Reversible neurochemical changes mediated by delayed intrastriatal glial cell line-derived neurotrophic factor gene delivery in a partial Parkinson's disease rat model

Background Efficient protection of dopaminergic neurons against a subsequent 6‐hydroxydopamine lesion by glial cell line‐derived neurotrophic factor (GDNF) gene delivery has been demonstrated. By contrast, the neurorestorative effects of GDNF administered several weeks after the toxin have been less...

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Published inThe journal of gene medicine Vol. 11; no. 10; pp. 899 - 912
Main Authors Yang, Xin, Mertens, Birgit, Lehtonen, Enni, Vercammen, Linda, Bockstael, Olivier, Chtarto, Abdelwahed, Levivier, Marc, Brotchi, Jacques, Michotte, Yvette, Baekelandt, Veerle, Sarre, Sophie, Tenenbaum, Liliane
Format Journal Article
LanguageEnglish
Published Chichester, UK John Wiley & Sons, Ltd 01.10.2009
Wiley Periodicals Inc
Subjects
6-hydroxydopamine
adeno-associated viral vector
Adeno-associated virus
Adrenergic Agents - administration & dosage
Adrenergic Agents - adverse effects
Animals
Dependovirus - genetics
Dopamine - analysis
Dopamine - biosynthesis
Doxycycline - administration & dosage
Female
Gene Expression - drug effects
Gene therapy
Gene Transfer Techniques
Genetic Vectors - administration & dosage
Genetic Vectors - genetics
Genetic Vectors - metabolism
glial cell line-derived neurotrophic factor
Glial Cell Line-Derived Neurotrophic Factor - administration & dosage
Glial Cell Line-Derived Neurotrophic Factor - biosynthesis
Glial Cell Line-Derived Neurotrophic Factor - genetics
Humans
Motor Activity - drug effects
Oxidopamine - administration & dosage
Oxidopamine - adverse effects
Parkinson Disease, Secondary - chemically induced
Parkinson Disease, Secondary - metabolism
Parkinson Disease, Secondary - therapy
Parkinson's disease
phosphorylation
Rats
tetracycline-inducible
Time Factors
Tyrosine 3-Monooxygenase - analysis
Tyrosine 3-Monooxygenase - biosynthesis
tyrosine hydroxylase
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Abstract Background Efficient protection of dopaminergic neurons against a subsequent 6‐hydroxydopamine lesion by glial cell line‐derived neurotrophic factor (GDNF) gene delivery has been demonstrated. By contrast, the neurorestorative effects of GDNF administered several weeks after the toxin have been less characterized. In particular, whether these were permanent or dependent on the continuous presence of GDNF remains elusive. Methods A tetracycline‐inducible adeno‐associated virus (AAV)‐1 vector expressing human GDNF cDNA was administered unilaterally in the rat striatum 5 weeks after 6‐hydroxydopamine. Rats were treated with doxycycline (dox) or untreated from the day of vector injection until sacrifice (4 or 14 weeks). A sub‐group was dox‐treated for 7 weeks then untreated until 14 weeks. The motor behavior was assessed by amphetamine‐induced rotations and spontaneous forelimb asymmetry. The amounts of tyrosine hydroxylase (TH), serine‐40‐phosphorylated TH (S40‐TH) and aromatic amino acid decarboxylase (AADC) proteins were compared by western blotting and the dopamine levels quantified by high‐performance liquid chromatography. Results Dox‐dependent behavioral improvements were demonstrated 4 weeks post‐vector injection. At later time points, spontaneous partial recovery was observed in all rats, but no further improvement was found in dox‐treated animals. TH levels were significantly increased in dox‐treated rats at all time points. By contrast, striatal dopamine and S40‐TH were increased at 4 weeks, but not 14 weeks, and AADC remained unchanged. Dox withdrawal after 7 weeks, resulted in TH levels comparable to the controls at 14 weeks. Conclusions Delayed GDNF gene delivery only transiently improved dopaminergic function. Over the long term, TH was more abundant, but not functional, and the increase was lost when GDNF gene expression was switched off. Copyright © 2009 John Wiley & Sons, Ltd.
