Dynactin Subunit p150Glued Is a Neuron-Specific Anti-Catastrophe Factor
Publication Date
July 16, 2013
Journal
PLOS Biology
Authors
Jacob E. Lazarus, Armen J. Moughamian, Mariko K. Tokito & Erika L. F. Holzbaur
Volume
11
Issue
7
Pages
e1001611
DOI
https://dx.plos.org/10.1371/journal.pbio.1001611
Publisher URL
http://journals.plos.org/plosbiology/article?id=10.1371%2Fjournal.pbio.1001611
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23874158
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3712912
Europe PMC
http://europepmc.org/abstract/MED/23874158
Web of Science
000322592700015
Scopus
84880944148
Mendeley
http://www.mendeley.com/research/dynactin-subunit-p150glued-neuronspecific-anticatastrophe-factor
Events
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Mendeley | Further Information

{"title"=>"Dynactin Subunit p150Glued Is a Neuron-Specific Anti-Catastrophe Factor", "type"=>"journal", "authors"=>[{"first_name"=>"Jacob E.", "last_name"=>"Lazarus", "scopus_author_id"=>"36955076800"}, {"first_name"=>"Armen J.", "last_name"=>"Moughamian", "scopus_author_id"=>"36962567300"}, {"first_name"=>"Mariko K.", "last_name"=>"Tokito", "scopus_author_id"=>"6701736394"}, {"first_name"=>"Erika L.F.", "last_name"=>"Holzbaur", "scopus_author_id"=>"7005370925"}], "year"=>2013, "source"=>"PLoS Biology", "identifiers"=>{"scopus"=>"2-s2.0-84880944148", "sgr"=>"84880944148", "issn"=>"15449173", "doi"=>"10.1371/journal.pbio.1001611", "pmid"=>"23874158", "isbn"=>"1545-7885 (Electronic)\\r1544-9173 (Linking)", "pui"=>"369462997"}, "id"=>"1e95a0dc-cb48-32ca-a792-65626d0c46a2", "abstract"=>"Regulation of microtubule dynamics in neurons is critical, as defects in the microtubule-based transport of axonal organelles lead to neurodegenerative disease. The microtubule motor cytoplasmic dynein and its partner complex dynactin drive retrograde transport from the distal axon. We have recently shown that the p150(Glued) subunit of dynactin promotes the initiation of dynein-driven cargo motility from the microtubule plus-end. Because plus end-localized microtubule-associated proteins like p150(Glued) may also modulate the dynamics of microtubules, we hypothesized that p150(Glued) might promote cargo initiation by stabilizing the microtubule track. Here, we demonstrate in vitro using assembly assays and TIRF microscopy, and in primary neurons using live-cell imaging, that p150(Glued) is a potent anti-catastrophe factor for microtubules. p150(Glued) alters microtubule dynamics by binding both to microtubules and to tubulin dimers; both the N-terminal CAP-Gly and basic domains of p150(Glued) are required in tandem for this activity. p150(Glued) is alternatively spliced in vivo, with the full-length isoform including these two domains expressed primarily in neurons. Accordingly, we find that RNAi of p150(Glued) in nonpolarized cells does not alter microtubule dynamics, while depletion of p150(Glued) in neurons leads to a dramatic increase in microtubule catastrophe. Strikingly, a mutation in p150(Glued) causal for the lethal neurodegenerative disorder Perry syndrome abrogates this anti-catastrophe activity. Thus, we find that dynactin has multiple functions in neurons, both activating dynein-mediated retrograde axonal transport and enhancing microtubule stability through a novel anti-catastrophe mechanism regulated by tissue-specific isoform expression; disruption of either or both of these functions may contribute to neurodegenerative disease.", "link"=>"http://www.mendeley.com/research/dynactin-subunit-p150glued-neuronspecific-anticatastrophe-factor", "reader_count"=>60, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>12, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>4, "Student > Master"=>7, "Other"=>2, "Student > Bachelor"=>8, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>12, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>4, "Student > Master"=>7, "Other"=>2, "Student > Bachelor"=>8, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>34, "Medicine and Dentistry"=>3, "Neuroscience"=>5, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Chemical Engineering"=>1, "Chemistry"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>5}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>34}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"United Kingdom"=>2, "Israel"=>1, "France"=>1, "Portugal"=>1, "Germany"=>1}, "group_count"=>3}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1119396"], "description"=>"<p>(A) Schematic depicting endogenous full-length p150<sup>Glued</sup> and dimeric and monomeric constructs. (B) Light scattering traces for recombinant polypeptides or buffer control incubated with tubulin show that the dimeric