Icariin, a natural flavonol glycoside, induces apoptosis in human hepatoma SMMC-7721 cells via a ROS/JNK-dependent mitochondrial pathway

Cancer Letters

Volumn 298, Issue 2, 2010, Pages 222-230

  Li, Songgang ^a   Dong, Ping ^a   Wang, Jianwei ^b   Zhang, Jie ^c   Gu, Jun ^a   Wu, Xiangsong ^b   Wu, Wenguang ^b   Fei, Xiaozhou ^b   Zhang, Zhiping ^b   Wang, Yong ^b   Quan, Zhiwei ^a   Liu, Yingbin ^a,b  

^a XINHUA HOSPITAL AFFILIATED TO SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Apoptosis; C Jun N terminal kinase; Hepatoma; Icariin; Reactive oxygen species; SMMC 7721 cells

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CASPASE; CYTOCHROME C; ICARIIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL STRAIN; CELL STRAIN SMMC 7721; CONTROLLED STUDY; CYTOTOXICITY; DRUG ANTAGONISM; DRUG EFFICACY; DRUG SAFETY; ENZYME ACTIVATION; ENZYME RELEASE; FEMALE; HEPATOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CASPASE 3; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUGS, CHINESE HERBAL; FEMALE; FLAVONOIDS; HEP G2 CELLS; HEPATOCYTES; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIVER NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, NUDE; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 77957932118     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2010.07.009     Document Type: Article

References (41)

