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Elementary Processes and Mechanisms of Interactions of Antimicrobial Peptides with Membranes—Single Giant Unilamellar Vesicle Studies—

  • Moynul Hasan
  • Masahito YamazakiEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1117)

Abstract

To elucidate the mechanisms of action of antimicrobial peptides (AMPs) and to develop de novo designed peptides with activities similar to those of AMPs, it is essential to elucidate the detailed processes of AMP interactions with plasma membranes of bacterial and fungal cells and model membranes (lipid bilayers). In this mini-review, we summarize the present state of knowledge of the interactions of AMPs with lipid vesicles obtained using the single giant unilamellar vesicle (GUV) method. Currently, three modes of action of AMPs on GUVs have been defined. The elementary processes of interactions of AMPs with lipid vesicles revealed by the single GUV method, and the advantages of this technique, are described and discussed. For example, the single GUV method can be used to determine rate constants of AMP-induced pore formation or local rupture and membrane permeation of internal contents through the pore or the local rupture, the transbilayer movement of lipids, and the relationship between the location of AMPs and pore formation. Effects of membrane tension and of asymmetric lipid packing in the bilayer on AMP-induced pore formation also are described. On the basis of these data, we discuss the present state of understanding of the interaction of AMPs with lipid bilayers and future prospects for AMP studies.

Keywords

Antimicrobial peptides Giant unilamellar vesicle Pore formation Local rupture Translocation across membranes Lipid bilayers Elementary process Rate constant Membrane tension 

