Human A53T α-Synuclein Causes Reversible Deficits in Mitochondrial Function and Dynamics in Primary Mouse Cortical Neurons
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{"title"=>"Human A53T α-synuclein causes reversible deficits in mitochondrial function and dynamics in primary mouse cortical neurons", "type"=>"journal", "authors"=>[{"first_name"=>"Li", "last_name"=>"Li", "scopus_author_id"=>"55218828300"}, {"first_name"=>"Sashi", "last_name"=>"Nadanaciva", "scopus_author_id"=>"6601961075"}, {"first_name"=>"Zdenek", "last_name"=>"Berger", "scopus_author_id"=>"8940934800"}, {"first_name"=>"Wei", "last_name"=>"Shen", "scopus_author_id"=>"55809083900"}, {"first_name"=>"Katrina", "last_name"=>"Paumier", "scopus_author_id"=>"55394765100"}, {"first_name"=>"Joel", "last_name"=>"Schwartz", "scopus_author_id"=>"56828557900"}, {"first_name"=>"Kewa", "last_name"=>"Mou", "scopus_author_id"=>"6506835482"}, {"first_name"=>"Paula", "last_name"=>"Loos", "scopus_author_id"=>"55918506300"}, {"first_name"=>"Anthony J.", "last_name"=>"Milici", "scopus_author_id"=>"56028817600"}, {"first_name"=>"John", "last_name"=>"Dunlop", "scopus_author_id"=>"14055994300"}, {"first_name"=>"Warren D.", "last_name"=>"Hirst", "scopus_author_id"=>"7005120264"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84893521264", "pui"=>"372325326", "doi"=>"10.1371/journal.pone.0085815", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"84893521264", "pmid"=>"24392030"}, "id"=>"35b504e1-2085-3757-83e8-bc8ca881e019", "abstract"=>"Parkinson's disease (PD) is the second most common neurodegenerative disease. A key pathological feature of PD is Lewy bodies, of which the major protein component is α-synuclein (α-syn). Human genetic studies have shown that mutations (A53T, A30P, E46K) and multiplication of the α-syn gene are linked to familial PD. Mice overexpressing the human A53T mutant α-syn gene develop severe movement disorders. However, the molecular mechanisms of α-syn toxicity are not well understood. Recently, mitochondrial dysfunction has been linked with multiple neurodegenerative diseases including Parkinson's disease. Here we investigated whether mitochondrial motility, dynamics and respiratory function are affected in primary neurons from a mouse model expressing the human A53T mutation. We found that mitochondrial motility was selectively inhibited in A53T neurons while transport of other organelles was not affected. In addition, A53T expressing neurons showed impairment in mitochondrial membrane potential and mitochondrial respiratory function. Furthermore, we found that rapamycin, an autophagy inducer, rescued the decreased mitochondrial mobility. Taken together, these data demonstrate that A53T α-syn impairs mitochondrial function and dynamics and the deficit of mitochondrial transport is reversible, providing further understanding of the disease pathogenesis and a potential therapeutic strategy for PD.", "link"=>"http://www.mendeley.com/research/human-a53t-%CE%B1synuclein-causes-reversible-deficits-mitochondrial-function-dynamics-primary-mouse-corti", "reader_count"=>52, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>2, "Researcher"=>14, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>11, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>4, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>2, "Researcher"=>14, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>11, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>4, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>5, "Medicine and Dentistry"=>9, "Agricultural and Biological Sciences"=>17, "Neuroscience"=>14, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>9}, "Neuroscience"=>{"Neuroscience"=>14}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Luxembourg"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1334176"], "description"=>"<p><b>A</b>, Representative kymographs showing treatment of rapamycin (1μM) for 7-9hr increased mobility of mitochondria in A53T α-syn neurons (7DIV). Images were acquired at the interval of 12s for 20min. B, C, Rapamycin rescued mitochondrial transport in A53T neurons to the level seen in wild-type cultures. One representative experiment is shown and 58-130 mitochondria were tracked in each condition. Experiments were repeated 3 times and results were consistent across all experiments. <b>D</b>, Rapamycin also rescued mitochondrial length in A53T neurons (6-7DIV) to the level seen in wild-type cultures. The results were pooled from three experiments. Mean +/- SEM is shown and t test was used to compare velocity in different conditions. *p<0.05; **p<0.01; ***p<0.001; ns=non-significant. The error bars depict SEM. wt=wild type, A53T=A53T α-synuclein, μm=micrometers, s=seconds, min=minutes.