Novel phage display-derived neuroblastoma-targeting peptides potentiate the effect of drug nanocarriers in preclinical settings

Journal of Controlled Release

Volumn 170, Issue 2, 2013, Pages 233-241

  Loi, Monica ^a   Di Paolo, Daniela ^a   Soster, Marco ^b   Brignole, Chiara ^a   Bartolini, Alice ^b   Emionite, Laura ^c   Sun, Jessica ^d   Becherini, Pamela ^a   Curnis, Flavio ^e   Petretto, Andrea ^a   Sani, Monica ^f   Gori, Alessandro ^f   Milanese, Marco ^g   Gambini, Claudio ^a   Longhi, Renato ^f   Cilli, Michele ^c   Allen, Theresa M ^h   Bussolino, Federico ^b   Arap, Wadih ^d   Pasqualini, Renata ^d   Corti, Angelo ^e   Ponzoni, Mirco ^a   Marchiò, Serena ^b   Pastorino, Fabio ^a   more..

^a G GASLINI INSTITUTE   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d UNIVERSITY OF TEXAS   (United States)

^e SAN RAFFAELE HOSPITAL   (Italy)

^f CNR   (Italy)

^g UNIVERSITY OF GENOA   (Italy)

^h UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Liposomes; Nanocarriers; Neuroblastoma; Peptides; Phage display screening; Targeted therapy

Indexed keywords

BINS; CELL CULTURE; CLONE CELLS; CLONING; LIPOSOMES; MAMMALS; PEPTIDES; POLYPEPTIDES; TUMORS;

CLINICAL DEVELOPMENT; HIGH-RISK NEUROBLASTOMA; MOLECULAR TARGETING; NANO-CARRIERS; NEUROBLASTOMAS; PHAGE DISPLAY SCREENING; TARGETED THERAPY; TARGETING PEPTIDES;

DIAGNOSIS;

ANTINEOPLASTIC AGENT; DOXORUBICIN; LIGAND; LIPOSOME; NANOCARRIER; NEUROBLASTOMA TARGETING PEPTIDE; UNCLASSIFIED DRUG; NANOPARTICLE; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER PATIENT; CANCER STAGING; CANCER SURVIVAL; CONTROLLED STUDY; DRUG BINDING; DRUG CLEARANCE; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG SCREENING; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MOLECULAR CLONING; MOLECULARLY TARGETED THERAPY; MOUSE; NEUROBLASTOMA; NONHUMAN; PHAGE DISPLAY; PLASMA CLEARANCE; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN BINDING; TUMOR BIOPSY; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; TUMOR VOLUME; ANIMAL; CELL CULTURE; CELL SURFACE DISPLAY; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; CELL LINE, TUMOR; CELL SURFACE DISPLAY TECHNIQUES; CELL SURVIVAL; CELLS, CULTURED; DOXORUBICIN; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIPOSOMES; MICE; MICE, NUDE; NANOPARTICLES; NEUROBLASTOMA; PEPTIDES; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84879491627     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.04.029     Document Type: Article

References (41)

