A cell penetrating peptide-integrated and enediyne-energized fusion protein shows potent antitumor activity

European Journal of Pharmaceutical Sciences

Volumn 47, Issue 4, 2012, Pages 781-789

  Ru, Qin ^a,b   Shang, Bo Yang ^a   Miao, Qing Fang ^a   Li, Liang ^a   Wu, Shu Ying ^a   Gao, Rui Juan ^a   Zhen, Yong Su ^a  

^a PEKING UNION MEDICAL COLLEGE   (China)

^b JIANGHAN UNIVERSITY   (China)

Author keywords

Cell penetrating peptides; Endocytosis; Enediyne energized fusion protein; Lidamycin

Indexed keywords

ANTINEOPLASTIC AGENT; APOPROTEIN; ARGININE; CELL PENETRATING PEPTIDE; ENEDIYNE; HYBRID PROTEIN; LIDAMYCIN; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CANCER GROWTH; CARCINOMA CELL; CELL SELECTION; CYTOTOXICITY; DNA RECOMBINATION; ENDOCYTOSIS; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; LUNG CARCINOMA; MOUSE; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; TUMOR XENOGRAFT;

AMINOGLYCOSIDES; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; APOPROTEINS; ARGININE; BASE SEQUENCE; CELL LINE, TUMOR; CELL-PENETRATING PEPTIDES; ENDOCYTOSIS; ENEDIYNES; FEMALE; HEP G2 CELLS; HUMANS; MCF-7 CELLS; MICE; MICE, NUDE; MOLECULAR SEQUENCE DATA; RECOMBINANT FUSION PROTEINS;

EID: 84867088042     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2012.09.002     Document Type: Article

References (52)