p150 Nt-GCN4 and neuronal MAPs tau23 and DCX-GFP robustly promote microtubule assembly, while monomeric p150 Nt and rKin430-GFP do not. (C) TIRF elongation assay. As shown in the schematic at top, rhodamine-labeled tubulin is polymerized from biotinylated Alexa488-labeled GMPCPP microtubule seeds. Montage below shows free tubulin assembly (red) from a stabilized seed (green) in the absence of p150. Arrowhead identifies the microtubule plus-end. (D) Kymograph plots showing representative examples with buffer, 200 nM p150 Nt, or p150 Nt-GCN4. (E) Polymerization rates and (F) catastrophe frequencies from seeded assembly shows that p150 Nt-GCN4 promotes polymerization and inhibits catastrophe. All error bars represent SEM of three or more independent experiments. Statistical testing was performed with a two-tailed <i>t</i> test. * <i>p</i><0.05; ** <i>p</i><0.01. For (E), <i>p</i><0.01 for all conditions compared to control.</p>", "links"=>[], "tags"=>["Biochemistry", "Molecular cell biology", "microtubule"], "article_id"=>745836, "categories"=>["Biological Sciences"], "users"=>["Jacob E. Lazarus", "Armen J. Moughamian", "Mariko K. Tokito", "Erika L. F. Holzbaur"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001611.g001", "stats"=>{"downloads"=>2, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_p150_Glued_promotes_microtubule_formation_/745836", "title"=>"p150<sup>Glued</sup> promotes microtubule formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-16 01:31:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1119405", "https://ndownloader.figshare.com/files/1119406", "https://ndownloader.figshare.com/files/1119407", "https://ndownloader.figshare.com/files/1119408", "https://ndownloader.figshare.com/files/1119409", "https://ndownloader.figshare.com/files/1119410", "https://ndownloader.figshare.com/files/1119411", "https://ndownloader.figshare.com/files/1119412"], "description"=>"<div><p>Regulation of microtubule dynamics in neurons is critical, as defects in the microtubule-based transport of axonal organelles lead to neurodegenerative disease. The microtubule motor cytoplasmic dynein and its partner complex dynactin drive retrograde transport from the distal axon. We have recently shown that the p150<sup>Glued</sup> subunit of dynactin promotes the initiation of dynein-driven cargo motility from the microtubule plus-end. Because plus end-localized microtubule-associated proteins like p150<sup>Glued</sup> may also modulate the dynamics of microtubules, we hypothesized that p150<sup>Glued</sup> might promote cargo initiation by stabilizing the microtubule track. Here, we demonstrate <i>in vitro</i> using assembly assays and TIRF microscopy, and in primary neurons using live-cell imaging, that p150<sup>Glued</sup> is a potent anti-catastrophe factor for microtubules. p150<sup>Glued</sup> alters microtubule dynamics by binding both to microtubules and to tubulin dimers; both the N-terminal CAP-Gly and basic domains of p150<sup>Glued</sup> are required in tandem for this activity. p150<sup>Glued</sup> is alternatively spliced <i>in vivo</i>, with the full-length isoform including these two domains expressed primarily in neurons. Accordingly, we find that RNAi of p150<sup>Glued</sup> in nonpolarized cells does not alter microtubule dynamics, while depletion of p150<sup>Glued</sup> in neurons leads to a dramatic increase in microtubule catastrophe. Strikingly, a mutation in p150<sup>Glued</sup> causal for the lethal neurodegenerative disorder Perry syndrome abrogates this anti-catastrophe activity. Thus, we find that dynactin has multiple functions in neurons, both activating dynein-mediated retrograde axonal transport and enhancing microtubule stability through a novel anti-catastrophe mechanism regulated by tissue-specific isoform expression; disruption of either or both of these functions may contribute to neurodegenerative disease.</p></div>", "links"=>[], "tags"=>["Biochemistry", "Molecular cell biology", "dynactin", "subunit", "neuron-specific", "anti-catastrophe"], "article_id"=>745845, "categories"=>["Biological Sciences"], "users"=>["Jacob E. Lazarus", "Armen J. Moughamian", "Mariko K. Tokito", "Erika L. F. Holzbaur"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1001611.s001", "https://dx.doi.org/10.1371/journal.pbio.1001611.s002", "https://dx.doi.org/10.1371/journal.pbio.1001611.s003", "https://dx.doi.org/10.1371/journal.pbio.1001611.s004", "https://dx.doi.org/10.1371/journal.pbio.1001611.s005", "https://dx.doi.org/10.1371/journal.pbio.1001611.s006", "https://dx.doi.org/10.1371/journal.pbio.1001611.s007", "https://dx.doi.org/10.1371/journal.pbio.1001611.s008"], "stats"=>{"downloads"=>13, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Dynactin_Subunit_p150_Glued_Is_a_Neuron_Specific_Anti_Catastrophe_Factor/745845", "title"=>"Dynactin