Resveratrol Enhances the Antitumor Effects of Temozolomide in Glioblastoma via ROS-dependent AMPK-TSC-mTOR Signaling Pathway

CNS Neuroscience and Therapeutics

Volumn 18, Issue 7, 2012, Pages 536-546

  Yuan, Yuan ^a,b   Xue, Xue ^a   Guo, Ruo Bing ^a   Sun, Xiu Lan ^a   Hu, Gang ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b JIANGSU CANCER HOSPITAL   (China)

Author keywords

AMPK; Glioblastoma; MTOR; Resveratrol; Temozolomide

Indexed keywords

ADENYLATE KINASE; GELATINASE B; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; RESVERATROL; TEMOZOLOMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME ACTIVATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MIGRATION INHIBITION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR VOLUME;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; CALCIUM-BINDING PROTEINS; CELL LINE, TUMOR; DACARBAZINE; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; FEMALE; GLIOBLASTOMA; HUMANS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, NUDE; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STILBENES; TOR SERINE-THREONINE KINASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84863516150     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/j.1755-5949.2012.00319.x     Document Type: Article

References (43)

1. Stupp R, Mason WP, van den Bent MJ, et al. European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group, Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-996.
2. Louis DN, Holland EC, Cairncross JG. Glioma classification: A molecular reappraisal. Am J Pathol 2001;159:779-786.
3. Uzzaman M, Keller G, Germano IM. Enhanced proapoptotic effects of tumor necrosis factor-related apoptosis-inducing ligand on temozolomide resistant glioma cells. J Neurosurg 2007;106:646-651.
4. Tentori L, Graziani G. Recent approaches to improve the antitumor efficacy of Temozolomide. Curr Med Chem 2009;16:245-257.
5. Gagliano N, Moscheni C, Torri C, et al. Effect of resveratrol on matrix metalloproteinase-2 (MMP-2) and secreted protein acidic and rich in cysteine (SPARC) on human cultured glioblastoma cells. Biomed Pharmacother 2005;59:359-364.
6. Boocock DJ, Faust GE, Patel KR, et al. Phase I dose escalation pharmacokinetic study in healthy volunteers of resveratrol, a potential cancer chemopreventive agent. Cancer Epidemiol Biomarkers Prev 2007;16:1246-1252.
7. Almeida L, Vaz-da-Silva M, Falcão A, et al. Pharmacokinetic and safety profile of trans-resvertral in a rising multiple-dose study in healthy volunteers. Mol Nutr Food Res 2009;53(Suppl 1):S7-S15.
8. Nunes T, Almeida L, Rocha JF, et al. Pharmacokinetics of trans-resveratrol following repeated administration in healthy elderly and young subjects. J Clin Pharmacol 2009;49:1477-1482.
9. Jang M, Cai L, Udeani GO, et al. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 1997;275:218-220.
10. Narayanan BA, Narayanan NK, Stoner GD, et al. Interactive gene expression pattern in prostate cancer cells exposed to phenolic antioxidants. Life Sci 2002;70:1821-1839.
11. Gupta SC, Kannappan R, Reuter S, et al. Chemosensitization of tumors by resveratrol. Ann N Y Acad Sci 2011;1215:150-160.
12. Bhardwaj A, Sethi G, Vadhan-Raj S, et al. Resveratrol inhibits proliferation, induces apoptosis, and overcomes chemoresistance through down-regulation of STAT3 and nuclear factor kappa B-regulated anti-apoptotic and cell survival gene products in human multiple myeloma cells. Blood 2007;109:2293-2302.
13. Kubota T, Uemura Y, Kobayashi M, Taguchi H. Combined effects of resveratrol and paclitaxel on lung cancer cells. Anticancer Res 2003;23:4039-4046.
14. Nigg EA. Centrosome aberrations: Cause or consequence of cancer progression? Nat Rev Cancer 2002;2:815-825.
15. Lee SC, Chan JY, Pervaiz S. Spontaneous and 5-fluorouracil-induced centrosome amplification lowers the threshold to resveratrol-evoked apoptosis in colon cancer cells. Cancer Let 2010;288:6-41.
