Wogonin induces reactive oxygen species production and cell apoptosis in human Glioma cancer cells

International Journal of Molecular Sciences

Volumn 13, Issue 8, 2012, Pages 9877-9892

  Tsai, Cheng Fang ^a   Yeh, Wei Lan ^b   Huang, Ssu Ming ^c,d   Tan, Tzu Wei ^e   Lu, Dah Yuu ^e  

^a ASIA UNIVERSITY   (Taiwan)

^b CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

^c BUDDHIST TZU CHI GENERAL HOSPITAL   (Taiwan)

^d NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^e CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; ER stress; Glioma; ROS; Wogonin

Indexed keywords

ACETYLCYSTEINE; APOCYNIN; CALPAIN 1; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; INITIATION FACTOR 2ALPHA; NICOTINAMIDE ADENINE DINUCLEOTIDE; REACTIVE OXYGEN METABOLITE; WOGONIN; CASPASE; FLAVANONE DERIVATIVE;

APOPTOSIS; ARTICLE; ASTROCYTE; CELL DEATH; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GLIOMA CELL; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SCUTELLARIA BAICALENSIS; UPREGULATION; CELL PROLIFERATION; DRUG EFFECTS; FLOW CYTOMETRY; GLIOMA; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; CASPASES; CELL PROLIFERATION; ENDOPLASMIC RETICULUM STRESS; FLAVANONES; FLOW CYTOMETRY; GLIOMA; HUMANS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84864989279     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms13089877     Document Type: Article

References (62)