AbstractList Background Efficient protection of dopaminergic neurons against a subsequent 6-hydroxydopamine lesion by glial cell line-derived neurotrophic factor (GDNF) gene delivery has been demonstrated. By contrast, the neurorestorative effects of GDNF administered several weeks after the toxin have been less characterized. In particular, whether these were permanent or dependent on the continuous presence of GDNF remains elusive. Methods A tetracycline-inducible adeno-associated virus (AAV)-1 vector expressing human GDNF cDNA was administered unilaterally in the rat striatum 5 weeks after 6-hydroxydopamine. Rats were treated with doxycycline (dox) or untreated from the day of vector injection until sacrifice (4 or 14 weeks). A sub-group was dox-treated for 7 weeks then untreated until 14 weeks. The motor behavior was assessed by amphetamine-induced rotations and spontaneous forelimb asymmetry. The amounts of tyrosine hydroxylase (TH), serine-40-phosphorylated TH (S40-TH) and aromatic amino acid decarboxylase (AADC) proteins were compared by western blotting and the dopamine levels quantified by high-performance liquid chromatography. Results Dox-dependent behavioral improvements were demonstrated 4 weeks post-vector injection. At later time points, spontaneous partial recovery was observed in all rats, but no further improvement was found in dox-treated animals. TH levels were significantly increased in dox-treated rats at all time points. By contrast, striatal dopamine and S40-TH were increased at 4 weeks, but not 14 weeks, and AADC remained unchanged. Dox withdrawal after 7 weeks, resulted in TH levels comparable to the controls at 14 weeks. Conclusions Delayed GDNF gene delivery only transiently improved dopaminergic function. Over the long term, TH was more abundant, but not functional, and the increase was lost when GDNF gene expression was switched off. Copyright © 2009 John Wiley & Sons, Ltd.
Efficient protection of dopaminergic neurons against a subsequent 6-hydroxydopamine lesion by glial cell line-derived neurotrophic factor (GDNF) gene delivery has been demonstrated. By contrast, the neurorestorative effects of GDNF administered several weeks after the toxin have been less characterized. In particular, whether these were permanent or dependent on the continuous presence of GDNF remains elusive.BACKGROUNDEfficient protection of dopaminergic neurons against a subsequent 6-hydroxydopamine lesion by glial cell line-derived neurotrophic factor (GDNF) gene delivery has been demonstrated. By contrast, the neurorestorative effects of GDNF administered several weeks after the toxin have been less characterized. In particular, whether these were permanent or dependent on the continuous presence of GDNF remains elusive.A tetracycline-inducible adeno-associated virus (AAV)-1 vector expressing human GDNF cDNA was administered unilaterally in the rat striatum 5 weeks after 6-hydroxydopamine. Rats were treated with doxycycline (dox) or untreated from the day of vector injection until sacrifice (4 or 14 weeks). A sub-group was dox-treated for 7 weeks then untreated until 14 weeks. The motor behavior was assessed by amphetamine-induced rotations and spontaneous forelimb asymmetry. The amounts of tyrosine hydroxylase (TH), serine-40-phosphorylated TH (S40-TH) and aromatic amino acid decarboxylase (AADC) proteins were compared by western blotting and the dopamine levels quantified by high-performance liquid chromatography.METHODSA tetracycline-inducible adeno-associated virus (AAV)-1 vector expressing human GDNF cDNA was administered unilaterally in the rat striatum 5 weeks after 6-hydroxydopamine. Rats were treated with doxycycline (dox) or untreated from the day of vector injection until sacrifice (4 or 14 weeks). A