Changes in glutathione, oxidative stress and mitochondrial membrane potential in apoptosis involving the anticancer activity of cantharidin isolated from redheaded blister beetles, epicauta hirticornis

Anti-Cancer Agents in Medicinal Chemistry

Volumn 13, Issue 7, 2013, Pages 1096-1114

  Verma, Akalesh Kumar ^a   Bali Prasad, Surya ^a  

^a NORTH EASTERN HILL UNIVERSITY   (India)

Author keywords

Antioxidant; Cytotoxicity; Docking; Glutathione peroxidase; Glutathione reductase; Glutathione s transferase

Indexed keywords

CANTHARIDIN; CASPASE 3; CASPASE 9; CATALASE; CISPLATIN; CYTOCHROME C; DITHIOTHREITOL; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; LIPOCORTIN 5; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BEETLE; BODY WEIGHT; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; FLOW CYTOMETRY; LIPID PEROXIDATION; LYMPHOMA; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR DOCKING; MOUSE; NEOPLASM; NONHUMAN; OXIDATIVE STRESS; PROTON NUCLEAR MAGNETIC RESONANCE; THIN LAYER CHROMATOGRAPHY; TUMOR VOLUME; WESTERN BLOTTING; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BEETLES; CANTHARIDIN; CELL LINE, TUMOR; CRYSTALLOGRAPHY, X-RAY; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MODELS, MOLECULAR; NEOPLASMS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84882745775     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/18715206113139990131     Document Type: Article

References (92)

