Inhibition of primary and metastatic tumors in mice by E-selectin-targeted polymer-drug conjugates

Journal of Controlled Release

Volumn 217, Issue , 2015, Pages 102-112

  Shamay, Yosi ^a   Raviv, Lior ^a   Golan, Moran ^a   Voronov, Elena ^a   Apte, Ron N ^a   David, Ayelet ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Cancer metastasis; Doxorubicin; E selectin; Nanomedicine; Polymer drug conjugates; Proapoptotic peptide

Indexed keywords

BIOLOGICAL ORGANS; BLOOD VESSELS; DISEASES; ENZYME INHIBITION; INFRARED DEVICES; MAMMALS; MEDICAL NANOTECHNOLOGY; PATHOLOGY; PEPTIDES; TUMORS;

CANCER METASTASIS; CHEMOTHERAPEUTIC DRUGS; DOXORUBICIN; INTRAVENOUS INJECTIONS; LEWIS LUNG CARCINOMATA; POLYMER DRUGS; PROPERTIES OF THE COPOLYMERS; SELECTINS;

DRUG DOSAGE;

DOXORUBICIN; E SELECTIN BINDING PEPTIDE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; N (2 HYDROXYPROPYL)METHACRYLAMIDE COPOLYMER; PEPTIDE DERIVATIVE; PROAPOPTOTIC PEPTIDE; UNCLASSIFIED DRUG; ACRYLAMIDE DERIVATIVE; ANTINEOPLASTIC AGENT; N-(2-HYDROXYPROPYL)METHACRYLAMIDE; PEPTIDE; POLYMER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DRUG CONJUGATION; DRUG EFFICACY; ENDOTHELIUM CELL; FEMALE; LEWIS CARCINOMA; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR REGRESSION; ANIMAL; C57BL MOUSE; CELL LINE; CHEMISTRY; DRUG EFFECTS; EXPERIMENTAL MELANOMA; METABOLISM; NEOPLASMS; PATHOLOGY; TUMOR CELL LINE; TUMOR VOLUME;

ACRYLAMIDES; ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; CELL LINE, TUMOR; DOXORUBICIN; E-SELECTIN; FEMALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEOPLASMS; PEPTIDES; POLYMERS; TUMOR BURDEN;

EID: 84941030901     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.08.029     Document Type: Article

References (48)

