed by Molecular Dynamics Simulations. J. Phys. Chem. B. 2018;122:3711–3722. doi: 10.1021/acs.jpcb.7b11707
  59. Kholina E.G., Kovalenko I.B., Bozdaganyan M.E., Strakhovskaya M.G., Orekhov P.S. Cationic Antiseptics Facilitate Pore Formation in Model Bacterial Membranes. J. Phys. Chem. B. 2020;124:8593–8600. doi: 10.1021/acs.jpcb.0c07212
  60. Meerovich G.A., Akhlyustina E.V., Romanishkin I.D., Makarova E.A., Tiganova I.G., Zhukhovitsky V.G., Kholina E.G., Kovalenko I.B., Romanova Y.M., Loschenov V.B. et al. Photodynamic Inactivation of Bacteria: Why It Is Not Enough to Excite a Photosensitizer. Photodiagnosis Photodyn. Ther. 2023;44:103853. doi: 10.1016/j.pdpdt.2023.103853
  61. Zgurskaya H.I., Rybenkov V.V. Permeability Barriers of Gram‐negative Pathogens. Ann. N. Y. Acad. Sci. 2020;1459:5–18. doi: 10.1111/nyas.14134
  62. Maher C., Hassan K.A. The Gram-Negative Permeability Barrier: Tipping the Balance of the in and the Out. mBio. 2023;14:e01205-23. doi: 10.1128/mbio.01205-23
  63. González-Fernández C., Bringas E., Oostenbrink C., Ortiz I. In Silico Investigation and Surmounting of Lipopolysaccharide Barrier in Gram-Negative Bacteria: How Far Has Molecular Dynamics Come? Comput. Struct. Biotechnol. J. 2022;20:5886–5901. doi: 10.1016/j.csbj.2022.10.039
  64. Pier G. Pseudomonas Aeruginosa Lipopolysaccharide: A Major Virulence Factor, Initiator of Inflammation and Target for Effective Immunity. Int. J. Med. Microbiol. 2007;297:277–295. doi: 10.1016/j.ijmm.2007.03.012
  65. Makin S.A., Beveridge T.J. Pseudomonas Aeruginosa PAO1 Ceases to Express Serotype-Specific Lipopolysaccharide at 45 Degrees C. J. Bacteriol. 1996;178:3350–3352. doi: 10.1128/jb.178.11.3350-3352.1996
  66. King J.D., Kocíncová D., Westman E.L., Lam J.S. Review: Lipopolysaccharide Biosynthesis in Pseudomonas aeruginosa. Innate Immun. 2009;15:261–312. doi: 10.1177/1753425909106436
  67. Vereshchagin A.N., Frolov N.A., Egorova K.S., Seitkalieva M.M., Ananikov V.P. Quaternary Ammonium Compounds (QACs) and Ionic Liquids (ILs) as Biocides: From Simple Antiseptics to Tunable Antimicrobials. Int. J. Mol. Sci. 2021;22:6793. doi: 10.3390/ijms22136793
  68. Vejzovic D., Iftic A., Ön A., Semeraro E.F., Malanovic N. Octenidine’s Efficacy: A Matter of Interpretation or the Influence of Experimental Setups? Antibiotics. 2022;11:1665. doi: 10.3390/antibiotics11111665
  69. Nasrollahian S., Graham J.P., Halaji M. A Review of the Mechanisms That Confer Antibiotic Resistance in Pathotypes of E. coli. Front. Cell. Infect. Microbiol. 2024;14:1387497. doi: 10.3389/fcimb.2024.1387497
Table of Contents Original Article
Math. Biol. Bioinf.
2024;19(2):261-275
doi: 10.17537/2024.19.261
published in English

Abstract (eng.)
Abstract (rus.)
Full text (eng., pdf)
References

 

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