Affinity of vitamin E analogues for the ubiquinone complex II site correlates with their toxicity to cancer cells

Molecular Nutrition and Food Research

Volumn 55, Issue 10, 2011, Pages 1543-1551

  Neuzil, Jiri ^a,b   Cerny, Jiri ^b   Dyason, Jeffrey C ^a   Dong, Lan Feng ^a   Ralph, Stephen J ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b INSTITUTE OF BIOTECHNOLOGY   (Czech Republic)

Author keywords

Anti cancer activity; Apoptosis; Complex II; Modelling; Vitamin E analogues

Indexed keywords

ALPHA TOCOPHEROL; ANTINEOPLASTIC AGENT; DRUG DERIVATIVE; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINONE;

ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG SCREENING; HUMAN; METABOLISM; STRUCTURE ACTIVITY RELATION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BINDING SITES; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; ELECTRON TRANSPORT COMPLEX II; HUMANS; MODELS, MOLECULAR; STRUCTURE-ACTIVITY RELATIONSHIP; UBIQUINONE; VITAMIN E;

TOSCANA VIRUS;

EID: 80053918718     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201100066     Document Type: Article

References (56)

1. Neuzil, J., Weber, T., Gellert, N., Weber, C., Selective cancer cell killing by α-tocopheryl succinate. Br. J. Cancer 2001, 84, 87-89.
2. Neuzil, J., Vitamin E succinate and cancer treatment: a vitamin E prototype for selective anti-tumour activity. Br. J. Cancer 2003, 89, 1822-1826.
3. Yu, W., Simmons-Menchaca, M., Gapor, A., Sanders, B. G., Kline, K., Induction of apoptosis in human breast cancer cells by tocopherols and tocotrienols. Nutr. Cancer 1999, 33, 26-32.
4. Pussinen, P. J., Lindner, H., Glatter, O., Reicher, H. et al., Lipoprotein-associated α-tocopheryl succinate inhibits cell growth and induces apoptosis in human MCF-7 and HBL-100 breast cancer cells. Biochim. Biophys. Acta 2000, 1485, 129-144.
5. Malafa, M. P., Neitzel, L. T., Vitamin E succinate promotes breast cancer tumor dormancy. J. Surg. Res. 2000, 93, 163-170.
6. Weber, T., Lu, M., Andera, L., Lahm, H. et al., Vitamin E succinate is a potent novel anti-neoplastic agent with high tumor selectivity and cooperativity with tumor necrosis factor-related apoptosis-inducing ligand (TRAIL, Apo2L) in vivo. Clin. Cancer Res. 2002, 8, 863-869.
7. Malafa, M. P., Fokum, F. D., Mowlavi, A., Abusief, M., King, M., Vitamin E inhibits melanoma growth in mice. Surgery 2002, 131, 85-91.
8. Barnett, K. T., Fokum, F. D., Malafa, M. P., Vitamin E succinate inhibits colon cancer liver metastases. J. Surg. Res. 2002, 106, 292-298.
9. Lawson, K. A., Anderson, K., Menchaca, M., Atkinson, J. et al., Novel vitamin E analogue decreases syngeneic mouse mammary tumor burden and reduces lung metastasis. Mol. Cancer Ther. 2003, 2, 437-444.
10. Hahn, T., Szabo, L., Gold, M., Ramanathapuram, L. et al., Dietary administration of the proapoptotic vitamin E analogue α-tocopheryloxyacetic acid inhibits metastatic murine breast cancer. Cancer Res. 2006, 66, 9374-9378.
11. Hahn, T., Fried, K., Hurley, L. H., Akporiaye, E. T., Orally active α-tocopheryloxyacetic acid suppresses tumor growth and multiplicity of spontaneous murine breast cancer. Mol. Cancer Ther. 2009, 8, 1570-1578.
12. Tomasetti, M., Gellert, N., Procopio, A., Neuzil, J., A vitamin E analogue suppresses malignant mesothelioma in a pre-clinical model: a prototype of a future drug against a fatal neoplastic disease? Int. J. Cancer 2004, 109, 641-642.
13. Stapelberg, M., Gellert, N., Swettenham, E., Tomasetti, M. et al., α-Tocopheryl succinate inhibits malignant mesothelioma by disrupting the FGF autocrine loop: the role of oxidative stress. J. Biol. Chem. 2005, 280, 25369-25376.
14. Wang, X. F., Birringer, M., Dong, L. F., Veprek, P. et al., A peptide adduct of vitamin E succinate targets breast cancer cells with high erbB2 expression. Cancer Res. 2007, 67, 3337-3344.
