Cell-penetrating peptides transport therapeutics into cells

Pharmacology and Therapeutics

Volumn 154, Issue , 2015, Pages 78-86

  Ramsey, Joshua D ^a   Flynn, Nicholas H ^a  

^a Oklahoma State University   (United States)

Author keywords

Cell penetrating peptide; Drug delivery; Internalization; Penetratin; Protein transduction domain; Tat

Indexed keywords

CELL PENETRATING PEPTIDE; CONTRAST MEDIUM; ENZYME; NUCLEIC ACID; PEPTIDE DERIVATIVE; PROTEIN DERIVATIVE; PROTEIN;

CELL MEMBRANE; CELLS BY BODY ANATOMY; DRUG DELIVERY SYSTEM; ENDOCYTOSIS; GENE DELIVERY SYSTEM; HUMAN; INTERNALIZATION; INTRACELLULAR SPACE; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULE; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVIEW; METABOLISM; PHYSIOLOGY; PROCEDURES; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELL-PENETRATING PEPTIDES; DRUG DELIVERY SYSTEMS; ENZYMES; HUMANS; NUCLEIC ACIDS; PROTEINS;

EID: 84941416356     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2015.07.003     Document Type: Review

References (136)

1. N.A. Alhakamy, A.S. Nigatu, C.J. Berkland, and J.D. Ramsey Noncovalently associated cell-penetrating peptides for gene delivery applications Ther Deliv 4 6 2013 741 757
2. I.D. Alves, M. Carré, M.-P. Montero, S. Castano, S. Lecomte, R. Marquant, and et al. A proapoptotic peptide conjugated to penetratin selectively inhibits tumor cell growth Biochim. Biophys. Acta Biomembr. 1838 8 2014 2087 2098
3. D. Araki, K. Takayama, M. Inoue, T. Watanabe, H. Kumon, S. Futaki, and et al. Cell-penetrating D-isomer peptides of p53 C-terminus: long-term inhibitory effect on the growth of bladder cancer Urology 75 4 2010 813 819
4. H. Bai, Y. You, H. Yan, J. Meng, X. Xue, Z. Hou, and et al. Antisense inhibition of gene expression and growth in gram-negative bacteria by cell-penetrating peptide conjugates of peptide nucleic acids targeted to< i> rpoD gene Biomaterials 33 2 2012 659 667
5. J.G. Beitz, P. Davol, J.W. Clark, J. Kato, M. Medina, A.R. Frackelton, and et al. Antitumor activity of basic fibroblast growth factor-saporin mitotoxin in vitro and in vivo Cancer Res 52 1 1992 227 230
6. R. Brock The uptake of arginine-rich cell-penetrating peptides: putting the puzzle together Bioconjug Chem 25 5 2014 863 868
7. D. Cai, W. Gao, B. He, W. Dai, H. Zhang, X. Wang, and et al. Hydrophobic penetrating peptide PFVYLI-modified stealth liposomes for doxorubicin delivery in breast cancer therapy Biomaterials 35 7 2014 2283 2294
8. H.-Z. Chen, C.P. Wu, Y.-C. Chao, and C.Y.-Y. Liu Membrane penetrating peptides greatly enhance baculovirus transduction efficiency into mammalian cells Biochem Biophys Res Commun 405 2 2011 297 302
9. M. Chen, M. Zakrewsky, V. Gupta, A.C. Anselmo, D.H. Slee, J.A. Muraski, and et al. Topical delivery of siRNA into skin using SPACE-peptide carriers J Control Release 179 2014 33 41
10. C.J. Cheng, and W.M. Saltzman Enhanced siRNA delivery into cells by exploiting the synergy between targeting ligands and cell-penetrating peptides Biomaterials 32 26 2011 6194 6203
11. D.M. Copolovici, K. Langel, E. Eriste, and U. Langel Cell-penetrating peptides: design, synthesis, and applications ACS Nano 8 3 2014 1972 1994
12. C. De Coupade, A. Fittipaldi, V. Chagnas, M. Michel, S. Carlier, E. Tasciotti, and et al. Novel human-derived cell-penetrating peptides for specific subcellular delivery of therapeutic biomolecules Biochem J 390 2005 407 418
13. J.B. Delehanty, I.L. Medintz, T. Pons, F.M. Brunel, P.E. Dawson, and H. Mattoussi Self-assembled quantum dot-peptide bioconjugates for selective intracellular delivery Bioconjug Chem 17 4 2006 920 927
