Sorafenib selectively depletes human glioblastoma tumor-initiating cells from primary cultures

Cell Cycle

Volumn 12, Issue 3, 2013, Pages 491-500

  Carra, Elisa ^a,b   Barbieri, Federica ^c   Marubbi, Daniela ^a,b   Pattarozzi, Alessandra ^c   Favoni, Roberto E ^a   Florio, Tullio ^c   Daga, Antonio ^b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c Center of Excellence for Biomedical Research (CEBR)   (Italy)

Author keywords

Glioblastoma; Mcl 1; Sorafenib; Stemness; Therapy; Tumor initiating cells

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NESTIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN MCL 1; SORAFENIB; TRANSCRIPTION FACTOR SOX2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER STEM CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL SUBPOPULATION; CLONOGENESIS; CONTROLLED STUDY; DOWN REGULATION; DRUG SELECTIVITY; ENRICHMENT CULTURE; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR RECURRENCE;

EID: 84875522870     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.23372     Document Type: Article

References (54)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007; 114: 97-109; PMID:17618441; http://dx.doi.org/10.1007/s00401- 007-0243-4
2. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007; 21: 2683-710; PMID:17974913; http://dx.doi.org/10.1101/gad.1596707
3. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CHM, Jones DL, et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66: 9339-44; PMID:16990346; http://dx.doi.org/10.1158/0008-5472.CAN-06-3126
4. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-11; PMID:11689955; http://dx.doi.org/ 10.1038/35102167
5. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-8; PMID:14522905
6. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401; PMID:15549107; http://dx.doi.org/10.1038/nature03128
7. Nicholas MK, Lukas RV, Chmura S, Yamini B, Lesniak M, Pytel P. Molecular heterogeneity in glioblastoma: therapeutic opportunities and challenges. Semin Oncol 2011; 38: 243-53; PMID:21421114; http://dx.doi.org/10.1053/j.seminoncol. 2011.01.009
8. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJB, Janzer RC, et al.; European Organisation for Research and Treatment of Cancer Brain Tumour and Radiation Oncology Groups; National Cancer Institute of Canada Clinical Trials Group. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009; 10: 459-66; PMID:19269895; http://dx.doi.org/10.1016/S1470-2045(09)70025-7
9. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-60; PMID:17051156; http://dx.doi.org/10.1038/ nature05236
10. Ghiaur G, Gerber J, Jones Rj.Concise review: Cancer stem cells and minimal residual disease. Stem Cells 2012; 30: 89-93; PMID:22045578; http://dx.doi.org/10.1002/stem.769
11. 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
12. Hothi P, Martins TJ, Chen L, Deleyrolle L, Yoon JG, Reynolds B, et al. High-throughput chemical screens identify disulfiram as an inhibitor of human glioblastoma stem cells. Oncotarget 2012; 3: 1124-36; PMID:23165409
13. Triscott J, Lee C, Hu K, Fotovati A, Berns R, Pambid M, et al. Disulfiram, a drug widely used to control alcoholism, suppresses the self-renewal of glioblastoma and over-rides resistance to temozolomide. Oncotarget 2012; 3: 1124-36; PMID:23165409
14. Wurth R, Pattarozzi A, Gatti M, Bajetto A, Corsaro A, Parodi A, et al. Metformin selectively affects human glioblastoma blastoma tumor-initiating cell viability: A role for metformin-induced inhibition of Akt. Cell Cycle 2013; 12: 145-56; http://dx.doi.org/10.4161/cc.23050
15. Nogueira L, Ruiz-Ontañon P, Vazquez-Barquero A, Moris F, Fernandez-Luna JL. The NFκB pathway: a therapeutic target in glioblastoma. Oncotarget 2011; 2: 646-53; PMID:21896960
16. Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455: 1061-8; PMID:18772890; http://dx.doi.org/10.1038/nature07385
17. Favoni RE, Daga A, Malatesta P, Florio T. Preclinical studies identify novel targeted pharmacological strategies for treatment of human malignant pleural mesothelioma. Br J Pharmacol 2012; 166: 532-53; PMID:22289125; http://dx.doi.org/10.1111/j.1476-5381.2012.01873.x