References

  1. Alam JM, Kobayashi T, Yamazaki M (2012) The single giant unilamellar vesicle method reveals lysenin induced pore formation in lipid membranes containing sphingomyelin. Biochemistry 51:5160–5172CrossRefGoogle Scholar
  2. Baumgart T, Hess ST, Webb WW (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425:821–824CrossRefGoogle Scholar
  3. Bigay J, Antonny B (2012) Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev Cell 23:886–895CrossRefGoogle Scholar
  4. Bleicken S, Landeta O, Landajuela L, Basañez G, García-Sáez AJ (2013) Proapoptotic Bax and Bak proteins form stable protein-permeable pores of tunable size. J Biol Chem 2013(288):33241–33252CrossRefGoogle Scholar
  5. Evans E, Heinrich V, Ludwig F, Rawicz W (2003) Dynamic tension spectroscopy and strength of biomembranes. Biophys J 85:2342–2350CrossRefGoogle Scholar
  6. Fuertes G, Garcia-Sáez A, Esteban-Martin S, Giménez D, Sánchez-Muñoz OL, Schwille P, Salgado J (2010) Pores formed by Baxα5 relax to a smaller size and keep at equilibrium. Biophys J 99:2917–2925CrossRefGoogle Scholar
  7. Gregory SM, Pokorny A, Almeida PFF (2009) Magainin 2 revisited: a test of the quantitative model for the all-or-none permeabilization of phospholipid vesicles. Biophys J 96:116–131CrossRefGoogle Scholar
  8. Hasan M, Karal MAS, Levadnyy V, Yamazaki M (2018a) Mechanism of initial stage of pore formation induced by antimicrobial peptide magainin 2. Langmuir 34:3349–3362CrossRefGoogle Scholar
  9. Hasan M, Saha SK, Yamazaki M (2018b) Effect of membrane tension on transbilayer movement of lipids. J Chem Phys 148:245101CrossRefGoogle Scholar
  10. Hwang PM, Vogel HJ (1998) Structure-function relationships of antimicrobial peptides. Biochem Cell Biol 76:235–246CrossRefGoogle Scholar
  11. Islam MZ, Ariyama H, Alam JM, Yamazaki M (2014a) Entry of cell-penetrating peptide transportan 10 into a single vesicle by translocating across lipid membrane and its induced pores. Biochemistry 53:386–396CrossRefGoogle Scholar
  12. Islam MZ, Alam JM, Tamba Y, Karal MAS, Yamazaki M (2014b) The single GUV method for revealing the functions of antimicrobial, pore-forming toxin, and cell-penetrating peptides or proteins. Phys Chem Chem Phys 16:15752–15767CrossRefGoogle Scholar
  13. Islam MZ, Sharmin S, Levadnyy V, Shibly SUA, Yamazaki M (2017) Effects of mechanical properties of lipid bilayers on entry of cell-penetrating peptides into single vesicles. Langmuir 33:2433–2443CrossRefGoogle Scholar
  14. Islam MZ, Sharmin S, Moniruzzaman M, Yamazaki M (2018) Elementary processes for the entry of cell-penetrating peptides into lipid bilayer vesicles and bacterial cells. Appl Microbiol Biotechnol 102:3879–3892CrossRefGoogle Scholar
  15. Israelachvili JN (1992) Intermolecular & surface forces, 2nd edn. Academic, New YorkGoogle Scholar
  16. Karal MAS, Alam JM, Takahashi T, Levadny V, Yamazaki M (2015) Stretch-activated pore of antimicrobial peptide magainin 2. Langmuir 31:3391–3401CrossRefGoogle Scholar
  17. Levadny V, Tsuboi T, Belaya M, Yamazaki M (2013) Rate constant of tension-induced pore formation in lipid membranes. Langmuir 29:3848–3852CrossRefGoogle Scholar
  18. Lipowsky R, Sackmann E (eds) (1995) Structure and dynamics of membranes. Elsevier Science BV, AmsterdamGoogle Scholar
  19. Ludtke SJ, He K, Heller KH, Harroun TA, Yang L, Huang HW (1996) Membrane pores induced by magainin. Biochemistry 35:13723–13728CrossRefGoogle Scholar
  20. Madani F, Lindberg S, Langel Ű, Futaki S, Gräslund A (2011) Mechanisms of cellular uptake of cell-penetrating peptides. J Biophys 2011:414729CrossRefGoogle Scholar
  21. Matsuzaki K, Murase K, Fujii N, Miyajima K (1995) Translocation of a channel-forming antimicrobial peptide, magainin 2, across lipid bilayers by forming a pore. Biochemistry 34:6521–6526CrossRefGoogle Scholar
  22. Matsuzaki K, Murase O, Fujii N, Miyajima K (1996) An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 35:11361–11368CrossRefGoogle Scholar
  23. Matsuzaki K, Sugishita K, Ishibe N, Ueha M, Nakata S, Miyajima K, Epand RM (1998) Relationship of membrane curvature to the formation of pores by magainin 2. Biochemistry 37:11856–11863CrossRefGoogle Scholar
  24. McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438:605–611CrossRefGoogle Scholar
  25. Melo MN, Ferre R, Castanho ARB (2009) Antimicrobial peptides: linking partition, activity and high membrane-bound concentrations. Nat Rev Microbiol 8:1–5Google Scholar