14. D. Derossi, S. Calvet, A. Trembleau, A. Brunissen, G. Chassaing, and A. Prochiantz Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent J Biol Chem 271 30 1996 18188 18193
15. D. Derossi, A.H. Joliot, G. Chassaing, and A. Prochiantz The third helix of the Antennapedia homeodomain translocates through biological membranes J Biol Chem 269 14 1994 10444 10450
16. L. Di, P. Artursson, A. Avdeef, G.F. Ecker, B. Faller, H. Fischer, and et al. Evidence-based approach to assess passive diffusion and carrier-mediated drug transport Drug Discov Today 17 15-16 2012 905 912
17. M. Dilber, A. Phelan, A. Aints, A. Mohamed, G. Elliott, C. Smith, and et al. Intercellular delivery of thymidine kinase prodrug activating enzyme by the herpes simplex virus protein, VP22 Gene Ther 6 1 1999 12 21
18. R.I. Dmitriev, A.V. Zhdanov, G.V. Ponomarev, D.V. Yashunski, and D.B. Papkovsky Intracellular oxygen-sensitive phosphorescent probes based on cell-penetrating peptides Anal Biochem 398 1 2010 24 33
19. P.D. Dobson, and D.B. Kell Carrier-mediated cellular uptake of pharmaceutical drugs: an exception or the rule? Nat Rev Drug Discov 7 3 2008 205 220
20. H.M. Ellerby, W. Arap, L.M. Ellerby, R. Kain, R. Andrusiak, G.D. Rio, and et al. Anti-cancer activity of targeted pro-apoptotic peptides Nat Med 5 9 1999 1032 1038
21. G. Elliott, and P. O'Hare Intercellular trafficking and protein delivery by a herpesvirus structural protein Cell 88 2 1997 223 233
22. Y. Eto, Y. Yoshioka, R. Asavatanabodee, S. Kida, M. Maeda, Y. Mukai, and et al. Transduction of adenovirus vectors modified with cell-penetrating peptides Peptides 30 8 2009 1548 1552
23. B. Fang, L. Jiang, M. Zhang, and F.Z. Ren A novel cell-penetrating peptide TAT-A1 delivers siRNA into tumor cells selectively Biochimie 95 2 2013 251 257
24. M. Favaro, M. de Toledo, R. Alves, C. Santos, L. Beloti, R. Janissen, and et al. Development of a non-viral gene delivery vector based on the dynein light chain Rp3 and the TAT peptide J Biotechnol 173 2014 10 18
25. L. Fei, L.P. Yap, P.S. Conti, W.C. Shen, and J.L. Zaro Tumor targeting of a cell penetrating peptide by fusing with a pH-sensitive histidine-glutamate co-oligopeptide Biomaterials 35 13 2014 4082 4087
26. J.F. Fennell, W.H. Shipman, and L.J. Cole Antibacterial action of melittin, a polypeptide from bee venom Exp Biol Med 127 3 1968 707 710
27. A. Ferrari, V. Pellegrini, C. Arcangeli, A. Fittipaldi, M. Giacca, and F. Beltram Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time Mol Ther 8 2 2003 284 294
28. L. Fisher, U. Soomets, V.C. Toro, L. Chilton, Y. Jiang, Ü. Langel, and et al. Cellular delivery of a double-stranded oligonucleotide NFκB decoy by hybridization to complementary PNA linked to a cell-penetrating peptide Gene Ther 11 16 2004 1264 1272
29. A. Fittipaldi, A. Ferrari, M. Zoppe, C. Arcangeli, V. Pellegrini, F. Beltram, and et al. Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins J Biol Chem 278 36 2003 34141 34149
30. A.D. Frankel, and C.O. Pabo Cellular uptake of the tat protein from human immunodeficiency virus Cell 55 6 1988 1189 1193
31. M.M. Fretz, N.A. Penning, S. Al-Taei, S. Futaki, T. Takeuchi, I. Nakase, and et al. Temperature-, concentration- and cholesterol-dependent translocation of l- and d-octa-arginine across the plasma and nuclear membrane of CD34+ leukaemia cells Biochem J 403 2 2007 335 342
32. M. Green, and P.M. Loewenstein Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein Cell 55 6 1988 1179 1188
