Liposomal encapsulation of the natural flavonoid fisetin improves bioavailability and antitumor efficacy

International Journal of Pharmaceutics

Volumn 444, Issue 1-2, 2013, Pages 146-154

  Seguin, Johanne ^a   Brullé, Laura ^a   Boyer, Renaud ^a   Lu, Yen Mei ^a   Ramos Romano, Miriam ^a   Touil, Yasmine S ^a   Scherman, Daniel ^a   Bessodes, Michel ^a   Mignet, Nathalie ^a   Chabot, Guy G ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Anticancer effect; Cyclophosphamide; Fisetin; Lewis lung carcinoma; Liposomes; Pharmacokinetics

Indexed keywords

CYCLOPHOSPHAMIDE; FISETIN; LIPOSOME; MACROGOL 2000;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; AREA UNDER THE CURVE; ARTICLE; CARCINOMA CELL; CONTROLLED STUDY; DISPERSION; DRUG ABSORPTION; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG COATING; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG ELIMINATION; DRUG FORMULATION; DRUG HALF LIFE; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INCUBATION TIME; LEWIS CARCINOMA; LIPOSOMAL DELIVERY; LOW DRUG DOSE; MAXIMUM PLASMA CONCENTRATION; MEAN RESIDENCE TIME; MOUSE; NANOENCAPSULATION; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOLOGICAL AVAILABILITY; CARCINOMA, LEWIS LUNG; CELL LINE, TUMOR; CYCLOPHOSPHAMIDE; FEMALE; FLAVONOIDS; LIPOSOMES; MICE; MICE, INBRED C57BL; TUMOR BURDEN;

EID: 84874311324     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2013.01.050     Document Type: Article

References (47)

