147
Views
11
CrossRef citations to date
0
Altmetric
Original Research

A Novel Nanomicellar Combination of Fenretinide and Lenalidomide Shows Marked Antitumor Activity in a Neuroblastoma Xenograft Model

ORCID Icon, , , ORCID Icon, , , ORCID Icon & ORCID Icon show all
Pages 4305-4319 | Published online: 19 Dec 2019

References

  • Uemura S, Ishida T, Thwin KKM, et al. Dynamics of minimal residual disease in neuroblastoma patients. Front Oncol. 2019;4(9):455. doi:10.3389/fonc.2019.00455
  • Applebaum MA, Vaksman Z, Lee SM, et al. Neuroblastoma survivors are at increased risk for second malignancies: a report from the international neuroblastoma risk group project. Eur J Cancer. 2017;72:177–185. doi:10.1016/j.ejca.2016.11.02228033528
  • Hobbie WL, Moshang Yang EJ, Wu C, Liu Y, Lv J, Sup Shim J. Revisiting non-cancer drugs for cancer therapy. Curr Top Med Chem. 2016;16(19):2144–2155. doi:10.2174/156802661666616021615444126881712
  • Cheung BB. Combination therapies improve the anticancer activities of retinoids in neuroblastoma. World J Clin Oncol. 2015;6(6):212–215. doi:10.5306/wjco.v6.i6.21226677433
  • Garaventa A, Luksch R, Lo Piccolo MS, et al. Phase I trial and pharmacokinetics of fenretinide in children with neuroblastoma. Clin Cancer Res. 2003;9(6):2032–2039.12796365
  • Maurer BJ, Kang MH, Villablanca JG, et al. Phase I trial of fenretinide delivered orally in a novel organized lipid complex in patients with relapsed/refractory neuroblastoma: a report from the new approaches to neuroblastoma therapy (NANT) consortium. Pediatr Blood Cancer. 2013;60:1801–1808. doi:10.1002/pbc.v60.1123813912
  • Moore MM, Stockler M, Lim R, Mok TS, Millward M, Boyer MJ. A Phase II study of fenretinide in patients with hormone refractory prostate cancer: a trial of the cancer therapeutics research group. Cancer Chemother Pharmacol. 2010;66(5):845–850. doi:10.1007/s00280-009-1228-x20082080
  • Schneider BJ, Worden FP, Gadgeel SM, et al. Phase II trial of fenretinide (NSC 374551) in patients with recurrent small cell lung cancer. Invest New Drugs. 2009;27(6):571–578. doi:10.1007/s10637-009-9228-619225720
  • Veronesi U, Mariani L, Decensi A, et al. Fifteen-year results of a randomized Phase III trial of fenretinide to prevent second breast cancer. Ann Oncol. 2006;17(7):1065–1071. doi:10.1093/annonc/mdl04716675486
  • Villablanca JG, London WB, Naranjo A, et al. 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. 2011;17(21):6858–6866. doi:10.1158/1078-0432.CCR-11-099521908574
  • Reynolds CP, Frgala T, Tsao-Wei DD, et al. High plasma levels of fenretinide (4-HPR) were associated with improved outcome in a phase II study of recurrent ovarian cancer: a study by the california cancer consortium. J Clin Oncol. 2007;25:5555.
  • Puduvalli VK, Yung WK, Hess KR; North American Brain Tumor Consortium, et al. Phase II study of fenretinide (NSC 374551) in adults with recurrent malignant gliomas: a North American brain tumor consortium study. J Clin Oncol. 2004;22(21):4282–4289. doi:10.1200/JCO.2004.09.09615514370
  • Vaishampayan U, Heilbrun LK, Parchment RE, et al. Phase II trial of fenretinide in advanced renal carcinoma. Invest New Drugs. 2005;23:179–185. doi:10.1007/s10637-005-5864-715744595
  • Oridate N, Suzuki S, Higuchi M, Mitchell MF, Hong WK, Lotan R. Involvement of reactive oxygen species in N-(4-hydroxyphenyl)retinamide-induced apoptosis in cervical carcinoma cells. J Natl Cancer Inst. 1997;89(16):1191–1198. doi:10.1093/jnci/89.16.11919274913
  • Rahmaniyan M, Curley RW Jr, Obeid LM, Hannun YA, Kraveka JM. Identification of dihydroceramide desaturase as a direct in vitro target for fenretinide. J Biol Chem. 2011;286(28):24754–24764. doi:10.1074/jbc.M111.25077921543327
  • Wang H, Maurer BJ, Liu -Y-Y, et al. N-(4-hydroxyphenyl)retinamide increases dihydroceramide and synergizes with dimethylsphingosine to enhance cancer cell killing. Mol Cancer Ther. 2008;7(9):2967–2976. doi:10.1158/1535-7163.MCT-08-054918790777
