Pomegranate extract, A prooxidant with antiproliferative and proapoptotic activities preferentially towards carcinoma cells

Anti-Cancer Agents in Medicinal Chemistry

Volumn 10, Issue 8, 2010, Pages 634-643

  Weisburg, Jeffrey H ^a   Schuck, Alyssa G ^a   Silverman, Malki S ^a   Ovits Levy, Channa G ^a   Solodokin, Loriel J ^a   Zuckerbraun, Harriet L ^a   Babich, Harvey ^a  

^a YESHIVA UNIVERSITY   (United States)

Author keywords

Apoptosis; Nutraceuticals; Oxidative stress; Polyphenols; Pomegranate; Prooxidant

Indexed keywords

1 CHLORO 2,4 DINITROBENZENE; 5 CHLOROMETHYLFLUORESCEIN DIACETATE; ACETYLCYSTEINE; BIOLOGICAL MARKER; CASPASE 3; CATALASE; COBALT; FLUORESCENT DYE; GLUTATHIONE; GLUTATHIONE DISULFIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POMEGRANATE EXTRACT; PYRUVIC ACID; SODIUM CHLORIDE; UNCLASSIFIED DRUG; WATER;

ACIDITY; ALKALINITY; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CARCINOMA CELL; CELL CULTURE; CELL DEATH; CELL FREE SYSTEM; CONTROLLED STUDY; CULTURE MEDIUM; CYTOTOXICITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MOUTH CANCER; MOUTH CAVITY; POMEGRANATE;

EID: 79551646699     PISSN: 18715206     EISSN: None     Source Type: Journal    
DOI: 10.2174/187152010794474000     Document Type: Article

References (60)

