Norcantharidin impairs medulloblastoma growth by inhibition of Wnt/β-catenin signaling

Journal of Neuro-Oncology

Volumn 106, Issue 1, 2012, Pages 59-70

  Cimmino, Flora ^a,b   Scoppettuolo, Maria Nunzia ^a,b   Carotenuto, Marianeve ^a,b   De Antonellis, Pasqualino ^a,b   Dato, Valeria Di ^a,b   De Vita, Gennaro ^a,b   Zollo, Massimo ^a,b  

^a CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Catenin; Medulloblastoma; TOP FOP FLASH; Wnt signaling; Xenograft

Indexed keywords

BETA CATENIN; CANTHARIDIN; NORCANTHARIDIN; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; CANCER INHIBITION; CELL DIFFERENTIATION; CELL NUCLEUS; CEREBELLUM TUMOR; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MEDULLOBLASTOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BETA CATENIN; BICYCLO COMPOUNDS, HETEROCYCLIC; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; G2 PHASE; GENES, REPORTER; INDICATORS AND REAGENTS; LUCIFERASES; MEDULLOBLASTOMA; MICE; MICE, SCID; NEOPLASM TRANSPLANTATION; POLYMERASE CHAIN REACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 83055173058     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-011-0645-y     Document Type: Article

References (59)

1. JM de Bont RJ Packer EM Michiels ML den Boer R Pieters 2008 Biological background of pediatric medulloblastoma and ependymoma: a review from a translational research perspective Neuro Oncol 10 6 1040 1060 18676356 10.1215/15228517-2008-059
2. Q Wang H Li N Liu XY Chen ML Wu KL Zhang QY Kong J Liu 2008 Correlative analyses of notch signaling with resveratrol-induced differentiation and apoptosis of human medulloblastoma cells Neurosci Lett 438 2 168 173 18456406 10.1016/j.neulet.2008.04.012 1:CAS:528:DC%2BD1cXmtlWiu7k%3D
3. ZJ Yang T Ellis SL Markant TA Read JD Kessler M Bourboulas U Schuller R Machold G Fishell DH Rowitch BJ Wainwright RJ Wechsler-Reya 2008 Medulloblastoma can be initiated by deletion of patched in lineage-restricted progenitors or stem cells Cancer Cell 14 2 135 145 18691548 10.1016/j.ccr.2008.07.003 1:CAS:528:DC%2BD1cXhtVSrtrjP
4. RJ Gilbertson DW Ellison 2008 The origins of medulloblastoma subtypes Annu Rev Pathol 3 341 365 18039127 10.1146/annurev.pathmechdis.3.121806.151518 1:CAS:528:DC%2BD1cXjsFersLo%3D (Pubitemid 351488285)
5. F Guessous Y Li R Abounader 2008 Signaling pathways in medulloblastoma J Cell Physiol 217 3 577 583 18651559 10.1002/jcp.21542 1:CAS:528: DC%2BD1cXhtlOqt7zL
6. MA Grotzer K von Hoff AO von Bueren T Shalaby W Hartmann M Warmuth-Metz A Emser RD Kortmann J Kuehl T Pietsch S Rutkowski 2007 Which clinical and biological tumor markers proved predictive in the prospective multicenter trial HIT'91-implications for investigating childhood medulloblastoma Klin Padiatr 219 6 312 317 18050040 10.1055/s-2007-985843 1:STN:280:DC%2BD1c%2FgvFyhuw%3D%3D (Pubitemid 350244522)