sub-group was dox-treated for 7 weeks then untreated until 14 weeks. The motor behavior was assessed by amphetamine-induced rotations and spontaneous forelimb asymmetry. The amounts of tyrosine hydroxylase (TH), serine-40-phosphorylated TH (S40-TH) and aromatic amino acid decarboxylase (AADC) proteins were compared by western blotting and the dopamine levels quantified by high-performance liquid chromatography.Dox-dependent behavioral improvements were demonstrated 4 weeks post-vector injection. At later time points, spontaneous partial recovery was observed in all rats, but no further improvement was found in dox-treated animals. TH levels were significantly increased in dox-treated rats at all time points. By contrast, striatal dopamine and S40-TH were increased at 4 weeks, but not 14 weeks, and AADC remained unchanged. Dox withdrawal after 7 weeks, resulted in TH levels comparable to the controls at 14 weeks.RESULTSDox-dependent behavioral improvements were demonstrated 4 weeks post-vector injection. At later time points, spontaneous partial recovery was observed in all rats, but no further improvement was found in dox-treated animals. TH levels were significantly increased in dox-treated rats at all time points. By contrast, striatal dopamine and S40-TH were increased at 4 weeks, but not 14 weeks, and AADC remained unchanged. Dox withdrawal after 7 weeks, resulted in TH levels comparable to the controls at 14 weeks.Delayed GDNF gene delivery only transiently improved dopaminergic function. Over the long term, TH was more abundant, but not functional, and the increase was lost when GDNF gene expression was switched off.CONCLUSIONSDelayed GDNF gene delivery only transiently improved dopaminergic function. Over the long term, TH was more abundant, but not functional, and the increase was lost when GDNF gene expression was switched off.
Background Efficient protection of dopaminergic neurons against a subsequent 6‐hydroxydopamine lesion by glial cell line‐derived neurotrophic factor (GDNF) gene delivery has been demonstrated. By contrast, the neurorestorative effects of GDNF administered several weeks after the toxin have been less characterized. In particular, whether these were permanent or dependent on the continuous presence of GDNF remains elusive. Methods A tetracycline‐inducible adeno‐associated virus (AAV)‐1 vector expressing human GDNF cDNA was administered unilaterally in the rat striatum 5 weeks after 6‐hydroxydopamine. Rats were treated with doxycycline (dox) or untreated from the day of vector injection until sacrifice (4 or 14 weeks). A sub‐group was dox‐treated for 7 weeks then untreated until 14 weeks. The motor behavior was assessed by amphetamine‐induced rotations and spontaneous forelimb asymmetry. The amounts of tyrosine hydroxylase (TH), serine‐40‐phosphorylated TH (S40‐TH) and aromatic amino acid decarboxylase (AADC) proteins were compared by western blotting and the dopamine levels quantified by high‐performance liquid chromatography. Results Dox‐dependent behavioral improvements were demonstrated 4 weeks post‐vector injection. At later time points, spontaneous partial recovery was observed in all rats, but no further improvement was found in dox‐treated animals. TH levels were significantly increased in dox‐treated rats at all time points. By contrast, striatal dopamine and S40‐TH were increased at 4 weeks, but not 14 weeks, and AADC remained unchanged. Dox withdrawal after 7 weeks, resulted in TH levels comparable to the controls at 14 weeks. Conclusions Delayed GDNF gene delivery only transiently improved dopaminergic function. Over the long term, TH was more abundant, but not functional, and the increase was lost when GDNF gene expression was switched off. Copyright © 2009 John Wiley & Sons, Ltd.
