Membrane potential drives direct translocation of cell-penetrating peptides

Cell-penetrating peptides (CPPs) are frequently employed as drug delivery agents with rapid cellular uptake, however, the uptake mechanism and the detailed translocation pathway are at present not completely understood. Both endocytosis and direct translocation through membrane pores have been obser...

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Published inNanoscale Vol. 11; no. 4; pp. 1949 - 1958
Main Authors Gao, Xinli, Hong, Song, Liu, Zhiping, Yue, Tongtao, Dobnikar, Jure, Zhang, Xianren
Format Journal Article
LanguageEnglish
Published England Royal Society of Chemistry 23.01.2019
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Abstract Cell-penetrating peptides (CPPs) are frequently employed as drug delivery agents with rapid cellular uptake, however, the uptake mechanism and the detailed translocation pathway are at present not completely understood. Both endocytosis and direct translocation through membrane pores have been observed in experiments and simulations under different conditions. Here we report the molecular dynamics simulations providing evidence for the direct translocation of CPPs across the membrane driven by the membrane electrostatic potential. The local membrane potential can be produced by the ion concentration imbalance across the membrane, which is ubiquitous in biological environments. Moreover, if positively charged CPPs are adsorbed on the membrane, this further enhances the membrane potential, opening membrane pores through which CPPs can be instantly transported in a chain-like configuration. The classical nucleation theory is applied to estimate the translocation time by calculating the changes in the free energy upon transferring CPPs across the membrane at different potentials, showing good agreement with available experimental measurements. The revealed CPP translocation mechanism can be broadly relevant for cellular processes in biology.
AbstractList Cell-penetrating peptides (CPPs) are frequently employed as drug delivery agents with rapid cellular uptake, however, the uptake mechanism and the detailed translocation pathway are at present not completely understood. Both endocytosis and direct translocation through membrane pores have been observed in experiments and simulations under different conditions. Here we report the molecular dynamics simulations providing evidence for the direct translocation of CPPs across the membrane driven by the membrane electrostatic potential. The local membrane potential can be produced by the ion concentration imbalance across the membrane, which is ubiquitous in biological environments. Moreover, if positively charged CPPs are adsorbed on the membrane, this further enhances the membrane potential, opening membrane pores through which CPPs can be instantly transported in a chain-like configuration. The classical nucleation theory is applied to estimate the translocation time by calculating the changes in the free energy upon transferring CPPs across the membrane at different potentials, showing good agreement with available experimental measurements. The revealed CPP translocation mechanism can be broadly relevant for cellular processes in biology.
Author Dobnikar, Jure
Liu, Zhiping
Gao, Xinli
Zhang, Xianren
Hong, Song
Yue, Tongtao
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30644958$$D View this record in MEDLINE/PubMed
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Cites_doi 10.1021/bi501392n
10.1021/jp107763b
10.1074/jbc.M303045200
10.1016/j.biocel.2012.02.010
10.1093/bioinformatics/btt055
