Anti-tumor activity of fenretinide complexed with human serum albumin in lung cancer xenograft mouse model

Oncotarget

Volumn 5, Issue 13, 2014, Pages 4811-4820

  Durante, Sandra ^a   Orienti, Isabella ^b   Teti, Gabriella ^a   Salvatore, Viviana ^a   Focaroli, Stefano ^a   Tesei, Anna ^c   Pignatta, Sara ^c   Falconi, Mirella ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c DEPARTMENT OF MEDICAL ONCOLOGY   (Italy)

Author keywords

ACSVL3; Albumin; Caveolin 1; Fenretinide; Lung cancer

Indexed keywords

CAVEOLIN 1; FENRETINIDE; HUMAN SERUM ALBUMIN; LONG CHAIN FATTY ACID COENZYME A LIGASE; UNCLASSIFIED DRUG; VERY LONG CHAIN ACYL COENZYME A SYNTHETASE 3; ANTINEOPLASTIC AGENT; SERUM ALBUMIN;

ANIMAL CELL; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CATALYSIS; CONTROLLED STUDY; DOWN REGULATION; DRUG BIOAVAILABILITY; DRUG SOLUBILITY; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; LUNG CANCER; MOUSE; NICK END LABELING; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR VOLUME; ANIMAL; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LUNG NEOPLASMS; METABOLISM; NUDE MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; TUNEL ASSAY;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CAVEOLIN 1; CELL LINE, TUMOR; COENZYME A LIGASES; FEMALE; FENRETINIDE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; LUNG NEOPLASMS; MICE, NUDE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERUM ALBUMIN; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84905051908     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2038     Document Type: Article

References (55)