Background Efficient protection of dopaminergic neurons against a subsequent 6-hydroxydopamine lesion by glial cell line-derived neurotrophic factor (GDNF) gene delivery has been demonstrated. By contrast, the neurorestorative effects of GDNF administered several weeks after the toxin have been less characterized. In particular, whether these were permanent or dependent on the continuous presence of GDNF remains elusive. Methods A tetracycline-inducible adeno-associated virus (AAV)-1 vector expressing human GDNF cDNA was administered unilaterally in the rat striatum 5 weeks after 6-hydroxydopamine. Rats were treated with doxycycline (dox) or untreated from the day of vector injection until sacrifice (4 or 14 weeks). A sub-group was dox-treated for 7 weeks then untreated until 14 weeks. The motor behavior was assessed by amphetamine-induced rotations and spontaneous forelimb asymmetry. The amounts of tyrosine hydroxylase (TH), serine-40-phosphorylated TH (S40-TH) and aromatic amino acid decarboxylase (AADC) proteins were compared by western blotting and the dopamine levels quantified by high-performance liquid chromatography. Results Dox-dependent behavioral improvements were demonstrated 4 weeks post-vector injection. At later time points, spontaneous partial recovery was observed in all rats, but no further improvement was found in dox-treated animals. TH levels were significantly increased in dox-treated rats at all time points. By contrast, striatal dopamine and S40-TH were increased at 4 weeks, but not 14 weeks, and AADC remained unchanged. Dox withdrawal after 7 weeks, resulted in TH levels comparable to the controls at 14 weeks. Conclusions Delayed GDNF gene delivery only transiently improved dopaminergic function. Over the long term, TH was more abundant, but not functional, and the increase was lost when GDNF gene expression was switched off.
Efficient protection of dopaminergic neurons against a subsequent 6-hydroxydopamine lesion by glial cell line-derived neurotrophic factor (GDNF) gene delivery has been demonstrated. By contrast, the neurorestorative effects of GDNF administered several weeks after the toxin have been less characterized. In particular, whether these were permanent or dependent on the continuous presence of GDNF remains elusive. A tetracycline-inducible adeno-associated virus (AAV)-1 vector expressing human GDNF cDNA was administered unilaterally in the rat striatum 5 weeks after 6-hydroxydopamine. Rats were treated with doxycycline (dox) or untreated from the day of vector injection until sacrifice (4 or 14 weeks). A sub-group was dox-treated for 7 weeks then untreated until 14 weeks. The motor behavior was assessed by amphetamine-induced rotations and spontaneous forelimb asymmetry. The amounts of tyrosine hydroxylase (TH), serine-40-phosphorylated TH (S40-TH) and aromatic amino acid decarboxylase (AADC) proteins were compared by western blotting and the dopamine levels quantified by high-performance liquid chromatography. Dox-dependent behavioral improvements were demonstrated 4 weeks post-vector injection. At later time points, spontaneous partial recovery was observed in all rats, but no further improvement was found in dox-treated animals. TH levels were significantly increased in dox-treated rats at all time points. By contrast, striatal dopamine and S40-TH were increased at 4 weeks, but not 14 weeks, and AADC remained unchanged. Dox withdrawal after 7 weeks, resulted in TH levels comparable to the controls at 14 weeks. Delayed GDNF gene delivery only transiently improved dopaminergic function. Over the long term, TH was more abundant, but not functional, and the increase was lost when GDNF gene expression was switched off.
Author Yang, Xin
Bockstael, Olivier
Brotchi, Jacques
Vercammen, Linda
Baekelandt, Veerle
Lehtonen, Enni
Chtarto, Abdelwahed
Levivier, Marc
Mertens, Birgit
Michotte, Yvette
Sarre, Sophie
Tenenbaum, Liliane
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  givenname: Liliane
  surname: Tenenbaum
  fullname: Tenenbaum, Liliane
  email: litenenb@ulb.ac.be
  organization: Laboratory of Experimental Neurosurgery, Université Libre de Bruxelles, Brussels, Belgium
BackLink https://www.ncbi.nlm.nih.gov/pubmed/19639608$$D View this record in MEDLINE/PubMed
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Bilang-Bleuel A, Revah F, Colin P, et al. Intrastriatal injection of an adenoviral vector expressing glial-cell-line-derived neurotrophic factor prevents dopaminergic neuron degeneration and behavioral impairment in a rat model of Parkinson disease. Proc Natl Acad Sci USA 1997; 94: 8818-8823.
