Applications of cell-penetrating peptides for tumor targeting and future cancer therapies

Pharmaceuticals

Volumn 5, Issue 9, 2012, Pages 991-1007

  Regberg, Jakob ^a   Srimanee, Artita ^a,b   Langel, Ülo ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Cancer; Cell penetrating peptides; Cell targeting peptides; Drug delivery; Oligonucleotides; siRNA therapeutics

Indexed keywords

ALKYLATING AGENT; ANTINEOPLASTIC AGENT; CELL PENETRATING PEPTIDE; CHEMOKINE RECEPTOR CXCR4; CHLORAMBUCIL; DOXORUBICIN; DRUG CARRIER; MAUROCALCINE; METHOTREXATE; PENETRATIN; PEPFECT 14; PEPFECT 3; PEPFECT 6; PEPTIDE D1; PEPTIDE D3; PEPTIDE K4; PLASMID DNA; POLYARGININE; PROTEIN P16; PROTEIN P53; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SMALL INTERFERING RNA; STERYLPOLYARGININE; SYNB1 PROTEIN; SYNB3 PROTEIN; TRANSPORTAN; TRANSPORTAN 10; UNCLASSIFIED DRUG; UNINDEXED DRUG; YTA2 PROTEIN; YTA4 PROTEIN;

CANCER CELL; CANCER CHEMOTHERAPY; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG TARGETING; DRUG UPTAKE; ENDOCYTOSIS; HUMAN; NONHUMAN; REVIEW;

EID: 84866535298     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph5090991     Document Type: Review

References (59)