1. R. Abes, A. Arzumanov, H. Moulton, S. Abes, G. Ivanova, M.J. Gait, P. Iversen, and B. Lebleu Arginine-rich cell penetrating peptides: design, structure-activity, and applications to alter pre-mRNA splicing by steric-block oligonucleotides J. Pept. Sci. 14 2008 455 460
2. L. Agemy, D. Friedmann-Morvinski, V.R. Kotamraju, L. Roth, K.N. Sugahara, O.M. Girard, R.F. Mattrey, I.M. Verma, and E. Ruoslahti Targeted nanoparticle enhanced proapoptotic peptide as potential therapy for glioblastoma Proc. Natl. Acad. Sci. USA 108 2011 17450 17455
3. S. Anandhakumar, V. Nagaraja, and A.M. Raichur Reversible polyelectrolyte capsules as carriers for protein delivery Colloids Surf. B Biointerf. 78 2010 266 274
4. S.E. Andaloussi, T. Lehto, P. Lundin, and U. Langel Application of PepFect peptides for the delivery of splice-correcting oligonucleotides Methods Mol. Biol. 683 2011 361 373
5. A.M. Angeles-Boza, A. Erazo-Oliveras, Y.J. Lee, and J.P. Pellois Generation of endosomolytic reagents by branching of cell-penetrating peptides: tools for the delivery of bioactive compounds to live cells in cis or trans Bioconjug. Chem. 21 2010 2164 2167
6. J. Bian, Z.B. Popovic, C. Benejam, M. Kiedrowski, L.L. Rodriguez, and M.S. Penn Effect of cell-based intercellular delivery of transcription factor GATA4 on ischemic cardiomyopathy Circ. Res. 100 2007 1626 1633
7. G.L. Bidwell 3rd, and D. Raucher Cell penetrating elastin-like polypeptides for therapeutic peptide delivery Adv. Drug Deliv. Rev. 62 2010 1486 1496
8. A. Bolhassani Potential efficacy of cell-penetrating peptides for nucleic acid and drug delivery in cancer Biochim. Biophys. Acta 1816 2011 232 246
9. R. Brasseur, and G. Divita Happy birthday cell penetrating peptides: already 20 years Biochim. Biophys. Acta 1798 2010 2177 2181
10. K. Cahill Cell-penetrating peptides, electroporation and drug delivery IET Syst. Biol. 4 2010 367 378
11. L. Cai, H. Chen, Q. Miao, S. Wu, Y. Shang, Y. Zhen, L.R. Tsuruta, K. Hayashi, T. Matsumoto, Y. Kato, S. Ishiwata, K. Itoh, T. Suzuki, M. Hirama, and M. Mizugaki Binding capability of the enediyne-associated apoprotein to human tumors and constitution of a ligand oligopeptide-integrated protein J. Biotechnol. 144 2009 142 150
12. T.Y. Chao, and R.T. Raines Mechanism of ribonuclease A endocytosis: analogies to cell-penetrating peptides Biochemistry (Mosc.) 50 2011 8374 8382
13. Y. Choi, J.R. McCarthy, R. Weissleder, and C.H. Tung Conjugation of a photosensitizer to an oligoarginine-based cell-penetrating peptide increases the efficacy of photodynamic therapy ChemMedChem 1 2006 458 463
14. 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 1994 10444 10450
15. I. Fischer, J.P. Gagner, M. Law, E.W. Newcomb, and D. Zagzag Angiogenesis in gliomas: biology and molecular pathophysiology Brain Pathol. 15 2005 297 310
16. M. Fotin-Mleczek, S. Welte, O. Mader, F. Duchardt, R. Fischer, H. Hufnagel, P. Scheurich, and R. Brock Cationic cell-penetrating peptides interfere with TNF signalling by induction of TNF receptor internalization J. Cell Sci. 118 2005 3339 3351
17. S.M. Fuchs, and R.T. Raines Pathway for polyarginine entry into mammalian cells Biochemistry (Mosc.) 43 2004 2438 2444
18. B. Gupta, T.S. Levchenko, and V.P. Torchilin Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides Adv. Drug Deliv. Rev. 57 2005 637 651
19. P. Jarver, and U. Langel Cell-penetrating peptides - a brief introduction Biochim. Biophys. Acta 1758 2006 260 263
20. R.M. Johnson, S.D. Harrison, and D. Maclean Therapeutic applications of cell-penetrating peptides Methods Mol. Biol. 683 2011 535 551
21. A. Kerkis, M.A. Hayashi, T. Yamane, and I. Kerkis Properties of cell penetrating peptides (CPPs) IUBMB Life 58 2006 7 13
22. S.S. Lakka, and J.S. Rao Antiangiogenic therapy in brain tumors Expert Rev. Neurother. 8 2008 1457 1473
23. D.X. Ma, N.Q. Shi, and X.R. Qi Distinct transduction modes of arginine-rich cell-penetrating peptides for cargo delivery into tumor cells Int. J. Pharm. 419 2011 200 208
24. S.P. Mathupala Delivery of small-interfering RNA (siRNA) to the brain Expert Opin. Ther. Pat. 19 2009 137 140
25. M.M. McHugh, L.S. Gawron, S. Matsui, and T.A. Beerman The antitumor enediyne C-1027 alters cell cycle progression and induces chromosomal aberrations and telomere dysfunction Cancer Res. 65 2005 5344 5351
26. Q.F. Miao, X.Y. Liu, B.Y. Shang, Z.G. Ouyang, and Y.S. Zhen An enediyne-energized single-domain antibody-containing fusion protein shows potent antitumor activity Anticancer Drugs 18 2007 127 137
