Nanoparticles consisting of tocopheryl succinate are a novel drug-delivery system with multifaceted antitumor activity

Biological and Pharmaceutical Bulletin

Volumn 37, Issue 2, 2014, Pages 196-200

  Hama, Susumu ^a   Kogure, Kentaro ^a  

^a KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Combination therapy; Multifaceted antitumor agent; Nanoparticle; Tocopheryl succinate

Indexed keywords

ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; DRUG DELIVERY SYSTEMS; HUMANS; NANOPARTICLES; NEOPLASMS; SUCCINIC ACID; TOCOPHEROLS;

EID: 84893224094     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b13-00848     Document Type: Review

References (45)

1. De Sousa E Melo F, Vermeulen L, Fessler E, Medema JP. Cancer heterogeneity - a multifaceted view. EMBO Rep., 14, 686-695 (2013).
2. Saunders NA, Simpson F, Thompson EW, Hill MM, Endo-Munoz L, Leggatt G, Minchin RF, Guminski A. Role of intratumoural heterogeneity in cancer drug resistance: molecular and clinical perspectives. EMBO Mol. Med., 4, 675-684 (2012).
3. Horiike A, Kudo K, Miyauchi E, Ohyanagi F, Kasahara K, Horai T, Nishio M. Phase I study of irinotecan and gefitinib in patients with gefitinib treatment failure for non-small cell lung cancer. Br. J. Cancer, 105, 1131-1136 (2011).
4. Takahashi T, Saikawa Y, Takaishi H, Takeuchi H, Wada N, Oyama T, Fukuda K, Fukada J, Kawaguchi O, Shigematsu N, Kitagawa Y. Phase I study of neoadjuvant chemoradiotherapy consisting of S-1 and cisplatin for patients with resectable advanced gastric cancer (KOGC-01). Anticancer Res., 31, 3079-3083 (2011).
5. Sun TM, Du JZ, Yao YD, Mao CQ, Dou S, Huang SY, Zhang PZ, Leong KW, Song EW, Wang J. Simultaneous delivery of siRNA and paclitaxel via a "two-in-one" micelleplex promotes synergistic tumor suppression. ACS Nano, 5, 1483-1494 (2011).
6. Kolishetti N, Dhar S, Valencia PM, Lin LQ, Karnik R, Lippard SJ, Langer R, Farokhzad OC. Engineering of self-assembled nanoparticle platform for precisely controlled combination drug therapy. Proc. Natl. Acad. Sci. U.S.A., 107, 17939-17944 (2010).
7. Kim C, Shah BP, Subramaniam P, Lee KB. Synergistic induction of apoptosis in brain cancer cells by targeted codelivery of siRNA and anticancer drugs. Mol. Pharm., 8, 1955-1961 (2011).
8. Yu YH, Kim E, Park DE, Shim G, Lee S, Kim YB, Kim CW, Oh YK. Cationic solid lipid nanoparticles for co-delivery of paclitaxel and siRNA. Eur. J. Pharm. Biopharm., 80, 268-273 (2012).
9. Bertucci C, Cimitan S, Riva A, Morazzoni P. Binding studies of taxanes to human serum albumin by bioaffinity chromatography and circular dichroism. J. Pharm. Biomed. Anal., 42, 81-87 (2006).
10. Sharma A, Straubinger RM. Novel taxol formulations: preparation and characterization of taxol-containing liposomes. Pharm. Res., 11, 889-896 (1994).
11. Kimelberg HK, Papahadjopoulos D. Phospholipid-protein interactions: membrane permeability correlated with monolayer "penetration." Biochim. Biophys. Acta, 233, 805-809 (1971).
12. Kogure K, Morita M, Hama S, Nakashima S, Tokumura A, Fukuzawa K. Enhancement by α-tocopheryl hemisuccinate of nitric oxide production induced by lypopolysaccharide and interferon-γ through the upregulation of protein kinase C in rat vascular smooth muscle cells. Eur. J. Biochem., 269, 2367-2372 (2002).