33. E. Harreither, H.A. Rydberg, H.L. Åmand, V. Jadhav, L. Fliedl, C. Benda, and et al. Characterization of a novel cell penetrating peptide derived from human Oct4 Cell Regeneration 3 1 2014 2
34. Y. Hayashi, J. Yamauchi, I.A. Khalil, K. Kajimoto, H. Akita, and H. Harashima Cell penetrating peptide-mediated systemic siRNA delivery to the liver Int J Pharm 419 1-2 2011 308 313
35. J. He, W.B. Kauffman, T. Fuselier, S.K. Naveen, T.G. Voss, K. Hristova, and et al. Direct cytosolic delivery of polar cargo to cells by spontaneous membrane-translocating peptides J Biol Chem 288 41 2013 29974 29986
36. H.D. Herce, and A.E. Garcia 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 52 2007 20805 20810
37. H. Hirose, T. Takeuchi, H. Osakada, S. Pujals, S. Katayama, I. Nakase, and et al. Transient focal membrane deformation induced by arginine-rich peptides leads to their direct penetration into cells Mol Ther 20 5 2012 984 993
38. T. Holm, S.E. Andaloussi, and U. Langel Comparison of CPP uptake methods Methods Mol Biol 683 2011 207 217
39. Y. Hu, B. Xu, Q. Ji, D. Shou, X. Sun, J. Xu, and et al. A mannosylated cell-penetrating peptide-graft-polyethylenimine as a gene delivery vector Biomaterials 35 13 2014 4236 4246
40. A. Jain, B.K. Yadav, and A. Chugh Marine antimicrobial peptide tachyplesin as an efficient nanocarrier for macromolecule delivery in plant and mammalian cells FEBS J 282 2015 732 745
41. M.M. Javadpour, M.M. Juban, W.-C.J. Lo, S.M. Bishop, J.B. Alberty, S.M. Cowell, and et al. De novo antimicrobial peptides with low mammalian cell toxicity J Med Chem 39 16 1996 3107 3113
42. Q.-Y. Jiang, L.-H. Lai, J. Shen, Q.-Q. Wang, F.-J. Xu, and G.-P. Tang Gene delivery to tumor cells by cationic polymeric nanovectors coupled to folic acid and the cell-penetrating peptide octaarginine Biomaterials 32 29 2011 7253 7262
43. T. Jiang, E.S. Olson, Q.T. Nguyen, M. Roy, P.A. Jennings, and R.Y. Tsien Tumor imaging by means of proteolytic activation of cell-penetrating peptides Proc Natl Acad Sci U S A 101 51 2004 17867 17872
44. L.H. Jin, J.H. Bahn, W.S. Eum, H.Y. Kwon, S.H. Jang, K.H. Han, and et al. Transduction of human catalase mediated by an HIV-1 TAT protein basic domain and arginine-rich peptides into mammalian cells Free Radic Biol Med 31 11 2001 1509 1519
45. E. Jin, B. Zhang, X. Sun, Z. Zhou, X. Ma, Q. Sun, and et al. Acid-active cell-penetrating peptides for in vivo tumor-targeted drug delivery J Am Chem Soc 135 2 2013 933 940
46. A. Joliot, C. Pernelle, H. Deagostini-Bazin, and A. Prochiantz Antennapedia homeobox peptide regulates neural morphogenesis Proc Natl Acad Sci U S A 88 5 1991 1864 1868
47. H. Kamada, T. Okamoto, M. Kawamura, H. Shibata, Y. Abe, A. Ohkawa, and et al. Creation of novel cell-penetrating peptides for intracellular drug delivery using systematic phage display technology originated from Tat transduction domain Biol Pharm Bull 30 2 2007 218 223
48. T. Kanazawa, K. Morisaki, S. Suzuki, and Y. Takashima Prolongation of life in rats with malignant glioma by intranasal siRNA/drug codelivery to the brain with cell-penetrating peptide-modified micelles Mol Pharm 11 5 2014 1471 1478
49. I.M. Kaplan, J.S. Wadia, and S.F. Dowdy Cationic TAT peptide transduction domain enters cells by macropinocytosis J Control Release 102 1 2005 247 253
50. D.B. Kell, P.D. Dobson, and S.G. Oliver Pharmaceutical drug transport: the issues and the implications that it is essentially carrier-mediated only Drug Discov Today 16 15-16 2011 704 714
