Characterization of apoptosis induced by emodin and related regulatory mechanisms in human neuroblastoma cells

International Journal of Molecular Sciences

Volumn 14, Issue 10, 2013, Pages 20139-20156

  Huang, Fu Jen ^a,b   Hsuuw, Yan Der ^c   Chan, Wen Hsiung ^d  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c NATIONAL PINGTUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^d CHUNG YUAN CHRISTIAN UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Calcium; Emodin; Nitric oxide; Oxidative stress

Indexed keywords

CALCIUM; CASPASE 3; CASPASE 9; EMODIN; NITRIC OXIDE; PROTEIN P21; PROTEIN P53; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; NEUROBLASTOMA CELL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

APOPTOSIS; CALCIUM; CASPASE 3; CASPASE 9; CELL DEATH; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYTOPLASM; EMODIN; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; NEUROBLASTOMA; NITRIC OXIDE; REACTIVE OXYGEN SPECIES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84885343357     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141020139     Document Type: Article

References (50)

1. Yim, H.; Lee, Y.H.; Lee, C.H.; Lee, S.K. Emodin, an anthraquinone derivative isolated from the rhizomes of Rheum palmatum, selectively inhibits the activity of casein kinase II as a competitive inhibitor. Planta Med. 1999, 65, 9-13.
2. Yang, F.; Zhang, T.; Tian, G.; Cao, H.; Liu, Q.; Ito, Y. Preparative isolation and purification of hydroxyanthraquinones from Rheum officinale Baill by high-speed counter-current chromatography using pH-modulated stepwise elution. J. Chromatogr. A 1999, 858, 103-107.
3. Huang, H.C.; Chu, S.H.; Chao, P.D. Vasorelaxants from Chinese herbs, emodin and scoparone, possess immunosuppressive properties. Eur. J. Pharmacol. 1991, 198, 211-213.
4. Zhou, X.M.; Chen, Q.H. Biochemical study of Chinese rhubarb. XXII. Inhibitory effect of anthraquinone derivatives on Na+-K+-ATPase of the rabbit renal medulla and their diuretic action. Yao Xue Xue Bao 1988, 23, 17-20.
5. Koyama, M.; Kelly, T.R.; Watanabe, K.A. Novel type of potential anticancer agents derived from chrysophanol and emodin. Some structure-activity relationship studies. J. Med. Chem. 1988, 31, 283-284.
6. Zhang, L.; Lau, Y.K.; Xia, W.; Hortobagyi, G.N.; Hung, M.C. 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. 1999, 5, 343-353.
7. Shieh, D.E.; Chen, Y.Y.; Yen, M.H.; Chiang, L.C.; Lin, C.C. Emodin-induced apoptosis through p53-dependent pathway in human hepatoma cells. Life Sci. 2004, 74, 2279-2290.
8. Wang, C.-G.; Yang, J.-Q.; Liu, B.-Z.; Jin, D.-T.; Wang, C.; Zhong, L.; Zhu, D.; Wu, Y. Anti-tumor activity of emodin against human chronic myelocytic leukemia K562 cell lines in vitro and in vivo. Eur. J. Pharmacol. 2010, 627, 33-41.
9. Su, Y.T.; Chang, H.L.; Shyue, S.K.; Hsu, S.L. Emodin induces apoptosis in human lung adenocarcinoma cells through a reactive oxygen species-dependent mitochondrial signaling pathway. Biochem. Pharmacol. 2005, 70, 229-241.
10. Lin, S.Y.; Lai, W.W.; Ho, C.C.; Yu, F.S.; Chen, G.W.; Yang, J.S.; Liu, K.C.; Lin, M.L.; Wu, P.P.; Fan, M.J.; et al. Emodin induces apoptosis of human tongue squamous cancer SCC-4 cells through reactive oxygen species and mitochondria-dependent pathways. Anticancer Res. 2009, 29, 327-335.
11. Kuo, T.C.; Yang, J.S.; Lin, M.W.; Hsu, S.C.; Lin, J.J.; Lin, H.J.; Hsia, T.C.; Liao, C.L.; Yang, M.D.; Fan, M.J.; et al. Emodin has cytotoxic and protective effects in rat C6 glioma cells: Roles of Mdr1a and nuclear factor kappaB in cell survival. J. Pharmacol. Exp. Ther. 2009, 330, 736-744.
