Antimicrobial peptides at work: Interaction of myxinidin and its mutant WMR with lipid bilayers mimicking the P. aeruginosa and E. coli membranes

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Lombardi, Lucia ^a   Stellato, Marco Ignazio ^b   Oliva, Rosario ^b   Falanga, Annarita ^b   Galdiero, Massimiliano ^a   Petraccone, Luigi ^b   D'Errico, Geradino ^b   De Santis, Augusta ^b   Galdiero, Stefania ^b   Del Vecchio, Pompea ^b  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; FISH PROTEIN; MUTANT PROTEIN; MYXINIDIN PEPTIDE, MYXINE GLUTINOSA; OLIGOPEPTIDE;

ANTAGONISTS AND INHIBITORS; ANTIBIOTIC RESISTANCE; CELL MEMBRANE; CHEMISTRY; DRUG EFFECT; ESCHERICHIA COLI; GENETICS; HUMAN; LIPID BILAYER; PATHOGENICITY; PSEUDOMONAS AERUGINOSA;

ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; FISH PROTEINS; HUMANS; LIPID BILAYERS; MUTANT PROTEINS; OLIGOPEPTIDES; PSEUDOMONAS AERUGINOSA;

EID: 85015270761     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep44425     Document Type: Article

References (47)

1. Jenssen, H., Hamill, P. & Hancock, R. E. Peptide antimicrobial agents. Clin. Microbiol. Rev. 19, 491-511, doi: 10.1128/CMR.00056-05 (2006).
2. Bowdish, D. M., Davidson, D. J. & Hancock, R. E. A re-evaluation of the role of host defence peptides in mammalian immunity. Curr. Protein Pept. Sci. 6, 35-51 (2005).
3. Wiesner, J. & Vilcinskas, A. Antimicrobial peptides: the ancient arm of the human immune system. Virulence 1, 440-464, doi: 10.4161/viru.1.5.12983 (2010).
4. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 415, 389-395, doi: 10.1038/415389a (2002).
5. Rotem, S. & Mor, A. Antimicrobial peptide mimics for improved therapeutic properties. Biochim. Biophys. Acta 1788, 1582-1592, doi: 10.1016/j.bbamem.2008.10.020 (2009).
6. Subramanian, S., Ross, N. W. & Mackinnon, S. L. Comparison of the biochemical composition of normal epidermal mucus and extruded slime of hagfish (Myxine glutinosa L.). Fish Shellfish Immunol. 25, 625-632, doi: 10.1016/j.fsi.2008.08.012 (2008).
7. Subramanian, S., Ross, N. W. & MacKinnon, S. L. Myxinidin, a novel antimicrobial peptide from the epidermal mucus of hagfish, Myxine glutinosa L. Mar. Biotechnol. (NY) 11, 748-757, doi: 10.1007/s10126-009-9189-y (2009).
8. Cantisani, M. et al. Structural insights into and activity analysis of the antimicrobial peptide myxinidin. Antimicrob. Agents Chemother. 58, 5280-5290, doi: 10.1128/AAC.02395-14 (2014).
9. Cantisani, M. et al. Structure-activity relations of myxinidin, an antibacterial peptide derived from the epidermal mucus of hagfish. Antimicrob. Agents Chemother. 57, 5665-5673, doi: 10.1128/AAC.01341-13 (2013).
10. Falanga, A. et al. Biophysical characterization and membrane interaction of the two fusion loops of glycoprotein B from herpes simplex type I virus. PloS one 7, e32186, doi: 10.1371/journal.pone.0032186 (2012).
11. de Planque, M. R. R. et al. Interfacial Anchor Properties of Tryptophan Residues in Transmembrane Peptides Can Dominate over Hydrophobic Matching Effects in Peptide-Lipid Interactions. Biochemistry 42, 5341-5348 (2003).
12. Yeaman, M. R. & Yount, N. Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55, 27-55, doi: 10.1124/ pr.55.1.2 (2003).
13. Shai, Y. & Oren, Z. From carpet mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides. Peptides 22, 1629-1641 (2001).
14. Sitaram, N. & Nagaraj, R. Interaction of antimicrobial peptides with biological and model membranes: structural and charge requirements for activity. Biochim. Biophys. Acta 1462, 29-54 (1999).
15. Shai, Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta 1462, 55-70 (1999).
16. Dennison, S. R., Wallace, J., Harris, F. & Phoenix, D. A. Amphiphilic alpha-helical antimicrobial peptides and their structure/ function relationships. Protein Pept. Lett. 12, 31-39 (2005).
17. Gazit, E., Lee, W. J., Brey, P. T. & Shai, Y. Mode of action of the antibacterial cecropin B2: a spectrofluorometric study. Biochemistry 33, 10681-10692 (1994).
18. Matsuzaki, K. et al. Modulation of magainin 2-lipid bilayer interactions by peptide charge. Biochemistry 36, 2104-2111, doi: 10.1021/bi961870p (1997).
19. Pouny, Y., Rapaport, D., Mor, A., Nicolas, P. & Shai, Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry 31, 12416-12423 (1992).
20. Finger, S., Kerth, A., Dathe, M. & Blume, A. The efficacy of trivalent cyclic hexapeptides to induce lipid clustering in PG/PE membranes correlates with their antimicrobial activity. Biochim. Biophys. Acta 1848, 2998-3006, doi: 10.1016/j.bbamem.2015.09.012 (2015).
21. Hunter, H. N., Demcoe, A. R., Jenssen, H., Gutteberg, T. J. & Vogel, H. J. Human lactoferricin is partially folded in aqueous solution and is better stabilized in a membrane mimetic solvent. Antimicrob. Agents Chemother. 49, 3387-3395, doi: 10.1128/AAC.49.8.3387- 3395.2005 (2005).
22. Vogel, H. J. et al. Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides. Biochem. Cell Biol. 80, 49-63 (2002).
