Enhanced anti-tumor and anti-angiogenic efficacy of a novel liposomal fenretinide on human neuroblastoma

Journal of Controlled Release

Volumn 170, Issue 3, 2013, Pages 445-451

  Di Paolo, Daniela ^a   Pastorino, Fabio ^a   Zuccari, Guendalina ^b   Caffa, Irene ^a,e   Loi, Monica ^a   Marimpietri, Danilo ^a   Brignole, Chiara ^a   Perri, Patrizia ^a   Cilli, Michele ^c   Nico, Beatrice ^d   Ribatti, Domenico ^d   Pistoia, Vito ^a   Ponzoni, Mirco ^a   Pagnan, Gabriella ^a  

^a G GASLINI INSTITUTE   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d UNIVERSITY OF BARI   (Italy)

^e UNIVERSITY OF GENOA   (Italy)

Author keywords

Fenretinide; Nanoliposomes; Neuroblastoma; Targeted therapy; Vascular targeting

Indexed keywords

CELL DEATH; ENDOTHELIAL CELLS; ENZYME INHIBITION; LIPOSOMES; MAMMALS; PATIENT TREATMENT; TARGETED DRUG DELIVERY; TUMORS;

FENRETINIDE; NANOLIPOSOMES; NEUROBLASTOMAS; TARGETED THERAPY; VASCULAR TARGETING;

DIAGNOSIS;

FENRETINIDE; GELATINASE A; GELATINASE B; LIPOSOME; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; DRUG FORMULATION; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; LIPOSOMAL DELIVERY; MOUSE; NANOENCAPSULATION; NEUROBLASTOMA; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL TIME; ZETA POTENTIAL;

FENRETINIDE; NANOLIPOSOMES; NEUROBLASTOMA; TARGETED THERAPY; VASCULAR TARGETING;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; FEMALE; FENRETINIDE; HUMANS; LIPOSOMES; MICE; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; NEUROBLASTOMA;

EID: 84885124167     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.06.015     Document Type: Article

References (43)