10.1016/j.bbamem.2010.09.009
10.1021/ja053129n
10.1038/nm996
10.1021/acsnano.6b07563
10.1074/jbc.M209548200
10.1021/jp310255r
10.1021/nl049170q
10.1186/1471-2091-5-10
10.1038/ncomms1459
10.1016/S0001-8686(00)00061-0
10.1016/j.bpj.2012.10.027
10.1021/nn4040553
10.1021/ja507790z
10.1016/j.bioelechem.2014.03.009
10.1063/1.470117
10.1073/pnas.1108795108
10.1016/S1359-6446(04)03042-9
10.1016/j.jconrel.2017.04.013
10.1063/1.2217737
10.1021/jp412600e
10.1063/1.464397
10.1039/C2SM26519B
10.1073/pnas.1411817111
10.1074/jbc.272.25.16010
10.1016/j.jconrel.2011.03.011
10.1016/j.bpj.2009.05.066
10.1016/j.addr.2004.10.010
10.1016/j.bbcan.2008.03.001
10.1529/biophysj.104.050617
10.1529/biophysj.108.129437
10.1073/pnas.0435906100
10.1021/ja0482536
10.1021/ja029504i
10.1063/1.1826056
10.1021/bi035293y
10.1021/acsnano.5b07036
10.1007/s00232-010-9277-y
10.1063/1.2052648
10.1073/pnas.0706574105
10.1038/260799a0
10.2174/1389203033487298
10.1002/jcc.20090
10.1021/nl3029637
10.1146/annurev.bb.18.060189.000553
10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
10.1021/jp3095165
10.1016/j.bpj.2010.03.065
10.1002/jcc.540130812
10.1016/j.bpj.2008.11.073
10.1529/biophysj.104.052787
10.1038/ncomms12906
10.1016/S1525-0016(03)00122-9
10.1063/1.2060666
10.1016/j.bpj.2009.03.059
10.1039/C4CP02211D
10.1111/j.1600-0854.2007.00572.x
10.1517/17425247.5.1.105
10.1007/s00232-012-9434-6
10.1016/S0006-3495(97)78845-3
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References Tarek (C8NR10447F-(cit47)/*[position()=1]) 2005; 88
Casciola (C8NR10447F-(cit63)/*[position()=1]) 2014; 100
Foged (C8NR10447F-(cit3)/*[position()=1]) 2007; 5
Gurtovenko (C8NR10447F-(cit42)/*[position()=1]) 2005; 127
Tieleman (C8NR10447F-(cit51)/*[position()=1]) 2003; 125
Duchardt (C8NR10447F-(cit1)/*[position()=1]) 2007; 8
Chen (C8NR10447F-(cit10)/*[position()=1]) 2012; 4
Hu (C8NR10447F-(cit34)/*[position()=1]) 2014; 118
Levine (C8NR10447F-(cit46)/*[position()=1]) 2010; 236
Mishra (C8NR10447F-(cit15)/*[position()=1]) 2011; 108
Huang (C8NR10447F-(cit29)/*[position()=1]) 2013; 104
Hess (C8NR10447F-(cit59)/*[position()=1]) 1997; 18
Vivès (C8NR10447F-(cit18)/*[position()=1]) 1997; 272
Herce (C8NR10447F-(cit12)/*[position()=1]) 2014; 136
Grafmüller (C8NR10447F-(cit66)/*[position()=1]) 2009; 96
Maniti (C8NR10447F-(cit14)/*[position()=1]) 2012; 44
Yesylevskyy (C8NR10447F-(cit37)/*[position()=1]) 2009; 97
Sun (C8NR10447F-(cit30)/*[position()=1]) 2014; 16
Fittipaldi (C8NR10447F-(cit20)/*[position()=1]) 2004; 278
Clarke (C8NR10447F-(cit40)/*[position()=1]) 2001; 89
Terrone (C8NR10447F-(cit17)/*[position()=1]) 2003; 42
Lensink (C8NR10447F-(cit31)/*[position()=1]) 2005; 88
Li (C8NR10447F-(cit53)/*[position()=1]) 2012; 9
Pourmousa (C8NR10447F-(cit36)/*[position()=1]) 2013; 117
Neher (C8NR10447F-(cit38)/*[position()=1]) 1976; 260
Pronk (C8NR10447F-(cit54)/*[position()=1]) 2013; 29
Ferrari (C8NR10447F-(cit19)/*[position()=1]) 2003; 8
Rothbard (C8NR10447F-(cit16)/*[position()=1]) 2004; 126
Li (C8NR10447F-(cit60)/*[position()=1]) 2016; 7
Yesylevskyy (C8NR10447F-(cit24)/*[position()=1]) 2009; 97
Kästner (C8NR10447F-(cit61)/*[position()=1]) 2005; 123
Mao (C8NR10447F-(cit33)/*[position()=1]) 2016; 10
Rossi (C8NR10447F-(cit5)/*[position()=1]) 2012; 116
Wadia (C8NR10447F-(cit22)/*[position()=1]) 2004; 10
Järver (C8NR10447F-(cit4)/*[position()=1]) 2004; 9
Richard (C8NR10447F-(cit21)/*[position()=1]) 2003; 278
Chen (C8NR10447F-(cit32)/*[position()=1]) 2016; 10
Torchilin (C8NR10447F-(cit9)/*[position()=1]) 2003; 100
Sachs (C8NR10447F-(cit41)/*[position()=1]) 2004; 121
Lättig-Tünnemann (C8NR10447F-(cit52)/*[position()=1]) 2011; 2
