Peptides for cancer therapy: A drug-development opportunity and a drug-delivery challenge

Therapeutic Delivery

Volumn 3, Issue 5, 2012, Pages 609-621

  Bidwell, Gene L ^a  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBINTERFERON ALPHA2B; ANTINEOPLASTIC AGENT; CELL PENETRATING PEPTIDE; DOXORUBICIN; GOSERELIN; INSULIN DETEMIR; INTERNALIZING ARGINYLGLYCYLASPARTIC ACID; LEUPRON DEPOT; LEUPRORELIN; LIPOSOME; LIRAGLUTIDE; MELITTIN; N (2 HYDROXYPROPYL)METHACRYLAMIDE; PACLITAXEL; PNC 28; PROTEIN C MYC H1; PROTEIN P16; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; THERAPEUTIC PEPTIDE; TRASTUZUMAB; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; BREAST CANCER; CANCER SURVIVAL; CANCER THERAPY; CELL MEMBRANE PERMEABILITY; CELL SURFACE; CONGESTIVE HEART FAILURE; DIABETES MELLITUS; DRUG APPROVAL; DRUG DEGRADATION; DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG EFFICACY; DRUG HALF LIFE; DRUG PENETRATION; DRUG RESEARCH; DRUG TARGETING; DRUG TUMOR LEVEL; GLIOBLASTOMA; GLIOMA; HEPATITIS; HUMAN; LIPOSOMAL DELIVERY; MACROMOLECULE; MELANOMA; NANOTECHNOLOGY; NONHUMAN; PANCREAS CANCER; PANCREAS TUMOR; PERSONALIZED MEDICINE; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE TUMOR; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; RETICULOENDOTHELIAL SYSTEM; REVIEW; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; SYSTEMIC CIRCULATION; TREATMENT DURATION; TREATMENT RESPONSE;

EID: 84861305475     PISSN: 20415990     EISSN: 20416008     Source Type: Journal    
DOI: 10.4155/tde.12.37     Document Type: Review

References (113)

1. Bidwell GL 3rd, Raucher D. Therapeutic peptides for cancer therapy. Part I - peptide inhibitors of signal transduction cascades. Expert Opin. Drug Deliv. 6(10), 1033-1047 (2009).
2. Raucher D, Moktan S, Massodi I, Bidwell GL 3rd. Therapeutic peptides for cancer therapy. Part II - cell cycle inhibitory peptides and apoptosis-inducing peptides. Expert Opin. Drug Deliv. 6(10), 1049-1064 (2009).
3. Draeger LJ, Mullen GP. Interaction of the bHLH-zip domain of c-Myc with H1-type peptides. Characterization of helicity in the H1 peptides by NMR. J. Biol. Chem. 269(3), 1785-1793 (1994).
4. Chen IT, Akamatsu M, Smith ML et al. Characterization of p21Cip1/Waf1 peptide domains required for cyclin E/Cdk2 and PCNA interaction. Oncogene 12(3), 595-607 (1996).
5. Ladner RC, Sato AK, Gorzelany J, De Souza M. Phage display-derived peptides as therapeutic alternatives to antibodies. Drug Discov. Today 9(12), 525-529 (2004).
6. Li Y, Mao Y, Rosal RV et al. Selective induction of apoptosis through the FADD/ caspase-8 pathway by a p53 C-terminal peptide in human pre-malignant and malignant cells. Int. J. Cancer 115(1), 55-64 (2005).
7. Carvalho G, Fabre C, Braun T et al. Inhibition of NEMO, the regulatory subunit of the IKK complex, induces apoptosis in high-risk myelodysplastic syndrome and acute myeloid leukemia. Oncogene 26(16), 2299-2307 (2007).
8. Fahraeus R, Lain S, Ball KL, Lane DP. Characterization of the cyclin-dependent kinase inhibitory domain of the INK4 family as a model for a synthetic tumour suppressor molecule. Oncogene 16(5), 587-596 (1998).
9. Adams PD, Sellers WR, Sharma SK, Wu AD, Nalin CM, Kaelin WG Jr. Identification of a cyclin-cdk2 recognition motif present in substrates and p21-like cyclin-dependent kinase inhibitors. Mol. Cell. Biol. 16(12), 6623-6633 (1996).
10. Widakowich C, De Castro G Jr, De Azambuja E, Dinh P, Awada A. Review: side effects of approved molecular targeted therapies in solid cancers. Oncologist 12(12), 1443-1455 (2007).