</p>", "links"=>[], "tags"=>["rescued", "mitochondrial", "mobility", "a53t"], "article_id"=>890654, "categories"=>["Biological Sciences"], "users"=>["Li Li", "Sashi Nadanaciva", "Zdenek Berger", "Wei Shen", "Katrina Paumier", "Joel Schwartz", "Kewa Mou", "Paula Loos", "Anthony J. Milici", "John Dunlop", "Warren D. Hirst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085815.g006", "stats"=>{"downloads"=>2, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rapamycin_rescued_mitochondrial_mobility_in_A53T_945_syn_neurons_/890654", "title"=>"Rapamycin rescued mitochondrial mobility in A53T α-syn neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:00:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334173"], "description"=>"<p><b>A</b>, <b>B</b>, Examples of mitochondrial morphology in wt (<b>A</b>) and A53T (<b>B</b>) cortical neurons at 7DIV. Cortical neurons were transfected with DsRed-mito. Higher magnification images at the bottom were from the areas highlighted by red boxes at the top images. <b>C</b>, Quantification of mitochondrial shape parameters (circularity, roundness and aspect ratio) in wt and A53T neurons at 6-7DIV in one representative experiment. There was no significant change in A53 neurons vs. wt neurons. <b>D</b>, Summary of mitochondrial length and mitochondria width in wt and A53T neurons from one representative experiment. Data plotted as Mean +/- SEM. t-test was used (****p<0.0001). Experiments were repeated 3 times (see results in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085815#pone.0085815.s003\" target=\"_blank\">Figure S3</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085815#pone.0085815.s006\" target=\"_blank\">tables S1</a> & <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085815#pone.0085815.s007\" target=\"_blank\">S2</a>). Scale bar=20μm. wt=wild type, A53T=A53T α-synuclein, μm=micrometers, DIV=days <i>in </i><i>vitro</i>.</p>", "links"=>[], "tags"=>["affected", "a53t", "cortical", "neurons"], "article_id"=>890651, "categories"=>["Biological Sciences"], "users"=>["Li Li", "Sashi Nadanaciva", "Zdenek Berger", "Wei Shen", "Katrina Paumier", "Joel Schwartz", "Kewa Mou", "Paula Loos", "Anthony J. Milici", "John Dunlop", "Warren D. Hirst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085815.g003", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mitochondrial_shape_was_not_substantially_affected_in_A53T_cortical_neurons_but_the_length_was_shortened_/890651", "title"=>"Mitochondrial shape was not substantially affected in A53T cortical neurons but the length was shortened.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:00:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334172"], "description"=>"<p><b>A</b>, An A53T α-syn cortical neuron transfected with EGFP-LC3 (green) showing diffuse signal in the cytosol and puncta which are autophagosomes. Autophagosomes were visible at the soma (white arrowhead) and a neurite (white and red arrows). <b>B</b>, Montage of images (~1min) from a 5min confocal time-lapse of the neurite area (outlined by red box in A). Two autophagosomes (white and red arrows) moved retrogradely along the neurite. <b>C</b>,<b>D</b>, Representative kymographs of autophagosome mobility demonstrated that most of autophagosomes in wt and A53T neurons underwent active retrograde movement, however, one of them in the wt group (white arrowhead) paused at the end of the imaging period and another one (red arrows) moved anterogradely. <b>E</b>, Bar graphs demonstrating that the average (Avg.) velocity and the instantaneous (Ins.) velocity of autophagosome movement were not reduced in A53T neurons, however, they almost doubled in the mutant cortical neurons. Data were pooled from 3 independent experiments and 309 autophagosomes were included in the analysis. Data plotted as Mean +/- SEM. t test, **p<0.01; ***p<0.001. Scale bar=20μm. wt=wild type, A53T=A53T α-synuclein, μm=micrometers, s=seconds, min=minutes.</p>", "links"=>[], "tags"=>["velocity", "autophagosomes", "reduced", "a53t"], "article_id"=>890650, "categories"=>["Biological Sciences"], "users"=>["Li Li", "Sashi Nadanaciva", "Zdenek Berger", "Wei Shen", "Katrina Paumier", "Joel Schwartz", "Kewa Mou", "Paula Loos", "Anthony J. Milici", "John Dunlop", "Warren D. Hirst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085815.g002", "stats"=>{"downloads"=>2, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transport_velocity_of_autophagosomes_was_not_substantially_reduced_in_A53T_945_syn_neurons_/890650", "title"=>"Transport velocity of autophagosomes was not substantially reduced in A53T α-syn neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:00:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334175"], "description"=>"<p>Bioenergetic parameters of A53T and wt neurons were analyzed using a Seahorse XF96 analyzer as described in Materials and Methods. <b>A</b>, Basal