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Neural Plasticity
Volume 2019, Article ID 6286197, 9 pages
https://doi.org/10.1155/2019/6286197
Research Article

Widespread Striatal Delivery of GDNF from Encapsulated Cells Prevents the Anatomical and Functional Consequences of Excitotoxicity

1Gloriana Therapeutics, Providence, Rhode Island, USA
2Department of Neurological Sciences, Rush University Medical Center, Chicago Illinois, USA
3Cytosolv, Providence, Rhode Island, USA
4Department of Diagnostic and Public Health, Section of Pharmacology, University of Verona P.le, LA Scuro, Verona, Italy

Correspondence should be addressed to Dwaine F. Emerich; moc.xtanairolg@efd

Received 9 November 2018; Accepted 11 February 2019; Published 11 March 2019

Guest Editor: Jolanta Dorszewska

Copyright © 2019 Dwaine F. Emerich 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. L. Wang, S. Muramatsu, Y. Lu et al., “Delayed delivery of AAV-GDNF prevents nigral neurodegeneration and promotes functional recovery in a rat model of Parkinson’s disease,” Gene Therapy, vol. 9, no. 6, pp. 381–389, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Grondin, Z. Zhang, Y. Ai, D. M. Gash, and G. A. Gerhardt, “Intracranial delivery of proteins and peptides as a therapy for neurodegenerative diseases,” in Peptide Transport and Delivery into the Central Nervous System, L. Prokai and K. Prokai-Tatrai, Eds., vol. 61 of Progress in Drug Research, pp. 101–123, Birkhäuser, Basel, 2003. View at Publisher · View at Google Scholar
  3. E. Dowd, C. Monville, E. M. Torres et al., “Lentivector-mediated delivery of GDNF protects complex motor functions relevant to human Parkinsonism in a rat lesion model,” The European Journal of Neuroscience, vol. 22, no. 10, pp. 2587–2595, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. J. S. Zheng, L. L. Tang, S. S. Zheng et al., “Delayed gene therapy of glial cell line-derived neurotrophic factor is efficacious in a rat model of Parkinson’s disease,” Molecular Brain Research, vol. 134, no. 1, pp. 155–161, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. Miyoshi, Z. Zhang, A. Ovadia et al., “Glial cell line-derived neurotrophic factor-levodopa interactions and reduction of side effects in parkinsonian monkeys,” Annals of Neurology, vol. 42, no. 2, pp. 208–214, 1997. View at Publisher · View at Google Scholar · View at Scopus
  6. D. M. Gash, Z. Zhang, A. Ovadia et al., “Functional recovery in parkinsonian monkeys treated with GDNF,” Nature, vol. 380, no. 6571, pp. 252–255, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Palfi, L. Leventhal, Y. Chu et al., “Lentivirally delivered glial cell line-derived neurotrophic factor increases the number of striatal dopaminergic neurons in primate models of nigrostriatal degeneration,” The Journal of Neuroscience, vol. 22, no. 12, pp. 4942–4954, 2002. View at Publisher · View at Google Scholar
  8. J. H. Kordower, M. E. Emborg, J. Bloch et al., “Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson’s disease,” Science, vol. 290, no. 5492, pp. 767–773, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. J. H. Kordower, S. Palfi, E. Y. Chen et al., “Clinicopathological findings following intraventricular glial-derived neurotrophic factor treatment in a patient with Parkinson’s disease,” Annals of Neurology, vol. 46, no. 3, pp. 419–424, 1999. View at Publisher · View at Google Scholar
  10. A. E. Lang, S. Gill, N. K. Patel et al., “Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease,” Annals of Neurology, vol. 59, no. 3, pp. 459–466, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. J. G. Nutt, K. J. Burchiel, C. L. Comella et al., “Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD,” Neurology, vol. 60, no. 1, pp. 69–73, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. T. B. Sherer, B. K. Fiske, C. N. Svendsen, A. E. Lang, and J. W. Langston, “Crossroads in GDNF therapy for Parkinson’s disease,” Movement Disorders, vol. 21, no. 2, pp. 136–141, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. M. F. Salvatore, Y. Ai, B. Fischer et al., “Point source concentration of GDNF may explain failure of phase II clinical trial,” Experimental Neurology, vol. 202, no. 2, pp. 497–505, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. P. F. Morrison, R. R. Lonser, and E. H. Oldfield, “Convective delivery of glial cell line–derived neurotrophic factor in the