Helenalin-induced apoptosis is dependent on production of reactive oxygen species and independent of induction of endoplasmic reticulum stress in renal cell carcinoma

Toxicology in Vitro

Volumn 27, Issue 2, 2013, Pages 588-596

  Jang, Ji Hoon ^a   Iqbal, Taha ^a   Min, Kyoung Jin ^a   Kim, Shin ^a   Park, Jong Wook ^a   Son, Eun Ik ^a   Lee, Tae Jin ^b   Kwon, Taeg Kyu ^a  

^a Keimyung University   (South Korea)

^b Yeungnam University College of Medicine   (South Korea)

Author keywords

Apoptosis; ATF4; Bcl 2; CHOP; Helenalin; ROS

Indexed keywords

ACETYLCYSTEINE; ACTIVATING TRANSCRIPTION FACTOR 4; GLUTATHIONE ETHYL ESTER; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HELENALIN; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA;

ACTIVATING TRANSCRIPTION FACTOR 4 GENE; APOPTOSIS; ARTICLE; CANCER CELL; CCAAT ENHANCER BINDING PROTEIN HOMOLOGOUS PROTEIN GENE; CELL STRAIN HCT116; CELL STRAIN HT29; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; GENE; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; REGULATED IN DEVELOPMENT AND DNA DAMAGE RESPONSE 1 GENE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; CELL SURVIVAL; DNA FRAGMENTATION; ENDOPLASMIC RETICULUM STRESS; HUMANS; KIDNEY NEOPLASMS; REACTIVE OXYGEN SPECIES; SESQUITERPENES;

EID: 84875243083     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2012.10.014     Document Type: Article

References (42)

