A Src-Tks5 Pathway Is Required for Neural Crest Cell Migration during Embryonic Development
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{"title"=>"A Src-Tks5 pathway is required for neural crest cell migration during embryonic development", "type"=>"journal", "authors"=>[{"first_name"=>"Danielle A.", "last_name"=>"Murphy", "scopus_author_id"=>"13611320500"}, {"first_name"=>"Begoña", "last_name"=>"Diaz", "scopus_author_id"=>"7005296576"}, {"first_name"=>"Paul A.", "last_name"=>"Bromann", "scopus_author_id"=>"6507763276"}, {"first_name"=>"Jeff H.", "last_name"=>"Tsai", "scopus_author_id"=>"7403610597"}, {"first_name"=>"Yasuhiko", "last_name"=>"Kawakami", "scopus_author_id"=>"35449731500"}, {"first_name"=>"Jochen", "last_name"=>"Maurer", "scopus_author_id"=>"7202735497"}, {"first_name"=>"Rodney A.", "last_name"=>"Stewart", "scopus_author_id"=>"7402706089"}, {"first_name"=>"Juan Carlos", "last_name"=>"Izpisúa-Belmonte", "scopus_author_id"=>"7005080486"}, {"first_name"=>"Sara A.", "last_name"=>"Courtneidge", "scopus_author_id"=>"7005085644"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"362208636", "sgr"=>"79960734896", "issn"=>"19326203", "pmid"=>"21799874", "scopus"=>"2-s2.0-79960734896", "doi"=>"10.1371/journal.pone.0022499"}, "id"=>"bc6f6241-6ae2-3649-bd2f-dc2f3f8b5c11", "abstract"=>"In the adult organism, cell migration is required for physiological processes such as angiogenesis and immune surveillance, as well as pathological events such as tumor metastasis. The adaptor protein and Src substrate Tks5 is necessary for cancer cell migration through extracellular matrix in vitro and tumorigenicity in vivo. However, a role for Tks5 during embryonic development, where cell migration is essential, has not been examined. We used morpholinos to reduce Tks5 expression in zebrafish embryos, and observed developmental defects, most prominently in neural crest-derived tissues such as craniofacial structures and pigmentation. The Tks5 morphant phenotype was rescued by expression of mammalian Tks5, but not by a variant of Tks5 in which the Src phosphorylation sites have been mutated. We further evaluated the role of Tks5 in neural crest cells and neural crest-derived tissues and found that loss of Tks5 impaired their ventral migration. Inhibition of Src family kinases also led to abnormal ventral patterning of neural crest cells and their derivatives. We confirmed that these effects were likely to be cell autonomous by shRNA-mediated knockdown of Tks5 in a murine neural crest stem cell line. Tks5 was required for neural crest cell migration in vitro, and both Src and Tks5 were required for the formation of actin-rich structures with similarity to podosomes. Additionally, we observed that neural crest cells formed Src-Tks5-dependent cell protrusions in 3-D culture conditions and in vivo. These results reveal an important and novel role for the Src-Tks5 pathway in neural crest cell migration during embryonic development. Furthermore, our data suggests that this pathway regulates neural crest cell migration through the generation of actin-rich pro-migratory structures, implying that similar mechanisms are used to control cell migration during embryogenesis and cancer metastasis.", "link"=>"http://www.mendeley.com/research/srctks5-pathway-required-neural-crest-cell-migration-during-embryonic-development-4", "reader_count"=>38, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>10, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>3, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>10, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>3, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Materials Science"=>1, "Agricultural and Biological Sciences"=>17, "Medicine and Dentistry"=>6, "Neuroscience"=>2, "Physics and Astronomy"=>1, "Chemistry"=>1, "Psychology"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Neuroscience"=>{"Neuroscience"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Belgium"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/379012", "https://ndownloader.figshare.com/files/379046", "https://ndownloader.figshare.com/files/379078", "https://ndownloader.figshare.com/files/379121", "https://ndownloader.figshare.com/files/379164", "https://ndownloader.figshare.com/files/379200", "https://ndownloader.figshare.com/files/379232"], "description"=>"<div><p>In