51. A.A. Keller, R. Breitling, P. Hemmerich, K. Kappe, M. Braun, B. Wittig, and et al. Transduction of proteins into Leishmania tarentolae by formation of non-covalent complexes with cell-penetrating peptides J Cell Biochem 115 2 2014 243 252
52. I.A. Khalil, K. Kogure, H. Akita, and H. Harashima Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery Pharmacol Rev 58 1 2006 32 45
53. J. Kim, Y.-L. Choi, A. Vallentin, B.S. Hunrichs, M.K. Hellerstein, D.M. Peehl, and et al. Centrosomal PKCβII and pericentrin are critical for human prostate cancer growth and angiogenesis Cancer Res 68 16 2008 6831 6839
54. W. Kim, D.W. Kim, D.Y. Yoo, J.Y. Chung, I.K. Hwang, M.-H. Won, and et al. Neuroprotective effects of PEP-1-Cu, Zn-SOD against ischemic neuronal damage in the rabbit spinal cord Neurochem Res 37 2 2012 307 313
55. S. Kobayashi, K. Takeshima, C.B. Park, S.C. Kim, and K. Matsuzaki Interactions of the novel antimicrobial peptide buforin 2 with lipid bilayers: proline as a translocation promoting factor† Biochemistry 39 29 2000 8648 8654
56. E. Koren, and V.P. Torchilin Cell-penetrating peptides: breaking through to the other side Trends Mol Med 18 7 2012 385 393
57. M. Kosuge, T. Takeuchi, I. Nakase, A.T. Jones, and S. Futaki Cellular internalization and distribution of arginine-rich peptides as a function of extracellular peptide concentration, serum, and plasma membrane associated proteoglycans Bioconjug Chem 19 3 2008 656 664
58. Y.M. Kwon, H.S. Chung, C. Moon, J. Yockman, Y.J. Park, S.D. Gitlin, and et al. l-Asparaginase encapsulated intact erythrocytes for treatment of acute lymphoblastic leukemia (ALL) J Control Release 139 3 2009 182 189
59. H.Y. Kwon, W.S. Eum, H.W. Jang, J.H. Kang, J. Ryu, B. Ryong Lee, and et al. Transduction of Cu, Zn-superoxide dismutase mediated by an HIV-1 Tat protein basic domain into mammalian cells FEBS Lett 485 2 2000 163 167
60. I. Le Roux, A.H. Joliot, E. Bloch-Gallego, A. Prochiantz, and M. Volovitch Neurotrophic activity of the Antennapedia homeodomain depends on its specific DNA-binding properties Proc Natl Acad Sci 90 19 1993 9120 9124
61. B. Leader, Q.J. Baca, and D.E. Golan Protein therapeutics: a summary and pharmacological classification Nat Rev Drug Discov 7 1 2008 21 39
62. M. Lelle, S.U. Frick, K. Steinbrink, and K. Peneva Novel cleavable cell-penetrating peptide-drug conjugates: synthesis and characterization J Pept Sci 20 5 2014 323 333
63. Y.-Z. Lin, S. Yao, R.A. Veach, T.R. Torgerson, and J. Hawiger Inhibition of nuclear translocation of transcription factor NF-κB by a synthetic peptide containing a cell membrane-permeable motif and nuclear localization sequence J Biol Chem 270 24 1995 14255 14258
64. S. Lindberg, A. Muñoz-Alarcón, H. Helmfors, D. Mosqueira, D. Gyllborg, O. Tudoran, and et al. PepFect15, a novel endosomolytic cell-penetrating peptide for oligonucleotide delivery via scavenger receptors Int J Pharm 441 1 2013 242 247
65. J. Liu, T. Gaj, J.T. Patterson, S.J. Sirk, and C.F. Barbas III Cell-penetrating peptide-mediated delivery of TALEN proteins via bioconjugation for genome engineering Plos One 9 1 2014 (e85755)
66. B.R. Liu, Y.-w. Huang, J.G. Winiarz, H.-J. Chiang, and H.-J. Lee Intracellular delivery of quantum dots mediated by a histidine- and arginine-rich HR9 cell-penetrating peptide through the direct membrane translocation mechanism Biomaterials 32 13 2011 3520 3537
67. Y. Liu, Y.J. Kim, M. Ji, J. Fang, N. Siriwon, L.I. Zhang, and et al. Enhancing gene delivery of adeno-associated viruses by cell-permeable peptides Mol Ther Methods Clin Dev 2014 1