23. Schibli, D. J., Hwang, P. M. & Vogel, H. J. The structure of the antimicrobial active center of lactoferricin B bound to sodium dodecyl sulfate micelles. FEBS Lett. 446, 213-217 (1999).
24. Vaz Gomes, A., de Waal, A., Berden, J. A. & Westerhoff, H. V. Electric potentiation, cooperativity, and synergism of magainin peptides in protein-free liposomes. Biochemistry 32, 5365-5372 (1993).
25. Hoch, F. L. Cardiolipins and biomembrane function. Biochim. Biophys. Acta 1113, 71-133 (1992).
26. Hope, M. J., Bally, M. B., Webb, G. & Cullis, P. R. Production of large unilamellar vesicles by a rapid extrusion procedure: characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim. Biophys. Acta 812, 55-65 (1985).
27. Struck, D. K., Hoekstra, D. & Pagano, R. E. Use of resonance energy transfer to monitor membrane fusion. Biochemistry 20, 4093-4099 (1981).
28. Ladokhin, A. S., Wimley, W. C. & White, S. H. Leakage of membrane vesicle contents: determination of mechanism using fluorescence requenching. Biophys. J. 69, 1964-1971, doi: 10.1016/S0006-3495(95)80066-4 (1995).
29. Parente, R. A., Nir, S. & Szoka, F. C. Jr. Mechanism of leakage of phospholipid vesicle contents induced by the peptide GALA. Biochemistry 29, 8720-8728 (1990).
30. Lomakin, A., Teplow, D. B. & Benedek, G. B. Quasielastic light scattering for protein assembly studies. Methods Mol. Biol. (Clifton, N.J.) 299, 153-174 (2005).
31. Mozsolits, H., Wirth, H. J., Werkmeister, J. & Aguilar, M. I. Analysis of antimicrobial peptide interactions with hybrid bilayer membrane systems using surface plasmon resonance. Biochim. Biophys. Acta 1512, 64-76 (2001).
32. Galdiero, S. et al. Role of membranotropic sequences from herpes simplex virus type I glycoproteins B and H in the fusion process. Biochim. Biophys. Acta 1798, 579-591, doi: 10.1016/j.bbamem.2010.01.006 (2010).
33. Vitiello, G., Di Marino, S., DUrsi, A. M. & DErrico, G. Omega-3 fatty acids regulate the interaction of the Alzheimer' s abeta(25-35) peptide with lipid membranes. Langmuir 29, 14239-14245 (2013).
34. Vitiello, G. et al. Fusion of raft-like lipid bilayers operated by a membranotropic domain of the HSV-type I glycoprotein gH occurs through a cholesterol-dependent mechanism. Soft matter 11, 3003-3016 (2015).
35. Oliva, R. et al. On the microscopic and mesoscopic perturbations of lipid bilayers upon interaction with the MPER domain of the HIV glycoprotein gp41. Biochim. Biophys. Acta 1858, 1904-1913 (2016).
36. DErrico, G., DUrsi, A. M. & Marsh, D. Interaction of a peptide derived from glycoprotein gp36 of feline immunodeficiency virus and its lipoylated analogue with phospholipid membranes. Biochemistry 47, 5317-5327 (2008).
37. Henzler-Wildman, K. A., Martinez, G. V., Brown, M. F. & Ramamoorthy, A. Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37. Biochemistry 43, 8459-8469, doi: 10.1021/bi036284s (2004).
38. Lohner, K. & Prenner, E. J. Differential scanning calorimetry and X-ray diffraction studies of the specificity of the interaction of antimicrobial peptides with membrane-mimetic systems. Biochim. Biophys. Acta 1462, 141-156 (1999).
39. McElhaney, R. N. Differential scanning calorimetric studies of lipid-protein interactions in model membrane systems. Biochim. Biophys. Acta 864, 361-421 (1986).
40. Lohner, K., Latal, A., Degovics, G. & Garidel, P. Packing characteristics of a model system mimicking cytoplasmic bacterial membranes. Chem. Phys. Lipids 111, 177-192 (2001).
41. Epand, R. M. et al. Lipid clustering by three homologous arginine-rich antimicrobial peptides is insensitive to amino acid arrangement and induced secondary structure. Biochim. Biophys. Acta 1798, 1272-1280, doi: 10.1016/j.bbamem.2010.03.012 (2010).
42. Seelig, J. Titration calorimetry of lipid-peptide interactions. Biochim. Biophys. Acta 1331, 103-116 (1997).
43. Oliva, R. et al. A thermodynamic signature of lipid segregation in biomembranes induced by a short peptide derived from glycoprotein gp36 of feline immunodeficiency virus. Biochim. Biophys. Acta 1848, 510-517 (2015).
44. Stark, M., Liu, L. P. & Deber, C. M. Cationic hydrophobic peptides with antimicrobial activity. Antimicrob. Agents Chemother. 46, 3585-3590 (2002).
45. Papo, N. & Shai, Y. Exploring peptide membrane interaction using surface plasmon resonance: differentiation between pore formation versus membrane disruption by lytic peptides. Biochemistry 42, 458-466, doi: 10.1021/bi0267846 (2003).
46. Arouri, A., Dathe, M. & Blume, A. Peptide induced demixing in PG/PE lipid mixtures: a mechanism for the specificity of antimicrobial peptides towards bacterial membranes? Biochim. Biophys. Acta 1788, 650-659, doi: 10.1016/j.bbamem.2008.11.022 (2009).
47. Fernandez, D. I. et al. The antimicrobial peptide aurein 1.2 disrupts model membranes via the carpet mechanism. Phys. Chem. Chem. Phys. 14, 15739-15751 (2012).