Involvement of reactive oxygen species and caspase-dependent pathway in berberine-induced cell cycle arrest and apoptosis in C6 rat glioma cells

International Journal of Oncology

Volumn 34, Issue 6, 2009, Pages 1681-1690

  Chen, Ting Ching ^a   Lai, Kuang Chi ^b,c   Yang, Jai Sing ^a   Liao, Ching Lung ^a   Hsia, Te Chun ^d   Chen, Guang Wei ^e   Lin, Jen Jyh ^a   Lin, Hui Ju ^a   Chiu, Tsan Hung ^a   Tang, Yih Jing ^f   Chung, Jing Gung ^a,g  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY BEIGANG HOSPITAL   (Taiwan)

^d CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^f TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^g ASIA UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Berberine; Cytochrome c; Mitochondria membrane potential; Reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; BERBERINE; CALCIUM ION; CASPASE; CASPASE 3; CASPASE 3 INHIBITOR; CASPASE 8; CASPASE 8 INHIBITOR; CASPASE 9; CASPASE 9 INHIBITOR; CYCLIN B; CYCLIN DEPENDENT KINASE 1; CYTOCHROME C; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; PROTEIN BAX; PROTEIN BCL 2; PROTEIN TYROSINE PHOSPHATASE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL STRESS; CELL STRUCTURE; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG PROTEIN BINDING; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME RELEASE; FLOW CYTOMETRY; GLIOMA CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BERBERINE; BLOTTING, WESTERN; CALCIUM; CASPASES; CELL DIVISION; CELL LINE, TUMOR; CYTOCHROMES C; DNA DAMAGE; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; FLOW CYTOMETRY; G2 PHASE; GLIOMA; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; REACTIVE OXYGEN SPECIES;

EID: 67649415924     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000299     Document Type: Article

References (38)