18. Puputti M, Tynninen O, Sihto H, Blom T, Mäenpää H, Isola J, et al. Amplification of KIT, PDGFRA, VEGFR2, and EGFR in gliomas. Mol Cancer Res 2006; 4: 927-34; PMID:17189383; http://dx.doi.org/10.1158/1541-7786.MCR-06- 0085
19. Chappell WH, Steelman LS, Long JM, Kempf RC, Abrams SL, Franklin RA, et al. Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR inhibitors: rationale and importance to inhibiting these pathways in human health. Oncotarget 2011; 2: 135-64; PMID:21411864
20. McCubrey JA, Steelman LS, Abrams SL, Lee JT, Chang F, Bertrand FE, et al. Roles of the RAF/MEK/ERK and PI3K/PTEN/AKT pathways in malignant transformation and drug resistance. Adv Enzyme Regul 2006; 46: 249-79; PMID:16854453; http://dx.doi.org/10.1016/j.advenzreg.2006.01.004
21. Griffero F, Daga A, Marubbi D, Capra MC, Melotti A, Pattarozzi A, 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
22. Snuderl M, Fazlollahi L, Le LP, Nitta M, Zhelyazkova BH, Davidson CJ, et al. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 2011; 20: 810-7; PMID:22137795; http://dx.doi.org/10. 1016/j.ccr.2011.11.005
23. Huang PH, Mukasa A, Bonavia R, Flynn RA, Brewer ZE, Cavenee WK, et al. Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc Natl Acad Sci U S A 2007; 104: 12867-72; PMID:17646646; http://dx.doi.org/10.1073/pnas.0705158104
24. Stommel JM, Kimmelman AC, Ying H, Nabioullin R, Ponugoti AH, Wiedemeyer R, et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 2007; 318: 287-90; PMID:17872411; http://dx.doi.org/10.1126/science. 1142946
25. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 2004; 64: 7099-109; PMID:15466206; http://dx.doi.org/10.1158/0008-5472.CAN-04-1443
26. Lyustikman Y, Momota H, Pao W, Holland EC. Constitutive activation of Raf-1 induces glioma formation in mice. Neoplasia 2008; 10: 501-10; PMID:18472967
27. Robinson JP, VanBrocklin MW, Guilbeault AR, Signorelli DL, Brandner S, Holmen SL. Activated BRAF induces gliomas in mice when combined with Ink4a/Arf loss or Akt activation. Oncogene 2010; 29: 335-44; PMID:19855433; http://dx.doi.org/10.1038/onc.2009.333
28. Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Siebels M, et al.; TARGET Study Group. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007; 356: 125-34; PMID:17215530; http://dx.doi.org/10.1056/ NEJMoa060655
29. Kane RC, Farrell AT, Madabushi R, Booth B, Chattopadhyay S, Sridhara R, et al. Sorafenib for the treatment of unresectable hepatocellular carcinoma. Oncologist 2009; 14: 95-100; PMID:19144678; http://dx.doi.org/10.1634/ theoncologist.2008-0185
30. Cervello M, Bachvarov D, Lampiasi N, Cusimano A, Azzolina A, McCubrey JA, et al. Molecular mechanisms of sorafenib action in liver cancer cells. Cell Cycle 2012; 11: 2843-55; PMID:22801548; http://dx.doi.org/10.4161/cc.21193
31. Yu C, Friday BB, Lai J-P, Yang L, Sarkaria J, Kay NE, et al. Cytotoxic synergy between the multikinase inhibitor sorafenib and the proteasome inhibitor bortezomib in vitro: induction of apoptosis through Akt and c-Jun NH2-terminal kinase pathways. Mol Cancer Ther 2006; 5: 2378-87; PMID:16985072; http://dx.doi.org/10.1158/1535-7163.MCT-06-0235
32. Wick W, Weller M, Weiler M, Batchelor T, Yung AWK, Platten M. Pathway inhibition: emerging molecular targets for treating glioblastoma. Neuro Oncol 2011; 13: 566-79; PMID:21636705; http://dx.doi.org/10.1093/neuonc/nor039
33. Secchiero P, Melloni E, Voltan R, Norcio A, Celeghini C, Zauli G. MCL1 down-regulation plays a critical role in mediating the higher anti-leukaemic activity of the multi-kinase inhibitor Sorafenib with respect to Dasatinib. Br J Haematol 2012; 157: 510-4; PMID:22313359; http://dx.doi.org/10.1111/j.1365- 2141.2012.09042.x
34. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, et al.; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. 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
35. Joensuu H, Puputti M, Sihto H, Tynninen O, Nupponen NN. Amplification of genes encoding KIT, PDGFRalpha and VEGFR2 receptor tyrosine kinases is frequent in glioblastoma multiforme. J Pathol 2005; 207: 224-31; PMID:16021678; http://dx.doi.org/10.1002/path.1823
36. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet 2000; 25: 55-7; PMID:10802656; http://dx.doi.org/ 10.1038/75596
