Saturday, May 18, 2024

Vesicle protrusion induced by antimicrobial peptides suggests common carpet mechanism for short antimicrobial peptides

BiochemistryVesicle protrusion induced by antimicrobial peptides suggests common carpet mechanism for short antimicrobial peptides


  • Antibiotic resistance (2023, accessed May 2023). https://www.who.int/news-room/fact-sheets/detail/antibiotic-resistance.

  • Urban-Chmiel, R. et al. Antibiotic resistance in bacteria—a review. Antibiotics 11, 1079 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bush, K. et al. Tackling antibiotic resistance. Nat. Rev. Microbiol. 9, 894–896 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Murray, C. J. et al. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. The Lancet 399, 629–655 (2022).

    Article 
    CAS 

    Google Scholar 

  • O’Neill, J. Tackling drug-resistant infections globally: Final report and recommendations (2016, accessed May 2023). https://amr-review.org/sites/default/files/160518_Final%20paper_with%20cover.pdf.

  • Mann, A., Nehra, K., Rana, J. S. & Dahiya, T. Antibiotic resistance in agriculture: Perspectives on upcoming strategies to overcome upsurge in resistance. Curr. Res. Microb. Sci. 202, 100030 (2021).

    Google Scholar 

  • Morris, S. & Cerceo, E. Trends, epidemiology, and management of multi-drug resistant gram-negative bacterial infections in the hospitalized setting. Antibiotics 9, 196 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Moretta, A. et al. Antimicrobial peptides: A new hope in biomedical and pharmaceutical fields. Front. Cell Infect. Microbiol. 11, 668632 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Brogden, K. A. Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria?. Nat. Rev. Microbiol. 3, 238–250 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Turner, K. B., Dean, S. N. & Walper, S. A. Bacterial Bioreactors: Outer Membrane Vesicles for Enzyme Encapsulation. Methods In Enzymology 187–31216 (Academic Press Inc., 2019).

    Google Scholar 

  • Sood, R. & Kinnunen, P. K. J. Cholesterol, lanosterol, and ergosterol attenuate the membrane association of LL-37(W27F) and temporin L. Biochim. Biophys. Acta Biomembr. 341778, 1460–1466 (2008).

    Article 

    Google Scholar 

  • Brender, J. R., McHenry, A. J. & Ramamoorthy, A. Does cholesterol play a role in the bacterial selectivity of antimicrobial peptides?. Front. Immunol. 3, 31501 (2012).

    Article 

    Google Scholar 

  • Torres, M. D. T. et al. Decoralin analogs with increased resistance to degradation and lower hemolytic activity. Chem. Select 2, 18–23 (2017).

    CAS 

    Google Scholar 

  • Somma, A. et al. Antibiofilm properties of temporin-l on Pseudomonas fluorescens in static and in-flow conditions. Int. J. Mol. Sci. 21, 1–17 (2020).

    Article 

    Google Scholar 

  • Torres, M. D. T. et al. Natural and redesigned wasp venom peptides with selective antitumoral activity. Beilstein J. Org. Chem. 14, 1693–1703 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ramesh, S., Govender, T., Kruger, H. G., de la Torre, B. G. & Albericio, F. Short AntiMicrobial Peptides (SAMPs) as a class of extraordinary promising therapeutic agents. J. Peptide Sci. 22, 438–451 (2016).

    Article 
    CAS 

    Google Scholar 

  • Wadhwani, P. et al. Dynamical structure of the short multifunctional peptide BP100 in membranes. Biochim. Biophys. Acta BBA Biomembr. 1838, 940–949 (2014).

    Article 
    CAS 

    Google Scholar 

  • Misiewicz, J. et al. Action of the multifunctional peptide BP100 on native biomembranes examined by solid-state NMR. J. Biomol. NMR 61, 287–298 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Grau-Campistany, A. et al. Hydrophobic mismatch demonstrated for membranolytic peptides and their use as molecular rulers to measure bilayer thickness in native cells. Sci. Rep. 5, 1–9 (2015).

    Article 

    Google Scholar 

  • Grau-Campistany, A., Strandberg, E., Wadhwani, P., Rabanal, F. & Ulrich, A. S. Extending the hydrophobic mismatch concept to amphiphilic membranolytic peptides. J. Phys. Chem. Lett. 7, 1116–1120 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Manzini, M. C. et al. Peptide: Lipid ratio and membrane surface charge determine the mechanism of action of the antimicrobial peptide BP100. Conformational and functional studies. Biochim. Biophys. Acta Biomembr. 1838, 1985–1999 (2014).

