The histone demethylase KDM5A is a key factor for the resistance to temozolomide in glioblastoma

Cell Cycle

Volumn 14, Issue 21, 2015, Pages 3418-3429

  Banelli, Barbara ^a   Carra, Elisa ^a   Barbieri, Federica ^b   Würth, Roberto ^b   Parodi, Federica ^a   Pattarozzi, Alessandra ^b   Carosio, Roberta ^a   Forlani, Alessandra ^a   Allemanni, Giorgio ^a   Marubbi, Daniela ^a,c   Florio, Tullio ^b   Daga, Antonio ^a   Romani, Massimo ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

Author keywords

Cancer stem cells; DNA methylation; Epigenetic; Glioblastoma; Histone demethylase; KDM5A; Temozolomide

Indexed keywords

BETA TUBULIN; DOXORUBICIN; GLIAL FIBRILLARY ACIDIC PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; RETINOBLASTOMA BINDING PROTEIN 2; TEMOZOLOMIDE; TRANSCRIPTION FACTOR SOX2; VORINOSTAT; ALKYLATING AGENT; ANTINEOPLASTIC AGENT; DACARBAZINE; HISTONE DEACETYLASE INHIBITOR; KDM5A PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER RESISTANCE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL SURVIVAL; CELL VIABILITY; CELLULAR DISTRIBUTION; COMPUTER MODEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA METHYLATION; DRUG DISTRIBUTION; EPIGENETICS; G2 PHASE CELL CYCLE CHECKPOINT; GENE OVEREXPRESSION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IC50; IMMUNOFLUORESCENCE; IN VITRO STUDY; REAL TIME POLYMERASE CHAIN REACTION; TRANSIENT EXPRESSION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BRAIN NEOPLASMS; CELL CYCLE; CELL SHAPE; DOSE RESPONSE; DRUG EFFECTS; DRUG POTENTIATION; DRUG RESISTANCE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC TRANSFECTION; GENETICS; GENOTYPE; METABOLISM; PATHOLOGY; PHENOTYPE; RNA INTERFERENCE; TIME FACTOR; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, ALKYLATING; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BRAIN NEOPLASMS; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL SHAPE; DACARBAZINE; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOTYPE; GLIOBLASTOMA; HISTONE DEACETYLASE INHIBITORS; HUMANS; NEOPLASTIC STEM CELLS; PHENOTYPE; RETINOBLASTOMA-BINDING PROTEIN 2; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION;

EID: 84958981949     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.1080/15384101.2015.1090063     Document Type: Article

References (55)

