Inhibition of EGFR signaling augments oridonin-induced apoptosis in human laryngeal cancer cells via enhancing oxidative stress coincident with activation of both the intrinsic and extrinsic apoptotic pathways

Cancer Letters

Volumn 294, Issue 2, 2010, Pages 147-158

  Kang, Ning ^a   Zhang, Jing Hai ^a   Qiu, Feng ^a   Tashiro, Shin ichi ^b   Onodera, Satoshi ^b   Ikejima, Takashi ^a  

^a SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

^b SHOWA PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Epidermal growth factor receptor (EGFR); Extrinsic apoptosis; Intrinsic apoptosis; Oridonin; Reactive oxygen species (ROS)

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; ACETYLCYSTEINE; APOPTOSIS INDUCING FACTOR; CASPASE 3; CASPASE 8; CASPASE 9; EPIDERMAL GROWTH FACTOR RECEPTOR; FAS ASSOCIATED DEATH DOMAIN PROTEIN; ORIDONIN; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; SIRTUIN 1;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG STRUCTURE; GENE AMPLIFICATION; GENE EXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; LARYNX CANCER; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; UPREGULATION;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; BCL-2-ASSOCIATED X PROTEIN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; DITERPENES, KAURANE; DRUG SYNERGISM; ENZYME INHIBITORS; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; HUMANS; LARYNGEAL NEOPLASMS; MEMBRANE POTENTIAL, MITOCHONDRIAL; OXIDATIVE STRESS; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SIRTUIN 1; TYRPHOSTINS;

RABDOSIA RUBESCENS;

EID: 77953359873     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2010.01.032     Document Type: Article

References (50)