7. S Pfister M Remke A Benner F Mendrzyk G Toedt J Felsberg A Wittmann F Devens NU Gerber S Joos A Kulozik G Reifenberger S Rutkowski OD Wiestler B Radlwimmer W Scheurlen P Lichter A Korshunov 2009 Outcome prediction in pediatric medulloblastoma based on DNA copy-number aberrations of chromosomes 6q and 17q and the MYC and MYCN loci J Clin Oncol 27 10 1627 1636 19255330 10.1200/JCO.2008.17.9432
8. DW Ellison M Kocak J Dalton H Megahed ME Lusher SL Ryan W Zhao SL Nicholson RE Taylor S Bailey SC Clifford 2010 Definition of disease-risk stratification groups in childhood medulloblastoma using combined clinical, pathologic, and molecular variables J Clin Oncol 29 1400 1407 20921458 10.1200/JCO.2010.30.2810
9. SC Clifford K O'Toole DW Ellison 2009 Chromosome 1q gain is not associated with a poor outcome in childhood medulloblastoma: requirements for the validation of potential prognostic biomarkers Cell Cycle 8 5 787 19221477 10.4161/cc.8.5.7709 1:CAS:528:DC%2BD1MXlvFWisr8%3D
10. M Kool J Koster J Bunt NE Hasselt A Lakeman P van Sluis D Troost NS Meeteren HN Caron J Cloos A Mrsic B Ylstra W Grajkowska W Hartmann T Pietsch D Ellison SC Clifford R Versteeg 2008 Integrated genomics identifies five medulloblastoma subtypes with distinct genetic profiles, pathway signatures and clinicopathological features PLoS One 3 8 e3088 18769486 10.1371/journal.pone. 0003088
11. PA Northcott A Korshunov H Witt T Hielscher CG Eberhart S Mack E Bouffet SC Clifford CE Hawkins P French JT Rutka S Pfister MD Taylor 2010 Medulloblastoma comprises four distinct molecular variants J Clin Oncol 29 11 1408 1414 20823417 10.1200/JCO.2009.27.4324
12. DJ Holthouse PB Dallas J Ford V Fabian AR Murch M Watson G Wong C Bertram S Egli DL Baker UR Kees 2009 Classic and desmoplastic medulloblastoma: complete case reports and characterizations of two new cell lines Neuropathology 29 4 398 409 19077040 10.1111/j.1440-1789.2008.00989.x
13. Y Katoh M Katoh 2009 Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation Curr mol med 9 7 873 886 19860666 10.2174/156652409789105570 1:CAS:528:DC%2BD1MXht1SrtbzL
14. A Perez-Martinez A Lassaletta M Gonzalez-Vicent J Sevilla MA Diaz L Madero 2005 High-dose chemotherapy with autologous stem cell rescue for children with high risk and recurrent medulloblastoma and supratentorial primitive neuroectodermal tumors J Neurooncol 71 1 33 38 15719272 10.1007/s11060-004-4527- 4 1:CAS:528:DC%2BD2MXhtlCjsLfJ (Pubitemid 40277251)
15. HA Rogers S Miller J Lowe MA Brundler B Coyle RG Grundy 2009 An investigation of WNT pathway activation and association with survival in central nervous system primitive neuroectodermal tumours (CNS PNET) Br J Cancer 100 8 1292 1302 19293793 10.1038/sj.bjc.6604979 1:CAS:528:DC%2BD1MXksF2gtrk%3D
16. DW Ellison OE Onilude JC Lindsey ME Lusher CL Weston RE Taylor AD Pearson SC Clifford 2005 Beta-catenin status predicts a favorable outcome in childhood medulloblastoma: the United Kingdom children's cancer study group brain tumour committee J Clin Oncol 23 31 7951 7957 16258095 10.1200/JCO.2005.01.5479 1:CAS:528:DC%2BD2MXht1CqsL7P (Pubitemid 46657395)
