The Nesprin Family Member ANC-1 Regulates Synapse Formation and Axon Termination by Functioning in a Pathway with RPM-1 and β-Catenin
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{"title"=>"The Nesprin Family Member ANC-1 Regulates Synapse Formation and Axon Termination by Functioning in a Pathway with RPM-1 and β-Catenin", "type"=>"journal", "authors"=>[{"first_name"=>"Erik D.", "last_name"=>"Tulgren", "scopus_author_id"=>"56195985200"}, {"first_name"=>"Shane M.", "last_name"=>"Turgeon", "scopus_author_id"=>"56184291000"}, {"first_name"=>"Karla J.", "last_name"=>"Opperman", "scopus_author_id"=>"23467085600"}, {"first_name"=>"Brock", "last_name"=>"Grill", "scopus_author_id"=>"6701689009"}], "year"=>2014, "source"=>"PLoS Genetics", "identifiers"=>{"issn"=>"15537404", "pui"=>"373701239", "doi"=>"10.1371/journal.pgen.1004481", "sgr"=>"84905483305", "scopus"=>"2-s2.0-84905483305", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "pmid"=>"25010424"}, "id"=>"095d22f1-6cc6-3b49-b064-0013555dd7ae", "abstract"=>"Mutations in Nesprin-1 and 2 (also called Syne-1 and 2) are associated with numerous diseases including autism, cerebellar ataxia, cancer, and Emery-Dreifuss muscular dystrophy. Nesprin-1 and 2 have conserved orthologs in flies and worms called MSP-300 and abnormal nuclear Anchorage 1 (ANC-1), respectively. The Nesprin protein family mediates nuclear and organelle anchorage and positioning. In the nervous system, the only known function of Nesprin-1 and 2 is in regulation of neurogenesis and neural migration. It remains unclear if Nesprin-1 and 2 regulate other functions in neurons. Using a proteomic approach in C. elegans, we have found that ANC-1 binds to the Regulator of Presynaptic Morphology 1 (RPM-1). RPM-1 is part of a conserved family of signaling molecules called Pam/Highwire/RPM-1 (PHR) proteins that are important regulators of neuronal development. We have found that ANC-1, like RPM-1, regulates axon termination and synapse formation. Our genetic analysis indicates that ANC-1 functions via the β-catenin BAR-1, and the ANC-1/BAR-1 pathway functions cell autonomously, downstream of RPM-1 to regulate neuronal development. Further, ANC-1 binding to the nucleus is required for its function in axon termination and synapse formation. We identify variable roles for four different Wnts (LIN-44, EGL-20, CWN-1 and CWN-2) that function through BAR-1 to regulate axon termination. Our study highlights an emerging, broad role for ANC-1 in neuronal development, and unveils a new and unexpected mechanism by which RPM-1 functions.", "link"=>"http://www.mendeley.com/research/nesprin-family-member-anc1-regulates-synapse-formation-axon-termination-functioning-pathway-rpm1-%CE%B2ca", "reader_count"=>22, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Ph. D. Student"=>7, "Other"=>1, "Student > Master"=>3, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Ph. D. Student"=>7, "Other"=>1, "Student > Master"=>3, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>13, "Medicine and Dentistry"=>2, "Neuroscience"=>4, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}}, "reader_count_by_country"=>{"Israel"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1587634"], "description"=>"<p>(A) Upper panel diagrams the GABAergic DD neurons (blue) that innervate dorsal muscles (inspired by Worm Atlas). DD Presynaptic terminals are shown in green. The red box highlights the region of the dorsal cord that was visualized by epifluorescent microscopy. The transgene <i>juIs1</i> [P<sub>unc-25</sub>SNB-1::GFP] was used to visualize the presynaptic terminals for the indicated genotypes. Arrows highlight regions lacking presynaptic terminals represented by SNB-1::GFP puncta. Arrowheads note abnormal aggregation of presynaptic terminals. Scale bar is 10 µm. (B) Quantitation of the average number of SNB-1::GFP puncta per 100 µm of dorsal cord for the indicated genotypes. Analysis was done on young adults grown at 25°C. Significance was determined using an unpaired Student's <i>t</i> test; error bars represent the standard error of the mean. ***<i>P</i><0.001, ns = not significant.</p>", "links"=>[], "tags"=>["Biochemistry", "genetics", "neuroscience", "regulates", "synapse", "gabaergic"], "article_id"=>1099392, "categories"=>["Biological Sciences"], "users"=>["Erik D. Tulgren", "Shane M. Turgeon", "Karla J. Opperman", "Brock Grill"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004481.