Cancer Letters
Volume 294, Issue 2 , Pages 147-158 , 28 August 2010

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

  • Ning Kang

      Affiliations

    • China-Japan Research Institute of Medical and Pharmaceutical Sciences, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang, 110016, PR China
    • Department of Biochemistry and Molecular Biology, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang, 110016, PR China
  • ,
  • Jing-Hai Zhang

      Affiliations

    • Department of Biochemistry and Molecular Biology, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang, 110016, PR China
  • ,
  • Feng Qiu

      Affiliations

    • Department of Natural Products Chemistry, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang, 110016, PR China
  • ,
  • Shin-ichi Tashiro

      Affiliations

    • Department of Clinical and Biomedical Science, Showa Pharmaceutical University, Tokyo 194-8543, Japan
  • ,
  • Satoshi Onodera

      Affiliations

    • Department of Clinical and Biomedical Science, Showa Pharmaceutical University, Tokyo 194-8543, Japan
  • ,
  • Takashi Ikejima

      Affiliations

    • China-Japan Research Institute of Medical and Pharmaceutical Sciences, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang, 110016, PR China
    • Corresponding Author InformationCorresponding author. Address: China-Japan Research Institute of Medical and Pharmaceutical Sciences, Shenyang Pharmaceutical University, 103 Wenhua Road, Shenyang, Liaoning 110016, PR China. Tel./fax: +86 24 2384 4463.

Received 6 November 2009 ,Revised 9 January 2010 ,Accepted 24 January 2010.

References 

  1. Debatin KM. Activation of apoptosis pathways by anti-cancer treatment. Toxicol. Lett. 2000;112/113:41–48
  2. Wilson MR. Apoptotic signal transduction: emerging pathways. Biochem. Cell Biol. 1998;76:573–582
  3. Daugas E, Nochy D, Ravagnan L, Loeffler M, Susin SA, Zamzami N, et al. Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett. 2000;476:118–123
  4. Sun XM, MacFarlane M, Zhuang J, Wolf BB, Green DR, Cohen GM. 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 VM. Apoptosis signaling. Annu. Rev. Biochem. 2000;69:217–225
  6. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, et al. 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 YH, Lee E, Choi MK, Ku JL, Kim SH, Park YG, et al. 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 GM, Sanna L, Deidda M, Diana A, et al. 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, et al. 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 EM, 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 CL. 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 JP. Epidermal growth factor receptor tyrosine kinase as a target for anticancer therapy. Drugs. 2000;60(Suppl 1):15–23
  14. Shin DM, Ro JY, Hong WK, Hittelman WN. Dysregulation of epidermal growth factor receptor expression in multistep process of head and neck tumorigenesis. Cancer Res. 1994;4:3153–3159
  15. Li FC, Li YH, Zhao X, Fu WN, Xu ZM, Li ZG, et al. 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 FC, Kang N, Fu WN, Sun XH, Gao HM, Sun KL. 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 DH. Small molecule inhibitors of receptor tyrosine kinases. Drugs Future. 1999;24:515–537
  18. Chen Z, Zhang X, Li M, Wang Z, Wieand HS, Grandis JR, et al. 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 HD, Minami Y, Marunaka T, Takeda S, et al. 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 LJ, 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 TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev. 2006;58:621–681
  26. Yang ML, Huang TS, Lee Y, Lu FJ. Free radical scavenging properties of sulfinpyrazone. Free Radical Res. 2002;36:685–693
  27. Saris NE, Teplova VV, Odinokova IV, Azarashvily TS. 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 TY, Kim SH, Suk K, Ha JH, Kim I, Lee MG, et al. Anti-allergic effects of Lycopus lucidus on mast cell-mediated allergy model. Toxicol. Appl. Pharmacol. 2005;209:255–262
  29. Sablina AA, Budanov AV, Ilyinskaya GV, Agapova LS, Kravchenko JE, Chumakov P. The antioxidant function of the p53 tumor suppressor. Nat. Med. 2005;11:1306–1313
  30. Wong YT, Ruan R, Tay FE. 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 HY, Lavu S, Bitterman KJ, Hekking B, Imahiyerobo TA, Miller C, et al. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol. Cell. 2004;13:627–638
  32. Mitsiades CS, Poulaki V, Fanourakis G, Sozopoulos E, McMillin D, Wen Z, et al. 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 YC, Thomas SD, Xu XH, Casson LK, Miller DM, Bates PJ. 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 MA, Fenton JE, Jones AS. The history, aetiology and epidemiology of laryngeal carcinoma. Clin. Otolaryngol. Allied Sci. 2001;26:442–446
  37. Lee KH. 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, et al. 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, et al. 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 TS, Hunot S, Kuida K, Momoi T, Srinivasan A, Nicholson DW, et al. Deficiency in caspase-9 or caspase-3 induces compensatory caspase activation. Nat. Med. 2000;6:1241–1247
  41. Herrera B, Alvarez AM, Sánchez A, Fernández M, Roncero C, Benito M, et al. 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 AM, Roncero C, Benito M, Gil J, et al. 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 AR, 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 ME. 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 YS, Hsieh MW, Wang CW, Liu GY, Huang CY, Lin CC, 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, et al. 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 SS, Choi JH, Oh YS, Perry DK, Ryu SH, Suh PG. Proteolytic cleavage of epidermal growth factor receptor by caspases. FEBS Lett. 2001;491:16–20
  50. Zhuang S, Ouedraogo GD, Kochevar IE. Downregulation of epidermal growth factor receptor signaling by singlet oxygen through activation of caspase-3 and protein phosphatases. Oncogene. 2003;22:4413–4424

PII: S0304-3835(10)00058-3

doi: 10.1016/j.canlet.2010.01.032

Cancer Letters
Volume 294, Issue 2 , Pages 147-158 , 28 August 2010