1. T.M. Allen, and P.R. Cullis Drug delivery systems: entering the mainstream Science 303 2004 1818 1822
2. Y. Arai, S. Watanabe, M. Kimira, K. Shimoi, R. Mochizuki, and N. Kinae Dietary intakes of flavonols, flavones and isoflavones by Japanese women and the inverse correlation between quercetin intake and plasma LDL cholesterol concentration J. Nutr. 130 2000 2243 2250
3. G. Batist, G. Ramakrishnan, C.S. Rao, A. Chandrasekharan, J. Gutheil, T. Guthrie, P. Shah, A. Khojasteh, M.K. Nair, K. Hoelzer, K. Tkaczuk, Y.C. Park, and L.W. Lee Reduced cardiotoxicity and preserved antitumor efficacy of liposome-encapsulated doxorubicin and cyclophosphamide compared with conventional doxorubicin and cyclophosphamide in a randomized, multicenter trial of metastatic breast cancer J. Clin. Oncol. 19 2001 1444 1454
4. T.A. Bhat, D. Nambiar, A. Pal, R. Agarwal, and R.P. Singh Fisetin inhibits various attributes of angiogenesis in vitro and in vivo-implications for angioprevention Carcinogenesis 33 2012 385 393
5. M. Böhl, S. Tietze, A. Sokoll, S. Madathil, F. Pfennig, J. Apostolakis, K. Fahmy, and H.O. Gutzeit Flavonoids affect actin functions in cytoplasm and nucleus Biophys. J. 93 2007 2767 2780
6. A. Constantinou, R. Mehta, C. Runyan, K. Rao, A. Vaughan, and R. Moon Flavonoids as DNA topoisomerase antagonists and poisons: structure-activity relationships J. Nat. Prod. 58 1995 217 225
7. A. Fahr, H.P. van, J. Kuntsche, and M.L. Leigh Lipophilic drug transfer between liposomal and biological membranes: what does it mean for parenteral and oral drug delivery? J. Liposome Res. 16 2006 281 301
8. T. Fotsis, M.S. Pepper, E. Aktas, S. Breit, S. Rasku, H. Adlercreutz, K. Wahala, R. Montesano, and L. Schweigerer Flavonoids, dietary-derived inhibitors of cell proliferation and in vitro angiogenesis Cancer Res. 57 1997 2916 2921
9. A.A. Gabizon Selective tumor localization and improved therapeutic index of anthracyclines encapsulated in long-circulating liposomes Cancer Res. 52 1992 891 896
10. A.A. Gabizon, O. Lyass, G.J. Berry, and M. Wildgust Cardiac safety of pegylated liposomal doxorubicin (Doxil/Caelyx) demonstrated by endomyocardial biopsy in patients with advanced malignancies Cancer Invest. 22 2004 663 669
11. A. Gabizon, H. Shmeeda, and T. Grenader Pharmacological basis of pegylated liposomal doxorubicin: impact on cancer therapy Eur. J. Pharm. Sci. 45 2012 388 398
12. M. Gibaldi, and D. Perrier Noncompartmental analysis based on statistical moment theory J. Swarbrick, Pharmacokinetics 1982 Marcel Dekker, Inc. New York and Basel 409 417
13. S.C. Gupta, J.H. Kim, S. Prasad, and B.B. Aggarwal Regulation of survival, proliferation, invasion, angiogenesis, and metastasis of tumor cells through modulation of inflammatory pathways by nutraceuticals Cancer Metastasis Rev. 29 2010 405 434
14. M.R. Guzzo, M. Uemi, P.M. Donate, S. Nikolaou, A.E. Machado, and L.T. Okano Study of the complexation of fisetin with cyclodextrins J. Phys. Chem. A 110 2006 10545 10551
15. B.H. Havsteen The biochemistry and medical significance of the flavonoids Pharmacol. Ther. 96 2002 67 202
16. K.Y. Jang, S.J. Jeong, S.H. Kim, J.H. Jung, J.H. Kim, W. Koh, C.Y. Chen, and S.H. Kim Activation of reactive oxygen species/AMP activated protein kinase signaling mediates fisetin-induced apoptosis in multiple myeloma U266 cells Cancer Lett. 319 2012 197 202
17. J. Jankun, S.H. Selman, J. Aniola, and E. Skrzypczak-Jankun Nutraceutical inhibitors of urokinase: potential applications in prostate cancer prevention and treatment Oncol. Rep. 16 2006 341 346
18. N. Khan, M. Asim, F. Afaq, Z.M. Abu, and H. Mukhtar A novel dietary flavonoid fisetin inhibits androgen receptor signaling and tumor growth in athymic nude mice Cancer Res. 68 2008 8555 8563
19. M. Kimira, Y. Arai, K. Shimoi, and S. Watanabe Japanese intake of flavonoids and isoflavonoids from foods J. Epidemiol. 8 1998 168 175
20. R. Langer Drug delivery and targeting Nature 392 1998 5 10
21. S. Lee, Y.J. Kim, S. Kwon, Y. Lee, S.Y. Choi, J. Park, and H.J. Kwon Inhibitory effects of flavonoids on TNF-alpha-induced IL-8 gene expression in HEK 293 cells BMC Rep. 42 2009 265 270
22. J. Li, Y. Cheng, W. Qu, Y. Sun, Z. Wang, H. Wang, and B. Tian Fisetin, a dietary flavonoid, induces cell cycle arrest and apoptosis through activation of p53 and inhibition of NF-kappa B pathways in bladder cancer cells Basic Clin. Pharmacol. Toxicol. 108 2011 84 93
23. M. Lopez-Lazaro Flavonoids as anticancer agents: structure-activity relationship study Curr. Med. Chem. Anticancer Agents 2 2002 691 714
24. H. Lu, D.J. Chang, B. Baratte, L. Meijer, and U. Schulze-Gahmen Crystal structure of a human cyclin-dependent kinase 6 complex with a flavonol inhibitor, fisetin J. Med. Chem. 48 2005 737 743