1. Armstrong J.L., Flockhart R., Veal G.J., Lovat P.E., Redfern C.P. Regulation of endoplasmic reticulum stress-induced cell death by ATF4 in neuroectodermal tumor cells. J. Biol. Chem. 2010, 285:6091-6100.
2. Averous J., Bruhat A., Jousse C., Carraro V., Thiel G., Fafournoux P. Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation. J. Biol. Chem. 2004, 279:5288-5297.
3. Berges C., Fuchs D., Opelz G., Daniel V., Naujokat C. Helenalin suppresses essential immune functions of activated CD4+ T cells by multiple mechanisms. Mol. Immunol. 2009, 46:2892-2901.
4. Borner C., Monney L. Apoptosis without caspases: an inefficient molecular guillotine?. Cell Death Differ. 1999, 6:497-507.
5. Broker L.E., Huisman C., Span S.W., Rodriguez J.A., Kruyt F.A., Giaccone G. Cathepsin B mediates caspase-independent cell death induced by microtubule stabilizing agents in non-small cell lung cancer cells. Cancer Res. 2004, 64:27-30.
6. Ellgaard L., Molinari M., Helenius A. Setting the standards: quality control in the secretory pathway. Science 1999, 286:1882-1888.
7. Fawcett T.W., Martindale J.L., Guyton K.Z., Hai T., Holbrook N.J. Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem. J. 1999, 339(Pt 1):135-141.
8. Fulda S. Tumor resistance to apoptosis. Int. J. Cancer 2009, 124:511-515.
9. Galehdar Z., Swan P., Fuerth B., Callaghan S.M., Park D.S., Cregan S.P. Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP-mediated induction of the Bcl-2 homology 3-only member PUMA. J. Neurosci. 2010, 30:16938-16948.
10. Genestra M. Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Cell. Signal. 2007, 19:1807-1819.
11. Gething M.J., Sambrook J. Protein folding in the cell. Nature 1992, 355:33-45.
12. Hall I.H., Lee K.H., Starnes C.O., Sumida Y., Wu R.Y., Waddell T.G., Cochran J.W., Gerhart K.G. Anti-inflammatory activity of sesquiterpene lactones and related compounds. J. Pharm. Sci. 1979, 68:537-542.
13. Hall I.H., Starnes C.O., Lee K.H., Waddell T.G. Mode of action of sesquiterpene lactones as anti-inflammatory agents. J. Pharm. Sci. 1980, 69:537-543.
14. Hall I.H., Williams W.L., Grippo A.A., Lee K.H., Holbrook D.J., Chaney S.G. Inhibition of nucleic acid synthesis in P-388 lymphocytic leukemia cells in culture by sesquiterpene lactones. Anticancer Res. 1988, 8:33-42.
15. Hengartner M.O. The biochemistry of apoptosis. Nature 2000, 407:770-776.
16. Henson P.M., Hume D.A. Apoptotic cell removal in development and tissue homeostasis. Trends Immunol. 2006, 27:244-250.
17. Hoffmann R., von Schwarzenberg K., Lopez-Anton N., Rudy A., Wanner G., Dirsch V.M., Vollmar A.M. Helenalin bypasses Bcl-2-mediated cell death resistance by inhibiting NF-kappaB and promoting reactive oxygen species generation. Biochem. Pharmacol. 2011, 82:453-463.
18. Huang P.R., Yeh Y.M., Wang T.C. Potent inhibition of human telomerase by helenalin. Cancer Lett. 2005, 227:169-174.
19. Jiang F., Zhang Y., Dusting G.J. NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol. Rev. 2011, 63:218-242.
20. Kamesaki S., Kamesaki H., Jorgensen T.J., Tanizawa A., Pommier Y., Cossman J. Bcl-2 protein inhibits etoposide-induced apoptosis through its effects on events subsequent to topoisomerase II-induced DNA strand breaks and their repair. Cancer Res. 1993, 53:4251-4256.
21. Kaufman R.J. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 1999, 13:1211-1233.
22. Kerr J.F., Winterford C.M., Harmon B.V. Apoptosis. Its significance in cancer and cancer therapy. Cancer 1994, 73:2013-2026.
23. Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 1972, 26:239-257.
24. LeBel C.P., Ischiropoulos H., Bondy S.C. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 1992, 5:227-231.
25. Lee K.H., Hall I.H., Mar E.C., Starnes C.O., ElGebaly S.A., Waddell T.G., Hadgraft R.I., Ruffner C.G., Weidner I. Sesquiterpene antitumor agents: inhibitors of cellular metabolism. Science 1977, 196:533-536.
26. Malhotra J.D., Kaufman R.J. The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 2007, 18:716-731.
27. Michel P.P., Lambeng N., Ruberg M. Neuropharmacologic aspects of apoptosis: significance for neurodegenerative diseases. Clin. Neuropharmacol. 1999, 22:137-150.
28. Mori K. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 2000, 101:451-454.
29. 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.
30. Rashedi I., Panigrahi S., Ezzati P., Ghavami S., Los M. Autoimmunity and apoptosis-therapeutic implications. Curr. Med. Chem. 2007, 14:3139-3151.
31. Rasheva V.I., Domingos P.M. Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 2009, 14:996-1007.
32. Rigoulet M., Yoboue E.D., Devin A. Mitochondrial ROS generation and its regulation: mechanisms involved in H(2)O(2) signaling. Antioxid. Redox Signal. 2011, 14:459-468.
33. Schroder H., Losche W., Strobach H., Leven W., Willuhn G., Till U., Schror K. Helenalin and 11 alpha,13-dihydrohelenalin, two constituents from Arnica montana L., inhibit human platelet function via thiol-dependent pathways. Thromb. Res. 1990, 57:839-845.
34. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006, 7:880-885.
35. Tatton W.G., Olanow C.W. Apoptosis in neurodegenerative diseases: the role of mitochondria. Biochim. Biophys. Acta 1999, 1410:195-213.
36. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
37. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
38. Whitney M.L., Jefferson L.S., Kimball S.R. ATF4 is necessary and sufficient for ER stress-induced upregulation of REDD1 expression. Biochem. Biophys. Res. Commun. 2009, 379:451-455.
39. Woehlbier U., Hetz C. Modulating stress responses by the UPRosome: a matter of life and death. Trends Biochem. Sci. 2011, 36:329-337.
40. Worth A., Thrasher A.J., Gaspar H.B. Autoimmune lymphoproliferative syndrome: molecular basis of disease and clinical phenotype. Br. J. Haematol. 2006, 133:124-140.
41. Yip K.W., Reed J.C. Bcl-2 family proteins and cancer. Oncogene 2008, 27:6398-6406.
42. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., Stevens J.L., Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 1998, 12:982-995.