Vivès (C8NR10447F-(cit7)/*[position()=1]) 2008; 1786
Zorko (C8NR10447F-(cit8)/*[position()=1]) 2005; 57
Di Pisa (C8NR10447F-(cit25)/*[position()=1]) 2014; 54
Säälik (C8NR10447F-(cit2)/*[position()=1]) 2011; 153
Gurtovenko (C8NR10447F-(cit43)/*[position()=1]) 2005; 127
McLaughlin (C8NR10447F-(cit39)/*[position()=1]) 1989; 18
Torchilin (C8NR10447F-(cit6)/*[position()=1]) 2003; 4
Oostenbrink (C8NR10447F-(cit55)/*[position()=1]) 2004; 25
Wallbrecher (C8NR10447F-(cit27)/*[position()=1]) 2017; 256
Tabaei (C8NR10447F-(cit35)/*[position()=1]) 2012; 12
Ciobanasu (C8NR10447F-(cit11)/*[position()=1]) 2010; 99
Berger (C8NR10447F-(cit56)/*[position()=1]) 1997; 72
Darden (C8NR10447F-(cit57)/*[position()=1]) 1993; 98
Lin (C8NR10447F-(cit49)/*[position()=1]) 2013; 7
Herce (C8NR10447F-(cit13)/*[position()=1]) 2009; 97
Kumar (C8NR10447F-(cit62)/*[position()=1]) 1992; 13
Dunkin (C8NR10447F-(cit23)/*[position()=1]) 2010; 115
Herce (C8NR10447F-(cit28)/*[position()=1]) 2007; 104
Tieleman (C8NR10447F-(cit48)/*[position()=1]) 2004; 5
Essmann (C8NR10447F-(cit58)/*[position()=1]) 1995; 103
Delemotte (C8NR10447F-(cit45)/*[position()=1]) 2012; 245
Rao (C8NR10447F-(cit64)/*[position()=1]) 2014; 111
Böckmann (C8NR10447F-(cit50)/*[position()=1]) 2008; 95
Wang (C8NR10447F-(cit65)/*[position()=1]) 2005; 123
Walrant (C8NR10447F-(cit26)/*[position()=1]) 2011; 1808
Kandasamy (C8NR10447F-(cit44)/*[position()=1]) 2006; 125
References_xml – volume: 54
  start-page: 194
  year: 2014
  ident: C8NR10447F-(cit25)/*[position()=1]
  publication-title: Biochemistry
  doi: 10.1021/bi501392n
  contributor:
    fullname: Di Pisa
– volume: 115
  start-page: 1188
  year: 2010
  ident: C8NR10447F-(cit23)/*[position()=1]
  publication-title: J. Phys. Chem. B
  doi: 10.1021/jp107763b
  contributor:
    fullname: Dunkin
– volume: 278
  start-page: 34141
  year: 2004
  ident: C8NR10447F-(cit20)/*[position()=1]
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M303045200
  contributor:
    fullname: Fittipaldi
– volume: 44
  start-page: 869
  year: 2012
  ident: C8NR10447F-(cit14)/*[position()=1]
  publication-title: Int. J. Biochem. Cell Biol.
  doi: 10.1016/j.biocel.2012.02.010
  contributor:
    fullname: Maniti
– volume: 29
  start-page: 845
  year: 2013
  ident: C8NR10447F-(cit54)/*[position()=1]
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btt055
  contributor:
    fullname: Pronk
– volume: 1808
  start-page: 382
  year: 2011
  ident: C8NR10447F-(cit26)/*[position()=1]
  publication-title: Biochim. Biophys. Acta, Biomembr.
  doi: 10.1016/j.bbamem.2010.09.009
  contributor:
    fullname: Walrant
– volume: 127
  start-page: 17570
  year: 2005
  ident: C8NR10447F-(cit43)/*[position()=1]
  publication-title: J. Am. Chem. Soc.
  doi: 10.1021/ja053129n
  contributor:
    fullname: Gurtovenko
– volume: 10
  start-page: 310
  year: 2004
  ident: C8NR10447F-(cit22)/*[position()=1]
  publication-title: Nat. Med.
  doi: 10.1038/nm996
  contributor:
    fullname: Wadia
– volume: 10
  start-page: 11541
  year: 2016
  ident: C8NR10447F-(cit32)/*[position()=1]
  publication-title: ACS Nano
  doi: 10.1021/acsnano.6b07563
  contributor:
    fullname: Chen
– volume: 278
  start-page: 585
  year: 2003
  ident: C8NR10447F-(cit21)/*[position()=1]
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M209548200
  contributor:
    fullname: Richard
– volume: 117
  start-page: 230
  year: 2013
  ident: C8NR10447F-(cit36)/*[position()=1]
  publication-title: J. Phys. Chem. B
  doi: 10.1021/jp310255r
  contributor:
    fullname: Pourmousa
– volume: 4
  start-page: 1827
  year: 2012
  ident: C8NR10447F-(cit10)/*[position()=1]
  publication-title: Nano Lett.
