RACK-1 Acts with Rac GTPase Signaling and UNC-115/abLIM in Caenorhabditis elegans Axon Pathfinding and Cell Migration
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{"title"=>"RACK-1 acts with Rac GTpase signaling and UNC-115/abLIM in Caenorhabditis elegans axon pathfinding and cell migration", "type"=>"journal", "authors"=>[{"first_name"=>"Rafael S.", "last_name"=>"Demarco", "scopus_author_id"=>"25639496300"}, {"first_name"=>"Erik A.", "last_name"=>"Lundquist", "scopus_author_id"=>"6602695915"}], "year"=>2010, "source"=>"PLoS Genetics", "identifiers"=>{"sgr"=>"78649716388", "doi"=>"10.1371/journal.pgen.1001215", "pui"=>"360082653", "pmid"=>"21124943", "scopus"=>"2-s2.0-78649716388", "issn"=>"15537390", "isbn"=>"1553-7404 (Electronic)\\n1553-7390 (Linking)"}, "id"=>"28003b79-57c6-3bdf-b775-6144a8abc143", "abstract"=>"Migrating cells and growth cones extend lamellipodial and filopodial protrusions that are required for outgrowth and guidance. The mechanisms of cytoskeletal regulation that underlie cell and growth cone migration are of much interest to developmental biologists. Previous studies have shown that the Arp2/3 complex and UNC-115/abLIM act redundantly to mediate growth cone lamellipodia and filopodia formation and axon pathfinding. While much is known about the regulation of Arp2/3, less is known about regulators of UNC-115/abLIM. Here we show that the Caenorhabditis elegans counterpart of the Receptor for Activated C Kinase (RACK-1) interacts physically with the actin-binding protein UNC-115/abLIM and that RACK-1 is required for axon pathfinding. Genetic interactions indicate that RACK-1 acts cell-autonomously in the UNC-115/abLIM pathway in axon pathfinding and lamellipodia and filopodia formation, downstream of the CED-10/Rac GTPase and in parallel to MIG-2/RhoG. Furthermore, we show that RACK-1 is involved in migration of the gonadal distal tip cells and that the signaling pathways involved in this process might be distinct from those involved in axon pathfinding. In sum, these studies pinpoint RACK-1 as a component of a novel signaling pathway involving Rac GTPases and UNC-115/abLIM and suggest that RACK-1 might be involved in the regulation of the actin cytoskeleton and lamellipodia and filopodia formation in migrating cells and growth cones.", "link"=>"http://www.mendeley.com/research/rack1-acts-rac-gtpase-signaling-unc115ablim-caenorhabditis-elegans-axon-pathfinding-cell-migration", "reader_count"=>26, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Materials Science"=>1, "Agricultural and Biological Sciences"=>20, "Neuroscience"=>2}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Neuroscience"=>{"Neuroscience"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>3}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/817060"], "description"=>"<p>The Y axis denotes genotype, and the X axis represents percentage of defects of the sort described in the legend. <i>Ex[rack-1(+)]</i> is the full-length <i>rack-1::myc</i> transgene under the <i>rack-1</i> endogenous promoter, and <i>Ex[unc-25::rack-1(+)]</i> is a transgene with <i>rack-1::gfp</i> expression driven by the <i>unc-25</i> promoter specifically in the GABAergic neurons, including the VD/DDs. VD/DD commissural axon pathfinding defects were scored by animal (the percent of animals with defective axons) or by axon (the percent of defect axons). Number of animals or axons scored is indicated in the bars. P-values for significance were determined by Fisher Exact Analysis.</p>", "links"=>[], "tags"=>["acts", "cell-autonomously", "axon"], "article_id"=>487428, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g003", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RACK_1_acts_cell_autonomously_in_VD_DD_motor_axon_pathfinding_/487428", "title"=>"RACK-1 acts cell-autonomously in VD/DD motor axon pathfinding.