OCR values were similar in wt and A53T neurons. <b>B</b>, A53T neurons had a lower OCR/ECAR ratio than wt both at 7DIV and at 13-14 DIV. <b>C</b>-<b>E</b>, A53T neurons had lower mitochondrial respiration, lower ATP linked respiration, higher non-mitochondrial respiration and lower maximum respiratory capacity than wt neurons at 7DIV (<b>C</b>,<b>D</b>) and at 13-14 DIV (<b>E</b>). Representative data from one experiment for neurons at 7DIV are shown as in C. Pooled data from 3 independent experiments for neurons at 7DIV are shown in D. As in <b>E</b>, pooled data from 3 independent experiments for neurons at 13-14 DIV are shown. Data plotted as Mean +/- SEM (t-test, *p<0.05; **p<0.01; ***p<0.001; ns=non-significant). wt=wild type, A53T=A53T α-synuclein, pMol=picomole, min=minutes, DIV=days <i>in </i><i>vitro</i>, OCR=oxygen consumption rates, ECAR=extracellular acidification rates.</p>", "links"=>[], "tags"=>["a53t", "impaired", "mitochondrial", "respiration", "respiratory"], "article_id"=>890653, "categories"=>["Biological Sciences"], "users"=>["Li Li", "Sashi Nadanaciva", "Zdenek Berger", "Wei Shen", "Katrina Paumier", "Joel Schwartz", "Kewa Mou", "Paula Loos", "Anthony J. Milici", "John Dunlop", "Warren D. Hirst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085815.g005", "stats"=>{"downloads"=>1, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_of_human_A53T_945_syn_impaired_mitochondrial_respiration_and_the_maximum_respiratory_capacity_/890653", "title"=>"Overexpression of human A53T α-syn impaired mitochondrial respiration and the maximum respiratory capacity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:00:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334174"], "description"=>"<p><b>A</b>, <b>B</b>, Representative images of mitochondria stained with MitoTracker Red. White arrows point to a few cell bodies and only the cytosol area was stained with MitoTracker red. Fluorescence intensity of MitoTracker Red was lower in A53T neurons compared to that in wt neurons. <b>C</b>, Bar graphs show a significant reduction in MitoTracker Red fluorescence intensity (normalized) in A53T neurons compared to wt neurons in 6-7 DIV and 11-14DIV. Since accumulation of MitoTracker Red is dependent on mitochondrial transmembrane potential, it suggests a loss of mitochondrial membrane potential in A53T neurons. Data plotted as Mean +/- SEM. Data were pooled from 3 independent experiments and > 150 neurons were measured in each condition (t-test, ***p<0.001). Scale bar=20μm. wt=wild type, A53T=A53T α-synuclein, DIV=days <i>in </i><i>vitro</i>.</p>", "links"=>[], "tags"=>["induced", "mitochondrial", "membrane"], "article_id"=>890652, "categories"=>["Biological Sciences"], "users"=>["Li Li", "Sashi Nadanaciva", "Zdenek Berger", "Wei Shen", "Katrina Paumier", "Joel Schwartz", "Kewa Mou", "Paula Loos", "Anthony J. Milici", "John Dunlop", "Warren D. Hirst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085815.g004", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A53T_945_syn_induced_loss_of_mitochondrial_membrane_potential_/890652", "title"=>"A53T α-syn induced loss of mitochondrial membrane potential.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:00:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334171"], "description"=>"<p><b>A</b>, An example of a cortical neuron from A53T mice transfected with dsRed-mito (red) and EGFP (green) at the time of plating. <b>B</b>, Montage of images (~7min) at the dsRed-mito channel from a 20min confocal time-lapse of the neurite area (outlined by white box in A). In the image area, the majority of mitochondria were stationary indicated by the blue and yellow arrows. Red arrows pointed to a mobile mitochondrion that entered the area at ~200s and moved along the axon. <b>C</b>, <b>D</b>, Kymographs constructed from five-pixel wide lines drawn through the extent of axons from wt or A53T neurons. Fluorescence intensities along kymograph lines are plotted horizontally for each frame of the 5min time-lapse with time interval of 3s (101 frames). Time is indicated on the y-axis and distance is indicated on the x-axis. In A53T neurons (<b>C</b>), most of mitochondria are stationary represented by the bright vertical lines. In wt neurons (<b>D</b>), there are diagonal lines representing moving mitochondria. <b>E</b>, <b>F</b>, Bar graphs from one representative experiment at 7DIV (<b>E</b>) and 14DIV (<b>F</b>) showing that mitochondria transport velocity was reduced significantly in A53T neurons. In each condition, 53-145 mitochondria were analyzed and ≥ 4 independent experiments showed consistent results. <b>G</b>, Percentage of mobile mitochondria significantly decreased in A53T (~8%) compared to that in wt neurons (>30%). Mobile mitochondria are defined as mitochondria that moved at ≥0.005 μm/s. H, Mitochondrial instantaneous velocity also reduced in A53T axons. Data plotted as Mean +/- SEM. t test, *p<0.05; **p<0.01; ****p<0.0001. Scale bar=20μm. wt=wild type, A53T=A53T α-synuclein, μm=micrometers, s=seconds, min=minutes, DIV=days <i>in </i><i>vitro</i>.