68. K. Liu, S. Timmons, Y.-Z. Lin, and J. Hawiger Identification of a functionally important sequence in the cytoplasmic tail of integrin beta 3 by using cell-permeable peptide analogs Proc Natl Acad Sci 93 21 1996 11819 11824
69. M. Lundberg, and M. Johansson Positively charged DNA-binding proteins cause apparent cell membrane translocation Biochem Biophys Res Commun 291 2 2002 367 371
70. J. Ma, J. Xu, L. Guan, T. Hu, Q. Liu, J. Xiao, and et al. Cell-penetrating peptides mediated protein cross-membrane delivery and its use in bacterial vector vaccine Fish Shellfish Immunol 39 2014 8 16
71. J.R. Maiolo, M. Ferrer, and E.A. Ottinger Effects of cargo molecules on the cellular uptake of arginine-rich cell-penetrating peptides Biochim Biophys Acta 1712 2 2005 161 172
72. R. Marchione, D. Dayde, J.L. Lenormand, and M. Cornet ZEBRA cell-penetrating peptide as an efficient delivery system in Candida albicans Biotechnol J 9 2014 1088 1094
73. J.R. Marks, J. Placone, K. Hristova, and W.C. Wimley Spontaneous membrane-translocating peptides by orthogonal high-throughput screening J Am Chem Soc 133 23 2011 8995 9004
74. M.H. Massaoka, A.L. Matsuo, C.R. Figueiredo, N. Girola, C.F. Faria, R.A. Azevedo, and et al. A novel cell-penetrating peptide derived from WT1 enhances p53 activity, induces cell senescence and displays antimelanoma activity in xeno- and syngeneic systems FEBS Open Bio 4 2014 153 161
75. I. Meerovich, N. Muthukrishnan, G.A. Johnson, A. Erazo-Oliveras, and J.P. Pellois Photodamage of lipid bilayers by irradiation of a fluorescently labeled cell-penetrating peptide Biochim Biophys Acta 1840 1 2014 507 515
76. H. Michiue, Y. Sakurai, N. Kondo, M. Kitamatsu, F. Bin, K. Nakajima, and et al. The acceleration of boron neutron capture therapy using multi-linked mercaptoundecahydrododecaborate (BSH) fused cell-penetrating peptide Biomaterials 35 10 2014 3396 3405
77. M.C. Morris, J. Depollier, J. Mery, F. Heitz, and G. Divita A peptide carrier for the delivery of biologically active proteins into mammalian cells Nat Biotechnol 19 12 2001 1173 1176
78. M.C. Morris, P. Vidal, L. Chaloin, F. Heitz, and G. Divita A new peptide vector for efficient delivery of oligonucleotides into mammalian cells Nucleic Acids Res 25 14 1997 2730 2736
79. I. Nakase, Y. Konishi, M. Ueda, H. Saji, and S. Futaki Accumulation of arginine-rich cell-penetrating peptides in tumors and the potential for anticancer drug delivery in vivo J Control Release 159 2 2012 181 188
80. F. Nakayama, S. Umeda, T. Yasuda, M. Fujita, M. Asada, V. Meineke, and et al. Cellular internalization of fibroblast growth factor-12 exerts radioprotective effects on intestinal radiation damage independently of FGFR signaling Int. J. Radiat. Oncol. Biol. Phys. 88 2 2014 377 384
81. F. Nakayama, T. Yasuda, S. Umeda, M. Asada, T. Imamura, V. Meineke, and et al. Fibroblast Growth Factor-12 (FGF12) translocation into intestinal epithelial cells is dependent on a novel cell-penetrating peptide domain: involvement of internalization in the in vivo role of exogenouS FGF12 J Biol Chem 286 29 2011 25823 25834
82. A. Nasrolahi Shirazi, R. Tiwari, B.S. Chhikara, D. Mandal, and K. Parang Design and biological evaluation of cell-penetrating peptide-doxorubicin conjugates as prodrugs Mol Pharm 10 2 2013 488 499
83. Q.T. Nguyen, E.S. Olson, T.A. Aguilera, T. Jiang, M. Scadeng, L.G. Ellies, and et al. Surgery with molecular fluorescence imaging using activatable cell-penetrating peptides decreases residual cancer and improves survival Proc Natl Acad Sci 107 9 2010 4317 4322