1. Kleihues, P.; Soylemezoglu, F.; Schauble, B.; Scheithauer, B.W.; Burger, P.C. Histopathology, classification, and grading of gliomas. Glia 1995, 15, 211-221.
2. Griscelli, F.; Li, H.; Cheong, C.; Opolon, P.; Bennaceur-Griscelli, A.; Vassal, G.; Soria, J.; Soria, C.; Lu, H.; Perricaudet, M., et al. Combined effects of radiotherapy and angiostatin gene therapy in glioma tumor model. Proc. Natl. Acad. Sci. USA 2000, 97, 6698-6703.
3. Amberger, V.R.; Hensel, T.; Ogata, N.; Schwab, M.E. Spreading and migration of human glioma and rat C6 cells on central nervous system myelin in vitro is correlated with tumor malignancy and involves a metalloproteolytic activity. Cancer Res. 1998, 58, 149-158.
4. Stupp, R.; Mason, W.P.; van den Bent, M.J.; Weller, M.; Fisher, B.; Taphoorn, M.J.; Belanger, K.; Brandes, A.A.; Marosi, C.; Bogdahn, U., et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352, 987-996.
5. Koul, D.; Shen, R.; Bergh, S.; Sheng, X.; Shishodia, S.; Lafortune, T.A.; Lu, Y.; de Groot, J.F.; Mills, G.B.; Yung, W.K. Inhibition of Akt survival pathway by a small-molecule inhibitor in human glioblastoma. Mol. Cancer Ther. 2006, 5, 637-644.
6. Soboloff, J.; Berger, S.A. Sustained ER Ca2+ depletion suppresses protein synthesis and induces activation-enhanced cell death in mast cells. J. Biol. Chem. 2002, 277, 13812-13820.
7. Abcouwer, S.F.; Marjon, P.L.; Loper, R.K.; Vander Jagt, D.L. Response of VEGF expression to amino acid deprivation and inducers of endoplasmic reticulum stress. Invest. Ophthalmol. Vis. Sci. 2002, 43, 2791-2798.
8. Feldman, D.E.; Chauhan, V.; Koong, A.C. The unfolded protein response: A novel component of the hypoxic stress response in tumors. Mol. Cancer Res. 2005, 3, 597-605.
9. Moenner, M.; Pluquet, O.; Bouchecareilh, M.; Chevet, E. Integrated endoplasmic reticulum stress responses in cancer. Cancer Res. 2007, 67, 10631-10634.
10. Lee, A.S. The glucose-regulated proteins: Stress induction and clinical applications. Trends Biochem. Sci. 2001, 26, 504-510.
11. Kubota, H.; Suzuki, T.; Lu, J.; Takahashi, S.; Sugita, K.; Sekiya, S.; Suzuki, N. Increased expression of GRP94 protein is associated with decreased sensitivity to X-rays in cervical cancer cell lines. Int. J. Radiat. Biol. 2005, 81, 701-709.
12. Wang, X.Z.; Lawson, B.; Brewer, J.W.; Zinszner, H.; Sanjay, A.; Mi, L.J.; Boorstein, R.; Kreibich, G.; Hendershot, L.M.; Ron, D. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol. 1996, 16, 4273-4280.
13. Rao, R.V.; Ellerby, H.M.; Bredesen, D.E. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ. 2004, 11, 372-380.
14. Harding, H.P.; Calfon, M.; Urano, F.; Novoa, I.; Ron, D. Transcriptional and translational control in the Mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 2002, 18, 575-599.
15. McCullough, K.D.; Martindale, J.L.; Klotz, L.O.; Aw, T.Y.; Holbrook, N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 2001, 21, 1249-1259.
16. Wek, R.C.; Jiang, H.Y.; Anthony, T.G. Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 2006, 34, 7-11.
17. Roos, W.P.; Kaina, B. DNA damage-induced cell death by apoptosis. Trends Mol. Med. 2006, 12, 440-450.
18. Gupta, S.C.; Hevia, D.; Patchva, S.; Park, B.; Koh, W.; Aggarwal, B.B. Upsides and downsides of reactive oxygen species for cancer: The roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid. Redox Sign 2012, 16, 1295-1322.
19. Tai, M.C.; Tsang, S.Y.; Chang, L.Y.; Xue, H. Therapeutic potential of wogonin: A naturally occurring flavonoid. CNS Drug Rev. 2005, 11, 141-150.
20. Wakabayashi, I.; Yasui, K. Wogonin inhibits inducible prostaglandin E(2) production in macrophages. Eur. J. Pharmacol. 2000, 406, 477-481.
21. Lee, H.; Kim, Y.O.; Kim, H.; Kim, S.Y.; Noh, H.S.; Kang, S.S.; Cho, G.J.; Choi, W.S.; Suk, K. Flavonoid wogonin from medicinal herb is neuroprotective by inhibiting inflammatory activation of microglia. FASEB J. 2003, 17, 1943-1944.
22. Huang, G.C.; Chow, J.M.; Shen, S.C.; Yang, L.Y.; Lin, C.W.; Chen, Y.C. Wogonin but not Nor-wogonin inhibits lipopolysaccharide and lipoteichoic acid-induced iNOS gene expression and NO production in macrophages. Int. Immunopharmacol. 2007, 7, 1054-1063.
23. Piao, H.Z.; Choi, I.Y.; Park, J.S.; Kim, H.S.; Cheong, J.H.; Son, K.H.; Jeon, S.J.; Ko, K.H.; Kim, W.K. Wogonin inhibits microglial cell migration via suppression of nuclear factor-kappa B activity. Int. Immunopharmacol. 2008, 8, 1658-1662.