</p>", "links"=>[], "tags"=>["reduced", "a53t"], "article_id"=>890649, "categories"=>["Biological Sciences"], "users"=>["Li Li", "Sashi Nadanaciva", "Zdenek Berger", "Wei Shen", "Katrina Paumier", "Joel Schwartz", "Kewa Mou", "Paula Loos", "Anthony J. Milici", "John Dunlop", "Warren D. Hirst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085815.g001", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mitochondrial_transport_was_reduced_in_A53T_945_syn_axons_/890649", "title"=>"Mitochondrial transport was reduced in A53T α-syn axons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:00:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334211", "https://ndownloader.figshare.com/files/1334212", "https://ndownloader.figshare.com/files/1334213", "https://ndownloader.figshare.com/files/1334214", "https://ndownloader.figshare.com/files/1334215", "https://ndownloader.figshare.com/files/1334216", "https://ndownloader.figshare.com/files/1334217", "https://ndownloader.figshare.com/files/1334218", "https://ndownloader.figshare.com/files/1334219", "https://ndownloader.figshare.com/files/1334220"], "description"=>"<div><p>Parkinson’s disease (PD) is the second most common neurodegenerative disease. A key pathological feature of PD is Lewy bodies, of which the major protein component is α-synuclein (α-syn). Human genetic studies have shown that mutations (A53T, A30P, E46K) and multiplication of the α-syn gene are linked to familial PD. Mice overexpressing the human A53T mutant α-syn gene develop severe movement disorders. However, the molecular mechanisms of α-syn toxicity are not well understood. Recently, mitochondrial dysfunction has been linked with multiple neurodegenerative diseases including Parkinson’s disease. Here we investigated whether mitochondrial motility, dynamics and respiratory function are affected in primary neurons from a mouse model expressing the human A53T mutation. We found that mitochondrial motility was selectively inhibited in A53T neurons while transport of other organelles was not affected. In addition, A53T expressing neurons showed impairment in mitochondrial membrane potential and mitochondrial respiratory function. Furthermore, we found that rapamycin, an autophagy inducer, rescued the decreased mitochondrial mobility. Taken together, these data demonstrate that A53T α-syn impairs mitochondrial function and dynamics and the deficit of mitochondrial transport is reversible, providing further understanding of the disease pathogenesis and a potential therapeutic strategy for PD.</p> </div>", "links"=>[], "tags"=>["a53t", "causes", "reversible", "deficits", "mitochondrial", "cortical"], "article_id"=>890675, "categories"=>["Biological Sciences"], "users"=>["Li Li", "Sashi Nadanaciva", "Zdenek Berger", "Wei Shen", "Katrina Paumier", "Joel Schwartz", "Kewa Mou", "Paula Loos", "Anthony J. Milici", "John Dunlop", "Warren D. Hirst"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0085815.s001", "https://dx.doi.org/10.1371/journal.pone.0085815.s002", "https://dx.doi.org/10.1371/journal.pone.0085815.s003", "https://dx.doi.org/10.1371/journal.pone.0085815.s004", "https://dx.doi.org/10.1371/journal.pone.0085815.s005", "https://dx.doi.org/10.1371/journal.pone.0085815.s006", "https://dx.doi.org/10.1371/journal.pone.0085815.s007", "https://dx.doi.org/10.1371/journal.pone.0085815.s008", "https://dx.doi.org/10.1371/journal.pone.0085815.s009", "https://dx.doi.org/10.1371/journal.pone.0085815.s010"], "stats"=>{"downloads"=>33, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Human_A53T_945_Synuclein_Causes_Reversible_Deficits_in_Mitochondrial_Function_and_Dynamics_in_Primary_Mouse_Cortical_Neurons_/890675", "title"=>"Human A53T α-Synuclein Causes Reversible Deficits in Mitochondrial Function and Dynamics in Primary Mouse Cortical Neurons", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-12-31 04:00:00"}

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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[272, 472, 600, 713, 815, 911, 1004, 1094, 1185, 1273, 1358, 1441]}, {"subject_area"=>"/Biology and life sciences/Physiology", "average_usage"=>[256, 449, 572, 676, 775, 866, 955, 1041, 1127, 1213, 1290, 1370, 1437]}, {"subject_area"=>"/Medicine and health sciences", "average_usage"=>[264, 460, 584, 692, 794, 887, 978, 1067, 1154, 1241, 1328, 1408, 1474]}, {"subject_area"=>"/Medicine and health sciences/Neurology", "average_usage"=>[271, 485, 617, 733, 835, 933, 1026, 1115, 1207, 1294, 1386, 1475, 1543]}]}
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