Curcumin inhibits the sonic hedgehog signaling pathway and triggers apoptosis in medulloblastoma cells

Molecular Carcinogenesis

Volumn 49, Issue 3, 2010, Pages 302-314

  Elamin, Maha H ^a   Shinwari, Zakia ^a   Hendrayani, Siti Faujiah ^a   Al Hindi, Hindi ^a   Al Shail, Essam ^a   Khafaga, Yasser ^a   Al kofide, Amani ^a   Aboussekhra, Abdelilah ^a,b  

^a KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^b ALFAISAL UNIVERSITY   (Saudi Arabia)

Author keywords

Bcl 2; Chemosensitization; Piperine; Radiosensitization

Indexed keywords

BETA CATENIN; CISPLATIN; CURCUMIN; CYCLIN D1; CYCLOPAMINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PIPERINE; PROTEIN BNIP3; PROTEIN KINASE B; PROTEIN PATCHED 1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; ANTINEOPLASTIC AGENT; MESSENGER RNA; SHH PROTEIN, HUMAN; VERATRUM ALKALOID;

APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENTIATION; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GAMMA RADIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MEDULLOBLASTOMA; ONCOGENE C MYB; ONCOGENE C MYC; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; CEREBELLUM TUMOR; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; ENZYME IMMUNOASSAY; FLOW CYTOMETRY; GENETICS; IMMUNOBLOTTING; METABOLISM; MITOCHONDRION; PATHOLOGY; RADIATION EXPOSURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ERINACEIDAE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CEREBELLAR NEOPLASMS; CURCUMIN; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; GAMMA RAYS; HEDGEHOG PROTEINS; HUMANS; IMMUNOBLOTTING; IMMUNOENZYME TECHNIQUES; MEDULLOBLASTOMA; MITOCHONDRIA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; VERATRUM ALKALOIDS;

EID: 77949890007     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20604     Document Type: Article

References (56)