  26. Moghal MMR, Islam MZ, Sharmin S, Levadnyy V, Moniruzzaman M, Yamazaki M (2018) Continuous detection of entry of cell-penetrating peptide transportan 10 into single vesicles. Chem Phys Lipids 212:120–129CrossRefGoogle Scholar
  27. Moniruzzaman M, Alam JM, Dohra H, Yamazaki M (2015) Antimicrobial peptide lactoferricin B-induced rapid leakage of internal contents from single giant unilamellar vesicles. Biochemistry 54:5802–5814CrossRefGoogle Scholar
  28. Moniruzzaman M, Islam MZ, Sharmin S, Dohra H, Yamazaki M (2017) Entry of a six-residue antimicrobial peptide derived from lactoferricin B into single vesicles and Escherichia coli cells without damaging their membranes. Biochemistry 56:4419–4431CrossRefGoogle Scholar
  29. Müller P, Schiller S, Wieprecht T, Dathe M, Herrmann A (2000) Continuous measurement of rapid transbilayer movement of a pyrene-labeled phospholipid analogue. Chem Phys Lipids 106:89–99CrossRefGoogle Scholar
  30. Nekhotiaeva N, Elmquist A, Rajarao GK, Hällbrink M, Langel C, Good L (2004) Cell entry and antimicrobial properties of eukaryotic cell-penetrating peptides. FASEB J 18:394–396CrossRefGoogle Scholar
  31. Propheter DC, Chara AL, Harris TA, Ruhn KA, Hooper LV (2017) Resistin-like molecule β is a bactericidal protein that promotes spatial segregation of the microbiota and the colonic epithelium. Proc Natl Acad Sci U S A 114:11027–11033CrossRefGoogle Scholar
  32. Qian S, Wang W, Yang L, Huang HW (2008) Structure of transmembrane pore induced by Bax-derived peptide: evidence for lipidic pores. Proc Natl Acad Sci U S A 105:17379–17383CrossRefGoogle Scholar
  33. Rawictz W, Olbrich KC, McIntosh T, Needham D, Evans E (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79:328–339CrossRefGoogle Scholar
  34. Sachs F (2010) Stretch-activated ion channels: what are they? Physiology 25:50–56CrossRefGoogle Scholar
  35. Sandre O, Moreaux L, Brochard-Wyard F (1999) Dynamics of transient pores in stretched vesicles. Proc Natl Acad Sci U S A 96:10591–10596CrossRefGoogle Scholar
  36. Sukharev SI, Blount P, Martinac B, Blattner FR, Kung C (1994) A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368:265–268CrossRefGoogle Scholar
  37. Tamba Y, Yamazaki M (2005) Single giant unilamellar vesicle method reveals effect of antimicrobial peptide, magainin 2, on membrane permeability. Biochemistry 44:15823–15833CrossRefGoogle Scholar
  38. Tamba Y, Yamazaki M (2009) Magainin 2-induced pore formation in membrane depends on its concentration in membrane interface. J Phys Chem B 113:4846–4852CrossRefGoogle Scholar
  39. Tamba Y, Ohba S, Kubota M, Yoshioka H, Yoshioka H, Yamazaki M (2007) Single GUV method reveals interaction of tea catechin (-)-epigallocatechin gallate with lipid membranes. Biophys J 92:3178–3194CrossRefGoogle Scholar
  40. Tamba Y, Ariyama H, Levadny V, Yamazaki M (2010) Kinetic pathway of antimicrobial peptide magainin 2-induced pore formation in lipid membranes. J Phys Chem B 114:12018–12026CrossRefGoogle Scholar
  41. Tanaka T, Sano R, Yamashita Y, Yamazaki M (2004) Shape changes and vesicle fission of giant unilamellar vesicles of liquid-ordered phase membrane induced by lysophosphatidylcholine. Langmuir 20:9526–9534CrossRefGoogle Scholar
  42. Wade D, Boman A, Wahlin B, Drain CM, Andreu A, Boman HG, Merrifield RB (1990) All-D amino acid-containing channel-forming antibiotic peptides. Proc Natl Acad Sci U S A 87:4761–4765CrossRefGoogle Scholar
  43. Wakabayashi H, Matsumoto H, Hashimoto K, Teraguchi S, Takase M, Hayasawa H (1999) N-acylated and D enantiomer derivatives of a nonamer core peptide of lactoferricin B showing improved antimicrobial activity. Antimicrob Agents Chemother 43:1267–1269CrossRefGoogle Scholar
  44. Yamazaki M (2008) The single GUV method to reveal elementary processes of leakage of internal contents from liposomes induced by antimicrobial substances. Adv Planar Lipid Bilayers Liposomes 7:121–142CrossRefGoogle Scholar
  45. Yang LT, Weiss M, Lehrer RI, Huang HW (2000) Crystallization of antimicrobial pores in membranes: magainin and protegrin. Biophys J 79:2002–2009CrossRefGoogle Scholar
  46. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Integrated Bioscience Section, Graduate School of Science and TechnologyShizuoka UniversityShizuokaJapan
  2. 2.Nanomaterials Research Division, Research Institute of ElectronicsShizuoka UniversityShizuokaJapan
  3. 3.Department of Physics, Graduate School of ScienceShizuoka UniversityShizuokaJapan

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