Gingerol sensitizes TRAIL-induced apoptotic cell death of glioblastoma cells

Toxicology and Applied Pharmacology

Volumn 279, Issue 3, 2014, Pages 253-265

  Lee, Dae Hee ^a   Kim, Dong Wook ^b   Jung, Chang Hwa ^c   Lee, Yong J ^a   Park, Daeho ^d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c Korea Food Research Institute   (South Korea)

^d Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

Apoptosis; Gingerol; Glioblastoma; P53; Reactive oxygen species (ROS); Tumor necrosis factor (TNF) related apoptosis inducing ligand (TRAIL)

Indexed keywords

CASPASE 3; CASPASE 7; DEATH RECEPTOR 5; FLICE INHIBITORY PROTEIN; GINGEROL; PROTEIN BCL 2; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; SURVIVIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; X LINKED INHIBITOR OF APOPTOSIS; (6) GINGEROL; PROTEIN BAX; PROTEIN BID;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER THERAPY; CELL DEATH; GINGER; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOBLOTTING; STABLE TRANSFECTION; APOPTOSIS; CANCER CELL; CONTROLLED STUDY; DRUG MECHANISM; DRUG SENSITIZATION; FEMALE; GLIOBLASTOMA; HCT116 CELL LINE; HELA CELL LINE; HEPG2 CELL LINE; LNCAP CELL LINE; MCF 7 CELL LINE; PROTEIN EXPRESSION;

APOPTOSIS; GINGEROL; GLIOBLASTOMA; P53; REACTIVE OXYGEN SPECIES (ROS); TUMOR NECROSIS FACTOR (TNF)-RELATED APOPTOSIS-INDUCING LIGAND (TRAIL);

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; ASTROCYTES; CASPASE 3; CASPASE 7; CATECHOLS; CELL LINE, TUMOR; FATTY ALCOHOLS; GLIOBLASTOMA; HUMANS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RNA, SMALL INTERFERING; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84907176517     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.06.030     Document Type: Article

References (44)