17. L Rogers J Pattisapu RR Smith P Parker 1988 Medulloblastoma in association with the Coffin-Siris syndrome Childs Nerv Syst 4 1 41 44 2456854 1:STN:280:DyaL1c3psFSitQ%3D%3D (Pubitemid 18087054)
18. Y Zhai R Wu DR Schwartz D Darrah H Reed FT Kolligs MT Nieman ER Fearon KR Cho 2002 Role of beta-catenin/T-cell factor-regulated genes in ovarian endometrioid adenocarcinomas Am J Pathol 160 4 1229 1238 11943708 10.1016/S0002-9440(10)62550-3 1:CAS:528:DC%2BD38XjsFGjsbk%3D (Pubitemid 34411627)
19. T Efferth R Rauh S Kahl M Tomicic H Bochzelt ME Tome MM Briehl R Bauer B Kaina 2005 Molecular modes of action of cantharidin in tumor cells Biochem Pharmacol 69 5 811 818 15710358 10.1016/j.bcp.2004.12.003 1:CAS:528: DC%2BD2MXhtlCrsb0%3D (Pubitemid 40248623)
20. R Rauh S Kahl H Boechzelt R Bauer B Kaina T Efferth 2007 Molecular biology of cantharidin in cancer cells Chin Med 2 8 17610718 10.1186/1749-8546-2-8
21. HB Shan YC Cai Y Liu WN Zeng HX Chen BT Fan XH Liu ZL Xu B Wang LJ Xian 2006 Cytotoxicity of cantharidin analogues targeting protein phosphatase 2A Anticancer Drugs 17 8 905 911 16940800 10.1097/01.cad.0000217428.90325.35 1:CAS:528:DC%2BD28XovVWjt7s%3D (Pubitemid 44350609)
22. SK Huan HH Lee DZ Liu CC Wu CC Wang 2006 Cantharidin-induced cytotoxicity and cyclooxygenase 2 expression in human bladder carcinoma cell line Toxicology 223 1-2 136 143 16697099 10.1016/j.tox.2006.03.012 1:CAS:528: DC%2BD28XkvVyntrw%3D (Pubitemid 43744401)
23. DC Dorn CA Kou KJ Png MA Moore 2009 The effect of cantharidins on leukemic stem cells Int J Cancer 124 9 2186 2199 19123473 10.1002/ijc.24157 1:CAS:528:DC%2BD1MXktVWnu7g%3D
24. M Sagawa T Nakazato H Uchida Y Ikeda M Kizaki 2008 Cantharidin induces apoptosis of human multiple myeloma cells via inhibition of the JAK/STAT pathway Cancer Sci 99 9 1820 1826 18544087 10.1111/j.1349-7006.2008.00872.x 1:CAS:528:DC%2BD1cXhtFKntbjL
25. TA Hill SG Stewart B Sauer J Gilbert SP Ackland JA Sakoff A McCluskey 2007 Heterocyclic substituted cantharidin and norcantharidin analogues-synthesis, protein phosphatase (1 and 2A) inhibition, and anti-cancer activity Bioorg Med Chem Lett 17 12 3392 3397 17451951 10.1016/j.bmcl.2007.03. 093 1:CAS:528:DC%2BD2sXmtVals7g%3D (Pubitemid 46819022)
26. TA Hill SG Stewart CP Gordon SP Ackland J Gilbert B Sauer JA Sakoff A McCluskey 2008 Norcantharidin analogues: synthesis, anticancer activity and protein phosphatase 1 and 2A inhibition Chem Med Chem 3 12 1878 1892 19025735 1:CAS:528:DC%2BD1MXotl2q
27. A McCluskey SP Ackland MC Bowyer ML Baldwin J Garner CC Walkom JA Sakoff 2003 Cantharidin analogues: synthesis and evaluation of growth inhibition in a panel of selected tumour cell lines Bioorg Chem 31 1 68 79 12697169 10.1016/S0045-2068(02)00524-2 1:CAS:528:DC%2BD3sXivFelt70%3D (Pubitemid 36411927)