  • Xie H, Zhu F, Huang Z, et al. Identification of mammalian target of rapamycin as a direct target of fenretinide both in vitro and in vivo. Carcinogenesis. 2012;33(9):1814–1821. doi:10.1093/carcin/bgs23422798378
  • Maurer B, Metelitsa L, Seeger R, Cabot M, Reynolds C. Increased of ceramide and induction of mixed apoptosis/necrosis by N-(4-hydroxyphenyl)retinamide in neuroblastoma cell lines. J Natl Cancer Inst. 1999;91:1138–1146. doi:10.1093/jnci/91.13.113810393722
  • Bassani B, Bartolini D, Pagani A, et al. Fenretinide (4-HPR) targets Caspase-9, ERK 1/2 and the Wnt3a/beta-catenin pathway in medulloblastoma cells and medulloblastoma cell spheroids. PLoS One. 2016;11(7):e0154111. doi:10.1371/journal.pone.015411127367907
  • Fettig LM, McGinn O, Finlay-Schultz J, LaBarbera DV, Nordeen SK, Sartorius CA. Cross talk between progesterone receptors and retinoic acid receptors in regulation of cytokeratin 5-positive breast cancer cells. Oncogene. 2017;36:6074–6084. doi:10.1038/onc.2017.20428692043
  • Mukherjee N, Reuland SN, Lu Y, et al. Combining a BCL2 inhibitor with the retinoid derivative fenretinide targets melanoma cells including melanoma initiating cells. J Invest Dermatol. 2015;135(3):842–850. doi:10.1038/jid.2014.46425350317
  • Yan W, Du J, Du Y, et al. Fenretinide targets the side population in myeloma cell line NCI-H929 and potentiates the efficacy of antimyeloma with bortezomib and dexamethasone regimen. Leuk Res. 2016;51:32–40. doi:10.1016/j.leukres.2016.10.01027821288
  • Villablanca JG, Krailo MD, Ames MM, Reid JM, Reaman GH, Reynolds CP. 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. 2006;24(21):3423–3430. doi:10.1200/JCO.2005.03.927116849757
  • Jasti BR, LoRusso PM, Parchment RE, Wozniak AJ, Flaherty LE, Shields AF. Phase I clinical trial of fenretinide (NSC374551) in advanced solid tumors. Proc Am Soc Clin Oncol. 2001;20:122a.
  • Cooper JP, Hwang K, Singh H, et al. Fenretinide metabolism in humans and mice: utilizing pharmacological modulation of its metabolic pathway to increase systemic exposure. Br J Pharmacol. 2011;163(6):1263–1275. doi:10.1111/j.1476-5381.2011.01310.x21391977
  • Maurer BJ, Kalous O, Yesair DW, et al. Improved oral delivery of N-(4-hydroxyphenyl)retinamide with a novel LYM-X-SORB organized lipid complex. Clin Cancer Res. 2007;13(10):3079–3086. doi:10.1158/1078-0432.CCR-06-188917505011
  • Kummar S, Gutierrez ME, Maurer BJ, et al. Phase I trial of fenretinide lym-x-sorb oral powder in adults with solid tumors and lymphomas. Anticancer Res. 2011;31(3):961–966.21498721
  • Mohrbacher AM, Yang AS, Groshen S, et al. Phase I study of fenretinide delivered intravenously in patients with relapsed or refractory hematologic malignancies: a california cancer consortium trial. Clin Cancer Res. 2017;23(16):4550–4555. doi:10.1158/1078-0432.CCR-17-023428420721
  • Cooper JP, Reynolds CP, Cho H, Kang MH. Clinical development of fenretinide as an antineoplastic drug: pharmacology perspectives. Exp Biol Med (Maywood). 2017;242(11):1178–1184. doi:10.1177/153537021770695228429653
  • Orienti I, Zuccari G, Falconi M, Teti G, Illingworth NA, Veal GJ, Novel micelles based on amphiphilic branched PEG as carriers for fenretinide. Nanomedicine. 2012;6:880–890. doi:10.1016/j.nano.2011.10.00822094120
  • Orienti I, Zuccari G, Carosio R, Montaldo PG. Improvement of aqueous solubility of fenretinide and other hydrophobic anti-tumor drugs by complexation with amphiphilic dextrins. Drug Deliv. 2009;16(7):389–398. doi:10.1080/1071754090310165519624248
  • Orienti I, Zuccari G, Bergamante V, et al. Amphiphilic poly(vinyl alcohol) derivatives as complexing agents for fenretinide. Biomacromolecules. 2006;7(11):3157–3163. doi:10.1021/bm060482s17096546
  • Pignatta S, Orienti I, Falconi M, et al. Albumin nanocapsules containing fenretinide: pre-clinical evaluation of cytotoxic activity in experimental models of human non-small cell lung cancer. Nanomedicine. 2015;11(2):263–273. doi:10.1016/j.nano.2014.10.00425461293