13. Crispen PL, Uzzo RG, Golovine K, Makhov P, Pollack A, Horwitz EM, Greenberg RE, Kolenko VM. Vitamin E succinate inhibits NF-kappaB and prevents the development of a metastatic phenotype in prostate cancer cells: implications for chemoprevention. Prostate, 67, 582-590 (2007).
14. You H, Yu W, Sanders BG, Kline K. RRR-α-tocopheryl succinate induces MDA-MB-435 and MCF-7 human breast cancer cells to undergo differentiation. Cell Growth Differ., 12, 471-480 (2001).
15. Ni J, Chen M, Zhang Y, Li R, Huang J, Yeh S. Vitamin E succinate inhibits human prostate cancer cell growth via modulating cell cycle regulatory machinery. Biochem. Biophys. Res. Commun., 300, 357-363 (2003).
16. Neuzil J, Weber T, Gellert N, Weber C. Selective cancer cell killing by alpha-tocopheryl succinate. Br. J. Cancer, 84, 87-89 (2001).
17. Kogure K, Hama S, Manabe S, Tokumura A, Fukuzawa K. High cytotoxicity of α-tocopheryl hemisuccinate to cancer cells is due to failure of their antioxidative defense systems. Cancer Lett., 186, 151-156 (2002).
18. Sun Y. Free radicals, antioxidant enzymes, and carcinogenesis. Free Radic. Biol. Med., 8, 583-599 (1990).
19. Kogure K, Morita M, Nakashima S, Hama S, Tokumura A, Fukuzawa K. Superoxide is responsible for apoptosis in rat vascular smooth muscle cells induced by α-tocopheryl hemisuccinate. Biochim. Biophys. Acta, 1528, 25-30 (2001).
20. Dong LF, Low P, Dyason JC, Wang XF, Prochazka L, Witting PK, Freeman R, Swettenham E, Valis K, Liu J, Zobalova R, Turanek J, Spitz DR, Domann FE, Scheffler IE, Ralph SJ, Neuzil J. α-Tocopheryl succinate induces apoptosis by targeting ubiquinone-binding sites in mitochondrial respiratory complex II. Oncogene, 27, 4324-4335 (2008).
21. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature, 438, 967-974 (2005).
22. Cross MJ, Claesson-Welsh L. FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol. Sci., 22, 201-207 (2001).
23. Dong LF, Swettenham E, Eliasson J, Wang XF, Gold M, Medunic Y, Stantic M, Low P, Prochazka L, Witting PK, Turanek J, Akporiaye ET, Ralph SJ, Neuzil J. Vitamin E analogues inhibit angiogenesis by selective induction of apoptosis in proliferating endothelial cells: the role of oxidative stress. Cancer Res., 67, 11906-11913 (2007).
24. Malafa MP, Neitzel LT. Vitamin E succinate promotes breast cancer tumor dormancy. J. Surg. Res., 93, 163-170 (2000).
25. Neuzil J, Swettenham E, Wang XF, Dong LF, Stapelberg M. α-Tocopheryl succinate inhibits angiogenesis by disrupting paracrine FGF2 signalling. FEBS Lett., 581, 4611-4615 (2007).
26. Malafa MP, Fokum FD, Smith L, Louis A. Inhibition of angiogenesis and promotion of melanoma dormancy by vitamin E succinate. Ann. Surg. Oncol., 9, 1023-1032 (2002).
27. Fodale V, Pierobon M, Liotta L, Petricoin E. Mechanism of cell adaptation: when and how do cancer cells develop chemoresistance? Cancer J., 17, 89-95 (2011).
28. Ueda K, Cardarelli C, Gottesman MM, Pastan I. Expression of a full-length cDNA for the human "MDR1" gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc. Natl. Acad. Sci. U.S.A., 84, 3004-3008 (1987).
29. Zhang X, Peng X, Yu W, Hou S, Zhao Y, Zhang Z, Huang X, Wu K. α-Tocopheryl succinate enhances doxorubicin-induced apoptosis in human gastric cancer cells via promotion of doxorubicin influx and suppression of doxorubicin efflux. Cancer Lett., 307, 174-181 (2011).