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_anc_1_regulates_synapse_formation_in_the_GABAergic_motor_neurons_/1099392", "title"=>"<i>anc-1</i> regulates synapse formation in the GABAergic motor neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-10 03:07:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1587656"], "description"=>"<p>Quantitation of axon termination defects (hook) in PLM neurons for the indicated genotypes using <i>muIs32</i>. (A) <i>unc-84</i> mutant analysis. (B) <i>emr-1</i> mutant analysis. Analysis was done on young adults grown at 23°C. Significance was determined using an unpaired Student's <i>t</i> test; error bars represent the standard error of the mean. *<i>P</i><0.05, ***<i>P</i><0.001, ns = not significant.</p>", "links"=>[], "tags"=>["Biochemistry", "genetics", "neuroscience", "pathway", "axon"], "article_id"=>1099404, "categories"=>["Biological Sciences"], "users"=>["Erik D. Tulgren", "Shane M. Turgeon", "Karla J. Opperman", "Brock Grill"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004481.g006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_anc_1_and_unc_84_function_in_the_same_genetic_pathway_to_regulate_axon_termination_/1099404", "title"=>"<i>anc-1</i> and <i>unc-84</i> function in the same genetic pathway to regulate axon termination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-10 03:07:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1587628"], "description"=>"<p>(A) Schematic of ANC-1 protein structure which consists of two calponin homology (CH) domains that bind F-actin (dashed boxes), 6 repeat regions (grey), and a KASH domain (black) that mediates binding to the nucleus. Also shown is the C-terminal domain of ANC-1 that functions as a dominant negative. (B) CoIP of endogenous ANC-1 with RPM-1::GFP. CoIPs were performed from whole worm lysates prepared from transgenic animals (<i>juIs58</i>) or non-transgenic animals (N2). (C) Epifluorescent microscopy was used to visualize SUR-5::GFP in the multinucleated hypodermal cells of <i>C. elegans</i>. In wild-type animals, nuclei are anchored to the actin cytoskeleton and evenly spaced throughout the syncytium (arrowheads). In <i>anc-1</i> mutants, impaired nuclear anchorage leads to aggregation of nuclei (arrows). Scale bar is 20 µm.</p>", "links"=>[], "tags"=>["Biochemistry", "genetics", "neuroscience", "binds"], "article_id"=>1099386, "categories"=>["Biological Sciences"], "users"=>["Erik D. Tulgren", "Shane M. Turgeon", "Karla J. Opperman", "Brock Grill"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004481.g001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ANC_1_binds_to_RPM_1_/1099386", "title"=>"ANC-1 binds to RPM-1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-10 03:07:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1587652"], "description"=>"<p>(A) Upper panel diagrams the mechanosensory neurons of <i>C. elegans</i> (inspired by Worm Atlas). PLM neurons were visualized using <i>muIs32</i> [P<sub>mec7</sub>GFP]. The black box indicates the region of the animal that is visualized by epifluorescent microscopy and shown on the right. Shown for the <i>rpm-1</i> mutant is the PLM axon termination phenotype that we refer to as a hook defect (arrowhead). Scale bar is 10 µm. (B) Quantitation of axon termination (hook) defects in PLM neurons for the indicated genotypes. (C) An ANC-1 dominant negative construct (ANC-1 DN) was expressed using a pan-neuronal promoter (P<i>rgef-1</i>) or a mechanosensory neuron specific promoter (P<i>mec-3</i>) with the indicated genotypes. A full length ANC-1 rescue construct (P<i>mec-7</i>::ANC-1) was expressed in <i>anc-1; fsn-1</i> double mutants. The data shown is an average of 5 or more transgenic lines for each genotype. Analysis was done on young adults grown at 23°C. Significance was determined using an unpaired Student's <i>t</i> test; error bars represent the standard error of the mean. *<i>P</i><0.05, **<i>P</i><0.01, ***<i>P</i><0.001, ns = not significant.