11. Wee S, Jagani Z, Xiang KX et al. PI3K pathway activation mediates resistance to MEK inhibitors in KRAS mutant cancers. Cancer Res. 69(10), 4286-4293 (2009).
12. Smalley KS, Haass NK, Brafford PA, Lioni M, Flaherty KT, Herlyn M. Multiple signaling pathways must be targeted to overcome drug resistance in cell lines derived from melanoma metastases. Mol. Cancer Ther. 5(5), 1136-1144 (2006).
13. Talmadge JE. Pharmacodynamic aspects of peptide administration biological response modifiers. Adv. Drug Deliv. Rev. 33(3), 241-252 (1998).
14. Lipka E, Crison J, Amidon GL. Transmembrane transport of peptide type compounds: prospects for oral delivery. J. Control. Release 39(2-3), 121-129 (1996).
15. Gregoriadis G, Jain S, Papaioannou I, Laing P. Improving the therapeutic efficacy of peptides and proteins: a role for polysialic acids. Int. J. Pharm. 300(1-2), 125-130 (2005).
16. Adler V, Pincus MR, Brandt-Rauf PW, Ronai Z. Complexes of p21RAS with JUN N-terminal kinase and JUN proteins. Proc. Natl Acad. Sci. USA 92(23), 10585-10589 (1995).
17. Chie L, Chen JM, Friedman FK et al. Identification of the site of inhibition of oncogenic ras-p21-induced signal transduction by a peptide from a ras effector domain. J. Protein Chem. 18(8), 881-884 (1999).
18. Chie L, Chen JM, Friedman FK et al. Inhibition of oncogenic and activated wild-type ras-p21 protein-induced oocyte maturation by peptides from the guanine-nucleotide exchange protein, SOS, identified from molecular dynamics calculations. Selective inhibition of oncogenic ras-p21. J. Protein Chem. 18(8), 875-879 (1999).
19. Chung D, Amar S, Glozman A et al. Inhibition of oncogenic and activated wild-type ras-p21 protein-induced oocyte maturation by peptides from the ras-binding domain of the raf-p74 protein, identified from molecular dynamics calculations. J. Protein Chem. 16(6), 631-635 (1997).
20. Clark GJ, Drugan JK, Terrell RS et al. Peptides containing a consensus Ras binding sequence from Raf-1 and the GTPase activating protein NF1 inhibit Ras function. Proc. Natl Acad. Sci. USA 93(4), 1577-1581 (1996).
21. Kelemen BR, Hsiao K, Goueli SA. Selective in vivo inhibition of mitogen-activated protein kinase activation using cell-permeable peptides. J. Biol. Chem. 277(10), 8741-8748 (2002).
22. Agou F, Courtois G, Chiaravalli J et al. Inhibition of NF-kappa B activation by peptides targeting NF-kappa B essential modulator (nemo) oligomerization. J. Biol. Chem. 279(52), 54248-54257 (2004).
23. Agou F, Traincard F, Vinolo E et al. The trimerization domain of NEMO is composed of the interacting C-terminal CC2 and LZ coiled-coil subdomains. J. Biol. Chem. 279(27), 27861-27869 (2004).
24. Lin YZ, Yao SY, Veach RA, Torgerson TR, Hawiger J. Inhibition of nuclear translocation of transcription factor NF-kappa B by a synthetic peptide containing a cell membrane-permeable motif and nuclear localization sequence. J. Biol. Chem. 270(24), 14255-14258 (1995).
25. May MJ, Dacquisto F, Madge LA, Glockner J, Pober JS, Ghosh S. Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkB kinase complex. Science 289(5484), 1550-1554 (2000).
26. Takada Y, Singh S, Aggarwal BB. Identification of a p65 peptide that selectively inhibits NF-kappa B activation induced by various inflammatory stimuli and its role in down-regulation of NF-kappaB-mediated gene expression and up-regulation of apoptosis. J. Biol. Chem. 279(15), 15096-15104 (2004).
27. Yaron A, Gonen H, Alkalay I et al. Inhibition of NF-kappa-B cellular function via specific targeting of the I-kappa-B-ubiquitin ligase. EMBO J. 16(21), 6486-6494 (1997).
28. Bottger A, Bottger V, Sparks A, Liu WL, Howard SF, Lane DP. Design of a synthetic Mdm2-binding mini protein that activates the p53 response in vivo. Curr. Biol. 7(11), 860-869 (1997).