1. Aggarwal B.B. Signalling pathways of the TNF superfamily: a double-edged sword. Nat. Rev. Immunol. 2003, 3:745-756.
2. Bellail A.C., Tse M.C., Song J.H., Phuphanich S., Olson J.J., Sun S.Y., Hao C. DR5-mediated DISC controls caspase-8 cleavage and initiation of apoptosis in human glioblastomas. J. Cell. Mol. Med. 2010, 14:1303-1317.
3. Bode A.M., Ma W.Y., Surh Y.J., Dong Z. Inhibition of epidermal growth factor-induced cell transformation and activator protein 1 activation by [6]-gingerol. Cancer Res. 2001, 61:850-853.
4. Boerman R.H., Anderl K., Herath J., Borell T., Johnson N., Schaeffer-Klein J., Kirchhof A., Raap A.K., Scheithauer B.W., Jenkins R.B. The glial and mesenchymal elements of gliosarcomas share similar genetic alterations. J. Neuropathol. Exp. Neurol. 1996, 55:973-981.
5. Bonavia R., Inda M.M., Cavenee W.K., Furnari F.B. Heterogeneity maintenance in glioblastoma: a social network. Cancer Res. 2011, 71:4055-4060.
6. Bunz F., Dutriaux A., Lengauer C., Waldman T., Zhou S., Brown J.P., Sedivy J.M., Kinzler K.W., Vogelstein B. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 1998, 282:1497-1501.
7. Burger P.C., Vollmer R.T. Histologic factors of prognostic significance in the glioblastoma multiforme. Cancer 1980, 46:1179-1186.
8. Chakraborty D., Bishayee K., Ghosh S., Biswas R., Mandal S.K., Khuda-Bukhsh A.R. [6]-Gingerol induces caspase 3 dependent apoptosis and autophagy in cancer cells: drug-DNA interaction and expression of certain signal genes in HeLa cells. Eur. J. Pharmacol. 2012, 694:20-29.
9. Chang S.M., Wen P., Cloughesy T., Greenberg H., Schiff D., Conrad C., Fink K., Robins H.I., De Angelis L., Raizer J., Hess K., Aldape K., Lamborn K.R., Kuhn J., Dancey J., Prados M.D. Phase II study of CCI-779 in patients with recurrent glioblastoma multiforme. Invest. New Drugs 2005, 23:357-361.
10. de Wilt L.H., Kroon J., Jansen G., de Jong S., Peters G.J., Kruyt F.A. Bortezomib and TRAIL: a perfect match for apoptotic elimination of tumour cells?. Crit. Rev. Oncol. Hematol. 2013, 85:363-372.
11. Doherty L., Gigas D.C., Kesari S., Drappatz J., Kim R., Zimmerman J., Ostrowsky L., Wen P.Y. Pilot study of the combination of EGFR and mTOR inhibitors in recurrent malignant gliomas. Neurology 2006, 67:156-158.
12. Fuller G.N. The WHO Classification of Tumours of the Central Nervous System, 4th Edition. Arch. Pathol. Lab. Med. 2008, 132:906.
13. Galli R., Binda E., Orfanelli U., Cipelletti B., Gritti A., De Vitis S., Fiocco R., Foroni C., Dimeco F., Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004, 64:7011-7021.
14. Goudar R.K., Shi Q., Hjelmeland M.D., Keir S.T., McLendon R.E., Wikstrand C.J., Reese E.D., Conrad C.A., Traxler P., Lane H.A., Reardon D.A., Cavenee W.K., Wang X.F., Bigner D.D., Friedman H.S., Rich J.N. Combination therapy of inhibitors of epidermal growth factor receptor/vascular endothelial growth factor receptor 2 (AEE788) and the mammalian target of rapamycin (RAD001) offers improved glioblastoma tumor growth inhibition. Mol. Cancer Ther. 2005, 4:101-112.
15. Hawkins C.J. TRAIL and malignant glioma. Vitam. Horm. 2004, 67:427-452.
16. Ishiguro K., Ando T., Maeda O., Ohmiya N., Niwa Y., Kadomatsu K., et al. Ginger ingredients reduce viability of gastric cancer cells via distinct mechanisms. Biochem. Biophys. Res. Commun. 2007, 362:218-223.
17. Karsy M., Gelbman M., Shah P., Balumbu O., Moy F., Arslan E. Established and emerging variants of glioblastoma multiforme: review of morphological and molecular features. Folia Neuropathol. 2012, 50:301-321.
18. Krakstad C., Chekenya M. Survival signalling and apoptosis resistance in glioblastomas: opportunities for targeted therapeutics. Mol. Cancer 2010, 9:135.
19. Lee E., Surh Y.J. Induction of apoptosis in HL-60 cells by pungent vanilloids, [6]-gingerol and [6]-paradol. Cancer Lett. 1998, 134:163-168.
20. Lee S.H., Cekanova M., Baek S.J. Multiple mechanisms are involved in 6-gingerol-induced cell growth arrest and apoptosis in human colorectal cancer cells. Mol. Carcinog. 2008, 47:197-208.
21. Lee D.H., Rhee J.G., Lee Y.J. Reactive oxygen species up-regulate p53 and puma; a possible mechanism for apoptosis during combined treatment with TRAIL and wogonin. Brit. J. Pharm. 2009, 157:1189-1202.
22. Lee T.Y., Lee K.C., Chen S.Y., Chang H.H. 6-Gingerol inhibits ROS and iNOS through the suppression of PKC-alpha and NF-kappaB pathways in lipopolysaccharide-stimulated mouse macrophages. Biochem. Biophys. Res. Commun. 2009, 382:134-139.
23. Lin C.B., Lin C.C., Tsay G.J. 6-Gingerol inhibits growth of colon cancer cell LoVo via induction of G2/M arrest. Evid. Based Complement. Alternat. Med. 2012, 326096.
24. Lluis J.M., Nachbur U., Cook W.D., Gentle I.E., Moujalled D., Moulin M., Wong W.W., Khan N., Chau D., Callus B.A., Vince J.E., Silke J., Vaux D.L. TAK1 is required for survival of mouse fibroblasts treated with TRAIL, and does so by NF-kappaB dependent induction of cFLIPL. PLoS One 2010, 5:e8620.
