Skip to main content
SpringerLink
Log in

The role of membrane tension in the action of antimicrobial peptides and cell-penetrating peptides in biomembranes

  • Review
  • Published:
Biophysical Reviews Aims and scope Submit manuscript

Abstract

For antimicrobial peptides (AMPs) with antimicrobial and bactericidal activities and cell-penetrating peptides (CPPs) with activity to permeate through plasma membrane, their interactions with lipid bilayer region in plasma membrane play important roles in these functions. However, the elementary processes and mechanisms of their functions have not been clear. The single giant unilamellar vesicle (GUV) method has revealed the details of elementary processes of interaction of some AMPs and CPPs with lipid vesicles. In this review, we summarize the mode of action of AMPs such as magainin 2 (Mag) and CPPs such as transportan 10 (TP10), revealed by the single GUV methods, and especially we focus on the role of membrane tension in actions of Mag and TP10 and the mechanisms of their actions. First, we explain the characteristics of the single GUV method briefly. Next, we summarize the recent view on the effect of tension on physical properties of lipid bilayers and describe the role of tension in actions of Mag and TP10. Some experimental results indicate that Mag-induced pore is a stretch-activated pore. The effect of packing of transbilayer asymmetric lipid on Mag-induced pore formation is described. On the other hand, entry of fluorescent dye, carboxyfluorescein (CF)-labeled TP10 (i.e., CF-TP10), into single GUVs without pore formation is affected by tension and high concentration of cholesterol. Pre-pore model for translocation of CF-TP10 across lipid bilayer is described. The experimental methods and their analysis described here are useful for investigation of functions of the other types of AMPs, CPPs, and proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aguilera O, Ostolaza H, Quirós LM, Fierro JF (1999) Permeabilizing action of an antimicrobial lactoferricin-derived peptide on bacterial and artificial membranes. FEBS Lett 462:273–277

    Article  CAS  PubMed  Google Scholar 

  • Akimov SA, Volynsky PE, Galimzyanov TR, Kuzmin PI, Pavlov KV, Batishchev OV (2017a) Pore formation in lipid membrane I: continuous reversible trajectory from intact bilayer through hydrophobic defect to transversal pore. Sci Rep 7:12152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Akimov SA, Volynsky PE, Galimzyanov TR, Kuzmin PI, Pavlov KV, Batishchev OV (2017b) Pore formation in lipid membrane II: energy landscape under external stress. Sci Rep 7:12509

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alam JM, Kobayashi T, Yamazaki M (2012) The single giant unilamellar vesicle method reveals lysenin-induced pore formation in lipid membranes containing sphingomyelin. Biochemistry 51:5160–5172

    Article  CAS  PubMed  Google Scholar 

  • Awasthi N, Hub JS (2016) Simulations of pore formation in lipid membranes: reaction coordinates, convergence, hysteresis, and finite-size effects. J Chem Theory Comput 12:3261–3269

    Article  CAS  PubMed  Google Scholar 

  • Bai J, Pagano RE (1997) Measurement of spontaneous transfer and transbilayer movement of BODIPY-labeled lipids in lipid vesicles. Biochemistry 36:8840–8848

    Article  CAS  PubMed  Google Scholar 

  • Bárány-Wallje E, Gaur J, Lundberg P, Langle Ű, Gräslund A (2007) Differential membrane perturbation caused by the cell penetrating peptide TP10 depending on attached cargo. FEBS Lett 581:2389–2393

    Article  PubMed  CAS  Google Scholar 

  • Bechara C, Sagan S (2013) Cell-penetrating peptides: 20 years later, where do we stand? FEBS Lett 587:1693–1702

    Article  CAS  PubMed  Google Scholar 

  • Bechniger B, Zasloff M, Opella SJ (1993) Structure and orientation of the antibiotic peptide magainin in membranes by solid-state nuclear magnetic resonance spectroscopy. Protein Sci 2:2077–2084

    Article  Google Scholar 

  • Berlose J-P, Convert O, Derossi D, Brunissen A, Chassaing G (1996) Conformational and associative behaviours of the third helix of antennapedia homeodomain in membrane-mimetic environments. Eur J Biochem 242:372–386

    Article  CAS  PubMed  Google Scholar 

  • Binder H, Lindblom G (2003) Charge-dependent translocation of the Trojan peptide penetratin across lipid membranes. Biophys J 85:982–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brochard-Wyart F, De Gennes P-G, Sandre O (2000) Transient pores in stretched vesicles: role of leak-out. Physics A 278:32–51

