Cancer Letters
Volume 291, Issue 1 , Pages 20-30 , 1 May 2010

Honokiol induces cell apoptosis in human chondrosarcoma cells through mitochondrial dysfunction and endoplasmic reticulum stress

  • Ying-Ju Chen

      Affiliations

    • Institute of Toxicology, National Taiwan University, Taipei, Taiwan, ROC
    • These authors contributed equally to this work.
  • ,
  • Chien-Lin Wu

      Affiliations

    • Department of Physical Medicine and Rehabilitation, Changhua Christian Hospital, Changhua, Taiwan, ROC
  • ,
  • Ju-Fang Liu

      Affiliations

    • Graduate Institute of Pharmaceutical Chemistry, China Medical University, Taichung, Taiwan, ROC
  • ,
  • Yi-Chin Fong

      Affiliations

    • School of Chinese Medicine, China Medical University, Taichung, Taiwan, ROC
    • Graduate Institute of Chinese Medical Science, China Medical University, Taichung, Taiwan, ROC
    • Department of Orthopaedic, China Medical University Hospital, Taichung, Taiwan, ROC
    • These authors contributed equally to this work.
  • ,
  • Sheng-Feng Hsu

      Affiliations

    • Graduate Institute of Acupuncture Science, China Medical University, Taichung, Taiwan, ROC
  • ,
  • Te-Mao Li

      Affiliations

    • Graduate Institute of Acupuncture Science, China Medical University, Taichung, Taiwan, ROC
  • ,
  • Yi-Chang Su

      Affiliations

    • Graduate Institute of Chinese Medical Science, China Medical University, Taichung, Taiwan, ROC
  • ,
  • Shing-Hwa Liu

      Affiliations

    • Institute of Toxicology, National Taiwan University, Taipei, Taiwan, ROC
    • Corresponding Author InformationCorresponding authors. Address: Department of Pharmacology, College of Medicine, China Medical University, No. 91, Hsueh-Shih Road, Taichung, Taiwan, ROC. Tel.: +886 4 22053366x2228; fax: +886 4 22053764 (C.-H. Tang).
  • ,
  • Chih-Hsin Tang

      Affiliations

    • Department of Pharmacology, China Medical University, Taichung, Taiwan, ROC
    • Graduate Institute of Basic Medical Science, China Medical University, Taichung, Taiwan, ROC
    • Corresponding Author InformationCorresponding authors. Address: Department of Pharmacology, College of Medicine, China Medical University, No. 91, Hsueh-Shih Road, Taichung, Taiwan, ROC. Tel.: +886 4 22053366x2228; fax: +886 4 22053764 (C.-H. Tang).

Received 16 May 2009 ,Revised 25 August 2009 ,Accepted 25 August 2009.