1. J.M. Maris, Recent advances in neuroblastoma, N. Engl. J. Med. 362 (2010) 2202-2211.
2. S. Mueller, K.K. Matthay, Neuroblastoma: biology and staging, Curr. Oncol. Rep. 11 (2009) 431-438.
3. S. Modak, N.K. Cheung, Neuroblastoma: therapeutic strategies for a clinical enigma, Cancer Treat. Rev. 36 (2010) 307-317.
4. K.K. Matthay, C.P. Reynolds, R.C. Seeger, H. Shimada, E.S. Adkins, D. Haas-Kogan, R.B. Gerbing, W.B. London, J.G. Villablanca, Long-term results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13-cis-retinoic acid: a children's oncology group study, J. Clin. Oncol. 27 (2009) 1007-1013.
5. M. Ponzoni, P. Bocca, V. Chiesa, A. Decensi, V. Pistoia, L. Raffaghello, C. Rozzo, P.G. Montaldo, Differential effects of N-(4-hydroxyphenyl)retinamide and retinoic acid on neuroblastoma cells: apoptosis versus differentiation, Cancer Res. 55 (1995) 853-861.
6. P.E. Lovat, M. Ranalli, M. Annichiarrico-Petruzzelli, F. Bernassola, M. Piacentini, A.J. Malcolm, A.D. Pearson, G. Melino, C.P. Redfern, Effector mechanisms of fenretinide-induced apoptosis in neuroblastoma, Exp. Cell Res. 260 (2000) 50-60.
7. J.G. Villablanca, M.D. Krailo, M.M. Ames, J.M. Reid, G.H. Reaman, C.P. Reynolds, Phase I trial of oral fenretinide in children with high-risk solid tumors: a report from the Children's Oncology Group (CCG 09709), J. Clin. Oncol. 24 (2006) 3423-3430. (Pubitemid 46638899)
8. A. Garaventa, R. Luksch, M.S. Lo Piccolo E. Cavadini, P.G. Montaldo, M.R. Pizzitola, L. Boni, M. Ponzoni, A. Decensi, B. De Bernardi, F.F. Bellani, F. Formelli, Phase I trial and pharmacokinetics of fenretinide in children with neuroblastoma, Clin. Cancer Res. 9 (2003) 2032-2039. (Pubitemid 36687622)
9. J.G. Villablanca, W.B. London, A. Naranjo, P. McGrady, M.M. Ames, J.M. Reid, R.M. McGovern, S.A. Buhrow, H. Jackson, E. Stranzinger, B.J. Kitchen, P.M. Sondel, M.T. Parisi, B. Shulkin, G.A. Yanik, S.L. Cohn, C.P. Reynolds, Phase II study of oral capsular 4-hydroxyphenylretinamide (4-HPR/fenretinide) in pediatric patients with refractory or recurrent neuroblastoma: a report from the Children's Oncology Group, Clin. Cancer Res. 17 (2011) 6858-6866.
10. L. Raffaghello, G. Pagnan, F. Pastorino, E. Cosimo, C. Brignole, D. Marimpietri, P.G. Montaldo, C. Gambini, T.M. Allen, E. Bogenmann, M. Ponzoni, In vitro and in vivo antitumor activity of liposomal Fenretinide targeted to human neuroblastoma, Int J. Cancer 104 (2003) 559-567. (Pubitemid 36337255)
11. B.J. Maurer, O. Kalous, D.W. Yesair, X. Wu, J. Janeba, V. Maldonado, V. Khankaldyyan, T. Frgala, B.C. Sun, R.T. McKee, S.W. Burgess, WA Shaw, C.P. Reynolds, Improved oral delivery of N-(4-hydroxyphenyl)retinamide with a novel LYM-X-SORB organized lipid complex, Clin. Cancer Res. 13 (2007) 3079-3086. (Pubitemid 46849585)
12. A.M.M.H. Kang, J.G. Villablanca, J.M. Maris, M.M. Ames, J.M. Reid, K.K. Matthay, C.P. Reynolds, B.J. Maurer, Fenretinide (4-HPR) orally formulated in Lym-X-Sorb(LXS) lipid matrix or as an intravenous emulsion increased 4-HPR systemic exposure in patients with recurrent or resistant neuroblastoma, A New Approaches to neuroblastoma Therapy (NANT) Consortium Trial, Proc ANR, 2010, p. 123.
13. I. Orienti, G. Zuccari, M. Falconi, G. Teti, N.A. Illingworth, G.J. Veal, Novel micelles based on amphiphilic branched PEG as carriers for fenretinide, Nanomedicine 8 (2012) 880-890.
14. D. Ribatti, M. Ponzoni, Antiangiogenic strategies in neuroblastoma, Cancer Treat. Rev. 31 (2005) 27-34. (Pubitemid 40246988)
15. G. Pagnan, P.G. Montaldo, F. Pastorino, L. Raffaghello, M. Kirchmeier, T.M. Allen, M. Ponzoni, GD2-mediated melanoma cell targeting and cytotoxicity of liposome-entrapped fenretinide, Int. J. Cancer 81 (1999) 268-274. (Pubitemid 29144758)
16. D. Neri, R. Bicknell, Tumour vascular targeting, Nat. Rev. Cancer 5 (2005) 436-446. (Pubitemid 40791486)
17. P. Di Matteo, G.L. Arrigoni, L. Alberici, A. Corti, C. Gallo-Stampino, C. Traversari, C. Doglioni, G.P. Rizzardi, Enhanced expression of CD13 in vessels of inflammatory and neoplastic tissues, J. Histochem. Cytochem. 59 (1) (2011) 47-59.
18. A. Corti, F. Pastorino, F. Curnis, W. Arap, M. Ponzoni, R. Pasqualini, Targeted drug delivery and penetration into solid tumors, Med. Res. Rev. 32 (2012) 1078-1091.
19. 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)
20. Y. Chen, J.J. Wu, L. Huang, Nanoparticles targeted with NGR motif deliver c-myc siRNA and doxorubicin for anticancer therapy, Mol. Ther. 18 (2010) 828-834.
21. 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.
