Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2016 (2016), Article ID 5623235, 10 pages
http://dx.doi.org/10.1155/2016/5623235
Research Article

A Systematic Comparison Identifies an ATP-Based Viability Assay as Most Suitable Read-Out for Drug Screening in Glioma Stem-Like Cells

1Department of Neurosurgery, Brain Tumor Center, Erasmus MC, 3015 CE Rotterdam, Netherlands
2Department of Neurosurgery, St. Elisabeth Hospital, 5022 GC Tilburg, Netherlands

Received 8 October 2015; Revised 15 February 2016; Accepted 17 February 2016

Academic Editor: Heinrich Sauer

Copyright © 2016 A. Kleijn et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Stupp, W. P. Mason, M. J. Van Den Bent et al., “Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma,” New England Journal of Medicine, vol. 352, no. 10, pp. 987–996, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. R. G. W. Verhaak, K. A. Hoadley, E. Purdom et al., “ntegrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1,” Cancer Cell, vol. 17, no. 1, pp. 98–110, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Liang, M. Diehn, N. Watson et al., “Gene expression profiling reveals molecularly and clinically distinct subtypes of glioblastoma multiforme,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 16, pp. 5814–5819, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. S. G. M. Piccirillo, R. Combi, L. Cajola et al., “Distinct pools of cancer stem-like cells coexist within human glioblastomas and display different tumorigenicity and independent genomic evolution,” Oncogene, vol. 28, no. 15, pp. 1807–1811, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Sottoriva, I. Spiteri, S. G. M. Piccirillo et al., “Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 10, pp. 4009–4014, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. A. P. Patel, I. Tirosh, J. J. Trombetta et al., “Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma,” Science, vol. 344, no. 6190, pp. 1396–1401, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. M. E. Hardee, A. E. Marciscano, C. M. Medina-Ramirez et al., “Resistance of glioblastoma-initiating cells to radiation mediated by the tumor microenvironment can be abolished by inhibiting transforming growth factor-β,” Cancer Research, vol. 72, no. 16, pp. 4119–4129, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. M. D. Blough, D. C. Beauchamp, M. R. Westgate, J. J. Kelly, and J. G. Cairncross, “Effect of aberrant p53 function on temozolomide sensitivity of glioma cell lines and brain tumor initiating cells from glioblastoma,” Journal of Neuro-Oncology, vol. 102, no. 1, pp. 1–7, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Lee, S. Kotliarova, Y. Kotliarov 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, vol. 9, no. 5, pp. 391–403, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. R. K. Balvers, A. Kleijn, J. J. Kloezeman et al., “Serum-free culture success of glial tumors is related to specific molecular profiles and expression of extracellular matrix-associated gene modules,” Neuro-Oncology, vol. 15, no. 12, pp. 1684–1695, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Galli, E. Binda, U. Orfanelli et al., “Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma,” Cancer Research, vol. 64, no. 19, pp. 7011–7021, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Ernst, S. Hofmann, R. Ahmadi et al., “Genomic and expression profiling of glioblastoma stem cell-like spheroid cultures identifies novel tumor-relevant genes associated with survival,” Clinical Cancer Research, vol. 15, no. 21, pp. 6541–6550, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. R. S. Hotchkiss, A. Strasser, J. E. McDunn, and P. E. Swanson, “Mechanisms of disease: cell death,” New England Journal of Medicine, vol. 361, no. 16, pp. 1570–1583, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. C. A. Schmitt, “Cellular senescence and cancer treatment,” Biochimica et Biophysica Acta—Reviews on Cancer, vol. 1775, no. 1, pp. 5–20, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Galluzzi, M. C. Maiuri, I. Vitale et al., “Cell death modalities: classification and pathophysiological implications,” Cell Death and Differentiation, vol. 14, no. 7, pp. 1237–1243, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Y. Wen, S. M. Chang, K. R. Lamborn et al., “Phase I/II study of erlotinib and temsirolimus for patients with recurrent malignant gliomas: North American Brain Tumor Consortium trial 04-02,” Neuro-Oncology, vol. 16, no. 4, pp. 567–578, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Chinnaiyan, M. Won, P. Y. Wen et al., “RTOG 0913: a phase 1 study of daily everolimus (RAD001) in combination with radiation therapy and temozolomide in patients with newly diagnosed glioblastoma,” International Journal of Radiation Oncology Biology Physics, vol. 86, no. 5, pp. 880–884, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. http://clinicaltrials.gov/ct2/show/NCT01582516?term=delta24rgd+glioma&rank=2.
  19. L. Barazzuol, R. Jena, N. G. Burnet et al., “In vitro evaluation of combined temozolomide and radiotherapy using X rays and high-linear energy transfer radiation for glioblastoma,” Radiation Research, vol. 177, no. 5, pp. 651–662, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Schoenherr, S. A. Krueger, L. Martin, L. Marignol, G. D. Wilson, and B. Marples, “Determining if low dose hyper-radiosensitivity (HRS) can be exploited to provide a therapeutic advantage: a cell line study in four glioblastoma multiforme (GBM) cell lines,” International Journal of Radiation Biology, vol. 89, no. 12, pp. 1009–1016, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Takeuchi, Y. Kondo, K. Fujiwara et al., “Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors,” Cancer Research, vol. 65, no. 8, pp. 3336–3346, 2005. View at Google Scholar · View at Scopus