1. Dunn GP, Rinne ML, Wykosky J, Genovese G, Quayle SN, Dunn IF, Agarwalla PK, Chheda MG, Campos B, Wang A, et al. Emerging insights into the molecular and cellular basis of glioblastoma. Genes Dev 2012; 26:756-84. PMID:22508724; http://dx.doi.org/10.1101/gad.187922.112
2. Dirks PB. Brain tumor stem cells: the cancer stem cell hypothesis writ large. Mol Oncol 2010; 4:420-30. PMID:20801091; http://dx.doi.org/10.1016/j.molonc.2010.08.001
3. Yamada R, Nakano I. Glioma stem cells: their role in chemoresistance. World Neurosurg 2012; 77:237-40. PMID:22501017; http://dx.doi.org/10.1016/j.wneu. 2012.01.004
4. Florio T, Barbieri F. The status of the art of human malignant glioma management: the promising role of targeting tumor-initiating cells. Drug Discov Today 2012; 17:1103-10. PMID:22704957; http://dx.doi.org/10.1016/j.drudis.2012.06.001
5. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352:987-96. PMID:15758009; http://dx.doi.org/10.1056/NEJMoa043330
6. 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 2005; 352:997-1003. PMID:15758010; http://dx.doi.org/10.1056/NEJMoa043331
7. Ivanov M, Kacevska M, Ingelman-Sundberg M. Epigenomics and interindividual differences in drug response. Clin Pharmacol Ther 2012; 92:727-36. PMID:23093317; http://dx.doi.org/10.1038/clpt. 2012.152
8. Cahill DP, Codd PJ, Batchelor TT, Curry WT, Louis DN. MSH6 inactivation and emergent temozolomide resistance in human glioblastomas. Clin Neurosurg 2008; 55:165-71. PMID:19248684
9. Shinsato Y, Furukawa T, Yunoue S, Yonezawa H, Minami K, Nishizawa Y, Ikeda R, Kawahara K, Yamamoto M, Hirano H, et al. Reduction of MLH1 and PMS2 confers temozolomide resistance and is associated with recurrence of glioblastoma. Oncotarget 2013; 4:2261-70. PMID:24259277; http://dx.doi.org/10.18632/oncotarget.1302
10. Yip S, Miao J, Cahill DP, Iafrate AJ, Aldape K, Nutt CL, Louis DN. MSH6 mutations arise in glioblastomas during temozolomide therapy and mediate temozolomide resistance. Clin Cancer Res 2009; 15:4622-9. PMID:19584161; http://dx.doi.org/10.1158/1078-0432.CCR-08-3012
11. Munoz JL, Rodriguez-Cruz V, Ramkissoon SH, Ligon KL, Greco SJ, Rameshwar P. Temozolomide resistance in glioblastoma occurs by miRNA-9-targeted PTCH1, independent of sonic hedgehog level. Oncotarget 2015; 6:1190-201. PMID:25595896; http://dx.doi.org/10.18632/oncotarget.2778
12. Wang Z, Yang J, Xu G, Wang W, Liu C, Yang H, Yu Z, Lei Q, Xiao L, Xiong J, et al. Targeting miR-381-NEFL axis sensitizes glioblastoma cells to temozolomide by regulating stemness factors and multidrug resistance factors. Oncotarget 2015; 6:3147-64. PMID:25605243; http://dx.doi.org/10.18632/oncotarget.3061
13. Hiddingh L, Tannous BA, Teng J, Tops B, Jeuken J, Hulleman E, Boots-Sprenger SH, Vandertop WP, Noske DP, Kaspers GJ, et al. EFEMP1 induces gamma-secretase/Notch-mediated temozolomide resistance in glioblastoma. Oncotarget 2014; 5:363-74. PMID:24495907; http://dx.doi.org/10.18632/oncotarget.1620
14. Fletcher JI, Haber M, Henderson MJ, Norris MD. ABC transporters in cancer: more than just drug efflux pumps. Nat Rev Cancer 2010; 10:147-56. PMID:20075923; http://dx.doi.org/10.1038/nrc2789
15. Cloos PA, Christensen J, Agger K, Helin K. Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev 2008; 22:1115-40. PMID:18451103; http://dx.doi.org/10.1101/gad.1652908
16. Agger K, Christensen J, Cloos PA, Helin K. The emerging functions of histone demethylases. Curr Opin Genet Dev 2008; 18:159-68. PMID:18281209; http://dx.doi.org/10.1016/j.gde.2007.12.003