1. Benigni, R.; Bossa, C. Mechanisms of chemical carcinogenicity and mutagenicity: A Review with implications for predictive toxicology. Chem. Rev., 2011, 111, 2507-2536.
2. Bray, F.; Moller, B. Predicting the future burden of cancer. Nat. Rev. Cancer, 2006, 6, 63-75.
3. Florea, A. M.; Busselberg, D. Cisplatin as an anti-tumor drug: cellular mechanisms of activity, drug resistance and induced side effects. Cancers, 2011, 3, 1351-1371.
4. Gottesman, M. M. Mechanisms of cancer drug resistance. Annu. Rev. MED., 2002, 53, 615-627.
5. Alves, R. R.; Rosa, I. L. Why study the use of animal products in traditional medicines? J. Ethnobiol. Ethnomed., 2005, 1, 1-5.
6. Alves, R. R. N.; Alves, H. N. The faunal drugstore: Animal-based remedies used in traditional medicines in Latin America. J. Ethnobiol. Ethnomed., 2011, 7, 9-51.
7. Watanabe, M. A. E.; Amarante, M. K.; Conti, B. J.; Sforcin, J. M. Cytotoxic constituents of propolis inducing anticancer effects: a review. J. Pharmacy Pharmacol., 2011, 63,1378-1386.
8. Quave, C. L.; Lohani, U.; Verde, A.; Fajardo, J.; Rivera, D.; Obon, C.; Valdes, A.; Pieroni, A. A comparative assessment of zootherapeutic remedies from selected areas in Albania, Italy, Spain and Nepal. J. Ethnobiol., 2010, 30, 92-125.
9. Mahawar, M. M.; Jaroli, D. P. Traditional zootherapeutic studies in India: a review. J. Ethnobiol. Ethnomed., 2008, 4, 17-28.
10. Liu, X. H.; Blazsek, I.; Comisso, M.; Legras, S.; Marion, S.; Quittet, P.; Anjo, A.; Wang, G S.; Misset, J. L. Effects of norcantharidin, a protein phosphatase type-2A inhibitor, on the growth of normal and malignant haemopoietic cells. Eur. J. Cancer, 1995, 31, 953-1963.
11. Wang, G. S. Medical uses of mylabris in ancient China and recent studies. J. Ethnopharmacol., 1989, 26, 147-162.
12. Liu, D.; Zhiwei, C. Z. The effects of cantharidin and cantharidin derivates on tumour cells. Anti-Cancer Agents Med. Chem., 2009, 9, 392-406.
13. Sagawa, M.; Nakazato, T.; Uchida, H.; Ikeda, Y.; Kizaki, M. Cantharidin induces apoptosis of human multiple myeloma cells via inhibition of the JAK/STAT pathway. Cancer Sci., 2008, 99, 1820-1826.
14. Cohen, P. T.; Philp, A.; Vazquez-Martin, C. Protein phosphatase 4 from obscurity to vital functions. FEBS Lett., 2005, 579, 3278-3286.
15. Verma, A. K.; Prasad, S. B. Bioactive component, cantharidin from Mylabris cichorii and its antitumor activity against Ehrlich ascites carcinoma. Cell Biol. Toxicol., 2012, 28, 133-147.
16. Meister, A.; Anderson, M. E. Glutathione. Ann. Rev. Biochemistry, 1983, 52, 711-760.
17. Wang, W.; Ballatori, N. Endogenous glutathione conjugates: occurrence and biological functions. Pharmacol. Reviews, 1998, 50, 335-355.
18. Campling, B. G.; Pym, J.; Galbraith, P. R. Use of the MTT assay for rapid determination of the chemosensitivity of human leukemic blast cells. Leuk. Res., 1988, 12, 823-831.
19. Baskic, D.; Popovic, S.; Ristic, P.; Arsenijevic, N. N. Analysis of cyclohexamide-induced apoptosis in human leukocytes: Fluorescence microscopy using annexin V/propidium iodide versus acridin orange/ethidium bromide. Cell Biol. Int., 2006, 11, 924-932.
20. Zhang, L.; Ruan, J.; Yan, L.; Li, W.; Wu, Y.; Tao, L.; Zhang, F.; Zheng, S.; Wang, A.; Lu, Y. Xanthatin induces cell cycle arrest at G2/M checkpoint and apoptosis via disrupting NF-κB pathway in A549 non-small-cell lung cancer cells. Molecules., 2012, 17, 3736-3750.
21. Zhu, Y.; Li, M.; Wang, X.; Jin, H.; Liu, S.; Xu, J.; Chen, Q. Caspase cleavage of cytochrome c1 disrupts mitochondrial function and enhances cytochrome c release. Cell Res., 2011, 22, 127-141.
22. Hyung, S. C.; Jun, W. K.; Young-Nam, C.; Chaekyun, K. A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J. Immunoassay Immunochem., 2006, 27, 31-44.
23. Buege, J. A.; Aust, S. D. Microsomal lipid peroxidation. Methods Enzymol., 1978, 52, 302-310.
24. Mihara, M.; Uchiama, M. Determination of malonaldheyde precursor in tissues by thiobarbituric acid test. Anal. Biochem., 1978, 86, 271-278.
25. Sedlak, L.; Lindsay, R. H. Estimation of total, protein-bound and nonprotein sulfhydryl groupsin tissue with Ellman's reagent. Anal. Biochem., 1969, 25, 192-205.