1. Debatin K.M. Activation of apoptosis pathways by anti-cancer treatment. Toxicol. Lett. 2000, 112/113:41-48.
2. Wilson M.R. Apoptotic signal transduction: emerging pathways. Biochem. Cell Biol. 1998, 76:573-582.
3. Daugas E., Nochy D., Ravagnan L., Loeffler M., Susin S.A., Zamzami N., Kroemer G. Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett. 2000, 476:118-123.
4. Sun X.M., MacFarlane M., Zhuang J., Wolf B.B., Green D.R., Cohen G.M. Distinct caspase cascades are initiated in receptor-mediated and chemical induced apoptosis. J. Biol. Chem. 1999, 274:5053-5060.
5. Strasser A., O'Connor L., Dixit V.M. Apoptosis signaling. Annu. Rev. Biochem. 2000, 69:217-225.
6. Ohsawa I., Ishikawa M., Takahashi K., Watanabe M., Nishimaki K., Yamagata K., Katsura K., Katayama Y., Asoh S., Ohta S. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat. Med. 2007, 13:688-694.
7. Nathan C. Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J. Clin. Invest. 2003, 111:769-778.
8. Kang Y.H., Lee E., Choi M.K., Ku J.L., Kim S.H., Park Y.G., Lim S.J. Role of reactive oxygen species in the induction of apoptosis by alpha-tocopherol succinate. Int. J. Cancer 2004, 112:385-392.
9. Simbula G., Columbano A., Ledda-Columbano G.M., Sanna L., Deidda M., Diana A., Pibiri M. Increased ROS generation and p53 activation in alpha-lipoic acid-induced apoptosis of hepatoma cells. Apoptosis 2007, 12:113-123.
10. Reinecke F., Levanets O., Olivier Y., Louw R., Semete B., Grobler A., Hidalgo J., Smeitink J., Olckers A., Van der Westhuizen F.H. Metallothionein isoform 2A expression is inducible and protects against ROS-mediated cell death in rotenone-treated HeLa cells. Biochem. J. 2006, 395:405-415.
11. Bublil E.M., Yarden Y. The EGF receptor family: superheading a merger of signaling and therapeutics. Curr. Opin. Cell Biol. 2007, 19:124-134.
12. Baselga J., Arteaga C.L. Critical update and emerging trends in epidermal growth factor receptor targeting in cancer. J. Clin. Oncol. 2005, 23:2445-2459.
13. Raymond E., Faivre S., Armand J.P. Epidermal growth factor receptor tyrosine kinase as a target for anticancer therapy. Drugs 2000, 60(Suppl 1):15-23.
14. Shin D.M., Ro J.Y., Hong W.K., Hittelman W.N. Dysregulation of epidermal growth factor receptor expression in multistep process of head and neck tumorigenesis. Cancer Res. 1994, 4:3153-3159.
15. Li F.C., Li Y.H., Zhao X., Fu W.N., Xu Z.M., Li Z.G., Sun K.L. Association of homozygous deletion of p15 and p16 gene and amplification of EGFR gene in laryngeal squamous cell carcinoma. Acta Genetica Sinica. 2004, 31:109-113.
16. Li F.C., Kang N., Fu W.N., Sun X.H., Gao H.M., Sun K.L. Detection of epidermal growth factor receptor gene amplification in human laryngeal carcinomas by means of fluorescence in situ hybridization. Chin. J. Med. Genet. 2000, 17:278-280.
17. Boscheli D.H. Small molecule inhibitors of receptor tyrosine kinases. Drugs Future 1999, 24:515-537.
18. Chen Z., Zhang X., Li M., Wang Z., Wieand H.S., Grandis J.R., Shin D.M. 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. 2004, 10:5930-5939.
19. Fujita T., Takeda Y., Sun H.D., Minami Y., Marunaka T., Takeda S., Yamada Y., Togo T. Cytotoxic and antitumor activities of Rabdosia diterpenoids. Planta. Med. 1988, 54:414-417.
20. Osawa K., Yasuda H., Maruyama T., Morita H., Takeya K., Stomata H. Antibacteria trichorabdal diterpenes from rabdosia trichocarpa. Phytochemistry 1994, 36:1287-1291.
21. Huang J., Wu L., Tashiro S., Onodera S., Ikejima T. Reactive oxygen species mediate oridonin-induced HepG2 apoptosis through p53, MAPK, and mitochondrial signaling pathways. J. Pharmacol. Sci. 2008, 107:370-379.
22. Li D., Wu L.J., Tashiro S., Onodera S., Ikejima T. Oridonin-induced A431 cell apoptosis partially through blockage of the Ras/Raf/ERK signal pathway. J. Pharmacol. Sci. 2007, 103:56-66.
23. Murakawa T., Tsuda H., Tanimoto T., Tanabe T., Kitahara S., Matsubara O. Expression of KIT, EGFR, HER-2 and tyrosine phosphorylation in undifferentiated thyroid carcinoma: implication for a new therapeutic approach. Pathol. Int. 2005, 55:757-765.
24. Bianco R., Gelardi T., Damiano V., Ciardiello F., Tortora G. Rational bases for the development of EGFR inhibitors for cancer treatment. Int. J. Biochem. Cell Biol. 2007, 34:1416-1431.
25. Chou T.C. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev. 2006, 58:621-681.
26. Yang M.L., Huang T.S., Lee Y., Lu F.J. Free radical scavenging properties of sulfinpyrazone. Free Radical Res. 2002, 36:685-693.
27. Saris N.E., Teplova V.V., Odinokova I.V., Azarashvily T.S. Interference of calmidazolium with measurement of mitochondrial membrane potential using the tetraphenylphosphonium electrode or the fluorescent probe rhodamine 123. Anal. Biochem. 2004, 328:109-112.