84. E.J.B. Nielsen, S. Yoshida, N. Kamei, R. Iwamae, E.-S. Khafagy, J. Olsen, and et al. In vivo proof of concept of oral insulin delivery based on a co-administration strategy with the cell-penetrating peptide penetratin J Control Release 189 2014 19 24
85. A.S. Nigatu, S. Vupputuri, N. Flynn, B.J. Neely, and J.D. Ramsey Evaluation of cell-penetrating peptide/adenovirus particles for transduction of CAR-negative cells J Pharm Sci 102 6 2013 1981 1993
86. J. Oehlke, E. Krause, B. Wiesner, M. Beyermann, and M. Bienert Nonendocytic, amphipathicity dependent cellular uptake of helical model peptides Protein Pept. Lett. 3 6 1996 393 398
87. J. Oehlke, A. Scheller, B. Wiesner, E. Krause, M. Beyermann, E. Klauschenz, and et al. Cellular uptake of an α-helical amphipathic model peptide with the potential to deliver polar compounds into the cell interior non-endocytically Biochim. Biophys. Acta Biomembr. 1414 1 1998 127 139
88. E.S. Olson, T.A. Aguilera, T. Jiang, L.G. Ellies, Q.T. Nguyen, E.H. Wong, and et al. In vivo characterization of activatable cell penetrating peptides for targeting protease activity in cancer Integr Biol 1 5-6 2009 382 393
89. E.S. Olson, T. Jiang, T.A. Aguilera, Q.T. Nguyen, L.G. Ellies, M. Scadeng, and et al. Activatable cell penetrating peptides linked to nanoparticles as dual probes for in vivo fluorescence and MR imaging of proteases Proc Natl Acad Sci 107 9 2010 4311 4316
90. C. Palm-Apergi, A. Lorents, K. Padari, M. Pooga, and M. Hallbrink The membrane repair response masks membrane disturbances caused by cell-penetrating peptide uptake FASEB J 23 1 2009 214 223
91. S. Park, J. Doh, S. Park, J. Lim, S. Kim, J. Youn, and et al. Branched oligomerization of cell-permeable peptides markedly enhances the transduction efficiency of adenovirus into mesenchymal stem cells Gene Ther 17 8 2010 1052 1061
92. J. Park, J. Ryu, K.A. Kim, H.J. Lee, J.H. Bahn, K. Han, and et al. Mutational analysis of a human immunodeficiency virus type 1 Tat protein transduction domain which is required for delivery of an exogenous protein into mammalian cells J Gen Virol 83 Pt 5 2002 1173 1181
93. M. Pooga, M. Hällbrink, M. Zorko, U. Langel, and lo, Cell penetration by transportan FASEB J 12 1 1998 67 77
94. M. Pooga, U. Soomets, M. Hallbrink, A. Valkna, K. Saar, K. Rezaei, and et al. Cell penetrating PNA constructs regulate galanin receptor levels and modify pain Nat Biotechnol 16 1998
95. Y. Pouny, D. Rapaport, A. Mor, P. Nicolas, and Y. Shai Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes Biochemistry 31 49 1992 12416 12423
96. P. Rajasekaran, J.C. Alexander, M.N. Seleem, N. Jain, N. Sriranganathan, A.R. Wattam, and et al. Peptide nucleic acids inhibit growth of Brucella suis in pure culture and in infected murine macrophages Int J Antimicrob Agents 41 4 2013 358 362
97. S. Ramakrishna, A.-B.K. Dad, J. Beloor, R. Gopalappa, S.-K. Lee, and H. Kim Gene disruption by cell-penetrating peptide-mediated delivery of Cas9 protein and guide RNA Genome Res 24 6 2014 1020 1027
98. M. Rhee, and P. Davis Mechanism of uptake of C105Y, a novel cell-penetrating peptide J Biol Chem 281 2 2006 1233 1240
99. J.P. Richard, K. Melikov, H. Brooks, P. Prevot, B. Lebleu, and L.V. Chernomordik Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors J Biol Chem 280 15 2005 15300 15306
100. J.P. Richard, K. Melikov, E. Vives, C. Ramos, B. Verbeure, M.J. Gait, and et al. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake J Biol Chem 278 1 2003 585 590
