Genipin-induced apoptosis in hepatoma cells is mediated by reactive oxygen species/c-Jun NH2-terminal kinase-dependent activation of mitochondrial pathway

Biochemical Pharmacology

Volumn 70, Issue 9, 2005, Pages 1398-1407

  Kim, Byung Chul ^a   Kim, Hong Gyum ^a   Lee, Sin Ae ^a   Lim, Seunghwan ^c   Park, Eun Hee ^b   Kim, Seong Jin ^c   Lim, Chang Jin ^a  

^a Kangwon National University   (South Korea)

^b Sookmyung Women's University   (South Korea)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Apoptosis; Caspase; Genipin; Mitochondria; NADPH oxidase; Reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CASPASE; CASPASE 3; CASPASE 7; CASPASE 9; CYTOCHROME C; DIPHENYLIODONIUM SALT; GENIPIN; GENIPOSIDE; GLUTATHIONE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CARCINOMA CELL; CELL DEATH; CELL STRUCTURE; CONTROLLED STUDY; DRUG ACTIVITY; ENZYME ACTIVATION; ENZYME INHIBITION; GENETIC TRANSFECTION; HEPATOMA CELL; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT;

ANIMALS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CASPASES; CELL LINE; HUMANS; IRIDOIDS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE 8; NADPH OXIDASE; PYRANS; RATS; REACTIVE OXYGEN SPECIES;

EID: 25644457401     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2005.07.025     Document Type: Article

References (54)

