Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2016, Article ID 4095072, 14 pages
http://dx.doi.org/10.1155/2016/4095072
Research Article

Monitoring the Bystander Killing Effect of Human Multipotent Stem Cells for Treatment of Malignant Brain Tumors

1Biomedical MRI, Department of Imaging and Pathology, KU Leuven, 3000 Leuven, Belgium
2Molecular Small Animal Imaging Center, KU Leuven, 3000 Leuven, Belgium
3Imec, 3000 Leuven, Belgium
4Morphology Research Group, Biomedical Research Institute, Hasselt University, 3590 Diepenbeek, Belgium
5Department of Development and Regeneration, Stem Cell Institute, KU Leuven, 3000 Leuven, Belgium
6Division of Radiology, University Hospitals Leuven, 3000 Leuven, Belgium

Received 13 August 2015; Accepted 16 November 2015

Academic Editor: Ian Y. Chen

Copyright © 2016 Cindy Leten 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. D. N. Louis, H. Ohgaki, O. D. Wiestler et al., “The 2007 WHO classification of tumours of the central nervous system,” Acta Neuropathologica, vol. 114, no. 2, pp. 97–109, 2007. View at Publisher · View at Google Scholar
  2. R. Stupp, W. P. Mason, M. J. Van Den Bent et al., “Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma,” The New England Journal of Medicine, vol. 352, no. 10, pp. 987–996, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. A. A. Thomas, C. W. Brennan, L. M. DeAngelis, and A. M. Omuro, “Emerging therapies for glioblastoma,” JAMA Neurology, vol. 71, no. 11, pp. 1437–1444, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. B. Auffinger, D. Spencer, P. Pytel, A. U. Ahmed, and M. S. Lesniak, “The role of glioma stem cells in chemotherapy resistance and glioblastoma multiforme recurrence,” Expert Review of Neurotherapeutics, vol. 15, no. 7, pp. 741–752, 2015. View at Publisher · View at Google Scholar
  5. H. Miletic, Y. Fischer, S. Litwak et al., “Bystander killing of malignant glioma by bone marrow-derived tumor-infiltrating progenitor cells expressing a suicide gene,” Molecular Therapy, vol. 15, no. 7, pp. 1373–1381, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Miletic, Y. H. Fischer, T. Giroglou et al., “Normal brain cells contribute to the bystander effect in suicide gene therapy of malignant glioma,” Clinical Cancer Research, vol. 13, no. 22, pp. 6761–6768, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. I. Paw, R. C. Carpenter, K. Watabe, W. Debinski, and H. W. Lo, “Mechanisms regulating glioma invasion,” Cancer Letters, vol. 362, no. 1, pp. 1–7, 2015. View at Publisher · View at Google Scholar
  8. G. Vassaux and P. Martin-Duque, “Use of suicide genes for cancer gene therapy: study of the different approaches,” Expert Opinion on Biological Therapy, vol. 4, no. 4, pp. 519–530, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Duarte, G. Carle, H. Faneca, M. C. P. D. Lima, and V. Pierrefite-Carle, “Suicide gene therapy in cancer: where do we stand now?” Cancer Letters, vol. 324, no. 2, pp. 160–170, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. F. L. Moolten, “Tumor chemosensitivity conferred by inserted herpes thymidine kinase genes: paradigm for a prospective cancer control strategy,” Cancer Research, vol. 46, no. 10, pp. 5276–5281, 1986. View at Google Scholar · View at Scopus
  11. A. H. Jacobs, A. Winkeler, M. Hartung et al., “Improved herpes simplex virus type 1 amplicon vectors for proportional coexpression of positron emission tomography marker and therapeutic genes,” Human Gene Therapy, vol. 14, no. 3, pp. 277–297, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Kucerova, V. Altanerova, M. Matuskova, S. Tyciakova, and C. Altaner, “Adipose tissue-derived human mesenchymal stem cells mediated prodrug cancer gene therapy,” Cancer Research, vol. 67, no. 13, pp. 6304–6313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Li, T. Tokuyama, J. Yamamoto, M. Koide, N. Yokota, and H. Namba, “Bystander effect-mediated gene therapy of gliomas using genetically engineered neural stem cells,” Cancer Gene Therapy, vol. 12, no. 7, pp. 600–607, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. K. S. Aboody, A. Brown, N. G. Rainov et al., “Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 23, pp. 12846–12851, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Nakamizo, F. Marini, T. Amano et al., “Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas,” Cancer Research, vol. 65, no. 8, pp. 3307–3318, 2005. View at Google Scholar
  16. E. Binello and I. M. Germano, “Stem cells as therapeutic vehicles for the treatment of high-grade gliomas,” Neuro-Oncology, vol. 14, no. 3, pp. 256–265, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Leten, J. Trekker, T. Struys et al., “Assessment of bystander killing-mediated therapy of malignant brain tumors using a multimodal imaging approach,” Stem Cell Research & Therapy, vol. 6, article 163, 2015. View at Publisher · View at Google Scholar
