Ependymoma stem cells are highly sensitive to temozolomide in vitro and in orthotopic models

Neuro-Oncology

Volumn 16, Issue 8, 2014, Pages 1067-1077

  Meco, Daniela ^a   Servidei, Tiziana ^a   Lamorte, Giuseppe ^b   Binda, Elena ^c   Arena, Vincenzo ^a   Riccardi, Riccardo ^a  

^a CATHOLIC UNIVERSITY   (Italy)

^b CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Differentiation; Ependymoma stem cells; MGMT; Orthotopic models; Temozolomide

Indexed keywords

6 O METHYLGUANINE; DNA METHYLTRANSFERASE; ETOPOSIDE; GALACTOSYLCERAMIDASE; GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEIN P21; PROTEIN P27; PROTEIN P53; TEMOZOLOMIDE; ALKYLATING AGENT; DACARBAZINE; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CELL PROLIFERATION ASSAY; DRUG EFFICACY; DRUG SENSITIVITY; EPENDYMOMA STEM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; ORTHOTOPIC TRANSPLANTATION; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; STEM CELL; ANALOGS AND DERIVATIVES; ANIMAL; DISEASE MODEL; DRUG RESISTANCE; DRUG SCREENING; EPENDYMOMA; GENETICS; GLIOBLASTOMA; METABOLISM; NUDE MOUSE; TUMOR CELL CULTURE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; DACARBAZINE; DISEASE MODELS, ANIMAL; DNA MODIFICATION METHYLASES; DRUG RESISTANCE, NEOPLASM; EPENDYMOMA; GLIOBLASTOMA; MICE, NUDE; O(6)-METHYLGUANINE-DNA METHYLTRANSFERASE; STEM CELLS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84904346409     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nou008     Document Type: Article

References (60)

