Skip to main content

Advertisement

Log in

Elementary processes for the entry of cell-penetrating peptides into lipid bilayer vesicles and bacterial cells

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Cell-penetrating peptides (CPPs) can translocate across the plasma membrane of living eukaryotic cells and enter the cytosol without significantly affecting cell viability. Consequently, CPPs have been used for the intracellular delivery of biological cargo such as proteins and oligonucleotides. However, the mechanisms underlying the translocation of CPPs across the plasma membrane remain unclear. In this mini-review, we summarize the experimental results regarding the entry of CPPs into lipid bilayer vesicles obtained using three methods: the large unilamellar vesicle (LUV) suspension method, the giant unilamellar vesicle (GUV) suspension method, and the single GUV method. The advantages and disadvantages of these methods are also discussed. Experimental results to date clearly indicate that CPPs can translocate across lipid bilayers and enter the vesicle lumen. Three models for the mechanisms and pathways by which CPPs translocate across lipid bilayers are described: (A) through pores induced by CPPs, (B) through transient prepores, and (C) via formation of inverted micelles. Both the pathway of translocation and the efficiency of entry of CPPs depend on the lipid composition of the bilayer and the type of CPP. We also describe the interaction of CPPs with bacterial cells. Some CPPs have strong antimicrobial activities. There are two modes of action of CPPs on bacterial cells: CPPs can induce damage to the plasma membrane and thus increase permeability, or CPPs enter the cytosol of bacterial cells without damaging the plasma membrane. The information currently available on the elementary processes by which CPPs enter lipid bilayer vesicles and bacterial cells is valuable for elucidating the mechanisms of entry of CPPs into the cytosol of various eukaryotic cells.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Akimov SA, Volynsky PE, Galimzyanov TR, Kuzmin PI, Pavlov KV, Batishchev OV (2017) 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  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 

  • Aota-Nakano Y, Li SJ, Yamazaki M (1999) Effects of electrostatic interaction on the phase stability and structures of cubic phases of monoolein/oleic acid mixture membranes. Biochim Biophys Acta 1461:96–102

    Article  CAS  PubMed  Google Scholar 

  • Bárány-Wallje E, Keller S, Serowy S, Geibel S, Pohl P, Bienert M, Dathe M (2005) A critical reassessment of penetratin translocation across lipid membranes. Biophys J 89:2513–2521

    Article  PubMed  PubMed Central  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  Google Scholar 

  • Baumgart T, Hess ST, Webb WW (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425:821–824

    Article  CAS  PubMed  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 

  • 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 

  • Bigay J, Antonny B (2012) Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev Cell 23:886–895

    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 

  • 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 

  • Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902

    Article  CAS  PubMed  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 

  • Duchardt F, Fotin-Mieczek M, Schwarz H, Fischer R, Brock R (2007) A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 8:848–866

    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 

  • Elmquist A, Lindgren M, Bartfai T, Langel U (2001) VE-cadherin-derived cell-penetrating peptide, VEC, with carrier functions. Exp Cell Res 269:237–244

    Article  CAS  PubMed  Google Scholar 

  • El-Sayed A, Futaki S, Harashima H (2009) Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment. AAPS J 11:13–21

    Article  CAS  PubMed  PubMed Central  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 

  • Fischer R, Köhler K, Fotin-Mleczek M, Brock R (2004) A stepwise dissection of the intracellular fate of cationic cell-penetrating peptides. J Biol Chem 279:12625–12635

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Futaki S, Suzuki T, Ohashi W, Yagami T, Tanaka S, Ueda K, Sugiura Y (2001) Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J Biol Chem 276:5836–5840

    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 

  • Herce HD, Garcia AE (2007) Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes. Proc Natl Acad Sci U S A 104:20805–20810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herce HD, Garcia AE, Litt J, Kane RS, Martin P, Enrique N, Rebolledo A, Milesi V (2009) Arginine-rich peptides destabilizes the plasma membrane, consistent with a pore formation translocation mechanism of cell-penetrating peptides. Biophys J 97:1917–1925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    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 

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

    Article  CAS  PubMed  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  Google Scholar 

  • Ladokhin AS, Wimley WC, White SH (1995) Leakage of membrane vesicle contents: determination of mechanism using fluorescence requenching. Biophys J 69:1964–1971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lakowicz JR (2006) Principles of fluorescence spectroscopy, 3rd edn. Springer, New York

    Book  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 

  • 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 

  • Lipowsky R, Sackmann E (eds) (1995) Structure and dynamics of membranes. Elsevier Science BV, Amsterdam

    Google Scholar 

  • Lonhienne TGA, Sagulenko E, Webb RI, Kee K-C, Franke J, Devos DP, Nouwens A, Carroll BJ, Fuerst JA (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sic USA 107:12883–12888

    Article  CAS  Google Scholar 

  • Luzzati V (1997) Biological significance of lipid polymorphism: the cubic phases. Curr Opin Struct Biol 7:661–668

    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 2011:414729

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438:605–611

    Article  CAS  PubMed  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 

  • 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 18:394–396

    Article  CAS  PubMed  Google Scholar 

  • Oka T, Tsuboi T, Saiki T, Takahashi T, Alam JM, Yamazaki M (2014) Initial step of pH-jump-induced lamellar to bicontinuous cubic phase transition in dioleoylphosphatidylserine/monoolein. Langmuir 30:8131–8140

    Article  CAS  PubMed  Google Scholar 

  • Okamoto Y, Masum SM, Miyazawa H, Yamazaki M (2008) Low pH-induced transformation of bilayer membrane into bicontinuous cubic phase in dioleoyl-phosphatidylserine/monoolein membranes. Langmuir 24:3400–3406

