Accumulation of arginine-rich cell-penetrating peptides in tumors and the potential for anticancer drug delivery in vivo

Journal of Controlled Release

Volumn 159, Issue 2, 2012, Pages 181-188

  Nakase, Ikuhiko ^a   Konishi, Yusuke ^a   Ueda, Masashi ^a,b   Saji, Hideo ^a   Futaki, Shiroh ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY HOSPITAL   (Japan)

Author keywords

Arginine rich cell penetrating peptide; Biodistribution; Doxorubicin; Drug delivery; In vivo fluorescent imaging; Tumor accumulation

Indexed keywords

BIODISTRIBUTIONS; CELL-PENETRATING PEPTIDE; DOXORUBICIN; FLUORESCENT IMAGING; TUMOR ACCUMULATION;

ARGININE; CELLS; CYTOLOGY; DRUG DELIVERY; MAMMALS; PEPTIDES;

TUMORS;

ANTINEOPLASTIC AGENT; CELL PENETRATING PEPTIDE; DEXTRO ARGININE; DOXORUBICIN; GLYCOSAMINOGLYCAN; OCTAARGININE; PENETRATIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG MEGADOSE; DRUG PENETRATION; ENANTIOMER; FEMALE; FLUORESCENCE; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR; TUMOR GROWTH; TUMOR XENOGRAFT; WEIGHT REDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; CARRIER PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; CELL-PENETRATING PEPTIDES; CHO CELLS; CRICETINAE; DOXORUBICIN; DRUG CARRIERS; FEMALE; HELA CELLS; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; MICROSCOPY, CONFOCAL; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; STEREOISOMERISM; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TIME FACTORS; TISSUE DISTRIBUTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84861057424     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.01.016     Document Type: Article

References (51)