17. Bezecny P. Histone deacetylase inhibitors in glioblastoma: pre-clinical and clinical experience. Med Oncol 2014; 31:985. PMID:24838514; http://dx.doi.org/10.1007/s12032-014-0985-5
18. Helin K, Dhanak D. Chromatin proteins and modifications as drug targets. Nature 2013; 502:480-8. PMID:24153301; http://dx.doi.org/10.1038/nature12751
19. Huang Y, Vasilatos SN, Boric L, Shaw PG, Davidson NE. Inhibitors of histone demethylation and histone deacetylation cooperate in regulating gene expression and inhibiting growth in human breast cancer cells. Breast Cancer Res Treat 2012; 131:777-89. PMID:21452019; http://dx.doi.org/10.1007/s10549-011-1480-8
20. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizian N, Zou L, Fischbach MA, et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010; 141:69-80. PMID:20371346; http://dx.doi.org/10.1016/j.cell.2010.02.027
21. Sareddy GR, Nair BC, Krishnan SK, Gonugunta VK, Zhang QG, Suzuki T, Miyata N, Brenner AJ, Brann DW, Vadlamudi RK. KDM1 is a novel therapeutic target for the treatment of gliomas. Oncotarget 2013; 4:18-28. PMID:23248157; http://dx.doi.org/10.18632/oncotarget.725
22. Roesch A, Vultur A, Bogeski I, Wang H, Zimmermann KM, Speicher D, Korbel C, Laschke MW, Gimotty PA, Philipp SE, et al. Overcoming intrinsic multidrug resistance in melanoma by blocking the mitochondrial respiratory chain of slow-cycling JARID1B(high) cells. Cancer Cell 2013; 23:811-25. PMID:23764003; http://dx.doi.org/10.1016/j.ccr.2013.05.003
23. Hou J, Wu J, Dombkowski A, Zhang K, Holowatyj A, Boerner JL, Yang ZQ. Genomic amplification and a role in drug-resistance for the KDM5A histone demethylase in breast cancer. Am J Transl Res 2012; 4:247-56. PMID:22937203
24. Yan H, Chen X, Zhang Q, Qin J, Li H, Liu C, Calhoun-Davis T, Coletta LD, Klostergaard J, Fokt I, et al. Drug-tolerant cancer cells show reduced tumorinitiating capacity: depletion of CD44 cells and evidence for epigenetic mechanisms. PLoS One 2011; 6: e24397. PMID:21935404; http://dx.doi.org/10.1371/journal.pone.0024397
25. Goldman M, Craft B, Swatloski T, Ellrott K, Cline M, Diekhans M, Ma S, Wilks C, Stuart J, Haussler D, et al. The UCSC cancer genomics browser: update 2013. Nucleic Acids Res 2013; 41:D949-54. PMID:23109555; http://dx.doi.org/10.1093/nar/gks1008
26. Klose RJ, Yan Q, Tothova Z, Yamane K, Erdjument-Bromage H, Tempst P, Gilliland DG, Zhang Y, Kaelin WG, Jr.. The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 2007; 128:889-900. PMID:17320163; http://dx.doi.org/10.1016/j.cell.2007.02.013
27. Rotili D, Mai A. Targeting Histone Demethylases: a new avenue for the fight against cancer. Genes Cancer 2011; 2:663-79. PMID:21941621; http://dx.doi.org/10.1177/1947601911417976
28. Alvarez AA, Field M, Bushnev S, Longo MS, Sugaya K. The effects of histone deacetylase inhibitors on Glioblastoma-Derived stem cells. J Mol Neurosci 2014; 55 (1):7-20
29. Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res 2010; 70:440-6. PMID:20068163; http://dx.doi.org/10.1158/0008-5472.CAN-09-1947
30. Mann BS, Johnson JR, Cohen MH, Justice R, Pazdur R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 2007; 12:1247-52. PMID:17962618; http://dx.doi.org/10.1634/theoncologist.12-10-1247
31. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, Hamou MF, de Tribolet N, Regli L, Wick W, Kouwenhoven MC, et al. Stem cell-related “self-renewal” signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol 2008; 26:3015-24. PMID:18565887; http://dx.doi.org/10.1200/JCO.2007.15.7164