the adult organism, cell migration is required for physiological processes such as angiogenesis and immune surveillance, as well as pathological events such as tumor metastasis. The adaptor protein and Src substrate Tks5 is necessary for cancer cell migration through extracellular matrix in vitro and tumorigenicity in vivo. However, a role for Tks5 during embryonic development, where cell migration is essential, has not been examined. We used morpholinos to reduce Tks5 expression in zebrafish embryos, and observed developmental defects, most prominently in neural crest-derived tissues such as craniofacial structures and pigmentation. The Tks5 morphant phenotype was rescued by expression of mammalian Tks5, but not by a variant of Tks5 in which the Src phosphorylation sites have been mutated. We further evaluated the role of Tks5 in neural crest cells and neural crest-derived tissues and found that loss of Tks5 impaired their ventral migration. Inhibition of Src family kinases also led to abnormal ventral patterning of neural crest cells and their derivatives. We confirmed that these effects were likely to be cell autonomous by shRNA-mediated knockdown of Tks5 in a murine neural crest stem cell line. Tks5 was required for neural crest cell migration in vitro, and both Src and Tks5 were required for the formation of actin-rich structures with similarity to podosomes. Additionally, we observed that neural crest cells formed Src-Tks5-dependent cell protrusions in 3-D culture conditions and in vivo. These results reveal an important and novel role for the Src-Tks5 pathway in neural crest cell migration during embryonic development. Furthermore, our data suggests that this pathway regulates neural crest cell migration through the generation of actin-rich pro-migratory structures, implying that similar mechanisms are used to control cell migration during embryogenesis and cancer metastasis.</p> </div>", "links"=>[], "tags"=>["src-tks5", "pathway", "neural", "crest", "embryonic"], "article_id"=>134900, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Danielle A. Murphy", "Begoña Diaz", "Paul A. Bromann", "Jeff H. Tsai", "Yasuhiko Kawakami", "Jochen Maurer", "Rodney A. Stewart", "Juan Carlos Izpisúa-Belmonte", "Sara A. Courtneidge"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0022499.s001", "https://dx.doi.org/10.1371/journal.pone.0022499.s002", "https://dx.doi.org/10.1371/journal.pone.0022499.s003", "https://dx.doi.org/10.1371/journal.pone.0022499.s004", "https://dx.doi.org/10.1371/journal.pone.0022499.s005", "https://dx.doi.org/10.1371/journal.pone.0022499.s006", "https://dx.doi.org/10.1371/journal.pone.0022499.s007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Src_Tks5_Pathway_Is_Required_for_Neural_Crest_Cell_Migration_during_Embryonic_Development/134900", "title"=>"A Src-Tks5 Pathway Is Required for Neural Crest Cell Migration during Embryonic Development", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-07-25 01:21:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/752645"], "description"=>"<p>(A) Schematic of Tks5 targeted morpholinos (MO) and the zebrafish Tks5 gene. (B) The morphology of Tks5 morphants (T5.1 MO+p53 MO) at 48 hpf compared to controls (Uninjected, Control MO, p53 MO). Enlarged images of the tail region show a reduction in posterior pigment cells (dashes outline tail in morphants). Scale bar represents 200 µm. (C) Tks5 MO specificity was determined by injecting embryos with either <i>tks5</i>:GFP mRNA or <i>tks5:</i>GFP mRNA together with Tks5 MO, and analyzing GFP expression. Two representative embryos from each injection are shown. (D) Quantification of murine Tks5 rescue of Tks5 morphant phenotypes. Embryos were injected as indicated in Experimental Procedures. The total number of morphants (white bars) was compared to the total number of normal embryos (black bars), and quantified as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022499#s4\" target=\"_blank\">Materials and Methods</a> (n = 3).