1. Jozwiak J, Grajkowska W, Wlodarski P. Pathogenesis of medulloblastoma and current treatment outlook. Med Res Rev 2007;6:869-890.
2. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70.
3. Gilbertson RJ. Medulloblastoma: Signalling a change in treatment. Lancet Oncol 2004;5:209-218.
4. Wechsler-Reya RJ, Scott MP. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 1999;22:103-114.
5. Ho KS, Scott MP. Sonic hedgehog in the nervous system: Functions, modifications and mechanisms. Curr Opin Neurobiol 2002;12:57-63.
6. Hooper JE, Scott MP. Communicating with Hedgehogs. Nat Rev Mol Cell Biol 2005;6:306-317.
7. Kenney AM, Widlund HR, Rowitch DH. Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 2004;131:217-228.
8. Kenney AM, Cole MD, Rowitch DH. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 2003;130:15-28.
9. Knoepfler PS, Cheng PF, Eisenman RN. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev 2002;16:2699-2712.
10. Hatton BA, Knoepfler PS, Kenney AM, et al. N-myc is an essential downstream effector of Shh signaling during both normal and neoplastic cerebellar growth. Cancer Res 2006;66:8655-8661.
11. Aldosari N, Bigner SH, Burger PC, et al. MYCC and MYCN oncogene amplification in medulloblastoma. A fluorescence in situ hybridization study on paraffin sections from the Children's Oncology Group. Arch Pathol Lab Med 2002;126: 540-544.
12. Vita M, Henriksson M. The Myc oncoprotein as a therapeutic target for human cancer. Semin Cancer Biol 2006;16:318-330.
13. Scheurlen WG, Schwabe GC, Joos S, Mollenhauer J, Sorensen N, Kuhl J. Molecular analysis of childhood primitive neuroectodermal tumors defines markers associated with poor outcome. J Clin Oncol 1998;16:2478-2485.
14. Grotzer MA, Hogarty MD, Janss AJ, et al. MYC messenger RNA expression predicts survival outcome in childhood primitive neuroectodermal tumor/medulloblastoma. Clin Cancer Res 2001;7:2425-2433.
15. Bar EE, Chaudhry A, Farah MH, Eberhart CG. Hedgehog signaling promotes medulloblastoma survival via BclII. Am J Pathol 2007;170:347-355.
16. McCall TD, Pedone CA, Fults DW. Apoptosis suppression by somatic cell transfer of Bcl-2 promotes Sonic hedgehog-dependent medulloblastoma formation in mice. Cancer Res 2007;67:5179-5185.
17. Rao G, Pedone CA, Del Valle L, Reiss K, Holland EC, Fults DW. Sonic hedgehog and insulin-like growth factor signaling synergize to induce medulloblastoma formation from nestin-expressing neural progenitors in mice. Oncogene 2004;23: 6156-6162.
18. Gajjar A, Chintagumpala M, Ashley D, et al. Risk-adapted craniospinal radiotherapy followed by high-dose chemotherapy and stem-cell rescue in children with newly diagnosed medulloblastoma (St Jude Medulloblastoma-96): Long-term results from a prospective, multicentre trial. Lancet Oncol 2006;7:813-820.
19. Brandes AA, Paris MK. Review of the prognostic factors in medulloblastoma of children and adults. Crit Rev Oncol Hematol 2004;50:121-128.
20. Rood BR, Macdonald TJ, Packer RJ. Current treatment of medulloblastoma: Recent advances and future challenges. Semin Oncol 2004;31:666-675.
21. Rossi A, Caracciolo V, Russo G, Reiss K, Giordano A. Medulloblastoma: From molecular pathology to therapy. Clin Cancer Res 2008;14:971-976.
22. Grill J, Sainte-Rose C, Jouvet A, et al. Treatment of medulloblastoma with postoperative chemotherapy alone: An SFOP prospective trial in young children. Lancet Oncol 2005;6:573-580.
23. Garg AK, Buchholz TA, Aggarwal BB. Chemosensitization and radiosensitization of tumors by plant polyphenols. Antioxid Redox Signal 2005;7:1630-1647.
24. Surh YJ. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 2003;3:768-780.
25. Goel A, Kunnumakkara AB, Aggarwal BB. Curcumin as "Curecumin": From kitchen to clinic. Biochem Pharmacol 2007;19:19.
26. Aggarwal BB, Kumar A, Bharti AC. Anticancer potential of curcumin: Preclinical and clinical studies. Anticancer Res 2003;23:363-398.
27. Syng-Ai C, Kumari AL, Khar A. Effect of curcumin on normal and tumor cells: Role of glutathione and bcl-2. Mol Cancer Ther 2004;3:1101-1108.
28. Bhattacharyya S, Mandal D, Saha B, Sen GS, Das T, Sa G. Curcumin prevents tumor-induced T cell apoptosis through Stat-5a-mediated Bcl-2 induction. J Biol Chem 2007;282: 15954-15964.
29. Raffel C. Medulloblastoma: Molecular genetics and animal models. Neoplasia 2004;6:310-322.
30. Oliver TG, Grasfeder LL, Carroll AL, et al. Transcriptional profiling of the Sonic hedgehog response: A critical role for N-myc in proliferation of neuronal precursors. Proc Natl Acad Sci USA 2003;100:7331-7336.