1. Tan S, Sagara Y, Liu Y, Maher P and Schubert D: The regulation of reactive oxygen species production during programmed cell death. J Cell Biol 141: 1423-1432, 1998.
2. Ikeda K, Kajiwara K, Tanabe E, et al: Involvement of hydrogen peroxide and hydroxyl radical in chemically induced apoptosis of HL-60 cells. Biochem Pharmacol 57: 1361-1365, 1999.
3. Muller I, Niethammer D and Bruchelt G: Anthracycline-derived chemotherapeutics in apoptosis and free radical cytotoxicity (Review). Int J Mol Med 1: 491-494, 1998.
4. Kroemer G and de The H: Arsenic trioxide, a novel mitochondriotoxic anticancer agent? J Natl Cancer Inst 91: 743-745, 1999.
5. Craig WJ: Health-promoting properties of common herbs. Am J Clin Nutr 70: 491S-499S, 1999.
6. Craig WJ: Phytochemicals: guardians of our health. J Am Diet Assoc 97: S199-S204, 1997.
7. Seth SD and Sharma B: Medicinal plants in India. Indian J Med Res 120: 9-11, 2004.
8. Fukuda K, Hibiya Y, Mutoh M, Koshiji M, Akao S and Fujiwara H: Inhibition of activator protein 1 activity by berberine in human hepatoma cells. Planta Med 65: 381-383, 1999.
9. Takase H, Yamamoto K, Ito K and Yumioka E: Pharmacological studies on antidiarrheal effects of berberine and geranii herba. Nippon Yakurigaku Zasshi 102: 101-112, 1993.
10. Huang WM, Wu ZD and Gan YQ: Effects of berberine on ischemic ventricular arrhythmia. Zhonghua Xin Xue Guan Bing Za Zhi 17: 300-3319, 1989.
11. Fukuda K, Hibiya Y, Mutoh M, Koshiji M, Akao S and Fujiwara H: Inhibition by berberine of cyclooxygenase-2 transcriptional activity in human colon cancer cells. J Ethnopharmacol 66: 227-233, 1999.
12. Lin JG, Chung JG, Wu LT, Chen GW, Chang HL and Wang TF: Effects of berberine on arylamine N-acetyltransferase activity in human colon tumor cells. Am J Chin Med 27: 265-275, 1999.
13. Nishino H, Kitagawa K, Fujiki H and Iwashima A: Berberine sulfate inhibits tumor-promoting activity of teleocidin in two-stage carcinogenesis on mouse skin. Oncology 43: 131-134, 1986.
14. Kim SA, Kwon Y, Kim JH, Muller MT and Chung IK: Induction of topoisomerase II-mediated DNA cleavage by a protoberberine alkaloid, berberrubine. Biochemistry 37: 16316-16324, 1998.
15. Wang LK, Rogers BD and Hecht SM: Inhibition of topoisomerase I function by coralyne and 5,6-dihydrocoralyne. Chem Res Toxicol 9: 75-83, 1996.
16. Mantena SK, Sharma SD and Katiyar SK: Berberine inhibits growth, induces G1 arrest and apoptosis in human epidermoid carcinoma A431 cells by regulating Cdki-Cdk-cyclin cascade, disruption of mitochondrial membrane potential and cleavage of caspase 3 and PARP. Carcinogenesis 27: 2018-2027, 2006.
17. Yu FS, Yang JS, Lin HJ, et al: Berberine inhibits WEHI-3 leukemia cells in vivo. In Vivo 21: 407-412, 2007.
18. Lin CC, Yang JS, Chen JT, et al: Berberine induces apoptosis in human HSC-3 oral cancer cells via simultaneous activation of the death receptor-mediated and mitochondrial pathway. Anticancer Res 27: 3371-3378, 2007.
19. Lin JP, Yang JS, Wu CC, et al: Berberine induced down-regulation of matrix metalloproteinase-1, -2 and -9 in human gastric cancer cells (SNU-5) in vitro. In Vivo 22: 223-230, 2008.
20. Lin SS, Huang HP, Yang JS, et al: DNA damage and endoplasmic reticulum stress mediated curcumin-induced cell cycle arrest and apoptosis in human lung carcinoma A-549 cells through the activation caspases cascade- and mitochondrial-dependent pathway. Cancer Lett (In prss).
21. 2+ in baicalein-induced apoptosis in human breast MDA-MB-231 cancer cells through mitochondria- and caspase-3-dependent pathway. Anticancer Res 28: 1701-1711, 2008.
22. 2+-dependent mitochondrial pathway. In Vivo 21: 1053-1058, 2007.
23. Wang SC, Chung JG, Chen CH and Chen SC: 2- and 4-Aminobiphenyls induce oxidative DNA damage in human hepatoma (Hep G2) cells via different mechanisms. Mutat Res 593: 9-21, 2006.
24. Chen JC, Lu KW, Tsai ML, et al: Gypenosides induced G0/G1 arrest via CHk2 and apoptosis through endoplasmic reticulum stress and mitochondria-dependent pathways in human tongue cancer SCC-4 cells. Oral Oncol 45: 273-283, 2009.
25. Chuang JY, Tsai YY, Chen SC, Hsieh TJ and Chung JG: Induction of G0/G1 arrest and apoptosis by 3-hydroxycinnamic acid in human cervix epithelial carcinoma (HeLa) cells. In Vivo 19: 683-688, 2005.
26. Pasqual MS, Lauer CP, Moyna P and Henriques JA: Genotoxicity of the isoquinoline alkaloid berberine in prokaryotic and eukaryotic organisms. Mutat Res 286: 243-252, 1993.
27. Ihmels H, Faulhaber K, Vedaldi D, Dall'Acqua F and Viola G: Intercalation of organic dye molecules into double-stranded DNA. Part 2: the annelated quinolizinium ion as a structural motif in DNA intercalators. Photochem Photobiol 81: 1107-1115, 2005.
28. Li TK, Bathory E, LaVoie EJ, et al: Human topoisomerase I poisoning by protoberberines: potential roles for both drug-DNA and drug-enzyme interactions. Biochemistry 39: 7107-7116, 2000.
29. Krey AK and Hahn FE: Berberine: complex with DNA. Science 166: 755-757, 1969.
30. Davidson MW, Lopp I, Alexander S and Wilson WD: The interaction of plant alkaloids with DNA. II. Berberinium chloride. Nucleic Acids Res 4: 2697-2712, 1977.
31. Makhey D, Gatto B, Yu C, Liu A, Liu LF and LaVoie EJ: Coralyne and related compounds as mammalian topoisomerase I and topoisomerase II poisons. Bioorg Med Chem 4: 781-791, 1996.
32. Gatto B, Sanders MM, Yu C, et al: Identification of topoisomerase I as the cytotoxic target of the protoberberine alkaloid coralyne. Cancer Res 56: 2795-2800, 1996.
33. Kobayashi Y, Yamashita Y, Fujii N, et al: Inhibitors of DNA topoisomerase I and II isolated from the Coptis rhizomes. Planta Med 61: 414-418, 1995.
34. Zhang RX, Dougherty DV and Rosenblum ML: Laboratory studies of berberine used alone and in combination with 1,3-bis (2-chloroethyl)-1-nitrosourea to treat malignant brain tumors. Chin Med J (Engl) 103: 658-665, 1990.
35. Lin JP, Yang JS, Lee JH, Hsieh WT and Chung JG: Berberine induces cell cycle arrest and apoptosis in human gastric carcinoma SNU-5 cell line. World J Gastroenterol 12: 21-28, 2006.
36. Lin CC, Lin SY, Chung JG, Lin JP, Chen GW and Kao ST: Down-regulation of cyclin B1 and up-regulation of Wee1 by berberine promotes entry of leukemia cells into the G2/M-phase of the cell cycle. Anticancer Res 26: 1097-1104, 2006.
37. Payne SR, Zhang S, Tsuchiya K, et al: p27kip1 deficiency impairs G2/M arrest in response to DNA damage, leading to an increase in genetic instability. Mol Cell Biol 28: 258-268, 2008.
38. Foijer F, Delzenne-Goette E, Dekker M and Te Riele H: In vivo significance of the G2 restriction point. Cancer Res 67: 9244-9247, 2007.