  doi: 10.1021/nl049170q
  contributor:
    fullname: Chen
– volume: 5
  start-page: 10
  year: 2004
  ident: C8NR10447F-(cit48)/*[position()=1]
  publication-title: BMC Biochem.
  doi: 10.1186/1471-2091-5-10
  contributor:
    fullname: Tieleman
– volume: 2
  start-page: 453
  year: 2011
  ident: C8NR10447F-(cit52)/*[position()=1]
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms1459
  contributor:
    fullname: Lättig-Tünnemann
– volume: 89
  start-page: 263
  year: 2001
  ident: C8NR10447F-(cit40)/*[position()=1]
  publication-title: Adv. Colloid Interface Sci.
  doi: 10.1016/S0001-8686(00)00061-0
  contributor:
    fullname: Clarke
– volume: 104
  start-page: 412
  year: 2013
  ident: C8NR10447F-(cit29)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1016/j.bpj.2012.10.027
  contributor:
    fullname: Huang
– volume: 127
  start-page: 17570
  year: 2005
  ident: C8NR10447F-(cit42)/*[position()=1]
  publication-title: J. Am. Chem. Soc.
  doi: 10.1021/ja053129n
  contributor:
    fullname: Gurtovenko
– volume: 7
  start-page: 10799
  year: 2013
  ident: C8NR10447F-(cit49)/*[position()=1]
  publication-title: ACS Nano
  doi: 10.1021/nn4040553
  contributor:
    fullname: Lin
– volume: 136
  start-page: 17459
  year: 2014
  ident: C8NR10447F-(cit12)/*[position()=1]
  publication-title: J. Am. Chem. Soc.
  doi: 10.1021/ja507790z
  contributor:
    fullname: Herce
– volume: 100
  start-page: 11
  year: 2014
  ident: C8NR10447F-(cit63)/*[position()=1]
  publication-title: Bioelectrochemistry
  doi: 10.1016/j.bioelechem.2014.03.009
  contributor:
    fullname: Casciola
– volume: 103
  start-page: 8577
  year: 1995
  ident: C8NR10447F-(cit58)/*[position()=1]
  publication-title: J. Chem. Phys.
  doi: 10.1063/1.470117
  contributor:
    fullname: Essmann
– volume: 108
  start-page: 16883
  year: 2011
  ident: C8NR10447F-(cit15)/*[position()=1]
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.1108795108
  contributor:
    fullname: Mishra
– volume: 9
  start-page: 395
  year: 2004
  ident: C8NR10447F-(cit4)/*[position()=1]
  publication-title: Drug Discovery Today
  doi: 10.1016/S1359-6446(04)03042-9
  contributor:
    fullname: Järver
– volume: 256
  start-page: 68
  year: 2017
  ident: C8NR10447F-(cit27)/*[position()=1]
  publication-title: J. Controlled Release
  doi: 10.1016/j.jconrel.2017.04.013
  contributor:
    fullname: Wallbrecher
– volume: 125
  start-page: 074901
  year: 2006
  ident: C8NR10447F-(cit44)/*[position()=1]
  publication-title: J. Chem. Phys.
  doi: 10.1063/1.2217737
  contributor:
    fullname: Kandasamy
– volume: 118
  start-page: 2670
  year: 2014
  ident: C8NR10447F-(cit34)/*[position()=1]
  publication-title: J. Phys. Chem. B
  doi: 10.1021/jp412600e
  contributor:
    fullname: Hu
– volume: 98
  start-page: 10089
  year: 1993
  ident: C8NR10447F-(cit57)/*[position()=1]
  publication-title: J. Chem. Phys.