1. P. Mehlen, and A. Puisieux Metastasis: a question of life or death Nat. Rev. Cancer 6 2006 449 458
2. I.J. Fidler Critical determinants of metastasis Semin. Cancer Biol. 12 2002 89 96
3. P.S. Steeg Tumor metastasis: mechanistic insights and clinical challenges Nat. Med. 12 2006 895 904
4. O.C. Farokhzad, J. Cheng, B.A. Teply, I. Sherifi, S. Jon, P.W. Kantoff, J.P. Richie, and R. Langer Targeted nanoparticle-aptamer bioconjugates for cancer chemotherapy in vivo Proc. Natl. Acad. Sci. U. S. A. 103 2006 6315 6320
5. Z.R. Lu, P. Kopeckova, and J. Kopecek Polymerizable Fab' antibody fragments for targeting of anticancer drugs Nat. Biotechnol. 17 1999 1101 1104
6. T. Minko, M.L. Patil, M. Zhang, J.J. Khandare, M. Saad, P. Chandna, and O. Taratula LHRH-targeted nanoparticles for cancer therapeutics Methods Mol. Biol. 624 2010 281 294
7. K. Riviere, Z. Huang, K. Jerger, N. Macaraeg, and F.C. Szoka Jr. Antitumor effect of folate-targeted liposomal doxorubicin in KB tumor-bearing mice after intravenous administration J. Drug Target. 19 2010 14 24
8. H. Shmeeda, D. Tzemach, L. Mak, and A. Gabizon Her2-targeted pegylated liposomal doxorubicin: retention of target-specific binding and cytotoxicity after in vivo passage J. Control. Release 136 2009 155 160
9. E. Aydar, C.P. Palmer, and M.B. Djamgoz Sigma receptors and cancer: possible involvement of ion channels Cancer Res. 64 2004 5029 5035
10. F.M. Kievit, Z.R. Stephen, O. Veiseh, H. Arami, T. Wang, V.P. Lai, J.O. Park, R.G. Ellenbogen, M.L. Disis, and M. Zhang Targeting of primary breast cancers and metastases in a transgenic mouse model using rationally designed multifunctional SPIONs ACS Nano 6 2012 2591 2601
11. D.X. Nguyen, P.D. Bos, and J. Massague Metastasis: from dissemination to organ-specific colonization Nat. Rev. Cancer 9 2009 274 284
12. D. Schmid, and C.J. Scott Emerging potential of nanoparticles for the treatment of solid tumors and metastasis Atul Tiwari, Ashutosh Tiwari, Bioengineered Nanomaterials 2013 CRC Press 1 28
13. P. Carmeliet, and R.K. Jain Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases Nat. Rev. Drug Discov. 10 2011 417 427
14. K.M. Laginha, S. Verwoert, G.J. Charrois, and T.M. Allen Determination of doxorubicin levels in whole tumor and tumor nuclei in murine breast cancer tumors Clin. Cancer Res. 11 2005 6944 6949
15. M. Magzoub, S. Jin, and A.S. Verkman Enhanced macromolecule diffusion deep in tumors after enzymatic digestion of extracellular matrix collagen and its associated proteoglycan decorin FASEB J. 22 2008 276 284
16. F. Yuan, M. Leunig, S.K. Huang, D.A. Berk, D. Papahadjopoulos, and R.K. Jain Microvascular permeability and interstitial penetration of sterically stabilized (stealth) liposomes in a human tumor xenograft Cancer Res. 54 1994 3352 3356
17. J. Folkman Angiogenesis and its inhibitors Important Adv. Oncol. 1985 42 62
18. L. Borsi, E. Balza, M. Bestagno, P. Castellani, B. Carnemolla, A. Biro, A. Leprini, J. Sepulveda, O. Burrone, D. Neri, and L. Zardi Selective targeting of tumoral vasculature: comparison of different formats of an antibody (L19) to the ED-B domain of fibronectin Int. J. Cancer 102 2002 75 85
19. T. Lammers, F. Kiessling, W.E. Hennink, and G. Storm Drug targeting to tumors: principles, pitfalls and (pre-) clinical progress J. Control. Release 161 2012 175 187
20. R.A. Brekken, and P.E. Thorpe Vascular endothelial growth factor and vascular targeting of solid tumors Anticancer Res. 21 2001 4221 4229
21. M.M. Burdick, O.J. McCarty, S. Jadhav, and K. Konstantopoulos Cell-cell interactions in inflammation and cancer metastasis IEEE Eng. Med. Biol. Mag. 20 2001 86 91
22. G. Siegel, and M. Malmsten The role of the endothelium in inflammation and tumor metastasis Int. J. Microcirc. Clin. Exp. 17 1997 257 272
23. L.A. Lasky Selectin-carbohydrate interactions and the initiation of the inflammatory response Annu. Rev. Biochem. 64 1995 113 139
24. R.P. McEver Selectin-carbohydrate interactions during inflammation and metastasis Glycoconj. J. 14 1997 585 591
25. V. Bhaskar, D.A. Law, E. Ibsen, D. Breinberg, K.M. Cass, R.B. DuBridge, F. Evangelista, S.M. Henshall, P. Hevezi, J.C. Miller, M. Pong, R. Powers, P. Senter, D. Stockett, R.L. Sutherland, U. von Freeden-Jeffry, D. Willhite, R. Murray, D.E. Afar, and V. Ramakrishnan E-selectin up-regulation allows for targeted drug delivery in prostate cancer Cancer Res. 63 2003 6387 6394
26. S. Kessner, A. Krause, U. Rothe, and G. Bendas Investigation of the cellular uptake of E-Selectin-targeted immunoliposomes by activated human endothelial cells Biochim. Biophys. Acta 1514 2001 177 190
