NEDD9 Stabilizes Focal Adhesions, Increases Binding to the Extra-Cellular Matrix and Differentially Effects 2D versus 3D Cell Migration
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{"title"=>"NEDD9 stabilizes focal adhesions, increases binding to the extra-cellular matrix and differentially effects 2D versus 3D cell migration", "type"=>"journal", "authors"=>[{"first_name"=>"Jessie", "last_name"=>"Zhong", "scopus_author_id"=>"25937008100"}, {"first_name"=>"Jaime B.", "last_name"=>"Baquiran", "scopus_author_id"=>"55180674500"}, {"first_name"=>"Navid", "last_name"=>"Bonakdar", "scopus_author_id"=>"30267449700"}, {"first_name"=>"Justin", "last_name"=>"Lees", "scopus_author_id"=>"9536747100"}, {"first_name"=>"Yu Wooi", "last_name"=>"Ching", "scopus_author_id"=>"55180025000"}, {"first_name"=>"Elena", "last_name"=>"Pugacheva", "scopus_author_id"=>"6603966187"}, {"first_name"=>"Ben", "last_name"=>"Fabry", "scopus_author_id"=>"57192109935"}, {"first_name"=>"Geraldine M.", "last_name"=>"O'Neill", "scopus_author_id"=>"7102253884"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84859563279", "doi"=>"10.1371/journal.pone.0035058", "issn"=>"19326203", "pui"=>"364606639", "sgr"=>"84859563279", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"22509381"}, "id"=>"a3d73d02-60df-3714-9e36-ecd3c2f55c55", "abstract"=>"The speed of cell migration on 2-dimensional (2D) surfaces is determined by the rate of assembly and disassembly of clustered integrin receptors known as focal adhesions. Different modes of cell migration that have been described in 3D environments are distinguished by their dependence on integrin-mediated interactions with the extra-cellular matrix. In particular, the mesenchymal invasion mode is the most dependent on focal adhesion dynamics. The focal adhesion protein NEDD9 is a key signalling intermediary in mesenchymal cell migration, however whether NEDD9 plays a role in regulating focal adhesion dynamics has not previously been reported. As NEDD9 effects on 2D migration speed appear to depend on the cell type examined, in the present study we have used mouse embryo fibroblasts (MEFs) from mice in which the NEDD9 gene has been depleted (NEDD9 −/− MEFs). This allows comparison with effects of other focal adhesion proteins that have previously been demonstrated using MEFs. We show that focal adhesion disassembly rates are increased in the absence of NEDD9 expression and this is correlated with increased paxillin phosphorylation at focal adhesions. NEDD9−/− MEFs have increased rates of migration on 2D surfaces, but conversely, migration of these cells is significantly reduced in 3D collagen gels. Importantly we show that myosin light chain kinase is activated in 3D in the absence of NEDD9 and is conversely inhibited in 2D cultures. Measurement of adhesion strength reveals that NEDD9−/− MEFs have decreased adhesion to fibronectin, despite upregulated α5β1 fibronectin receptor expression. We find that β1 integrin activation is significantly suppressed in the NEDD9−/−, suggesting that in the absence of NEDD9 there is decreased integrin receptor activation. Collectively our data suggest that NEDD9 may promote 3D cell migration by slowing focal adhesion disassembly, promoting integrin receptor activation and increasing adhesion force to the ECM.", "link"=>"http://www.mendeley.com/research/nedd9-stabilizes-focal-adhesions-increases-binding-extracellular-matrix-differentially-effects-2d-ve", "reader_count"=>41, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>2, "Student > Bachelor"=>3, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. 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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/336482"], "description"=>"<div><p>The speed of cell migration on 2-dimensional (2D) surfaces is determined by the rate of assembly and disassembly of clustered integrin receptors known as focal adhesions. Different modes of cell migration that have been described in 3D environments are distinguished by their dependence on integrin-mediated interactions with the extra-cellular matrix. In particular, the mesenchymal invasion mode is the most dependent on focal adhesion dynamics. The focal adhesion protein NEDD9 is a key signalling intermediary in mesenchymal cell migration, however whether NEDD9 plays a role in regulating focal adhesion dynamics has not previously been reported. As NEDD9 effects on 2D migration speed appear to depend on the cell type examined, in the present study we have used mouse embryo fibroblasts (MEFs) from mice in which the NEDD9 gene has been depleted (NEDD9 −/− MEFs). This allows comparison with effects of other focal adhesion proteins that have previously been demonstrated using MEFs. We show that focal adhesion disassembly rates are increased in the absence of NEDD9 expression and this is correlated with increased paxillin phosphorylation at focal adhesions. NEDD9−/− MEFs have increased rates of migration on 2D surfaces, but conversely, migration of these cells is significantly reduced in 3D collagen gels. Importantly we show that myosin light chain kinase is activated in 3D in the absence of NEDD9 and is conversely inhibited in 2D cultures. Measurement of adhesion strength reveals that NEDD9−/− MEFs have decreased adhesion to fibronectin, despite upregulated α5β1 fibronectin receptor expression. We find that β1 integrin activation is significantly suppressed in the NEDD9−/−, suggesting that in the absence of NEDD9 there is decreased integrin receptor activation. Collectively our data suggest that NEDD9 may promote 3D cell migration by slowing focal adhesion disassembly, promoting integrin receptor activation and increasing adhesion force to the ECM.