Rgs6 is Required for Adult Maintenance of Dopaminergic Neurons in the Ventral Substantia Nigra
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{"title"=>"Rgs6 is Required for Adult Maintenance of Dopaminergic Neurons in the Ventral Substantia Nigra", "type"=>"journal", "authors"=>[{"first_name"=>"Panojot", "last_name"=>"Bifsha", "scopus_author_id"=>"15847998400"}, {"first_name"=>"Jianqi", "last_name"=>"Yang", "scopus_author_id"=>"25623905900"}, {"first_name"=>"Rory A.", "last_name"=>"Fisher", "scopus_author_id"=>"7403555912"}, {"first_name"=>"Jacques", "last_name"=>"Drouin", "scopus_author_id"=>"7103137042"}], "year"=>2014, "source"=>"PLoS Genetics", "identifiers"=>{"issn"=>"15537404", "pui"=>"601033600", "doi"=>"10.1371/journal.pgen.1004863", "sgr"=>"84919682713", "scopus"=>"2-s2.0-84919682713", "pmid"=>"25501001"}, "id"=>"d764756c-1035-375d-afda-af55b3c953f6", "abstract"=>"Parkinson disease (PD) is characterized by the preferential, but poorly understood, vulnerability to degeneration of midbrain dopaminergic (mDA) neurons in the ventral substantia nigra compacta (vSNc). These sensitive mDA neurons express Pitx3, a transcription factor that is critical for their survival during development. We used this dependence to identify, by flow cytometry and expression profiling, the negative regulator of G-protein signaling Rgs6 for its restricted expression in these neurons. In contrast to Pitx3-/- mDA neurons that die during fetal (vSNc) or post-natal (VTA) period, the vSNc mDA neurons of Rgs6-/- mutant mice begin to exhibit unilateral signs of degeneration at around 6 months of age, and by one year cell loss is observed in a fraction of mice. Unilateral cell loss is accompanied by contralateral degenerating neurons that exhibit smaller cell size, altered morphology and reduced dendritic network. The degenerating neurons have low levels of tyrosine hydroxylase (TH) and decreased nuclear Pitx3; accordingly, expression of many Pitx3 target gene products is altered, including Vmat2, Bdnf, Aldh1a1 (Adh2) and Fgf10. These low TH neurons also express markers of increased dopamine signaling, namely increased DAT and phospho-Erk1/2 expression. The late onset degeneration may reflect the protective action of Rgs6 against excessive DA signaling throughout life. Rgs6-dependent protection is thus critical for adult survival and maintenance of the vSNc mDA neurons that are most affected in PD.", "link"=>"http://www.mendeley.com/research/rgs6-required-adult-maintenance-dopaminergic-neurons-ventral-substantia-nigra", "reader_count"=>31, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>2, "Other"=>3, "Student > Master"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>2, "Other"=>3, "Student > Master"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>20, "Medicine and Dentistry"=>1, "Neuroscience"=>5, "Psychology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>5}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United Kingdom"=>2, "South Africa"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1840585"], "description"=>"<p>(A) Differentially expressed probesets were clustered in an unbiased manner into three-dimensional Cartesian-type coordinates defined according to the relative enrichment attributes for each probeset in the comparisons between SNc WT/VTA WT, SNc KO/SNc WT and VTA KO/VTA WT. Each cluster was named according to the observed preferential expression pattern (label and shown in red in diagrams). The heatmaps show relative enrichments for 20 genes that are highly enriched and/or that have documented functions (the complete gene lists for each subset is provided in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004863#pgen.1004863.s005\" target=\"_blank\">Table S1</a>). The total number of genes (not probesets) in each cluster is indicated together with the number of those that are either activated or repressed by Pitx3 based on the VTA KO/WT comparison. (B) qRT-PCR quantification of mRNAs with preferential expression in either SN or VTA assessed in FACS-sorted cells from <i>WT</i> or <i>Pitx3</i><sup>−/−</sup> (KO) tissues. mRNA levels are normalized relative to Gapdh mRNA. Data are shown as means ± S.D.