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:14:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/817567"], "description"=>"<p>A) Quantitation of VD/DD defects caused by expression of MYR::UNC-115 from the <i>unc-115</i> promoter, which is expressed in the VD/DD neurons. The asterisks represent a test of additivity of the represented genotypes. The double mutant is significantly different from each single, and the double mutant had defects that were significantly stronger than the additive effects of each single. The following formula was used to predict the additive effect of the double mutant based on the single mutant phenotypes: <i>rack-1(tm2262)</i> + <i>lqIs62</i>− (<i>rack-1(tm2262)</i> * <i>lqIs62</i>); or 0.42+0.21− (0.42 * 0.21)  = 0.54. At least 100 animals were scored, and p-value significance was determined by Fisher Exact Analysis. B) A VD neuron cell body was laterally displaced (arrow) in a <i>rack-1(tm2262M+); lqIs62[myr::unc-115]</i> animal. <i>rack-1(tm2262)</i> partially suppressed this phenotype compared to <i>lqIs62</i> alone. Arrowheads indicate VD/DD cell bodies in their normal positions in the ventral nerve cord.</p>", "links"=>[], "tags"=>["neurons", "suppressed"], "article_id"=>487942, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g008", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Activated_MYR_UNC_115_in_VD_DD_motor_neurons_is_not_suppressed_by_rack_1_tm2262_/487942", "title"=>"Activated MYR::UNC-115 in VD/DD motor neurons is not suppressed by <i>rack-1(tm2262)</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:17:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/817795"], "description"=>"<p>(A and B) Differential Interference Contrast micrographs of wild type and <i>rack-1(tm2262)</i> gonads. Dashed lines trace the outline of the gonad arm. The scale bar in A represents 10 µm. C) Quantitation of gonad arm migration defects. Number of gonad arms scored is indicated in the bars (>100). P-value significance was determined by Fisher Exact Analysis. The predicted additive effect of the <i>rack-1(tm2262M+) ced-10(n1993M+)</i> double if they did not interact was calculated by the formula <i>rack-1(tm2262)</i> + <i>ced-10(n1993)</i> − (<i>rack-1(tm2262)</i> * <i>ced-10(n1993</i>); or 0.32+0.14− (0.32 * 0.14)  = 0.42. This number was also significantly different from the observed <i>rack-1(tm2262M+) ced-10(n1993M+)</i> double mutant.</p>", "links"=>[], "tags"=>["gonadal", "distal"], "article_id"=>488166, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g010", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RACK_1_is_required_for_gonadal_distal_tip_cell_migration_/488166", "title"=>"RACK-1 is required for gonadal distal tip cell migration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:18:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/817348"], "description"=>"<p>(A and B) Micrographs of animals with <i>osm-6::gfp</i> expression in the PDE neurons. The arrow in A indicates a wild-type axon, and the arrow in B indicates a misguided axon in a <i>mig-2(mu28)</i> mutant. The scale bar represents 5 µm for A and B. C) The graph represents percent of PDE axon pathfinding defects in different genotypes. At least 100 neurons were scored for each genotype, and p-value significance was determined by Fisher Exact Analysis. The genotypes indicated with an NS are not significantly different in any pairwise combination.</p>", "links"=>[], "tags"=>["acts", "genetically"], "article_id"=>487722, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g006", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RACK_1_acts_genetically_in_the_CED_10_Rac_and_UNC_115_abLIM_pathway_/487722", "title"=>"RACK-1 acts genetically in the CED-10/Rac and UNC-115/abLIM pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:15:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/817478"], "description"=>"<p>A) A micrograph of the PDE neuron of an adult animal expressing activated CED-10(G12V). An ectopic lamellipodial protrusion is indicated by an arrow. The scale bar represents 5 µm. B) Quantitation of PDE defects. <i>lqIs14</i> is the <i>osm-6::ced-10(G12V)</i> transgene; <i>lqIs46</i> is the <i>osm-6::mig-2(G16V)</i> transgene; and <i>lqIs62</i> is the <i>unc-115::myr::unc-115</i> transgene. At least 100 neurons were scored for each genotype, and p-value significance was determined by Fisher Exact Analysis.</p>", "links"=>[], "tags"=>["suppresses", "activated"], "article_id"=>487853, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g007", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_rack_1_tm2262_partially_suppresses_activated_CED_10_G12V_but_not_MIG_2_G16V_or_activated_MYR_UNC_115_/487853", "title"=>"<i>rack-1(tm2262)</i> partially suppresses activated CED-10(G12V), but not MIG-2(G16V) or activated MYR::UNC-115.