Emodin induces apoptosis in human lung adenocarcinoma cells through a reactive oxygen species-dependent mitochondrial signaling pathway

Biochemical Pharmacology

Volumn 70, Issue 2, 2005, Pages 229-241

  Su, Yu Ting ^a   Chang, Huei Ling ^b   Shyue, Song Kun ^c   Hsu, Shih Lan ^a,d,e  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^d TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^e CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Bcl 2 family; Caspase; Cytochrome c; Emodin; ROS

Indexed keywords

ACETYLCYSTEINE; ANTHRAQUINONE DERIVATIVE; ASCORBIC ACID; AURINTRICARBOXYLIC ACID; CASPASE 2; CASPASE 3; CASPASE 9; CASPASE INHIBITOR; CYTOCHROME C; EMODIN; FUROSEMIDE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; DRUG ISOLATION; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHUBARB; SIGNAL TRANSDUCTION; TUMOR REGRESSION;

ADENOCARCINOMA; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; EMODIN; HUMANS; LUNG NEOPLASMS; MITOCHONDRIA; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 20444505248     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2005.04.026     Document Type: Article

References (58)

1. G.C. Chang, K.C. Chen, T.Y. Yang, M.C. Yin, C.P. Lin, and B.I. Kuo Activity of gefitinib in advanced non-small-cell lung cancer with very poor performance status Invest New Drugs 23 2005 73 77
2. A. Carnero Targeting the cell cycle for cancer therapy Br J Cancer 87 2002 129 133
3. X. Jing, N. Ueki, J. Cheng, H. Imanishi, and T. Hada Induction of apoptosis in hepatocellular carcinoma cell lines by emodin Jpn J Cancer Res 93 2002 874 882
4. W. Hu, and J.J. Kavanagh Anticancer therapy targeting the apoptotic pathway Lancet Oncol 4 2003 721 729
5. L.O. Demirezer, A. Kuruuzum-Uz, I. Bergere, H.J. Schiewe, and A. Zeeck The structures of antioxidant and cytotoxic agents from natural source: anthraquinones and tannins from roots of Rumex patientia Phytochemistry 58 2001 1213 1217
6. H.H. Wang, and J.G. Chung Emodin-induced inhibition of growth and DNA damage in the Helicobacter pylori Curr Microbiol 35 1997 262 266
7. C.H. Chang, C.C. Lin, J.J. Yang, T. Namba, and M. Hattori Anti-inflammatory effects of emodin from ventilago leiocarpa Am J Chin Med 24 1996 139 142
8. H.C. Huang, J.H. Chang, S.F. Tung, R.T. Wu, M.L. Foegh, and S.H. Chu Immunosuppressive effect of emodin, a free radical generator Eur J Pharmacol 211 1992 359 364
9. M. Sato, G. Maulik, D. Bagchi, and D.K. Das Myocardial protection by protykin, a novel extract of trans-resveratrol and emodin Free Radic Res 32 2000 135 144
10. R.K. Goel, G. Das Gupta, S.N. Ram, and V.B. Pandey Antiulcerogenic and anti-inflammatory effects of emodin, isolated from Rhamnus triquerta wall Indian J Exp Biol 29 1991 230 232
11. G. Srinivas, R.J. Anto, P. Srinivas, S. Vidhyalakshmi, V.P. Senan, and D. Karunagaran Emodin induces apoptosis of human cervical cancer cells through poly(ADP-ribose) polymerase cleavage and activation of caspase-9 Eur J Pharmacol 473 2003 117 125
12. Y.C. Chen, S.C. Shen, W.R. Lee, F.L. Hsu, H.Y. Lin, and C.H. Ko Emodin induces apoptosis in human promyeloleukemic HL-60 cells accompanied by activation of caspase 3 cascade but independent of reactive oxygen species production Biochem Pharmacol 64 2002 1713 1724
13. L. Zhang, Y.K. Lau, L. Xi, R.L. Hong, D.S. Kim, and C.F. Chen Tyrosine kinase inhibitors, emodin and its derivative repress HER-2/neu-induced cellular transformation and metastasis-associated properties Oncogene 16 1998 2855 2863
14. L. Zhang, C.J. Chang, S.S. Bacus, and M.C. Hung Suppressed transformation and induced differentiation of HER-2/neu-overexpressing breast cancer cells by emodin Cancer Res 55 1995 3890 3896
15. H.Z. Lee Protein kinase C involvement in aloe-emodin- and emodin-induced apoptosis in lung carcinoma cell Br J Pharmacol 134 2001 1093 1103