25. X. Lu, J. Jung, H.J. Cho, D.Y. Lim, H.S. Lee, H.S. Chun, D.Y. Kwon, and J.H. Park Fisetin inhibits the activities of cyclin-dependent kinases leading to cell cycle arrest in HT-29 human colon cancer cells J. Nutr. 135 2005 2884 2890
26. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review J. Control. Release 65 2000 271 284
27. E. Middleton Jr.; C. Kandaswami, and T.C. Theoharides The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer Pharmacol. Rev. 52 2000 673 751
28. N. Mignet, J. Seguin, M. Ramos Romano, L. Brullé, Y.S. Touil, D. Scherman, M. Bessodes, and G.G. Chabot Development of a liposomal formulation of the natural flavonoid fisetin Int. J. Pharm. 423 2012 69 76
29. Y. Nishioka, and H. Yoshino Lymphatic targeting with nanoparticulate system Adv. Drug Deliv. Rev. 47 2001 55 64
30. M.E. O'Brien, N. Wigler, M. Inbar, R. Rosso, E. Grischke, A. Santoro, R. Catane, D.G. Kieback, P. Tomczak, S.P. Ackland, F. Orlandi, L. Mellars, L. Alland, and C. Tendler Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl (CAELYX/Doxil) versus conventional doxorubicin for first-line treatment of metastatic breast cancer Ann. Oncol. 15 2004 440 449
31. A.J. Olaharski, S.T. Mondrala, and D.A. Eastmond Chromosomal malsegregation and micronucleus induction in vitro by the DNA topoisomerase II inhibitor fisetin Mutat. Res. 582 2005 79 86
32. H.H. Park, S. Lee, J.M. Oh, M.S. Lee, K.H. Yoon, B.H. Park, J.W. Kim, H. Song, and S.H. Kim Anti-inflammatory activity of fisetin in human mast cells (HMC-1) Pharmacol. Res. 55 2007 31 37
33. H. Ragelle, S. Crauste-Manciet, J. Seguin, D. Brossard, D. Scherman, P. Arnaud, and G.G. Chabot Nanoemulsion formulation of fisetin improves bioavailability and antitumour activity in mice Int. J. Pharm. 427 2012 452 459
34. J.M. Siehl, E. Thiel, A. Schmittel, G. Hutter, P.M. Deckert, H. Szelenyi, and U. Keilholz Ifosfamide/liposomal daunorubicin is a well tolerated and active first-line chemotherapy regimen in advanced soft tissue sarcoma: results of a phase II study Cancer 104 2005 611 617
35. Y. Suh, F. Afaq, J.J. Johnson, and H. Mukhtar A plant flavonoid fisetin induces apoptosis in colon cancer cells by inhibition of COX2 and Wnt/EGFR/NF-kappa B-signaling pathways Carcinogenesis 30 2009 300 307
36. B. Sung, M.K. Pandey, and B.B. Aggarwal Fisetin, an inhibitor of cyclin-dependent kinase 6, down-regulates nuclear factor-kappaB-regulated cell proliferation, antiapoptotic and metastatic gene products through the suppression of TAK-1 and receptor-interacting protein-regulated IkappaBalpha kinase activation Mol. Pharmacol. 71 2007 1703 1714
37. Y.J. Surh Cancer chemoprevention with dietary phytochemicals Nat. Rev. Cancer 3 2003 768 780
38. D.N. Syed, F. Afaq, N. Maddodi, J.J. Johnson, S. Sarfaraz, A. Ahmad, V. Setaluri, and H. Mukhtar Inhibition of human melanoma cell growth by the dietary flavonoid fisetin is associated with disruption of Wnt/beta-catenin signaling and decreased Mitf levels J. Invest. Dermatol. 131 2011 1291 1299
39. Y.S. Touil, A. Fellous, D. Scherman, and G.G. Chabot Flavonoid-induced morphological modifications of endothelial cells through microtubule stabilization Nutr. Cancer 61 2009 310 321
40. Y.S. Touil, N. Auzeil, F. Boulinguez, H. Saighi, A. Regazzetti, D. Scherman, and G.G. Chabot Fisetin disposition and metabolism in mice: identification of geraldol as an active metabolite Biochem. Pharmacol. 82 2011 1731 1739
41. Y.S. Touil, J. Seguin, D. Scherman, and G.G. Chabot Improved antiangiogenic and antitumour activity of the combination of the natural flavonoid fisetin and cyclophosphamide in Lewis lung carcinoma-bearing mice Cancer Chemother. Pharmacol. 68 2011 445 455
42. J.E. Willson, D.E. Brown, and E.K. Timmens A toxicologic study of dimethyl sulfoxide Toxicol. Appl. Pharmacol. 7 1965 104 112
43. O.L. Woodman, and E.C. Chan Vascular and anti-oxidant actions of flavonols and flavones Clin. Exp. Pharmacol. Physiol. 31 2004 786 790
44. P.M. Yang, H.H. Tseng, C.W. Peng, W.S. Chen, and S.J. Chiu Dietary flavonoid fisetin targets caspase-3-deficient human breast cancer MCF-7 cells by induction of caspase-7-associated apoptosis and inhibition of autophagy Int. J. Oncol. 40 2012 469 478
45. T.H. Ying, S.F. Yang, S.J. Tsai, S.C. Hsieh, Y.C. Huang, D.T. Bau, and Y.H. Hsieh Fisetin induces apoptosis in human cervical cancer HeLa cells through ERK1/2-mediated activation of caspase-8-/caspase-3-dependent pathway Arch. Toxicol. 86 2012 263 273
46. Z.P. Yuan, L.J. Chen, L.Y. Fan, M.H. Tang, G.L. Yang, H.S. Yang, X.B. Du, G.Q. Wang, W.X. Yao, Q.M. Zhao, B. Ye, R. Wang, P. Diao, W. Zhang, H.B. Wu, X. Zhao, and Y.Q. Wei Liposomal quercetin efficiently suppresses growth of solid tumors in murine models Clin. Cancer Res. 12 2006 3193 3199
47. F. Yuan, M. Dellian, D. Fukumura, M. Leunig, D.A. Berk, V.P. Torchilin, and R.K. Jain Vascular permeability in a human tumor xenograft: molecular size dependence and cutoff size Cancer Res. 55 1995 3752 3756