28. Shin T.Y., Kim S.H., Suk K., Ha J.H., Kim I., Lee M.G., Jun C.D., Kim S.Y., Lim J.P., Eun J.S., Shin H.Y., Kim H.M. Anti-allergic effects of Lycopus lucidus on mast cell-mediated allergy model. Toxicol. Appl. Pharmacol. 2005, 209:255-262.
29. Sablina A.A., Budanov A.V., Ilyinskaya G.V., Agapova L.S., Kravchenko J.E., Chumakov P. The antioxidant function of the p53 tumor suppressor. Nat. Med. 2005, 11:1306-1313.
30. Wong Y.T., Ruan R., Tay F.E. Relationship between levels of oxidative DNA damage, lipid peroxidation and mitochondrial membrane potential in young and old F344 rats. Free Radical Res. 2006, 40:393-402.
31. Cohen H.Y., Lavu S., Bitterman K.J., Hekking B., Imahiyerobo T.A., Miller C., Frye R., Ploegh H., Kessler B.M., Sinclair D.A. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol. Cell 2004, 13:627-638.
32. Mitsiades C.S., Poulaki V., Fanourakis G., Sozopoulos E., McMillin D., Wen Z., Voutsinas G., Tseleni-Balafouta S., Mitsiades N. Fas signaling in thyroid carcinomas is diverted from apoptosis to proliferation. Clin. Cancer Res. 2006, 12:3705-3712.
33. Sakahira H., Enari M., Nagata S. Functional differences of two forms of the inhibitor of caspase-activated DNase, ICAD-L, and ICAD-S. J. Bio. Chem. 1999, 274:15740-15744.
34. Mi Y.C., Thomas S.D., Xu X.H., Casson L.K., Miller D.M., Bates P.J. Apoptosis in leukemia cell is accompanied by alterations in the level and localization of nucleolin. J. Bio. Chem. 2003, 278:8572-8579.
35. Marioni G., Marchese-Ragona R., Cartei G., Marchese F., Staffieri A. Current opinion in diagnosis and treatment of laryngeal carcinoma. Cancer Treat. Rev. 2006, 32:504-515.
36. Rafferty M.A., Fenton J.E., Jones A.S. The history, aetiology and epidemiology of laryngeal carcinoma. Clin. Otolaryngol. Allied Sci. 2001, 26:442-446.
37. Lee K.H. Anticancer drug design based on plant-derived natural products. J. Biomed. Sci. 1999, 6:236-250.
38. Takayama K., Ishida K., Matsushita T., Fujita N., Hayashi S., Sasaki K., Tei K., Kubo S., Matsumoto T., Fujioka H., Kurosaka M., Kuroda R. SIRT1 regulation of apoptosis of human chondrocytes. Arthritis Rheum 2009, 60:2731-2740.
39. Skvortsov S., Skvortsova I., Sarg B., Loeffler-Ragg J., Lindner H., Lukas P., Tabernero J., Zwierzina H. Irreversible pan-ErbB tyrosine kinase inhibitor CI-1033 induces caspase-independent apoptosis in colorectal cancer DiFi cell line. Apoptosis 2005, 10:1175-1186.
40. Zheng T.S., Hunot S., Kuida K., Momoi T., Srinivasan A., Nicholson D.W., Lazebnik Y., Flavell R.A. Deficiency in caspase-9 or caspase-3 induces compensatory caspase activation. Nat. Med. 2000, 6:1241-1247.
41. Herrera B., Alvarez A.M., Sánchez A., Fernández M., Roncero C., Benito M., Fabregat I. Reactive oxygen species (ROS) mediates the mitochondrial-dependent apoptosis induced by transforming growth factor (beta) in fetal hepatocytes. FASEB J. 2001, 15:741-751.
42. Herrera B., Fernández M., Alvarez A.M., Roncero C., Benito M., Gil J., Fabregat I. Activation of caspases occurs downstream from radical oxygen species production, Bcl-xL down-regulation, and early cytochrome c release in apoptosis induced by transforming growth factor beta in rat fetal hepatocytes. Hepatology 2001, 34:548-556.
43. Ramjaun A.R., Tomlinson S., Eddaoudi A., Downward J. Upregulation of two BH3-only proteins, Bmf and Bim, during TGF beta-induced apoptosis. Oncogene 2007, 26:970-981.
44. Chandra J., Samali A., Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radical Biol. Med. 2000, 29:323-333.
45. Efferth T., Ramirez T., Gebhart E., Halatsch M.E. Combination treatment of glioblastoma multiforme cell lines with the anti-malarial artesunate and the epidermal growth factor receptor tyrosine kinase inhibitor OSI-774. Biochem. Pharmacol. 2004, 67:1689-1700.
46. Pu Y.S., Hsieh M.W., Wang C.W., Liu G.Y., Huang C.Y., Lin C.C., et al. Epidermal growth factor receptor inhibitor (PD168393) potentiates cytotoxic effects of paclitaxel against androgen-independent prostate cancer cells. Biochem. Pharmacol. 2006, 71:751-760.
47. Reinehr R., Häussinger D. Epidermal growth factor receptor signaling in liver cell proliferation and apoptosis. Biol. Chem. 2009, 390:1033-1037.
48. Iwase M., Takaoka S., Uchida M., Yoshiba S., Kondo G., Watanabe H., Ohashi M., Nagumo M. Epidermal growth factor receptor inhibitors enhance susceptibility to Fas-mediated apoptosis in oral squamous cell carcinoma cells. Oral Oncol. 2008, 44:361-368.
49. Bae S.S., Choi J.H., Oh Y.S., Perry D.K., Ryu S.H., Suh P.G. Proteolytic cleavage of epidermal growth factor receptor by caspases. FEBS Lett. 2001, 491:16-20.
50. Zhuang S., Ouedraogo G.D., Kochevar I.E. Downregulation of epidermal growth factor receptor signaling by singlet oxygen through activation of caspase-3 and protein phosphatases. Oncogene 2003, 22:4413-4424.