Advertisement

Membrane Permeabilization Mechanisms

  • Katsumi MatsuzakiEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1117)

Abstract

Many antimicrobial peptides are considered to kill microbes by permeabilizing cell membranes. This chapter summarizes the driving force of peptide binding to membranes; various mechanisms of lipid bilayer permeabilization including the barrel-stave, toroidal pore, and carpet models; and modes of permeabilization of bacterial and mammalian membranes.

Keywords

Membrane permeabilization Membrane binding Membrane curvature Barrel-stave model Toroidal pore model Carpet model 

References

  1. Andersson E, Rydengard V, Sonesson A, Morgelin M, Bjorck L, Schmidtchen A (2004) Antimicrobial activities of heparin-binding peptides. Eur J Biochem 271:1219–1226CrossRefGoogle Scholar
  2. Bechinger B, Lohner K (2006) Detergent-like actions of linear amphipathic cationic antimicrobial peptides. Biochim Biophys Acta 1758:1529–1539CrossRefGoogle Scholar
  3. Bessalle R, Kapitkovsky A, Gorea A, Shalit I, Fridkin M (1990) All-D-magainin: chirality, antimicrobial activity and proteolytic resistance. FEBS Lett 274:151–155CrossRefGoogle Scholar
  4. Furse S, Scott DJ (2016) Three-dimensional distribution of phospholipids in gram negative bacteria. Biochemistry 55:4742–4747CrossRefGoogle Scholar
  5. Hancock REW, Chapple DS (1999) Peptide antibiotics. Antimicrob Agents Chemother 43:1317–1323CrossRefGoogle Scholar
  6. Hara T, Kodama H, Kondo M, Wakamatsu K, Takeda A, Tachi T et al (2001) Effect of peptide dimerization on pore formation: antiparallel disulfide-dimerized magainin 2 analog. Biopolymers 58:437–446CrossRefGoogle Scholar
  7. Huang HW (2006) Molecular mechanism of antimicrobial peptides: the origin of cooperativity. Biochim Biophys Acta 1758:1292–1302CrossRefGoogle Scholar
  8. Imura Y, Nishida M, Ogawa Y, Takakura Y, Matsuzaki K (2007) Action mechanism of tachyplesin I and effects of PEGylation. Biochim Biophys Acta 1768:1160–1169CrossRefGoogle Scholar
  9. Imura Y, Choda N, Matsuzaki K (2008) Magainin 2 in action: distinct modes of membrane permeabilization in living bacterial and mammalian cells. Biophys J 95:5757–5765CrossRefGoogle Scholar
  10. Kobayashi S, Takeshima K, Park CB, Kim SC, Matsuzaki K (2000) Interactions of the novel antimicrobial peptide buforin 2 with lipid bilayers: proline as a translocation promoting factor. Biochemistry 39:8648–8654CrossRefGoogle Scholar
  11. Kobayashi S, Chikushi A, Tougu S, Imura Y, Nishida M, Yano Y et al (2004) Membrane translocation mechanism of the antimicrobial peptide buforin 2. Biochemistry 43:15610–15616CrossRefGoogle Scholar
  12. Lee C-C, Sun Y, Qian S, Huang HW (2011) Transmembrane pores formed by human antimicrobial peptide LL-37. Biophys J 100:1688–1696CrossRefGoogle Scholar
  13. Ludtke SJ, He K, Heller WT, Harroun TA, Yang L, Huang HW (1996) Membrane pores induced by magainin. Biochemistry 35:13723–13728CrossRefGoogle Scholar
  14. Matsuzaki K (2009) Control of cell selectivity of antimicrobial peptides. Biochim Biophys Acta 1788:1687–1692CrossRefGoogle Scholar
  15. Matsuzaki K, Harada M, Handa T, Funakoshi S, Fujii N, Yajima H et al (1989) Magainin 1-induced leakage of entrapped calcein out of negatively-charged lipid vesicles. Biochim Biophys Acta 981:130–134CrossRefGoogle Scholar
  16. Matsuzaki K, Harada M, Funakoshi S, Fujii N, Miyajima K (1991a) Physicochemical determinants for the interactions of magainins 1 and 2 with acidic lipid bilayers. Biochim Biophys Acta 1063:162–170CrossRefGoogle Scholar
  17. Matsuzaki K, Fukui M, Fujii N, Miyajima K (1991b) Interactions of an antimicrobial peptide, tachyplesin I, with lipid membranes. Biochim Biophys Acta 1070:259–264CrossRefGoogle Scholar
  18. Matsuzaki K, Sugishita K, Fujii N, Miyajima K (1995a) Molecular basis for membrane selectivity of an antimicrobial peptide, magainin 2. Biochemistry 34:3423–3429CrossRefGoogle Scholar
  19. Matsuzaki K, Murase O, Miyajima K (1995b) Kinetics of pore formation induced by an antimicrobial peptide, magainin 2. Biochemistry 34:12553–12559CrossRefGoogle Scholar
  20. Matsuzaki K, Murase O, Fujii N, Miyajima K (1996a) An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 35:11361–11368CrossRefGoogle Scholar
  21. Matsuzaki K, Yoneyama S, Murase O, Miyajima K (1996b) Transbilayer transport of ions and lipids coupled with mastoparan X translocation. Biochemistry 35:8450–8456CrossRefGoogle Scholar
  22. Matsuzaki K, Sugishita K, Harada M, Fujii N, Miyajima K (1997a) Interactions of an antimicrobial peptide, magainin 2, with outer and inner membranes of gram-negative bacteria. Biochim Biophys Acta 1327:119–130CrossRefGoogle Scholar
  23. Matsuzaki K, Nakamura A, Murase O, Sugishita K, Fujii N, Miyajima K (1997b) Modulation of magainin 2–lipid bilayer interactions by peptide charge. Biochemistry 36:2104–2111CrossRefGoogle Scholar