31. Bigelow RL, Chari NS, Unden AB, et al. Transcriptional regulation of bcl-2 mediated by the sonic hedgehog signaling pathway through gli-1. J Biol Chem 2004;279:1197-1205.
32. Hoseong Yang, S, Andl, T, Grachtchouk, V, et al. Pathological responses to oncogenic Hedgehog signaling in skin are dependent on canonical Wnt/beta-catenin signaling. Nat Genet 2008;40:1130-1135.
33. Berman DM, Karhadkar SS, Hallahan AR, et al. Medulloblastoma growth inhibition by hedgehog pathway blockade. Science 2002;297:1559-1561.
34. Romer JT, Kimura H, Magdaleno S, et al. Suppression of the Shh pathway using a small molecule inhibitor eliminates medulloblastoma in Ptc1(+/-)p53(-/-) mice. Cancer Cell 2004;6:229-240.
35. Chen JK, Taipale J, Cooper MK, Beachy PA. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev 2002;16:2743-2748.
36. Shoba G, Joy D, Joseph T, Majeed M, Rajendran R, Srinivas PS. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med 1998;64:353-356.
37. Strimpakos AS, Sharma RA. Curcumin: Preventive and therapeutic properties in laboratory studies and clinical trials. Antioxid Redox Signal 2008;10:511-545.
38. Bala K, Tripathy BC, Sharma D. Neuroprotective and antiageing effects of curcumin in aged rat brain regions. Biogerontology 2006;7:81-89.
39. Yang F, Lim GP, Begum AN, et al. Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J Biol Chem 2005; 280:5892-5901.
40. Ryu EK, Choe YS, Lee KH, Choi Y, Kim BT. Curcumin and dehydrozingerone derivatives: Synthesis, radiolabeling, and evaluation for beta-amyloid plaque imaging. J Med Chem 2006;49:6111-6119.
41. Pan MH, Huang TM, Lin JK. Biotransformation of curcumin through reduction and glucuronidation in mice. Drug Metab Dispos 1999;27:486-494.
42. Cole GM, Teter B, Frautschy SA. Neuroprotective effects of curcumin. Adv Exp Med Biol 2007;595:197-212.
43. Thangapazham RL, Sharma A, Maheshwari RK. Multiple molecular targets in cancer chemoprevention by curcumin. AAPS J 2006;8:E443-E449.
44. Schuller U, Heine VM, Mao J, et al. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 2008;14:123-134.
45. Yang ZJ, Ellis T, Markant SL, et al. Medulloblastoma can be initiated by deletion of Patched in lineage-restricted progenitors or stem cells. Cancer Cell 2008;14:135-145.
46. Hartmann W, Digon-Sontgerath B, Koch A, et al. Phosphatidylinositol 3′-kinase/AKT signaling is activated in medulloblastoma cell proliferation and is associated with reduced expression of PTEN. Clin Cancer Res 2006;12:3019-3027.
47. Taipale J, Beachy PA. The Hedgehog and Wnt signalling pathways in cancer. Nature 2001;411:349-354.
48. Henriksson M, Luscher B. Proteins of the Myc network: Essential regulators of cell growth and differentiation. Adv Cancer Res 1996;68:109-182.
49. Altieri DC, Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer 2008;8:61-70.
50. Haberler C, Slavc I, Czech T, et al. Histopathological prognostic factors in medulloblastoma: High expression of survivin is related to unfavourable outcome. Eur J Cancer 2006;42:2996-3003.
51. Romer J,Curran T. Targeting medulloblastoma: Small-molecule inhibitors of the Sonic Hedgehog pathway as potential cancer therapeutics. Cancer Res 2005;65:4975-4978.
52. Bar EE, Stearns D. New developments in medulloblastoma treatment: The potential of a cyclopamine-lovastatin combination. Expert Opin Investig Drugs 2008;17:185-195.
53. Li M, Zhang Z, Hill DL, Wang H, Zhang R. Curcumin, a dietary component, has anticancer, chemosensitization, and radiosensitization effects by down-regulating the MDM2 oncogene through the PI3K/mTOR/ETS2 pathway. Cancer Res 2007;67:1988-1996.
54. Kunnumakkara AB, Guha S, Krishnan S, Diagaradjane P, Gelovani J, Aggarwal BB. Curcumin potentiates antitumor activity of gemcitabine in an orthotopic model of pancreatic cancer through suppression of proliferation, angiogenesis, and inhibition of nuclear factor-kappaB-regulated gene products. Cancer Res 2007;67:3853-3861.
55. Bava SV, Puliappadamba VT, Deepti A, Nair A, Karunagaran D, Anto RJ. Sensitization of taxol-induced apoptosis by curcumin involves down-regulation of nuclear factor-kappaB and the serine/threonine kinase Akt and is independent of tubulin polymerization. J Biol Chem 2005;280:6301-6308.
56. Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB. Bioavailability of curcumin: Problems and promises. Mol Pharm 2007;4:807-818.