1. Vivès, E.; Brodin, P.; Lebleu, B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 1997, 272, 16010-16017.
2. Derossi, D.; Joliot, H.; Chassaing, G.; Prochiantz, A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 1994, 269, 10444-10450.
3. Pooga, M.; Hällbrink, M.; Zorko, M.; Langel, Ü. Cell penetration by transportan. FASEB J. 1998, 12, 67-77.
4. Kilk, K.; EL-Andaloussi, S.; Järver, P.; Meikas, A.; Valkna, A.; Bartfai, T.; Kogerman, P.; Metsis, M.; Langel, Ü. Evaluation of transportan 10 in PEI mediated plasmid delivery assay. J. Control. Release 2005, 103, 511-523.
5. Futaki, S.; Ohashi, W.; Suzuki, T.; Niwa, M.; Tanaka, S.; Ueda, K.; Harashima, H.; Sugiura, Y. Stearylated arginine-rich peptides: A new class of transfection systems. Bioconjugate Chem. 2001, 12, 1005-1011.
6. Mäe, M.; EL-Andaloussi, S.; Lundin, P.; Oskolkov, N.; Johansson, H. J.; Guterstam, P.; Langel, Ü. A stearylated CPP for delivery of splice correcting oligonucleotides using a non-covalent coincubation strategy. J. Control. Release 2009, 134, 221-227.
7. Lehto, T.; Kurrikoff, K.; Langel, Ü. Cell-penetrating peptides for the delivery of nucleic acids. Expert Opin. Drug Del. 2012, 9, 823-836.
8. Sarko, D.; Beijer, B.; Boy, R. G.; Nothelfer, E.-M.; Leotta, K.; Eisenhut, M.; Altmann, A.; Haberkorn, U.; Walter, M. The pharmacokinetics of cell-penetrating peptides. Mol. Biopharm. 2010, 7, 2224-2231.
9. Elmquist, A.; Lindgren, M.; Bartfai, T.; Langel, Ü. VE-cadherin-derived cell-penetrating peptide, pVEC, with carrier functions. Exp. Cell Res. 2001, 269, 237-244.
10. Crombez, L.; Morris, M.C.; Heitz, F.; Divita, G. A non-covalent peptide-based strategy for ex vivo and in vivo oligonucleotide delivery. Meth. Mol. Biol. 2011, 764, 59-73.
11. Lindgren, M.; Gallet, X.; Soomets, U.; Hällbrink, M.; Bråkenhielm, E.; Pooga, M.; Brasseur, R.; Langel, Ü. Translocation properties of novel cell penetrating transportan and penetratin analogues. Bioconjugate Chem. 2000, 11, 619-626.
12. EL-Andaloussi, S.; Lehto, T.; Mäger, I.; Rosenthal-Aizman, K.; Oprea, I.I.; Simonson, O.E.; Sork, H.; Ezzat, K.; Copolovici, D.M.; Kurrikoff K. et al. Design of a peptide-based vector, PepFect6, for efficient delivery of siRNA in cell culture and systemically in vivo. Nucleic Acids Res. 2011, 39, 3972-3987.
13. Ezzat, K.; EL-Andaloussi, S.; Zaghloul, E.M.; Lehto, T.; Lindberg, S.; Moreno, P.M.D.; Viola, J.R.; Magdy, T.; Abdo, R.; Guterstam, P. et al. PepFect 14, a novel cell-penetrating peptide for oligonucleotide delivery in solution and as solid formulation. Nucleic Acids Res. 2011, 39, 5284-5298.
14. Futaki, S.; Nakase, I.; Tadokoro, A.; Takeuchi, T.; Jones, T. Arginine-rich peptides and their internalization mechanisms. Biochem. Soc. Trans. 2007, 35, 784-787.
15. Heitz, F.; Morris, M.C.; Divita, G. Twenty years of cell penetrating peptides: From molecular mechanisms to therapeutics. Br. J. Pharmacol. 2009, 157, 195-206.
16. Morris, M.C.; Gros, E.; Aldrian-Herrada, G.; Choob, M.; Archdeacon, J.; Heitz, F.; Divita, G. A non-covalent peptide-based carrier for in vivo delivery of DNA mimics. Nucleic Acids Res. 2007, 35, e49.
17. Rydström, A.; Deshayes, S.; Konate, K.; Crombez, L.; Padari, K.; Boukhaddaoui, H.; Aldrian, G.; Pooga, M.; Divita, G. Direct translocation as major cellular uptake for CADY self-assembling peptide-based nanoparticles. PLoS One 2011, 6, e25924.
18. Myrberg, H.; Lindgren, M.; Langel, Ü. Protein delivery by the cell-penetrating peptide YTA2. Bioconjugate Chem. 2007, 18, 170-174.
19. Mäe, M.; Rautsi, O.; Enbäck, J.; Hällbrink, M.; Aizman, K.R.; Lindgren, M.; Laakkonen, P.; Langel, Ü. Tumour targeting with rationally modified cell-penetrating peptides. Int. J. Pept. Res. and Ther. 2012, doi:10.1007/s10989-012-9312-1.
20. Rousselle, C.; Smirnova, M.; Clair, P.; Lefauconnier, J.M.; Chavanieu, A.; Calas, B.; Scherrmann, J.M.; Temsamani, J. Enhanced delivery of doxorubicin into the brain via a peptide-vectormediated strategy: Saturation kinetics and specificity. J. Pharmacol. Exp. Ther. 2001, 296, 124-131.