  18. M. Mesnil, C. Piccoli, G. Tiraby, K. Willecke, and H. Yamasaki, “Bystander killing of cancer cells by herpes simplex virus thymidine kinase gene is mediated by connexins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 5, pp. 1831–1835, 1996. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Fick, F. G. Barker II, P. Dazin, E. M. Westphale, E. C. Beyer, and M. A. Israel, “The extent of heterocellular communication mediated by gap junctions is predictive of bystander tumor cytotoxicity in vitro,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 24, pp. 11071–11075, 1995. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Estin, M. Li, D. Spray, and J. K. Wu, “Connexins are expressed in primary brain tumors and enhance the bystander effect in gene therapy,” Neurosurgery, vol. 44, no. 2, pp. 361–369, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Leten, V. D. Roobrouck, T. Struys et al., “Controlling and monitoring stem cell safety in vivo in an experimental rodent model,” Stem Cells, vol. 32, no. 11, pp. 2833–2844, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Matuskova, K. Hlubinova, A. Pastorakova et al., “HSV-tk expressing mesenchymal stem cells exert bystander effect on human glioblastoma cells,” Cancer Letters, vol. 290, no. 1, pp. 58–67, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Van Cauter, F. De Keyzer, D. M. Sima et al., “Integrating diffusion kurtosis imaging, dynamic susceptibility-weighted contrast-enhanced MRI, and short echo time chemical shift imaging for grading gliomas,” Neuro-Oncology, vol. 16, no. 7, pp. 1010–1021, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. M. R. Neagu, R. Y. Huang, D. A. Reardon, and P. Y. Wen, “How treatment monitoring is influencing treatment decisions in glioblastomas,” Current Treatment Options in Neurology, vol. 17, article 15, 2015. View at Publisher · View at Google Scholar
  25. W.-D. Heiss, P. Raab, and H. Lanfermann, “Multimodality assessment of brain tumors and tumor recurrence,” Journal of Nuclear Medicine, vol. 52, no. 10, pp. 1585–1600, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Cha, “Update on brain tumor imaging: From anatomy to physiology,” American Journal of Neuroradiology, vol. 27, no. 3, pp. 475–487, 2006. View at Google Scholar · View at Scopus
  27. R. B. Luwor, S. S. Stylli, and A. H. Kaye, “Using bioluminescence imaging in glioma research,” Journal of Clinical Neuroscience, vol. 22, no. 5, pp. 779–784, 2015. View at Publisher · View at Google Scholar
  28. A. Winkeler, M. Sena-Esteves, L. E. M. Paulis et al., “Switching on the lights for gene therapy,” PLoS ONE, vol. 2, no. 6, article e528, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Waerzeggers, M. Klein, H. Miletic et al., “Multimodal imaging of neural progenitor cell fate in rodents,” Molecular Imaging, vol. 7, no. 2, pp. 77–91, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. U. Himmelreich and M. Hoehn, “Stem cell labeling for magnetic resonance imaging,” Minimally Invasive Therapy and Allied Technologies, vol. 17, no. 2, pp. 132–142, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Reyes, A. Dudek, B. Jahagirdar, L. Koodie, P. H. Marker, and C. M. Verfaillie, “Origin of endothelial progenitors in human postnatal bone marrow,” Journal of Clinical Investigation, vol. 109, no. 3, pp. 337–346, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Trekker, C. Leten, T. Struys et al., “Sensitive in vivo cell detection using size-optimized superparamagnetic nanoparticles,” Biomaterials, vol. 35, no. 5, pp. 1627–1635, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Trekker, K. Jans, H. Damm et al., “Synthesis of PEGylated magnetic nanoparticles with different core sizes,” IEEE Transactions on Magnetics, vol. 49, no. 1, pp. 219–226, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Leten, T. Struys, T. Dresselaers, and U. Himmelreich, “In vivo and ex vivo assessment of the blood brain barrier integrity in different glioblastoma animal models,” Journal of Neuro-Oncology, vol. 119, no. 2, pp. 297–306, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. X. L. Aranguren, J. D. McCue, B. Hendrickx et al., “Multipotent adult progenitor cells sustain function of ischemic limbs in mice,” The Journal of Clinical Investigation, vol. 118, no. 2, pp. 505–514, 2008. View at Google Scholar
  36. H. Namba, M. Tagawa, T. Miyagawa, Y. Iwadate, and S. Sakiyama, “Treatment of rat experimental brain tumors by herpes simplex virus thymidine kinase gene-transduced allogeneic tumor cells and ganciclovir,” Cancer Gene Therapy, vol. 7, no. 6, pp. 947–953, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Namba, Y. Iwadate, K. Kawamura, S. Sakiyama, and M. Tagawa, “Efficacy of the bystander effect in the herpes simplex virus thymidine kinase-mediated gene therapy is influenced by the expression of connexin43 in the target cells,” Cancer Gene Therapy, vol. 8, no. 6, pp. 414–420, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Stupp, M. E. Hegi, W. P. Mason et al., “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,” The Lancet Oncology, vol. 10, no. 5, pp. 459–466, 2009. View at Publisher · View at Google Scholar
  39. E. A. Chiocca, K. M. Abbed, S. Tatter et al., “A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting,” Molecular Therapy, vol. 10, no. 5, pp. 958–966, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Pu, Z. Xia, S. Yu, and Q. Huang, “Altered expression of Cx43 in astrocytic tumors,” Clinical Neurology and Neurosurgery, vol. 107, no. 1, pp. 49–54, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. R. G. Vile, R. M. Diaz, S. Castleden, and H. Chong, “Targeted gene therapy for cancer: herpes simplex virus thymidine kinase gene-mediated cell killing leads to anti-tumour immunity that can be augmented by co-expression of cytokines in the tumour cells,” Biochemical Society Transactions, vol. 25, no. 2, pp. 717–722, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. R. G. Vile, S. Castleden, J. Marshall, R. Camplejohn, C. Uptov, and H. Chong, “Generation of an anti-tumour immune response in a non-immunogenic tumour: HSVtk killing in vivo stimulates a mononuclear cell infiltrate and a Th1-like profile of intratumoural cytokine expression,” International Journal of Cancer, vol. 71, no. 2, pp. 267–274, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Braumüller, T. Wieder, E. Brenner et al., “T-helper-1-cell cytokines drive cancer into senescence,” Nature, vol. 494, no. 7437, pp. 361–365, 2013. View at Publisher · View at Google Scholar · View at Scopus