    Article  CAS  Google Scholar 

  • Buch I, Harvey MJ, Giorgino T, Anderson DP, Fabritiis GD (2010) High-throughput all-atom molecular dynamics simulations using distributed computing. J Chem Inf Model 50:397–403

    Article  CAS  PubMed  Google Scholar 

  • Ciobanasu C, Siebrasse J, Kubitscheck U (2010) Cell-penetrating HIV1 TAT peptides can generate pores in model membranes. Biophys J 99:153–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drin G, Déméné H, Temsamani J, Brasseur R (2001) Translocation of the pAntp peptide and its amphipathic analogue AP-2AL. Biochemistry 40:1824–1834

    Article  CAS  PubMed  Google Scholar 

  • EL-Andaloussi S, Johansson H, Magnusdottir A, Järver P, Lundberg P, Langel Ű (2005) TP10, a delivery vector for decoy oligonucleotides targeting the Myc protein. J Control Release 110:189–201

    Article  CAS  PubMed  Google Scholar 

  • Evans E, Smith BA (2011) Kinetics of hole nucleation in biomembrane rupture. New J Phys 13:095010

    Article  PubMed  PubMed Central  Google Scholar 

  • Evans E, Heinrich V, Ludwig F, Rawicz W (2003) Dynamic tension spectroscopy and strength of biomembranes. Biophys J 85:2342–2350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fadzen C, Wolfe JM, Cho C-F, Chiocca EA, Lawler SE, Pentelute BL (2017) Perfluoroarene-based peptide macrocycles to enhance penetration across the blood-brain barrier. J Am Chem Soc 139:15628–15631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fanghänel S, Wadhwani P, Strandberg E, Verdurmen WPR, Bűeck J, Ehni S, Mykhailiuk PK, Afonin S, Gerthsen D, Komarov IV, Brock R, Ulrich AS (2014) Structure analysis and conformational transitions of the cell penetrating peptide transportan 10 in the membrane-bound state. PLoS One 9:e99653

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fuertes G, Giménez D, Esteban-Martín S, Sánchez-Muñoz O, Salgado J (2011) A lipocentric view of peptide-induced pores. Eur Biophys J 40:399–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardiner CW (1990) Handbook of stochastic methods for physics, chemistry, and the natural sciences. Springer-Verlag, Berlin

    Google Scholar 

  • Gesell J, Zasloff M, Opella SJ (1997) Two-dimensional 1H NMR experiments show that the 23-residue magainin antibiotic peptide is an α-helix in dodecylphosphocholine micelles, sodium dodecylsulfate micelles, and trifluoroethanol/water solution. J Biomol NMR 9:127–135

    Article  CAS  PubMed  Google Scholar 

  • Glaser RW, Leikin SL, Chernomordik LV, Pastushenko VF, Sokirko AI (1988) Reversible electrical breakdown of lipid bilayers: formation and evolution of pores. Biochim Biophys Acta 940:275–287

    Article  CAS  PubMed  Google Scholar 

  • Gozen I, Dommersnes P (2014) Pore dynamics in lipid membranes. Eur Phys J 223:1813–1829

    CAS  Google Scholar 

  • 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 96:116–131

    Article  CAS  PubMed  Google Scholar 

  • Hänggi P, Talkner P, Borkovec M (1990) Reaction-rate theory: fifty years after Kramers. Rev Mod Phys 62:251–341

    Article  Google Scholar 

  • Hasan M, Yamazaki M (2019) Elementary processes and mechanisms of interactions of antimicrobial peptides with membranes-single GUV studies. In: Matsuzaki K (ed) Antimicrobial peptides: basic for clinical application. Springer Nature, Singapore, pp 17–32

    Chapter  Google Scholar 

  • Hasan M, Karal MAS, Levadnyy V, Yamazaki M (2018a) Mechanism of initial stage of pore formation induced by antimicrobial peptide magainin 2. Langmuir 34:3349–3362

    Article  CAS  PubMed  Google Scholar 

  • Hasan M, Saha SK, Yamazaki M (2018b) Effect of membrane tension on transbilayer movement of lipids. J Chem Phys 148:245101

    Article  PubMed  CAS  Google Scholar 

  • Hille B (1992) Ionic channels of excitable membranes, 2nd edn. Sinauer Association Inc., Massachusetts

    Google Scholar 

  • Homan R, Pownall HJ (1988) Transbilayer diffusion of phospholipids: dependence on headgroup structure and acyl chain length. Biochim Biophys Acta Biomembr 938:155–166