21. Rousselle, C.; Clair, P.; Lefauconnier, J.M.; Kaczorek, M.; Scherrmann, J.M.; Temsamani, J. New advances in the transport of doxorubicin through the blood-brain barrier by a peptide vectormediated strategy. Mol. Pharmacol. 2000, 57, 679-686.
22. Aroui, S.; Ram, N.; Appaix, F.; Ronjat, M.; Kenani, A.; Pirollet, F.; De Waard, M. Maurocalcine as a non toxic drug carrier overcomes doxorubicin resistance in the cancer cell line MDA-MB 231. Pharm. Res. 2009, 26, 836-845.
23. Fajloun, Z.; Kharrat, R.; Chen, L.; Lecomte, C.; Di Luccio, E.; Bichet, D.; El Ayeb, M.; Rochat, H.; Allen, P.D.; Pessah, I.N.; et al. Chemical synthesis and characterization of maurocalcine, a scorpion toxin that activates Ca(2+) release channel/ryanodine receptors. FEBS Lett. 2000, 469, 179-185.
24. Wang, H.; Chen, X.; Chen, Y.; Sun, L.; Li, G.; Zhai, M.; Zhai, W.; Kang, Q.; Gao, Y.; Qi, Y. Antitumor activity of novel chimeric peptides derived from cyclinD/CDK4 and the protein transduction domain 4. Amino Acids 2012, doi:10.1007/s00726-012-1360-5.
25. Richard, J.P.; Melikov, K.; Vives, E.; Ramos, C.; Verbeure, B.; Gait, M.J.; Chernomordik, L.V.; Lebleu, B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol.Chem. 2003, 278, 585-590.
26. Lundin, P.; Johansson, H.; Guterstam, P.; Holm, T.; Hansen, M.; Langel, Ü.; EL-Andaloussi, S. Distinct uptake routes of cell-penetrating peptide conjugates. Bioconjugate Chem. 2008, 19, 2535-2542.
27. Drin, G.; Cottin, S.; Blanc, E.; Rees, A.R.; Temsamani, J. Studies on the internalization mechanism of cationic cell-penetrating peptides. J. Biol.Chem. 2003, 278, 31192-201.
28. Yamagata, M.; Kawano, T.; Shiba, K.; Mori, T.; Katayama, Y.; Niidome, T. Structural advantage of dendritic poly(L-lysine) for gene delivery into cells. Bioorg. Med. Chem. 2007, 15, 526-532.
29. Letoha, T.; Keller-Pintér, A.; Kusz, E.; Kolozsi, C.; Bozsó, Z.; Tóth, G.; Vizler, C.; Oláh, Z.; Szilák, L. Cell-penetrating peptide exploited syndecans. Biochim. Biophys. Acta 2010, 1798, 2258-2265.
30. Subrizi, A.; Tuominen, E.; Bunker, A.; Róg, T.; Antopolsky, M.; Urtti, A. Tat(48-60) peptide amino acid sequence is not unique in its cell penetrating properties and cell-surface glycosaminoglycans inhibit its cellular uptake. J. Control. Release 2012, 158, 277-285.
31. Ezzat, K.; Helmfors, H.; Tudoran, O.; Juks, C.; Lindberg, S.; Padari, K.; EL-Andaloussi, S.; Pooga, M.; Langel, Ü. Scavenger receptor-mediated uptake of cell-penetrating peptide nanocomplexes with oligonucleotides. FASEB J. 2012, 26, 1172-1180.
32. Tünnemann, G.; Martin, R.M.; Haupt, S.; Patsch, C.; Edenhofer, F.; Cardoso, M.C. Cargodependent mode of uptake and bioavailability of TAT-containing proteins and peptides in living cells. FASEB J. 2006, 20, 1175-1184.
33. Bolhassani, A. Potential efficacy of cell-penetrating peptides for nucleic acid and drug delivery in cancer. Biochim. Biophys. Acta 2011, 1816, 232-246.
34. Munyendo, W.L.L.; Lv, H.; Benza-Ingoula, H.; Baraza, L.D.; Zhou, J. Cell penetrating peptides in the delivery of biopharmaceuticals. Biomolecules 2012, 2, 187-202.
35. Vivès, E.; Schmidt, J.; Pèlegrin, A. Cell-penetrating and cell-targeting peptides in drug delivery. Biochim. Biophys. Acta 2008, 1786, 126-138.
36. Mäe, M.; Myrberg, H.; EL-Andaloussi, S.; Langel, Ü. Design of a tumor homing cell-penetrating peptide for drug delivery. Int. J. Pept. Res. Ther. 2008, 15, 11-15.
37. Zhang, X.X.; Eden, H.S.; Chen, X. Peptides in cancer nanomedicine: Drug carriers, targeting ligands and protease substrates. J. Control. Release 2012, 159, 2-13.
38. Myrberg, H.; Zhang, L.; Mäe, M.; Langel, Ü. Design of a tumor-homing cell-penetrating peptide. Bioconjugate Chem. 2008, 19, 70-75.
39. Kersemans, V.; Cornelissen, B. Targeting the tumour: Cell Penetrating peptides for molecular imaging and radiotherapy. Pharmaceuticals 2010, 3, 600-620.
