Tea polyphenols induce apoptosis through mitochondrial pathway and by inhibiting nuclear factor-κB and Akt activation in human cervical cancer cells

Oncology Research

Volumn 19, Issue 6, 2011, Pages 245-257

  Singh, Madhulika ^a   Singh, Richa ^a   Bhui, Kulpreet ^a   Tyagi, Shilpa ^a   Mahmood, Zafar ^a   Shukla, Yogeshwer ^a  

^a CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

Author keywords

Akt; Apoptosis; Cervical cancer; Cyclooxygenase 2; Nuclear factor B (NF B); Tea polyphenols

Indexed keywords

CYCLIN D1; CYCLOOXYGENASE 2; CYTOCHROME C; EPIGALLOCATECHIN GALLATE; GLUTATHIONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROCASPASE 3; PROCASPASE 9; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN P53; THEAFLAVIN; BIFLAVONOID; CATECHIN; DRUG DERIVATIVE; FLAVONOID; PHENOL DERIVATIVE; POLYPHENOLS; REACTIVE OXYGEN METABOLITE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 18; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TEA; TREATMENT OUTCOME; UTERINE CERVIX CANCER; CELL CYCLE; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; MITOCHONDRION; TIME; TUMOR CELL CULTURE; WESTERN BLOTTING;

APOPTOSIS; BIFLAVONOIDS; BLOTTING, WESTERN; CATECHIN; CELL CYCLE; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FLAVONOIDS; HELA CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NF-KAPPA B; PHENOLS; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; TEA; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 80051621155     PISSN: 09650407     EISSN: None     Source Type: Journal    
DOI: 10.3727/096504011X13021877989711     Document Type: Article

References (49)