1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C and Thun MJ. Cancer statistics, CA Cancer J Clin. 2006; 56: 106-130.
2. Woodward RM, Brown ML, Stewart ST, Cronin KA and Cutler DM. The value of medical interventions for lung cancer in the elderly: results from SEER-CMHSF. Cancer. 2007;110: 2511-2518.
3. Travis WD, Travis LB and Devesa SS. Lung cancer. Cancer 1995; 75:191-202.
4. Okamoto T, Schlegel A, Scherer PE et al. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem. 1998; 273: 5419-5422.
5. Krajewska WM and Maslowska I. Caveolins: structure and function in signal transduction. Cell Mol Biol Lett. 2004; 9: 195-220.
6. Engelman JA, Zhang XL and Lisanti MP. Genes encoding human caveolin-1 and-2 are co-localized to the D7S522 locus (7q31.1), a known fragile site (FRA7G) that is frequently deleted in human cancers. FEBS Lett. 1998; 436: 403-410.
7. Matsuura K, Shiga K, Yokoyama J et al. Loss of heterozygosity of chromosome 9p21 and 7q31 is correlated with high incidence of recurrent tumor in head and neck squamous cell carcinoma. Anticancer Res. 1998; 18: 453-458.
8. Sáinz-Jaspeado M, Martin-Liberal J, Lagares-Tena L, Mateo-Lozano S, Garcia del Muro X, Tirado OM. Caveolin-1 in sarcomas: friend or foe? Oncotarget. 2011; 2(4):305-12.
9. Nassar ZD, Moon H, Duong T, Neo L, Hill MM, Francois M, Patron RG, Parat MO.PTRF/Cavin-1 decreases prostate cancer angiogenesis and lymphangiogenesis. Oncotarget. 2013; 4(10): 1844-55.
10. Shridhar V, Sun QC, Miller OJ et al. Loss of heterozygosity on the long arm of human chromosome 7 in sporadic renal cell carcinomas. Oncogene 1997; 15: 2727-2733.
11. Zenklusen JC, Weitzel JN, Ball HG et al. Allelic loss at 7q31.1 in human primary ovarian carcinomas suggests the existence of a tumor suppressor gene. Oncogene.1995; 11: 359-363.
12. Wiechen K, Sers C, Agoulnik A et al. Down-regulation of caveolin-1, a candidate tumor suppressor gene, in sarcomas. Am J Pathol. 2001; 158: 833-839.
13. Wiechen K, Diatchenko L, Agoulnik A et al. Caveolin-1 is downregulated in human ovarian carcinoma and acts as a candidate tumor suppressor gene. Am J Pathol. 2001; 159: 1635-1643.
14. Bender FC, Reymond MA, Bron C et al. Caveolin-1 levels are down-regulated in human colon tumors, and ectopic expression of caveolin-1 in colon carcinoma cell lines reduces cell tumorigenicity. Cancer Res. 2000; 60: 5870-5878.
15. Fine SW, Lisanti MP, Galbiati F et al. Elevated expression of caveolin-1 in adenocarcinoma of the colon. Am J Clin Pathol. 2001; 115: 719-724.
16. Yoo SH, Park YS, Kim HR et al. Expression of caveolin-1 is associated with poor prognosis of patients with squamous cell carcinoma of the lung. Lung Cancer.2003;42: 195-202.
17. Chunhacha P, Pongrakhananon V, Rojanasakul Y, Chanvorachote P. Caveolin-1 Regulates Mcl-1 Stability and Anoikis in Lung Carcinoma. Cells. Am J Physiol Cell Physiol. 2012; 302: C1284 C1292.
18. Schubert W, Frank PG, Razani B, Park DS, Chow CW, Lisanti MP. Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J Biol Chem. 2001; 276(52):48619-22.
19. Ghitescu, L, Fixman, A, Simonescu, M, and Simonescu, N. J. CellBiol. 1986. 102, 1304-1311.
20. Ghitescu, L., and Bendayan, M. (1992) J. Cell Biol. 117, 745-755.
21. Predescu, D., and Palade, G. E. (1993) Am. J. Physiol. 265, H725-733.
22. Predescu, S. A., Predescu, D. N., and Palade, G. E. (1997) Am. J. Physiol. 272, H937-949.
23. Pei Z, Fraisl P, Shi X, Gabrielson E, Forss-Petter S, Berger J, Watkins PA. Very long-chain acyl-CoA synthetase 3: overexpression and growth dependence in lung cancer. PLoS One. 2013; 8(7):e69392.
24. Chodak GW, Rukstalis D, Kellman HM, Williams M. Phase II study of the retinoid analogue 4-HPR in men with carcinoma of the prostate. J Urol. 1993; 149:257.
25. Veronesi U, De Palo G, Marubini E et al. Randomized trial of fenretinide to prevent second breast malignancy in women with early breast cancer. J Natl Cancer Inst. 1999; 91:1847-1856.
26. Chiesa F, Tradati N, Grigolato R et al. Randomized trial of fenretinide (4-HPR) to prevent recurrences, new localizations and carcinomas in patients operated on for oral leukoplakia: Long-term results. Int J Cancer. 2005; 115:625-629.
27. Formelli F, Barua AB, Olson JA. Bioactivities of N-(4-hydroxyphenyl)-retinamide and retinoyl β-glucuronide. FASEB J. 1996; 10:1014-1024.
28. Ulukaya E, Kurt A, Wood EJ. 4-(N-hydroxyphenyl)retinamide can selectively induce apoptosis in human epidermoid carcinoma cells but not in normal dermal fibroblasts. Cancer Invest. 2001; 19:145-154.
29. Darwiche N, Hatoum A, Dbaibo G et al. N-(4-hydroxyphenyl)retinamide induces growth arrest and apoptosis in HTLV-I-transformed cells. Leukemia. 2004; 18:607-615.
30. Asumendi A, Morales MC, Alvarez A, Arechaga J, Perez-Yarza G. Implication of mitochondria-derived ROS and cardiolipin peroxidation in N-(4-hydroxyphenyl)retinamide-induced apoptosis. Br J Cancer. 2002; 86:1951-1956.
31. Broaddus RR, Xie S, Hsu CJ, Wang J, Zhang S, Zou C. The chemopreventive agents 4-HPR and DFMO inhibit growth and induce apoptosis in uterine leiomyomas. Am J Obstet Gynecol. 2004; 190:686-692.