22. G. Pagnan, D. Di Paolo, R. Carosio, F. Pastorino, D. Marimpietri, C. Brignole, A. Pezzolo, M. Loi, L.J. Galietta, F. Piccardi, M. Cilli, B. Nico, D. Ribatti, V. Pistoia, M. Ponzoni, The combined therapeutic effects of bortezomib and fenretinide on neu-roblastoma cells involve endoplasmic reticulum stress response, Clin. Cancer Res. 15 (2009) 1199-1209.
23. C. Brignole, D. Marimpietri, D. Di Paolo, P. Perri, F. Morandi, F. Pastorino, A. Zorzoli, G. Pagnan, M. Loi, I. Caffa, G. Erminio, R. Haupt, C. Gambini, V. Pistoia, M. Ponzoni, Therapeutic targeting of TLR9 inhibits cell growth and induces apoptosis in neuroblastoma, Cancer Res. 70 (2010) 9816-9826.
24. G. Pagnan, D.D. Stuart, F. Pastorino, L. Raffaghello, P.G. Montaldo, T.M. Allen, B. Calabretta, M. Ponzoni, Delivery of c-myb antisense oligodeoxynucleotides to human neuroblastoma cells via disialoganglioside GD(2)-targeted immunoliposomes: antitumor effects, J. Natl. Cancer Inst. 92 (2000) 253-261. (Pubitemid 30099785)
25. N. Takahashi, K. Tamagawa, K. Shimizu, T. Fukui, Y. Maitani, Effects on M5076-hepatic metastasis of retinoic acid and N-(4-hydroxyphenyl) retinamide, fenretinide entrapped in SG-liposomes, Biol. Pharm. Bull. 26 (2003) 1060-1063. (Pubitemid 41685443)
26. 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)
27. D.D. Stuart, T.M. Allen, A new liposomal formulation for antisense oligodeoxynucleotides with small size, high incorporation efficiency and good stability, Biochim. Biophys. Acta 1463 (2000) 219-229. (Pubitemid 30081782)
28. 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)
29. D. Di Paolo, M. Loi, F. Pastorino, C. Brignole, D. Marimpietri, P. Becherini, I. Caffa, A. Zorzoli, R. Longhi, C. Gagliani, C. Tacchetti, A. Corti, T.M. Allen, M. Ponzoni, G. Pagnan, Liposome-mediated therapy of neuroblastoma, Methods Enzymol. 465 (2009) 225-249.
30. A. Corti, M. Ponzoni, Tumor vascular targeting with tumor necrosis factor alpha and chemotherapeutic drugs, Ann. N. Y. Acad. Sci. 1028 (2004) 104-112. (Pubitemid 40361814)
31. 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)
32. D. Di Paolo, C. Brignole, F. Pastorino, R. Carosio, A. Zorzoli, M. Rossi, M. Loi, G. Pagnan, L. Emionite, M. Cilli, S. Bruno, R. Chiarle, T.M. Allen, M. Ponzoni, P. Perri, Neuroblastoma-targeted nanoparticles entrapping siRNA specifically knockdown ALK, Mol. Ther. 19 (2011) 1131-1140.
33. I. Sogno, R. Vene, N. Ferrari, A. De Censi, A. Imperatori, D.M. Noonan, F. Tosetti, A. Albini, Angioprevention with fenretinide: targeting angiogenesis in prevention and therapeutic strategies, Crit. Rev. Oncol. Hematol. 75 (2010) 2-14.
34. J. George, N.L. Banik, S.K. Ray, Survivin knockdown and concurrent 4-HPR treatment controlled human glioblastoma in vitro and in vivo, Neuro Oncol. 12 (2010) 1088-1101.
35. J.L. Armstrong, G.J. Veal, C.P. Redfern, P.E. Lovat, Role of Noxa in p53-independent fenretinide-induced apoptosis of neuroectodermal tumours, Apoptosis 12 (2007) 613-622.
36. D. Belotti, C. Calcagno, A. Garofalo, D. Caronia, E. Riccardi, R. Giavazzi, G. Taraboletti, Vascular endothelial growth factor stimulates organ-specific host matrix metalloproteinase-9 expression and ovarian cancer invasion, Mol. Cancer Res. 6 (2008) 525-534. (Pubitemid 351521834)
37. J. Becker, H. Pavlakovic, F. Ludewig, F. Wilting, H.A. Weich, R. Albuquerque, J. Ambati, J. Wilting, Neuroblastoma progression correlates with downregulation of the lymphangiogenesis inhibitor sVEGFR-2, Clin. Cancer Res. 16 (2010) 1431-1441.
38. B. Gorantla, P. Bhoopathi, C. Chetty, V.R. Gogineni, G.S. Sailaja, C.S. Gondi, J.S. Rao, Notch signaling regulates tumor-induced angiogenesis in SPARC-overexpressed neuroblastoma, Angiogenesis 16 (2013) 85-100.
39. S. Roy Choudhury, S. Karmakar, N.L. Banik, S.K. Ray, Targeting angiogenesis for controlling neuroblastoma, J. Oncol. 2012 (2012) 782020.
40. D. Bourboulia, W.G. Stetler-Stevenson, Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): positive and negative regulators in tumor cell adhesion, Semin. Cancer Biol. 20 (2010) 161-168.
41. S. Jodele, L. Blavier, J.M. Yoon, Y.A. DeClerck, Modifying the soil to affect the seed: role of stromal-derived matrix metalloproteinases in cancer progression, Cancer Metastasis Rev. 25 (2006) 35-43. (Pubitemid 43723980)
42. D. Ribatti, Anti-angiogenesis in neuroblastoma, Crit. Rev. Oncol. Hematol. 86 (3) (2013) 212-221.
43. S.J. Conley, E. Gheordunescu, P. Kakarala, B. Newman, H. Korkaya, A.N. Heath, S.G. Clouthier, M.S. Wicha, Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia, Proc. Natl. Acad. Sci. U. S. A. 109 (2012) 2784-2789.