1. Beliveau, R.; Gingras, D. Role of nutrition in preventing cancer. Can. Fam. Phys. 2007, 53, 1905-1911.
2. Klass, C.M.; Shin, D.M. Current status and future perspectives of chemoprevention in head and neck cancer. Curr. Cancer Drug Targets 2007, 7, 623-632.
3. Halder, A.; Raychowdhury, R.; Ghosh, A.; De, M. Black tea (Camellia sinensis) as a chemopreventive agent in oral precancerous lesions. J. Environ. Pathol. Toxicol. Oncol. 2005, 24, 141-144.
4. Li, N.; Sun, Z.; Han, C.; Chen, J. The chemopreventive effects of tea on human oral precancerous mucosa lesions. Proc. Soc. Exp. Biol. Med. 1999, 220, 218-224.
5. Koyama, S.; Cobb, L.J.; Mehta, H.H.; Seeram, N.P.; Heber, D.; Pantuck, A.J.; Cohen, P. Pomegranate extract induces apoptosis in human cancer cells by modulation of the IGF-IGFBP axis. Growth Horm. IGF Res. 2010, 20, 55-62.
6. Aviram, M; Rosenblat, M.; Gaitini, D.; Nitecki, S.; Hoffman, A.; Dornfeld, L.; Volkova, N.; Presser, D.; Attias, J.; Liker, H.; Hayek, T. Pomegranate juice consumption for 3 years by patients with carotid artery stenosis reduces common carotid intima-media thickness, blood pressure and LDL oxidation. Clin. Nutr. 2004, 23, 423-433.
7. Sumner, M.D.; Elliott-Eller, M.; Weidner, G.; Daubenmier, J.J.; Chew, M.H.; Marlin, R.; Raisin, C.J.; Ornish, D. Effects of pomegranate juice consumption on myocardial perfusion in patients with coronary heart disease. Am. J. Cardiol. 2005, 96, 810-814.
8. Heber, D.; Seeram, N.P.; Wyatt, H.; Henning, S.M.; Zhang, Y.; Ogden, L.G.; Dreher, M.; Hill, J.O. Safety and antioxidant activity of a pomegranate ellagitannin-enriched polyphenols dietary supplement in overweight individuals with increased waist size. J. Agric. Food Chem. 2007, 55, 10050-10054.
9. Pantuck, A.J.; Zomorodian, N.; Belldegrun, A.S. Phase-II study of pomegranate juice for men with prostate cancer and increasing PSA. Curr. Urol. Rep. 2006, 7, 7.
10. Malik, A.; Afaq, F.; Sarfaraz, S.; Adhami, V.M.; Syed, D.N.; Mukhtar, H. Pomegranate fruit juice for chemoprevention and chemotherapy of prostate cancer. Proc. Natl. Acad. Sci. USA, 2005, 102, 14813-14818.
11. Loren, D.J.; Seeram; N.P.; Schulman, N.; Holtzman, D.M. Maternal dietary supplementation with pomegranate juice is neuroprotective in an animal model of neonatal hypoxic-ischemic brain injury. Pediatr. Res. 2005, 57, 858-864.
12. de Nigris, F.; Balestrieri, M.L.; Williams-Ignarro, S.; D'Armiento, F.P.; Fiorito, C.; Ignarro, L.J.; Napoli, C. The influence of pomegranate fruit extract in comparison to regular pomegranate juice and seed oil on nitric oxide and arterial function in obese Zucker rats. Nitric Oxide 2007, 17, 50-54.
13. Seeram, N.P.; Adams, L.S.; Henning, S.M.; Niu, Y.; Zhang, Y.; Nair, M.G.; Heber, D. In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegran ate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J. Nutr. Biochem. 2005, 16, 360-367.
14. Rasheed, Z.; Akhtar, N.; Anbazhagan, A.N.; Ramamurthy, S.; Shukla, M.; Haqqi, T.M. Polyphenol-rich pomegranate fruit extract (PE) suppresses PMACI-induced expression of pro-inflammatory cytokines by inhibiting the activation of MAP kinases and NFkappaB in human KU812 cells. J. Inflamm. 2009, 6, 1.
15. Vasconcelos, L.C.; Sampaio, F.C.; Sampaio, M.C.; Mdo, S.P.; Higino, J.S.; Peixoto, M.H. Minimum inhibitory concentration of adherence of Punica granatum Linn (pomegranate) gel against S. mutans, S. mitans, and C. albicans. Braz. Dent. J. 2006, 17, 223-227.
16. Decker, E.A. Phenolics: prooxidants or antioxidants? Nutr. Rev. 1997, 55, 396-398.
17. Atsumi, T.; Tonosaki, K.; Fujisawa, S. Induction of early apoptosis and ROS-generation activity in human gingival fibroblasts (HGF) and human submandibular gland carcinoma (HSG) cells treated with curcumin. Arch. Oral Biol. 2006, 51, 913-921.
18. Su, Y.; Sun, C.-M.; Chuang, H.H.; Chang, P.-T. Studies on the cytotoxic mechanisms of ginkgetin in a human ovarian adenocarcinoma cell line. Naunyn-Schmiedeberg's Arch. Pharmacol. 2000, 362, 82-90.
19. Nakagawa, H.; Hasumi, K.; Woo, L.T.; Nagai, K.; Wachi, M. Generation of hydrogen peroxide primarily contributes to the induction of Fe(II)-dependent apoptosis in Jurkat cells by (-)-epigallocatechin gallate. Carcinogenesis 2004, 25, 1567-1574.
