The DNA damage/repair cascade in glioblastoma cell lines after chemotherapeutic agent treatment

International Journal of Oncology

Volumn 46, Issue 6, 2015, Pages 2299-2308

  Annovazzi, Laura ^a   Caldera, Valentina ^a   Mellai, Marta ^a   Riganti, Chiara ^b   Battaglia, Luigi ^c   Chirio, Daniela ^c   Melcarne, Antonio ^d   Schiffer, Davide ^a  

^a Neuro Bio Oncology Center   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d CTO HOSPITAL   (Italy)

Author keywords

Chemoresistance; DNA damage repair; Glioblastoma; Glioma stem cells

Indexed keywords

ATM PROTEIN; CHECKPOINT KINASE 2; DOXORUBICIN; HISTONE H2AX; KU ANTIGEN; PACLITAXEL; RAD51 PROTEIN; TEMOZOLOMIDE; ANTINEOPLASTIC AGENT; DACARBAZINE; DNA;

APOPTOSIS; ARTICLE; CELL ADHESION; CELL DAMAGE; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; CLONOGENESIS; COMET ASSAY; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; DOSE RESPONSE; GENOTOXICITY; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; METAPHASE; OLIGODENDROGLIOMA; PHENOTYPE; PILOCYTIC ASTROCYTOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; BRAIN NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DACARBAZINE; DNA DAMAGE; DNA REPAIR; DNA, NEOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; GLIOBLASTOMA; HUMANS; PACLITAXEL;

EID: 84928551204     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2015.2963     Document Type: Article

References (40)