  24. Matsuzaki K, Mitani Y, Akada K, Murase O, Yoneyama S, Zasloff M et al (1998a) Mechanism of synergism between antimicrobial peptides magainin 2 and PGLa. Biochemistry 37:15144–15153CrossRefGoogle Scholar
  25. Matsuzaki K, Sugishita K, Ishibe N, Ueha M, Nakata S, Miyajima K et al (1998b) Relationship of membrane curvature to the formation of pores by magainin. Biochemistry 37:11856–11863CrossRefGoogle Scholar
  26. Matsuzaki K, Sugishita K, Miyajima K (1999) Interactions of an antimicrobial peptide, magainin 2 with lipopolysaccharide-containing liposomes as a model for outer membranes of gram-negative bacteria. FEBS Lett 449:221–224CrossRefGoogle Scholar
  27. Miyazaki Y, Aoki M, Yano Y, Matsuzaki K (2012) Interaction of antimicrobial peptide magainin 2 with gangliosides as a target for human cell binding. Biochemistry 51:10229–10235CrossRefGoogle Scholar
  28. Oren Z, Shai Y (1998) Mode of action of linear amphipathic alpha-helical antimicrobial peptides. Biopolymers 47:451–463CrossRefGoogle Scholar
  29. Park CB, Kim HS, Kim SC (1998) Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem Biophys Res Commun 244:253–257CrossRefGoogle Scholar
  30. Patrzykat A, Friedrich CL, Zhang L, Mendoza V, Hancock RE (2002) Sublethal concentrations of pleurocidin-derived antimicrobial peptides inhibit macromolecular synthesis in Escherichia coli. Antimicrob Agents Chemother 46:605–614CrossRefGoogle Scholar
  31. Roversi D, Luca V, Aureli S, Park Y, Mangoni ML, Stella L (2014) How many antimicrobial peptide molecules kill a bacterium? The case of PMAP-23. ACS Chem Biol 9:2003–2007CrossRefGoogle Scholar
  32. Sansom MSP (1991) The biophysics of peptide models of ion channels. Prog Biophys Mol Biol 55:139–235CrossRefGoogle Scholar
  33. Schwarz G, Arbuzova A (1995) Pore kinetics reflected in the dequenching of a lipid vesicle entrapped fluorescent dye. Biochim Biophys Acta 1239:51–57CrossRefGoogle Scholar
  34. Schwarz G, Robert CH (1992) Kinetics of pore-mediated release of marker molecules from liposomes or cells. Biophys Chem 42:291–296CrossRefGoogle Scholar
  35. Shai Y (1995) Molecular recognition between membrane-spanning polypeptides. Trends Biol Sci 20:460–465CrossRefGoogle Scholar
  36. Sochacki KA, Barns KJ, Bucki R, Weisshaar JC (2011) Real-time attack on single Escherichia coli cells by the human antimicrobial peptide LL-37. Proc Natl Acad Sci U S A 108:E77–E81CrossRefGoogle Scholar
  37. Takeshima K, Chikushi A, Lee K-K, Yonehara S, Matsuzaki K (2003) Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes. J Biol Chem 278:1310–1315CrossRefGoogle Scholar
  38. Tomasinsig L, Skerlavaj B, Papo N, Giabbai B, Shai Y, Zanetti M (2006) Mechanistic and functional studies of the interaction of a proline-rich antimicrobial peptide with mammalian cells. J Biol Chem 281:383–391CrossRefGoogle Scholar
  39. Utsugi T, Schroit AJ, Connor J, Bucana CD, Fidler IJ (1991) Elevated expression of phosphatidylserine in the outer membrane leaflet of human tumor cells and recognition by activated human blood monocytes. Cancer Res 51:3062–3066PubMedGoogle Scholar
  40. Wade D, Boman A, Wåhlin B, Drain CM, Andreu D, Boman HG et al (1990) All-D amino acid-containing channel forming antibiotic peptides. Proc Natl Acad Sci U S A 87:4761–4765CrossRefGoogle Scholar
  41. Wenk MR, Seelig J (1998) Magainin 2 amide interaction with lipid membranes: calorimetric detection of peptide binding and pore formation. Biochemistry 37:3909–3916CrossRefGoogle Scholar
  42. Wieprecht T, Beyermann M, Seelig J (1999) Binding of antibacterial magainin peptides to electrically neutral membranes: thermodynamics and structure. Biochemistry 38:10377–10387CrossRefGoogle Scholar
  43. Wimley WC (2010) Describing the mechanism of antimicrobial peptide action with the interfacial activity model. ACS Chem Biol 5:905–917CrossRefGoogle Scholar
  44. Yang L, Harroun TA, Weiss TM, Ding L, Huang HW (2001) Barrel-stave model or toroidal model? A case study on melittin pores. Biophys J 81:1475–1485CrossRefGoogle Scholar
  45. Yoneyama F, Imura Y, Ohno K, Zendo T, Nakayama J, Matsuzaki K et al (2009) Peptide-lipid huge toroidal pore, a new antimicrobial mechanism mediated by a lactococcal bacteriocin, lacticin Q. Antimicrob Agents Chemother 53:3211–3217CrossRefGoogle Scholar
  46. Zasloff M (1987) Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, and partial cDNA sequence of a precursor. Proc Natl Acad Sci U S A 84:5449–5453CrossRefGoogle Scholar
  47. Zhang L, Benz R, Hancock REW (1999) Influence of proline residues on the antibacterial and synergistic activities of α-helical peptides. Biochemistry 38:8102–8111CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Graduate School of Pharmaceutical SciencesKyoto UniversitySakyo-kuJapan

Personalised recommendations