    Article  CAS  Google Scholar 

  • Huang HW (2009) Free energies of molecular bound states in lipid bilayers: lethal concentrations of antimicrobial peptides. Biophys J 96:3263–3272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang PM, Vogel HJ (1998) Structure-function relationships of antimicrobial peptides. Biochem Cell Biol 76:235–246

    Article  CAS  PubMed  Google Scholar 

  • 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 53:386–396

    Article  CAS  PubMed  Google Scholar 

  • 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 16:15752–15767

    Article  CAS  PubMed  Google Scholar 

  • 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 33:2433–2443

    Article  CAS  PubMed  Google Scholar 

  • 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 102:3879–3892

    Article  CAS  PubMed  Google Scholar 

  • Israelachvili JN (1992) Intermolecular and surface forces, 2nd edn. Academic Press, New York

    Google Scholar 

  • Jing W, Svendsen JS, Vogel HJ (2006) Comparison of NMR structures and model-membrane interactions of 15-residue antimicrobial peptides derived from bovine lactoferricin. Biochem Cell Biol 84:312–326

    Article  CAS  PubMed  Google Scholar 

  • Karal MAS, Yamazaki M (2015) Activation energy of tension-induced pore formation in lipid membranes. J Chem Phys 143:081103

    Article  PubMed  CAS  Google Scholar 

  • Karal MAS, Alam JM, Takahashi T, Levadny V, Yamazaki M (2015a) Stretch-activated pore of antimicrobial peptide magainin 2. Langmuir 31:3391–3401

    Article  CAS  PubMed  Google Scholar 

  • Karal MAS, Levadny V, Tsuboi T, Belaya M, Yamazaki M (2015b) Electrostatic interaction effects on tension-induced pore formation in lipid membranes. Phys Rev E 92:012708

    Article  CAS  Google Scholar 

  • Karal MAS, Levadnyy V, Yamazaki M (2016) Analysis of constant tension-induced rupture of lipid membranes using activation energy. Phys Chem Chem Phys 18:13487–13495

    Article  CAS  PubMed  Google Scholar 

  • Karatekin E, Sandre O, Guitouni H, Borghi N, Puech P–H, Brochard-Wyart F (2003) Cascades of transient pores in giant vesicles: line tension and transport. Biophys J 84:1734–1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawamoto S, Takasu M, Miyakawa T, Morikawa R, Oda T, Futaki S, Nagao H (2011) Inverted micelles formation of cell-penetrating peptide studied by coarse-grained simulation: importance of attractive force between cell-penetrating peptides and lipid head group. J Chem Phys 134:095103

    Article  PubMed  CAS  Google Scholar 

  • Kwok R, Evans E (1981) Thermoelasticity of large lecithin bilayer vesicles. Biophys J 35:637–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee M-T, Chen F-Y, Huang HW (2004) Energetics of pore formation induced by membrane active peptides. Biochemistry 43:3590–3599

    Article  CAS  PubMed  Google Scholar 

  • Levadny V, Tsuboi T, Belaya M, Yamazaki M (2013) Rate constant of tension-induced pore formation in lipid membranes. Langmuir 29:3848–3852

    Article  CAS  PubMed  Google Scholar 

  • Levina N, Totemeyer S, Stokes NR, Louis P, Jones MA, Booth IR (1999) Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18:1730–1737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li SJ, Yamashita Y, Yamazaki M (2001) Effect of electrostatic interactions on phase stability of cubic phases of membranes of monoolein/dioleoylphosphatidic acid mixture. Biophys J 81:983–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lister JD (1975) Stability of lipid bilayers and red blood cell membranes. Phys Lett A 53:193–194

    Article  Google Scholar 

  • Ludtke SJ, He K, Heller KH, Harroun TA, Yang L, Huang HW (1996) Membrane pores induced by magainin. Biochemistry 35:13723–13728

    Article  CAS  PubMed  Google Scholar 

  • Madani F, Lindberg S, Langel Ű, Futaki S, Gräslund A (2011) Mechanisms of cellular uptake of cell-penetrating peptides. J Biophysics 414729

  • Magzoub M, Gräslund A (2004) Cell-penetrating peptides: small from inception to application. Q Rev Biophys 37:147–195

    Article  CAS  PubMed  Google Scholar 

  • 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 34:6521–6526

    Article  CAS  PubMed  Google Scholar 

  • 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 35:11361–11368

    Article  CAS  PubMed  Google Scholar 

  • 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 37:11856–11863

    Article  CAS  PubMed  Google Scholar 

  • McConnell HM, Kornberg RD (1971) Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry 10:1111–1120