    Article 
    CAS 

    Google Scholar 

  • Melo, M. N., Ferre, R. & Castanho, M. A. R. B. Antimicrobial peptides: Linking partition, activity and high membrane-bound concentrations. Nat. Rev. Microbiol. 2009(7), 245–250 (2009).

    Article 

    Google Scholar 

  • Shai, Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by α-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta BBA Biomembr. 1462, 55–70 (1999).

    Article 
    CAS 

    Google Scholar 

  • Carretero, G. P. B. et al. Synthesis, biophysical and functional studies of two BP100 analogues modified by a hydrophobic chain and a cyclic peptide. Biochim. Biophys. Acta Biomembr. 1860, 1502–1516 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Mink, C. et al. Overlapping properties of the short membrane-active peptide BP100 with (i) Polycationic TAT and (ii) α-helical magainin family peptides. Front. Cell Infect. Microbiol. 11, 350 (2021).

    Article 

    Google Scholar 

  • Palmer, N., Maasch, J. R. M. A., Torres, M. D. T. & De La Fuente-Nunez, C. Molecular dynamics for antimicrobial peptide discovery. Infect. Immun. 89, 4 (2021).

    Article 

    Google Scholar 

  • Ulmschneider, J. P. & Ulmschneider, M. B. Molecular dynamics simulations are redefining our view of peptides interacting with biological membranes. Acc. Chem. Res. 51, 1106–1116 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Aronica, P. G. A. et al. Computational methods and tools in antimicrobial peptide research. J. Chem. Inf. Model. 61, 3172–3196 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Leontiadou, H., Mark, A. E. & Marrink, S. J. Antimicrobial peptides in action. J. Am. Chem. Soc. 128, 12156–12161 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wang, Y., Chen, C. H., Hu, D., Ulmschneider, M. B. & Ulmschneider, J. P. Spontaneous formation of structurally diverse membrane channel architectures from a single antimicrobial peptide. Nat. Commun. 7, 1–9 (2016).

    Article 

    Google Scholar 

  • Bond, P. J., Parton, D. L., Clark, J. F. & Sansom, M. S. P. Coarse-grained simulations of the membrane-active antimicrobial peptide maculatin 1.1. Biophys. J. 95, 3802–3815 (2008).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Thøgersen, L., Schiøtt, B., Vosegaard, T., Nielsen, N. C. & Tajkhorshid, E. Peptide aggregation and pore formation in a lipid bilayer: A combined coarse-grained and all atom molecular dynamics study. Biophys. J. 95, 4337–4347 (2008).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rzepiela, A. J., Sengupta, D., Goga, N. & Marrink, S. J. Membrane poration by antimicrobial peptides combining atomistic and coarse-grained descriptions. Faraday Discuss. 144, 431–443 (2009).

    Article 
    ADS 

    Google Scholar 

  • Santo, K. P. & Berkowitz, M. L. Difference between magainin-2 and melittin assemblies in phosphatidylcholine bilayers: Results from coarse-grained simulations. J. Phys. Chem. B 116, 3021–3030 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Su, J., Marrink, S. J. & Melo, M. N. Localization preference of antimicrobial peptides on liquid-disordered membrane domains. Front. Cell Dev. Biol. 8, 350 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Badosa, E. et al. A library of linear undecapeptides with bactericidal activity against phytopathogenic bacteria. Peptides N. Y. 28, 2276–2285 (2007).

    Article 
    CAS 

    Google Scholar 

  • Park, P. et al. Binding and flip as initial steps for BP-100 antimicrobial actions. Sci. Rep. 9, 8622 (2019).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Franco, L. R. et al. Simulations reveal that antimicrobial BP100 induces local membrane thinning, slows lipid dynamics and favors water penetration. RSC Adv. 12, 4573–4588 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Miao, X. et al. Enhanced cell selectivity of hybrid peptides with potential antimicrobial activity and immunomodulatory effect. Biochim. Biophys. Acta Gen. Subj. 2020, 1864 (2020).

    Google Scholar 

  • Woolley, G. A. & Deber, C. M. Peptides in membranes: Lipid-induced secondary structure of substance P. Biopolymers 26, S109–S121 (1987).