26. Flohe, L.; Gunzler, W. A. Assay of glutathione peroxidase. Method Enzymol., 1984, 105, 114-121.
27. Smith, I. K.; Vierheller, T. L.; Thome, C. A. Assay of glutathione reductase in crude tissue homogenates using 5, S'-dithiobis (2-nitrobenzoic acid). Anal. Biochem., 1988, 175, 408-413.
28. Habig, W. H.; Pabst, M. J.; Jakoby, W. B. Glutathione Stransferases, the first enzymatic step in mercapturic acid formation. Biol. Chem., 1974, 249, 7130-139.
29. Lowry, O. H.; Rosebrough, N. J.; Farr, A. L.; Randall, R. J. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 1951, 193, 265-275.
30. Thomsen, R.; Christensen, M. H. MolDock: A new technique for high-accuracy molecular docking. J. Med. Chem., 2006, 49, 3315-3321.
31. Aaron, D. D.; Andrew, S.; Mitchell, J. W. E.; Rush, J. Q. Elevated skeletal muscle apoptotic signaling following glutathione depletion. Apoptosis, 2012, 17, 48-60.
32. Rosangkima, G.; Rongpi, T.; Prasad, S. B. Role of Glutathione and Glutathione-Related Enzymes in the Antitumor Activity of Dillenia pentagyna in Dalton's Lymphoma-bearing mice. Internat. J. Cancer Res., 2008, 4, 92-102.
33. Sharma, V. P.; Khan, A. U. Drugs of mammals' origin used by aborigines of Garo hills of Meghalaya State, India. Bionature, 1995, 15, 1-5.
34. Wang, C. C.; Wu, C. H.; Hsieh, K. J.; Yen, K. Y.; Yang, L. L. Cytotoxic effects of cantharidin on the growth of normal and carcinoma cells. Toxicology, 2000, 147, 77-87.
35. Prasad, S. B.; Verma, A. K.; Rosangkima, G.; Brahma, B.; Rongpi, T.; Amenla; Arjun, J. Antitumor activity of Mylabris cichorii extracts against murine ascites Dalton's lymphoma. J. Pharmacy Res., 2010, 3, 3006-3009.
36. Nicholls, D. S.; Christmas, T. I.; Greig, D. E. Oedemerid blister beetle dermatosis: a review. J. Am. Acad. Dermatol., 1990, 22, 815-819.
37. Carrel, J. E.; McCairel, M. H.; Slagle, A. J.; Doom, J. P.; Brill, J.; McCormick, J. P. Cantharidin production in a blister beetle. Experientia, 1993, 49,171-174.
38. Eldridge, R.; Casida, J. E. Cantharidin effects on protein phosphatases and the phosphorylation state of phosphoproteins in mice. Toxicol. Appl. Pharmacol., 1995, 130, 95-100.
39. Cirrito, T. P.; Bergstein, I. Cancer therapy with cantharidin and cantharidin analogs. Patent WO/2008/030617, Stemline Therapeutics: Inc. New York, 2008.
40. Wu, J. Z.; Situ, Z. Q.; Chen, J. Y.; Liu, B.; Wang, W. Chemosensitivity of salivary gland and oral cancer cell lines. Chin. Med. J., 1992, 105, 1026-1028.
41. McCluskey, A.; Bowyer, M. C.; Collins, E.; Sim, A. T. R.; Sakoff, J. A.; Baldwin, M. L. Anhydride modified cantharidin analogues: synthesis, inhibition of protein phosphatases 1 and 2A and anticancer activity. Bioorg. Med. Chem. Lett., 2000, 10, 1687-1690.
42. Sakoff, J. A.; Ackland, S. P.; Baldwin, M. L.; Keane, M. A.; McCluskey, A. Anticancer activity and protein phosphatase 1 and 2A inhibition of a new generation of cantharidin analogues. Invest. New Drugs, 2002, 20, 1-11.
43. Goldie, H.; Felix, M. D. Growth characteristics of free tumor cells transformed serially in the peritoneal fluid of the mouse. Cancer Res., 1951, 11, 73-80.
44. Prasad, S. B.; Giri, A.; Khynriam, D. Studies on the chromosomes of murine Dalton's lymphoma cells and the effect of cisplatin on chromosomes of these cells and bone marrow cell in vivo. Cytologia, 1998, 63, 405-413.
45. Martin, S.; Reutelingsperger, C.; McGahon, A.; Rader, J.; Van Schie, R.; LaFace, D.; Green, D. R. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med., 1995, 182, 1545-1556.
46. Toykuni, S. Reactive oxygen species-induced molecular damage and its application in pathology. Pathol. Int., 1994, 49, 91-102.
47. Nordberg, J.; Arner, E. Reactive oxygen species, antioxidants, and mammalian thioredoxin system. Free Radic. Biol. Med., 2001, 31, 1287-312.
48. Cai F.; Dupertuis, Y. M.; Pichard, C. Role of polyunsaturated fatty acids and lipid peroxidation on colorectal cancer risk and treatments. Curr. Opin. Clin. Nutr. Metab. Care., 2012, 15, 99-106.
49. Heneberg, P. Use of protein tyrosine phosphatase inhibitors as promising targeted therapeutic drugs. Curr. Med. Chem., 2009, 16, 706-33.