Subunit p150<sup>Glued</sup> Is a Neuron-Specific Anti-Catastrophe Factor", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-07-16 01:31:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1119401"], "description"=>"<p>(A) Schematic depicting p150<sup>Glued</sup> spliceforms (and corresponding recombinant proteins): the neuronally-enriched p150 and p135 (p135 Nt-GCN4), and the ubiquitous isoform lacking the basic region (exons 5–7, Δ5–7 Nt-GCN4). (B, D) Size exclusion chromatography with (B) p135 Nt-GCN4 or (D) Δ5–7 Nt-GCN4 indicates that they cannot form stable complexes with tubulin. (C) Microtubule affinity of 400 nM dimeric polypeptides for increasing concentrations of Taxol-stabilized microtubules demonstrates that these constructs bind microtubules. (E) Light scattering traces for 1 µM constructs suggest that only the brain-specific full-length p150 isoform can promote microtubule formation. Error bars (± SEM) are smaller than the symbols. (F) Single frames from 6 min posttubulin perfusion contrasting the inability of Δ5–7 Nt-GCN4 or p135 Nt-GCN4 to nucleate microtubules with the full-length p150 Nt-GCN4. Scale bar, 12.5 µm.</p>", "links"=>[], "tags"=>["Biochemistry", "Molecular cell biology", "isoforms", "differentially", "microtubule"], "article_id"=>745841, "categories"=>["Biological Sciences"], "users"=>["Jacob E. Lazarus", "Armen J. Moughamian", "Mariko K. Tokito", "Erika L. F. Holzbaur"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001611.g004", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tissue_specific_p150_Glued_isoforms_differentially_modify_microtubule_assembly_dynamics_/745841", "title"=>"Tissue-specific p150<sup>Glued</sup> isoforms differentially modify microtubule assembly dynamics.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-16 01:31:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1119400"], "description"=>"<p>(A) Size exclusion chromatograms for p150 Nt-GCN4 run alone or pre-incubated with tubulin reveal that p150 forms a stable complex with tubulin. For the red trace, maximum absorbance is scaled to the complex peak. (B) Size exclusion chromatograms for subtilisin-treated tubulin incubated with p150 Nt-GCN4 suggest that the p150<sup>Glued</sup> binds tubulin C-termini in solution, as complex formation is not observed after cleavage. (C) Size exclusion chromatograms for p150 Nt-GCN4 incubated with tubulin and eluted at increasing ionic strength indicate that electrostatic interactions between tubulin and the p150 basic domain stabilize the p150-tubulin complex because progressively reduced complex formation is observed.</p>", "links"=>[], "tags"=>["Biochemistry", "Molecular cell biology", "forms", "soluble"], "article_id"=>745840, "categories"=>["Biological Sciences"], "users"=>["Jacob E. Lazarus", "Armen J. Moughamian", "Mariko K. Tokito", "Erika L. F. Holzbaur"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001611.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_p150_Glued_forms_a_complex_with_soluble_tubulin_/745840", "title"=>"p150<sup>Glued</sup> forms a complex with soluble tubulin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-16 01:31:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1119398"], "description"=>"<p>(A) Light scattering traces for increasing concentrations of p150 Nt-GCN4. At right, the scale was magnified to illustrate the initial increase in light scattering observed with increasing concentrations of p150 Nt-GCN4. Error bars represent SEM of three or more independent experiments and are omitted for clarity at right. (B) p150 Nt-GCN4 decreases nucleation time, defined as initial appearance of signal over background. Fit is to a double exponential decay. Note that error bars are smaller than symbols. (C) Schematic of the TIRF nucleation assay. p150 constructs are immobilized and the chamber is then perfused with rhodamine-labeled tubulin. (D) Montage from TIRF nucleation assay shows that dimeric p150 Nt-GCN4 catalyzes microtubule nucleation in contrast to monomeric p150 Nt. Scale bar, 12.5 µm. (E) Montage of representative microtubules nucleated in the presence of a low concentration of p150 dimer. Yellow arrows identify the site of nucleation. Red arrows identify the growing plus- and minus-ends. Scale bar, 5 µm.