101. J.G. Rodriguez Plaza, R. Morales-Nava, C. Diener, G. Schreiber, Z.D. Gonzalez, M.T. Lara Ortiz, and et al. Cell penetrating peptides and cationic antibacterial peptides: two sides of the same coin J Biol Chem 289 2014 14448 14457
102. G.E. Roeder, J.L. Parish, P.L. Stern, and K. Gaston Herpes simplex virus VP22-human papillomavirus E2 fusion proteins produced in mammalian or bacterial cells enter mammalian cells and induce apoptotic cell death Biotechnol Appl Biochem 40 2 2004 157 165
103. J.B. Rothbard, T.C. Jessop, and P.A. Wender Adaptive translocation: the role of hydrogen bonding and membrane potential in the uptake of guanidinium-rich transporters into cells Adv Drug Deliv Rev 57 4 2005 495 504
104. K. Sadler, K.D. Eom, J.-L. Yang, Y. Dimitrova, and J.P. Tam Translocating proline-rich peptides from the antimicrobial peptide bactenecin 7† Biochemistry 41 48 2002 14150 14157
105. E.N. Savariar, C.N. Felsen, N. Nashi, T. Jiang, L.G. Ellies, P. Steinbach, and et al. Real-time in vivo molecular detection of primary tumors and metastases with ratiometric activatable cell-penetrating peptides Cancer Res 73 2 2013 855 864
106. S.R. Schwarze, A. Ho, A. Vocero-Akbani, and S.F. Dowdy In vivo protein transduction: delivery of a biologically active protein into the mouse Science 285 5433 1999 1569 1572
107. F. Sgolastra, B.M. Deronde, J.M. Sarapas, A. Som, and G.N. Tew Designing mimics of membrane active proteins Acc Chem Res 46 12 2013 2977 2987
108. G. Sharma, A. Modgil, B. Layek, K. Arora, C. Sun, B. Law, and et al. Cell penetrating peptide tethered bi-ligand liposomes for delivery to brain in vivo: biodistribution and transfection J Control Release 167 1 2013 1 10
109. I. Shin, J. Edl, S. Biswas, P.C. Lin, R. Mernaugh, and C.L. Arteaga Proapoptotic activity of cell-permeable anti-Akt single-chain antibodies Cancer Res 65 7 2005 2815 2824
110. M.J. Shin, D.W. Kim, Y.P. Lee, E.H. Ahn, H.S. Jo, D.-S. Kim, and et al. Tat-glyoxalase protein inhibits against ischemic neuronal cell damage and ameliorates ischemic injury Free Radic Biol Med 67 2014 195 210
111. E.G. Stebbins, and D. Mochly-Rosen Binding specificity for RACK1 resides in the V5 region of βII protein kinase C J Biol Chem 276 32 2001 29644 29650
112. L.A. Sternson Obstacles to polypeptide delivery Ann N Y Acad Sci 507 1987 19 21
113. K. Sugano, M. Kansy, P. Artursson, A. Avdeef, S. Bendels, L. Di, and et al. Coexistence of passive and carrier-mediated processes in drug transport Nat Rev Drug Discov 9 8 2010 597 614
114. J.S. Suh, J.Y. Lee, G. Lee, C.P. Chung, and Y.J. Park Simultaneous imaging and restoration of cell function using cell permeable peptide probe Biomaterials 35 24 2014 6287 6298
115. J.S. Suk, J. Suh, K. Choy, S.K. Lai, J. Fu, and J. Hanes Gene delivery to differentiated neurotypic cells with RGD and HIV Tat peptide functionalized polymeric nanoparticles Biomaterials 27 29 2006 5143 5150
116. G. Tunnemann, R.M. Martin, S. Haupt, C. Patsch, F. Edenhofer, and M.C. Cardoso Cargo-dependent mode of uptake and bioavailability of TAT-containing proteins and peptides in living cells FASEB J 20 11 2006 1775 1784
117. G. Tünnemann, G. Ter-Avetisyan, R.M. Martin, M. Stöckl, A. Herrmann, and M.C. Cardoso Live-cell analysis of cell penetration ability and toxicity of oligo-arginines J Pept Sci 14 4 2008 469 476
118. J. Turkson, D. Ryan, J.S. Kim, Y. Zhang, Z. Chen, E. Haura, and et al. Phosphotyrosyl peptides block Stat3-mediated DNA binding activity, gene regulation, and cell transformation J Biol Chem 276 48 2001 45443 45455