28. Y Huang Q Liu K Liu K Yagasaki G Zhang 2009 Suppression of growth of highly-metastatic human breast cancer cells by norcantharidin and its mechanisms of action Cytotechnology 59 3 209 19649717 10.1007/s10616-009-9221-0
29. J Luan H Duan Q Liu K Yagasaki G Zhang 2010 Inhibitory effects of norcantharidin against human lung cancer cell growth and migration Cytotechnology 62 4 349 355 20087654 10.1007/s10616-009-9250-8 1:CAS:528:DC%2BC3cXhsVSisrjE
30. YJ Chen YM Tsai CD Kuo KL Ku HS Shie HF Liao 2009 Norcantharidin is a small-molecule synthetic compound with anti-angiogenesis effect Life Sci 85 17-18 642 651 19765597 10.1016/j.lfs.2009.09.003 1:CAS:528:DC%2BD1MXht1GntLrN
31. YN Chen JC Chen SC Yin GS Wang W Tsauer SF Hsu SL Hsu 2002 Effector mechanisms of norcantharidin-induced mitotic arrest and apoptosis in human hepatoma cells Int J Cancer 100 2 158 165 12115564 10.1002/ijc.10479 1:CAS:528:DC%2BD38XkvFynsr4%3D (Pubitemid 34666189)
32. SH Kok SJ Cheng CY Hong JJ Lee SK Lin YS Kuo CP Chiang MY Kuo 2005 Norcantharidin-induced apoptosis in oral cancer cells is associated with an increase of proapoptotic to antiapoptotic protein ratio Cancer Lett 217 1 43 52 15596295 10.1016/j.canlet.2004.07.045 1:CAS:528:DC%2BD2cXhtVKksbfJ (Pubitemid 39642865)
33. SH Kok CY Hong MY Kuo CH Lee JJ Lee IU Lou MS Lee M Hsiao SK Lin 2003 Comparisons of norcantharidin cytotoxic effects on oral cancer cells and normal buccal keratinocytes Oral Oncol 39 1 19 26 12457717 10.1016/S1368-8375(01)00129- 4 1:STN:280:DC%2BD3s%2FgtVSnuw%3D%3D (Pubitemid 35385638)
34. C Peng X Liu E Liu K Xu W Niu R Chen J Wang Z Zhang P Lin J Wang M Agrez J Niu 2009 Norcantharidin induces HT-29 colon cancer cell apoptosis through the alphavbeta6-extracellular signal-related kinase signaling pathway Cancer Sci 100 12 2302 2308 19744110 10.1111/j.1349-7006.2009.01320.x 1:CAS:528: DC%2BD1MXhsFOltrjM
35. K Bonness IV Aragon B Rutland S Ofori-Acquah NM Dean RE Honkanen 2006 Cantharidin-induced mitotic arrest is associated with the formation of aberrant mitotic spindles and lagging chromosomes resulting, in part, from the suppression of PP2A-alpha Mol Cancer Ther 5 11 2727 2736 17121919 10.1158/1535-7163.MCT-06-0273 1:CAS:528:DC%2BD28Xht1els7nE (Pubitemid 44848999)
36. J Yang J Wu C Tan PS Klein 2003 PP2A:B56epsilon is required for Wnt/beta-catenin signaling during embryonic development Development 130 23 5569 5578 14522869 10.1242/dev.00762 1:CAS:528:DC%2BD3sXpvV2hsbc%3D (Pubitemid 37540834)
37. W Li L Xie Z Chen Y Zhu Y Sun Y Miao Z Xu X Han 2010 Cantharidin, a potent and selective PP2A inhibitor, induces an oxidative stress-independent growth inhibition of pancreatic cancer cells through G2/M cell-cycle arrest and apoptosis Cancer Sci 101 5 1226 1233 20331621 10.1111/j.1349-7006.2010.01523.x 1:CAS:528:DC%2BC3cXmsF2qur0%3D