  doi: 10.1063/1.464397
  contributor:
    fullname: Darden
– volume: 9
  start-page: 1281
  year: 2012
  ident: C8NR10447F-(cit53)/*[position()=1]
  publication-title: Soft Matter
  doi: 10.1039/C2SM26519B
  contributor:
    fullname: Li
– volume: 111
  start-page: 12684
  year: 2014
  ident: C8NR10447F-(cit64)/*[position()=1]
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.1411817111
  contributor:
    fullname: Rao
– volume: 272
  start-page: 16010
  year: 1997
  ident: C8NR10447F-(cit18)/*[position()=1]
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.272.25.16010
  contributor:
    fullname: Vivès
– volume: 153
  start-page: 117
  year: 2011
  ident: C8NR10447F-(cit2)/*[position()=1]
  publication-title: J. Controlled Release
  doi: 10.1016/j.jconrel.2011.03.011
  contributor:
    fullname: Säälik
– volume: 97
  start-page: 1917
  year: 2009
  ident: C8NR10447F-(cit13)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1016/j.bpj.2009.05.066
  contributor:
    fullname: Herce
– volume: 57
  start-page: 529
  year: 2005
  ident: C8NR10447F-(cit8)/*[position()=1]
  publication-title: Adv. Drug Delivery Rev.
  doi: 10.1016/j.addr.2004.10.010
  contributor:
    fullname: Zorko
– volume: 1786
  start-page: 126
  year: 2008
  ident: C8NR10447F-(cit7)/*[position()=1]
  publication-title: Biochim. Biophys. Acta, Rev. Cancer
  doi: 10.1016/j.bbcan.2008.03.001
  contributor:
    fullname: Vivès
– volume: 88
  start-page: 4045
  year: 2005
  ident: C8NR10447F-(cit47)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1529/biophysj.104.050617
  contributor:
    fullname: Tarek
– volume: 95
  start-page: 1837
  year: 2008
  ident: C8NR10447F-(cit50)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1529/biophysj.108.129437
  contributor:
    fullname: Böckmann
– volume: 100
  start-page: 1972
  year: 2003
  ident: C8NR10447F-(cit9)/*[position()=1]
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.0435906100
  contributor:
    fullname: Torchilin
– volume: 126
  start-page: 9506
  year: 2004
  ident: C8NR10447F-(cit16)/*[position()=1]
  publication-title: J. Am. Chem. Soc.
  doi: 10.1021/ja0482536
  contributor:
    fullname: Rothbard
– volume: 125
  start-page: 6382
  year: 2003
  ident: C8NR10447F-(cit51)/*[position()=1]
  publication-title: J. Am. Chem. Soc.
  doi: 10.1021/ja029504i
  contributor:
    fullname: Tieleman
– volume: 121
  start-page: 10847
  year: 2004
  ident: C8NR10447F-(cit41)/*[position()=1]
  publication-title: J. Chem. Phys.
  doi: 10.1063/1.1826056
  contributor:
    fullname: Sachs
– volume: 42
  start-page: 13787
  year: 2003
  ident: C8NR10447F-(cit17)/*[position()=1]
  publication-title: Biochemistry
  doi: 10.1021/bi035293y
  contributor:
    fullname: Terrone
– volume: 10
  start-page: 1493
  year: 2016
  ident: C8NR10447F-(cit33)/*[position()=1]
  publication-title: ACS Nano
  doi: 10.1021/acsnano.5b07036
  contributor:
    fullname: Mao
– volume: 236
  start-page: 27
  year: 2010
  ident: C8NR10447F-(cit46)/*[position()=1]
  publication-title: J. Membr. Biol.
  doi: 10.1007/s00232-010-9277-y
  contributor:
    fullname: Levine
– volume: 123
  start-page: 144104
  year: 2005
  ident: C8NR10447F-(cit61)/*[position()=1]
  publication-title: J. Chem. Phys.
  doi: 10.1063/1.2052648
  contributor:
    fullname: Kästner
– volume: 104
  start-page: 20805
  year: 2007
  ident: C8NR10447F-(cit28)/*[position()=1]
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.0706574105
  contributor:
    fullname: Herce
– volume: 260
  start-page: 799
  year: 1976
  ident: C8NR10447F-(cit38)/*[position()=1]
  publication-title: Nature
  doi: 10.1038/260799a0
  contributor:
    fullname: Neher
– volume: 4
  start-page: 133
  year: 2003
  ident: C8NR10447F-(cit6)/*[position()=1]
  publication-title: Curr. Protein Pept. Sci.
  doi: 10.2174/1389203033487298
  contributor:
    fullname: Torchilin
– volume: 25
  start-page: 1656–1676
  year: 2004
  ident: C8NR10447F-(cit55)/*[position()=1]
  publication-title: J. Comput. Chem.
  doi: 10.1002/jcc.20090
  contributor:
    fullname: Oostenbrink
– volume: 12
  start-page: 5719
  year: 2012
  ident: C8NR10447F-(cit35)/*[position()=1]
  publication-title: Nano Lett.