References 

  1. Terek RM, Schwartz GK, Devaney K, Glantz L, Mak S, Healey JH, et al. Chemotherapy and P-glycoprotein expression in chondrosarcoma. J. Orthop. Res. 1998;16:585–590
  2. Yuan J, Dutton CM, Scully SP. RNAi mediated MMP-1 silencing inhibits human chondrosarcoma invasion. J. Orthop. Res. 2005;23:1467–1474
  3. AbouEl Hassan MA, Braam SR, Kruyt FA. Paclitaxel and vincristine potentiate adenoviral oncolysis that is associated with cell cycle and apoptosis modulation, whereas they differentially affect the viral life cycle in non-small-cell lung cancer cells. Cancer Gene Ther. 2006;13:1105–1114
  4. Liou KT, Shen YC, Chen CF, Tsao CM, Tsai SK. Honokiol protects rat brain from focal cerebral ischemia–reperfusion injury by inhibiting neutrophil infiltration and reactive oxygen species production. Brain Res. 2003;992:159–166
  5. Lo YC, Teng CM, Chen CF, Chen CC, Hong CY. Magnolol and honokiol isolated from Magnolia officinalis protect rat heart mitochondria against lipid peroxidation. Biochem. Pharmacol. 1994;47:549–553
  6. Chiang CK, Sheu ML, Hung KY, Wu KD, Liu SH. Honokiol, a small molecular weight natural product, alleviates experimental mesangial proliferative glomerulonephritis. Kidney Int. 2006;70:682–689
  7. Park J, Lee J, Jung E, Park Y, Kim K, Park B, et al. In vitro antibacterial and anti-inflammatory effects of honokiol and magnolol against Propionibacterium sp.. Eur. J. Pharmacol. 2004;496:189–195
  8. Bai X, Cerimele F, Ushio-Fukai M, Waqas M, Campbell PM, Govindarajan B, et al. Honokiol, a small molecular weight natural product, inhibits angiogenesis in vitro and tumor growth in vivo. J. Biol. Chem. 2003;278:35501–35507
  9. Ishitsuka K, Hideshima T, Hamasaki M, Raje N, Kumar S, Hideshima H, et al. Honokiol overcomes conventional drug resistance in human multiple myeloma by induction of caspase-dependent and -independent apoptosis. Blood. 2005;106:1794–1800
  10. Battle TE, Arbiser J, Frank DA. The natural product honokiol induces caspase-dependent apoptosis in B-cell chronic lymphocytic leukemia (B-CLL) cells. Blood. 2005;106:690–697
  11. Abcouwer SF, Marjon PL, Loper RK, Vander Jagt DL. Response of VEGF expression to amino acid deprivation and inducers of endoplasmic reticulum stress. Invest. Ophthalmol. Vis. Sci. 2002;43:2791–2798
  12. Soboloff J, Berger SA. Sustained ER Ca2+ depletion suppresses protein synthesis and induces activation-enhanced cell death in mast cells. J. Biol. Chem. 2002;277:13812–13820
  13. Yung HW, Korolchuk S, Tolkovsky AM, Charnock-Jones DS, Burton GJ. Endoplasmic reticulum stress exacerbates ischemia–reperfusion-induced apoptosis through attenuation of Akt protein synthesis in human choriocarcinoma cells. FASEB J. 2007;21:872–884
  14. Feldman DE, Chauhan V, Koong AC. The unfolded protein response: a novel component of the hypoxic stress response in tumors. Mol. Cancer Res. 2005;3:597–605
  15. Moenner M, Pluquet O, Bouchecareilh M, Chevet E. Integrated endoplasmic reticulum stress responses in cancer. Cancer Res. 2007;67:10631–10634
  16. Lee AS. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 2001;26:504–510
  17. Little E, Ramakrishnan M, Roy B, Gazit G, Lee AS. The glucose-regulated proteins (GRP78 and GRP94): functions, gene regulation, and applications. Crit. Rev. Eukaryot. Gene Expr. 1994;4:1–18
  18. Kubota H, Suzuki T, Lu J, Takahashi S, Sugita K, Sekiya S, et al. 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
  19. Fu Y, Lee AS. Glucose regulated proteins in cancer progression, drug resistance and immunotherapy. Cancer Biol. Ther. 2006;5:741–744
  20. Tomida A, Yun J, Tsuruo T. Glucose-regulated stresses induce resistance to camptothecin in human cancer cells. Int. J. Cancer. 1996;68:391–396
  21. Liu S, Wang H, Yang Z, Kon T, Zhu J, Cao Y, et al. Enhancement of cancer radiation therapy by use of adenovirus-mediated secretable glucose-regulated protein 94/gp96 expression. Cancer Res. 2005;65:9126–9131