29. Friedler A, Hansson LO, Veprintsev DB et al. A peptide that binds and stabilizes p53 core domain: chaperone strategy for rescue of oncogenic mutants. Proc. Natl Acad. Sci. USA 99(2), 937-942 (2002).
30. Hupp TR, Sparks A, Lane DP. Small peptides activate the latent sequence-specific DNA binding function of p53. Cell 83(2), 237-245 (1995).
31. Kanovsky M, Raffo A, Drew L et al. Peptides from the amino terminal mdm-2-binding domain of p53, designed from conformational analysis, are selectively cytotoxic to transformed cells. Proc. Natl Acad. Sci. USA 98(22), 12438-12443 (2001).
32. Selivanova G, Iotsova V, Okan I et al. Restoration of the growth suppression function of mutant p53 by a synthetic peptide derived from the p53 C-terminal domain. Nat. Med. 3(6), 632-638 (1997).
33. Selivanova G, Ryabchenko L, Jansson E, Iotsova V, Wiman KG. Reactivation of mutant p53 through interaction of a C-terminal peptide with the core domain. Mol. Cell. Biol. 19(5), 3395-3402 (1999).
34. Bidwell GL 3rd, Raucher D. Application of thermally responsive polypeptides directed against c-Myc transcriptional function for cancer therapy. Mol. Cancer Ther. 4(7), 1076-1085 (2005).
35. Bonfanti M, Taverna S, Salmona M, DIncalci M, Broggini M. p21WAF1-derived peptides linked to an internalization peptide inhibit human cancer cell growth. Cancer Res. 57(8), 1442-1446 (1997).
36. Massodi I, Moktan S, Rawat A, Bidwell GL 3rd, Raucher D. Inhibition of ovarian cancer cell proliferation by a cell cycle inhibitory peptide fused to a thermally responsive polypeptide carrier. Int. J. Cancer 126(2), 533-544 (2010).
37. Mutoh M, Lung FD, Long YQ, Roller PP, Sikorski RS, OConnor PM. A p21(Waf1/ Cip1) carboxyl-terminal peptide exhibited cyclin-dependent kinase-inhibitory activity and cytotoxicity when introduced into human cells. Cancer Res. 59(14), 3480-3488 (1999).
38. Warbrick E, Lane DP, Glover DM, Cox LS. A small peptide inhibitor of DNA replication defines the site of interaction between the cyclin-dependent kinase inhibitor p21WAF1 and proliferating cell nuclear antigen. Curr. Biol. 5(3), 275-282 (1995).
39. Fahraeus R, Paramio JM, Ball KL, Lain S, Lane DP. Inhibition of pRb phosphorylation and cell-cycle progression by a 20-residue peptide derived from p16CDKN2/INK4A. Curr. Biol. 6(1), 84-91 (1996).
40. Andrews MJ, Mcinnes C, Kontopidis G et al. Design, synthesis, biological activity and structural analysis of cyclic peptide inhibitors targeting the substrate recruitment site of cyclin-dependent kinase complexes. Org. Biomol. Chem. 2(19), 2735-2741 (2004).
41. Gondeau C, Gerbal-Chaloin S, Bello P, Aldrian-Herrada G, Morris MC, Divita G. Design of a novel class of peptide inhibitors of cyclin-dependent kinase/cyclin activation. J. Biol. Chem. 280(14), 13793-13800 (2005).
42. Adams PD, Li X, Sellers WR et al. Retinoblastoma protein contains a C-terminal motif that targets it for phosphorylation by cyclin-cdk complexes. Mol. Cell. Biol. 19(2), 1068-1080 (1999).
43. Kashiwagi H, Mcdunn JE, Goedegebuure PS et al. TAT-Bim induces extensive apoptosis in cancer cells. Ann. Surg. Oncol. 14(5), 1763-1771 (2007).
44. Polster BM, Kinnally KW, Fiskum G. BH3 death domain peptide induces cell type-selective mitochondrial outer membrane permeability. J. Biol. Chem. 276(41), 37887-37894 (2001).
45. Sattler M, Liang H, Nettesheim D et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275(5302), 983-986 (1997).
46. Schimmer AD, Hedley DW, Chow S et al. The BH3 domain of BAD fused to the antennapedia peptide induces apoptosis via its alpha helical structure and independent of Bcl-2. Cell Death Differ. 8(7), 725-733 (2001).
47. Chai J, Du C, Wu JW, Kyin S, Wang X, Shi Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature 406(6798), 855-862 (2000).