    Article  CAS  PubMed  Google Scholar 

  • Palm C, Netzereab S, Hällbrink M (2006) Quantitatively determined uptake of cell-penetrating peptides in non-mammalian cells with an evaluation of degradation and antimicrobial effects. Peptides 27:1710–1716

    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 

  • Pisa MD, Chassaing G, Swiecicki J-M (2015) Translocation mechanism(s) of cell-penetrating peptides: biophysical studies using artificial membrane bilayers. Biochemistry 54:194–207

    Article  PubMed  Google Scholar 

  • Pooga M, Hällbrink M, Zorko M, Langel Ű (1998) Cell penetration by transportan. FASEB J 12:67–77

    Article  CAS  PubMed  Google Scholar 

  • Pooga M, Kut C, Kihlmark M, Hällbrink M, Fernaeus S, Raid R, Land T, Hallberg E, Bartfai TM, Langel Ű (2001) Cellular translocation of proteins by transportan. FASEB J 15:1451–1453

    Article  CAS  PubMed  Google Scholar 

  • Qian Z, Dougherty PG, Pei D (2015) Monitoring the cytosolic entry of cell-penetrating peptides using a pH-sensitive fluorophore. Chem Commun 51:2162–2165

    Article  CAS  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 

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

    Article  Google Scholar 

  • Richard JP, Melikov K, Vivès E, Ramos C, Verbeure B, Gait MJ, Chernomordik LV, Lebleu B (2003) Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J Biol Chem 278:585–590

    Article  CAS  PubMed  Google Scholar 

  • Rothbard JB, Jessop TC, Wender PA (2005) Adaptive translocation: the role of hydrogen bonding and membrane potential in the uptake of guanidium-rich transporters into cells. Adv Drug Deliv Rev 57:495–504

    Article  CAS  PubMed  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 

  • Seddon JM, Templer RH (1995) Polymorphism of lipid-water systems. In: Lipowsky R, Sackmann E (eds) Structure and dynamics of membranes. Elsevier Science BV, Amsterdam, pp 97–160

    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 

  • 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 

  • 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 

  • Sun D, Forsman J, Lund M, Woodward CE (2014) Effect of arginine-rich cell penetrating peptides on membrane pore formation and life-times: a molecular simulation study. Phys Chem Chem Phys 16:20785–20795

    Article  CAS  PubMed  Google Scholar 

  • Sun D, Forsman J, Woodward CE (2015) Atomistic molecular simulations suggest a kinetic model for membrane translocation by arginine-rich peptides. J Phys Chem B 119:14413–14420

    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 

  • Takechi Y, Yoshii H, Tanaka M, Kawakami T, Aimoto S, Saito H (2011) Physicochemical mechanism for the enhanced ability of lipid membrane penetration of polyarginine. Langmuir 27:7099–7107

    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 

  • 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 20:9526–9534

    Article  CAS  PubMed  Google Scholar 

  • Ter-Avetisyan G, Tünnemann G, Nowak D, Nitschke M, Herrmann A, Drab M, Cardoso MC (2009) Cell entry of arginine-rich peptides is independent of endocytosis. J Biol Chem 284:3370–3378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terrone D, Sang SLW, Roudaia L, Silvius JR (2003) Penetratin and related cell-penetrating cationic peptides can translocate across lipid bilayers in the presence of a transbilayer potential. Biochemistry 42:13787–13799

    Article  CAS  PubMed  Google Scholar 

  • Thorén PEG, Persson D, Karlsson M, Nordén B (2000) The Antennapedia peptide penetratin translocates across lipid bilayers—the first direct observation. FEBS Lett 482:265–268

    Article  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  Google Scholar 

  • Vivès E, Brodin P, Lebleu B (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 272:16010–16017

    Article  PubMed  Google Scholar 

  • Wadia JS, Stan RV, Dowdy SE (2004) Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 37:147–195

    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 T-Y, Sun Y, Muthukrishnan N, Erazo-Oliveras A, Hajjar K, Pellois J-P (2016) Membrane oxidation enables the cytosolic entry of polyarginine cell-penetrating peptides. J Biol Chem 291:7902–7814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wheaten SA, Ablan FDO, Spaller BL, Trieu JM, Almeida PF (2013) Translocation of cationic amphipathic peptides across the membranes of pure phospholipid giant vesicles. J Am Chem Soc 135:16517–16525

    Article  CAS  PubMed  PubMed Central  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, Miyazu M, Asano T, Yuba A, Kume N (1994) Direct evidence of induction of interdigitated gel structure in large unilamellar vesicles of dipalmitoylphophatidylcholine by ethanol: studies by excimer method and high-resolution electron cyromicroscopy. Biophys J 66:729–733

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Yesylevskyy S, Marrink S-J, Mark AE (2009) Alternative mechanisms for the interaction of the cell-penetrating peptides penetratin and the TAT peptide with lipid bilayers. Biophys J 97:40–49

    Article  CAS  PubMed  PubMed Central  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) from the Japan Society for the Promotion of Science (JSPS) to M.Y. This work was also supported in part by the Cooperative Research Project of the Research Center for Biomedical Engineering.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masahito Yamazaki.

Ethics declarations

Ethical approval

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

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Islam, M.Z., Sharmin, S., Moniruzzaman, M. et al. Elementary processes for the entry of cell-penetrating peptides into lipid bilayer vesicles and bacterial cells. Appl Microbiol Biotechnol 102, 3879–3892 (2018). https://doi.org/10.1007/s00253-018-8889-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-018-8889-5

Keywords

Navigation