16. H.Z. Lee Effects and mechanisms of emodin on cell death in human lung squamous cell carcinoma Br J Pharmacol 134 2001 11 20
17. H. Jayasuriya, N.M. Koonchanok, R.L. Geahlen, J.L. McLaughlin, and C.J. Chang Emodin, a protein tyrosine kinase inhibitor from Polygonum cuspidatum J Nat Prod 55 1992 696 698
18. J. Yi, J. Yang, R. He, F. Gao, H. Sang, and X. Tang Emodin enhances arsenic trioxide-induced apoptosis via generation of reactive oxygen species and inhibition of survival signaling Cancer Res 64 2004 108 116
19. L. Zhang, Y.K. Lau, W. Xia, G.N. Hortobagyi, and M.C. Hung Tyrosine kinase inhibitor emodin suppresses growth of HER-2/neu-overexpressing breast cancer cells in athymic mice and sensitizes these cells to the inhibitory effect of paclitaxel Clin Cancer Res 5 1999 343 353
20. P.S. Richards, T.M. Saba, P.J. Del Vecchio, P.A. Vincent, and V.C. Gray Matrix fibronectin disruption in association with altered endothelial cell adhesion induced by activated polymorphonuclear leukocytes Exp Mol Pathol 45 1986 1 21
21. Y.H. Kang, F. Berthiaume, B.D. Nath, and M.L. Yarmush Growth factors and nonparenchymal cell conditioned media induce mitogenic responses in stable long-term adult rat hepatocyte cultures Exp Cell Res 293 2004 239 247
22. Z. Chen, X. Zhang, M. Li, Z. Wang, H.S. Wieand, and J.R. Grandis Simultaneously targeting epidermal growth factor receptor tyrosine kinase and cyclooxygenase-2, an efficient approach to inhibition of squamous cell carcinoma of the head and neck Clin Cancer Res 10 2004 5930 5939
23. S.E. Yang, M.T. Hsieh, T.H. Tsai, and S.L. Hsu Down-modulation of Bcl-XL, release of cytochrome c and sequential activation of caspases during honokiol-induced apoptosis in human squamous lung cancer CH27 cells Biochem Pharmacol 63 2002 1641 1651
24. T. Rosse, R. Olivier, L. Monney, M. Rager, S. Conus, and I. Fellay Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c Nature 391 1998 496 499
25. D.L. Vaux, and S.J. Korsmeyer Cell death in development Cell 96 1999 245 254
26. J.L. Martindale, and N.J. Holbrook Cellular response to oxidative stress: signaling for suicide and survival J Cell Physiol 192 2002 1 15
27. H.U. Simon, A. Haj-Yehia, and F. Levi-Schaffer Role of reactive oxygen species (ROS) in apoptosis induction Apoptosis 5 2000 415 418
28. B. Antonsson Bax and other pro-apoptotic Bcl-2 family "killer-proteins" and their victim the mitochondrion Cell Tissue Res 306 2001 347 361
29. S. Krajewski, S. Tanaka, S. Takayama, M.J. Schibler, W. Fenton, and J.C. Reed Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes Cancer Res 53 1993 4701 4714
30. M. Tafani, J.A. Cohn, N.O. Karpinich, R.J. Rothman, M.A. Russo, and J.L. Farber Regulation of intracellular pH mediates Bax activation in HeLa cells treated with staurosporine or tumor necrosis factor-alpha J Biol Chem 277 2002 49569 49576
31. H. Yamaguchi, and H.G. Wang The protein kinase PKB/Akt regulates cell survival and apoptosis by inhibiting Bax conformational change Oncogene 20 2001 7779 7786
32. C. Tournier, P. Hess, D.D. Yang, J. Xu, T.K. Turner, and A. Nimnual Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway Science 288 2000 870 874
33. L. Zhang, and M.C. Hung Sensitization of HER-2/neu-overexpressing non-small cell lung cancer cells to chemotherapeutic drugs by tyrosine kinase inhibitor emodin Oncogene 12 1996 571 576
34. H. Matsuda, H. Shimoda, T. Morikawa, and M. Yoshikawa Phytoestrogens from the roots of Polygonum cuspidatum (Polygonaceae): structure-requirement of hydroxyanthraquinones for estrogenic activity Bioorg Med Chem Lett 11 2001 1839 1842
35. S. Zhang, C. Qin, and S.H. Safe Flavonoids as aryl hydrocarbon receptor agonists/antagonists: effects of structure and cell context Environ Health Perspect 111 2003 1877 1882
36. D.R. Green, and J.C. Reed Mitochondria and apoptosis Science 281 1998 1309 1312