</p>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268664, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004863.g002", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Subset_specific_expression_signatures_of_mDA_neurons_/1268664", "title"=>"Subset-specific expression signatures of mDA neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-11 03:18:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1840603"], "description"=>"<p>(A) Rgs6 expression revealed by immunohistofluorescence (red) together with TH (green) in mDA neurons of SNc but not VTA. Scale bar 410 µm. (B) Co-immunofluorescence analysis of TH (green) and Rgs6 or Pitx3 (red, as indicated) in SNc and VTA of adult mice. Arrowheads point to Pitx3-negative or Rgs6-negative mDA neurons in dorsal SNc. Scale bar 100 µm. (C) Triple immunofluorescence staining for TH (green), Pitx3 (red) and Calb1 (blue) on tissue sections of adult mice indicates that the majority of TH+Pitx3− cells of dSNc (arrowheads) are positive for Calb1, while TH+Pitx3+ cells of vSNc are negative for Calb1, consistent with depiction in A. Scale bar 100 µm.</p>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268680, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004863.g003", "stats"=>{"downloads"=>4, "page_views"=>32, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Restricted_expression_of_Rgs6_in_Pitx3_positive_Pitx3_dopaminergic_neurons_of_ventral_SNc_/1268680", "title"=>"Restricted expression of Rgs6 in Pitx3-positive (Pitx3+) dopaminergic neurons of ventral SNc.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-11 03:18:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1840754"], "description"=>"<p>(A) Immunohistofluorescence staining for TH and Drd2 in coronal sections of 1 y-old Rgs6<sup>−/−</sup> mice and WT controls. mDA neurons of vSNc express higher levels of glycosylated dopamine receptor D2 (Drd2) than those of dSNc (arrowheads). Scale bar 50 µm. (B) Phospho-Erk1/2 (red) staining is only present in degenerating vSNc TH<sup>low</sup> (green) neurons of <i>Rgs6<sup>−/−</sup></i> mice and not in <i>WT</i> controls. Scale bar 20 µm. Arrowheads indicate unaffected neurons. (C) DAT (red) staining is stronger in degenerating vSNc TH<sup>low</sup> (green) neurons of <i>Rgs6<sup>−/−</sup></i> mice than in <i>WT</i> controls. Scale bar 20 µm.</p>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268739, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004863.g008", "stats"=>{"downloads"=>7, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Drd2_related_changes_of_gene_expression_in_degenerating_neurons_of_vSNc_/1268739", "title"=>"Drd2-related changes of gene expression in degenerating neurons of vSNc.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-11 03:18:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1840643"], "description"=>"<p>(A) Immunoperoxidase staining for TH on representative coronal midbrain sections showing dysmorphic TH+ neurons (low TH staining, TH<sup>low</sup>, inset) in ventral SNc of <i>Rgs6</i><sup>−/−</sup> mice. The dSNc and VTA mDA neurons are unaffected (strong/normal TH staining, inset). Scale bar 200 µm. (B) Triple staining for TH (red), Dapi (blue) and Fluoro-Jade C (FJC, green) showing presence of degenerating TH<sup>low</sup> cells in vSNc of 1 y-old <i>Rgs6</i><sup>−/−</sup> mice (middle panels) and not in control vSNc (upper panels) or in dorsal SNc (lower panels). Scale bar 20 µm. (C) Bilateral cell counts of FJC<sup>+</sup> mDA neurons in SNc and VTA of coronal sections from control and 1 y-old <i>Rgs6</i><sup>−/−</sup> mice. (D) Co-immunostaining for TH (green) and LC3B (red) in vSNc of <i>WT</i> and <i>Rgs6</i><sup>−/−</sup> mice. Scale bar 20 µm. Arrowheads indicate unaffected neurons while arrows point to TH<sup>low</sup> cells. (E) Co-immunostaining for TH (green) and phosphorylated p27<sup>Kip1</sup> (phospho-p27, red) in vSNc of <i>WT</i> and <i>Rgs6</i><sup>−/−</sup> mice. Scale bar 20 µm.</p>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268696, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004863.g005", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Unilateral_degeneration_of_vSNc_neurons_in_a_subset_of_Rgs6_8722_8722_mice_/1268696", "title"=>"Unilateral degeneration of vSNc neurons in a subset of <i>Rgs6−/−</i> mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-11 03:18:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1840572"], "description"=>"<p>Dissected SN and VTA from newborn <i>TH-EGFP</i> transgenic <i>Pitx3<sup>+/+</sup></i> and <i>Pitx3<sup>−/</sup></i><sup>−</sup> mice were used for FACS purification of catecholaminergic neurons. The EGFP<sup>+</sup> cells consists in various proportions (approximate % shown) of Pitx3+ (red), Pitx3− (white) and Pitx3del (yellow) mDA neurons, depending on the region dissected and mDA neuronal loss resulting from <i>Pitx3</i> inactivation. RNA from four cell preparations (SNc WT, VTA WT, SNc KO, VTA KO) were analyzed by hybridization in duplicates to Affymetrix Mouse Gene 1.0ST microarrays.