15. Neuzil, J., Weber, T., Schröder, A., Lu, M. et al., Induction of apoptosis in cancer cells by α-tocopheryl succinate: molecular pathways and structural requirements. FASEB J. 2001, 15, 403-415.
16. Neuzil, J., Tomasetti, M., Zhao, Y., Dong, L. F. et al., Vitamin E analogs, a novel group of 'mitocans', as anti-cancer agents: the importance of being redox-silent. Mol. Pharmacol. 2007, 71, 1185-1199.
17. Neuzil, J., Dong, L. F., Ramanathapuram, L., Hahn, T. et al., Vitamin E analogues: a novel group of mitocans, anti-cancer agents that act by targeting mitochondria. Mol. Asp. Med. 2007, 28, 607-645.
18. L/Bcl-2 function. J. Biol. Chem. 2006, 281, 11819-11825.
19. Neuzil, J., Dyason, J. C., Freeman, R., Dong, L. F. et al., Mitocans as anti-cancer agents targeting mitochondria: Lessons from studies with vitamin E analogues, inhibitors of complex II. J. Bioenerg. Biomembr. 2007, 39, 65-72.
20. Ottino, P., Duncan, J. R., Effect of α-tocopherol succinate on free radical and lipid peroxidation levels in BL6 melanoma cells. Free Radic. Biol. Med. 1997, 22, 1145-1151.
21. 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. 2002, 186, 151-156.
22. Weber, T., Dalen, H., Andera, L., Nègre-Salvayre, A. et al., Mitochondria play a central role in apoptosis induced by α-tocopheryl succinate, an agent with anticancer activity. Comparison with receptor-mediated pro-apoptotic signalling. Biochemistry 2003, 42, 4277-4291.
23. Kang, Y. H., Lee, E., Choi, M. K., Ku, J. L. et al., Role of reactive oxygen species in the induction of apoptosis by α-tocopheryl succinate. Int. J. Cancer 2004, 112, 385-392.
24. Swettenham, E., Witting, P. K., Salvatore, B. A., Neuzil, J., α-Tocopheryl succinate selectively induces apoptosis in neuroblastoma cells: potential therapy of malignancies of the nervous system? J. Neurochem. 2005, 94, 1448-1456.
25. Dong, L. F., Swettenham, E., Eliasson, J., Wang, X. F. et al., Vitamin E analogs inhibit angiogenesis by selective apoptosis induction in proliferating endothelial cells: the role of oxidative stress. Cancer Res. 2007, 67, 11906-11913.
26. Dong, L. F., Low, P., Dyason, J., Wang, X. F. et al., α-Tocopheryl succinate induces apoptosis by targeting ubiquinone-binding sites in mitochondrial respiratory complex II. Oncogene 2008, 27, 4324-4335.
27. Dong, L. F., Freeman, R., Liu, J., Zobalova, R. et al., Suppression of tumour growth in vivo by the mitocan α-tocopheryl succinate requires respiratory complex II. Clin. Cancer Res. 2009, 15, 1593-1600.
28. Arya, P., Alibhai, N., Qin, H., Burton, G. W. et al., Design and synthesis of analogs of vitamin E: antiproliferative activity against human breast adenocarcinoma cells. Bioorg. Med. Chem. Lett. 1998, 8, 2433-2438.
29. Birringer, M., EyTina, J. H., Salvatore, B. A., Neuzil, J., Vitamin E analogues as inducers of apoptosis: Structure-function relationship. Br. J. Cancer 2003, 88, 1948-1955.
30. Galli, F., Stabile, A. M., Betti, M., Conte, C. et al., The effect of α- and γ-tocopherol and their carboxyethyl hydroxychroman metabolites on prostate cancer cell proliferation. Arch. Biochem. Biophys. 2004, 423, 97-102.
31. Tomic-Vatic, A., EyTina, J. H., Chapmann, J. M., Mahdavian, E. et al., Vitamin E amides, a new class of vitamin E analogues with enhanced pro-apoptotic activity. Int. J. Cancer 2005, 117, 118-123.
32. Sun, F., Huo, X., Zhai, Y., Wang, A. et al., Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 2005, 21, 1043-1057.
33. Word, J. M., Lovell, S. C., Richardson, J. S., Richardson, D. C., Asparagine and glutamine: Using hydrogen atom contacts in the choice of side-chain amide orientation. J. Mol. Biol. 1999, 285, 1735-1747.
34. Case, D. A., Pearlman, D. A., Caldwell, J. W., Amber 7. University of California, San Francisco 2002.