37. Robinson JP, Vanbrocklin MW, McKinney AJ, Gach HM, Holmen SL. Akt signaling is required for glioblastoma maintenance in vivo. Am J Cancer Res 2011; 1: 155-67; PMID:21796274
38. Molina JR, Hayashi Y, Stephens C, Georgescu MM. Invasive glioblastoma cells acquire stemness and increased Akt activation. Neoplasia 2010; 12: 453-63; PMID:20563248
39. Sonoda Y, Ozawa T, Aldape KD, Deen DF, Berger MS, Pieper RO. Akt pathway activation converts anaplastic astrocytoma to glioblastoma multiforme in a human astrocyte model of glioma. Cancer Res 2001; 61: 6674-8; PMID:11559533
40. de la Iglesia N, Puram SV, Bonni A. STAT3 regulation of glioblastoma pathogenesis. Curr Mol Med 2009; 9: 580-90; PMID:19601808; http://dx.doi.org/10. 2174/156652409788488739
41. Yang F, Brown C, Buettner R, Hedvat M, Starr R, Scuto A, et al. Sorafenib induces growth arrest and apoptosis of human glioblastoma cells through the dephosphorylation of signal transducers and activators of transcription 3. Mol Cancer Ther 2010; 9: 953-62; PMID:20371721; http://dx.doi.org/10.1158/1535-7163. MCT-09-0947
42. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006; 9: 391-403; PMID:16697959; http://dx.doi.org/10.1016/j.ccr. 2006.03.030
43. Ligon KL, Huillard E, Mehta S, Kesari S, Liu H, Alberta JA, et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 2007; 53: 503-17; PMID:17296553; http://dx.doi.org/10.1016/j.neuron. 2007.01.009
44. Liang Y, Diehn M, Watson N, Bollen AW, Aldape KD, Nicholas MK, et al. Gene expression profiling reveals molecularly and clinically distinct subtypes of glioblastoma multiforme. Proc Natl Acad Sci U S A 2005; 102: 5814-9; PMID:15827123; http://dx.doi.org/10.1073/pnas.0402870102
45. Gangemi RMR, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P, et al. 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
46. Bonavia R, Inda MM, Cavenee WK, Furnari FB. Heterogeneity maintenance in glioblastoma: a social network. Cancer Res 2011; 71: 4055-60; PMID:21628493; http://dx.doi.org/10.1158/0008-5472.CAN-11-0153
47. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006; 5:67; PMID:17140455; http://dx.doi.org/10.1186/1476-4598-5-67
48. Bleau A-M, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, Brennan CW, 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: 226-35; PMID:19265662; http://dx.doi.org/10.1016/j.stem.2009.01.007
49. Siegelin MD, Raskett CM, Gilbert CA, Ross AH, Altieri DC. Sorafenib exerts anti-glioma activity in vitro and in vivo. Neurosci Lett 2010; 478: 165-70; PMID:20470863; http://dx.doi.org/10.1016/j.neulet. 2010.05.009
50. Yang F, Brown C, Buettner R, Hedvat M, Starr R, Scuto A, et al. Sorafenib induces growth arrest and apoptosis of human glioblastoma cells through the dephosphorylation of signal transducers and activators of transcription 3. Mol Cancer Ther 2010; 9: 953-62; PMID:20371721; http://dx.doi.org/10.1158/1535-7163. MCT-09-0947
51. Reardon DA, Vredenburgh JJ, Desjardins A, Peters K, Gururangan S, Sampson JH, et al. Effect of CYP3Ainducing anti-epileptics on sorafenib exposure: results of a phase II study of sorafenib plus daily temozolomide in adults with recurrent glioblastoma. J Neurooncol 2011; 101: 57-66; PMID:20443129; http://dx.doi.org/10.1007/s11060-010-0217-6
52. Den RB, Kamrava M, Sheng Z, Werner-Wasik M, Dougherty E, Marinucchi M, et al. A Phase I Study of the Combination of Sorafenib With Temozolomide and Radiation Therapy for the Treatment of Primary and Recurrent High-Grade Gliomas. International Journal of Radiation Oncology Biology Physics 2012; http://dx.doi.org/10.1016/j.ijrobp.2012.04.017
53. Favoni RE, Pattarozzi A, Lo Casto M, Barbieri F, Gatti M, Paleari L, et al. Gefitinib targets EGFR dimerization and ERK1/2 phosphorylation to inhibit pleural mesothelioma cell proliferation. Curr Cancer Drug Targets 2010; 10: 176-91; PMID:20088784; http://dx.doi.org/10.2174/156800910791054130
54. Barbieri F, Würth R, Favoni RE, Pattarozzi A, Gatti M, Ratto A, et al. Receptor tyrosine kinase inhibitors and cytotoxic drugs affect pleural mesothelioma cell proliferation: insight into EGFR and ERK1/2 as antitumor targets. Biochem Pharmacol 2011; 82: 1467-77; PMID:21787763; http://dx.doi.org/10.1016/j.bcp.2011.07.073