24. Chi, Y.S.; Lim, H.; Park, H.; Kim, H.P. Effects of wogonin, a plant flavone from Scutellaria radix, on skin inflammation: In vivo regulation of inflammation-associated gene expression. Biochem. Pharmacol. 2003, 66, 1271-1278.
25. Huang, W.H.; Lee, A.R.; Yang, C.H. Antioxidative and anti-inflammatory activities of polyhydroxyflavonoids of Scutellaria baicalensis GEORGI. Biosci. Biotechnol. Biochem. 2006, 70, 2371-2380.
26. Cho, J.; Lee, H.K. Wogonin inhibits ischemic brain injury in a rat model of permanent middle cerebral artery occlusion. Biol. Pharm. Bull. 2004, 27, 1561-1564.
27. Piao, H.Z.; Jin, S.A.; Chun, H.S.; Lee, J.C.; Kim, W.K. Neuroprotective effect of wogonin: Potential roles of inflammatory cytokines. Arch. Pharm. Res. 2004, 27, 930-936.
28. Son, D.; Lee, P.; Lee, J.; Kim, H.; Kim, S.Y. Neuroprotective effect of wogonin in hippocampal slice culture exposed to oxygen and glucose deprivation. Eur. J. Pharmacol. 2004, 493, 99-102.
29. Cho, J.; Lee, H.K. Wogonin inhibits excitotoxic and oxidative neuronal damage in primary cultured rat cortical cells. Eur. J. Pharmacol. 2004, 485, 105-110.
30. Chen, C.C.; Hung, T.H.; Wang, Y.H.; Lin, C.W.; Wang, P.Y.; Lee, C.Y.; Chen, S.F. Wogonin improves histological and functional outcomes, and reduces activation of TLR4/NF-kappaB signaling after experimental traumatic brain injury. PLoS One 2012, 7, e30294.
31. Himeji, M.; Ohtsuki, T.; Fukazawa, H.; Tanaka, M.; Yazaki, S.; Ui, S.; Nishio, K.; Yamamoto, H.; Tasaka, K.; Mimura, A. Difference of growth-inhibitory effect of Scutellaria baicalensis-producing flavonoid wogonin among human cancer cells and normal diploid cell. Cancer Lett. 2007, 245, 269-274.
32. Lin, C.C.; Kuo, C.L.; Lee, M.H.; Lai, K.C.; Lin, J.P.; Yang, J.S.; Yu, C.S.; Lu, C.C.; Chiang, J.H.; Chueh, F.S., et al. Wogonin triggers apoptosis in human osteosarcoma U-2 OS cells through the endoplasmic reticulum stress, mitochondrial dysfunction and caspase-3-dependent signaling pathways. Int. J. Oncol. 2011, 39, 217-224.
33. Yu, C.S.; Yu, F.S.; Chuang, Y.C.; Lu, H.F.; Lin, S.Y.; Chiu, T.H.; Chung, J.G. Wogonin inhibits N-acetyltransferase activity and gene expression in human leukemia HL-60 cells. Anticancer Res. 2005, 25, 127-132.
34. Chung, H.; Jung, Y.M.; Shin, D.H.; Lee, J.Y.; Oh, M.Y.; Kim, H.J.; Jang, K.S.; Jeon, S.J.; Son, K.H.; Kong, G. Anticancer effects of wogonin in both estrogen receptor-positive and -negative human breast cancer cell lines in vitro and in nude mice xenografts. Int. J. Cancer 2008, 122, 816-822.
35. Parajuli, P.; Joshee, N.; Rimando, A.M.; Mittal, S.; Yadav, A.K. In vitro antitumor mechanisms of various Scutellaria extracts and constituent flavonoids. Planta Med. 2009, 75, 41-48.
36. Perez, A.T.; Arun, B.; Tripathy, D.; Tagliaferri, M.A.; Shaw, H.S.; Kimmick, G.G.; Cohen, I.; Shtivelman, E.; Caygill, K.A.; Grady, D., et al. A phase 1B dose escalation trial of Scutellaria barbata (BZL101) for patients with metastatic breast cancer. Breast Cancer Res. Treat. 2010, 120, 111-118.
37. Rugo, H.; Shtivelman, E.; Perez, A.; Vogel, C.; Franco, S.; Tan Chiu, E.; Melisko, M.; Tagliaferri, M.; Cohen, I.; Shoemaker, M., et al. Phase I trial and antitumor effects of BZL101 for patients with advanced breast cancer. Breast Cancer Res. Treat. 2007, 105, 17-28.
38. Wang, W.; Guo, Q.L.; You, Q.D.; Zhang, K.; Yang, Y.; Yu, J.; Liu, W.; Zhao, L.; Gu, H.Y.; Hu, Y., et al. The anticancer activities of wogonin in murine sarcoma S180 both in vitro and in vivo. Biol. Pharm. Bull. 2006, 29, 1132-1137.
39. Baumann, S.; Fas, S.C.; Giaisi, M.; Muller, W.W.; Merling, A.; Gulow, K.; Edler, L.; Krammer, P.H.; Li-Weber, M. Wogonin preferentially kills malignant lymphocytes and suppresses T-cell tumor growth by inducing PLCgamma1- and Ca2+-dependent apoptosis. Blood 2008, 111, 2354-2363.
40. Lu, N.; Gao, Y.; Ling, Y.; Chen, Y.; Yang, Y.; Gu, H.Y.; Qi, Q.; Liu, W.; Wang, X.T.; You, Q.D.; Guo, Q.L. Wogonin suppresses tumor growth in vivo and VEGF-induced angiogenesis through inhibiting tyrosine phosphorylation of VEGFR2. Life Sci. 2008, 82, 956-963.
41. Fas, S.C.; Baumann, S.; Zhu, J.Y.; Giaisi, M.; Treiber, M.K.; Mahlknecht, U.; Krammer, P.H.; Li-Weber, M. Wogonin sensitizes resistant malignant cells to TNFα- and TRAIL-induced apoptosis. Blood 2006, 108, 3700-3706.