37. G.H. Lai, Z. Zhang, and A.E. Sirica Celecoxib acts in a cyclooxygenase-2-independent manner and in synergy with emodin to suppress rat cholangiocarcinoma growth in vitro through a mechanism involving enhanced Akt inactivation and increased activation of caspases-9 and -3 Mol Cancer Ther 2 2003 265 271
38. H.Z. Lee, S.L. Hsu, M.C. Liu, and C.H. Wu Effects and mechanisms of aloe-emodin on cell death in human lung squamous cell carcinoma Eur J Pharmacol 431 2001 287 295
39. S. Pervin, R. Singh, and G. Chaudhuri Nitric-oxide-induced Bax integration into the mitochondrial membrane commits MDA-MB-468 cells to apoptosis: essential role of Akt Cancer Res 63 2003 5470 5479
40. 3 is associated with the inherent cellular level of reactive oxygen species World J Gastroenterol 8 2002 36 39
41. J. Yi, F. Gao, G. Shi, H. Li, Z. Wang, and X. Shi The inherent cellular level of reactive oxygen species: one of the mechanisms determining apoptotic susceptibility of leukemic cells to arsenic trioxide Apoptosis 7 2002 209 215
42. J. Yang, H. Li, Y.Y. Chen, X.J. Wang, G.Y. Shi, and Q.S. Hu Anthraquinones sensitize tumor cells to arsenic cytotoxicity in vitro and in vivo via reactive oxygen species-mediated dual regulation of apoptosis Free Radic Biol Med 37 2004 2027 2041
43. N. Watanabe, and H.J. Forman Autoxidation of extracellular hydroquinones is a causative event for the cytotoxicity of menadione and DMNQ in A549-S cells Arch Biochem Biophys 411 2003 145 157
44. M.O. Goulart, P. Falkowski, T. Ossowski, and A. Liwo Electrochemical study of oxygen interaction with lapachol and its radical anions Bioelectrochemistry 59 2003 85 87
45. M. Sugawara, Y. Sugawara, K. Wen, and C. Giulivi Generation of oxygen free radicals in thyroid cells and inhibition of thyroid peroxidase Exp Biol Med (Maywood) 227 2002 141 146
46. W.A. Pry or Free radical biology: xenobiotics, cancer, and aging Ann N Y Acad Sci 393 1982 1 22
47. R.R. Rosato, J.A. Almenara, and S. Grant The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21CIP1/WAF1 1 Cancer Res 63 2003 3637 3645
48. B.C. Park, K.O. Bosire, E.S. Lee, Y.S. Lee, and J.A. Kim Asiatic acid induces apoptosis in SK-MEL-2 human melanoma cells Cancer Lett 218 2005 81 90
49. D.M. Hockenbery, Z.N. Oltvai, X.M. Yin, C.L. Milliman, and S.J. Korsmeyer Bcl-2 functions in an antioxidant pathway to prevent apoptosis Cell 75 1993 241 251
50. J. Haendeler, A.M. Zeiher, and S. Dimmeler Vitamin C and E prevent lipopolysaccharide-induced apoptosis in human endothelial cells by modulation of Bcl-2 and Bax Eur J Pharmacol 317 1996 407 411
51. S.R. Datta, H. Dudek, X. Tao, S. Masters, H. Fu, and Y. Gotoh Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery Cell 91 1997 231 241
52. J. Xu, and K. Liao Protein kinase B/AKT 1 plays a pivotal role in insulin-like growth factor-1 receptor signaling induced 3T3-L1 adipocyte differentiation J Biol Chem 279 2004 35914 35922
53. F. Tsuruta, N. Masuyama, and Y. Gotoh The phosphatidylinositol 3-kinase (PI3K)-Akt pathway suppresses Bax translocation to mitochondria J Biol Chem 277 2002 14040 14047
54. J.M. Kyriakis, and J. Avruch Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation Physiol Rev 81 2001 807 869
55. Q. Huang, H.M. Shen, and C.N. Ong Inhibitory effect of emodin on tumor invasion through suppression of activator protein-1 and nuclear factor-kappaB Biochem Pharmacol 68 2004 361 371
56. C.J. Chang, C.L. Ashendel, R.L. Geahlen, J.L. McLaughlin, and D.J. Waters Oncogene signal transduction inhibitors from medicinal plants In Vivo 10 1996 185 190
57. L.A. Allan, N. Morrice, S. Brady, G. Magee, S. Pathak, and P.R. Clarke Inhibition of caspase-9 through phosphorylation at Thr 125 by ERK MAPK Nat Cell Biol 5 2003 647 654
58. M.P. Scheid, K.M. Schubert, and V. Duronio Regulation of bad phosphorylation and association with Bcl-x(L) by the MAPK/Erk kinase J Biol Chem 274 1999 31108 31113