48. Mai JC, Mi Z, Kim SH, Ng B, Robbins PD. A proapoptotic peptide for the treatment of solid tumors. Cancer Res. 61(21), 7709-7712 (2001).
49. Leuschner C, Hansel W. Membrane disrupting lytic peptides for cancer treatments. Curr. Pharm. Des. 10(19), 2299-2310 (2004).
50. Michl J, Scharf B, Schmidt A et al. PNC-28, a p53-derived peptide that is cytotoxic to cancer cells, blocks pancreatic cancer cell growth in vivo. Int. J. Cancer 119(7), 1577-1585 (2006).
51. Bidwell GL, Perkins E, Raucher D. A thermally targeted c-Myc inhibitory polypeptide inhibits breast tumor growth. Cancer Lett. 319(2), 136-143 (2012).
52. Hosotani R, Miyamoto Y, Fujimoto K et al. Trojan p16 peptide suppresses pancreatic cancer growth and prolongs survival in mice. Clin. Cancer Res. 8(4), 1271-1276 (2002).
53. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 8(8), 808-815 (2002
54. Chengalvala MV, Pelletier JC, Kopf GS. GnRH agonists and antagonists in cancer therapy. Curr. Med. Chem. Anti Cancer Agents 3(6), 399-410 (2003).
55. Cheer SM, Plosker GL, Simpson D, Wagstaff AJ. Goserelin: a review of its use in the treatment of early breast cancer in premenopausal and perimenopausal women. Drugs 65(18), 2639-2655 (2005).
56. Perez-Marrero R, Tyler RC. A subcutaneous delivery system for the extended release of leuprolide acetate for the treatment of prostate cancer. Expert Opin. Pharmacother. 5(2), 447-457 (2004).
57. Pescarolo MP, Bagnasco L, Malacarne D et al. A retro-inverso peptide homologous to helix 1 of c-Myc is a potent and specific inhibitor of proliferation in different cellular systems. FASEB J. 15(1), 31-33 (2001).
58. Walensky LD, Kung AL, Escher I et al. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 305(5689), 1466-1470 (2004).
59. Patch JA, Barron AE. Mimicry of bioactive peptides via non-natural, sequence-specific peptidomimetic oligomers. Curr. Opin. Chem. Biol. 6(6), 872-877 (2002).
60. Torchilin V. Tumor delivery of macromolecular drugs based on the EPR effect. Adv. Drug Deliv. Rev. 63(3), 131-135 (2011).
61. Greish K. Enhanced permeability and retention of macromolecular drugs in solid tumors: a royal gate for targeted anticancer nanomedicines. J. Drug Target. 15(7-8), 457-464 (2007).
62. Maeda H. The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting. Adv. Enzyme. Regul. 41, 189-207 (2001).
63. Torchilin VP, Lukyanov AN. Peptide and protein drug delivery to and into tumors: challenges and solutions. Drug Discov. Today 8(6), 259-266 (2003).
64. Sato AK, Viswanathan M, Kent RB, Wood CR. Therapeutic peptides: technological advances driving peptides into development. Curr. Opin. Biotechnol. 17(6), 638-642 (2006).
65. Rosen O, Muller HJ, Gokbuget N et al. PEGylated asparaginase in combination with high-dose methotrexate for consolidation in adult acute lymphoblastic leukaemia in first remission: a pilot study. Br. J. Haematol. 123(5), 836-841 (2003).
66. Bottomley A, Coens C, Suciu S et al. Adjuvant therapy with pegylated interferon a-2b versus observation in resected stage III melanoma: a phase III randomized controlled trial of health-related quality of life and symptoms by the European Organisation for Research and Treatment of Cancer Melanoma Group. J. Clin. Oncol. 27(18), 2916-2923 (2009).
67. Eggermont AM, Suciu S, Santinami M et al. Adjuvant therapy with pegylated interferon a-2b versus observation alone in resected stage III melanoma: final results of EORTC 18991, a randomised phase III trial. Lancet 372(9633), 117-126 (2008).
68. Van Der Auwera P, Platzer E, Xu ZX et al. Pharmacodynamics and pharmacokinetics of single doses of subcutaneous PEGylated human G-CSF mutant (Ro 25-8315) in healthy volunteers: comparison with single and multiple daily doses of filgrastim. Am. J. Hematol. 66(4), 245-251 (2001).
69. Bowen S, Tare N, Inoue T et al. Relationship between molecular mass and duration of activity of polyethylene glycol conjugated granulocyte colony-stimulating factor mutein. Exp. Hematol. 27(3), 425-432 (1999).