42. Huang, S.M.; Cheung, C.W.; Chang, C.S.; Tang, C.H.; Liu, J.F.; Lin, Y.H.; Chen, J.H.; Ko, S.H.; Wong, K.L.; Lu, D.Y. Phloroglucinol derivative MCPP induces cell apoptosis in human colon cancer. J. Cell. Biochem. 2011, 112, 643-652.
43. Cotter, T.G. Apoptosis and cancer: The genesis of a research field. Nat. Rev. Cancer 2009, 9, 501-507.
44. Leber, B.; Lin, J.; Andrews, D.W. Still embedded together binding to membranes regulates Bcl-2 protein interactions. Oncogene 2010, 29, 5221-5230.
45. Lau, A.T.; Wang, Y.; Chiu, J.F. Reactive oxygen species: Current knowledge and applications in cancer research and therapeutic. J. Cell. Biochem. 2008, 104, 657-667.
46. Mates, J.M.; Sanchez-Jimenez, F.M. Role of reactive oxygen species in apoptosis: Implications for cancer therapy. Int. J. Biochem. Cell Biol. 2000, 32, 157-170.
47. Zu, K.; Hawthorn, L.; Ip, C. Up-regulation of c-Jun-NH2-kinase pathway contributes to the induction of mitochondria-mediated apoptosis by alpha-tocopheryl succinate in human prostate cancer cells. Mol. Cancer Ther. 2005, 4, 43-50.
48. Iwamaru, A.; Iwado, E.; Kondo, S.; Newman, R.A.; Vera, B.; Rodriguez, A.D.; Kondo, Y. Eupalmerin acetate, a novel anticancer agent from Caribbean gorgonian octocorals, induces apoptosis in malignant glioma cells via the c-Jun NH2-terminal kinase pathway. Mol. Cancer Ther. 2007, 6, 184-192.
49. Wenzel, U.; Nickel, A.; Kuntz, S.; Daniel, H. Ascorbic acid suppresses drug-induced apoptosis in human colon cancer cells by scavenging mitochondrial superoxide anions. Carcinogenesis 2004, 25, 703-712.
50. Reddy, R.K.; Mao, C.; Baumeister, P.; Austin, R.C.; Kaufman, R.J.; Lee, A.S. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: Role of ATP binding site in suppression of caspase-7 activation. J. Biol. Chem. 2003, 278, 20915-20924.
51. Masud, A.; Mohapatra, A.; Lakhani, S.A.; Ferrandino, A.; Hakem, R.; Flavell, R.A. Endoplasmic reticulum stress-induced death of mouse embryonic fibroblasts requires the intrinsic pathway of apoptosis. J. Biol. Chem. 2007, 282, 14132-14139.
52. Kamata, H.; Hirata, H. Redox regulation of cellular signalling. Cell. Signal. 1999, 11, 1-14.
53. Annunziato, L.; Amoroso, S.; Pannaccione, A.; Cataldi, M.; Pignataro, G.; D'Alessio, A.; Sirabella, R.; Secondo, A.; Sibaud, L.; Di Renzo, G.F. Apoptosis induced in neuronal cells by oxidative stress: Role played by caspases and intracellular calcium ions. Toxicol. Lett. 2003, 139, 125-133.
54. Monks, T.J.; Xie, R.; Tikoo, K.; Lau, S.S. ROS-induced histone modifications and their role in cell survival and cell death. Drug Metab. Rev. 2006, 38, 755-767.
55. Schumacker, P.T. Reactive oxygen species in cancer cells: Live by the sword, die by the sword. Cancer Cell 2006, 10, 175-176.
56. Yu, J.S.; Kim, A.K. Wogonin induces apoptosis by activation of ERK and p38 MAPKs signaling pathways and generation of reactive oxygen species in human breast cancer cells. Mol. Cells 2011, 31, 327-335.
57. Lee, D.H.; Kim, C.; Zhang, L.; Lee, Y.J. Role of p53, PUMA, and Bax in wogonin-induced apoptosis in human cancer cells. Biochem. Pharmacol. 2008, 75, 2020-2033.
58. Liu, Z.L.; Tanaka, S.; Horigome, H.; Hirano, T.; Oka, K. Induction of apoptosis in human lung fibroblasts and peripheral lymphocytes in vitro by Shosaiko-to derived phenolic metabolites. Biol. Pharm. Bull. 2002, 25, 37-41.
59. Lim, S.C.; Hahm, K.S.; Lee, S.H.; Oh, S.H. Autophagy involvement in cadmium resistance through induction of multidrug resistance-associated protein and counterbalance of endoplasmic reticulum stress WI38 lung epithelial fibroblast cells. Toxicology 2010, 276, 18-26.
60. Park, J.W.; Woo, K.J.; Lee, J.T.; Lim, J.H.; Lee, T.J.; Kim, S.H.; Choi, Y.H.; Kwon, T.K. Resveratrol induces pro-apoptotic endoplasmic reticulum stress in human colon cancer cells. Oncol. Rep. 2007, 18, 1269-1273.
61. Kim, A.J.; Shi, Y.; Austin, R.C.; Werstuck, G.H. Valproate protects cells from ER stress-induced lipid accumulation and apoptosis by inhibiting glycogen synthase kinase-3. J. Cell Sci. 2005, 118, 89-99.
62. Lu, D.Y.; Chang, C.S.; Yeh, W.L.; Tang, C.H.; Cheung, C.W.; Leung, Y.M.; Liu, J.F.; Wong, K.L. The novel phloroglucinol derivative BFP induces apoptosis of glioma cancer through reactive oxygen species and endoplasmic reticulum stress pathways. Phytomedicine 2012, in press.