119. A.H. van Asbeck, A. Beyerle, H. McNeill, P.H.M. Bovee-Geurts, S. Lindberg, W.P.R. Verdurmen, and et al. Molecular parameters of siRNA-cell penetrating peptide nanocomplexes for efficient cellular delivery ACS Nano 7 5 2013 3797 3807
120. E. Vives, P. Brodin, and B. Lebleu A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus J Biol Chem 272 25 1997 16010 16017
121. E. Vivès, C. Granier, P. Prevot, and B. Lebleu Structure-activity relationship study of the plasma membrane translocating potential of a short peptide from HIV-1 Tat protein Lett Pept Sci 4 4-6 1997 429 436
122. M. Wang, K. Alberti, S. Sun, C.L. Arellano, and Q. Xu Combinatorially designed lipid-like nanoparticles for intracellular delivery of cytotoxic protein for cancer therapy Angew Chem 126 11 2014 2937 2942
123. F. Wang, Y. Wang, X. Zhang, W. Zhang, S. Guo, and F. Jin Recent progress of cell-penetrating peptides as new carriers for intracellular cargo delivery J Control Release 174 2014 126 136
124. C.L. Watkins, P. Brennan, C. Fegan, K. Takayama, I. Nakase, S. Futaki, and et al. Cellular uptake, distribution and cytotoxicity of the hydrophobic cell penetrating peptide sequence PFVYLI linked to the proapoptotic domain peptide PAD J Control Release 140 3 2009 237 244
125. Y. Wei, C. Li, L. Zhang, and X. Xu Design of novel cell penetrating peptides for the delivery of trehalose into mammalian cells Biochim Biophys Acta 1838 7 2014 1911 1920
126. R. Weinstain, E.N. Savariar, C.N. Felsen, and R.Y. Tsien In vivo targeting of hydrogen peroxide by activatable cell-penetrating peptides J Am Chem Soc 136 3 2013 874 877
127. P.A. Wender, D.J. Mitchell, K. Pattabiraman, E.T. Pelkey, L. Steinman, and J.B. Rothbard The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: peptoid molecular transporters Proc Natl Acad Sci 97 24 2000 13003 13008
128. M. Whitney, E.N. Savariar, B. Friedman, R.A. Levin, J.L. Crisp, H.L. Glasgow, and et al. Ratiometric activatable cell-penetrating peptides provide rapid in vivo readout of thrombin activation Angew Chem Int Ed Engl 52 1 2013 325 330
129. Y. Woods, and D. Lane Exploiting the p53 pathway for cancer diagnosis and therapy Hematol J 4 1 2013 233 247
130. Y. Wu, S.M. Mikulski, W. Ardelt, S.M. Rybak, and R.J. Youle A cytotoxic ribonuclease. Study of the mechanism of onconase cytotoxicity J Biol Chem 268 14 1993 10686 10693
131. H. Xia, G. Gu, Q. Hu, Z. Liu, M. Jiang, T. Kang, and et al. Activatable cell penetrating peptide-conjugated nanoparticles with enhanced permeability for site-specific targeting delivery of anticancer drug Bioconjug Chem 24 3 2013 419 430
132. S. Yamano, J. Dai, S. Hanatani, K. Haku, T. Yamanaka, M. Ishioka, and et al. Efficient in vivo gene delivery using modified Tat peptide with cationic lipids Biotechnol Lett 2014 1 6
133. S. Yamano, J. Dai, S. Hanatani, K. Haku, T. Yamanaka, M. Ishioka, and et al. Long-term efficient gene delivery using polyethylenimine with modified Tat peptide Biomaterials 35 5 2014 1705 1715
134. D. Yu, C. Jin, J. Leja, N. Majdalani, B. Nilsson, F. Eriksson, and et al. Adenovirus with hexon Tat-protein transduction domain modification exhibits increased therapeutic effect in experimental neuroblastoma and neuroendocrine tumors J Virol 85 24 2011 13114 13123
135. L. Zender, F. Kühnel, R. Köck, M. Manns, and S. Kubicka VP22-mediated intercellular transport of p53 in hepatoma cells in vitro and in vivo Cancer Gene Ther 9 6 2002 489 496
136. C. Zhang, N. Tang, X. Liu, W. Liang, W. Xu, and V.P. Torchilin siRNA-containing liposomes modified with polyarginine effectively silence the targeted gene J Control Release 112 2 2006 229 239