</p>", "links"=>[], "tags"=>["embryonic"], "article_id"=>423014, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Danielle A. Murphy", "Begoña Diaz", "Paul A. Bromann", "Jeff H. Tsai", "Yasuhiko Kawakami", "Jochen Maurer", "Rodney A. Stewart", "Juan Carlos Izpisúa-Belmonte", "Sara A. Courtneidge"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0022499.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tks5_is_required_for_embryonic_development_in_Danio_rerio_/423014", "title"=>"Tks5 is required for embryonic development in <i>Danio rerio</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-25 00:50:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/752830"], "description"=>"<p>(A–B) Melanophores within the trunk region above the yolk sac extension in control MO-injected and Tks5 MO-injected embryos were qualitatively (A) and quantitatively (B) analyzed. n = 15 embryos and SEM is shown by bar. p values obtained from Student's t-test. ** denotes p<0.01. (C) Melanophores present in the dorsal, ventral, and lateral pigment lines were quantified to determine degree of murine Tks5 rescue of the decreased pigmentation seen in morphants. Mean values (n = 3) and SEM are shown in graph. p values obtained from Student's t-test. ** denotes p<0.01. (D) Alcian blue staining was performed on indicated embryos to identify craniofacial structures (Meckel's cartilage (mc), palatoquadrate (pq), ceratobranchials (ch), ethmoid plate (ep)). (*) denotes missing structures. (E) Alcian blue staining was performed on indicated embryos to determine if murine Tks5 could rescue craniofacial defects seen in morphants. Structures were identified as in (D). (*) denotes missing structures.</p>", "links"=>[], "tags"=>["tks5", "neural", "crest-derived"], "article_id"=>423199, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Danielle A. Murphy", "Begoña Diaz", "Paul A. Bromann", "Jeff H. Tsai", "Yasuhiko Kawakami", "Jochen Maurer", "Rodney A. Stewart", "Juan Carlos Izpisúa-Belmonte", "Sara A. Courtneidge"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0022499.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Decreased_Tks5_expression_results_in_neural_crest_derived_defects_/423199", "title"=>"Decreased Tks5 expression results in neural crest-derived defects.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-25 00:53:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/752999"], "description"=>"<p>(A–B) Whole mount in situ hybridizations to detect neural crest cells were performed on control (Tks5 MM) and Tks5 morphant (Tks5 MO) embryos at 26 hpf. (A) Neural crest specific riboprobes against <i>foxd3</i>, <i>sox10</i>, and <i>crestin</i> (ctn) were used. Bars indicate anterior-posterior area of migrating cells. (*) indicates an increase in pre-migratory cells compared to controls (B) The number of cells migrating into the trunk region was quantified as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022499#s4\" target=\"_blank\">Materials and Methods</a>. Mean values (n = 18) and SEM were shown in graph. p values obtained from Student's t-test. ** denotes p<0.01. (C) Control (T5 MM) and Tks5 morphant (T5 MO) Tg(<i>sox10</i>:RFP) embryos (28 hpf) were incubated with acridine orange as a marker for apoptosis and imaged by fluorescence microscopy. NC = neural crest cells, AO = acridine orange, brackets designate similar regions of migrating NC cells, and boxes label similarly positioned individual NC cells in the control and morphant embryos (enlarged in bottom left corner of top panel). (D) Control (T5 MM) and Tks5 morphant (T5 MO) Tg(<i>sox10</i>:RFP) embryos (30 hpf) were analyzed for neural crest migration by confocal time-lapse microscopy for 1.5 hours as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022499#s4\" target=\"_blank\">Materials and Methods</a>. Arrows follow ventral cell migration of an individual cell over the duration. * = protrusions emanating from neural crest cells (D = dorsal, V = ventral, A = anterior, P = posterior). (E) The average velocities of individual neural crest (NC) cells for control (T5 MM)-, Tks5 MO-injected, Tks5myc RNA and Tks5 MO co-injected, or Tks5FFmyc RNA and Tks5 MO co-injected Tg(<i>sox10</i>:RFP) embryos were quantified as detailed in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022499#s4\" target=\"_blank\">Materials and Methods</a>. Mean values (n = 10) and SEM are shown. p values obtained from Student's t-test.