38. JA Sakoff SP Ackland ML Baldwin MA Keane A McCluskey 2002 Anticancer activity and protein phosphatase 1 and 2A inhibition of a new generation of cantharidin analogues Invest New Drugs 20 1 1 11 12003183 10.1023/A: 1014460818734 1:CAS:528:DC%2BD38Xjt1ylt7c%3D (Pubitemid 34251646)
39. F Cimmino JH Schulte M Zollo J Koster R Versteeg A Iolascon A Eggert A Schramm 2009 Galectin-1 is a major effector of TrkB-mediated neuroblastoma aggressiveness Oncogene 28 19 2015 2023 19363525 10.1038/onc.2009.70 1:CAS:528:DC%2BD1MXksVemsbs%3D
40. L Garzia I Andolfo E Cusanelli N Marino G Petrosino D De Martino V Esposito A Galeone L Navas S Esposito S Gargiulo S Fattet V Donofrio G Cinalli A Brunetti LD Vecchio PA Northcott O Delattre MD Taylor A Iolascon M Zollo 2009 MicroRNA-199b-5p impairs cancer stem cells through negative regulation of HES1 in medulloblastoma PloS One 4 3 e4998 19308264 10.1371/journal.pone.0004998
41. N Yokota TG Mainprize MD Taylor T Kohata M Loreto S Ueda W Dura W Grajkowska JS Kuo JT Rutka 2004 Identification of differentially expressed and developmentally regulated genes in medulloblastoma using suppression subtraction hybridization Oncogene 23 19 3444 3453 15064731 10.1038/sj.onc.1207475 1:CAS:528:DC%2BD2cXjtlCgsrY%3D (Pubitemid 38669834)
42. M van Noort J Meeldijk R van der Zee O Destree H Clevers 2002 Wnt signaling controls the phosphorylation status of beta-catenin J Biol Chem 277 20 17901 17905 11834740 10.1074/jbc.M111635200 (Pubitemid 34967600)
43. F Massicot H Dutertre-Catella C Pham-Huy XH Liu HT Duc JM Warnet 2005 In vitro assessment of renal toxicity and inflammatory events of two protein phosphatase inhibitors cantharidin and nor-cantharidin Basic Clin Pharmacol Toxicol 96 1 26 32 15667592 10.1111/j.1742-7843.2005.pto960104.x 1:CAS:528:DC%2BD2MXhsFeksbs%3D (Pubitemid 40260843)
44. N Barker H Clevers 2006 Mining the Wnt pathway for cancer therapeutics Nat Rev Drug Discov 5 12 997 1014 17139285 10.1038/nrd2154 1:CAS:528: DC%2BD28Xht1Kju7vK (Pubitemid 44835127)
45. N Baryawno B Sveinbjornsson P Kogner JI Johnsen 2010 Medulloblastoma: a disease with disorganized developmental signaling cascades Cell Cycle 9 13 2548 2554 20581434 10.4161/cc.9.13.12170 1:CAS:528:DC%2BC3cXhsFCnt7vL
46. N Baryawno B Sveinbjornsson S Eksborg CS Chen P Kogner JI Johnsen 2010 Small-molecule inhibitors of phosphatidylinositol 3-kinase/Akt signaling inhibit Wnt/beta-catenin pathway cross-talk and suppress medulloblastoma growth Cancer Res 70 1 266 276 20028853 10.1158/0008-5472.CAN-09-0578 1:CAS:528:DC%2BC3cXkvF2r
47. RC Widau Y Jin SA Dixon BE Wadzinski PJ Gallagher 2010 Protein phosphatase 2A (PP2A) holoenzymes regulate death-associated protein kinase (DAPK) in ceramide-induced anoikis J Biol Chem 285 18 13827 13838 20220139 10.1074/jbc.M109.085076 1:CAS:528:DC%2BC3cXltFOgt70%3D