32. Han HS, Kwon YJ, Park SH et al. Potent effect of 5-HPBR, a butanoate derivative of 4-HPR, on cell growth and apoptosis in cancer cells. Int J Cancer 2004; 109:58-64.
33. 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; 89:1191-1198.
34. 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.
35. Faderl S, Lotan R, Kantarjian HM, Harris D, Van Q, Estrov Z. N-(4-Hydroxylphenyl)retinamide (fenretinide, 4-HPR), a retinoid compound with antileukemic and proapoptotic activity in acute lymphoblastic leukemia (ALL). Leuk Res. 2003; 27:259-266.
36. Chan LN, Zhang S, Shao J, Waikel R, Thompson EA, Chan TS. N-(4-hydroxyphenyl)retinamide induces apoptosis in T lymphoma and T lymphoblastoid leukemia cells. Leuk Lymphoma. 1997; 25:271-280.
37. Gopal AK, Pagel JM, Hedin N, Press OW. Fenretinide enhances rituximab-induced cytotoxicity against B-cell lymphoma xenografts through a caspase-dependent mechanism. Blood. 2003; 103:3516-3520.
38. 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;6:880-90.
39. Falconi M, Focaroli S, Teti G, Salvatore V, Durante S, Nicolini B, Orienti I. Novel PLA microspheres with hydrophilic and bioadhesive surfaces for the controlled delivery of fenretinide. J Microencapsul. 2014; 31(1):41-8.
40. 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):389-98.
41. Orienti I, Zuccari G, Bergamante V, Carosio R, Gotti R, Cilli M, Montaldo PG. Fenretinide-polyvinylalcohol conjugates: new systems allowing fenretinide intravenous administration. Biomacromolecules. 2007 8(10):3258-62.
42. Li HH, Li J, Wasserloos KJ, Wallace C, Sullivan MG, Bauer PM, Stolz DB, Lee JS, Watkins SC, St Croix CM, Pitt BR, Zhang LM. Caveolae-dependent and-independent uptake of albumin in cultured rodent pulmonary endothelial cells. PLoS One. 2013 27;8(11)
43. Hartung G, Stehle G, Sinn H, Wunder A, Schrenk HH, Heeger S, Kränzle M, Edler L, Frei E, Fiebig HH, Heene DL, Maier-Borst W, Queisser W. Phase I trial of methotrexate-albumin in a weekly intravenous bolus regimen in cancer patients. Phase I Study Group of the Association for Medical Oncology of the German Cancer Society. Clin Cancer Res. 1999 4:753-9.
44. Bolling C, Graefe T, Lübbing C, Jankevicius F, Uktveris S, Cesas A, Meyer-Moldenhauer WH, Starkmann H, Weigel M, Burk K, Hanauske AR. Phase II study of MTX-HSA in combination with cisplatin as first line treatment in patients with advanced or metastatic transitional cell carcinoma. Invest New Drugs. 2006; 24(6):521-7.
45. Unger C, Häring B, Medinger M, Drevs J, Steinbild S, Kratz F, Mross K. Phase I and pharmacokinetic study of the (6-maleimidocaproyl)hydrazone derivative of doxorubicin. Clin Cancer Res. 2007; 13(16):4858-66.
46. Kratz F. DOXO-EMCH (INNO-206): the first albumin-binding prodrug of doxorubicin to enter clinical trials. Expert Opin Investig Drugs. 2007; 16(6):855-66.
47. Ibrahim NK, Desai N, Legha S, Soon-Shiong P, Theriault RL, Rivera E, Esmaeli B, Ring SE, Bedikian A, Hortobagyi GN, Ellerhorst JA. Phase I and pharmacokinetic study of ABI-007, a Cremophor-free, protein-stabilized, nanoparticle formulation of paclitaxel. Clin Cancer Res. 2002; 5:1038-44.
48. Ibrahim NK, Samuels B, Page R, Doval D, Patel KM, Rao SC, Nair MK, Bhar P, Desai N, Hortobagyi GN. Multicenter phase II trial of ABI-007, an albumin-bound paclitaxel, in women with metastatic breast cancer. J Clin Oncol. 2005; 23(25):6019-26.
49. Gradishar WJ, Tjulandin S, Davidson N, Shaw H, Desai N, Bhar P, Hawkins M, O'Shaughnessy J. Phase III trial of nanoparticle albumin-bound paclitaxel compared with polyethylated castor oil-based paclitaxel in women with breast cancer. J Clin Oncol. 2005; 23(31):7794-803.
50. Hong WK, Lippman SM, Itri LM, Karp DD, Lee JS, Byers RM, Schantz SP, Kramer AM, Lotan R, Peters LJ, et al. Prevention of second primary tumors with isotretinoin in squamous-cell carcinoma of the head and neck. N Engl J Med 1990; 323: 795-801.
51. Kalemkerian GP, Slusher R, Ramalingam S, Gadgeel S and Mabry M. Growth inhibition and induction of apoptosis by fenretinide in small cell lung cancer cell lines. J Natl Cancer Inst. 1995; 87: 1674-1680.
52. Ulukaya E and Wood EJ. Fenretinide and its relation to cancer. Cancer Treat Rev. 1999; 25: 229-235.
53. Zou CP, Kurie JM, Lotan D, Zou CC, Hong WK and Lotan R. Higher potency of n-(4-hydroxyphenyl)retinamide than alltrans-retinoic acid in induction of apoptosis in non-small cell lung cancer cell lines. Clin Cancer Res. 1998; 4: 1345-1355.
54. Ho CC, Kuo SH, Huang PH, Huang HY, Yang CH, Yang PC. Caveolin-1 expression is significantly associated with drug resistance and poor prognosis in advanced non-small cell lung cancer patients treated with gemcitabine-based chemotherapy. Lung Cancer. 2008 59(1):105-10.
55. Carosio R, Pistoia V, Orienti I, Formelli F, Cavadini E, Mangraviti S, Montaldo PG, Ognio E, Emionite L, Zuccari G. Enhanced anti-neuroblastoma activity of a fenretinide complexed form after intravenous administration. J Pharm Pharmacol. 2012;64(2):228-36. doi:10.1111/j.20427158.2011.01403.x.