20. Weisburg, J.H.; Weissman, D.B.; Sedaghat, T.; Babich, H. In vitro cytotoxicity of epigallocatechin gallate and tea extracts to cancerous and normal cells from the human oral cavity. Basic Clin. Pharmacol. Toxicol. 2004, 95, 191-200.
21. Schuck, A.G.; Ausubel, M.B.; Zuckerbraun, H.L.; Babich, H. Theaflavin-3,3'-digallate, a component of black tea: an inducer of oxidative stress and apoptosis. Toxicol. In Vitro 2008, 22, 598-609.
22. Lee, K.W.; Hur, H.J.; Lee, H.J.; Lee, C.Y. Antiproliferative effects of dietary phenolic substances and hydrogen peroxide. J. Agric. Food Chem. 2005, 54, 7036-7040.
23. Babich, H.; Ackerman, N.J.; Burekhovich, F.; Zuckerbraun, H.L.; Schuck, A.G. Gingko biloba leaf extract induces oxidative stress in carcinoma HSC-2 cells. Toxicol. In Vitro 2009, 23, 992-999.
24. Pelicano, H.; Carney, D.; Huang, P. ROS stress in cancer cells and therapeutic applications. Drug Resist. Updat. 2004, 7, 97-110.
25. Ahmad, N.; Gupta, S.; Mukhtar, H. Green tea polyphenols epigallocatechin-3-gallate differentially modulates nuclear factor κB in cancer cells versus normal cells. Arch. Biochem. Biophys. 2000, 376, 338-346.
26. Hadi, S.M.; Bhat, S.H.; Azmi, A.S.; Hanif, S.; Shamim, U.; Ullah, M.F. Oxidative breakage of cellular DNA by plant polyphenols: a putative mechanism for anticancer properties. Semin. Cancer Biol. 2007, 17, 370-376.
27. Yamamoto, T.; Hsu, S.; Lewis, J.; Wataha, J.; Dickinson, D.; Singh, B.; Bollag, W.B.; Lockwood, P.; Ueta, E.; Osaki, T.; Schuster, G. Green tea polyphenols causes differential oxidative environments in tumor versus normal epithelial cells. J. Pharmacol. Exp. Ther. 2003, 307, 230-236.
28. Borenfreund, E.; Babich, H.; Martin-Alguacil, N. Rapid chemosensitivity assay with normal and tumor cells in vitro. In Vitro Cell. Dev. Biol. 1990, 26, 147-154.
29. Babich, H.; Liebling, E.J.: Burger, R.F.; Zuckerbraun, H.L.; Schuck, A.G. Choice of DMEM, formulated with or without pyruvate, plays an important role in assessing the in vitro cytotoxicity of oxidants and prooxidant nutraceuticals. In Vitro Cell. Dev. Biol. - Anim. 2009, 45, 226-233.
30. Subapriya, R.; Kumaraguruparan, R.; Nagini, S.; Thangavelu, A. Oxidant-antioxidant status in oral precancer and oral cancer patients. Toxicol. Mech. Meth. 2003, 13, 77-81.
31. Chen, Z.P.; Schell, J.B.; Ho, C.-T.; Chen, K.Y. Green tea epigallocatechin gallate shows a pronounced growth inhibitory effect on cancerous cells but not on their normal counterparts. Cancer Lett. 1998, 129, 173-179.
32. 2 during interaction of phenolic compounds and cell culture media. J. Agric. Food Chem., 2002, 50, 3156-3160.
33. Ebling, L.; Weiss, R.-M,; Teufelhofer, O.; Uhl, M.; Knasmueller, S.; Schulte-Hermann, R.; Berger, W.; Micksche, M. Green tea extract and (-)-epigallocatechin-3-gallate, the major tea catechin, exert oxidant but lack antioxidant activities. FASEB J. 2005, 19, 807-809.
34. Bhat, S.H.; Azmi, A.S.; Hadi, S.M. Prooxidant DNA breakage induced by caffeic acid in human peripheral lymphocytes: involvement of endogenous copper and a putative mechanism for anticancer properties. Toxicol. Appl. Pharmacol. 2007, 218, 249-255.
35. Ruweler, M.; Gulden, M.; Maser, E.; Murias, M.; Seibert, H. Cytotoxic, cytoprotective and antioxidant activities of resveratrol and analogues in C6 astroglioma cells in vitro. Chem.-Biol. Int., 2009, 182, 128-135.
36. Seeram, N.P.; Zhang, Y.; McKeever, R.; Henning, S.M.; Lee, R.; Suchard, M.A.; Li, Z.; Chen, S.; Thames, G.; Zerlin, A.; Nguyen, M.; Wang, D.; Dreher, M.; Heber, D. Pomegranate juice and extracts provide similar levels of plasma and urinary ellagitannin metabolites in human subjects. J. Med. Food 2008, 11, 390-394.
37. Long, L.H.; Clement, M.V.; Halliwell, B. Artifacts in cell culture: rapid generation of hydrogen peroxide on addition of (-)-epigallocatechin, (-)-epigallocatechin gallate, (+)-catechin, and quercetin to commonly used cell culture media. Biochem. Biophys. Res. Commun., 2000, 273, 50-53.
38. Nath, K.A.; Enright, H.; Nutter, L.; Fischereder, M.; Zou, J.N.; Hebbel, R.P. Effect of pyruvate on oxidant injury to isolated and cellular DNA. Kidney Intern. 1994, 45, 166-176.
39. Babich, H.; Gottesman, R.T.; Liebling, E.J.; Schuck, A.G. Theaflavin-3-gallate and theaflavin-3'-gallate, polyphenols in black tea with prooxidant properties. Basic Clin. Pharmacol. Toxicol., 2008, 103, 66-74.