70. Nie Y, Zhang X, Wang X, Chen J. Preparation and stability of N-terminal mono-PEGylated recombinant human endostatin. Bioconjug. Chem. 17(4), 995-999 (2006).
71. Zhu B, Xu HM, Zhao L, Huang X, Zhang F. Site-specific modification of anti-angiogenesis peptide HM-3 by polyethylene glycol molecular weight of 20 kDa. J. Biochem. 148(3), 341-347 (2010).
72. Zhang G, Han B, Lin X, Wu X, Yan H. Modification of antimicrobial peptide with low molar mass poly(ethylene glycol). J. Biochem. 144(6), 781-788 (2008).
73. Jørgensen L, Nielsen HM. Delivery Technologies for Biopharmaceuticals: Peptides, Proteins, Nucleic Acids and Vaccines. Wiley, Chichester, UK (2009).
74. Wang J, Chow D, Heiati H, Shen WC. Reversible lipidization for the oral delivery of salmon calcitonin. J. Control. Release 88(3), 369-380 (2003).
75. Wang J, Hogenkamp DJ, Tran M et al. Reversible lipidization for the oral delivery of leu-enkephalin. J. Drug Target. 14(3), 127-136 (2006).
76. Pardridge WM. Drug and gene delivery to the brain: the vascular route. Neuron 36(4), 555-558 (2002).
77. Duncan R. Polymer conjugates for tumour targeting and intracytoplasmic delivery. The EPR effect as a common gateway? Pharm. Sci. Technol. Today 2(11), 441-449 (1999).
78. Duvall CL, Convertine AJ, Benoit DS, Hoffman AS, Stayton PS. Intracellular delivery of a proapoptotic peptide via conjugation to a RAFT synthesized endosomolytic polymer. Mol. Pharm. 7(2), 468-476 (2010).
79. Bidwell GL 3rd, Raucher D. Cell penetrating elastin-like polypeptides for therapeutic peptide delivery. Adv. Drug Deliv. Rev. 62(15), 1486-1496 (2010).
80. Meyer DE, Chilkoti A. Purification of recombinant proteins by fusion with thermally responsive polypeptides. Nat. Biotechnol. 17, 1112-1115 (1999).
81. Meyer DE, Chilkoti A. Genetically encoded synthesis of protein-based polymers with precisely specified molecular weight and sequence by recursive directional ligation: examples from the elastin-like polypeptide system. Biomacromolecules 3(2), 357-367 (2002).
82. Urry DW, Luan C-H, Parker TM et al. Temperature of polypeptide inverse temperature transition depends on mean residue hydrophobicity. J. Am. Chem. Soc. 113, 4346-4348 (1991).
83. Dreher MR, Liu W, Michelich CR, Dewhirst MW, Chilkoti A. Thermal cycling enhances the accumulation of a temperature-sensitive biopolymer in solid tumors. Cancer Res. 67(9), 4418-4424 (2007).
84. Bidwell GL 3rd, Davis AN, Raucher D. Targeting a c-Myc inhibitory polypeptide to specific intracellular compartments using cell penetrating peptides. J. Control. Release 135(1), 2-10 (2009).
85. Massodi I, Bidwell GL 3rd, Raucher D. Evaluation of cell penetrating peptides fused to elastin-like polypeptide for drug delivery. J. Control. Release 108(2-3), 396-408 (2005).
86. Massodi I, Thomas E, Raucher D. Application of thermally responsive elastin-like polypeptide fused to a lactoferrin-derived peptide for treatment of pancreatic cancer. Molecules 14(6), 1999-2015 (2009).
87. Bidwell GL 3rd, Whittom AA, Thomas E, Lyons D, Hebert MD, Raucher D. A thermally targeted peptide inhibitor of symmetrical dimethylation inhibits cancer-cell proliferation. Peptides 31(5), 834-841 (2010).
88. Pan H, Soman NR, Schlesinger PH, Lanza GM, Wickline SA. Cytolytic peptide nanoparticles (NanoBees) for cancer therapy. Nanomed. Nanobiotechnol. 3(3), 318-327 (2011).
89. Tosteson MT, Holmes SJ, Razin M, Tosteson DC. Melittin lysis of red cells. J. Membr. Biol. 87(1), 35-44 (1985
90. Bell HS, Dufes C, Oprey J et al. A p53- derived apoptotic peptide derepresses p73 to cause tumor regression in vivo. J. Clin. Invest. 117(4), 1008-1018 (2007).