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:16:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/817928"], "description"=>"<p>A linear pathway representing the genetic interactions between <i>ced-10/Rac, rack-1</i>, and <i>unc-115</i>. RACK-1 acts downstream of CED-10/Rac and controls UNC-115/abLIM. LIM  =  LIM domain; VHD  =  villin headpiece domain.</p>", "links"=>[], "tags"=>["downstream", "lamellipodia", "filopodia"], "article_id"=>488302, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g011", "stats"=>{"downloads"=>5, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RACK_1_might_regulate_UNC_115_abLIM_downstream_of_CED_10_Rac_in_lamellipodia_and_filopodia_formation_/488302", "title"=>"RACK-1 might regulate UNC-115/abLIM downstream of CED-10/Rac in lamellipodia and filopodia formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:18:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/817258"], "description"=>"<p>Micrographs are of animals harboring an <i>unc-25::rack-1::gfp</i> transgene that expresses a full-length RACK-1::GFP fusion protein specifically in the VD/DD GABAergic motor neurons. A) RACK-1::GFP expression is specific to the VD/DD motor neurons. Arrowheads indicate cell bodies in the ventral nerve cord, and arrows indicate commissural axons. The punctate fluorescence throughout the animal is autofluorescence of the gut. B) RACK-1::GFP accumulated in a VD growth cone in an early L2 animal (arrow). The diagram at the right traces the outline of the growth cone and axon. The scale bars represent 5 µm.</p>", "links"=>[], "tags"=>["gabaergic"], "article_id"=>487633, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g005", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RACK_1_GFP_expression_in_GABAergic_motor_neurons_/487633", "title"=>"RACK-1::GFP expression in GABAergic motor neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:15:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/816948"], "description"=>"<p>All panels are micrographs of animals with <i>unc-25promoter::gfp</i> expression (<i>juIs76</i> transgene) in the VD/DD GABAergic motor neurons. The scale bar in A represents 10 µm for all panels. (A and B) Wild type and <i>rack-1(RNAi)</i> showing the DD1/VD2 commissure on the left side of the animal. Misrouted and branched axons are indicated by an arrow. Dorsal is up, and anterior is left. (C and D) Dorsal views of the dorsal nerve cords (marked by a D) of wild type and <i>rack-1(tm2262)</i>. This dorsal view allows for demonstration of the sidedness of axon pathfinding. The cell bodies in the ventral nerve cord are out of focus (marked by a V). The arrow in C points to the DD1/VD2 commissure on the left side of the animal. All other VD/DD commissures go up the right side. Arrows in D point to VD/DD commissures that aberrantly extend up the left side of the animal in <i>rack-1(tm2262)</i>. (E and F) VD/DD commissures in wild type and <i>rack-1(tm2262)</i>. The arrow in F points to a misguided axon.</p>", "links"=>[], "tags"=>["axon"], "article_id"=>487321, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RACK_1_is_required_for_VD_DD_motor_axon_pathfinding_/487321", "title"=>"RACK-1 is required for VD/DD motor axon pathfinding.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:13:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/817145"], "description"=>"<p>Panels are fluorescent micrographs of animals harboring <i>rack-1::gfp</i> transgenes. (A and B) are fusions of the <i>rack-1</i> promoter to <i>gfp</i>; and (C and D) are fusions of the entire full-length <i>rack-1</i> coding region to GFP. A) A distal tip cell expressed <i>rack-1::gfp</i>. B) Neurons expressed <i>rack-1::gfp</i>. C) Full-length RACK-1::GFP was expressed in neurons in the ventral nerve cord (arrows) and in the amphid (arrowhead). D) Full-length RACK-1::GFP was excluded from nuclei in tail hypodermis and gut (arrows). The scale bar in A represents 5 µm for A–C, and the scale bar in D represents 5 µm.