Sajadi A, Bensadoun JC, Schneider BL, Lo BC, Aebischer P. 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.
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.
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Marks WJ, Jr., Ostrem JL, Verhagen L, et al. Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson's disease: an open-label, phase I trial. Lancet Neurol 2008; 7: 400-408.
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Sauer H, Oertel WH. 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.
Eslamboli A, Cummings RM, Ridley RM, et al. Recombinant adeno-associated viral vector (rAAV) delivery of GDNF provides protection against 6-OHDA lesion in the common marmoset monkey (Callithrix jacchus). Exp Neurol 2003; 184: 536-548.
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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.
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Paratcha G, Ledda F, Ibanez CF. The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 2003; 113: 867-879.
Mandel RJ, Spratt SK, Snyder RO, Leff SE. Midbrain injection of recombinant adeno-associated virus encoding rat glial cell line-derived neurotrophic factor protects nigral neurons in a progressive 6-hydroxydopamine-induced degeneration model of Parkinson's disease in rats. Proc Natl Acad Sci USA 1997; 94: 14083-14088.
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Beck KD, Irwin I, Valverde J, et al. GDNF induces a dystonia-like state in neonatal rats and stimulates dopamine and serotonin synthesis. Neuron 1996; 16: 665-673.
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– reference: Bjorklund A, Kirik D, Rosenblad C, et al. Towards a neuroprotective gene therapy for Parkinson's disease: use of adenovirus, AAV and lentivirus vectors for gene transfer of GDNF to the nigrostriatal system in the rat Parkinson model. Brain Res 2000; 886: 82-98.
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Snippet Background Efficient protection of dopaminergic neurons against a subsequent 6‐hydroxydopamine lesion by glial cell line‐derived neurotrophic factor (GDNF)...
Efficient protection of dopaminergic neurons against a subsequent 6-hydroxydopamine lesion by glial cell line-derived neurotrophic factor (GDNF) gene delivery...
Background Efficient protection of dopaminergic neurons against a subsequent 6-hydroxydopamine lesion by glial cell line-derived neurotrophic factor (GDNF)...
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SubjectTerms 6-hydroxydopamine
adeno-associated viral vector
Adeno-associated virus
Adrenergic Agents - administration & dosage
Adrenergic Agents - adverse effects
Animals
Dependovirus - genetics
Dopamine - analysis
Dopamine - biosynthesis
Doxycycline - administration & dosage
Female
Gene Expression - drug effects
Gene therapy
Gene Transfer Techniques
Genetic Vectors - administration & dosage
Genetic Vectors - genetics
Genetic Vectors - metabolism
glial cell line-derived neurotrophic factor
Glial Cell Line-Derived Neurotrophic Factor - administration & dosage
Glial Cell Line-Derived Neurotrophic Factor - biosynthesis
Glial Cell Line-Derived Neurotrophic Factor - genetics
Humans
Motor Activity - drug effects
Oxidopamine - administration & dosage
Oxidopamine - adverse effects
Parkinson Disease, Secondary - chemically induced
Parkinson Disease, Secondary - metabolism
Parkinson Disease, Secondary - therapy
Parkinson's disease
phosphorylation
Rats
tetracycline-inducible
Time Factors
Tyrosine 3-Monooxygenase - analysis
Tyrosine 3-Monooxygenase - biosynthesis
tyrosine hydroxylase
Title Reversible neurochemical changes mediated by delayed intrastriatal glial cell line-derived neurotrophic factor gene delivery in a partial Parkinson's disease rat model
URI https://api.istex.fr/ark:/67375/WNG-SK30C7VQ-8/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fjgm.1377
https://www.ncbi.nlm.nih.gov/pubmed/19639608
https://www.proquest.com/docview/1757699822
https://www.proquest.com/docview/734064327
https://www.proquest.com/docview/883029191
Volume 11
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