30. Kogure K, Hama S, Kisaki M, Takemasa H, Tokumura A, Suzuki I, Fukuzawa K. Structural characteristic of terminal dicarboxylic moiety required for apoptogenic activity of α-tocopheryl esters. Biochim. Biophys. Acta, 1672, 93-99 (2004).
31. Youk HJ, Lee E, Choi MK, Lee YJ, Chung JH, Kim SH, Lee CH, Lim SJ. Enhanced anticancer efficacy of α-tocopheryl succinate by conjugation with polyethylene glycol. J. Control. Release, 107, 43-52 (2005).
32. Traber MG, Kayden HJ, Green JB, Green MH. Absorption of water-miscible forms of vitamin E in a patient with cholestasis and in thoracic duct-cannulated rats. Am. J. Clin. Nutr., 44, 914-923 (1986).
33. Varma MV, Panchagnula R. Enhanced oral paclitaxel absorption with vitamin E-TPGS: effect on solubility and permeability in vitro, in situ and in vivo. Eur. J. Pharm. Sci., 25, 445-453 (2005).
34. Wang XF, Birringer M, Dong LF, Veprek P, Low P, Swettenham E, Stantic M, Yuan LH, Zobalova R, Wu K, Ledvina M, Ralph SJ, Neuzil J. A peptide conjugate of vitamin E succinate targets breast cancer cells with high ErbB2 expression. Cancer Res., 67, 3337-3344 (2007).
35. Hrzenjak A, Reicher H, Wintersperger A, Steinecker-Frohnwieser B, Sedlmayr P, Schmidt H, Nakamura T, Malle E, Sattler W. Inhibition of lung carcinoma cell growth by high density lipoproteinassociated α-tocopheryl- succinate. Cell. Mol. Life Sci., 61, 1520-1531 (2004).
36. Jizomoto H, Kanaoka E, Hirano K. pH-sensitive liposomes composed of tocopherol hemisuccinate and of phosphatidylethanolamine including tocopherol hemisuccinate. Biochim. Biophys. Acta, 1213, 343-348 (1994).
37. Kogure K, Manabe S, Hama S, Tokumura A, Fukuzawa K. Potentiation of anti-cancer effect by intravenous administration of vesiculated α-tocopheryl hemisuccinate on mouse melanoma in vivo. Cancer Lett., 192, 19-24 (2003).
38. Ramanathapuram LV, Hahn T, Graner MW, Katsanis E, Akporiaye ET. Vesiculated α-tocopheryl succinate enhances the anti-tumor effect of dendritic cell vaccines. Cancer Immunol. Immunother., 55, 166-177 (2006).
39. Hauser H. Spontaneous vesiculation of uncharged phospholipid dispersions consisting of lecithin and lysolecithin. Chem. Phys. Lipids, 43, 283-299 (1987).
40. Hama S, Utsumi S, Fukuda Y, Nakayama K, Okamura Y, Tsuchiya H, Fukuzawa K, Harashima H, Kogure K. Development of a novel drug delivery system consisting of an antitumor agent tocopheryl succinate. J. Control. Release, 161, 843-851 (2012).
41. Maruyama K. Intracellular targeting delivery of liposomal drugs to solid tumors based on EPR effects. Adv. Drug Deliv. Rev., 63, 161-169 (2011).
42. Kogure K, Hama S, Goto S, Munakata T, Tokumura A, Fukuzawa K. α-Tocopheryl succinate activates protein kinase C in cellular and cell-free systems. J. Nutr. Sci. Vitaminol., 49, 310-314 (2003).
43. Gu X, Schwartz JL, Pang X, Zhou Y, Sirois DA, Sridhar R. Cytotoxicity of liposomal α-tocopheryl succinate towards hamster cheek pouch carcinoma (HCPC-1) cells in culture. Cancer Lett., 239, 281-291 (2006).
44. Gu X, Song X, Dong Y, Cai H, Walters E, Zhang R, Pang X, Xie T, Guo Y, Sridhar R, Califano JA. Vitamin E succinate induces ceramide-mediated apoptosis in head and neck squamous cell carcinoma in vitro and in vivo. Clin. Cancer Res., 14, 1840-1848 (2008).
45. Nakamura Y, Kogure K, Futaki S, Harashima H. Octaarginine-modified multifunctional envelope-type nano device for siRNA. J. Control. Release, 119, 360-367 (2007).