35. Sanner, M. F., Python: a programming language for software integration and development. J. Mol. Graphic Mod. 1999, 17, 57-61.
36. Accelrys., InsightII, Accelrys Inc, San Diego 2001.
37. Allen, F. H., The Cambridge Structural Database: a quarter of a million crystal structures and rising. Acta Crystallogr. B 2002, 5, 380-388.
38. Morris, G. M., Goodsell, D. S., Halliday, R. S., Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J. Comp. Chem. 1998, 19, 1639-1662.
39. ™: An aid for structure-based drug design. J. Computer Aided Mol. Des. 2002, 16, 871-881.
40. Kubar, T., Jurecka, P., Cerny, J., Rezac, J. et al., Density-functional, density-functional tight-binding, and wave function calculations on biomolecular systems. J. Phys. Chem. A 2007, 111, 26, 5642-5647.
41. Elstner, M., Porezag, D., Jungnickel, G., Elsner, J. et al., Self-consistent-charge density-functional tight-binding method for simulations of complex materials properties. Phys. Rev. B 1998, 58, 7260-7268.
42. Elstner, M., Hobza, P., Frauenheim, T., Suhai, S., Kaxiras, E., Hydrogen bonding and stacking interactions of nucleic acid base pairs: A density-functional-theory based treatment. J. Chem. Phys. 2001, 114, 5149-5155.
43. Dong, L. F., Jameson, V. J. A., Tilly, D., Cerny, J. et al., Mitochondrial targeting of vitamin E succinate enhances its pro-apoptotic and anti-cancer activity via mitochondrial complex II. J. Biol. Chem. 2011, 286, 3717-3728.
44. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., Case, D. A., Development and testing of a general AMBER force field. J. Comput. Chem. 2004, 25, 1157-1174.
45. Wang, J. M., Cieplak, P., Kollman, P. A., How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 2000. 21, 1049-1074.
46. Bayly, C. I., Cieplak, P., Cornell, W. D., Kollman, P. A., A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model. J. Phys. Chem. 1993, 97, 10269-10280.
47. Van der Spoel, D., Lindahl, E., Hess, B., Groenhof, G. et al., GROMACS: Fast, flexible, and free. J. Comput. Chem. 2005, 26, 1701-1718.
48. Neuzil, J., Wang, X. F., Dong, L. F., Low, P., Ralph, S. J., Molecular mechanism of 'mitocan'-induced apoptosis in cancer cells epitomizes the multiple roles of reactive oxygen species and Bcl-2 family proteins. FEBS Lett. 2006, 580, 5125-5129.
49. Prochazka, L., Dong, L. F., Valis, K., Freeman, R. et al., α-Tocopheryl succinate causes mitochondrial permeabilization by preferential formation of Bak channel. Apoptosis 2010, 15, 782-794.
50. Valis, K., Prochazka, L., Boura, E., Chladova, M. et al., Hippo/Mst1 stimulates transcription of NOXA in a FoxO1-dependent manner. Cancer Res. 2011, 71, 946-954.
51. Albayrak, T., Scherhammer, V., Schoenfeld, N., Braziulis, E. et al., The tumor suppressor cybL, a component of the respiratory chain, mediates apoptosis induction. Mol. Biol. Cell 2003, 14, 3082-3096.
52. Xu, R. H., Pelicano, H., Zhou, Y., Carew, J. S. et al., Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res. 2005, 65, 613-621.
53. Golstein, P., Kroemer, G., Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci. 2007, 32, 37-43.
54. Turanek, J., Wang, X. F., Knotigova, P., Dong, L. F. et al., Liposomal formulation of α-tocopheryl maleamide: in vitro and in vivo toxicological profile and anticancer effect against spontaneous breast carcinomas in mice. Toxicol. Appl. Pharmacol. 2009, 237, 249-257.
55. Miyadera, H., Shiomi, K., Ui, H., Yamaguchi, Y. et al., Atpenins, potent and specific inhibitors of mitochondrial complex II (succinate-ubiquinone oxidoreductase). Proc. Natl. Acad. Sci. USA 2003, 100, 473-477.
56. Selby, T. P., Hughes, K. A., Rauh, J. J., Hanna, W. S., Synthetic atpenin analogs: potent mitochondrial inhibitors of mammalian and fungal succinate-ubiquinone oxidoreductase. Bioorg. Med. Chem. Lett. 2010, 20, 1665-1668.