32. Gangemi RM, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P, Ravetti GL, Zona GL, Daga A, Corte G. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 2009; 27:40-8. PMID:18948646; http://dx.doi.org/10.1634/stemcells.2008-0493
33. Griffero F, Daga A, Marubbi D, Capra MC, Melotti A, Pattarozzi A, Gatti M, Bajetto A, Porcile C, Barbieri F, et al. Different response of human glioma tumor-initiating cells to epidermal growth factor receptor kinase inhibitors. J Biol Chem 2009; 284:7138-48. PMID:19147502; http://dx.doi.org/10.1074/jbc. M807111200
34. Castriconi R, Daga A, Dondero A, Zona G, Poliani PL, Melotti A, Griffero F, Marubbi D, Spaziante R, Bellora F, et al. NK cells recognize and kill human glioblastoma cells with stem cell-like properties. J Immunol 2009; 182:3530-9; http://dx.doi.org/10.4049/jimmunol.0802845
35. Gritti M, Wurth R, Angelini M, Barbieri F, Peretti M, Pizzi E, Pattarozzi A, Carra E, Sirito R, Daga A, et al. Metformin repositioning as antitumoral agent: selective antiproliferative effects in human glioblastoma stem cells, via inhibition of CLIC1-mediated ion current. Oncotarget 2014; 5:11252-68. PMID:25361004; http://dx.doi.org/10.18632/oncotarget.2617
36. Costa BM, Smith JS, Chen Y, Chen J, Phillips HS, Aldape KD, Zardo G, Nigro J, James CD, Fridlyand J, et al. Reversing HOXA9 oncogene activation by PI3K inhibition: epigenetic mechanism and prognostic significance in human glioblastoma. Cancer Res 2010; 70:453-62. PMID:20068170; http://dx.doi.org/10.1158/0008-5472.CAN-09-2189
37. Di Vinci A, Casciano I, Marasco E, Banelli B, Ravetti GL, Borzi L, Brigati C, Forlani A, Dorcaratto A, Allemanni G, et al. Quantitative methylation analysis of HOXA3, 7, 9, and 10 genes in glioma: association with tumor WHO grade and clinical outcome. J Cancer Res Clin Oncol 2012; 138:35-47. PMID:21947269; http://dx.doi.org/10.1007/s00432-011-1070-5
38. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010; 17:510-22. PMID:20399149; http://dx.doi.org/10.1016/j.ccr.2010.03.017
39. Johannessen TC, Bjerkvig R. Molecular mechanisms of temozolomide resistance in glioblastoma multiforme. Expert Rev Anticancer Ther 2012; 12:635-42. PMID:22594898; http://dx.doi.org/10.1586/era.12.37
40. Friedman HS, Kerby T, Calvert H. Temozolomide and treatment of malignant glioma. Clin Cancer Res 2000; 6:2585-97. PMID:10914698
41. Kitange GJ, Mladek AC, Carlson BL, Schroeder MA, Pokorny JL, Cen L, Decker PA, Wu W, Lomberk GA, Gupta SK, et al. Inhibition of histone deacetylation potentiates the evolution of acquired temozolomide resistance linked to MGMT upregulation in glioblastoma xenografts. Clin Cancer Res 2012; 18:4070-9. PMID:22675172; http://dx.doi.org/10.1158/1078-0432.CCR-12-0560
42. Brandes AA, Franceschi E, Tosoni A, Bartolini S, Bacci A, Agati R, Ghimenton C, Turazzi S, Talacchi A, Skrap M, et al. O(6)-methylguanine DNA-methyltransferase methylation status can change between first surgery for newly diagnosed glioblastoma and second surgery for recurrence: clinical implications. Neuro Oncol 2010; 12:283-8. PMID:20167816; http://dx.doi.org/10.1093/neuonc/nop050
43. Oberstadt MC, Bien-Moller S, Weitmann K, Herzog S, Hentschel K, Rimmbach C, Vogelgesang S, Balz E, Fink M, Michael H, et al. Epigenetic modulation of the drug resistance genes MGMT, ABCB1 and ABCG2 in glioblastoma multiforme. BMC Cancer 2013; 13:617. PMID:24380367; http://dx.doi.org/10.1186/1471-2407-13-617