</p>", "links"=>[], "tags"=>["Biochemistry", "Molecular cell biology", "catalyzes", "microtubules"], "article_id"=>745838, "categories"=>["Biological Sciences"], "users"=>["Jacob E. Lazarus", "Armen J. Moughamian", "Mariko K. Tokito", "Erika L. F. Holzbaur"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001611.g002", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_p150_catalyzes_microtubules_nucleation_/745838", "title"=>"p150 catalyzes microtubules nucleation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-16 01:31:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1119403"], "description"=>"<p>p150<sup>Glued</sup> inhibits microtubule catastrophe by binding both to microtubules and to soluble tubulin, leading to enhanced microtubule stability along the axon. Depletion of endogenous p150<sup>Glued</sup> by RNAi leads to more frequent microtubule catastrophe in neurons.</p>", "links"=>[], "tags"=>["Biochemistry", "Molecular cell biology", "neuron-specific", "microtubule", "anti-catastrophe"], "article_id"=>745843, "categories"=>["Biological Sciences"], "users"=>["Jacob E. Lazarus", "Armen J. Moughamian", "Mariko K. Tokito", "Erika L. F. Holzbaur"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001611.g006", "stats"=>{"downloads"=>4, "page_views"=>232, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_p150_Glued_is_a_neuron_specific_microtubule_anti_catastrophe_factor_/745843", "title"=>"p150<sup>Glued</sup> is a neuron-specific microtubule anti-catastrophe factor.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-16 01:31:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1119402"], "description"=>"<p>(A) Depletion of p150<sup>Glued</sup> in COS7 cells by siRNA (KD) relative to control cells treated with scrambled (Scram) oligonucleotides; upper panel is a Western blot probed with a monoclonal antibody to p150<sup>Glued</sup>, and lower panel is Coomassie staining to show equal protein loading. (B) Representative rainbow-coded maximum intensity projections show that the overall microtubule architecture and dynamics are not perturbed in COS7 cells depleted of p150<sup>Glued</sup> relative to control cells. (C) PlusTipTracker quantitation of EB3-GFP comet velocities shows that knockdown does not alter parameters of microtubule dynamics, including distance to catastrophe, a measure of the catastrophe frequency (<i>p</i>>0.1). (D) Western blot showing knockdown of p150<sup>Glued</sup> in DRG neurons (KD), relative to control neurons or COS7 cells treated with scrambled oligonucleotide. Note the differential splice forms of p150<sup>Glued</sup> expressed in neurons relative to COS7 cells. (E) Space-filling fluorescence in representative neurites used to investigate microtubule dynamics in primary DRG neurons. (F) Rainbow-coded maximum intensity projections of selected EB3-GFP comets demonstrate microtubule dynamics in DRG neurons. (G) Kymographs of GFP-EB3 comets in cultured DRG neurons treated with either scrambled or p150<sup>Glued</sup> RNAi reveal that in neurons, p150<sup>Glued</sup> inhibits catastrophe. (H) Camera lucida tracing of the kymographs in panel G to indicate polymerization events persisting greater than 5 µm (black) and less than 2 µm (magenta). (I) Kymographs of GFP-EB3 comets in neurons depleted of endogenous p150<sup>Glued</sup> by RNAi and rescued with either full-length p150, Δ5–7, or the neuron-specific alternative splice form p135. (J) Analysis of microtubule dynamics in scrambled control neurons, and neurons depleted of endogenous p150<sup>Glued</sup> with or without rescue with resistant constructs of p150 or p135 and Δ5–7. Bars represent mean of comet parameters from multiple cells on multiple days ± SEM. Statistical testing was performed via <i>t</i> test with correction for multiple comparisons. *** <i>p</i><0.001. (K) In vitro analysis of catastrophe rates demonstrates that the Perry syndrome-associated mutation Q74P p150 Nt-GCN4 does not inhibit microtubule catastrophe (<i>p</i>>0.5), as compared to the wild-type p150Nt-GCN4 construct. (L, M) Kymographs and quantitation of GFP-EB3 comets in cultured DRG neurons depleted of endogenous p150<sup>Glued</sup> and rescued with either wild-type or Q74P p150<sup>Glued</sup> reveal that mutant p150 is defective in inhibiting microtubule catastrophe in neurons.</p>", "links"=>[], "tags"=>["Biochemistry", "Molecular cell biology", "stabilizes", "microtubules"], "article_id"=>745842, "categories"=>["Biological Sciences"], "users"=>["Jacob E. Lazarus", "Armen J. Moughamian", "Mariko K. Tokito", "Erika L. F. Holzbaur"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001611.g005", "stats"=>{"downloads"=>3, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_p150_Glued_stabilizes_microtubules_in_neurons_/745842", "title"=>"p150<sup>Glued</sup> stabilizes microtubules in neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-16 01:31:36"}

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Relative Metric

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