12. Chang, M.H.; Huang, F.J.; Chan, W.H. Emodin induces embryonic toxicity in mouse blastocysts through apoptosis. Toxicology 2012, 299, 25-32.
13. Halliwell, B.; Gutteridge, J.M. Role of free radicals and catalytic metal ions in human disease: An overview. Methods Enzymol. 1990, 186, 1-85.
14. Chan, W.H. Ginkgolide B induces apoptosis and developmental injury in mouse embryonic stem cells and blastocysts. Hum. Reprod. 2006, 21, 2985-2995.
15. Chan, W.H.; Shiao, N.H.; Lu, P.Z. CdSe quantum dots induce apoptosis in human neuroblastoma cells via mitochondrial-dependent pathways and inhibition of survival signals. Toxicol. Lett. 2006, 167, 191-200.
16. Ekmekcioglu, S.; Tang, C.H.; Grimm, E.A. NO news is not necessarily good news in cancer. Curr. Cancer Drug Targets 2005, 5, 103-115.
17. Zhou, J.; Brune, B. NO and transcriptional regulation: From signaling to death. Toxicology 2005, 208, 223-233.
18. Rao, C.V. Nitric oxide signaling in colon cancer chemoprevention. Mutat. Res. 2004, 555, 107-119.
19. Lu, Z.; Tao, Y.; Zhou, Z.; Zhang, J.; Li, C.; Ou, L.; Zhao, B. Mitochondrial reactive oxygen species and nitric oxide-mediated cancer cell apoptosis in 2-butylamino-2-demethoxyhypocrellin B photodynamic treatment. Free Radic. Biol. Med. 2006, 41, 1590-1605.
20. Nazarewicz, R.R.; Zenebe, W.J.; Parihar, A.; Larson, S.K.; Alidema, E.; Choi, J.; Ghafourifar, P. Tamoxifen induces oxidative stress and mitochondrial apoptosis via stimulating mitochondrial nitric oxide synthase. Cancer Res. 2007, 67, 1282-1290.
21. Xu, Y.; Liu, B.; Zweier, J.L.; He, G. Formation of hydrogen peroxide and reduction of peroxynitrite via dismutation of superoxide at reperfusion enhances myocardial blood flow and oxygen consumption in postischemic mouse heart. J. Pharmacol. Exp. Ther. 2008, 327, 402-410.
22. Ghafourifar, P.; Cadenas, E. Mitochondrial nitric oxide synthase. Trends Pharmacol. Sci. 2005, 26, 190-195.
23. Brookes, P.S. Mitochondrial nitric oxide synthase. Mitochondrion 2004, 3, 187-204.
24. Dennis, J.; Bennett, J.P., Jr. Interactions among nitric oxide and Bcl-family proteins after MPP+ exposure of SH-SY5Y neural cells I: MPP+ increases mitochondrial NO and Bax protein. J. Neurosci. Res. 2003, 72, 76-88.
25. Taylor, C.T.; Moncada, S. Nitric oxide, cytochrome C oxidase, and the cellular response to hypoxia. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 643-647.
26. Elfering, S.L.; Sarkela, T.M.; Giulivi, C. Biochemistry of mitochondrial nitric-oxide synthase. J. Biol. Chem. 2002, 277, 38079-38086.
27. Dedkova, E.N.; Ji, X.; Lipsius, S.L.; Blatter, L.A. Mitochondrial calcium uptake stimulates nitric oxide production in mitochondria of bovine vascular endothelial cells. Am. J. Physiol. Cell Physiol. 2004, 286, C406-415.
28. Chan, W.H. Effect of resveratrol on high glucose-induced stress in human leukemia K562 cells. J. Cell Biochem. 2005, 94, 1267-1279.
29. Hsuuw, Y.D.; Chang, C.K.; Chan, W.H.; Yu, J.S. Curcumin prevents methylglyoxal-induced oxidative stress and apoptosis in mouse embryonic stem cells and blastocysts. J. Cell Physiol. 2005, 205, 379-386.
30. Lin, M.L.; Lu, Y.C.; Su, H.L.; Lin, H.T.; Lee, C.C.; Kang, S.E.; Lai, T.C.; Chung, J.G.; Chen, S.S. Destabilization of CARP mRNAs by aloe-emodin contributes to caspase-8-mediated p53-independent apoptosis of human carcinoma cells. J. Cell Biochem. 2011, 112, 1176-1191.
31. Li, C.Q.; Robles, A.I.; Hanigan, C.L.; Hofseth, L.J.; Trudel, L.J.; Harris, C.C.; Wogan, G.N. Apoptotic signaling pathways induced by nitric oxide in human lymphoblastoid cells expressing wild-type or mutant p53. Cancer Res. 2004, 64, 3022-3029.