  22. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 2003;4:552–565
  23. Tan Y, Dourdin N, Wu C, De Veyra T, Elce JS, Greer PA. Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress-induced apoptosis. J. Biol. Chem. 2006;281:16016–16024
  24. Sheu ML, Liu SH, Lan KH. Honokiol induces calpain-mediated glucose-regulated protein-94 cleavage and apoptosis in human gastric cancer cells and reduces tumor growth. PLoS One. 2007;2:e1096
  25. Yoshida H, Haze K, Yanagi H, Yura T, Mori K. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J. Biol. Chem. 1998;273:33741–33749
  26. Chiu YC, Yang RS, Hsieh KH, Fong YC, Way TD, Lee TS, et al. Stromal cell-derived factor-1 induces matrix metalloprotease-13 expression in human chondrocytes. Mol. Pharmacol. 2007;72:695–703
  27. Dijkers PF, Birkenkamp KU, Lam EW, Thomas NS, Lammers JW, Koenderman L, et al. FKHR-L1 can act as a critical effector of cell death induced by cytokine withdrawal: protein kinase B-enhanced cell survival through maintenance of mitochondrial integrity. J. Cell Biol. 2002;156:531–542
  28. Ye J, Wang S, Leonard SS, Sun Y, Butterworth L, Antonini J, et al. Role of reactive oxygen species and p53 in chromium(VI)-induced apoptosis. J. Biol. Chem. 1999;274:34974–34980
  29. Benali-Furet NL, Chami M, Houel L, De Giorgi F, Vernejoul F, Lagorce D, et al. Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion. Oncogene. 2005;24:4921–4933
  30. Thastrup O, Cullen PJ, Drobak BK, Hanley MR, Dawson AP. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc. Natl. Acad. Sci. USA. 1990;87:2466–2470
  31. Fong YC, Yang WH, Hsu SF, Hsu HC, Tseng KF, Hsu CJ, et al. 2-methoxyestradiol induces apoptosis and cell cycle arrest in human chondrosarcoma cells. J. Orthop. Res. 2007;25:1106–1114
  32. Susin SA, Zamzami N, Castedo M, Daugas E, Wang HG, Geley S, et al. The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis. J. Exp. Med. 1997;186:25–37
  33. Zamzami N, Brenner C, Marzo I, Susin SA, Kroemer G. Subcellular and submitochondrial mode of action of Bcl-2-like oncoproteins. Oncogene. 1998;16:2265–2282
  34. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 1996;86:147–157
  35. Adams JM, Cory S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci. 2001;26:61–66
  36. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 1999;13:1211–1233
  37. Lin SS, Huang HP, Yang JS, Wu JY, Hsia TC, Lin CC, et al. DNA damage and endoplasmic reticulum stress mediated curcumin-induced cell cycle arrest and apoptosis in human lung carcinoma A-549 cells through the activation caspases cascade- and mitochondrial-dependent pathway. Cancer Lett. 2008;272:77–90
  38. Joyce MA, Walters KA, Lamb SE, Yeh MM, Zhu LF, Kneteman N, et al. HCV induces oxidative and ER stress, and sensitizes infected cells to apoptosis in SCID/Alb-uPA mice. PLoS Pathog. 2009;5:e1000291
  39. Hsu YL, Wu LY, Kuo PL. Dehydrocostuslactone, a medicinal plant-derived sesquiterpene lactone, induces apoptosis coupled to endoplasmic reticulum stress in liver cancer cells. J. Pharmacol. Exp. Ther. 2009;329:808–819
  40. Fettucciari K, Fetriconi I, Mannucci R, Nicoletti I, Bartoli A, Coaccioli S, et al. Group B Streptococcus induces macrophage apoptosis by calpain activation. J. Immunol. 2006;176:7542–7556
  41. Pezzuto JM. Plant-derived anticancer agents. Biochem. Pharmacol. 1997;53:121–133
  42. Park EJ, Min HY, Chung HJ, Hong JY, Kang YJ, Hung TM, et al. Down-regulation of c-Src/EGFR-mediated signaling activation is involved in the honokiol-induced cell cycle arrest and apoptosis in MDA-MB-231 human breast cancer cells. Cancer Lett. 2009;277:133–140
  43. Raja SM, Chen S, Yue P, Acker TM, Lefkove B, Arbiser JL, et al. The natural product honokiol preferentially inhibits cellular FLICE-inhibitory protein and augments death receptor-induced apoptosis. Mol. Cancer Ther. 2008;7:2212–2223

PII: S0304-3835(09)00625-9

doi: 10.1016/j.canlet.2009.08.032

Cancer Letters
Volume 291, Issue 1 , Pages 20-30 , 1 May 2010