Reduction of Protein Translation and Activation of Autophagy Protect against PINK1 Pathogenesis in Drosophila melanogaster
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{"title"=>"Reduction of protein translation and activation of autophagy protect against PINK1 pathogenesis in drosophila melanogaster", "type"=>"journal", "authors"=>[{"first_name"=>"Song", "last_name"=>"Liu", "scopus_author_id"=>"55164375500"}, {"first_name"=>"Bingwei", "last_name"=>"Lu", "scopus_author_id"=>"34771714700"}], "year"=>2010, "source"=>"PLoS Genetics", "identifiers"=>{"isbn"=>"15537390 (ISSN)", "pmid"=>"21151574", "doi"=>"10.1371/journal.pgen.1001237", "pui"=>"361011552", "issn"=>"15537390", "sgr"=>"78650694150", "scopus"=>"2-s2.0-78650694150"}, "id"=>"6c9b353b-9c82-3629-805d-0e97353a1194", "abstract"=>"Mutations in PINK1 and Parkin cause familial, early onset Parkinson's disease. In Drosophila melanogaster, PINK1 and Parkin mutants show similar phenotypes, such as swollen and dysfunctional mitochondria, muscle degeneration, energy depletion, and dopaminergic (DA) neuron loss. We previously showed that PINK1 and Parkin genetically interact with the mitochondrial fusion/fission pathway, and PINK1 and Parkin were recently proposed to form a mitochondrial quality control system that involves mitophagy. However, the in vivo relationships among PINK1/Parkin function, mitochondrial fission/fusion, and autophagy remain unclear; and other cellular events critical for PINK1 pathogenesis remain to be identified. Here we show that PINK1 genetically interacted with the protein translation pathway. Enhanced translation through S6K activation significantly exacerbated PINK1 mutant phenotypes, whereas reduction of translation showed suppression. Induction of autophagy by Atg1 overexpression also rescued PINK1 mutant phenotypes, even in the presence of activated S6K. Downregulation of translation and activation of autophagy were already manifested in PINK1 mutant, suggesting that they represent compensatory cellular responses to mitochondrial dysfunction caused by PINK1 inactivation, presumably serving to conserve energy. Interestingly, the enhanced PINK1 mutant phenotype in the presence of activated S6K could be fully rescued by Parkin, apparently in an autophagy-independent manner. Our results reveal complex cellular responses to PINK1 inactivation and suggest novel therapeutic strategies through manipulation of the compensatory responses.", "link"=>"http://www.mendeley.com/research/reduction-protein-translation-activation-autophagy-protect-against-pink1-pathogenesis-drosophila-mel", "reader_count"=>81, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>5, "Researcher"=>27, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>4, "Student > Bachelor"=>2, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>5, "Researcher"=>27, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>4, "Student > Bachelor"=>2, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>59, "Medicine and Dentistry"=>10, "Neuroscience"=>3, "Design"=>1}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Neuroscience"=>{"Neuroscience"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>59}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>1, "Germany"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/814147"], "description"=>"<p>Overexpression of Atg1 in the muscle of <i>PINK1<sup>B9</sup></i> mutants rescued their abnormal wing posture (A), thoracic indentation (B), jump/flight activity (C) and muscle ATP level (D). Data are presented as mean ± s.e.m. Statistical significance was determined by Student's <i>t</i> test (*<i>P</i><0.001). (E) Atg1 overexpression did not completely rescue the mitochondrial aggregation phenotype in the muscle of <i>PINK1 RNAi</i> flies. mitoGFP was expressed in the muscle using <i>Mhc-Gal4</i> driver to visualize mitochondrial morphology by live imaging. Wild type flies showed mitochondria of relatively uniform sizes (bottom right), while <i>PINK1 RNAi</i> flies had bright mitochondrial aggregates. Only the co-expression of Marf RNAi or Parkin OE was able to efficiently rescue the mitochondrial aggregation phenotype in the <i>PINK1</i> RNAi background.