40. Sakagami, H.; Arakawa, H.; Maeda, M.; Satoh, K.; Kadofuku, T.; Fukuchi, K.; Gomi, K. Production of hydrogen peroxide and methionine sulfoxide by epigallocatechin gallate and antioxidants. Anticancer Res. 2001, 21, 2633-2642.
41. Hong, J.; Lu, H.; Meng, X.; Ryu, J.H.; Hara, Y.; Yang, C.S. Stability, cellular uptake, biotransformation, and efflux of tea polyphenols (-)-epigallocatechin-3-gallate in HT-29 human colon HT29 adenocarcinoma cells. Cancer Res. 2002, 62, 7241-7246.
42. Raza, H.; John, A. Green tea polyphenols epigallocatechin-3-gallate differentially modulates oxidative stress in PC12 cell compartments. Toxicol. Appl. Pharmacol. 2005, 207, 212-220.
43. He, J.; Lin, J.L.; Li, J.; Zhang, J.-H.; Sun, X.-M.; Zeng, C.-M. Dual effects of Ginkgo biloba leaf extract on human red blood cells. Basic Clin. Pharmacol. Toxicol., 2008, 104, 138-144.
44. Awasthi, Y.; Garg, H.S.; Dao, D.D.; Partridge, C.A.; Srivastava, S.K. Enzymatic conjugation of erythrocyte glutathione with 1-chloro-2,4-dinitrobezene: the fate of glutathione conjugate in erythrocytes and the effect of glutathione depletion on hemoglobin. Blood 1981, 58, 733-738.
45. Furukawa, A.; Oikawa, S.; Murata, Y.; Hiraku, Y.; Kawanishi, S. (-)-Epigallocatechin gallate causes oxidative damage to isolated and cellular DNA. Biochem. Pharmacol. 2003, 66, 1769-1778.
46. Eberhardt, M.K.; Santos, C.; Soto, M.A. Formation of hydroxyl radicals and Co2+ in the reaction of Co2+-EDTA with hydrogen peroxide. Catalytic effect of Fe3+. Biochem. Biophys. Acta 1993, 1157, 102-106.
47. Ishino, A.; Kusama, K.; Watanabe, S.; Sakagami, H. Inhibition of epigallocatechin gallate-induced apoptosis by CoCl2 in human oral tumor cell lines. Anticancer Res., 1999, 19, 5197-5201.
48. Simon, H.U.; Haj-Yehia, A.; Levi-Schaffer, F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5, 415-418.
49. Nakazato, T.; Ito, K.; Miyakawa, Y.; Kinjo, K.; Yamada, T.; Hozumi, N.; Ikeda, Y.; Kizaki, M. Catechin, a green tea component, rapidly induces apoptosis of myeloid leukemic cells via modulation of reactive oxygen species production in vitro and inhibits tumor growth in vivo. Haematologica 2005, 90, 317-325.
50. 2 production in transformed and nontransformed human bronchial cell lines: possible mechanisms of cell growth and apoptosis induction. Carcinogenesis 2000, 21, 2035-2039.
51. Babich, H.; Krupka, M.E.; Nissim, H.A.; Zuckerbraun, H.L. Differential in vitro cytotoxicity of (-)-epicatechin gallate (ECG) to cancer and normal cells from the human oral cavity. Toxicol. In Vitro 2005, 19, 233-242.
52. Larrosa, M.; Tomas-Barberan, F.A.; Espin, J.C. The dietary hydrolysable tannin punicalagin releases ellagic acid that induces apoptosis in human colon adenocarcinoma Caco-2 cells by using the mitochondrial pathway. J. Nutr. Biochem. 2006, 17, 611-625.
53. Edderkaoul, M.; Odinokova, I.; Ohno, I.; Gukovsky, I.; Go, V.L.W.; Pandol, S.J.; Gukovskaya, A.S. Ellagic acid induces apoptosis through inhibition of nuclear factor κB in pancreatic cancer cells. World J. Gastroenterol. 2008, 14, 3672-3680.
54. Kasimsetty, S.G.; Bialonska, D.; Reddy, M.K.; Ma, G.; Khan, S.I.; Ferreira, D. Colon cancer chemopreventive activities of pomegranate ellagitannins and urolithins. J. Agric. Food Chem. 2010, 58, 2180-2187.
55. Jeune, M.A.L.; Kumi-Diaka, J.; Brown, J. Anticancer activities of pomegranate extracts and genistein in human breast cancer cells. J. Med. Food 2005, 8, 469-475.
56. Malik, A.; Afaq, F.; Sarfaraz, S.; Vaqar, M.; Adhami, M.; Syed, N.: Mukhtar, H. Pomegranate fruit juice for chemoprevention and chemotherapy of prostate cancer. Proc. Natl. Acad. Sci. USA 2005, 102, 14813-18818.
57. Lambert, J.D.; Kwon, S.J.; Hong, J.; Yang, C.S. Salivary hydrogen peroxide produced by holding or chewing green tea leaves in the oral cavity Free Radic. Res., 2007, 41,850-853.
58. Lambert, J.D.; Elias, R.J. The antioxidant and pro-oxidant activities of green tea polyphenols: a role in cancer prevention. Arch. Biochem. Biophys. Jun 15. [Epub ahead of print] doi:10.1016/ j.abb.2010.06.013.
59. Gil, M.I.; Tomas-Barberan, F.A.; Hess-Pierce, B.; Holcroft, D.M.; Kader, A.A. Antioxidant activity of pomegranate juice and its relationship with phenolic composition and processing. J. Agric. Food Chem. 2000, 48, 4581-4589.
60. Kim, J.W.; Amin, R.A.R.M.; Shin, D.M. Chemoprevention of head and neck cancer with green tea polyphenols. Cancer Prev. Res. 2010, 3, 900-909.