1. J.M. Maris, Recent advances in neuroblastoma, N. Engl. J. Med. 362 (2010) 2202-2211.
2. P.E. Zage, C.U. Louis, S.L. Cohn, New aspects of neuroblastoma treatment: ASPHO 2011 symposium review, Pediatr. Blood Cancer 58 (2011) 1099-1105.
3. K.K. Matthay, R.E. George, A.L. Yu, Promising therapeutic targets in neuroblasto-ma, Clin. Cancer Res. 18 (2012) 2740-2753.
4. E.L. Carpenter, Y.P. Mosse, Targeting ALK in neuroblastoma-preclinical and clinical advancements, Nat. Rev. Clin. Oncol. 9 (2012) 391-399.
5. H. Carol, I. Boehm, C.P. Reynolds, M.H. Kang, J.M. Maris, C.L. Morton, R. Gorlick, E.A. Kolb, S.T. Keir, J. Wu, A.E. Wozniak, Y. Yang, M. Manfredi, J. Ecsedy, J. Wang, G. Neale, P.J. Houghton, M.A. Smith, R.B. Lock, Efficacy and pharmacokinetic/ pharmacodynamic evaluation of the Aurora kinase A inhibitor MLN8237 against preclinical models of pediatric cancer, Cancer Chemother. Pharmacol. 68 (2011) 1291-1304.
6. W.L. Furman, L.M. McGregor, M.B. McCarville, M. Onciu, A.M. Davidoff, S. Kovach, D. Hawkins, V. McPherson, P.J. Houghton, C.A. Billups, J. Wu, C.F. Stewart, V.M. Santana, A single-arm pilot phase II study of gefitinib and irinotecan in children with newly diagnosed high-risk neuroblastoma, Invest. New Drugs (2011).
7. L.M. Wagner, M.K. Danks, New therapeutic targets for the treatment of high-risk neuroblastoma, J. Cell. Biochem. 107 (2009) 46-57.
8. C.L. Morton, J.M. Maris, S.T. Keir, R. Gorlick, E.A. Kolb, C.A. Billups, J. Wu, M.A. Smith, P.J. Houghton, Combination testing of cediranib (AZD2171) against childhood cancer models by the pediatric preclinical testing program, Pediatr. Blood Cancer 58 (2011) 566-571.
9. C.S. Verissimo, J.J. Molenaar, C.P. Fitzsimons, E. Vreugdenhil, Neuroblastoma therapy: what is in the pipeline? Endocr. Relat. Cancer 18 (2011) R213-R231.
10. A. Koshkaryev, R. Sawant, M. Deshpande, V. Torchilin, Immunoconjugates and long circulating systems: origins, current state of the art and future directions, Adv. Drug Deliv. Rev. (2012).
11. T.M. Allen, P.R. Cullis, Liposomal drug delivery systems: from concept to clinical applications, Adv. Drug Deliv. Rev. (2012).
12. S. Marchio, W. Arap, R. Pasqualini, Targeting the extracellular signature of meta-static colorectal cancers, Expert Opin. Ther. Targets 13 (2009) 363-379.
13. A. Corti, F. Pastorino, F. Curnis, W. Arap, M. Ponzoni, R. Pasqualini, Targeted drug delivery and penetration into solid tumors, Med. Res. Rev. (2011).
14. R. Pasqualini, E. Koivunen, R. Kain, J. Lahdenranta, M. Sakamoto, A. Stryhn, R.A. Ashmun, L.H. Shapiro, W. Arap, E. Ruoslahti, Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis, Cancer Res. 60 (2000) 722-727. (Pubitemid 30094573)
15. S. Marchio, J. Lahdenranta, R.O. Schlingemann, D. Valdembri, P. Wesseling, M.A. Arap, A. Hajitou, M.G. Ozawa, M. Trepel, R.J. Giordano, D.M. Nanus, H.B. Dijkman, E. Oosterwijk, R.L. Sidman, M.D. Cooper, F. Bussolino, R. Pasqualini, W. Arap, Aminopeptidase A is a functional target in angiogenic blood vessels, Cancer Cell 5 (2004) 151-162. (Pubitemid 38283801)