50. Heneberg, P.; Draberova, L.; Bambouskova, M.; Pompach, P.; Draber, P. Down-regulation of protein-tyrosine phosphatases activates an immune receptor in the absence of its translocation into lipid rafts. J. Biol. Chem., 2010, 285, 12787-12802.
51. Rosen, G. M.; Pou, S.; Ramos, C. L.; Cohen, M. S.; Britigan, B. E. Free radicals and phagocytic cells. FASEB J., 1995, 9, 200-209.
52. Lander, H. M. An essential role for free radicals and derived species in signal transduction. FASEB J., 1997, 11, 118-124.
53. Hail, N. Mitochondrial reactive oxygen species affect sensitivity to curcumin induced apoptosis. Free Radic. Biol. Med., 2008, 44, 1382-1393.
54. Tsauer, W.; Lin, J. G.; Lin, P. Y.; Hsu, F. L; Chiang, H. C. The effects of cantharidin analogues on xanthine oxidase. Anticancer Res., 1997, 17, 2095-2098.
55. Rauh, R.; Kahl, S.; Boechzelt, H.; Bauer, R.; Kaina, B.; Efferth T. Molecular biology of cantharidin in cancer cells. Chinese Med., 2007, 2, 1-9.
56. Liu, D.; Chen, Z. The effects of cantharidin and cantharidin derivates on tumour cells. Anticancer Agents Med. Chem., 2009, 9, 392-396.
57. Deng, L.; Yang, B.; He, Q.; Hu, Y. Novel 1, 2, 3-Triazole-linked norcantharidin analogues: synthesis and evaluation of growth inhibition in a panel of selected tumor-cell lines. Lett. Drug Des. Discov., 2008, 5, 225-231.
58. Deng, L.; Yang, B.; He, Q.; Hu, Y. Disodium phosphate of novel pyrazole-linked norcantharidin analogs: design, synthesis and their anticancer evaluation. Lett. Drug Des. Discov., 2008, 5, 346-352.
59. Fujiki, H.; Suganuma, M. Tumor promoters-microcystin-LR, Nodularin and TNF-alpha and human cancer development. Anticancer Agents Med. Chem., 2011, 11, 4-18.
60. Amaia, F. G.; Anabel, P. G.; Antonello, N.; Sanchez, M. T. F. Inhibition of protein phosphatases impairs the ability of astrocytes to detoxify hydrogen peroxide. Free Radic. Biol. Med., 2008, 44, 1806-1816.
61. Cheng, A.; Balczon, R.; Zuo, Z.; Koons, J. S.; Walsh, A. H.; Honkanen, R. E. Fostriecin-mediated G2-M-phase growth arrest correlates with abnormal centrosome replication, the formation of aberrant mitotic spindles, and the inhibition of serine/threonine protein phosphatase activity. Cancer Res., 1998, 58, 3611-3619.
62. Alam, J. J. Apoptosis: target for novel drugs. Trends Biotechnol., 2003, 21, 479-483.
63. Crompton, M. Bax, Bid and the permeabilization of the mitochondrial outer membrane in apoptosis. Curr. Opin. Cell Biol., 2000, 12, 414-419.
64. Rastogi, R. P.; Richa; Sinha, R. P. Apoptosis: molecular mechanisms and pathogenicity. EXCLI Journal, 2009, 8, 155-181.
65. Liu, C. Y.; Lee, C. F.; Wei, Y. H. Role of reactive oxygen specieselicited apoptosis in the pathophysiology of mitochondrial and neuro degenerative diseases associated with mitochondrial DNA mutations. J. Formosan Med. Association, 2009, 108, 599-611.
66. Pamplona, R.; Prat, J.; Cadenas, S.; Rojas, C.; Perez-Campo, R.; Lopez, T.M.; Barja, G. Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from long-lived species, the pigeon and human case. Mech. Aging. Dev., 1996, 86, 53-66.
67. Catala, A.; Arcemis, C.; Cerruti, A. Interaction of rat liver microsomes saturated and unsaturated fatty acids with fatty acid binding protein: peroxidation effect. Mol. Cell. Biochem., 1994, 137, 135-139.
68. Vladimirov, Y. A.; Olenev, V. I.; Suslova, T. B.; Cheremisina, Z. P. Lipid peroxidation in mitochondrial membrane. Adv. Lipid. Res., 1980, 17, 173-149.
69. Kidd, M. P. Glutathione: systemic protectants against oxidative and free radical damage. Alternat. Med. Rev., 1997, 2, 155-176.
70. Ahmad, S.; Okine, L.; LE, B.; Najarian, P.; Vistica, D. T. Elevation of glutathione in phenylalanine mustard-resistant murine L1210 leukemia cells. J. Biol. Chem., 1987, 262, 15048-15053.
71. Hospers, G. A. P.; Mulder, N. H.; Dejong, B.; Deley, L.; Uges, D. R. A.; Fichtinger-Schepmnan, A. M. J.; Scheper, R. J.; Devries, E. G. E. Characterization of a human small cell lung carcinoma cell line with acquired resistance to cisdiamminedichloroplatinum (II) in vitro. Cancer Res., 1988; 48, 6803-6807.