human putamen,” Journal of Neurosurgery, vol. 107, no. 1, pp. 74–83, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Shi, G. Chen, L. Lv et al., “The effect of lentivirus-mediated TH and GDNF genetic engineering mesenchymal stem cells on Parkinson’s disease rat model,” Neurological Sciences, vol. 32, no. 1, pp. 41–51, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. O. Lindvall and L. U. Wahlberg, “Encapsulated cell biodelivery of GDNF: a novel clinical strategy for neuroprotection and neuroregeneration in Parkinson’s disease?” Experimental Neurology, vol. 209, no. 1, pp. 82–88, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. D. F. Emerich, G. Orive, C. Thanos, J. Tornoe, and L. U. Wahlberg, “Encapsulated cell therapy for neurodegenerative diseases: from promise to product,” Advanced Drug Delivery Reviews, vol. 67-68, pp. 131–141, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. M. D. Lindner, S. R. Winn, E. E. Baetge et al., “Implantation of encapsulated catecholamine and GDNF-producing cells in rats with unilateral dopamine depletions and parkinsonian symptoms,” Experimental Neurology, vol. 132, no. 1, pp. 62–76, 1995. View at Publisher · View at Google Scholar · View at Scopus
  19. D. F. Emerich, M. Plone, J. Francis, B. R. Frydel, S. R. Winn, and M. D. Lindner, “Alleviation of behavioral deficits in aged rodents following implantation of encapsulated GDNF-producing fibroblasts,” Brain Research, vol. 736, no. 1-2, pp. 99–110, 1996. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Kishima, T. Poyot, J. Bloch et al., “Encapsulated GDNF-producing C2C12 cells for Parkinson’s disease: a pre-clinical study in chronic MPTP-treated baboons,” Neurobiology of Disease, vol. 16, no. 2, pp. 428–439, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Fjord-Larsen, P. Kusk, D. F. Emerich et al., “Increased encapsulated cell biodelivery of nerve growth factor in the brain by transposon-mediated gene transfer,” Gene Therapy, vol. 19, no. 10, pp. 1010–1017, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Fjord-Larsen, P. Kusk, J. Tornøe et al., “Long-term delivery of nerve growth factor by encapsulated cell biodelivery in the Göttingen minipig basal forebrain,” Molecular Therapy, vol. 18, no. 12, pp. 2164–2172, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. L. U. Wahlberg, G. Lind, P. M. Almqvist et al., “Targeted delivery of nerve growth factor via encapsulated cell biodelivery in Alzheimer disease: a technology platform for restorative neurosurgery,” Journal of Neurosurgery, vol. 117, no. 2, pp. 340–347, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Saito, A. Washio, K. Miyashita et al., “Effects of polymer encapsulated glial cell line-derived neurotrophic factor secreting cells on odontoblast-like cell survival,” Journal of Regenerative Medicine, vol. 6, no. 3, p. 3, 2017. View at Publisher · View at Google Scholar
  25. J. Tornøe, M. Torp, J. R. Jørgensen et al., “Encapsulated cell-based biodelivery of meteorin is neuroprotective in the quinolinic acid rat model of neurodegenerative disease,” Restorative Neurology and Neuroscience, vol. 30, no. 3, pp. 225–236, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. R. T. Bartus, C. D. Herzog, Y. Chu et al., “Bioactivity of AAV2-neurturin gene therapy (CERE-120): differences between Parkinson’s disease and nonhuman primate brains,” Movement Disorders, vol. 26, no. 1, pp. 27–36, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Chu, G. A. Morfini, L. B. Langhamer, Y. He, S. T. Brady, and J. H. Kordower, “Alterations in axonal transport motor proteins in sporadic and experimental Parkinson’s disease,” Brain, vol. 135, no. 7, pp. 2058–2073, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. H. J. G. Gundersen and E. B. Jensen, “The efficiency of systematic sampling in stereology and its prediction,” Journal of Microscopy, vol. 147, no. 3, pp. 229–263, 1987. View at Publisher · View at Google Scholar · View at Scopus
  29. W. M. Pardridge, “The blood-brain barrier: bottleneck in brain drug development,” NeuroRX, vol. 2, no. 1, pp. 3–14, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Fjord-Larsen, P. Kusk, M. Torp et al., “Encapsulated cell biodelivery of transposon-mediated high-dose NGF to the Göttingen mini pig basal forebrain,” The Open Tissue Engineering and Regenerative Medicine Journal, vol. 5, no. 1, pp. 35–42, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Falcicchia, G. Paolone, D. F. Emerich et al., “Seizure-suppressant and neuroprotective effects of encapsulated BDNF-producing cells in a rat model of temporal lobe epilepsy,” Molecular Therapy - Methods & Clinical Development, vol. 9, pp. 211–224, 2018. View at Publisher · View at Google Scholar