1. E. Ruoslahti, and M.D. Pierschbacher New perspectives in cell adhesion: RGD and integrins Science 238 1987 491 497 (Pubitemid 17147032)
2. S. Liu Radiolabeled cyclic RGD peptides as integrin alpha(v)beta(3)- targeted radiotracers: maximizing binding affinity via bivalency Bioconjug. Chem. 20 2009 2199 2213
3. A.V. Schally, and A. Nagy New approaches to treatment of various cancers based on cytotoxic analogs of LHRH, somatostatin and bombesin Life Sci. 72 2003 2305 2320 (Pubitemid 36287676)
4. S.M. Okarvi Peptide-based radiopharmaceuticals and cytotoxic conjugates: potential tools against cancer Cancer Treat. Rev. 34 2008 13 26 (Pubitemid 351168607)
5. S.E. Pool, E.P. Krenning, G.A. Koning, C.H. van Eijck, J.J. Teunissen, B. Kam, R. Valkema, D.J. Kwekkeboom, and M. de Jong Preclinical and clinical studies of peptide receptor radionuclide therapy Semin. Nucl. Med. 40 2010 209 218
6. X.L. Wang, R. Xu, and Z.R. Lu A peptide-targeted delivery system with pH-sensitive amphiphilic cell membrane disruption for efficient receptor-mediated siRNA delivery J. Control. Release 134 2009 207 213
7. J. Enbäck, and P. Laakkonen Tumour-homing peptides: tools for targeting, imaging and destruction Biochem. Soc. Trans. 35 2007 780 783 (Pubitemid 47310367)
8. A. Rivinoja, and P. Laakkonen Identification of homing peptides using the in vivo phage display technology Meth. Mol. Biol. 683 2011 401 415
9. W. Tai, R. Mahato, and K. Cheng The role of HER2 in cancer therapy and targeted drug delivery J. Control. Release 146 2010 264 275
10. V. Askoxylakis, S. Zitzmann-Kolbe, F. Zoller, A. Altmann, A. Markert, S. Rana, A. Marr, W. Mier, J. Debus, and U. Haberkorn Challenges in optimizing a prostate carcinoma binding peptide, identified through the phage display technology Molecules 16 2011 1559 1578
11. E. Vivès, 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 (Pubitemid 27265584)
12. J.B. Rothbard, S. Garlington, Q. Lin, T. Kirschberg, E. Kreider, P.L. McGrane, P.A. Wender, and P.A. Khavari Conjugation of arginine oligomers to cyclosporin A facilitates topical delivery and inhibition of inflammation Nat. Med. 6 2000 1253 1257
13. S. Futaki, T. Suzuki, W. Ohashi, T. Yagami, S. Tanaka, K. Ueda, and Y. Sugiura Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery J. Biol. Chem. 276 2001 5836 5840
14. Special Theme Issue on Membrane Permeable Peptide Vectors: Chemistry and Functional Design for the Therapeutic Applications S. Futaki Adv. Drug Deliv. Rev. vol. 60 2008 447 614
15. E.A. Dubikovskaya, S.H. Thorne, T.H. Pillow, C.H. Contag, and P.A. Wender Overcoming multidrug resistance of small-molecule therapeutics through conjugation with releasable octaarginine transporters Proc. Natl. Acad. Sci. U. S. A. 105 2008 12128 12133
16. S. Fawell, J. Seery, Y. Daikh, C. Moore, L.L. Chen, B. Pepinsky, and J. Barsoum Tat-mediated delivery of heterologous proteins into cells Proc. Natl. Acad. Sci. U. S. A. 91 1994 664 668 (Pubitemid 24041462)
17. 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 1999 1569 1572 (Pubitemid 29420581)
18. H.J. Lee, and W.M. Pardridge Pharmacokinetics and delivery of tat and tat-protein conjugates to tissues in vivo Bioconjug. Chem. 12 2001 995 999 (Pubitemid 33136870)
19. K.E. Bullok, M. Dyszlewski, J.L. Prior, C.M. Pica, V. Sharma, and D. Piwnica-Worms Characterization of novel histidine-tagged Tat-peptide complexes dual-labeled with (99m)Tc-tricarbonyl and fluorescein for scintigraphy and fluorescence microscopy Bioconjug. Chem. 13 2002 1226 1237 (Pubitemid 35420014)
20. P. Wunderbaldinger, L. Josephson, and R. Weissleder Tat peptide directs enhanced clearance and hepatic permeability of magnetic nanoparticles Bioconjug. Chem. 13 2002 264 268 (Pubitemid 34267937)
21. S. Kameyama, R. Okada, T. Kikuchi, T. Omura, I. Nakase, T. Takeuchi, Y. Sugiura, and S. Futaki Distribution of immunoglobulin Fab fragment conjugated with HIV-1 REV peptide following intravenous administration in rats Mol. Pharm. 3 2006 174 180 (Pubitemid 43672253)
22. S. Kameyama, M. Horie, T. Kikuchi, T. Omura, T. Takeuchi, I. Nakase, Y. Sugiura, and S. Futaki Effects of cell-permeating peptide binding on the distribution of 125I-labeled Fab fragment in rats Bioconjug. Chem. 17 2006 597 602 (Pubitemid 43794368)
23. E.L. Snyder, B.R. Meade, C.C. Saenz, and S.F. Dowdy Treatment of terminal peritoneal carcinomatosis by a transducible p53-activating peptide PLoS Biol. 2 2004 E36
24. M. Tan, K.H. Lan, J. Yao, C.H. Lu, M. Sun, C.L. Neal, J. Lu, and D. Yu Selective inhibition of ErbB2-overexpressing breast cancer in vivo by a novel TAT-based ErbB2-targeting signal transducers and activators of transcription 3-blocking peptide Cancer Res. 66 2006 3764 3772
25. S. Kizaka-Kondoh, S. Itasaka, L. Zeng, S. Tanaka, T. Zhao, Y. Takahashi, K. Shibuya, K. Hirota, G.L. Semenza, and M. Hiraoka Selective killing of hypoxia-inducible factor-1-active cells improves survival in a mouse model of invasive and metastatic pancreatic cancer Clin. Cancer Res. 15 2009 3433 3441