40. Laakkonen, P.; Vuorinen, K. Homing peptides as targeted delivery vehicles. Integr. Biol. 2010, 2, 326-337.
41. Kumar, P.; Wu, H.; McBride, J.L.; Jung, K.E.; Kim, M.H.; Davidson, B.L.; Lee, S.K.; Shankar, P.; Manjunath, N. Transvascular delivery of small interfering RNA to the central nervous system. Nature 2007, 448, 39-43.
42. Snyder, E.L.; Saenz, C.C.; Denicourt, C.; Meade, B.R.; Cui, X.S.; Kaplan, I.M.; Dowdy, S.F. Enhanced targeting and killing of tumor cells expressing the CXC chemokine receptor 4 by transducible anticancer peptides. Cancer Res. 2005, 65, 10646-10650.
43. Jiang, Q.Y.; Lai, L.H.; Shen, J.; Wang, Q.Q.; Xu, F.J.; Tang, G.P. Gene delivery to tumor cells by cationic polymeric nanovectors coupled to folic acid and the cell-penetrating peptide octaarginine. Biomaterials 2011, 32, 7253-7262.
44. Bauer, C.; Bauder-Wuest, U. 131I-labeled peptides as caspase substrates for apoptosis imaging. J. Nucl. Med. 2005, 46, 1066-1074.
45. Shi, N.Q.; Gao, W.; Xiang, B.; Qi, X.R. Enhancing cellular uptake of activable cell-penetrating peptide-doxorubicin conjugate by enzymatic cleavage. Int. J. Nanomed. 2012, 7, 1613-1621.
46. Olson, E.; Aguilera, T.; Jiang, T.; Ellies, L.G.; Nguyen, Q.T.; Wong, E.H.; Gross, L.A.; Tsien, R.Y. In vivo characterization of activatable cell penetrating peptides for targeting protease activity in cancer. Integr. Biol. 2009, 1, 382-393.
47. van Duijnhoven, S.M.J.; Robillard, M.S.; Nicolay, K.; Grüll, H. Tumor targeting of MMP-2/9 activatable cell-penetrating imaging probes is caused by tumor-independent activation. J. Nucl. Med. 2011, 52, 279-286.
48. Aguilera, T.; Olson, E.S.; Timmers, M.M.; Jiang, T.; Tsien, R.Y. Systemic in vivo distribution of activatable cell penetrating peptides is superior to that of cell penetrating peptides. Integr. Biol. 2009, 1, 371-381.
49. Curran, S.; Murray, G.I. Matrix metalloproteinases: Molecular aspects of their roles in tumour invasion and metastasis. Eur. J. Cancer 2000, 36, 1621-1630.
50. Polette, M.; Nawrocki-Raby, B.; Gilles, C.; Clavel, C.; Birembaut, P. Tumour invasion and matrix metalloproteinases. Crit. Rev. Oncol./Hematol. 2004, 49, 179-186.
51. Deryugina, E.I.; Quigley, J.P. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006, 25, 9-34.
52. Snyder, E.L.; Dowdy, S.F. Cell penetrating peptides in drug delivery. Pharm. Res. 2004, 21, 389-393.
53. Harada, H.; Hiraoka, M.; Kizaka-Kondoh, S. Antitumor effect of TAT-oxygen-dependent degradation-caspase-3 fusion protein specifically stabilized and activated in hypoxic tumor cells. Cancer Res. 2002, 1, 2013-2018.
54. Harada, H.; Kizaka-Kondoh, S.; Hiraoka, M. Antitumor protein therapy; application of the protein transduction domain to the development of a protein drug for cancer treatment. Breast Cancer 2006, 13, 16-26.
55. Li, Y.; Zheng, X.; Cao, Z.; Xu, W.; Zhang, J.; Gong, M. Self-assembled peptide (CADY-1) improved the clinical application of doxorubicin. Int. J. Pharm. 2012, 434, 209-214.
56. Aroui, S.; Brahim, S.; Waard, M.D.; Kenani, A. Cytotoxicity, intracellular distribution and uptake of doxorubicin and doxorubicin coupled to cell-penetrating peptides in different cell lines: A comparative study. Biochem. Biophys. Res. Commun. 2010, 391, 419-425.
57. Patel, L.N.; Zaro, J.L.; Shen, W.C. Cell penetrating peptides: Intracellular pathways and pharmaceutical perspectives. Pharm. Res. 2007, 24, 1977-1992.
58. Lindgren, M.; Rosenthal-Aizman, K.; Saar, K.; Eiríksdóttir, E.; Jiang, Y.; Sassian, M.; Ostlund, P.; Hällbrink, M.; Langel, Ü. Overcoming methotrexate resistance in breast cancer tumour cells by the use of a new cell-penetrating peptide. Biochem. Pharmacol. 2006, 71, 416-425.
59. Chaloin, L.; Bigey, P.; Loup, C.; Marin, M.; Galeotti, N.; Piechaczyk, M.; Heitz, F.; Meunier, B. Improvement of porphyrin cellular delivery and activity by conjugation to a carrier peptide. Bioconjugate Chem. 2001, 12, 691-700.