    Article 
    PubMed 

    Google Scholar 

  • Konno, K. et al. Decoralin, a novel linear cationic α-helical peptide from the venom of the solitary eumenine wasp Oreumenes decoratus. Peptides N.Y. 28, 2320–2327 (2007).

    Article 
    CAS 

    Google Scholar 

  • Rinaldi, A. C. et al. Temporin L: Antimicrobial, haemolytic and cytotoxic activities, and effects on membrane permeabilization in lipid vesicles. Biochem. J. 368, 91–100 (2002).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Carotenuto, A. et al. A different molecular mechanism underlying antimicrobial and hemolytic actions of temporins A and L. J. Med. Chem. 51, 2354–2362 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Zhao, H. & Kinnunen, P. K. J. Binding of the antimicrobial peptide temporin L to liposomes assessed by Trp fluorescence. J. Biol. Chem. 277, 25170–25177 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Guerra, M. E. R. et al. MD simulations and multivariate studies for modeling the antileishmanial activity of peptides. Chem. Biol. Drug Des. 90, 501–510 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Ferguson, P. M. et al. Temporin B forms hetero-oligomers with temporin L, modifies its membrane activity, and increases the cooperativity of its antibacterial pharmacodynamic profile. Biochemistry 61, 1029–1040 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Manzo, G. et al. Temporin L and aurein 2.5 have identical conformations but subtly distinct membrane and antibacterial activities. Sci. Rep. 9, 1–13 (2019).

    Article 
    ADS 

    Google Scholar 

  • Wang, G., Li, X. & Wang, Z. APD3: The antimicrobial peptide database as a tool for research and education. Nucleic Acids Res. 44, D1087–D1093 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hess, B., Kutzner, C., van der Spoel, D. & Lindahl, E. GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435–447 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Van Der Spoel, D. et al. GROMACS: Fast, flexible, and free. J. Comput. Chem. 26, 1701–1718 (2005).

    Article 
    PubMed 

    Google Scholar 

  • Abraham, M. J. et al. GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1, 19–25 (2015).

    Article 
    ADS 

    Google Scholar 

  • Beauchamp, K. A., Lin, Y. S., Das, R. & Pande, V. S. Are protein force fields getting better? A systematic benchmark on 524 diverse NMR measurements. J. Chem. Theory Comput. 8, 1409–1414 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jämbeck, J. P. M. M. & Lyubartsev, A. P. An extension and further validation of an all-atomistic force field for biological membranes. J. Chem. Theory Comput. 8, 2938–2948 (2012).

    Article 
    PubMed 

    Google Scholar 

  • Jämbeck, J. P. M. & Lyubartsev, A. P. Derivation and systematic validation of a refined all-atom force field for phosphatidylcholine lipids. J. Phys. Chem. B 116, 3164–3179 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jämbeck, J. P. M. & Lyubartsev, A. P. Another piece of the membrane puzzle: Extending slipids further. J. Chem. Theory Comput. 9, 774–784 (2013).

    Article 
    PubMed 

    Google Scholar 

  • Martinez, L. et al. PACKMOL: A package for building initial configurations for molecular dynamics simulations. J. Comput. Chem. 30, 2157–2164 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Humphrey, W., Dalke, A. & Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph. 14, 33–38 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Pettersen, E. F. et al. UCSF ChimeraX: Structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hess, B., Bekker, H., Berendsen, H. J. C. & Fraaije, J. G. E. M. LINCS: A linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463–1472 (1997).

    Article 
    CAS 

    Google Scholar 

  • Essmann, U. et al. A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577 (1995).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 2007, 126 (2007).

    Google Scholar 

  • Parrinello, M. & Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method. J. Appl. Phys. 52, 7182–7190 (1981).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Santos, D. E. S., Pontes, F. J. S., Lins, R. D., Coutinho, K. & Soares, T. A. SuAVE: A tool for analyzing curvature-dependent properties in chemical interfaces. J. Chem. Inf. Model. 60, 473–484 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • 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 111, 7812–7824 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Monticelli, L. et al. The MARTINI coarse-grained force field: Extension to proteins. J. Chem. Theory Comput. 4, 819–834 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Souza, P. C. T. et al. Martini 3: A general purpose force field for coarse-grained molecular dynamics. Nat. Methods 18, 382–388 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kroon, P. C. et al. Martinize2 and vermouth: Unified framework for topology generation. arXiv:2212.01191 (2022).