1. T. Akao, K. Kobayashi, and M. Aburada Enzymic studies on the animal and intestinal bacterial metabolism of geniposide Biol Pharm Bull 17 1994 1573 1576
2. W.H. Kuo, C.J. Wang, S.C. Young, Y.C. Sun, Y.J. Chen, and F.P. Chou Differential induction of the expression of GST subunits by geniposide in rat hepatocytes Pharmacology 70 2004 15 22
3. H.-J. Koo, S. Lee, K.-H. Shin, B.-C. Kim, C.-J. Lim, and E.-H. Park Geniposide, an anti-angiogenic compound from the fruits of Gardenia jasminoides Planta Med 70 2004 467 469
4. Y.-C. Chang, F.-P. Chou, H.-P. Huang, J.-D. Hsu, and C.-J. Wang Inhibition of cell cycle progression by penta-acetyl geniposide in rat C6 glioma cells Toxicol Appl Pharmacol 198 2004 11 20
5. C.-H. Peng, T.-H. Tseng, J.-Y. Liu, Y.H. Hsieh, C.N. Huang, and S.P. Hsu Penta-acetyl geniposide-induced C6 glioma cell apoptosis was associated with activation of protein kinase C-delta Chem Biol Interact 147 2004 287 296
6. M. Yamazaki, K. Chiba, T. Mohri, and M. Hatanaka Activation of the mitogen-activated kinase cascade through nitric oxide synthesis as a mechanism of neuritogenic effect of genipin in PC12h cells J Neurochem 79 2001 45 54
7. M. Yamazaki, K. Chiba, T. Mohri, and H. Hatanaka Cyclic GMP-dependent neurite outgrowth by genipin and nerve growth factor in PC12h cells Eur J Pharmacol 488 2004 35 43
8. H.-J. Koo, Y.S. Song, H.-J. Kim, Y.H. Lee, S.M. Hong, and S.J. Kim Antiinflammatory effects of genipin, an active principle of gardenia Eur J Pharmacol 495 2004 201 208
9. J. Nordberg, and E.S. Arner Reactive oxygen species, antioxidants, and the mammalian thioredoxin system Free Radic Biol Med 31 2001 1287 1312
10. E. Cadenas, and K.J.A. Davies Mitochondrial free radical generation, oxidative stress, and aging Free Radic Biol Med 29 2000 222 230
11. J.M. McCord Human diseases, free radicals, and the oxidant/antioxidant balance Clin Biochem 26 1993 351 357
12. D.-Y. Shi, Y.-R. Deng, S.-L. Liu, Y.-D. Zhang, and L. Wei Redox stress regulates cell proliferation and apoptosis of human hepatoma through Akt protein phosphorylation FEBS Lett 542 2003 60 64
13. A.K. Bhunia, G. Schwarzmann, and S. Chatterjee GD3 recruits reactive oxygen species to induce cell proliferation and apoptosis in human aortic smooth muscle cells J Biol Chem 277 2002 16396 16402
14. A.M. Di Pietrantonio, T. Hsieh, and J.M. Wu Activation of caspase-3 in HL-60 cells exposed to hydrogen peroxide Biochem Biophys Res Commun 255 1999 477 482
15. G. Simbula, M. Pibiri, L. Sanna, C. Cossu, F. Molotzu, and A. Columbano The peroxisome proliferators BR931 kills FaO cells by p53-dependent apoptosis Life Sci 75 2004 271 286
16. R.J. Carmody, and T.G. Cotter Signaling apoptosis: a radical approach Redox Rep 6 2001 77 90
17. B.M. Babior Activation of the respiratory burst oxidase Environ Health Perspect 102 1994 53 56
18. Y. Kasahara, K. Iwai, A. Yachie, K. Ohta, A. Konno, and H. Seki Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/Apo-1)-mediated apoptosis of neutrophils Blood 89 1997 1748 1753
19. W. Hiraoka, N. Vazquez, W. Nieves-Neira, S.J. Chanock, and Y. Pommier Role of oxygen radicals generated by NADPH oxidase in apoptosis induced in human leukemia cells J Clin Invest 102 1998 1961 1968
20. B.M. Babior NADPH oxidase Blood 93 1999 1464 1476
21. 2 Mol Cell Biol 24 2004 4384 4394
22. phox participate in activation of superoxide-producing NADPH oxidase J Biol Chem 278 2003 25234 25246
23. V. Gurtu, S.R. Kain, and G. Zhang Fluorimetric and colorimetric detection of caspase activity associated with apoptosis Anal Biochem 251 1997 98 102
24. B. Chelli, A. Lena, R. Vanacore, E.D. Pozzo, B. Costa, and L. Rossi Peripheral benzodiazephine receptor ligands: mitochondrial transmembrane potential depolarization and apoptosis induction in rat C6 glioma cells Biochem Pharmacol 68 2004 125 134
25. B.-C. Kim, M. Mamura, K.S. Choi, B. Calabretta, and S.-J. Kim Transforming growth factor beta 1 induces apoptosis through cleavage of BAD in a Smad3-dependent mechanism in FaO hepatoma cells Mol Cell Biol 22 2002 1369 1378
26. 2 in cultured endothelial cells Arch Biochem Biophys 302 1993 348 355
27. F. Kugawa, K. Matsumoto, and M. Aoki Apoptosis-like cell death of human breast cancer cell line MCF-7 induced by buprenorphine hydrochloride Life Sci 75 2004 287 299
28. B. Halliwell, and M. Whiteman Measuring reactive oxygen species and oxidative damage in vivo and cell culture. How should you do it and what do the results mean? Br J Pharmacol 142 2004 231 255
29. A.J. Freemerman, A.J. Turner, M.J. Birrer, E. Szabo, K. Valerie, and S. Grant Role of c-Jun in human myeloid leukemia cell apoptosis induced by pharmacological inhibitors of protein kinase C Mol Pharmacol 49 1996 788 795
