Pharmacologically controlled, discontinuous GDNF gene therapy restores motor function in a rat model of Parkinson's disease

Neurobiology of Disease

Volumn 65, Issue , 2014, Pages 35-42

  Tereshchenko, Julia ^a   Maddalena, Andrea ^a   Bähr, Mathias ^a   Kügler, Sebastian ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

AAV vector; Gene therapy; Neurotrophic factor; Parkinson; Regulation

Indexed keywords

AAV VECTOR; GENE THERAPY; NEUROTROPHIC FACTOR; PARKINSON; REGULATION;

ADENOVIRIDAE; ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; FUNCTIONAL LATERALITY; GENETIC THERAPY; GENETIC VECTORS; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; HORMONE ANTAGONISTS; MIFEPRISTONE; MOTOR ACTIVITY; OXIDOPAMINE; PARKINSON DISEASE; RATS; ROTATION; SYMPATHOLYTICS; TIME FACTORS; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 84893493523     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.01.009     Document Type: Article

References (38)

1. Akerud P., Alberch J., Eketjall S., et al. Differential effects of glial cell line-derived neurotrophic factor and neurturin on developing and adult substantia nigra dopaminergic neurons. J. Neurochem. 1999, 73:70-78.
2. Bartus R.T., Herzog C.D., Chu Y., et al. Bioactivity of AAV2-neurturin gene therapy (CERE-120): differences between Parkinson's disease and nonhuman primate brains. Mov. Disord. 2011, 26:27-36.
3. Bartus R.T., Baumann T.L., Brown L., et al. Advancing neurotrophic factors as treatments for age-related neurodegenerative diseases: developing and demonstrating "clinical proof-of-concept" for AAV-neurturin (CERE-120) in Parkinson's disease. Neurobiol. Aging 2013, 34:35-61.
4. Cress D.E. The need for regulatable vectors for gene therapy for Parkinson's disease. Exp. Neurol. 2008, 209:30-33.
5. Decressac M., Ulusoy A., Mattsson B., et al. GDNF fails to exert neuroprotection in a rat alpha-synuclein model of Parkinson's disease. Brain 2011, 134:2302-2311.
6. Decressac M., Volakakis N., Bjorklund A., Perlmann T. NURR1 in Parkinson disease-from pathogenesis to therapeutic potential. Nat. Rev. Neurol. 2013, 9:629-636.
7. Drinkut A., Tereshchenko Y., Schulz J.B., et al. Efficient gene therapy for Parkinson's disease using astrocytes as hosts for localized neurotrophic factor delivery. Mol. Ther. 2012, 20:534-543.
8. Eslamboli A., Georgievska B., Ridley R.M., et al. Continuous low-level glial cell line-derived neurotrophic factor delivery using recombinant adeno-associated viral vectors provides neuroprotection and induces behavioral recovery in a primate model of Parkinson's disease. J. Neurosci. 2005, 25:769-777.
9. Gallagher P., Young A.H. Mifepristone (RU-486) treatment for depression and psychosis: a review of the therapeutic implications. Neuropsychiatr. Dis. Treat. 2006, 2:33-42.
10. Georgievska B., Kirik D., Bjorklund A. Aberrant sprouting and downregulation of tyrosine hydroxylase in lesioned nigrostriatal dopamine neurons induced by long-lasting overexpression of glial cell line derived neurotrophic factor in the striatum by lentiviral gene transfer. Exp. Neurol. 2002, 177:461-474.
11. Georgievska B., Kirik D., Bjorklund A. Overexpression of glial cell line-derived neurotrophic factor using a lentiviral vector induces time- and dose-dependent downregulation of tyrosine hydroxylase in the intact nigrostriatal dopamine system. J. Neurosci. 2004, 24:6437-6445.
12. Ginhoux F., Turbant S., Gross D.A., et al. HLA-A*0201-restricted cytolytic responses to the rtTA transactivator dominant and cryptic epitopes compromise transgene expression induced by the tetracycline on system. Mol. Ther. 2004, 10:279-289.
13. Herzog C.D., Dass B., Holden J.E., et al. Striatal delivery of CERE-120, an AAV2 vector encoding human neurturin, enhances activity of the dopaminergic nigrostriatal system in aged monkeys. Mov. Disord. 2007, 22:1124-1132.
14. Herzog C.D., Brown L., Gammon D., et al. Expression, bioactivity, and safety 1 year after adeno-associated viral vector type 2-mediated delivery of neurturin to the monkey nigrostriatal system support cere-120 for Parkinson's disease. Neurosurgery 2009, 64:602-612. (discussion 612-603).
15. Hoane M.R., Gulwadi A.G., Morrison S., et al. Differential in vivo effects of neurturin and glial cell-line-derived neurotrophic factor. Exp. Neurol. 1999, 160:235-243.