** denotes p<0.01.</p>", "links"=>[], "tags"=>["crest", "vivo", "requires"], "article_id"=>423364, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Danielle A. Murphy", "Begoña Diaz", "Paul A. Bromann", "Jeff H. Tsai", "Yasuhiko Kawakami", "Jochen Maurer", "Rodney A. Stewart", "Juan Carlos Izpisúa-Belmonte", "Sara A. Courtneidge"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0022499.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Neural_crest_migration_in_vivo_requires_Tks5_/423364", "title"=>"Neural crest migration in vivo requires Tks5.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-25 00:56:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/753146"], "description"=>"<p>(A) Tg(<i>sox10:</i>RFP) embryos (8 hpf) were treated with either vehicle (DMSO) or SU6656 for 24 hours and imaged by confocal microscopy to detect neural crest cells. (D = dorsal, V = ventral). Brackets indicate the position of the somites. Scale bar represents 50 µm. (B–C) Embryos at 15 hpf were treated as indicated for 24 hours and analyzed for pigmentation defects. (B) Embryos where treatment was initiated at 15 hpf were examined for melanophore patterning in the trunk region above the yolk sac extension. (D = dorsal, V = ventral, A = anterior, P = posterior) (C) The total number of melanophores present in the dorsal and ventral pigment lines was counted for embryos within each group as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022499#s4\" target=\"_blank\">Materials and Methods</a>. Mean values (n = 3) and SEM were shown in graph. ** denotes p<0.01 for vehicle treated vs. SFK treated comparison. (D–E) Embryos were injected as indicated and qualitatively analyzed for defects described previously. Morpholino and RNA concentrations detailed in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022499#s4\" target=\"_blank\">Materials and Methods</a>. (E) Morphants were identified as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022499#pone-0022499-g001\" target=\"_blank\">Figure 1D</a> and embryos within each group were quantified (white = morphants, black = normal).</p>", "links"=>[], "tags"=>["crest", "derivatives", "src-tks5-dependent", "pathway"], "article_id"=>423508, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Danielle A. Murphy", "Begoña Diaz", "Paul A. Bromann", "Jeff H. Tsai", "Yasuhiko Kawakami", "Jochen Maurer", "Rodney A. Stewart", "Juan Carlos Izpisúa-Belmonte", "Sara A. Courtneidge"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0022499.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Neural_crest_derivatives_require_a_Src_Tks5_dependent_pathway_in_vivo_/423508", "title"=>"Neural crest derivatives require a Src-Tks5-dependent pathway in vivo.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-25 00:58:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/753354"], "description"=>"<p>(A–B) Control (Scr) and Tks5 knockdown (shT5.1 and shT5.2) JOMA1.3 cells were exposed to a TGFβ gradient using the transwell migration assay. The number of migrating cells was qualitatively analyzed in each group (A) and quantified as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022499#s4\" target=\"_blank\">Materials and Methods</a> (B). Mean values (n = 3) and SEM were shown in graph. ** denotes p<0.01. (C) TGFβ-stimulated (25 ng/ml) JOMA1.3 cells were immunostained for F-actin (using phalloidin) and the podosome markers cortactin, Arp2/3, and Tks5 to identify formation of podosomes (arrows). In all cases, scale bars represent 10 µm and white