32. Okada, H.; Mak, T.W. Pathways of apoptotic and non-apoptotic death in tumour cells. Nat. Rev. Cancer 2004, 4, 592-603.
33. Wei, W.T.; Chen, H.; Ni, Z.L.; Liu, H.B.; Tong, H.F.; Fan, L.; Liu, A.; Qiu, M.X.; Liu, D.L.; Guo, H.C.; et al. Antitumor and apoptosis-promoting properties of emodin, an anthraquinone derivative from Rheum officinale Baill, against pancreatic cancer in mice via inhibition of Akt activation. Int. J. Oncol. 2011, 39, 1381-1390.
34. Buttke, T.M.; Sandstrom, P.A. Oxidative stress as a mediator of apoptosis. Immunol. Today 1994, 15, 7-10.
35. Slater, A.F.; Nobel, C.S.; Maellaro, E.; Bustamante, J.; Kimland, M.; Orrenius, S. Nitrone spin traps and a nitroxide antioxidant inhibit a common pathway of thymocyte apoptosis. Biochem. J. 1995, 306, 771-778.
36. Chan, W.H.; Wu, C.C.; Yu, J.S. Curcumin inhibits UV irradiation-induced oxidative stress and apoptotic biochemical changes in human epidermoid carcinoma A431 cells. J. Cell Biochem. 2003, 90, 327-338.
37. Almeida, R.D.; Manadas, B.J.; Carvalho, A.P.; Duarte, C.B. Intracellular signaling mechanisms in photodynamic therapy. Biochim. Biophys. Acta 2004, 1704, 59-86.
38. Inanami, O.; Yoshito, A.; Takahashi, K.; Hiraoka, W.; Kuwabara, M. Effects of BAPTA-AM and forskolin on apoptosis and cytochrome c release in photosensitized Chinese hamster V79 cells. Photochem. Photobiol. 1999, 70, 650-655.
39. Chan, W.H. Citrinin induces apoptosis in mouse embryonic stem cells. IUBMB Life 2008, 60, 171-179.
40. Hsieh, M.S.; Chan, W.H. Impact of methylglyoxal and high glucose co-treatment on human mononuclear cells. Int. J. Mol. Sci. 2009, 10, 1445-1464.
41. Lin, S.Z.; Wei, W.T.; Chen, H.; Chen, K.J.; Tong, H.F.; Wang, Z.H.; Ni, Z.L.; Liu, H.B.; Guo, H.C.; Liu, D.L. Antitumor activity of emodin against pancreatic cancer depends on its dual role: Promotion of apoptosis and suppression of angiogenesis. PLoS One 2012, 7, e42146.
42. Chen, T.G.; Chen, J.Z.; Wang, X.X. Effects of rapamycin on number activity and eNOS of endothelial progenitor cells from peripheral blood. Cell Prolif. 2006, 39, 117-125.
43. Li, C.Q.; Wogan, G.N. Nitric oxide as a modulator of apoptosis. Cancer Lett. 2005, 226, 1-15.
44. Gomes, E.R.; Almeida, R.D.; Carvalho, A.P.; Duarte, C.B. Nitric oxide modulates tumor cell death induced by photodynamic therapy through a cGMP-dependent mechanism. Photochem. Photobiol. 2002, 76, 423-430.
45. Wu, H.J.; Chan, W.H. Genistein protects methylglyoxal-induced oxidative DNA damage and cell injury in human mononuclear cells. Toxicol. In Vitro 2007, 21, 335-342.
46. Chan, W.H.; Chang, Y.J. Dosage effects of resveratrol on ethanol-induced cell death in the human K562 cell line. Toxicol Lett. 2006, 161, 1-9.
47. Behl, C.; Davis, J.B.; Lesley, R.; Schubert, D. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 1994, 77, 817-827.
48. Aoshima, H.; Satoh, T.; Sakai, N.; Yamada, M.; Enokido, Y.; Ikeuchi, T.; Hatanaka, H. Generation of free radicals during lipid hydroperoxide-triggered apoptosis in PC12h cells. Biochim. Biophys. Acta 1997, 1345, 35-42.
49. Nakatsubo, N.; Kojima, H.; Kikuchi, K.; Nagoshi, H.; Hirata, Y.; Maeda, D.; Imai, Y.; Irimura, T.; Nagano, T. Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators: Diaminofluoresceins. FEBS Lett. 1998, 427, 263-266.
50. Hsieh, Y.J.; Wu, C.C.; Chang, C.J.; Yu, J.S. Subcellular localization of Photofrin determines the death phenotype of human epidermoid carcinoma A431 cells triggered by photodynamic therapy: When plasma membranes are the main targets. J. Cell Physiol. 2003, 194, 363-375.