16. F. Pastorino, C. Brignole, D. Marimpietri, M. Cilli, C. Gambini, D. Ribatti, R. Longhi, T.M. Allen, A. Corti, M. Ponzoni, Vascular damage and anti-angiogenic effects of tumor vessel-targeted liposomal chemotherapy, Cancer Res. 63 (2003) 7400-7409. (Pubitemid 37413482)
17. F. Pastorino, D. Di Paolo, F. Piccardi, B. Nico, D. Ribatti, A. Daga, G. Baio, C.E. Neumaier, C. Brignole, M. Loi, D. Marimpietri, G. Pagnan, M. Cilli, E.A. Lepekhin, S.V. Garde, R. Longhi, A. Corti, T.M. Allen, J.J. Wu, M. Ponzoni, Enhanced antitumor efficacy of clinical-grade vasculature-targeted liposomal doxorubicin, Clin. Cancer Res. 14 (2008) 7320-7329.
18. M. Loi, S. Marchio, P. Becherini, D. Di Paolo, M. Soster, F. Curnis, C. Brignole, G. Pagnan, P. Perri, I. Caffa, R. Longhi, B. Nico, F. Bussolino, C. Gambini, D. Ribatti, M. Cilli, W. Arap, R. Pasqualini, T.M. Allen, A. Corti, M. Ponzoni, F. Pastorino, Combined targeting of perivascular and endothelial tumor cells enhances anti-tumor efficacy of liposomal chemotherapy in neuroblastoma, J. Control. Release 145 (2010) 66-73.
19. F. Pastorino, C. Brignole, D. Marimpietri, P. Sapra, E.H. Moase, T.M. Allen, M. Ponzoni, Doxorubicin-loaded Fab' fragments of anti-disialoganglioside immunoliposomes selectively inhibit the growth and dissemination of human neuroblastoma in nude mice, Cancer Res. 63 (2003) 86-92. (Pubitemid 36070424)
20. D. Marimpietri, C. Brignole, B. Nico, F. Pastorino, A. Pezzolo, F. Piccardi, M. Cilli, D. Di Paolo, G. Pagnan, L. Longo, P. Perri, D. Ribatti, M. Ponzoni, Combined therapeutic effects of vinblastine and rapamycin on human neuroblastoma growth, apo-ptosis, and angiogenesis, Clin. Cancer Res. 13 (2007) 3977-3988. (Pubitemid 47037606)
21. J.K. Scott, G.P. Smith, Searching for peptide ligands with an epitope library, Science 249 (1990) 386-390.
22. G.P. Smith, J.K. Scott, Libraries of peptides and proteins displayed on filamentous phage, Methods Enzymol. 217 (1993) 228-257.
23. F. Pastorino, C. Brignole, D. Di Paolo, B. Nico, A. Pezzolo, D. Marimpietri, G. Pagnan, F. Piccardi, M. Cilli, R. Longhi, D. Ribatti, A. Corti, T.M. Allen, M. Ponzoni, Targeting lipo-somal chemotherapy via both tumor cell-specific and tumor vasculature-specific ligands potentiates therapeutic efficacy, Cancer Res. 66 (2006) 10073-10082. (Pubitemid 44672061)
24. C. Brignole, D. Marimpietri, F. Pastorino, B. Nico, D. Di Paolo, M. Cioni, F. Piccardi, M. Cilli, A. Pezzolo, M.V. Corrias, V. Pistoia, D. Ribatti, G. Pagnan, M. Ponzoni, Effect of bortezomib on human neuroblastoma cell growth, apoptosis, and angiogenesis, J. Natl. Cancer Inst. 98 (2006) 1142-1157. (Pubitemid 44288789)
25. A. Gabizon, R. Catane, B. Uziely, B. Kaufman, T. Safra, R. Cohen, F. Martin, A. Huang, Y. Barenholz, Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes, Cancer Res. 54 (1994) 987-992. (Pubitemid 24085451)
26. T. Ishida, K. Atobe, X. Wang, H. Kiwada, Accelerated blood clearance of PEGylated liposomes upon repeated injections: effect of doxorubicin- encapsulation and high-dose first injection, J. Control. Release 115 (2006) 251-258. (Pubitemid 44634849)
27. R.K. Jain, T. Stylianopoulos, Delivering nanomedicine to solid tumors, Nat. Rev. Clin. Oncol. 7 (2010) 653-664.