  32. G. Paolone, C. Falcicchia, F. Lovisari et al., “Long-term, targeted delivery of GDNF from encapsulated cells is neuroprotective and reduces seizures in the pilocarpine model of epilepsy,” The Journal of Neuroscience, 2019. View at Publisher · View at Google Scholar
  33. A. Nanobashvili, E. Melin, D. Emerich et al., “Unilateral ex vivo gene therapy by GDNF in epileptic rats,” Gene Therapy, 2018. View at Publisher · View at Google Scholar
  34. S. Ramaswamy, J. L. McBride, and J. H. Kordower, “Animal models of Huntington’s disease,” ILAR Journal, vol. 48, no. 4, pp. 356–373, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. J. R. Pineda, N. Rubio, P. Akerud et al., “Neuroprotection by GDNF-secreting stem cells in a Huntington’s disease model: optical neuroimage tracking of brain-grafted cells,” Gene Therapy, vol. 14, no. 2, pp. 118–128, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Alberch, E. Pérez-Navarro, and J. M. Canals, “Neuroprotection by neurotrophins and GDNF family members in the excitotoxic model of Huntington’s disease,” Brain Research Bulletin, vol. 57, no. 6, pp. 817–822, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Marco, E. Pérez-Navarro, E. Tolosa, E. Arenas, and J. Alberch, “Striatopallidal neurons are selectively protected by neurturin in an excitotoxic model of Huntington’s disease,” Journal of Neurobiology, vol. 50, no. 4, pp. 323–332, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Gratacòs, E. Pérez-Navarro, E. Tolosa, E. Arenas, and J. Alberch, “Neuroprotection of striatal neurons against kainate excitotoxicity by neurotrophins and GDNF family members,” Journal of Neurochemistry, vol. 78, no. 6, pp. 1287–1296, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. E. Pérez-Navarro, E. Arenas, J. Reiriz, N. Calvo, and J. Alberch, “Glial cell line-derived neurotrophic factor protects striatal calbindin-immunoreactive neurons from excitotoxic damage,” Neuroscience, vol. 75, no. 2, pp. 345–352, 1996. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Ramaswamy, J. L. McBride, I. Han et al., “Intrastriatal CERE-120 (AAV-neurturin) protects striatal and cortical neurons and delays motor deficits in a transgenic mouse model of Huntington’s disease,” Neurobiology of Disease, vol. 34, no. 1, pp. 40–50, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Ramaswamy, J. L. McBride, C. D. Herzog et al., “Neurturin gene therapy improves motor function and prevents death of striatal neurons in a 3-nitropropionic acid rat model of Huntington’s disease,” Neurobiology of Disease, vol. 26, no. 2, pp. 375–384, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. J. L. McBride, S. Ramaswamy, M. Gasmi et al., “Viral delivery of glial cell line-derived neurotrophic factor improves behavior and protects striatal neurons in a mouse model of Huntington’s disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 24, pp. 9345–9350, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. D. M. Araujo and D. C. Hilt, “Glial cell line-derived neurotrophic factor attenuates the excitotoxin-induced behavioral and neurochemical deficits in a rodent model of Huntington’s disease,” Neuroscience, vol. 81, no. 4, pp. 1099–1110, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. D. M. Araujo and D. C. Hilt, “Glial cell line-derived neurotrophic factor attenuates the locomotor hypofunction and striatonigral neurochemical deficits induced by chronic systemic administration of the mitochondrial toxin 3-nitropropionic acid,” Neuroscience, vol. 82, no. 1, pp. 117–127, 1998. View at Google Scholar
  45. J. L. McBride, M. J. During, J. Wuu, E.-Y. Chen, S. E. Leurgans, and J. H. Kordower, “Structural and functional neuroprotection in a rat model of Huntington’s disease by viral gene transfer of GDNF,” Experimental Neurology, vol. 181, no. 2, pp. 213–223, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. The Huntington’s Disease Collaborative Research Group, “A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes,” Cell, vol. 72, no. 6, pp. 971–983, 1993. View at Publisher · View at Google Scholar · View at Scopus