30. C. Rust, and G.J. Gores Apoptosis and liver disease Am J Med 108 2000 567 574
31. Y.-C. Chang, T.-H. Tseng, M.-J. Lee, J.-D. Hsu, and C.-J. Wang Induction of apoptosis by penta-acetyl geniposide in rat C6 glioma cells Chem Biol Interact 141 2002 243 257
32. C.H. Ko, S.-C. Shen, C.-S. Hsu, and Y.-C. Chen Mitochondrial-dependent, reactive oxygen species-independent apoptosis by myricetin: role of protein kinase C, cytochrome c, and caspase cascade Biochem Pharmacol 69 2005 913 927
33. 2-induced apoptosis via anti-oxidant activity and heme oxygenase 1 gene expression in macrophages Biochem Pharmacol 69 2005 1839 1851
34. X. Jiang, and X. Wang Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to Apaf-1 J Biol Chem 275 2000 31199 31203
35. H. Kamata, and H. Hirata Redox regulation of cellular signaling Cell Signal 11 1999 1 14
36. 2-induced cell death Eur J Pharmacol 483 2004 163 173
37. J.H. Woo, Y.H. Kim, Y.J. Choi, D.G. Kim, K.S. Lee, and J.H. Bae Molecular mechanisms of curcumin-induced cytotoxicity: induction of apoptosis through generation of reactive oxygen species, down-regulation of Bcl-XL and IAP, the release of cytochrome c and inhibition of Akt Carcinogen 24 2003 1199 1208
38. D. Li, E. Ueta, T. Kimura, T. Yamamoto, and T. Osaki Reactive oxygen species (ROS) control the expression of Bcl-2 family proteins by regulating their phosphorylation and ubiquitination Cancer Sci 95 2004 644 650
39. W.-X. Guo, Q.N. Pye, K.S. Williamson, C.A. Stewart, K.L. Hensley, and Y. Kotake Reactive oxygen species in choline deficiency-induced apoptosis in rat hepatocytes Free Radic Biol Med 37 2004 1081 1089
40. B.V. Pardhasaradhi, A.M. Ali, A.L. Kumari, P. Reddanna, and A. Khar Phycocyanin-mediated apoptosis in AK-5 tumor cells involves down-regulation of Bcl-2 and generation of ROS Mol Cancer Ther 2 2003 1165 1170
41. T. Pararetakis, I.G. Shabalina, D. Grandér, M.C. Shoshan, and J.W. DePierre Reactive oxygen species and mitochondrial mediate the induction of apoptosis in human hepatoma HepG2 cells by the rodent peroxisome proliferators and hepatocarcinogen, perfluorooctanoic acid Toxicol Appl Pharmacol 173 2001 56 64
42. L. Chang, and M. Karin Mammalian MAP kinase signaling cascade Nature 410 2001 37 40
43. G.L. Johnson, and R. Lapadat Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases Science 298 2002 1911 1912
44. X. Wang, J.L. Martindale, and N.J. Holbrook Requirement for ERK activation in cisplatin-induced apoptosis J Biol Chem 275 2000 39435 39443
45. J. Raingeaud, S. Gupta, J.S. Rogers, M. Dickens, J. Han, and R.J. Ulevitch Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine J Biol Chem 270 1995 7420 7426
46. A. Minden, and M. Karin Regulation and function of the JNK subgroup of MAP kinases Biochim Biophys Acta 1333 1997 F85 F104
47. C. Communal, W.S. Colucci, and K. Singh p38 mitogen-activated protein kinase pathway protects adult rat ventricular myocytes against beta-adrenergic receptor-stimulated apoptosis. Evidence for Gi-dependent activation J Biol Chem 275 2000 19395 19400
48. B. Liu, M. Fang, Y. Lu, G.B. Mills, and Z. Fan Involvement of JNK1/2-mediated pathway in EGF-mediated protection against paclitaxel-induced apoptosis in SiHa human cervical cancer cells Br J Cancer 85 2001 303 311
49. M. Benhar, I. Dalyot, D. Engelberg, and A. Levitzki Enhanced ROS production in oncogenically transformed cells potentiates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase activation and sensitization to genotoxic stress Mol Cell Biol 21 2001 6913 6926
50. X. Zhang, P. Shan, M. Sasidhar, G.L. Chupp, R.A. Flavell, and A.M. Choi Reactive oxygen species and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase mediates hyperoxia-induced cell death in lung epithelium Am J Respir Cell Mol Biol 28 2003 305 315
51. E. Pedruzzi, C. Guichard, V. Ollivier, F. Driss, M. Fay, and C. Prunet NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells Mol Cell Biol 24 2004 10703 10717
52. S. Sim, T.-S. Yong, S.-J. Park, K. Im, Y. Kong, and J.-S. Ryu NADPH oxidase-derived reactive oxygen species-mediated activation of ERK1/2 is required for apoptosis of human neutrophil induced by Entamoeba histolytica J Immunol 174 2005 4279 4288
53. E.C. Vaquero, M. Edderkaoui, S.J. Pandol, I. Gukovsky, and A.S. Gukovskaya Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells J Biol Chem 279 2004 34643 34654
54. M. Yamamoto, N. Miura, N. Ohtake, S. Amagaya, A. Ishige, and H. Sasaki Genipin, a metabolite derived from the herbal medicine Inchin-ko-to, and suppression of Fas-induced lethal liver apoptosis in mice Gastroenterology 118 2000 380 389