28. E. Ruoslahti, S.N. Bhatia, M.J. Sailor, Targeting of drugs and nanoparticles to tumors, J. Cell Biol. 188 (2010) 759-768.
29. S.M. Weis, D.A. Cheresh, Tumor angiogenesis: molecular pathways and therapeutic targets, Nat. Med. 17 (2011) 1359-1370.
30. Chapter 4. M. Trepel, R. Pasqualini, W. Arap, Screening phage-display peptide libraries for vascular targeted peptides, Methods Enzymol. 445 (2008) 83-106.
31. K. Karjalainen, D.E. Jaalouk, C.E. Bueso-Ramos, A.J. Zurita, A. Kuniyasu, B.L. Eckhardt, F.C. Marini, B. Lichtiger, S. O'Brien, H.M. Kantarjian, J.E. Cortes, E. Koivunen, W. Arap, R. Pasqualini, Targeting neuropilin-1 in human leukemia and lymphoma, Blood 117 (2011) 920-927.
32. K.N. Sugahara, T. Teesalu, P.P. Karmali, V.R. Kotamraju, L. Agemy, D.R. Greenwald, E. Ruoslahti, Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs, Science 328 (2010) 1031-1035.
33. T.M. Hong, Y.L. Chen, Y.Y. Wu, A. Yuan, Y.C. Chao, Y.C. Chung, M.H. Wu, S.C. Yang, S.H. Pan, J.Y. Shih, W.K. Chan, P.C. Yang, Targeting neuropilin 1 as an antitumor strategy in lung cancer, Clin. Cancer Res. 13 (2007) 4759-4768. (Pubitemid 47294782)
34. M. Fakhari, D. Pullirsch, D. Abraham, K. Paya, R. Hofbauer, P. Holzfeind, M. Hofmann, S. Aharinejad, Selective upregulation of vascular endothelial growth factor receptors neuropilin-1 and -2 in human neuroblastoma, Cancer 94 (2002) 258-263. (Pubitemid 34049067)
35. E. Kluza, D.W. van der Schaft, P.A. Hautvast, W.J. Mulder, K.H. Mayo, A.W. Griffioen, G.J. Strijkers, K. Nicolay, Synergistic targeting of alphavbeta3 integrin and galectin-1 with heteromultivalent paramagnetic liposomes for combined MR imaging and treatment of angiogenesis, Nano Lett. 10 (2010) 52-58.
36. U. Prabhakar, H. Maeda, R.K. Jain, E.M. Sevick-Muraca, W. Zamboni, O.C. Farokhzad, S.T. Barry, A. Gabizon, P. Grodzinski, D.C. Blakey, Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology, Cancer Res. 73 (2013) 2412-2417.
37. F. Pastorino, D. Di Paolo, M. Loi, P. Becherini, I. Caffa, A. Zorzoli, D. Marimpietri, R. Carosio, P. Perri, P.G. Montaldo, C. Brignole, G. Pagnan, D. Ribatti, T.M. Allen, M. Ponzoni, Recent advances in targeted anti-vasculature therapy: the neuroblasto-ma model, Curr. Drug Targets 10 (2009) 1021-1027.
38. E. Blanco, T. Sangai, A. Hsiao, S. Ferrati, L. Bai, X. Liu, F. Meric-Bernstam, M. Ferrari, Multistage delivery of chemotherapeutic nanoparticles for breast cancer treatment, Cancer Lett. (2012).
39. E. Blanco, A. Hsiao, G.U. Ruiz-Esparza, M.G. Landry, F. Meric-Bernstam, M. Ferrari, Molecular-targeted nanotherapies in cancer: enabling treatment specificity, Mol. Oncol. 5 (2011) 492-503.
40. B. Godin, E. Tasciotti, X. Liu, R.E. Serda, M. Ferrari, Multistage nanovectors: from concept to novel imaging contrast agents and therapeutics, Acc. Chem. Res. 44 (2011) 979-989.
41. V. Moura, M. Lacerda, P. Figueiredo, M.L. Corvo, M.E. Cruz, R. Soares, M.C. de Lima, S. Simoes, J.N. Moreira, Targeted and intracellular triggered delivery of therapeutics to cancer cells and the tumor microenvironment: impact on the treatment of breast cancer, Breast Cancer Res. Treat. 133 (2012) 61-73.