27. T. Mino, T. Mori, Y. Aoyama, and T. Sera Cell-permeable artificial zinc-finger proteins as potent antiviral drugs for human papillomaviruses Arch. Virol. 153 2008 1291 1298
28. D.J. Mitchell, D.T. Kim, L. Steinman, C.G. Fathman, and J.B. Rothbard Polyarginine enters cells more efficiently than other polycationic homopolymers J. Pept. Res. 56 2000 318 325
29. H.B. Newton Advances in strategies to improve drug delivery to brain tumors Expert Rev. Neurother. 6 2006 1495 1509
30. J.P. Richard, K. Melikov, E. Vives, C. Ramos, B. Verbeure, M.J. Gait, L.V. Chernomordik, and B. Lebleu Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake J. Biol. Chem. 278 2003 585 590
31. S. Santra, H. Yang, J.T. Stanley, P.H. Holloway, B.M. Moudgil, G. Walter, and R.A. Mericle Rapid and effective labeling of brain tissue using TAT-conjugated CdS:Mn/ZnS quantum dots Chem. Commun. (Camb.) 2005 3144 3146
32. S. Sathornsumetee, D.A. Reardon, A. Desjardins, J.A. Quinn, J.J. Vredenburgh, and J.N. Rich Molecularly targeted therapy for malignant glioma Cancer 110 2007 13 24
33. R.G. Shao Pharmacology and therapeutic applications of enediyne antitumor antibiotics Curr. Mol. Pharmacol. 1 2008 50 60
34. R.G. Shao, and Y.S. Zhen Enediyne anticancer antibiotic lidamycin: chemistry, biology and pharmacology Anticancer Agents Med. Chem. 8 2008 123 131
35. D.J. Stephens, and R. Pepperkok The many ways to cross the plasma membrane Proc. Natl. Acad. Sci. USA 98 2001 4295 4298
36. J.S. Suh, K.S. Kim, J.Y. Lee, Y.J. Choi, C.P. Chung, and Y.J. Park A cell-permeable fusion protein for the mineralization of human dental pulp stem cells J. Dent. Res. 91 2012 90 96
37. J. Temsamani, and P. Vidal The use of cell-penetrating peptides for drug delivery Drug Discov. Today 9 2004 1012 1019
38. K. Tsumoto, K. Shinoki, H. Kondo, M. Uchikawa, T. Juji, and I. Kumagai Highly efficient recovery of functional single-chain Fv fragments from inclusion bodies overexpressed in Escherichia coli by controlled introduction of oxidizing reagent-application to a human single-chain Fv fragment J. Immunol. Methods 219 1998 119 129
39. E.G. Van Meir, C.G. Hadjipanayis, A.D. Norden, H.K. Shu, P.Y. Wen, and J.J. Olson Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma CA Cancer J. Clin. 60 2010 166 193
40. 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 1997 16010 16017
41. J.S. Wadia, R.V. Stan, and S.F. Dowdy Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis Nat. Med. 10 2004 310 315
42. 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. USA 97 2000 13003 13008
43. Y.J. Xu, D.D. Li, and Y.S. Zhen Mode of action of C-1027, a new macromolecular antitumor antibiotic with highly potent cytotoxicity, on human hepatoma BEL-7402 cells Cancer Chemother. Pharmacol. 27 1990 41 46
44. Y.J. Xu, Y.S. Zhen, and I.H. Goldberg C1027 chromophore, a potent new enediyne antitumor antibiotic, induces sequence-specific double-strand DNA cleavage Biochemistry (Mosc.) 33 1994 5947 5954
45. T. Yamada, Y. Iwasaki, H. Tada, H. Iwabuki, M.K. Chuah, T. VandenDriessche, H. Fukuda, A. Kondo, M. Ueda, M. Seno, K. Tanizawa, and S. Kuroda Nanoparticles for the delivery of genes and drugs to human hepatocytes Nat. Biotechnol. 21 2003 885 890
46. S.R. Yang, S.B. Kim, C.O. Joe, and J.D. Kim Intracellular delivery enhancement of poly(amino acid) drug carriers by oligoarginine conjugation J. Biomed. Mater. Res. A 86 2008 137 148
47. X.H. Zhai, M. Liu, X.J. Guo, S.C. Wang, H.X. Zhang, and Y.M. Guo SKOV-3 cell imaging by paramagnetic particles labeled with hairpin cell-penetrating peptides Chin. Med. J. (Engl.) 124 2011 111 117
48. J. Zhao, P. Gao, W. Xiao, L.Q. Fan, F.J. Wang, S.X. Li, and J.W. Liu A novel human derived cell-penetrating peptide in drug delivery Mol. Biol. Rep. 38 2011 2649 2656
49. Y.S. Zhen, X.Y. Ming, B. Yu, T. Otani, H. Saito, and Y. Yamada A new macromolecular antitumor antibiotic, C-1027. III. Antitumor activity J. Antibiot. (Tokyo) 42 1989 1294 1298
50. Y.Z. Zhen, Y.J. Lin, Y. Li, and Y.S. Zhen Lidamycin shows highly potent cytotoxic to myeloma cells and inhibits tumor growth in mice Acta Pharmacol. Sin. 30 2009 1025 1032
51. G. Zhong, S. Zhang, Y. Li, X. Liu, R. Gao, Q. Miao, and Y. Zhen A tandem scFv-based fusion protein and its enediyne-energized analogue show intensified therapeutic efficacy against lung carcinoma xenograft in athymic mice Cancer Lett. 295 2010 124 133
52. M. Zorko, and U. Langel Cell-penetrating peptides: mechanism and kinetics of cargo delivery Adv. Drug Deliv. Rev. 57 2005 529 545.