    Article  CAS  PubMed  Google Scholar 

  • Melikov KC, Frolov VA, Shcherbakov A, Samsonov AV, Chizmadzhev YA, Chernomordik LV (2001) Voltage-induced nonconductive pre-pores and metastable single pores in unmodified planar lipid bilayer. Biophys J 80:1829–1836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melo MN, Ferre R, Castanho ARB (2009) Antimicrobial peptides: linking partition, activity and high membrane-bound concentrations. Nat Rev Microbiol 8:1–5

    Google Scholar 

  • Mishra A, Gordon VD, Yang L, Coridan R, Wong GCL (2008) HIV TAT forms pores in membranes by inducing saddle-spray curvature: potential role of bidentate hydrogen bonding. Angew Chem Int Ed 47:2986–2989

    Article  CAS  Google Scholar 

  • Mishra A, Lai GH, Schmidt NW, Sun VZ, Rodriguez AR, Tong R, Tang L, Cheng J, Deming TJ, Kamei DT, Wong GCL (2011) Translocation of HIV TAT peptide and analogues induced by multiplexed membrane and cytoskeletal interactions. Proc Natl Acad Sci U S A 108:16883–16888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 212:120–129

    Article  CAS  PubMed  Google Scholar 

  • 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 54:5802–5814

    Article  CAS  PubMed  Google Scholar 

  • 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 56:4419–4431

    Article  CAS  PubMed  Google Scholar 

  • Moreno MJ, Estronca LMBB, Vaz WLC (2006) Translocation of phospholipids and dithionite permeability in liquid-ordered and liquid-disordered membranes. Biophys J 91:873–881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano M, Fukuda M, Kudo T, Matsuzaki N, Azuma T, Sekine K, Endo H, Handa T (2009) Flip-flop of phospholipids in vesicles: kinetic analysis with time-resolved small-angle neutron scattering. J Phys Chem B 113:6745–6748

    Article  CAS  PubMed  Google Scholar 

  • Needham D, Nunn RS (1990) Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys J 58:998–1009

    Article  Google Scholar 

  • Parvez F, Alam JM, Dohra H, Yamazaki M (2018) Elementary processes of antimicrobial peptide PGLa-induced pore formation in lipid bilayers. BBA-Biomembranes 1860:2262–2271

    Article  CAS  PubMed  Google Scholar 

  • Persson D, Thorén PEG, Ksbjörner EK, Goksör M, Lincoln P, Nordén B (2004) Vesicles size-dependent translocation of penetratin analogs across lipid membranes. Biochim Biophys Acta 1665:142–155

    Article  CAS  PubMed  Google Scholar 

  • Portet P, Dimova R (2010) A new method for measuring edge tensions and stability of lipid bilayers: effect of membrane composition. Biophys J 99:3264–3273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 114:11027–11033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 105:17379–17383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian Z, Martyna A, Hard RL, Wang J, Appiah-Kubi G, Coss C, Phelps MA, Rossman JS, Pei D (2016) Discovery and mechanism of highly efficient cyclic cell-penetrating peptides. Biochemistry 55:2601–2612

    Article  CAS  PubMed  Google Scholar 

  • Rawicz W, Olbrich KC, McIntosh T, Needham D, Evans E (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79:328–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruczyński J, Rusiecka I, Turecka K, Kozlowska A, Alenowicz M, Gągalo I, Kawiak A, Rekowski P, Waleron K, Kocić I (2019) Transportan10 improves the pharmacokinetics and pharmacodynamics of vancomycin. Sci Rep 9:3247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rusiecka I, Ruczyński J, Kozlowska A, Backtrog E, Mucha P, Kocić I, Rekowski P (2019) TP10-dopamine conjugate as a potential therapeutic agent in the treatment of Parkinson’s disease. Bioconjug Chem 30:760–774

    Article  CAS  PubMed  Google Scholar 

  • Ryham R, Berezovik I, Cohen FS (2011) Aqueous viscosity is the primary source of friction in lipidic pore dynamics. Biophys J 101:2929–2938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sachs F (2010) Stretch-activated ion channels: what are they? Physiology 25:50–56

    Article  CAS  PubMed  Google Scholar 

  • Sakmann B, Neher E (eds) (1995) Single-channel recording, 2nd edn. Plenum Press, New York