72. Kramer, R. A.; Zakher, J.; Kim, G. Role of the glutathione redox cycle in acquired and de novo multidrug resistance. Science, 1988, 241, 694-697.
73. Coppola, S.; Ghibelli, L. GSH extrusion and the mitochondrial pathway of apoptotic signaling. Biochem. Soc. Trans., 2000, 28, 56-61.
74. Jantova, S.; Cipak, L.; Letasiova, S. Berberine induces apoptosis through a mitochondria/caspase pathway in human promonocytic U937 cells. Toxicol. In Vitro, 2007, 21, 25-31.
75. Shaw, J. P.; Chou, I. N. Elevation of intracellular glutathione content associated with mitogenic stimulation of quiescent fibroblasts. J. Cell Physiol., 1986, 129, 193-198.
76. Terradez, P.; Asensi, M.; Lasso, D. E.; La.; Vega, M. C.; Puertes, I. R.; Vina, J.; Estrela, J. M. Depletion of tumor glutathione in vivo by butathione sulphoximine: modulation by the rate of cellular proliferation and inhibition of cancer growth. Biochem. J., 1993, 292, 477-483.
77. Estrela, J. M.; Hernandez, R.; Terradez, P.; Asensi, M.; Inmaculada R. P.; Vina, J. Regulation of glutathione metabolism in Ehrlich ascites tumor cells. Biochem. J., 1992, 286, 257-262.
78. Sadzuka, Y.; Shoji, T.; Takino, Y. Change of lipid peroxide levels in rat tissues after cisplatin administration. Toxicol. Lett., 1991, 57, 159-166.
79. Olafsdottir, K.; Pascoe, G. A.; Reed, D. J. Mitochondrial glutathione status during Ca2 + ionophore-induced injury to isolated hepatocytes. Arch. Biochem. Biophys., 1988, 263, 226-235.
80. Sheehan, D.; Meade, G.; Foley, Y. M.; Dowel, C. A. Structure, function and evolution of glutathione transferases: Implications for classification of non-manunalian members of an ancient enzyme superfamily. Biochem., 2001, 360, 1-16.
81. Li, H. Z.; Yong, L. B.; Yin, W.; Chun, L. Y.; Xiang, Y. M.; Yu, X. L. Cantharidin reverses multidrug resistance of human hepatoma HepG2/ADM cells via down-regulation of P-glycoprotein expression. Cancer Lett., 2008, 272, 102-109.
82. Chavkova, Z.; Guzy Barnova, E.; Marekova, M.; Torneckova, V.; Dubayova, K.; Kusnir, I. In vitro effect of stobadine on Fe2+-induced oxidative stress in rat liver mitochondria. Bratisl. Lek. Listy., 2001, 102, 543-547.
83. Li, S.; Yan T.; Yang, I. Q.; Oberley, T. H.; Oberley, L. W. The role of cellular glutathione peroxidase redox regulation in the suppression of tumor cell growth by manganese superoxide dismutase. Cancer Res., 2000, 60, 3927-3939.
84. Haustedt, L. O.; Mang, C.; Siems, K.; Schiewe, H. Rational approaches to naturalproduct-based drug design. Curr. Opin. Drug. Discov. Devel., 2006, 9, 445-462.
85. Shen, J.; Xu, X.; Cheng, F.; Liu, H.; Luo, X.; Shen, J.; Chen, K.; Zhao, W.; Shen, X.; Jiang, H. Virtual screening on natural products for discovering active compounds and target information. Curr. Med. Chem., 2003, 10, 2327-2342.
86. Basu-Baul, T. S.; Paul, A.; Pellerito, L.; Scopelliti, M.; Singh, P.; Verma, P.; Duthie, A.; Vos D-de.; Tiekink, E. R. T. Dibutyltin (IV) complexes containing arylazobenzoate ligands: chemistry, in vitro cytotoxic effects on human tumor cell lines and mode of interaction with some enzymes. Invest. New Drugs, 2011, 29, 285-299.
87. Nikbakhtzadeh, M. R.; Dettne, K.; Boland, W.; Dotterl, S. A novel approach to the quantitation of coeluting cantharidin and deuterium labelled cantharidin in blister beetles (Coleoptera: Meloidae). Iran. J. Arthropod Borne Dis., 2007, 1, 19-26.
88. Moed, L.; Shwayder, T. A.; Chang, M. W. Cantharidin revisited: a blistering defense of an ancient medicine. Arch. Dermatol., 2001, 137, 1357-1360.
89. Funt, T. R.; Mehr, K. A. Cantharidin: a valuable office treatment of molluscum contagiosum. South. Med. J., 1979, 72, 1019-1025.
90. Honkanen, R. E. Cantharidin, another natural toxin that inhibits the activity of serine/threonine protein phosphatases types 1 and 2A. FEBS Lett., 1993, 330, 283-286.
91. Efferth, T. Microarray-based prediction of cytotoxicity of tumor cells to cantharidin. Oncol. Rep., 2005, 13, 459-463.
92. McConnell, J. L.; Wadzinski, B. E. Targeting protein serine/threonine phosphatases for drug development. Mol. Pharmacol., 2009, 75, 1249-1261.