</p>", "links"=>[], "tags"=>["atg1", "rescues", "mutant"], "article_id"=>484516, "categories"=>["Neuroscience"], "users"=>["Song Liu", "Bingwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001237.g005", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_of_Atg1_rescues_PINK1_mutant_phenotypes_/484516", "title"=>"Overexpression of Atg1 rescues <i>PINK1</i> mutant phenotypes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-09 01:15:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/814048"], "description"=>"<p>Overexpression of <i>RpS6</i> or <i>RpS9 RNAi</i> transgenes in <i>PINK1 RNAi</i> or <i>PINK1 RNAi/UAS-S6K-TE</i> flies efficiently rescued the abnormal wing posture (A), thoracic indentation (B), and energy depletion (D) phenotypes in 1-day-old flies and partially suppressed these phenotypes in 14-day-old flies. Data are presented as mean ± s.e.m. Statistical significance was determined by Student's <i>t</i> test (*<i>P</i><0.001). (C) <i>RpS6</i> or <i>RpS9</i> RNAi blocked increased mitochondrial aggregation in <i>PINK1 RNAi, UAS-S6K-TE</i> flies. The scale bar represents 5 µm. (E) Western blot analysis comparing the levels of dS6K and phosphorylated S6K (T398) in wild type, <i>Mhc-Gal4>PINK1 RNAi</i> and <i>PINK1<sup>B9</sup></i> mutant flies. The phosphorylation of S6K was significantly decreased in <i>PINK1 RNAi</i> or mutant flies.</p>", "links"=>[], "tags"=>["rnai", "blocks", "enhancing", "s6k-te"], "article_id"=>484420, "categories"=>["Neuroscience"], "users"=>["Song Liu", "Bingwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001237.g004", "stats"=>{"downloads"=>4, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RpS6_or_RpS9_RNAi_blocks_the_enhancing_effects_of_S6K_TE_in_PINK1_RNAi_background_/484420", "title"=>"<i>RpS6</i> or <i>RpS9</i> RNAi blocks the enhancing effects of S6K-TE in <i>PINK1 RNAi</i> background.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-09 01:13:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/813674"], "description"=>"<p>The flies of each indicated genotype were crossed to <i>Mhc-Gal4>PINK1 RNAi</i> flies (A) or <i>Mhc-Gal4</i> flies (B), and the percentage of male offspring with abnormal wing posture phenotype was scored at 1-day and 14-day after eclosion. The flies were aged at 29°C. Data are presented as mean ± s.e.m. The genetic interactions between <i>PINK1</i> and genes of the TOR pathway, autophagy pathway, mitochondrial fusion and fission machinery or antioxidant genes are demonstrated. The differences in abnormal wing posture phenotype between the genetic interaction flies and control flies shown in (A) are all statistically significant (<i>P</i><0.005 in Student's <i>t</i>-test).</p>", "links"=>[], "tags"=>["atg1", "modifiers"], "article_id"=>484047, "categories"=>["Neuroscience"], "users"=>["Song Liu", "Bingwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001237.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_S6K_and_Atg1_act_as_genetic_modifiers_of_PINK1_RNAi_/484047", "title"=>"S6K and Atg1 act as genetic modifiers of <i>PINK1</i> RNAi.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-09 01:07:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/813939"], "description"=>"<p>(A) Overexpression of constitutively active S6K increased the size of swollen or aggregated mitochondria in the DA neurons of <i>PINK1</i> mutants. Mitochondrially targeted GFP (mitoGFP) was expressed in the DA neurons using <i>TH-Gal4</i> driver <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1001237#pgen.1001237-FriggiGrelin1\" target=\"_blank\">[44]</a> to help visualize mitochondrial morphology. Brains of 7-day-old adult flies of the indicated genotypes were immunostained with anti-TH antibody (red) to label DA neuron and anti-GFP antibody (green) to label mitochondria. Images of DA neurons in the PPL1 cluster were shown. Overexpression of S6K-TE in <i>PINK1</i> mutant significantly increased the size of mitochondrial aggregates in DA neurons. The scale bar represents 5 µm. (B) Comparison of mitochondrial size distribution in <i>PINK1</i> mutants with or without S6K-TE overexpression. Statistical significance was determined by Student's <i>t</i> test (**<i>P</i><0.001, *<i>P</i><0.05). (C) Overexpression of constitutively active S6K increased DA neuron loss in the PPL1 cluster of <i>PINK1</i> mutant. DA neuron number was scored in flies aged for 14 days at 25°C. At least 7 flies were used for each genotype. Statistical significance was determined by Student's <i>t</i> test (<i>**P</i><0.001). Data are presented as mean ± s.e.m.