</p>", "links"=>[], "tags"=>["neurons", "gonadal", "distal"], "article_id"=>487513, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g004", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RACK_1_is_expressed_in_most_cells_including_neurons_and_the_gonadal_distal_tip_cells_/487513", "title"=>"RACK-1 is expressed in most cells, including neurons and the gonadal distal tip cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:14:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/817659"], "description"=>"<p>A) A micrograph of MYR::RACK-1::GFP expression in the PDE neuron driven by the <i>osm-6</i> promoter. The arrowhead points to the cell surface accumulation of MYR::RACK-1::GFP, and the arrow points to an ectopic lamellipodium. The scale bar represents 5 µm. B) Quantitation of ectopic lamellipodial defects in PDEs expressing MYR::RACK-1::GFP. At least 100 animals were scored for each genotype, and p-value significance was determined by Fisher Exact Analysis.</p>", "links"=>[], "tags"=>["developmental biology/morphogenesis and cell biology", "developmental biology/neurodevelopment", "neuroscience/neurodevelopment"], "article_id"=>488028, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g009", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_UNC_115_is_required_for_the_effects_of_MYR_RACK_1_/488028", "title"=>"UNC-115 is required for the effects of MYR::RACK-1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:17:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/816851"], "description"=>"<p>A) A schematic diagram of the 639-residue UNC-115 molecule. LIM = LIM domains; VHD  =  villin headpiece domain; UAD  =  unc-115/abLIM/dematin domain. The bar represents the region of the molecule used as bait in a two-hybrid screen. B) UNC-115 co-immunoprecipitated with MYC-tagged RACK-1. Lysates of worms expressing MYC-tagged RACK-1 were used in immunoprecipitation experiments with and without anti-Myc antibody. Western blots using anti-UNC-115 antibody <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1001215#pgen.1001215-Yang1\" target=\"_blank\">[26]</a> (top) showed that UNC-115 co-immunoprecipitated with RACK-1::MYC. Western blots using anti-Myc showed that RACK-1::MYC was expressed (input) and was immunoprecipitated. RACK-1::MYC ran just below the Ig heavy chain of the anti-Myc antibody used in the immunoprecipitation. C) The <i>rack-1</i> gene and <i>tm2262</i> allele. This model is based on the K07D7.1 gene model in Wormbase and on the cDNAs sequenced from the two-hybrid screen. <i>tm2262</i> is a 331-bp deletion. (D) Schematic diagram of the 325-residue RACK-1 protein. WD  =  WD repeat; PKC  =  conserved protein kinase C interaction sites; Y =  conserved tyrosine phosphorylated by Src in mammalian RACK. The region removed by the <i>tm2262</i> deletion is indicated. E) Sequence of the <i>rack-1</i> cDNA and protein. <u>cDNA sequence:</u> The sequence of the RACK-1 cDNA is based upon sequencing seven cDNAs isolated from the two-hybrid screen and on cDNA sequences in Wormbase. The predicted open reading frame is upper case, and the 5′ and 3′ untranslated regions are lower case. A predicted poly-A addition site is underlined, and poly A residues are present in the cDNAs at the end of the sequence shown here. The nucleotides removed by the <i>tm2262</i> deletion are shaded in grey. The starting points of the five independent cDNAs isolated in the two-hybrid screen are highlighted in black. <u>Amino acid sequence:</u> The predicted amino acid sequence is shown below the cDNA sequence. The WD repeats are underlined; the two conserved PKC interaction sites are highlighted in black; and the conserved tyrosine residue that is phosphorylated by Src in mammalian RACK is highlighted in black.</p>", "links"=>[], "tags"=>["unc-115", "two-hybrid"], "article_id"=>487225, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Rafael S. Demarco", "Erik A. Lundquist"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1001215.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RACK_1_and_UNC_115_interact_by_two_hybrid_and_co_immunoprecipitation_/487225", "title"=>"RACK-1 and UNC-115 interact by two-hybrid and co-immunoprecipitation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 22:13:20"}

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