48. YJ Chen CJ Shieh TH Tsai CD Kuo LT Ho TY Liu HF Liao 2005 Inhibitory effect of norcantharidin, a derivative compound from blister beetles, on tumor invasion and metastasis in CT26 colorectal adenocarcinoma cells Anti-cancer drugs 16 3 293 299 15711181 10.1097/00001813-200503000-00008 1:CAS:528:DC%2BD2MXht1Omtr0%3D (Pubitemid 40283944)
49. YN Chen CC Cheng JC Chen W Tsauer SL Hsu 2003 Norcantharidin-induced apoptosis is via the extracellular signal-regulated kinase and c-Jun-NH2-terminal kinase signaling pathways in human hepatoma HepG2 cells Br J Pharmacol 140 3 461 470 12970086 10.1038/sj.bjp.0705461 1:CAS:528: DC%2BD3sXosFOgs7o%3D (Pubitemid 37330490)
50. H Yang W Guo B Xu M Li J Cui 2007 Anticancer activity and mechanisms of norcantharidin-Nd3II on hepatoma Anticancer Drugs 18 10 1133 1137 17893513 10.1097/CAD.0b013e3282eeb1c5 1:CAS:528:DC%2BD2sXhtVOgurrL (Pubitemid 47485648)
51. KA Chuang CH Lieu WJ Tsai MH Wu YC Chen JF Liao CC Wang YC Kuo 2010 Evaluation of anti-Wnt/beta-catenin signaling agents by pGL4-TOP transfected stable cells with a luciferase reporter system Braz J Med Biol Res 43 10 931 941 20835687 10.1590/S0100-879X2010007500091 1:CAS:528:DC%2BC3cXhsFyhtr%2FL
52. J Pizem A Cort L Zadravec-Zaletel M Popovic 2005 Survivin is a negative prognostic marker in medulloblastoma Neuropathol Appl Neurobiol 31 4 422 428 16008826 10.1111/j.1365-2990.2005.00664.x 1:CAS:528:DC%2BD2MXpslWisr0%3D (Pubitemid 41059863)
53. M Mimeault SK Batra 2010 Frequent deregulations in the hedgehog signaling network and cross-talks with the epidermal growth factor receptor pathway involved in cancer progression and targeted therapies Pharmacol Rev 62 3 497 524 20716670 10.1124/pr.109.002329 1:CAS:528:DC%2BC3cXhsVSltbbK
54. X Guo XF Wang 2009 Signaling cross-talk between TGF-beta/BMP and other pathways Cell Res 19 1 71 88 19002158 10.1038/cr.2008.302 1:CAS:528: DC%2BD1MXht1GgsQ%3D%3D
55. C Li Y Zhang Y Lu Z Cui M Yu S Zhang X Xue 2010 Evidence of the cross talk between Wnt and Notch signaling pathways in non-small-cell lung cancer (NSCLC): Notch3-siRNA weakens the effect of LiCl on the cell cycle of NSCLC cell lines J Cancer Res Clin Oncol 5 771 778
56. S Orsulic O Huber H Aberle S Arnold R Kemler 1999 E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1-mediated transactivation J Cell Sci 112 Pt 8 1237 1245 10085258 1:CAS:528: DyaK1MXjtFGhsLk%3D (Pubitemid 29218912)
57. L Zhang X Sun ZR Zhang 2005 An investigation on liver-targeting microemulsions of norcantharidin Drug Deliv 12 5 289 295 16188728 10.1080/10717540500176829 1:CAS:528:DC%2BD2MXhtV2gtLnP (Pubitemid 41356185)
58. J Malaterre RG Ramsay T Mantamadiotis 2007 Wnt-Frizzled signalling and the many paths to neural development and adult brain homeostasis Front Biosci 12 492 506 17127312 10.2741/2077 1:CAS:528:DC%2BD28Xht1WgsLrO (Pubitemid 46852801)
59. A Chenn CA Walsh 2002 Regulation of cerebral cortical size by control of cell cycle exit in neural precursors Science 297 5580 365 369 12130776 10.1126/science.1074192 1:CAS:528:DC%2BD38Xls1Cis74%3D (Pubitemid 34790759)