1. Caldera V, Mellai M, Annovazzi L, Monzeglio O, Piazzi A and Schiffer D: MGMT hypermethylation and MDR system in glioblastoma cancer stem cells. Cancer Genomics Proteomics 9: 171-178, 2012.
2. Salmaggi A, Boiardi A, Gelati M, Russo A, Calatozzolo C, Ciusani E, Sciacca FL, Ottolina A, Parati EA, La Porta C, Alessandri G, Marras C, Croci D and De Rossi M: Glioblastoma-derived tumorospheres identify a population of tumor stem-like cells with angiogenic potential and enhanced multidrug resistance phenotype. Glia 54: 850-860, 2006.
3. Johannessen TC and Bjerkvig R: Molecular mechanisms of temozolomide resistance in glioblastoma multiforme. Expert Rev Anticancer Ther 12: 635-642, 2012.
4. Alexander BM, Pinnell N, Wen PY and D'Andrea A: Targeting DNA repair and the cell cycle in glioblastoma. J Neurooncol 107: 463-477, 2012.
5. Schmalz PG, Shen MJ and Park JK: Treatment resistance mechanisms of malignant glioma tumor stem cells. Cancers (Basel) 3: 621-635, 2011.
6. Frosina G: The bright and the dark sides of DNA repair in stem cells. J Biomed Biotechnol 2010: 845396, 2010.
7. Frosina G: DNA repair and resistance of gliomas to chemotherapy and radiotherapy. Mol Cancer Res 7: 989-999, 2009.
8. Sarkaria JN, Kitange GJ, James CD, Plummer R, Calvert H, Weller M and Wick W: Mechanisms of chemoresistance to alkylating agents in malignant glioma. Clin Cancer Res 14: 2900-2908, 2008.
9. Kastan MB and Bartek J: Cell-cycle checkpoints and cancer. Nature 432: 316-323, 2004.
10. Bolderson E, Richard DJ, Zhou BB and Khanna KK: Recent advances in cancer therapy targeting proteins involved in DNA double-strand break repair. Clin Cancer Res 15: 6314-6320, 2009.
11. Pardo B, Gómez-González B and Aguilera A: DNA repair in mammalian cells: DNA double-strand break repair: how to fix a broken relationship. Cell Mol Life Sci 66: 1039-1056, 2009.
12. Johannessen TC, Bjerkvig R and Tysnes BB: DNA repair and cancer stem-like cells - potential partners in glioma drug resistance? Cancer Treat Rev 34: 558-567, 2008.
13. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD and Rich JN: Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760, 2006.
14. + cancer stem cells in glioblastoma. Mol Cancer 5: 67, 2006.
15. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, et al: MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352: 997-1003, 2005.
16. Hirose Y, Berger MS and Pieper RO: p53 effects both the duration of G2/M arrest and the fate of temozolomide-treated human glioblastoma cells. Cancer Res 61: 1957-1963, 2001.
17. Günther W, Pawlak E, Damasceno R, Arnold H and Terzis AJ: Temozolomide induces apoptosis and senescence in glioma cells cultured as multicellular spheroids. Br J Cancer 88: 463-469, 2003.
18. Roos WP, Batista LF, Naumann SC, Wick W, Weller M, Menck CF and Kaina B: Apoptosis in malignant glioma cells triggered by the temozolomide-induced DNA lesion O6-methylguanine. Oncogene 26: 186-197, 2007.
19. Kurz EU, Douglas P and Lees-Miller SP: Doxorubicin activates ATM-dependent phosphorylation of multiple downstream targets in part through the generation of reactive oxygen species. J Biol Chem 279: 53272-53281, 2004.
20. Branham MT, Nadin SB, Vargas-Roig LM and Ciocca DR: DNA damage induced by paclitaxel and DNA repair capability of peripheral blood lymphocytes as evaluated by the alkaline comet assay. Mutat Res 560: 11-17, 2004.
21. Stan AC, Casares S, Radu D, Walter GF and Brumeanu TD: Doxorubicin-induced cell death in highly invasive human gliomas. Anticancer Res 19 (2A): 941-950, 1999.
22. Lesniak MS, Upadhyay U, Goodwin R, Tyler B and Brem H: Local delivery of doxorubicin for the treatment of malignant brain tumors in rats. Anticancer Res 25 (6B): 3825-3831, 2005. Erratum in: Anticancer Res 26: 445, 2006.
23. Chang SM, Kuhn JG, Robins HI, Schold SC Jr, Spence AM, Berger MS, Mehta M, Pollack IF, Rankin C and Prados MD: A Phase II study of paclitaxel in patients with recurrent malignant glioma using different doses depending upon the concomitant use of anticonvulsants: A North American Brain Tumor Consortium report. Cancer 91: 417-422, 2001.
24. Caldera V, Mellai M, Annovazzi L, Piazzi A, Lanotte M, Cassoni P and Schiffer D: Antigenic and genotypic similarity between primary glioblastomas and their derived neurospheres. J Oncol 2011: 314962, 2011.
25. Mellai M, Monzeglio O, Piazzi A, Caldera V, Annovazzi L, Cassoni P, Valente G, Cordera S, Mocellini C and Schiffer D: MGMT promoter hypermethylation and its associations with genetic alterations in a series of 350 brain tumors. J Neurooncol 107: 617-631, 2012.
26. th edition. International Agency for Research on Cancer (IARC), Lyon, 2007.
27. Singh NP, McCoy MT, Tice RR and Schneider EL: A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175: 184-191, 1988.
28. Collins AR, Oscoz AA, Brunborg G, Gaivão I, Giovannelli L, Kruszewski M, Smith CC and Stetina R: The comet assay: Topical issues. Mutagenesis 23: 143-151, 2008.
29. Mellai M and Schiffer D: Apoptosis in brain tumors: Prognostic and therapeutic considerations. Anticancer Res 27 (1A): 437-448, 2007.
30. Beier D, Röhrl S, Pillai DR, Schwarz S, Kunz-Schughart LA, Leukel P, Proescholdt M, Brawanski A, Bogdahn U, Trampe-Kieslich A, et al: Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 68: 5706-5715, 2008.
31. Mihaliak AM, Gilbert CA, Li L, Daou MC, Moser RP, Reeves A, Cochran BH and Ross AH: Clinically relevant doses of chemotherapy agents reversibly block formation of glioblastoma neurospheres. Cancer Lett 296: 168-177, 2010.
32. Hermisson M, Klumpp A, Wick W, Wischhusen J, Nagel G, Roos W, Kaina B and Weller M: O6-methylguanine DNA methyltransferase and p53 status predict temozolomide sensitivity in human malignant glioma cells. J Neurochem 96: 766-776, 2006.
33. Bocangel DB, Finkelstein S, Schold SC, Bhakat KK, Mitra S and Kokkinakis DM: Multifaceted resistance of gliomas to temozolomide. Clin Cancer Res 8: 2725-2734, 2002.
34. Knizhnik AV, Roos WP, Nikolova T, Quiros S, Tomaszowski KH, Christmann M and Kaina B: Survival and death strategies in glioma cells: Autophagy, senescence and apoptosis triggered by a single type of temozolomide-induced DNA damage. PLoS One 8: e55665, 2013.
35. Beier D, Schriefer B, Brawanski K, Hau P, Weis J, Schulz JB and Beier CP: Efficacy of clinically relevant temozolomide dosing schemes in glioblastoma cancer stem cell lines. J Neurooncol 109: 45-52, 2012.
36. Kase M, Vardja M, Lipping A, Asser T and Jaal J: Impact of PARP-1 and DNA-PK expression on survival in patients with glioblastoma multiforme. Radiother Oncol 101: 127-131, 2011.
37. Bartek J, Bartkova J and Lukas J: DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene 26: 7773-7779, 2007.
38. Bartkova J, Hamerlik P, Stockhausen MT, Ehrmann J, Hlobilkova A, Laursen H, Kalita O, Kolar Z, Poulsen HS, Broholm H, et al: Replication stress and oxidative damage contribute to aberrant constitutive activation of DNA damage signalling in human gliomas. Oncogene 29: 5095-5102, 2010.
39. Battaglia L, Gallarate M, Peira E, Chirio D, Muntoni E, Biasibetti E, Capucchio MT, Valazza A, Panciani PP, Lanotte M, et al: Solid lipid nanoparticles for potential doxorubicin delivery in glioblastoma treatment: Preliminary in vitro studies. J Pharm Sci 103: 2157-2165, 2014.
40. Chirio D, Gallarate M, Peira E, Battaglia L, Muntoni E, Riganti C, Biasibetti E, Capucchio MT, Valazza A, Panciani P, et al: Positive-charged solid lipid nanoparticles as paclitaxel drug delivery system in glioblastoma treatment. Eur J Pharm Biopharm 88: 746-758, 2014.