  • Durante S, Orienti I, Teti G, et al. Anti-tumor activity of fenretinide complexed with human serum albumin in lung cancer xenograft mouse model. Oncotarget. 2014;5(13):4811–4820. doi:10.18632/oncotarget.v5i1325015569
  • Falconi M, Focaroli S, Teti G, et al. Novel PLA microspheres with hydrophilic and bioadhesive surfaces for the controlled delivery of fenretinide. J Microencapsul. 2014;31(1):41–48. doi:10.3109/02652048.2013.80583823862726
  • Di Paolo D, Pastorino F, Zuccari G, et al. Enhanced anti-tumor and anti-angiogenic efficacy of a novel liposomal fenretinide on human neuroblastoma. J Control Release. 2013;170(3):445–451. doi:10.1016/j.jconrel.2013.06.01523792118
  • Orienti I, Francescangeli F, De Angelis ML, et al. A new bioavailable fenretinide formulation with antiproliferative, antimetabolic, and cytotoxic effects on solid tumors. Cell Death Dis. 2019;10(7):529. doi:10.1038/s41419-019-1775-y31332161
  • Orienti I, Salvati V, Sette G, et al. A novel oral micellar fenretinide formulation with enhanced bioavailability and antitumour activity against multiple tumours from cancer stem cells. J Exp Clin Cancer Res. 2019;38(1):373. doi:10.1186/s13046-019-1383-931439019
  • Dredge K, Marriott JB, Macdonald CD, et al. Novel thalidomide analogues display anti-angiogenic activity independently of immunomodulatory effects. Br J Cancer. 2002;87:1166–1172. doi:10.1038/sj.bjc.660060712402158
  • Kotla V, Goel S, Nischal S, et al. Mechanism of action of lenalidomide in hematological malignancies. J Hematol Oncol. 2009;2:36. doi:10.1186/1756-8722-2-3619674465
  • Buesche G, Dieck S, Giagounidis A, et al. Antiangiogenic in vivo effect of lenalidomide (CC-5013) in myelodysplastic syndrome with del (5q) chromosome abnormality and its relation to the course of disease [abstract]. Blood. 2005;106(suppl):. doi:10.1182/blood-2004-04-1622
  • Dredge K, Horsfall R, Robinson SP, et al. Orally administered lenalidomide (CC-5013) is anti-angiogenic in vivo and inhibits endothelial cell migration and Akt phosphorylation in vitro. Microvasc Res. 2005;69(1–2):56–63. doi:10.1016/j.mvr.2005.01.00215797261
  • Lu L, Payvandi F, Wu L, et al. The anti-cancer drug lenalidomide inhibits angiogenesis and metastasis via multiple inhibitory effects on endothelial cell function in normoxic and hypoxic conditions. Microvasc Res. 2009;77(2):78–86. doi:10.1016/j.mvr.2008.08.00318805433
  • Xu Y, Sun J, Sheard MA, et al. Lenalidomide overcomes suppression of human natural killer cell anti-tumor functions by neuroblastoma microenvironment-associated IL-6 and TGFβ1. Cancer Immunol Immunother. 2013;62(10):1637–1648. doi:10.1007/s00262-013-1466-y23982484
  • Roy Choudhury S, Karmakar S, Banik NL, Ray SK. Targeting angiogenesis for controlling neuroblastoma. J Oncol. 2012;15:2012.
  • Pereira S, Egbu R, Jannati G, Al-Jamal WT. Docetaxel-loaded liposomes: the effect of lipid composition and purification on drug encapsulation and in vitro toxicity. Int J Pharm. 2016;514(1):150–159. doi:10.1016/j.ijpharm.2016.06.05727863659
  • Mennucci B, Tomasi J. Continuum solvation models: a new approach to the problem of solute’s charge distribution and cavity boundaries. J Chem Phys. 1997;106:5151–5155. doi:10.1063/1.473558
  • Nguyen F, Alferiev I, Guan P, et al. Enhanced intratumoral delivery of SN38 as a tocopherol oxyacetate prodrug using nanoparticles in a neuroblastoma xenograft model. Clin Cancer Res. 2018;24(11):2585–2593. doi:10.1158/1078-0432.CCR-17-381129514842
  • Torchilin VP. Passive and active drug targeting: drug delivery to tumors as an example. Handb Exp Pharmacol. 2010;197:3–53.
  • Golombek SK, May JN, Theek B, et al. Tumor targeting via EPR: strategies to enhance patient responses. Adv Drug Deliv Rev. 2018;130:17–38. doi:10.1016/j.addr.2018.07.00730009886
  • Date AA, Hanes J, Ensign LM. Nanoparticles for oral delivery: design, evaluation and state-of-the-art. J Control Release. 2016;28(240):504–526. doi:10.1016/j.jconrel.2016.06.016