44. Park CK, Kim JE, Kim JY, Song SW, Kim JW, Choi SH, Kim TM, Lee SH, Kim IH, Park SH. The changes in MGMT promoter methylation status in initial and recurrent Glioblastomas. Transl Oncol 2012; 5:393-7. PMID:23066447; http://dx.doi.org/10.1593/tlo.12253
45. Pojo M, Goncalves CS, Xavier-Magalhaes A, Oliveira AI, Goncalves T, Correia S, Rodrigues AJ, Costa S, Pinto L, Pinto AA, et al. A transcriptomic signature mediated by HOXA9 promotes human glioblastoma initiation, aggressiveness and resistance to temozolomide. Oncotarget 2015; 6:7657-74. PMID:25762636; http://dx.doi.org/10.18632/oncotarget.3150
46. Beier D, Rohrl 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 2008; 68:5706-15. PMID:18632623; http://dx.doi.org/10.1158/0008-5472.CAN-07-6878
47. Carra E, Barbieri F, Marubbi D, Pattarozzi A, Favoni RE, Florio T, Daga A. Sorafenib selectively depletes human glioblastoma tumor-initiating cells from primary cultures. Cell Cycle 2013; 12:491-500. PMID:23324350; http://dx.doi.org/10.4161/cc.23372
48. Wurth R, Pattarozzi A, Gatti M, Bajetto A, Corsaro A, Parodi A, Sirito R, Massollo M, Marini C, Zona G, et al. Metformin selectively affects human glioblastoma tumor-initiating cell viability: A role for metformininduced inhibition of Akt. Cell Cycle 2013; 12:145-56. PMID:23255107; http://dx.doi.org/10.4161/cc.23050
49. Gatti M, Pattarozzi A, Bajetto A, Wurth R, Daga A, Fiaschi P, Zona G, Florio T, Barbieri F. Inhibition of CXCL12/CXCR4 autocrine/paracrine loop reduces viability of human glioblastoma stem-like cells affecting self-renewal activity. Toxicology 2013; 314:209-20; http://dx.doi.org/10.1016/j.tox.2013.10.003
50. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. Clonogenic assay of cells in vitro. Nature Protoc 2006; 1:2315-9. PMID:17406473; http://dx.doi.org/10.1038/nprot.2006.339
51. Riganti C, Salaroglio IC, Caldera V, Campia I, Kopecka J, Mellai M, Annovazzi L, Bosia A, Ghigo D, Schiffer D. Temozolomide downregulates P-glycoprotein expression in glioblastoma stem cells by interfering with the Wnt3a/glycogen synthase-3 kinase/b-catenin pathway. Neuro Oncol 2013; 15:1502-17. PMID:23897632; http://dx.doi.org/10.1093/neuonc/not104
52. Nakagawachi T, Soejima H, Urano T, Zhao W, Higashimoto K, Satoh Y, Matsukura S, Kudo S, Kitajima Y, Harada H, et al. Silencing effect of CpG island hypermethylation and histone modifications on O6-methylguanine-DNA methyltransferase (MGMT) gene expression in human cancer. Oncogene 2003; 22:8835-44. PMID:14647440
53. Banelli B, Bonassi S, Casciano I, Mazzocco K, Di Vinci A, Scaruffi P, Brigati C, Allemanni G, Borzi L, Tonini GP, et al. Outcome prediction and risk assessment by quantitative pyrosequencing methylation analysis of the SFN gene in advanced stage, high-risk, neuroblastic tumor patients. Int J Cancer 2010; 126:656-68. PMID:19626586; http://dx.doi.org/10.1002/ijc.24768
54. Banelli B, Brigati C, Di Vinci A, Casciano I, Forlani A, Borzi L, Allemanni G, Romani M. A pyrosequencing assay for the quantitative methylation analysis of the PCDHB gene cluster, the major factor in neuroblastoma methylator phenotype. Lab Invest 2011; 92:458-65. PMID:22157715; http://dx.doi.org/10.1038/labinvest.2011.169
55. Banelli B, Merlo DF, Allemanni G, Forlani A, Romani M. Clinical potentials of methylator phenotype in stage 4 high-risk neuroblastoma: an open challenge. PLoS One 2013; 8:e63253. PMID:23717404; http://dx.doi.org/10.1371/journal.pone.0063253