26. E.S. Olson, T. Jiang, T.A. Aguilera, Q.T. Nguyen, L.G. Ellies, M. Scadeng, and R.Y. Tsien Activatable cell penetrating peptides linked to nanoparticles as dual probes for in vivo fluorescence and MR imaging of proteases Proc. Natl. Acad. Sci. U. S. A. 107 2010 4311 4316
27. S. Futaki, M. Niwa, I. Nakase, A. Tadokoro, Y. Zhang, M. Nagaoka, N. Wakako, and Y. Sugiura Arginine carrier peptide bearing Ni(II) chelator to promote cellular uptake of histidine-tagged proteins Bioconjug. Chem. 15 2004 475 481 (Pubitemid 38657852)
28. R.P. Haugland Handbook of Fluorescent Probes and Research Products ninth edition 2002 Molecular Probes Inc
29. D.Y. Furgeson, M.R. Dreher, and A. Chilkoti Structural optimization of a "smart" doxorubicin-polypeptide conjugate for thermally targeted delivery to solid tumors J. Control. Release 110 2006 362 369 (Pubitemid 41827490)
30. K. Sano, T. Temma, T. Azuma, R. Nakai, M. Narazaki, Y. Kuge, and H. Saji A Pre-targeting Strategy for MR Imaging of Functional Molecules Using Dendritic Gd-Based Contrast Agents Mol. Imaging Biol. 13 2011 1196 1203
31. I. Nakase, M. Niwa, T. Takeuchi, K. Sonomura, N. Kawabata, Y. Koike, M. Takehashi, S. Tanaka, K. Ueda, J.C. Simpson, A.T. Jones, Y. Sugiura, and S. Futaki Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement Mol. Ther. 10 2004 1011 1022 (Pubitemid 39625245)
32. 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 (Pubitemid 24198241)
33. R. Bessalle, A. Kapitkovsky, A. Gorea, I. Shalit, and M. Fridkin All-D-magainin: chirality, antimicrobial activity and proteolytic resistance FEBS Lett. 274 1990 151 155 (Pubitemid 20378143)
34. I. Nakase, A. Tadokoro, N. Kawabata, T. Takeuchi, H. Katoh, K. Hiramoto, M. Negishi, M. Nomizu, Y. Sugiura, and S. Futaki Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis Biochemistry 46 2007 492 501 (Pubitemid 46105438)
35. I. Nakase, H. Hirose, G. Tanaka, A. Tadokoro, S. Kobayashi, T. Takeuchi, and S. Futaki Cell-surface accumulation of flock house virus-derived peptide leads to efficient internalization via macropinocytosis Mol. Ther. 17 2009 1868 1876
36. K. Matsuda, H. Maruyama, F. Guo, J. Kleeff, J. Itakura, Y. Matsumoto, A.D. Lander, and M. Korc Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells Cancer Res. 61 2001 5562 5569 (Pubitemid 32694943)
37. J.H. Lee, H. Park, H. Chung, S. Choi, Y. Kim, H. Yoo, T.Y. Kim, H.J. Hann, I. Seong, J. Kim, K.G. Kang, I.O. Han, and E.S. Oh Syndecan-2 regulates the migratory potential of melanoma cells J. Biol. Chem. 284 2009 27167 27175
38. R.D. Sanderson Heparan sulfate proteoglycans in invasion and metastasis Semin. Cell Dev. Biol. 12 2001 89 98
39. I. Vlodavsky, O. Goldshmidt, E. Zcharia, R. Atzmon, Z. Rangini-Guatta, M. Elkin, T. Peretz, and Y. Friedmann Mammalian heparanase: involvement in cancer metastasis, angiogenesis and normal development Semin. Cancer Biol. 12 2002 121 129 (Pubitemid 34680741)
40. R.L. Momparler, M. Karon, S.E. Siegel, and F. Avila Effect of adriamycin on DNA, RNA, and protein synthesis in cell-free systems and intact cells Cancer Res. 36 1976 2891 2895
41. C.A. Frederick, L.D. Williams, G. Ughetto, G.A. van der Marel, J.H. van Boom, A. Rich, and A.H. Wang Structural comparison of anticancer drug-DNA complexes: adriamycin and daunomycin Biochemistry 29 1990 2538 2549 (Pubitemid 20100850)
42. D.A. Gewirtz A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin Biochem. Pharmacol. 57 1999 727 741 (Pubitemid 29094544)
43. M.J. Aiken, V. Suhag, C.A. Garcia, E. Acio, S. Moreau, D.A. Priebat, S.P. Chennupati, and D. Van Nostrand Doxorubicin-induced cardiac toxicity and cardiac rest gated blood pool imaging Clin. Nucl. Med. 34 2009 762 767
44. Y.W. Zhang, J. Shi, Y.J. Li, and L. Wei Cardiomyocyte death in doxorubicin-induced cardiotoxicity Arch. Immunol. Ther. Exp. (Warsz.) 57 2009 435 445
45. T. Kaneko, D. Willner, I. Monkovíc, J.O. Knipe, G.R. Braslawsky, R.S. Greenfield, and D.M. Vyas New hydrazone derivatives of adriamycin and their immunoconjugates-a correlation between acid stability and cytotoxicity Bioconjug. Chem. 2 1991 133 141
46. S. Cai, S. Thati, T.R. Bagby, H.M. Diab, N.M. Davies, M.S. Cohen, and M.L. Forrest Localized doxorubicin chemotherapy with a biopolymeric nanocarrier improves survival and reduces toxicity in xenografts of human breast cancer J. Control. Release 146 2010 212 218
47. T.M. Allen Ligand-targeted therapeutics in anticancer therapy Nat. Rev. Cancer 2 2002 750 763 (Pubitemid 37328910)
48. F. Danhier, O. Feron, and V. Préat To exploit the tumor microenvironment: passive and active tumor targeting of nanocarriers for anti-cancer drug delivery J. Control. Release 148 2010 135 146
49. Y. Matsumura, and H. Maeda A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs Cancer Res. 46 1986 6387 6392 (Pubitemid 17221789)
50. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review J. Control. Release 65 2000 271 284 (Pubitemid 30122932)
51. 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 2008 656 664 (Pubitemid 351431397)