</p>", "links"=>[], "tags"=>["Biochemistry", "genetics", "neuroscience", "functions", "autonomously", "axon", "termination", "plm", "mechanosensory"], "article_id"=>1099400, "categories"=>["Biological Sciences"], "users"=>["Erik D. Tulgren", "Shane M. Turgeon", "Karla J. Opperman", "Brock Grill"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004481.g004", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_anc_1_functions_cell_autonomously_to_regulate_axon_termination_in_the_PLM_mechanosensory_neurons_/1099400", "title"=>"<i>anc-1</i> functions cell autonomously to regulate axon termination in the PLM mechanosensory neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-10 03:07:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1587665", "https://ndownloader.figshare.com/files/1587666", "https://ndownloader.figshare.com/files/1587667", "https://ndownloader.figshare.com/files/1587668"], "description"=>"<div><p>Mutations in Nesprin-1 and 2 (also called Syne-1 and 2) are associated with numerous diseases including autism, cerebellar ataxia, cancer, and Emery-Dreifuss muscular dystrophy. Nesprin-1 and 2 have conserved orthologs in flies and worms called MSP-300 and abnormal nuclear <u>Anc</u>horage 1 (ANC-1), respectively. The Nesprin protein family mediates nuclear and organelle anchorage and positioning. In the nervous system, the only known function of Nesprin-1 and 2 is in regulation of neurogenesis and neural migration. It remains unclear if Nesprin-1 and 2 regulate other functions in neurons. Using a proteomic approach in <i>C. elegans</i>, we have found that ANC-1 binds to the <u>R</u>egulator of <u>P</u>resynaptic <u>M</u>orphology 1 (RPM-1). RPM-1 is part of a conserved family of signaling molecules called <u>P</u>am/<u>H</u>ighwire/<u>R</u>PM-1 (PHR) proteins that are important regulators of neuronal development. We have found that ANC-1, like RPM-1, regulates axon termination and synapse formation. Our genetic analysis indicates that ANC-1 functions via the β-catenin BAR-1, and the ANC-1/BAR-1 pathway functions cell autonomously, downstream of RPM-1 to regulate neuronal development. Further, ANC-1 binding to the nucleus is required for its function in axon termination and synapse formation. We identify variable roles for four different Wnts (LIN-44, EGL-20, CWN-1 and CWN-2) that function through BAR-1 to regulate axon termination. Our study highlights an emerging, broad role for ANC-1 in neuronal development, and unveils a new and unexpected mechanism by which RPM-1 functions.</p></div>", "links"=>[], "tags"=>["Biochemistry", "genetics", "neuroscience", "nesprin", "anc-1", "regulates", "synapse", "axon", "termination", "functioning", "pathway", "rpm-1"], "article_id"=>1099413, "categories"=>["Biological Sciences"], "users"=>["Erik D. Tulgren", "Shane M. Turgeon", "Karla J. Opperman", "Brock Grill"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004481.s001", "https://dx.doi.org/10.1371/journal.pgen.1004481.s002", "https://dx.doi.org/10.1371/journal.pgen.1004481.s003", "https://dx.doi.org/10.1371/journal.pgen.1004481.s004"], "stats"=>{"downloads"=>11, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Nesprin_Family_Member_ANC_1_Regulates_Synapse_Formation_and_Axon_Termination_by_Functioning_in_a_Pathway_with_RPM_1_and_946_Catenin_/1099413", "title"=>"The Nesprin Family Member ANC-1 Regulates Synapse Formation and Axon Termination by Functioning in a Pathway with RPM-1 and β-Catenin", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-07-10 03:07:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1587640"], "description"=>"<p>(A) Epifluorescent microscopy was used to visualize presynaptic terminals labeled using the transgene <i>juIs1</i> for the indicated genotypes. Arrows highlight regions lacking presynaptic terminals represented by SNB-1::GFP puncta. Arrowheads note abnormal aggregation of presynaptic terminals. Scale bar is 10 µm. (B) Quantitation of the average number of SNB-1::GFP puncta per 100 µm of dorsal cord for the indicated genotypes. Analysis was done on young adults grown at 25°C. Significance was determined using an unpaired Student's <i>t</i> test; error bars represent the standard error of the mean. ***<i>P</i><0.001, ns = not significant.