</p>", "links"=>[], "tags"=>["s6k", "increases", "mitochondrial", "aggregation", "da", "neuron"], "article_id"=>484306, "categories"=>["Neuroscience"], "users"=>["Song Liu", "Bingwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001237.g003", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Constitutively_active_S6K_increases_mitochondrial_aggregation_and_DA_neuron_loss_in_PINK1_mutants_/484306", "title"=>"Constitutively active S6K increases mitochondrial aggregation and DA neuron loss in <i>PINK1</i> mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-09 01:11:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/814256"], "description"=>"<p>(A, B) The rescuing effect of Atg1 OE in <i>PINK1 RNAi</i> flies was not dependent on S6K inhibition. Atg1 OE, as well as Parkin OE or <i>Marf</i> RNAi, efficiently rescued the abnormal wing posture (A) and muscle energy depletion (B) in <i>PINK1 RNAi/S6K-TE</i> flies. In contrast, overexpression of 4E-BP and the antioxidant genes were not as effective. Data are presented as mean ± s.e.m. Statistical significance was determined by Student's <i>t</i> test (*<i>P</i><0.001). (C) Overexpression of Atg1 was sufficient to induce autophagy in fly muscle. <i>UAS-LC3-GFP</i> was expressed in the muscle of flies with the indicated genetic background, and the level of autophagy was determined by Western Blot using anti-GFP antibody. Overexpression of Atg1 significantly increased the level of LC3-II in the muscle, indicating increased autophagy. Increased autophagy was also observed in <i>PINK1 RNAi</i> and <i>PINK1</i> mutant flies. (* indicates a cross-reaction band).</p>", "links"=>[], "tags"=>["oe", "rescues", "rnai", "phenotype", "inducing"], "article_id"=>484630, "categories"=>["Neuroscience"], "users"=>["Song Liu", "Bingwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001237.g006", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Atg1_OE_rescues_PINK1_RNAi_phenotype_by_inducing_autophagy_/484630", "title"=>"Atg1 OE rescues <i>PINK1</i> RNAi phenotype by inducing autophagy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-09 01:17:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/814329"], "description"=>"<p>The rescuing effect of Atg1 OE on the abnormal wing posture (A) and muscle energy depletion (B) phenotypes could be blocked by the co-expression of <i>Atg18</i> RNAi, suggesting that Atg1 functions through inducing autophagy to rescue <i>PINK1</i> RNAi phenotype. In contrast, the rescue of <i>PINK1</i> RNAi phenotypes by Parkin OE or <i>Marf</i> RNAi were largely unaffected by the disruption of Atg1 or Atg18 through RNAi. The tests were carried out in both <i>PINK1<sup>B9</sup></i> mutant and <i>Mhc-Gal4>PINK1 RNAi/S6K-TE</i> backgrounds. Data are presented as mean ± s.e.m. Statistical significance was determined by Student's <i>t</i> test (**<i>P</i><0.001). (C) <i>Atg1</i> or <i>Atg18</i> RNAi did not abolish the rescuing effect of Parkin OE in DA neurons. mitoGFP was expressed in DA neurons using the <i>TH-Gal4</i> driver to visualize mitochondrial morphology. Overexpression of Parkin efficiently rescued the mitochondrial aggregation phenotype in <i>PINK1</i> mutant (top panel). Similar rescuing effect was observed when <i>Atg1</i> RNAi or <i>Atg18</i> RNAi was co-expressed with Parkin (middle and bottom panels). The scale bar represents 5 µm.</p>", "links"=>[], "tags"=>["rnai", "blocks", "rescuing", "atg1", "oe", "parkin"], "article_id"=>484696, "categories"=>["Neuroscience"], "users"=>["Song Liu", "Bingwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001237.g007", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Atg18_RNAi_blocks_the_rescuing_effect_of_Atg1_OE_but_not_that_of_Parkin_OE_or_Marf_RNAi_/484696", "title"=>"<i>Atg18</i> RNAi blocks the rescuing effect of Atg1 OE but not that of Parkin OE or <i>Marf</i> RNAi.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-09 01:18:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/813817"], "description"=>"<p>Overexpression of constitutively active S6Ks (S6K-TE, S6K-STDE and S6K-STDETE) in the muscle of <i>PINK1 RNAi</i> flies completely abolished their jump/flight ability (A), significantly decreased their muscle ATP level (B) and dramatically increased their thoracic indentation (C). In contrast, the overexpression of <i>S6K RNAi</i> transgene partially rescued these phenotypes in <i>PINK1 RNAi</i> flies. Open and closed bars represented data scored on Day 1 and Day 14 after eclosion, respectively. Data are presented as mean ± s.e.m. Significance was determined by Student's <i>t</i> test (*<i>P</i><0.005). (D) Representative image of thoracic indentation (indicated by the white arrowhead) of <i>Mhc-Gal4; PINK1 RNAi; S6K-TE</i> fly at 1-day old (bottom) compared to the normal thoracic phenotype of <i>Mhc-Gal4, PINK1 RNAi</i> fly of the same age (top). (E) Overexpression of constitutively active S6K in <i>PINK1 RNAi</i> flies dramatically increased muscle degeneration. Sections from resin-embedded thoraces of 1-day-old adult flies were either stained with toluidine blue to visualize overall muscle structure (top panel) or directly visualized using TEM for mitochondrial morphology (bottom panel). WT flies or flies expressing constitutively active S6K show normal muscle structure with healthy, electron-dense mitochondria. Flies expressing <i>PINK1 RNAi</i> transgene had small lesions in the muscle with dysfunctional mitochondria showing broken cristae. Co-expression of S6K-TE in <i>PINK1 RNAi</i> flies caused more severe degeneration of mitochondria and muscle fibers, generating large lesions in the muscle that were filled with resin during embedding and are readily recognizable (indicated by black arrows).</p>", "links"=>[], "tags"=>["knockdown", "s6k", "modifies", "rnai", "phenotypes"], "article_id"=>484185, "categories"=>["Neuroscience"], "users"=>["Song Liu", "Bingwei Lu"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001237.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_or_knockdown_of_S6K_strongly_modifies_PINK1_RNAi_phenotypes_in_the_muscle_/484185", "title"=>"Overexpression or knockdown of S6K strongly modifies <i>PINK1</i> RNAi phenotypes in the muscle.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-09 01:09:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/405683", "https://ndownloader.figshare.com/files/405688", "https://ndownloader.figshare.com/files/405706"], "description"=>"<div><p>Mutations in PINK1 and Parkin cause familial, early onset Parkinson's disease. In <em>Drosophila melanogaster</em>, <em>PINK1</em> and <em>Parkin</em> mutants show similar phenotypes, such as swollen and dysfunctional mitochondria, muscle degeneration, energy depletion, and dopaminergic (DA) neuron loss. We previously showed that PINK1 and Parkin genetically interact with the mitochondrial fusion/fission pathway, and PINK1 and Parkin were recently proposed to form a mitochondrial quality control system that involves mitophagy. However, the <em>in vivo</em> relationships among PINK1/Parkin function, mitochondrial fission/fusion, and autophagy remain unclear; and other cellular events critical for PINK1 pathogenesis remain to be identified. Here we show that PINK1 genetically interacted with the protein translation pathway. Enhanced translation through S6K activation significantly exacerbated <em>PINK1</em> mutant phenotypes, whereas reduction of translation showed suppression. Induction of autophagy by Atg1 overexpression also rescued <em>PINK1</em> mutant phenotypes, even in the presence of activated S6K. Downregulation of translation and activation of autophagy were already manifested in <em>PINK1</em> mutant, suggesting that they represent compensatory cellular responses to mitochondrial dysfunction caused by PINK1 inactivation, presumably serving to conserve energy. Interestingly, the enhanced <em>PINK1</em> mutant phenotype in the presence of activated S6K could be fully rescued by Parkin, apparently in an autophagy-independent manner. Our results reveal complex cellular responses to PINK1 inactivation and suggest novel therapeutic strategies through manipulation of the compensatory responses.</p></div>", "links"=>[], "tags"=>["activation", "autophagy", "pink1", "pathogenesis"], "article_id"=>140164, "categories"=>["Neuroscience"], "users"=>["Song Liu", "Bingwei Lu"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1001237.s001", "https://dx.doi.org/10.1371/journal.pgen.1001237.s002", "https://dx.doi.org/10.1371/journal.pgen.1001237.s003"], "stats"=>{"downloads"=>4, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Reduction_of_Protein_Translation_and_Activation_of_Autophagy_Protect_against_PINK1_Pathogenesis_in_Drosophila_melanogaster_/140164", "title"=>"Reduction of Protein Translation and Activation of Autophagy Protect against PINK1 Pathogenesis in <em>Drosophila melanogaster</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-12-09 00:02:44"}

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Relative Metric

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