1. Parkin D.M., Bray F., Ferlay J., Pisani P. Global cancer statistics, 2002. CA Cancer J. Clin. 2005, 55:74-108.
2. Trevisani F., Cantarini M.C., Wands J.R., Bernardi M. Recent advances in the natural history of hepatocellular carcinoma. Carcinogenesis 2008, 29:1299-1305.
3. El-Serag H.B., Siegel A.B., Davila J.A., Shaib Y.H., Cayton-Woody M., McBride R., McGlynn K.A. Treatment and outcomes of treating of hepatocellular carcinoma among medicare recipients in the United States: a population-based study. J. Hepatol. 2006, 44:158-166.
4. Llovet J.M., Bruix J. Testing molecular therapies in hepatocellular carcinoma: the need for randomized phase II trials. J. Clin. Oncol. 2009, 27:833-835.
5. Llovet J.M., Burroughs A., Bruix J. Hepatocellular carcinoma. Lancet 2003, 362:1907-1917.
6. Middleton E., Kandaswami C., Theoharides T.C. The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol. Rev. 2000, 52:673-751.
7. Li Y.L., Gan G.P., Zhang H.Z., Wu H.Z., Li C.L., Huang Y.P., Liu Y.W., Liu J.W. A flavonoid glycoside isolated from smilax China L. rhizome in vitro anticancer effects on human cancer cell lines. J. Ethnopharmacol. 2007, 113:115-124.
8. Diaz J.G., Carmona A.J., Torres F., Quintana J., Estevez F., Herz W. Cytotoxic activities of flavonoid glycoside acetates from consolida oliveriana. Planta Med. 2008, 74:171-174.
9. Pan Y., Kong L.D., Li Y.C., Xia X., Kung H.F., Jiang F.X. Icariin from epimedium brevicornum attenuates chronic mild stress-induced behavioral and neuroendocrinological alterations in male wistar rats. Pharmacol. Biochem. Behav. 2007, 87:130-140.
10. Xu H.B., Huang Z.Q. Icariin enhances endothelial nitric-oxide synthase expression on human endothelial cells in vitro. Vasc. Pharmacol. 2007, 47:18-24.
11. He W., Sun H., Yang B., Zhang D., Kabelitz D. Immunoregulatory effects of the herba epimediia-glycoside-icariin. Arznei-Forschung 1995, 45:910-913.
12. Zhao J., Ohba S., Shinkai M., Chung U.I., Nagamune T. Icariin induces osteogenic differentiation in vitro in a BMP- and Runx2-dependent manner. Biochem. Biophys. Res. Commun. 2008, 369:444-448.
13. Ding L., Liang X.G., Hu Y., Zhu D.Y., Lou Y.J. Involvement of p38MAPK and reactive oxygen species in icariin-induced cardiomyocyte differentiation of murine embryonic stem cells in vitro. Stem Cells Dev. 2008, 17:751-760.
14. Wo Y.B., Zhu D.Y., Yu Y.P., Lou Y.J. Involvement of NF-kappa B and AP-1 activation in icariin promoted cardiac differentiation of mouse embryonic stem cells. Eur. J. Pharmacol. 2008, 586:59-66.
15. Yang J.X., Fichtner I., Becker M., Lemm M., Wang X.M. Anti-proliferative efficacy of icariin on HepG2 hepatoma and its possible mechanism of action. Am. J. Chin. Med. 2009, 37:1153-1165.
16. Sun Y., Liu J.L., Qian F., Xu Q. Nitric oxide inhibits T cell adhesion and migration by down-regulation of β1 integrin expression in immunologically liver-injured mice. Int. Immunopharmacol. 2006, 6:616-626.
17. Sun Y., Qin Y., Gong F.Y., Wu X.F., Hua Z.C., Chen T., Xu Q. Selective triggering of apoptosis of concanavalin A-activated T cells by fraxinellone for the treatment of T-cell-dependent hepatitis in mice. Biochem. Pharmacol. 2009, 77:1717-1724.
18. Deeb D., Gao X.H., Jiang H., Janic B., Arbab A.S., Rojanasakul Y., Dulchavsky S.A., Gautam S.C. Oleanane triterpenoid CDDO-Me inhibits growth and induces apoptosis in prostate cancer cells through a ROS-dependent mechanism. Biochem. Pharmacol. 2010, 79:350-360.
19. Calvino-Fernandez M., Benito-Martinez S., Parra-Cid T. Oxidative stress by Helicobacter pylori causes apoptosis through mitochondrial pathway in gastric epithelial cells. Apoptosis 2008, 13:1267-1280.
20. Appierto V., Tiberio P., Villani M.G., Cavadini E., Formelli F. PLAB induction in fenretinide-induced apoptosis of ovarian cancer cells occurs via a ROS-dependent mechanism involving ER stress and JNK activation. Carcinogenesis 2009, 30:824-831.
21. Wang Y., He Q.Y., Che C.M., Tsao S.W., Sun R.W.Y., Chiu J.F. Modulation of gold(III) porphyrin 1a-induced apoptosis by mitogen-activated protein kinase signaling pathways. Biochem. Pharmacol. 2008, 75:1282-1291.
22. Wang C.C.C., Chiang Y.M., Sung S.C., Hsu Y.L., Chang J.K., Kuo P.L. Plumbagin induces cell cycle arrest and apoptosis through reactive oxygen species/c-Jun N-terminal kinase pathways in human melanoma A375.S2 cells. Cancer Lett. 2008, 259:82-98.
23. Chauhan D., Li G.L., Sattler M., Podar K., Mitsiades C., Mitsiades N., Munshi N., Hideshima T., Anderson K.C. Superoxide-dependent and -independent mitochondrial signaling during apoptosis in multiple myeloma cells. Oncogene 2003, 22:6296-6300.
24. Farazi P.A., DePinho R.A. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat. Rev. Cancer 2006, 6:674-687.
25. Yang Y., Yang L., You Q.D., Nie F.F., Gu H.Y., Zhao L., Wang X.T., Guo Q.L. Differential apoptotic induction of gambogic acid, a novel anticancer natural product, on hepatoma cells and normal hepatocytes. Cancer Lett. 2007, 256:259-266.
26. Wang X.D. The expanding role of mitochondria in apoptosis. Gene. Dev. 2001, 15:2922-2933.
27. Kroemer G., Reed J.C. Mitochondrial control of cell death. Nat. Med. 2000, 6:513-519.
28. van Loo G., Saelens X., van Gurp M., MacFarlane M., Martin S.J., Vandenabeele P. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 2002, 9:1031-1042.
29. Amantana A., London C.A., Iversen P.L., Devi G.R. X-linked inhibitor of apoptosis protein inhibition induces apoptosis and enhances chemotherapy sensitivity in human prostate cancer cells. Mol. Cancer Ther. 2004, 3:699-707.
30. Dai Y., Qiao L., Chan K.W., Yang M., Ye J.Y., Zhang R.X., Ma J., Zou B., Lam C.S.C., Wang J., Pang R., Tan V.P.Y., Lan H.Y., Wong B.C.Y. Adenovirus-mediated down-regulation of X-linked inhibitor of apoptosis protein inhibits colon cancer. Mol. Cancer Ther. 2009, 8:2762-2770.
31. Ballif B.A., Blenis J. Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth Differ. 2001, 12:397-408.
32. Ding L., Liang X.G., Zhu D.Y., Lou Y.J. Icariin promotes expression of PGC-1 alpha, PPAR alpha, and NRF-1 during cardiomyocyte differentiation of murine embryonic stem cells in vitro. Acta Pharmacol. Sin. 2007, 28:1541-1549.
33. Wang L., Zhang L., Chen Z.B., Wu J.Y., Zhang X., Xu Y. Icariin enhances neuronal survival after oxygen and glucose deprivation by increasing SIRT1. Eur. J. Pharmacol. 2009, 609:40-44.
34. Kondo N., Nakamura H., Masutani H., Yodoi J. Redox regulation of human thioredoxin network. Antioxidants Redox Signal. 2006, 8:1881-1890.
35. Moon D.O., Kim M.O., Kang S.H., Choi Y.H., Kim G.Y. Sulforaphane suppresses TNF-alpha-mediated activation of NF-kappa B and induces apoptosis through activation of reactive oxygen species-dependent caspase-3. Cancer Lett. 2009, 274:132-142.
36. Kim B.C., Kim H.G., Lee S.A., Lim S., Park E.H., Kim S.J., Lim C.J. Genipin-induced apoptosis in hepatoma cells is mediated by reactive oxygen species/c-Jun NH2-terminal kinase-dependent activation of mitochondrial pathway. Biochem. Pharmacol. 2005, 70:1398-1407.
37. Lee W.Y.W., Liu K.W.K., Yeung J.H.K. Reactive oxygen species-mediated kinase activation by dihydrotanshinone in tanshinones-induced apoptosis in HepG2 cells. Cancer Lett. 2009, 285:46-57.
38. Gomez-Lazaro M., Galindo M.F., de Mera R., Fernandez-Gomez F.J., Concannon C.G., Segura M.F., Comella J.X., Prehn J.H.M., Jordan J. Reactive oxygen species and p38 mitogen-activated protein kinase activate bax to induce mitochondrial cytochrome c release and apoptosis in response to malonate. Mol. Pharmacol. 2007, 71:736-743.
39. Zhang R., Humphreys I., Sahu R., Shi Y., Srivastava S. In vitro and in vivo induction of apoptosis by capsaicin in pancreatic cancer cells is mediated through ROS generation and mitochondrial death pathway. Apoptosis 2008, 13:1465-1478.
40. Singh M., Singh N. Molecular mechanism of curcumin induced cytotoxicity in human cervical carcinoma cells. Mol. Cell. Biochem. 2009, 325:107-119.
41. Sun S.Y., Hail N., Lotan R. Apoptosis as a novel target for cancer chemoprevention. J. Nat. Cancer Inst. 2004, 96:662-672.