1. Witt H, Korshunov A, Pfister SM, et al. Molecular approaches to ependymoma: The next step(s). Curr Opin Neurol. 2012;25:745-750
2. Grundy RG, Wilne SA, Weston CL, et al. Childrens Cancer and Leukaemia Group (formerly UKCCSG) Brain Tumour Committee. Primary postoperative chemotherapy without radiotherapy for intracranial ependymoma in children: The UKCCSG/SIOP prospective study. Lancet Oncol. 2007;8:696-705 (Pubitemid 47189085)
3. Koos B, Bender S, Witt H, et al. The transcription factor evi-1 is overexpressed, promotes proliferation, and is prognostically unfavorable in infratentorial ependymomas. Clin Cancer Res. 2011; 17:3631-3637
4. Bouffet E, Perilongo G, Canete A, et al. Intracranial ependymomas in children: A critical review of prognostic factors and a plea for cooperation. Med Pediatr Oncol. 1998;30:319-329
5. de Bont JM, Packer RJ, Michiels EM, et al. Biological background of pediatric medulloblastoma and ependymoma: A review from a translational research perspective. Neuro Oncol. 2008;10: 1040-1060
6. Kilday JP, Rahman R, Dyer S, et al. Pediatric ependymoma: Biological perspectives. Mol Cancer Res. 2009;7:765-786
7. Shonka NA. Targets for therapy in ependymoma. Target Oncol. 2011; 6:163-169
8. Atkinson JM, Shelat AA, Carcaboso AM, et al. An integrated in vitro and in vivo high-Throughput screen identifies treatment leads for ependymoma. Cancer Cell. 2011;20:384-399
9. Massimino M, Gandola L, Barra S, et al. Infant ependymoma in a 10-year AIEOP (Associazione Italiana Ematologia Oncologia Pediatrica) experience with omitted or deferred radiotherapy. Int J Radiat Oncol Biol Phys. 2011;80:807-814
10. Witt H, Mack SC, Ryzhova M, et al. Delineation of two clinically and molecularly distinct subgroups of posterior fossa ependymoma. Cancer Cell. 2011;20:143-157
11. Zacharoulis S, Ashley S, Moreno L, et al. Treatment and outcome of children with relapsed ependymoma: A multi-institutional retrospective analysis. Childs Nerv Syst. 2010;26:905-911
12. Hadjipanayis CG, Van Meir EG. Brain cancer propagating cells: Biology, genetics and targeted therapies. Trends Mol Med. 2009;15: 519-530
13. Magee JA, Piskounova E, Morrison SJ. Cancer stem cells: Impact, heterogeneity, and uncertainty. Cancer Cell. 2012;21:283-296
14. Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821-5828 (Pubitemid 37187480)
15. Taylor MD, Poppleton H, Fuller C, et al. Radial glia cells are candidate stem cells of ependymoma. Cancer Cell. 2005;8:323-335 (Pubitemid 41443417)
16. Akyüz C, Demir HA, Varan A, et al. Temozolomide in relapsed pediatric brain tumors: 14 cases from a single center. Childs Nerv Syst. 2012;28:111-116
17. Teo C, Nakaji P, Symons P, et al. Ependymoma. Childs Nerv Syst. 2003; 19:270-285 (Pubitemid 36869196)
18. Guan S, Shen R, Lafortune T, et al. Establishment and characterization of clinically relevant models of ependymoma: A true challenge for targeted therapy. Neuro Oncol. 2011;13:748-758
19. Hussein D, Punjaruk W, Storer LC, et al. Pediatric brain tumor cancer stem cells: Cell cycle dynamics, DNA repair, and etoposide extrusion. Neuro Oncol. 2011;13:70-83
20. Milde T, Kleber S, Korshunov A, et al. A novel human high-risk ependymoma stem cell model reveals the differentiation-inducing potential of the histone deacetylase inhibitor Vorinostat. Acta Neuropathol. 2011;122:637-650
21. Servidei T, Meco D, Trivieri N, et al. Effects of epidermal growth factor receptor blockade on ependymoma stem cells in vitro and in orthotopic mouse models. Int J Cancer. 2012;131:E791-E803
22. Nemati F, Livartowski A, De Cremoux P, et al. Distinctive potentiating effects of cisplatin and/or ifosfamide combined with etoposide in human small cell lung carcinoma xenografts. Clin Cancer Res. 2000;6:2075-2086 (Pubitemid 30305108)
23. de Vries NA, Bruggeman SW, Hulsman D, et al. Rapid and robust transgenic high-grade glioma mouse models for therapy intervention studies. Clin Cancer Res. 2010;16:3431-3441
24. Banissi C, Ghiringhelli F, Chen L, et al. Treg depletion with a low-dose metronomic temozolomide regimen in a rat glioma model. Cancer Immunol Immunother. 2009;58:1627-1634
25. Clarke JL, Iwamoto FM, Sul J, et al. Randomized phase II trial of chemoradiotherapy followed by either dose-dense or metronomic temozolomide for newly diagnosed glioblastoma. J Clin Oncol. 2009;27:3861-3867
26. Beier D, Röhrl S, Pillai DR, et al. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res. 2010;68:5706-5715
27. Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352: 997-1003 (Pubitemid 40349502)
28. Palmisano WA, Divine KK, Saccomanno G, et al. Predicting lung cancer by detecting aberrant promoter methylation in sputum. Cancer Res. 2000;60:5954-5958
29. Gaspar N, Marshall L, Perryman L, et al. MGMT-independent temozolomide resistance in pediatric glioblastoma cells associated with a PI3-kinase-mediated HOX/stem cell gene signature. Cancer Res. 2010;70:9243-9252
30. Lapenna S, Giordano A. Cell cycle kinases as therapeutic targets for cancer. Nat Rev Drug Discov. 2009;8:547-566