    Google Scholar 

  • Sandre O, Moreaux L, Brochard-Wyard F (1999) Dynamics of transient pores in stretched vesicles. Proc Natl Acad Sci U S A 96:10591–10596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharmin S, Islam MZ, Karal MAS, Shibly SUA, Dohra H, Yamazaki M (2016) Effects of lipid composition on the entry of cell-penetrating peptide oligoarginine into single vesicles. Biochemistry 55:4154–4165

    Article  CAS  PubMed  Google Scholar 

  • Shibly SUA, Ghatak C, Karal MAS, Moniruzzaman MM, Yamazaki M (2016) Experimental estimation of membrane tension induced by osmotic pressure. Biophys J 111:2190–2201

    Article  CAS  Google Scholar 

  • Shigematsu T, Koshiyama K, Wada S (2015) Effects of stretching speed on mechanical rupture of phospholipid/cholesterol bilayers: molecular dynamics simulation. Sci Rep 5:15369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigematsu T, Koshiyama K, Wada S (2016) Line tension of the pore edge in phospholipid/cholesterol bilayer from stretch molecular dynamics simulation. J Biomech Sci Tech 11:15–00422

    Google Scholar 

  • Soomets U, Lindgren M, Gallet X, Pooga M, Hällbrink M, Elmquist A, Balaspiri L, Zorko M, Pooga M, Brasseur R, Langel Ű (2000) Deletion analogues of transportan. Biochim Biophys Acta 1467:165–176

    Article  CAS  PubMed  Google Scholar 

  • Srividya N, Muralidharan S (2008) Determination of the line tension of giant vesicles from pore-closing dynamics. J Phys Chem B 112:7147–7152

    Article  CAS  PubMed  Google Scholar 

  • Stalmans S, Bracke N, Wynerdaele E, Gavert B, Peremans K, Burvenich C, Polls I, Spiegeleer BD (2015) Cell-penetrating peptides selectively cross the blood-brain barrier in vivo. PLoS One 10:e0139652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stanzl EG, Trantow BM, Vargas JR, Wender PA (2013) Fifteen years of cell-penetrating, guanidinium-rich molecular transporters: basic science, research tools, and clinical applications. Acc Chem Res 46:2944–2954

    Article  CAS  PubMed  Google Scholar 

  • Strandberg E, Tremouihac P, Wadhwani P, Ulrich AS (2009) Synergetic transmembrane insertion of the heterodimeric PGLa/magainin 2 complex studied by solid-state NMR. Biochim Biophys Acta 1788:1667–1679

    Article  CAS  PubMed  Google Scholar 

  • Sukharev SI, Blount P, Martinac B, Blattner FR, Kung C (1994) A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368:265–268

    Article  CAS  PubMed  Google Scholar 

  • Swiecicki J-M, Bartsch A, Tailhades J, Di Pisa M, Heller B, Chassaing G, Mansuy C, Burlina F, Lavielle S (2014) The efficacies of cell-penetrating peptides in accumulating in large unilamellar vesicles depend on their ability to form inverted micelles. ChemBioChem 15:884–891

    Article  CAS  PubMed  Google Scholar 

  • Tamba Y, Yamazaki M (2005) Single giant unilamellar vesicle method reveals effect of antimicrobial peptide, magainin 2, on membrane permeability. Biochemistry 44:15823–15833

    Article  CAS  PubMed  Google Scholar 

  • Tamba Y, Yamazaki M (2009) Magainin 2-induced pore formation in membrane depends on its concentration in membrane interface. J Phys Chem B 113:4846–4852

    Article  CAS  PubMed  Google Scholar 

  • 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 92:3178–3194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 114:12018–12026

    Article  CAS  PubMed  Google Scholar 

  • Tamba Y, Terashima H, Yamazaki M (2011) A membrane filtering method for the purification of giant unilamellar vesicles. Chem Phys Lipids 164:351–358

    Article  CAS  PubMed  Google Scholar 

  • Thorén PEG, Persson D, Ksbjörner EK, Goksör M, Lincoln P, Nordén B (2004) Membrane binding and translocation of cell-penetrating peptides. Biochemistry 43:3471–3489

    Article  PubMed  CAS  Google Scholar 

  • Tieleman DP, Leontiadou H, Mark AE, Marrink S-J (2003) Simulation of pore formation in lipid bilayers by mechanical stress and electric fields. J Am Chem Soc 125:6382–6383