</p>", "links"=>[], "tags"=>["Biochemistry", "genetics", "neuroscience", "pathway", "synapse"], "article_id"=>1099398, "categories"=>["Biological Sciences"], "users"=>["Erik D. Tulgren", "Shane M. Turgeon", "Karla J. Opperman", "Brock Grill"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004481.g003", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_anc_1_and_bar_1_function_in_the_same_genetic_pathway_to_regulate_synapse_formation_/1099398", "title"=>"<i>anc-1</i> and <i>bar-1</i> function in the same genetic pathway to regulate synapse formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-10 03:07:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1587659"], "description"=>"<p>Canonical Wnt signaling through Disheveled (Dis) and APR-1 (APC ortholog) regulates the β-catenin BAR-1. In the absence of Wnt, APR-1 is active and inhibits BAR-1. In the presence of Wnt, APR-1 is inhibited and BAR-1 activity is increased. Higher levels of BAR-1 lead to increased nuclear import and activation of the transcription factor POP-1 (TCF/LEF). We have shown that RPM-1 binds to ANC-1, and RPM-1 and ANC-1 function in the same pathway to positively regulate BAR-1 activity. RPM-1 and ANC-1 are likely to function in a protein complex at the nuclear envelope to regulate BAR-1 nuclear levels by inhibition of EMR-1. Canonical Wnt signaling is likely to act coordinately with RPM-1 and ANC-1 to regulate BAR-1 activity.</p>", "links"=>[], "tags"=>["Biochemistry", "genetics", "neuroscience", "rpm-1"], "article_id"=>1099407, "categories"=>["Biological Sciences"], "users"=>["Erik D. Tulgren", "Shane M. Turgeon", "Karla J. Opperman", "Brock Grill"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004481.g008", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_RPM_1_signaling_through_the_ANC_1_BAR_1_pathway_/1099407", "title"=>"Summary of RPM-1 signaling through the ANC-1/BAR-1 pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-10 03:07:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1587658"], "description"=>"<p>Quantitation of axon termination defects (hook) in PLM neurons for the indicated genotypes using <i>muIs32</i>. Note that <i>zdIs5</i> (P<sub>mec-4</sub>GFP) was used for <i>cwn-2</i> analysis because both <i>muIs32</i> and <i>cwn-2</i> are on chromosome II. Analysis was done on young adults grown at 23°C. Significance was determined using an unpaired Student's <i>t</i> test; error bars represent the standard error of the mean. *<i>P</i><0.05, **<i>P</i><0.01, ***<i>P</i><0.001, ns = not significant.</p>", "links"=>[], "tags"=>["Biochemistry", "genetics", "neuroscience", "wnts", "plm", "axon"], "article_id"=>1099406, "categories"=>["Biological Sciences"], "users"=>["Erik D. Tulgren", "Shane M. Turgeon", "Karla J. Opperman", "Brock Grill"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004481.g007", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Wnts_egl_20_and_lin_44_function_through_bar_1_to_regulate_PLM_axon_termination_/1099406", "title"=>"The Wnts <i>egl-20</i> and <i>lin-44</i> function through <i>bar-1</i> to regulate PLM axon termination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-10 03:07:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1587653"], "description"=>"<p>Quantitation of axon termination defects (hook) in PLM neurons for the indicated genotypes using <i>muIs32</i>. (A) <i>bar-1</i> and <i>pop-1</i> analysis. (B) <i>apr-1</i> analysis. (C) A cell specific promoter (<i>Pmec</i>-7) was used to transgenically express BAR-1. Analysis was done on young adults grown at 23°C. Significance was determined using an unpaired Student's <i>t</i> test; error bars represent the standard error of the mean. **<i>P</i><0.01, ***<i>P</i><0.001, ns = not significant.</p>", "links"=>[], "tags"=>["Biochemistry", "genetics", "neuroscience", "functions", "downstream", "axon"], "article_id"=>1099402, "categories"=>["Biological Sciences"], "users"=>["Erik D. Tulgren", "Shane M. Turgeon", "Karla J. Opperman", "Brock Grill"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004481.g005", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_bar_1_functions_downstream_of_anc_1_and_rpm_1_to_regulate_axon_termination_/1099402", "title"=>"<i>bar-1</i> functions downstream of <i>anc-1</i> and <i>rpm-1</i> to regulate axon termination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-10 03:07:56"}

PMC Usage Stats | Further Information

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Relative Metric

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