27. R. Kannagi, M. Izawa, T. Koike, K. Miyazaki, and N. Kimura Carbohydrate-mediated cell adhesion in cancer metastasis and angiogenesis Cancer Sci. 95 2004 377 384
28. S.R. Barthel, J.D. Gavino, L. Descheny, and C.J. Dimitroff Targeting selectins and selectin ligands in inflammation and cancer Expert Opin. Ther. Targets 11 2007 1473 1491
29. S. Gout, P.L. Tremblay, and J. Huot Selectins and selectin ligands in extravasation of cancer cells and organ selectivity of metastasis Clin. Exp. Metastasis 25 2008 335 344
30. S.R. Barthel, G.K. Wiese, J. Cho, M.J. Opperman, D.L. Hays, J. Siddiqui, K.J. Pienta, B. Furie, and C.J. Dimitroff Alpha 1,3 fucosyltransferases are master regulators of prostate cancer cell trafficking Proc. Natl. Acad. Sci. U. S. A. 106 2009 19491 19496
31. A.M. Khatib, M. Kontogiannea, L. Fallavollita, B. Jamison, S. Meterissian, and P. Brodt Rapid induction of cytokine and E-selectin expression in the liver in response to metastatic tumor cells Cancer Res. 59 1999 1356 1361
32. A.P. Mann, R.C. Bhavane, A. Somasunderam, B. Liz Montalvo-Ortiz, K.B. Ghaghada, D. Volk, R. Nieves-Alicea, K.S. Suh, M. Ferrari, A. Annapragada, D.G. Gorenstein, and T. Tanaka Thioaptamer conjugated liposomes for tumor vasculature targeting Oncotarget 2 2011 298 304
33. Y. Shamay, D. Paulin, G. Ashkenasy, and A. David Multivalent display of quinic acid based ligands for targeting E-selectin expressing cells J. Med. Chem. 52 2009 5906 5915
34. Y. Shamay, D. Paulin, G. Ashkenasy, and A. David E-selectin binding peptide-polymer-drug conjugates and their selective cytotoxicity against vascular endothelial cells Biomaterials 30 2009 6460 6468
35. C.L. Martens, S.E. Cwirla, R.Y. Lee, E. Whitehorn, E.Y. Chen, A. Bakker, E.L. Martin, C. Wagstrom, P. Gopalan, C.W. Smith, and et al. Peptides which bind to E-selectin and block neutrophil adhesion J. Biol. Chem. 270 1995 21129 21136
36. H. Maeda Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects Bioconjug. Chem. 21 2010 797 802
37. Y. Shamay, L. Adar, G. Ashkenasy, and A. David Light induced drug delivery into cancer cells Biomaterials 32 2011 1377 1386
38. J. Drobník, J. Kopeček, J. Labský, P. Rejmanová, J. Exner, V. Saudek, and J. Kálal Enzymatic cleavage of side chains of synthetic water-soluble polymers Makromol. Chem. 177 1976 2833 2848
39. V. Omelyanenko, P. Kopeckova, C. Gentry, and J. Kopecek Targetable HPMA copolymer-adriamycin conjugates. Recognition, internalization, and subcellular fate J. Control. Release 53 1998 25 37
40. J. Kopecek, and H. Bazilova Poly[N-(2-hydroxypropyl)methacrylamide] I. Radical polymerization and copolymerization Eur. Polym. J. 9 1973 7 14
41. B. Rihova, T. Etrych, M. Pechar, M. Jelinkova, M. Stastny, O. Hovorka, M. Kovar, and K. Ulbrich Doxorubicin bound to a HPMA copolymer carrier through hydrazone bond is effective also in a cancer cell line with a limited content of lysosomes J. Control. Release 74 2001 225 232
42. C. Forster, C. Silwedel, N. Golenhofen, M. Burek, S. Kietz, J. Mankertz, and D. Drenckhahn Occludin as direct target for glucocorticoid-induced improvement of blood-brain barrier properties in a murine in vitro system J. Physiol. 565 2005 475 486
43. I. Kogan-Zviagin, Y. Shamay, A. Nissan, O. Sella-Tavor, M. Golan, and A. David Intra-colonic administration of a polymer-bound NIRF probe for improved colorectal cancer detection during colonoscopy J. Control. Release 192 2014 182 191
44. T. Etrych, V. Subr, J. Strohalm, M. Sirova, B. Rihova, and K. Ulbrich HPMA copolymer-doxorubicin conjugates: the effects of molecular weight and architecture on biodistribution and in vivo activity J. Control. Release 164 2012 346 354
45. T. Nishisho, K. Hata, M. Nakanishi, Y. Morita, G.H. Sun-Wada, Y. Wada, N. Yasui, and T. Yoneda The a3 isoform vacuolar type H(+)-ATPase promotes distant metastasis in the mouse B16 melanoma cells Mol. Cancer Res. 9 2011 845 855
46. M.V. Pimm, A.C. Perkins, J. Strohalm, K. Ulbrich, and R. Duncan Gamma scintigraphy of the biodistribution of 123I-labelled N-(2-hydroxypropyl)methacrylamide copolymer-doxorubicin conjugates in mice with transplanted melanoma and mammary carcinoma J. Drug Target. 3 1996 375 383
47. J.G. Shiah, Y. Sun, C.M. Peterson, R.C. Straight, and J. Kopecek Antitumor activity of N-(2-hydroxypropyl) methacrylamide copolymer-mesochlorine e6 and adriamycin conjugates in combination treatments Clin. Cancer Res. 6 2000 1008 1015
48. S. Kohler, S. Ullrich, U. Richter, and U. Schumacher E-/P-selectins and colon carcinoma metastasis: first in vivo evidence for their crucial role in a clinically relevant model of spontaneous metastasis formation in the lung Br. J. Cancer 102 2010 602 609