91. Noble CO, Kirpotin DB, Hayes ME et al. Development of ligand-targeted liposomes for cancer therapy. Expert Opin. Ther. Targets 8(4), 335-353 (2004).
92. Torchilin VP, Levchenko TS. TAT-liposomes: a novel intracellular drug carrier. Curr. Protein Pept. Sci. 4(2), 133-140 (2003).
93. Ducat E, Deprez J, Gillet A et al. Nuclear delivery of a therapeutic peptide by long circulating pH-sensitive liposomes: benefits over classical vesicles. Int. J. Pharm. 420(2), 319-332 (2011).
94. Li C, Shen J, Wei X, Xie C, Lu W. Targeted delivery of a novel palmitylated d-peptide for antiglioblastoma molecular therapy. J. Drug Target. 20(3), 264-271 (2012).
95. Kim SK, Huang L. Nanoparticle delivery of a peptide targeting EGFR signaling. J. Control. Release 157(2), 279-286 (2012).
96. Pasqualini R, Koivunen E, Ruoslahti E. Alpha v integrins as receptors for tumor targeting by circulating ligands. Nat. Biotechnol. 15(6), 542-546 (1997).
97. Ogris M, Walker G, Blessing T, Kircheis R, Wolschek M, Wagner E. Tumor-targeted gene therapy: strategies for the preparation of ligand-polyethylene glycol-polyethylenimine/ DNA complexes. J. Control. Release 91(1-2), 173-181 (2003).
98. Aina OH, Sroka TC, Chen ML, Lam KS. Therapeutic cancer targeting peptides. Biopolymers 66(3), 184-199 (2002).
99. Fay F, Scott CJ. Antibody-targeted nanoparticles for cancer therapy. Immunotherapy 3(3), 381-394 (2011).
100. Giorello L, Clerico L, Pescarolo MP et al. Inhibition of cancer cell growth and c-Myc transcriptional activity by a c-Myc helix 1-type peptide fused to an internalization sequence. Cancer Res. 58(16), 3654-3659 (1998).
101. Mae M, Langel U. Cell-penetrating peptides as vectors for peptide, protein and oligonucleotide delivery. Curr. Opin. Pharmacol. 6(5), 509-514 (2006).
102. Gupta B, Levchenko TS, Torchilin VP. Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv. Drug Deliv. Rev. 57(4), 637-651 (2005).
103. Rousselle C, Clair P, Lefauconnier JM, Kaczorek M, Scherrmann JM, Temsamani J. New advances in the transport of doxorubicin through the blood-brain barrier by a peptide vector-mediated strategy. Mol. Pharmacol. 57(4), 679-686 (2000).
104. Rousselle C, Clair P, Smirnova M et al. Improved brain uptake and pharmacological activity of dalargin using a peptide-vector-mediated strategy. J. Pharmacol. Exp. Ther. 306(1), 371-376 (2003).
105. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285(5433), 1569-1572 (1999).
106. Aguilera TA, Olson ES, Timmers MM, Jiang T, Tsien RY. Systemic in vivo distribution of activatable cell penetrating peptides is superior to that of cell penetrating peptides. Integr. Biol. (Camb.) 1(5-6), 371-381 (2009).
107. Van Den Berg A, Dowdy SF. Protein transduction domain delivery of therapeutic macromolecules. Curr. Opin. Biotechnol. 22(6), 888-893 (2011).
108. Teesalu T, Sugahara KN, Kotamraju VR, Ruoslahti E. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc. Natl Acad. Sci. USA 106(38), 16157-16162 (2009).
109. Sugahara KN, Teesalu T, Karmali PP et al. Tissue-penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell 16(6), 510-520 (2009).
110. Sugahara KN, Teesalu T, Karmali PP et al. Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science 328(5981), 1031-1035 (2010).
111. Agemy L, Friedmann-Morvinski D, Kotamraju VR et al. Targeted nanoparticle enhanced proapoptotic peptide as potential therapy for glioblastoma. Proc. Natl Acad. Sci. USA 108(42), 17450-17455 (2011).
112. Olson ES, Aguilera TA, Jiang T et al. In vivo characterization of activatable cell penetrating peptides for targeting protease activity in cancer. Integr. Biol. (Camb.) 1(5-6), 382-393 (2009).
113. Olson ES, Jiang T, Aguilera TA 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. USA 107(9), 4311-4316 (2010