25. Manzo F., Nebbioso A., Miceli M., Conte M., De Bellis F., Carafa V., Franci G., Tambaro F.P., Altucci L. TNF-related apoptosis-inducing ligand: signalling of a 'smart' molecule. Int. J. Biochem. Cell Biol. 2009, 41:460-466.
26. Nigam N., George J., Srivastava S., Roy P., Bhui K., et al. Induction of apoptosis by [6]-gingerol associated with the modulation of p53 and involvement of mitochondrial signaling pathway in B[a]P-induced mouse skin tumorigenesis. Cancer Chemother. Pharmacol. 2010, 65:687-696.
27. Ohgaki H., Kleihues P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J. Neuropathol. Exp. Neurol. 2005, 64:479-489.
28. Oyagbemi A.A., Saba A.B., Azeez O.I. Molecular targets of [6]-gingerol: its potential roles in cancer chemoprevention. Biofactors 2010, 36:169-178.
29. Panner A., Parsa A.T., Pieper R.O. Use of APO2L/TRAIL with mTOR inhibitors in the treatment of glioblastoma multiforme. Expert. Rev. Anticancer. Ther. 2006, 6:1313-1322.
30. Pitti R.M., Marsters S.A., Ruppert S., Donahue C.J., Moore A., Ashkenazi A. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 1996, 271:12687-12690.
31. Rao R.D., Mladek A.C., Lamont J.D., Goble J.M., Erlichman C., James C.D., Sarkaria J.N. Disruption of parallel and converging signaling pathways contributes to the synergistic antitumor effects of simultaneous mTOR and EGFR inhibition in GBM cells. Neoplasia 2005, 7:921-929.
32. Reardon D.A., Quinn J.A., Vredenburgh J.J., Gururangan S., Friedman A.H., Desjardins A., Sathornsumetee S., Herndon J.E., Dowell J.M., McLendon R.E., Provenzale J.M., Sampson J.H., Smith R.P., Swaisland A.J., Ochs J.S., Lyons P., Tourt-Uhlig S., Bigner D.D., Friedman H.S., Rich J.N. Phase 1 trial of gefitinib plus sirolimus in adults with recurrent malignant glioma. Clin. Cancer Res. 2006, 12:860-868.
33. Rich J.N., Reardon D.A., Peery T., Dowell J.M., Quinn J.A., Penne K.L., Wikstrand C.J., Van Duyn L.B., Dancey J.E., McLendon R.E., Kao J.C., Stenzel T.T., Ahmed Rasheed B.K., Tourt-Uhlig S.E., Herndon J.E., Vredenburgh J.J., Sampson J.H., Friedman A.H., Bigner D.D., Friedman H.S. Phase II trial of gefitinib in recurrent glioblastoma. J. Clin. Oncol. 2004, 22:133-142.
34. Roth W., Isenmann S., Naumann U., Kugler S., Bahr M., Dichgans J., Ashkenazi A., Weller M. Locoregional Apo2L/TRAIL eradicates intracranial human malignant glioma xenografts in athymic mice in the absence of neurotoxicity. Biochem. Biophys. Res. Commun. 1999, 265:479-483.
35. Saito R., Bringas J.R., Panner A., Tamas M., Pieper R.O., Berger M.S., Bankiewicz K.S. Convection-enhanced delivery of tumor necrosis factor-related apoptosis-inducing ligand with systemic administration of temozolomide prolongs survival in an intracranial glioblastoma xenograft model. Cancer Res. 2004, 64:6858-6862.
36. Shukla Y., Singh M. Cancer preventive properties of ginger: a brief review. Food Chem. Toxicol. 2007, 45:683-690.
37. Stupp R., Mason W.P., van den Bent M.J., Weller M., Fisher B., Taphoorn M.J., Belanger K., Brandes A.A., Marosi C., Bogdahn U., Curschmann J., Janzer R.C., Ludwin S.K., Gorlia T., Allgeier A., Lacombe D., Cairncross J.G., Eisenhauer E., Mirimanoff R.O. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352:987-996.
38. Stupp R., Hegi M.E., Mason W.P., van den Bent M.J., Taphoorn M.J., Janzer R.C., Ludwin S.K., Allgeier A., Fisher B., Belanger K., Hau P., Brandes A.A., Gijtenbeek J., Marosi C., Vecht C.J., Mokhtari K., Wesseling P., Villa S., Eisenhauer E., Gorlia T., Weller M., Lacombe D., Cairncross J.G., Mirimanoff R.O. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009, 10:459-466.
39. Surget S., Chiron D., Gomez-Bougie P., Descamps G., Menoret E., Bataille R., Moreau P., Le Gouill S., Amiot M., Pellat-Deceunynck C. Cell death via DR5, but not DR4, is regulated by p53 in myeloma cells. Cancer Res. 2012, 72:4562-4573.
40. van den Bent M.J., Brandes A.A., Rampling R., Kouwenhoven M.C., Kros J.M., Carpentier A.F., Clement P.M., Frenay M., Campone M., Baurain J.F., Armand J.P., Taphoorn M.J., Tosoni A., Kletzl H., Klughammer B., Lacombe D., Gorlia T. Randomized phase II trial of erlotinib versus temozolomide or carmustine in recurrent glioblastoma: EORTC brain tumor group study 26034. J. Clin. Oncol. 2009, 27:1268-1274.
41. Waldman T., Kinzler K.W., Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res. 1995, 55:5187-5190.
42. Wang S., El-Deiry W.S. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 2003, 22:8628-8633.
43. Wu G.S. TRAIL as a target in anti-cancer therapy. Cancer Lett. 2009, 285:1-5.
44. Yang G., Wang S., Zhong L., Dong X., Zhang W., Jiang L., Geng C., Sun X., Liu X., Chen M., Ma Y. 6-Gingerol induces apoptosis through lysosomal-mitochondrial axis in human hepatoma G2 cells. Phytother. Res. 2012, 26:1667-1673.