1. Suba, E. J.; Cibas, E. S.; Raab, S. S. HPV screening for cervical cancer in rural India. N. Engl. J. Med. 361(3): 304; 2009.
2. Hougardy, B. M.; Maduro, J. H.; van der Zee, A. G.; Willemse, P. H.; de Jong, S.; de Vries, E. G. Clinical potential of inhibitors of survival pathways and activators of apoptotic pathways in treatment of cervical cancer: Changing the apoptotic balance. Lancet Oncol. 6:589-598; 2005.
3. Liu, R. H. Potential synergy of phytochemicals in cancer prevention: Mechanism of action. J. Nutr. 134:3479S-3485S; 2004.
4. Thomasset, S. C.; Berry, D. P.; Garcea, G.; Marczylo, T.; Steward, W. P.; Gescher, A. J. Dietary polyphenolic phytochemicals-promising cancer chemopreventive agents in humans? A review of their clinical properties. Int. J. Cancer 120(3):451-458; 2007.
5. Baliga, M. S.; Meleth, S.; Katiyar, S. K. Growth inhibitory and antimetastatic effect of green tea polyphenols on metastasis- specific mouse mammary carcinoma 4T1 cells in vitro and in vivo systems. Clin. Cancer Res. 11:1918-1927; 2005.
6. Kondo, T.; Ohta, T.; Igura, K.; Hara, Y.; Kaji, K. Tea catechins inhibit angiogenesis in vitro, measured by human endothelial cell growth, migration and tube formation, through inhibition of VEGF receptor binding. Cancer Lett. 180:139-144; 2002.
7. Singh, M.; Tyagi, S.; Bhui, K.; Prasad, S.; Shukla, Y. Regulation of cell growth through cell cycle arrest and apoptosis in HPV 16 positive human cervical cancer cells by tea polyphenols. Invest. New Drugs 28(3):216-224; 2010.
8. Yang, C. S. Inhibition of carcinogenesis by tea. Nature 389:134-135; 1997.
9. Levin, A. J. p53, the cellular gatekeeper for growth and division. Cell 88:323-331; 1997.
10. Miyashita, T.; Reed, J. C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80(2):293-299; 1995.
11. Bickers, D. R.; Athur, M. Novel approaches to chemo-aprevention of skin cancer. J. Dermatol. 27:691-695; 2000.
12. Wang, W.; Abbruzzese, J. L.; Evans, D. B.; Larry, L.; Cleary, K. R.; Chiao, P. J. The nuclear factor-kB RelA transcription factor is constitutively activated in human pancreatic adenocarcinoma cells. Clin. Cancer Res. 5: 119-127; 1999.
13. Liptay, S.; Weber, C. K.; Ludwig, L.; Wagner, M.; Adler, G.; Schmid, R. M. Mitogenic and antiapoptotic role of constitutive NF-kB/Rel activity in pancreatic cancer. Int. J. Cancer 105:735-746; 2003.
14. Perkins, N. D. The Rel/NF-kB family: Friend and foe. Trends Biochem. Sci. 25:434-440; 2000.
15. Baldwin, Jr., A. S. The NF-kB and IkB proteins: New discoveries and insights. Annu. Rev. Immunol. 14:649-683; 1996.
16. Gutteridge, D. C.; Albanese, C.; Reuther, J. Y.; Pestell, R. G.; Baldwin, Jr., A. S. NF-kB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol. Cell Biol. 19:5785-5799; 1999.
17. Kim, Y.; Fischer, S. M. Transcriptional regulation ofcyclooxygenase-2 in mouse skin carcinoma cells. Regulatory role of CCAAT/enhancer-binding proteins in the differential expression of cyclooxygenase-2 in normal and neoplastic tissues. J. Biol. Chem. 273:27686-27694; 1998.
18. Prusty, B. K.; Husain, S. A.; Das, B. C. Constitutive activation of nuclear factor-kB: Preferential homodimerization of p50 subunits in cervical carcinoma. Front. Biosci. 10:1510-1519; 2005.
19. Dai, Y.; Zhang, X.; Peng, Y.; Wang, Z. The expression of cyclooxygenase-2, VEGF and PGs in CIN and cervical carcinoma. Gynecol. Oncol. 97:96-103; 2005
20. Silverman, N.; Maniatis, T. NF-kappaB signaling pathways in mammalian and insect innate immunity. Genes Dev. 15(18):2321-2342; 2001.
21. Choi, E. K.; Jang, H. C.; Kim, J. H.; Kang, H. C.; Paek, Y. W. Enhancement of cytokine-mediated NF-kappa B activation by phosphatidylinositol 3-kinase inhibitors in monocytic cells. Int. Immunopharmacol. 6:908-915; 2006.
22. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxic assays. J. Immunol. Methods 65:55-63; 1983.
23. Hu, R.; Kim, B. R.; Chen, C.; Hebbar, V.; Kong, A. N. The role of JNK and apoptotic signaling pathways in PEITC-mediated responses in human HT-29 colon adenocarcinoma cell. Carcinogenesis 24:1361-1367; 2003.
24. Chen, C. Y.; Liu, T. Z.; Liu, Y. W.; Tseng, W. C.; Liu, R. H.; Lu, F. J.; Lin, Y. S.; Chen, C. H. 6-Shogaol (alkanone from ginger) induces apoptotic cell death of human hepatoma p53 mutant Mahlavu subline via an oxidative stress-mediated caspase-dependent mechanism. J. Agric. Food Chem. 55:948-954; 2007.
25. Cossarizza, A.; Ceccarelli, D.; Masini, A. Functional heterogeneity of an isolated mitochondrial population revealed by cytofluorometric analysis at the single organelle level. Exp. Cell Res. 222:84-94; 1996.
26. Siddiqui, I. A.; Adhami, V. M.; Afaq, F.; Ahmad, N.; Mukhtar, H. Modulation of phosphatidylinositol-3-kinase/ protein kinase B- and mitogen-activated protein kinase- pathways by tea polyphenols in human prostate cancer cells. J. Cell Biochem. 91:232-242; 2004.