31. Mhaidat NM, Zhang XD, Allen J, et al. Temozolomide induces senescence but not apoptosis in human melanoma cells. Br J Cancer. 2007;97:1225-1233 (Pubitemid 350035808)
32. Sato Y, Kurose A, Ogawa A, et al. Diversity of DNA damage response of astrocytes and glioblastoma cell lines with various p53 status to treatment with etoposide and temozolomide. Cancer Biol Ther. 2009;8:452-457
33. Avery-Kiejda KA, Zhang XD, Adams LJ, et al. Small molecular weight variants of p53 are expressed in human melanoma cells and are induced by the DNA-damaging agent cisplatin. Clin Cancer Res. 2012;14:1659-1668 (Pubitemid 351469449)
34. Khoury MP, Bourdon JC. The isoforms of the p53 protein. Cold Spring Harb Perspect Biol. 2010;2:a000927
35. Weller M, Stupp R, Reifenberger G, et al. MGMTpromoter methylation in malignant gliomas: Ready for personalized medicine?. Nat Rev Neurol. 2010;6:39-51
36. Christmann M, Verbeek B, Roos WP, et al. O(6)-Methylguanine-DNA methyltransferase (MGMT) in normal tissues and tumors: Enzyme activity, promoter methylation and immunohistochemistry. Biochim Biophys Acta. 2012;1816:179-190
37. Sciuscio D, Diserens AC, van Dommelen K, et al. Extent and patterns of MGMT promoter methylation in glioblastoma- and respective glioblastoma-derived spheres. Clin Cancer Res. 2011;17:255-266
38. Zucchetti M, Catapano CV, Filippeschi S, et al. Temozolomide induced differentiation of K562 leukemia cells is not mediated by gene hypomethylation. Biochem Pharmacol. 1989;38:2069-2075 (Pubitemid 19171206)
39. Persano L, Pistollato F, Rampazzo E, et al. BMP2 sensitizes glioblastoma stem-like cells to Temozolomide by affecting HIF-1a stability and MGMT expression. Cell Death Dis. 2012;3:e412
40. Bocangel DB, Finkelstein S, Schold SC, et al. Multifaceted resistance of gliomas to temozolomide. Clin Cancer Res. 2002;8:2725-2734 (Pubitemid 34856362)
41. Caporali S, Falcinelli S, Starace G, et al. DNA damage induced by temozolomide signals to both ATM and ATR: Role of the mismatch repair system. Mol Pharmacol. 2004;66:478-491 (Pubitemid 39329246)
42. Roos WP, Batista LF, Naumann SC, et al. Apoptosis in malignant glioma cells triggered by the temozolomide-induced DNA lesion O6-methylguanine. Oncogene. 2007;26:186-197 (Pubitemid 46095730)
43. Ubezio P, Lupi M, Branduardi D, et al. Quantitative assessment of the complex dynamics of G1, S, and G2-M checkpoint activities. Cancer Res. 2009;69:5234-5240
44. Coqueret O. New roles for p21 and p27 cell-cycle inhibitors: A function for each cell compartment?. Trends Cell Biol. 2003;13:65-70 (Pubitemid 36135887)
45. Silden E, Hjelle SM, Wergeland L, et al. Expression of TP53 isoforms p53b or p53g enhances chemosensitivity in TP53(null) cell lines. PLoS One. 2013;8:e56276
46. Bleau AM, Hambardzumyan D, Ozawa T, et al. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell. 2009;4:226-235
47. Pistollato F, Abbadi S, Rampazzo E, et al. Intratumoral hypoxic gradient drives stem cells distribution and MGMT expression in glioblastoma. Stem Cells. 2010;28:851-862
48. Sato A, Sunayama J, Matsuda K, et al. MEK-ERK signaling dictates DNA-repair gene MGMT expression and temozolomide resistance of stem-like glioblastoma cells via the MDM2-p53 axis. Stem Cells. 2011;29:1942-1951
49. Blough MD, Westgate MR, Beauchamp D, et al. Sensitivity to temozolomide in brain tumor initiating cells. Neuro Oncol. 2010; 12:756-760
50. Koos B, Peetz-Dienhart S, Riesmeier B, et al. O6-methylguanine-DNA methyltransferase (MGMT) promoter methylation is significantly less frequent in ependymal tumours as compared to malignant astrocytic gliomas. Neuropathol Appl Neurobiol. 2010;36:356-358
51. Mack SC, Witt H, Wang X, et al. Emerging insights into the ependymoma epigenome. Brain Pathol. 2013;23:206-209
52. Rogers HA, Kilday JP, Mayne C, et al. Supratentorial and spinal pediatric ependymomas display a hypermethylated phenotype which includes the loss of tumor suppressor genes involved in the control of cell growth and death. Acta Neuropathol. 2012;123: 711-725
53. Muñoz P, Iliou MS, Esteller M. Epigenetic alterations involved in cancer stem cell reprogramming. Mol Oncol. 2012;6:620-636
54. Martinez R, Esteller M. The DNA methylome of glioblastoma multiforme. Neurobiol Dis. 2010;39:40-46
55. Tolcher AW, Gerson SL, Denis L, et al. Marked inactivation of O6-Alkylguanine-DNA alkyltransferase activity with protracted temozolomide schedules. Br J Cancer. 2003;88:1004-1011 (Pubitemid 36560766)
56. Kong DS, Lee JI, Kim JH, et al. Phase II trial of low-dose continuous (metronomic) treatment of temozolomide for recurrent glioblastoma. Neuro Oncol. 2010;12:289-296
57. Neyns B, Tosoni A, Hwu WJ, et al. Dose-dense temozolomide regimens: Antitumor activity, toxicity, and immunomodulatory effects. Cancer. 2010;116:2868-2877
58. Chen C, Xu T, Lu Y, et al. The efficacy of temozolomide for recurrent glioblastoma multiforme. Eur J Neurol. 2013;20:223-230
59. Gasparini G. Metronomic scheduling: The future of chemotherapy?. Lancet Oncol. 2001;2:733-740 (Pubitemid 33134058)
60. Campos B, Wan F, Farhadi M, et al. Differentiation therapy exerts antitumor effects on stem-like glioma cells. Clin Cancer Res. 2010; 16:2715-2728