    Article  CAS  PubMed  Google Scholar 

  • Tolpekina TV, den Otter WK, Briels WJ (2004) Nucleation free energy of pore formation in an amphiphilic bilayer studied by molecular dynamics simulation. J Chem Phys 121:12060–12066

    Article  CAS  PubMed  Google Scholar 

  • Walrant A, Matheron L, Cribier S, Chaignepain S, Jobin M-L, Sagan S, Alves ID (2013) Direct translocation of cell-penetrating peptides in liposomes: a combined mass spectrometry quantification and fluorescence detection study. Anal Biochem 438:1–10

    Article  CAS  PubMed  Google Scholar 

  • Wang Z-J, Frenkel D (2005) Pore nucleation in mechanically stretched bilayer membranes. J Chem Phys 123:154701

    Article  PubMed  CAS  Google Scholar 

  • Wimley WC, Thompson TE (1990) Exchange and flip-flop of dimiristoylphosphatidylcholine in liquid-crystalline, gel, and two-component, two-phase large unilamellar vesicles. Biochemistry 29:1296–1303

    Article  CAS  PubMed  Google Scholar 

  • Wohlert J, den Otter WK, Edholm O, Briels WJ (2006) Free energy of a trans-membrane pore calculated from atomistic molecular dynamics simulations. J Chem Phys 124:154905

    Article  CAS  PubMed  Google Scholar 

  • 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 7:121–142

    Article  CAS  Google Scholar 

  • Yamazaki M, Furuike S, Ito T (2002) Mechanical response of single filamin A (ABP-280) molecules and its role in the actin cytoskeleton. J Muscle Res Cell Motil 23:525–534

    Article  PubMed  Google Scholar 

  • Yandek LE, Pokomy A, Floren A, Knoeike K, Langel Ű, Almeida PFF (2007) Mechanism of the cell-penetrating peptide transportan 10 permeation of lipid bilayers. Biophys J 92:2434–2444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yandek LE, Pokomy A, Almeida PFF (2008) Small changes in the primary structure of transportan 10 alter the thermodynamics and kinetics of its interaction with phospholipid vesicles. Biochemistry 47:3051–3060

    Article  CAS  PubMed  Google Scholar 

  • Yang LT, Weiss M, Lehrer RI, Huang HW (2000) Crystallization of antimicrobial pores in membranes: magainin and protegrin. Biophys J 79:2002–2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 84:5449–5453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395

    Article  CAS  PubMed  Google Scholar 

  • Zorko M, Langel Ű (2005) Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv Drug Deliv Rev 57:529–545

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported in part by a Grant-in-Aid for Scientific Research (B) (No. 15H04361 and 19H03193) from the Japan Society for the Promotion of Science (JSPS) to M.Y.

Author information

Author notes

  1. Moynul Hasan

    Present address: Department of Pharmacy, Jagannath University, Dhaka, 1100, Bangladesh

Authors and Affiliations

  1. Integrated Bioscience Section, Graduate School of Science and Technology, Shizuoka University, Shizuoka, 422-8529, Japan

    Moynul Hasan, Md. Mizanur Rahman Moghal, Samiron Kumar Saha & Masahito Yamazaki

  2. Nanomaterials Research Division, Research Institute of Electronics, Shizuoka University, 836 Oya, Suruga-ku, Shizuoka, 422-8529, Japan

    Masahito Yamazaki

  3. Department of Physics, Faculty of Science, Shizuoka University, Shizuoka, 422-8529, Japan

    Masahito Yamazaki

Authors
  1. Moynul Hasan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Md. Mizanur Rahman Moghal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samiron Kumar Saha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masahito Yamazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masahito Yamazaki.

Ethics declarations

Conflict of interest

Moynul Hasan declares that he has no conflict of interest. Md. Mizanur Rahman Moghal declares that he has no conflict of interest. Samiron Kumar Saha declares that he has no conflict of interest. Masahito Yamazaki declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

This article is part of a Special Issue dedicated to the ‘2018 Joint Conference of the Asian Biophysics Association and Australian Society for Biophysics’ edited by Kuniaki Nagayama, Raymond Norton, Kyeong Kyu Kim, Hiroyuki Noji, Till Böcking, and Andrew Battle.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hasan, M., Moghal, M.M.R., Saha, S.K. et al. The role of membrane tension in the action of antimicrobial peptides and cell-penetrating peptides in biomembranes. Biophys Rev 11, 431–448 (2019). https://doi.org/10.1007/s12551-019-00542-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12551-019-00542-1

Keywords

Search

Navigation