16. Harikumar KB, Kunnumakkara AB, Sethi G, et al. Resveratrol, a multitargeted agent, can enhance antitumor activity of gemcitabine in vitro and in orthotopic mousemodel of human pancreatic cancer. Int J Cancer 2010;127:257-268.
17. Lal S, Lacroix M, Tofilon P, et al. An implantable guide screw system for brain tumor studies in small animals. J Neurosurg 2000;92:326-333.
18. Brada M, Judson I, Beale P, et al. Phase I dose-escalation and pharmacokinetic study of temozolomide(SCH 52365) for refractory or relapsing malignancies. Br J Cancer 1999;81:1022-1030.
19. Kawamata H, Tachibana M, Fujimori T, Imai Y. Differentiation-inducing therapy for solid tumors. Curr Pharm Des 2006;12:379-385.
20. Kim DS, Woo ER, Chae SW, et al. Plantainoside D protects adriamycin-induced apoptosis in H9c2 cardiac muscle cells via the inhibition of ROS generation and NF-kappaB activation. Life Sci 2007;80:314-323.
21. Zhang JF, Liu JJ, Lu MQ, et al. Rapamycin inhibits cell growth by induction of apoptosis on hepatocellular carcinoma cells in vitro. Transpl Immunol 2007;17:162-168.
22. Kim WH, Lee JW, Suh YH, et al. AICAR potentiates ROS production induced by chronic high glucose: Roles of AMPK in pancreatic beta-cell apoptosis. Cell Signal 2007;19:791-805.
23. Kopelovich L, Fay JR, Sigman CC, Crowell JA. The mammalian target of rapamycin pathway as a potential target for cancer chemoprevention. Cancer Epidemiol Biomarkers Prev 2007;16:1330-1340.
24. Meric-Bernstam F, Gonzalez-Angulo AM. Targeting the mTOR signaling network for cancer therapy. J Clin Oncol 2009;27:2278-2287.
25. Garami A, Zwartkruis FJ, Nobukuni T, et al. Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol Cell 2003;11:1457-1466.
26. Guha A, Mukherjee J. Advances in the biology of astrocytomas. Curr Opin Neurol 2004;17:655-662.
27. Zhang JF, Liu JJ, Lu MQ, et al. Rapamycin inhibits cell growth by induction of apoptosis on hepatocellular carcinoma cells in vitro. Transpl Immunol 2007;17:162-168.
28. Romano MF, Avellino R, Petrella A, et al. Rapamycin inhibits doxorubicin-induced NF-kappaB/Rel nuclear activity and enhances the apoptosis of melanoma cells. Eur J Cancer 2004;40:2829-2836.
29. Saha AK, Persons K, Safer JD, et al. AMPK regulation of the growth of cultured human keratinocytes. Biochem Biophys Res Commun 2006;349:519-524.
30. Motoshima H, Goldstein BJ, Igata M, Araki E. AMPK and cell proliferation-AMPK as a therapeutic target for atherosclerosis and cancer. J Physiol 2006;574:63-71.
31. Yu SY, Chan DW, Liu VW, Ngan HY. Inhibition of cervical cancer cell growth through activation of upstream kinases of AMP-activated protein kinase. Tumour Biol 2009;30:80-85.
32. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003;115:577-590.
33. Wang W, Guan KL. AMP-activated protein kinase and cancer. Acta Physiol (Oxf) 2009;196:55-63.
34. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003;115:577-590.
35. Cheng SW, Fryer LG, Carling D, Shepherd PR. Thr2446 is a novel mammalian target of rapamycin (mTOR) phosphorylation site regulated by nutrient status. J Biol Chem 2004;279:15719-15722.
36. Cantley LC, Neel BG. New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc Natl Acad Sci U S A 1999;96:4240-4245.
37. Yu SY, Chan DW, Liu VW, Ngan HY. Inhibition of cervical cancer cell growth through activation of upstream kinases of AMP-activated protein kinase. Tumour Biol 2009;30:80-85.
38. Zhou H, Huang S. mTOR signaling in cancer cell motility and tumor metastasis. Crit Rev Eukaryot Gene Expr 2010;20:1-16.
39. Lee PP, Hwang JJ, Murphy G, Ip MM. Functional significance of MMP-9 in tumor necrosis factor-induced proliferation and branching morphogenesis of mammary epithelial cells. Endocrinology 2000;14:3764-3773.
40. Waas ET, Lomme RM, DeGroot J, et al. Tissue levels of active matrix metalloproteinase-2 and -9 in colorectal cancer. Br J Cancer 2002;86:1876-1883.
41. Hiratsuka S, Nakamura K, Iwai S, et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2002;2:289-300.
42. Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000;2:737-744.
43. Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000;103:481-490.