16. Kells A.P., Eberling J., Su X., et al. Regeneration of the MPTP-lesioned dopaminergic system after convection-enhanced delivery of AAV2-GDNF. J. Neurosci. 2010, 30:9567-9577.
17. Kordower J.H., Olanow C.W. Regulatable promoters and gene therapy for Parkinson's disease: is the only thing to fear, fear itself?. Exp. Neurol. 2008, 209:34-40.
18. Kordower J.H., Olanow C.W., Dodiya H.B., et al. Disease duration and the integrity of the nigrostriatal system in Parkinson's disease. Brain 2013, 136:2419-2431.
19. Le Guiner C., Stieger K., Snyder R.O., et al. Immune responses to gene product of inducible promoters. Curr. Gene Ther. 2007, 7:334-346.
20. Lee Y., Messing A., Su M., Brenner M. GFAP promoter elements required for region-specific and astrocyte-specific expression. Glia 2008, 56:481-493.
21. Maddalena A., Tereshchenko J., Bähr M., Kügler S. Adeno-associated virus-mediated, mifepristone-regulated transgene expression in the brain. Mol. Ther. Nucleic Acids 2013, 2:e106.
22. Manfredsson F.P., Tumer N., Erdos B., et al. Nigrostriatal rAAV-mediated GDNF overexpression induces robust weight loss in a rat model of age-related obesity. Mol. Ther. 2009, 17:980-991.
23. Manfredsson F.P., Burger C., Rising A.C., et al. Tight long-term dynamic doxycycline responsive nigrostriatal GDNF using a single rAAV vector. Mol. Ther. 2009, 17:1857-1867.
24. Marks W.J., Bartus R.T., Siffert J., et al. Gene delivery of AAV2-neurturin for Parkinson's disease: a double-blind, randomised, controlled trial. Lancet Neurol. 2010, 9:1164-1172.
25. Mickiewicz A.L., Kordower J.H. GDNF family ligands: a potential future for Parkinson's disease therapy. CNS Neurol. Disord. Drug Targets 2011, 10:703-711.
26. Reagan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008, 22:659-661.
27. Rosenblad C., Kirik D., Devaux B., et al. Protection and regeneration of nigral dopaminergic neurons by neurturin or GDNF in a partial lesion model of Parkinson's disease after administration into the striatum or the lateral ventricle. Eur. J. Neurosci. 1999, 11:1554-1566.
28. Rosenblad C., Georgievska B., Kirik D. Long-term striatal overexpression of GDNF selectively downregulates tyrosine hydroxylase in the intact nigrostriatal dopamine system. Eur. J. Neurosci. 2003, 17:260-270.
29. Sajadi A., Bensadoun J.C., Schneider B.L., et al. Transient striatal delivery of GDNF via encapsulated cells leads to sustained behavioral improvement in a bilateral model of Parkinson disease. Neurobiol. Dis. 2006, 22:119-129.
30. Sauer H., Oertel W.H. Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine: a combined retrograde tracing and immunocytochemical study in the rat. Neuroscience 1994, 59:401-415.
31. Schallert T., Fleming S.M., Leasure J.L., et al. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, Parkinsonism and spinal cord injury. Neuropharmacology 2000, 39:777-787.
32. Stieger K., Belbellaa B., Le Guiner C., et al. In vivo gene regulation using tetracycline-regulatable systems. Adv. Drug Deliv. Rev. 2009, 61:527-541.
33. Su X., Kells A.P., Huang E.J., et al. Safety evaluation of AAV2-GDNF gene transfer into the dopaminergic nigrostriatal pathway in aged and Parkinsonian rhesus monkeys. Hum. Gene Ther. 2009, 20:1627-1640.
34. Tai K., Quintino L., Isaksson C., et al. Destabilizing domains mediate reversible transgene expression in the brain. PLoS One 2012, 7:e46269.
35. Watson S., Gallagher P., Porter R.J., et al. A randomized trial to examine the effect of mifepristone on neuropsychological performance and mood in patients with bipolar depression. Biol. Psychiatry 2012, 72:943-949.
36. Xiao M.F., Xu J.C., Tereshchenko Y., et al. Neural cell adhesion molecule modulates dopaminergic signaling and behavior by regulating dopamine D2 receptor internalization. J. Neurosci. 2009, 29:14752-14763.
37. Yang X., Mertens B., Lehtonen E., et al. Reversible neurochemical changes mediated by delayed intrastriatal glial cell line-derived neurotrophic factor gene delivery in a partial Parkinson's disease rat model. J. Gene Med. 2009, 11:899-912.
38. Ye X., Schillinger K., Burcin M.M., et al. Ligand-inducible transgene regulation for gene therapy. Methods Enzymol. 2002, 346:551-561.