arrows point to clusters of podosomes. (D) Confocal microscopy of TGFβ-stimulated JOMA1.3 cells co-stained for F-actin (using phalloidin) and cortactin. (E) JOMA 1.3 cells were treated with TGF-β and stained for SMAD2 by immunofluorescence to confirm activation of TGF-β-dependent pathways. (F–G) Vehicle (DMSO) or SFK inhibitors (SU6656 and PP2) were added to JOMA1.3 cells prior to TGF-β stimulation followed by analysis of podosome formation by immunostaining for F-actin (phalloidin) and cortactin (arrows). (G) The total number of cells with podosomes was quantified for each treatment group and analyzed as fold change of cells with podosomes compared to untreated cells. Fold change of cells was compared to vehicle treated cells. Mean values (n = 3) and SEM were shown in graph. ** denotes p<0.01 for vehicle vs. SFK treated comparison. (H–J) Tks5 was knocked-down in JOMA1.3 cells by two independent shRNA constructs [shTks5.1 (shT5.1), shTks5.2 (shT5.2)]. (H) Untreated, control (scrambled shRNA), and Tks5 knockdown cells were stimulated with TGFβ for 5 hours and stained for F-actin and cortactin to identify podosomes. (I) The percentage of cells with podosomes was quantified (as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022499#s4\" target=\"_blank\">Materials and Methods</a>. Mean values (n = 3) and SEM are shown. p values obtained from Student's t-test. ** denotes p<0.01. (J) Tks5 knockdown was confirmed by immunoblot analysis for Tks5 using whole cell lysates and anti-Tks5 antibody. Protein levels were normalized to tubulin.</p>", "links"=>[], "tags"=>["podosome", "neural", "crest", "cells", "requires"], "article_id"=>423717, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Danielle A. Murphy", "Begoña Diaz", "Paul A. Bromann", "Jeff H. Tsai", "Yasuhiko Kawakami", "Jochen Maurer", "Rodney A. Stewart", "Juan Carlos Izpisúa-Belmonte", "Sara A. Courtneidge"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0022499.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Migration_of_and_podosome_formation_in_neural_crest_stem_cells_requires_Tks5_/423717", "title"=>"Migration of, and podosome formation in, neural crest stem cells requires Tks5.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-25 01:01:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/753528"], "description"=>"<p>(A) Control (scrambled) and Tks5 knocked-down (shT5.2) JOMA1.3 cells were placed in a three-dimensional collagen matrix and cultured for six days. Cells embedded in the collagen matrix were stained for F-actin (phalloidin) and analyzed for differences in cell structure (40×). (B) Neural crest cell and neural crest-derived cell protrusions were qualitatively examined by either enlarging images of neural crest cells in Tg(<i>sox10:</i>RFP) embryos obtained in 4A (left panels) or imaging melanophores in vehicle or SU6656 treated embryos at a higher magnification (23×) (right panels). (C) Control (Tks5 MM injected) and Tks5 morphant Tg(<i>foxd3</i>:GFP) embryos (30 hpf) were fixed and imaged by confocal microscopy. The width and length of protrusions was measured by Volocity software. Mean values (n = 20) and SEM are shown. p values obtained from Student's t-test. ** denotes p<0.01. (D = dorsal, V = ventral, A = anterior, P = posterior).</p>", "links"=>[], "tags"=>["tks5-dependent", "neural", "crest", "dendritic-like", "protrusions", "3-d"], "article_id"=>423891, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Danielle A. Murphy", "Begoña Diaz", "Paul A. Bromann", "Jeff H. Tsai", "Yasuhiko Kawakami", "Jochen Maurer", "Rodney A. Stewart", "Juan Carlos Izpisúa-Belmonte", "Sara A. Courtneidge"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0022499.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Src_and_Tks5_dependent_neural_crest_cell_dendritic_like_protrusions_in_3_D_culture_and_in_vivo_/423891", "title"=>"Src- and Tks5-dependent neural crest cell dendritic-like protrusions in 3-D culture and in vivo.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-25 01:04:51"}

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