  doi: 10.1021/nl3029637
  contributor:
    fullname: Tabaei
– volume: 18
  start-page: 113
  year: 1989
  ident: C8NR10447F-(cit39)/*[position()=1]
  publication-title: Annu. Rev. Biophys. Biophys. Chem.
  doi: 10.1146/annurev.bb.18.060189.000553
  contributor:
    fullname: McLaughlin
– volume: 18
  start-page: 1463
  year: 1997
  ident: C8NR10447F-(cit59)/*[position()=1]
  publication-title: J. Comput. Chem.
  doi: 10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
  contributor:
    fullname: Hess
– volume: 116
  start-page: 14353
  year: 2012
  ident: C8NR10447F-(cit5)/*[position()=1]
  publication-title: J. Phys. Chem. B
  doi: 10.1021/jp3095165
  contributor:
    fullname: Rossi
– volume: 99
  start-page: 153
  year: 2010
  ident: C8NR10447F-(cit11)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1016/j.bpj.2010.03.065
  contributor:
    fullname: Ciobanasu
– volume: 13
  start-page: 1011
  year: 1992
  ident: C8NR10447F-(cit62)/*[position()=1]
  publication-title: J. Comput. Chem.
  doi: 10.1002/jcc.540130812
  contributor:
    fullname: Kumar
– volume: 96
  start-page: 2658
  year: 2009
  ident: C8NR10447F-(cit66)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1016/j.bpj.2008.11.073
  contributor:
    fullname: Grafmüller
– volume: 88
  start-page: 939
  year: 2005
  ident: C8NR10447F-(cit31)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1529/biophysj.104.052787
  contributor:
    fullname: Lensink
– volume: 7
  start-page: 12906
  year: 2016
  ident: C8NR10447F-(cit60)/*[position()=1]
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms12906
  contributor:
    fullname: Li
– volume: 8
  start-page: 284
  year: 2003
  ident: C8NR10447F-(cit19)/*[position()=1]
  publication-title: Mol. Ther.
  doi: 10.1016/S1525-0016(03)00122-9
  contributor:
    fullname: Ferrari
– volume: 123
  start-page: 154701
  year: 2005
  ident: C8NR10447F-(cit65)/*[position()=1]
  publication-title: J. Chem. Phys.
  doi: 10.1063/1.2060666
  contributor:
    fullname: Wang
– volume: 97
  start-page: 40
  year: 2009
  ident: C8NR10447F-(cit24)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1016/j.bpj.2009.03.059
  contributor:
    fullname: Yesylevskyy
– volume: 16
  start-page: 20785
  year: 2014
  ident: C8NR10447F-(cit30)/*[position()=1]
  publication-title: Phys. Chem. Chem. Phys.
  doi: 10.1039/C4CP02211D
  contributor:
    fullname: Sun
– volume: 8
  start-page: 848
  year: 2007
  ident: C8NR10447F-(cit1)/*[position()=1]
  publication-title: Traffic
  doi: 10.1111/j.1600-0854.2007.00572.x
  contributor:
    fullname: Duchardt
– volume: 5
  start-page: 105
  year: 2007
  ident: C8NR10447F-(cit3)/*[position()=1]
  publication-title: Expert Opin. Drug Delivery
  doi: 10.1517/17425247.5.1.105
  contributor:
    fullname: Foged
– volume: 97
  start-page: 40
  year: 2009
  ident: C8NR10447F-(cit37)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1016/j.bpj.2009.03.059
  contributor:
    fullname: Yesylevskyy
– volume: 245
  start-page: 531
  year: 2012
  ident: C8NR10447F-(cit45)/*[position()=1]
  publication-title: J. Membr. Biol.
  doi: 10.1007/s00232-012-9434-6
  contributor:
    fullname: Delemotte
– volume: 72
  start-page: 2002
  year: 1997
  ident: C8NR10447F-(cit56)/*[position()=1]
  publication-title: Biophys. J.
  doi: 10.1016/S0006-3495(97)78845-3
  contributor:
    fullname: Berger
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Snippet Cell-penetrating peptides (CPPs) are frequently employed as drug delivery agents with rapid cellular uptake, however, the uptake mechanism and the detailed...
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SubjectTerms Drug delivery systems
Free energy
Ion concentration
Molecular dynamics
Nucleation
Peptides
Title Membrane potential drives direct translocation of cell-penetrating peptides
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