  22. H. Ito, H. Aoki, F. Kuhnel et al., “Autophagic cell death of malignant glioma cells induced by a conditionally replicating adenovirus,” Journal of the National Cancer Institute, vol. 98, no. 9, pp. 625–636, 2006. View at Publisher · View at Google Scholar
  23. A. V. Knizhnik, W. P. Roos, T. Nikolova et al., “Survival and death strategies in glioma cells: autophagy, senescence and apoptosis triggered by a single type of temozolomide-induced DNA damage,” PLoS ONE, vol. 8, no. 1, Article ID e55665, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Jiang, E. J. White, C. I. Ríos-Vicil, J. Xu, C. Gomez-Manzano, and J. Fueyo, “Human adenovirus type 5 induces cell lysis through autophagy and autophagy-triggered caspase activity,” Journal of Virology, vol. 85, no. 10, pp. 4720–4729, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Castedo, K. F. Ferri, and G. Kroemer, “Mammalian target of rapamycin (mTOR): Pro- and anti-apoptotic,” Cell Death and Differentiation, vol. 9, no. 2, pp. 99–100, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. E. Cohen-Jonathan, E. J. Bernhard, and W. G. McKenna, “How does radiation kill cells?” Current Opinion in Chemical Biology, vol. 3, no. 1, pp. 77–83, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. R. K. Balvers, M. L. M. Lamfers, J. J. Kloezeman et al., “ABT-888 enhances cytotoxic effects of temozolomide independent of MGMT status in serum free cultured glioma cells,” Journal of Translational Medicine, vol. 13, article 74, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. L. M. Berghauser Pont, J. K. Spoor, S. Venkatesan et al., “The Bcl-2 inhibitor Obatoclax overcomes resistance to histone deacetylase inhibitors SAHA and LBH589 as radiosensitizers in patient-derived glioblastoma stem-like cells,” Genes & Cancer, vol. 5, no. 11-12, pp. 445–459, 2014. View at Google Scholar
  29. K. Suzuki, J. Fueyo, V. Krasnykh, P. N. Reynolds, D. T. Curiel, and R. Alemany, “A conditionally replicative adenovirus with enhanced infectivity shows improved oncolytic potency,” Clinical Cancer Research, vol. 7, no. 1, pp. 120–126, 2001. View at Google Scholar · View at Scopus
  30. M. L. M. Lamfers, J. Grill, C. M. F. Dirven et al., “Potential of the conditionally replicative adenovirus Ad5-Delta24RGD in the treatment of malignant gliomas and its enhanced effect with radiotherapy,” Cancer Research, vol. 62, no. 20, pp. 5736–5742, 2002. View at Google Scholar · View at Scopus
  31. L. M. Berghauser Pont, A. Kleijn, J. J. Kloezeman et al., “The HDAC inhibitors scriptaid and LBH589 combined with the oncolytic virus Delta24-RGD exert enhanced anti-tumor efficacy in patient-derived glioblastoma cells,” PLoS ONE, vol. 10, no. 5, Article ID e0127058, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. N. A. P. Franken, H. M. Rodermond, J. Stap, J. Haveman, and C. van Bree, “Clonogenic assay of cells in vitro,” Nature Protocols, vol. 1, no. 5, pp. 2315–2319, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Idema, A. A. Geldof, C. M. F. Dirven et al., “Evaluation of adenoviral oncolytic effect on glioma spheroids by 18F-DG positron-emission tomography,” Oncology Research, vol. 16, no. 10, pp. 471–477, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Galluzzi, J. M. Bravo-San Pedro, I. Vitale et al., “Essential versus accessory aspects of cell death: recommendations of the NCCD 2015,” Cell Death and Differentiation, vol. 22, no. 1, pp. 58–73, 2015. View at Publisher · View at Google Scholar
  35. D. C. Fingar, C. J. Richardson, A. R. Tee, L. Cheatham, C. Tsou, and J. Blenis, “mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E,” Molecular and Cellular Biology, vol. 24, no. 1, pp. 200–216, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Li, S. G. Kim, and J. Blenis, “Rapamycin: one drug, many effects,” Cell Metabolism, vol. 19, no. 3, pp. 373–379, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. J. L. Yecies and B. D. Manning, “Transcriptional control of cellular metabolism by mtor signaling,” Cancer Research, vol. 71, no. 8, pp. 2815–2820, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. A. A. Stepanenko and V. V. Dmitrenko, “Pitfalls of the MTT assay: direct and off-target effects of inhibitors can result in over/underestimation of cell viability,” Gene, vol. 574, no. 2, pp. 193–203, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Ramanathan and S. L. Schreiber, “Direct control of mitochondrial function by mTOR,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 52, pp. 22229–22232, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. S. M. Pollard, K. Yoshikawa, I. D. Clarke et al., “Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens,” Cell Stem Cell, vol. 4, no. 6, pp. 568–580, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. L. M. Berghauser Pont, R. K. Balvers, J. J. Kloezeman et al., “In vitro screening of clinical drugs identifies sensitizers of oncolytic viral therapy in glioblastoma stem-like cells,” Gene Therapy, vol. 22, no. 12, pp. 947–959, 2015. View at Publisher · View at Google Scholar · View at Scopus