</p>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268651, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004863.g001", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Strategy_for_isolation_of_FACS_purified_Pitx3_dependent_red_and_Pitx3_independent_white_mDA_neurons_for_expression_profiling_analysis_/1268651", "title"=>"Strategy for isolation of FACS-purified Pitx3-dependent (red) and Pitx3-independent (white) mDA neurons for expression profiling analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-11 03:18:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1840761"], "description"=>"<p>(A) Rgs6-dependent signaling pathways in vSNc mDA neurons control Pitx3 expression, which itself controls expression of Aldh1a1, TH, Fgf10, Vmat2 and Bdnf. Together, Rgs6 and Pitx3 define a survival pathway in these neurons. The dopamine receptor Drd2 may be a target of Rgs6 action and consistent with this hypothesis, expression of the dopamine transporter DAT is up-regulated in <i>Rgs6<sup>−/−</sup></i> vSNc. (B) Schematic representation of major subsets of SNc mDA neurons present at different ages in midbrains of <i>Rgs6</i><sup>−/−</sup> mice showing progressive degeneration (small pale green) followed by loss of vSNc mDA neurons.</p>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268746, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004863.g009", "stats"=>{"downloads"=>0, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rgs6_8722_8722_mice_as_a_model_for_Parkinsonian_neurodegeneration_/1268746", "title"=>"<i>Rgs6−/−</i> mice as a model for Parkinsonian neurodegeneration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-11 03:18:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1840726"], "description"=>"<p>(A) Double immunofluorescence staining against TH (green) and Pitx3 (red) in SNc of control and 1 y-old <i>Rgs6</i><sup>−/−</sup> mice that display dysmorphic mDA neurons. Arrowheads indicate Pitx3-negative neurons of dSNc. Scale bar 20 µm. (B) Co-immunofluorescence staining against TH (green), nuclear Dapi (blue) and Vmat2 (red) in SNc of <i>WT</i> and <i>Rgs6</i><sup>−/−</sup> mice. Scale bar 20 µm. (C) Co-immunofluorescence staining against TH (green), nuclear Dapi (blue) and Bdnf (red) in SNc and VTA of <i>WT</i> and <i>Rgs6</i><sup>−/−</sup> mice. Scale bar 20 µm. (D) Double immunofluorescence staining against TH (green) and Pitx3, Aldh1a1, Fgf10 (red) in control and 1 y-old <i>Rgs6</i><sup>−/−</sup> mice that display dysmorphic mDA neurons. Arrowheads indicate unaffected dSNc neurons and arrows point to affected vSNc neurons. Scale bar 100 µm.</p>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268728, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004863.g007", "stats"=>{"downloads"=>4, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reduced_expression_of_Pitx3_and_its_target_genes_in_degenerating_neurons_/1268728", "title"=>"Reduced expression of Pitx3 and its target genes in degenerating neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-11 03:18:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1840797", "https://ndownloader.figshare.com/files/1840798", "https://ndownloader.figshare.com/files/1840799", "https://ndownloader.figshare.com/files/1840800", "https://ndownloader.figshare.com/files/1840801", "https://ndownloader.figshare.com/files/1840802", "https://ndownloader.figshare.com/files/1840803"], "description"=>"<div><p>Parkinson disease (PD) is characterized by the preferential, but poorly understood, vulnerability to degeneration of midbrain dopaminergic (mDA) neurons in the ventral substantia nigra compacta (vSNc). These sensitive mDA neurons express Pitx3, a transcription factor that is critical for their survival during development. We used this dependence to identify, by flow cytometry and expression profiling, the negative regulator of G-protein signaling Rgs6 for its restricted expression in these neurons. In contrast to <i>Pitx3<sup>−/−</sup></i> mDA neurons that die during fetal (vSNc) or post-natal (VTA) period, the vSNc mDA neurons of <i>Rgs6</i><sup>−/−</sup> mutant mice begin to exhibit unilateral signs of degeneration at around 6 months of age, and by one year cell loss is observed in a fraction of mice. Unilateral cell loss is accompanied by contralateral degenerating neurons that exhibit smaller cell size, altered morphology and reduced dendritic network. The degenerating neurons have low levels of tyrosine hydroxylase (TH) and decreased nuclear Pitx3; accordingly, expression of many Pitx3 target gene products is altered, including Vmat2, Bdnf, Aldh1a1 (Adh2) and Fgf10. These low TH neurons also express markers of increased dopamine signaling, namely increased DAT and phospho-Erk1/2 expression. The late onset degeneration may reflect the protective action of Rgs6 against excessive DA signaling throughout life. Rgs6-dependent protection is thus critical for adult survival and maintenance of the vSNc mDA neurons that are most affected in PD.</p></div>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268772, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004863.s001", "https://dx.doi.org/10.1371/journal.pgen.1004863.s002", "https://dx.doi.org/10.1371/journal.pgen.1004863.s003", "https://dx.doi.org/10.1371/journal.pgen.1004863.s004", "https://dx.doi.org/10.1371/journal.pgen.1004863.s005", "https://dx.doi.org/10.1371/journal.pgen.1004863.s006", "https://dx.doi.org/10.1371/journal.pgen.1004863.s007"], "stats"=>{"downloads"=>6, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rgs6_is_Required_for_Adult_Maintenance_of_Dopaminergic_Neurons_in_the_Ventral_Substantia_Nigra/1268772", "title"=>"<i>Rgs6</i> is Required for Adult Maintenance of Dopaminergic Neurons in the Ventral Substantia Nigra", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-12-11 03:18:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1840692"], "description"=>"<p>Double immunofluorescence staining against TH (green) and (A) DJ-1 (red) or (B) Pink1 (red) or (C) Lrrk2 (red) in SNc of control and 1 y-old <i>Rgs6</i><sup>−/−</sup> mice that display dysmorphic TH<sup>low</sup> mDA neurons. Arrowheads indicate unaffected neurons while arrows point to TH<sup>low</sup> cells. Scale bar 20 µm.</p>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268705, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004863.g006", "stats"=>{"downloads"=>2, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_familial_PD_genes_is_altered_in_degenerating_neurons_of_vSNc_/1268705", "title"=>"Expression of familial PD genes is altered in degenerating neurons of vSNc.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-11 03:18:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1840613"], "description"=>"<p>(A) Immunoperoxidase staining for TH on representative coronal midbrain sections showing less SNc TH+ neurons on one side of <i>Rgs6</i><sup>−/−</sup> mice at 1 year of age compared to sib control. Sections are identified with Bregma position. Scale bar 400 µm. (B) Number of TH+ cells in SNc and VTA of TH-stained coronal sections across midbrain (every 30 µm). Cell counts are represented as means +/− S.D. (***p<0.005). (C) Nissl staining of vSNc sections contiguous to A shows fewer cell bodies and abnormal elongated neurons in <i>Rgs6</i><sup>−/−</sup> mice compared to control. Scale bar 100 µm. (D) Double immunofluorescence staining for TH (green) and Pitx3 (red) on sections contiguous to A showing a marked loss of TH+Pitx3+ cells in <i>Rgs6<sup>−/−</sup></i> mice. Scale bar 100 µm.</p>", "links"=>[], "tags"=>["year cell loss", "Rgs 6", "pd", "expression", "vta", "Unilateral cell loss", "Ventral Substantia Nigra Parkinson disease", "contralateral degenerating neurons", "vSNc mDA neurons", "dat", "th", "ventral substantia nigra compacta", "Pitx 3 target gene products"], "article_id"=>1268690, "categories"=>["Biological Sciences"], "users"=>["Panojot Bifsha", "Jianqi Yang", "Rory A. Fisher", "Jacques Drouin"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004863.g004", "stats"=>{"downloads"=>2, "page_views"=>77, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Unilateral_loss_of_Pitx3_positive_dopaminergic_neurons_in_ventral_SNc_of_Rgs6_8722_8722_mice_/1268690", "title"=>"Unilateral loss of Pitx3-positive dopaminergic neurons in ventral SNc of <i>Rgs6</i><sup>−/−</sup> mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-11 03:18:45"}

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