27. Lowry, O. H.; Rosenbrough, N. K.; Farr, A. L. Protein measurement with folin phenol reagent. J. Biol. Chem. 193:265-275; 1951.
28. Deeb, D.; Gao, X.; Jiang, H.; Janic, B.; Arbab, A. S.; Rojanasakul, Y.; Dulchavsky, S. A.; Gautam, S. C. Oleanane triterpenoid CDDO-Me inhibits growth and induces apoptosis in prostate cancer cells through a ROS-dependent mechanism. Biochem. Pharmacol. 79:350-360; 2010.
29. Fleury, C.; Mignotte, B.; Vayssiè L. Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84:131-141; 2002.
30. Kroemer, G. Mitochondrial implication in apoptosis. Towards an endosymbiont hypothesis of apoptosis evolution. Cell Death Differ. 4(6):443-456; 1997.
31. Earnshaw, W. C.; Martins, L. M.; Kaufmann, S. H. Mam14. malian caspases: Structure, activation, substrates and functions during apoptosis. Annu. Rev. Biochem. 68:383-424; 1999.
32. Bahnassy, A. A.; Zekri, A. R.; Saleh, M.; Lotayef, M.; Moneir, M.; Shawki, O. The possible role of cell cycle regulators in multistep process of HPV-associated cervical carcinoma. BMC Clin. Pathol. 7:4; 2007.
33. Bhattacharyya, A.; Lahiry, L.; Mandal, D.; Sa, G.; Das, T. Black tea induces tumor cell apoptosis by Bax translocation, loss in mitochondrial transmembrane potential, cytochrome c release and caspase activation. Int. J. Cancer 117:308-315; 2005.
34. Qanungo, S.; Das, M.; Haldar, S.; Basu, A. Epigallocatechin-3-gallate induces mitochondrial membrane depolarization and caspase-dependent apoptosis in pancreatic cancer cells. Carcinogenesis 26:958-967; 2005.
35. Chung, Y. M.; Bae, Y. S.; Lee, S. Y. Molecular ordering of ROS production, mitochondrial changes, and caspase activation during sodium salicylate-induced apoptosis. Free Radic. Biol. Med. 34:434-442; 2003.
36. Hsieh, T. J.; Liu, T. Z.; Lu, F. J.; Hsieh, P. Y.; Chen, C. H. Actinodaphnine induces apoptosis through increased nitric oxide, reactive oxygen species and down-regulation of NF-κB signaling in human hepatoma Mahlavu cells. Food Chem Toxicol. 44:344-354; 2006.
37. Chen, C. H.; Lo, W. L.; Liu, Y. C.; Chen, C. Y. Chemical and cytotoxic constituents from the leaves of Cinnamomum kotoense. J. Nat. Prod. 69:927-933; 2006.
38. Giannkakou, P.; Robey, R.; Fojo, T.; Blagosklonny, M. V. Low concentrations of paclitaxel induce cell type-dependent p53, p21 and G1/G2 arrest instead of mitotic arrest: Molecular determinants of paclitaxel-induced cytotoxicity. Oncogene 20:3806-3813; 2001.
39. Marzo, I.; Brenner, C.; Zamzami, N.; Jürgensmeier, J. M.; Susin, S. A.; Vieira, H. L.; Prévost, M. C.; Xie, Z.; Matsuyama, S.; Reed, J. C.; Kroemer, G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281:2027-2031; 1998.
40. Oltvai, Z. N.; Milliman, C. L.; Korsmeyer, S. J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619; 1993.
41. Bursztajn, S.; Feng, J. J.; Berman, S. A.; Nanda, A. R. Poly (ADP-ribose) polymerase induction is an early signal of apoptosis in human neuroblastoma. Brain Res. Mol. Brain Res. 76:363-376; 2000.
42. Kolthur-Seetharam, U.; Dantzer, F.; McBurney, M. W.; de Murcia, G.; Sassone-Corsi, P. Control of AIF mediatedcell death by the functional interplay of SIRT1 and PARP- 1 in response to DNA damage. Cell Cycle 5:873-877; 2006.
43. Nomura, M.; Ma, W.; Chen, N.; Bode, A. M.; Dong, Z. Inhibition of 12-O-tetradecanoylphorbol-13-acetate-induced NF-kappaB activation by tea polyphenols, (-)-epigallocatechin gallate and theaflavins. Carcinogenesis 21: 1885-1890; 2000.
44. Roy, P.; Nigam, N.; Singh, M.; George, J.; Srivastava, S.; Naqvi, H.; Shukla, Y. Tea polyphenols inhibit cyclooxy-genase-2 expression and block activation of nuclear factor-kappa B and Akt in diethylnitrosoamine induced lung tumors in Swiss mice. Invest. New Drugs 28(4):466-471; 2010.
45. Chang, F.; Lee, J. T.; Navolanic, P. M.; Steelman, L. S.; Shelton, J. G.; Blalock, W. L.; Franklin, R. A.; McCubrey, J. A. Involvement of PI3K/Akt pathway in cell cycle progression, apoptosis, and neoplastic transformation: A target for cancer chemotherapy. Leukemia 17:590-603; 2003.
46. Romashkova, J. A.; Makarov, S. S. NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401:86-90; 1999.
47. Dohadwala, M.; Batra, R. K.; Luo, J.; Lin, Y.; Krysan, K.; Pold, M.; Sharma, S.; Dubinett, S. M. Autocrine/paracrine prostaglandin E2 production by non-small cell lung cancer cells regulates matrix metalloproteinase-2 and CD44 in cyclooxygenase-2-dependent invasion. J. Biol. Chem. 277:50828-50833; 2002.
48. Krysan, K.; Dalwadi, H.; Sharma, S.; P?ld, M.; Dubinett, S. COX-2-dependent stabilization of survivin in non-small cell lung cancer. FASEB J. 18:206-208; 2004.
49. Conesa-Zamora, P.; Doménech-Peris, A.; Orantes-Casado, F. J.; Ortiz-Reina, S.; Sahuquillo-Frías, L.; Acosta-Ortega, J.; García-Solano, J.; Pérez-Guillermo, M. Effect of human papillomavirus on cell cycle-related proteins p16, Ki- 67, Cyclin D1, p53, and ProEx C in precursor lesions of cervical carcinoma: A tissue microarray study. Am. J. Clin. Pathol. 132:378-390; 2009.