  • Jo, S., Kim, T., Iyer, V. G. & Im, W. CHARMM-GUI: A web-based graphical user interface for CHARMM. J. Comput. Chem. 29, 1859–1865 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Qi, Y. et al. CHARMM-GUI martini maker for coarse-grained simulations with the martini force field. J. Chem. Theory Comput. 11, 4486–4494 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • De Jong, D. H., Baoukina, S., Ingólfsson, H. I. & Marrink, S. J. Martini straight: Boosting performance using a shorter cutoff and GPUs. Comput. Phys. Commun. 199, 1–7 (2016).

    Article 
    ADS 
    MathSciNet 

    Google Scholar 

  • Santos, D. E. S., Coutinho, K. & Soares, T. A. Surface assessment via grid evaluation (SuAVE) for every surface curvature and cavity shape. J. Chem. Inf. Model. 62, 4690–4701 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Grage, S. L., Afonin, S., Kara, S., Buth, G. & Ulrich, A. S. Membrane thinning and thickening induced by membrane-active amphipathic peptides. Front. Cell Dev. Biol. 4, 202784 (2016).

    Article 

    Google Scholar 

  • Polyansky, A. A. et al. Antimicrobial peptides induce growth of phosphatidylglycerol domains in a model bacterial membrane. J. Phys. Chem. Lett. 1, 3108–3111 (2010).

    Article 
    CAS 

    Google Scholar 

  • Steinkühler, J. et al. Controlled division of cell-sized vesicles by low densities of membrane-bound proteins. Nat. Commun. 11, 1–11 (2020).

    Article 

    Google Scholar 

  • Pezeshkian, W. & Ipsen, J. H. Fluctuations and conformational stability of a membrane patch with curvature inducing inclusions. Soft Matter. 15, 9974–9981 (2019).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Ferre, R. et al. Synergistic effects of the membrane actions of cecropin-melittin antimicrobial hybrid peptide BP100. Biophys. J. 96, 1815–1827 (2009).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zamora-Carreras, H. et al. Alanine scan and 2H NMR analysis of the membrane-active peptide BP100 point to a distinct carpet mechanism of action. Biochim. Biophys. Acta BBA Biomembranes. 1858, 1328–1338 (2016).

    Article 
    CAS 
    PubMed 

    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 115, 8122–8129 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Zhang, S. et al. Structure and formation mechanism of antimicrobial peptides temporin b-and l-induced tubular membrane protrusion. Int. J. Mol. Sci. 22, 11015 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Miyazaki, Y. & Shinoda, W. Cooperative antimicrobial action of melittin on lipid membranes: A coarse-grained molecular dynamics study. Biochim. Biophys. Acta BBA Biomembranes. 1864, 183955 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Safinya, C. R. & Rädler, J. O. Handbook of Lipid Membranes. Handbook of Lipid Membranes (CRC Press, 2021).

    Book 

    Google Scholar 

  • Zemel, A., Ben-Shaul, A. & May, S. Modulation of the spontaneous curvature and bending rigidity of lipid membranes by interfacially adsorbed amphipathic peptides. J. Phys. Chem. B 112, 6988–6996 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Tytler, E. M. et al. Reciprocal effects of apolipoprotein and lytic peptide analogs on membranes. Cross-sectional molecular shapes of amphipathic alpha helixes control membrane stability. J. Biol. Chem. 268, 22112–22118 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Epand, R. M., Shai, Y., Segrest, J. P. & Anantharamiah, G. M. Mechanisms for the modulation of membrane bilayer properties by amphipathic helical peptides. Biopolymers 37, 319–338 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Decker, A. P., Mechesso, A. F. & Wang, G. Expanding the landscape of amino acid-rich antimicrobial peptides: Definition, deployment in nature, implications for peptide design and therapeutic potential. Int. J. Mol. Sci. 2022, 23 (2022).

    Google Scholar 

  • Srivastava, S., Kumar, A., Tripathi, A. K., Tandon, A. & Ghosh, J. K. Modulation of anti-endotoxin property of Temporin L by minor amino acid substitution in identified phenylalanine zipper sequence. Biochem. J. 473, 4045–4062 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Bennett, W. F. D. & Tieleman, D. P. Water defect and pore formation in atomistic and coarse-grained lipid membranes: Pushing the limits of coarse graining. J. Chem. Theory Comput. 37, 2981–2988 (2011).

    Article 

    Google Scholar 

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