</p> </div>", "links"=>[], "tags"=>["nedd9", "stabilizes", "focal", "increases", "binding", "extra-cellular", "matrix", "differentially", "effects", "2d", "3d"], "article_id"=>126494, "categories"=>["Biochemistry", "Cell Biology"], "users"=>["Jessie Zhong", "Jaime B. Baquiran", "Navid Bonakdar", "Justin Lees", "Yu Wooi Ching", "Elena Pugacheva", "Ben Fabry", "Geraldine M. O'Neill"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0035058"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/NEDD9_Stabilizes_Focal_Adhesions_Increases_Binding_to_the_Extra_Cellular_Matrix_and_Differentially_Effects_2D_versus_3D_Cell_Migration/126494", "title"=>"NEDD9 Stabilizes Focal Adhesions, Increases Binding to the Extra-Cellular Matrix and Differentially Effects 2D versus 3D Cell Migration", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-11 01:48:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/657187"], "description"=>"<p>A. Western blot analysis of extracts of wild-type (WT) and NEDD9 knockout (−/−) MEFs. Blots were probed with antibodies to NEDD9 which detects the 105 kD and 115 kD phospho-forms of NEDD9 and p130Cas antibodies as indicated. Blots were then probed with anti-tubulin or anti-HSP70 antibodies to confirm equal loading. B. WT and NEDD9 −/− MEFs immunostained with antibodies to paxillin (pax) to detect focal adhesions (white arrows) and TRITC-phalloidin to detect actin stress fibres. C. Examples of YFP-paxillin positive focal adhesions in transfected WT (72 minute lifetime) and NEDD9−/− MEFs (52 minute lifetime) are shown. D. Focal adhesion assembly rate constants (<i>k</i>) for cells transfected with YFP-paxillin (n = 32 focal adhesions per cell line). Horizontal bars show the average value per cell line. E. As for D, except data showing the disassembly rate constants (<i>k</i>). (WT n = 26, −/− n = 33). *p<0.01, N.S. = not significant.</p>", "links"=>[], "tags"=>["adhesion", "turnover", "nedd9"], "article_id"=>327665, "categories"=>["Biochemistry", "Cell Biology"], "users"=>["Jessie Zhong", "Jaime B. Baquiran", "Navid Bonakdar", "Justin Lees", "Yu Wooi Ching", "Elena Pugacheva", "Ben Fabry", "Geraldine M. O'Neill"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0035058.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Focal_adhesion_turnover_is_more_rapid_in_the_absence_of_NEDD9_expression_/327665", "title"=>"Focal adhesion turnover is more rapid in the absence of NEDD9 expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-11 02:07:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/657280"], "description"=>"<p>A. Paxillin (pax) and phospho-paxillin (ppax) immunostaining. Merged images show colour overlays of paxillin (green) and phospho-paxillin (red). Right hand panels show ratio images of paxillin phosphorylation. Red hues reflect regions of highest phosphorylated paxillin. Boxed insets shows magnified focal adhesions. B. Ratio of phosphorylated paxillin at focal adhesions in WT (n = 197 from 10 individual cells) and NEDD9 −/− MEFs (n = 201 from 10 individual cells). ***p<0.0001, Students' <i>t</i>-test.</p>", "links"=>[], "tags"=>["phosphorylation", "nedd9"], "article_id"=>327763, "categories"=>["Biochemistry", "Cell Biology"], "users"=>["Jessie Zhong", "Jaime B. Baquiran", "Navid Bonakdar", "Justin Lees", "Yu Wooi Ching", "Elena Pugacheva", "Ben Fabry", "Geraldine M. O'Neill"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0035058.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Paxillin_phosphorylation_is_increased_in_NEDD9_8722_8722_MEFs_/327763", "title"=>"Paxillin phosphorylation is increased in NEDD9 −/− MEFs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-11 02:09:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/657386"], "description"=>"<p>A. MSD calculated from trajectories of WT (black squares), and NEDD9−/− (white squares) MEFs in 2D cell migration assays. Data are the average values from 3 independent experiments, n>45 cells tracked per experiment. B. Cell speed is significantly increased in NEDD9−/− MEFs (WT n = 150, −/− n = 143). C. MSD calculated from the trajectories of GFP-transfected NEDD9−/− MEFs (black squares) and GFP.NEDD9 transfected NEDD9−/− MEFs (white squares). D. GFP.NEDD9 expression significantly reduces the migration speed of NEDD9−/− MEFs. (n = 53 each). *** <i>p</i><0.0001, Students' <i>t</i>-test.</p>", "links"=>[], "tags"=>["mefs", "2d"], "article_id"=>327866, "categories"=>["Biochemistry", "Cell Biology"], "users"=>["Jessie Zhong", "Jaime B. Baquiran", "Navid Bonakdar", "Justin Lees", "Yu Wooi Ching", "Elena Pugacheva", "Ben Fabry", "Geraldine M. O'Neill"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0035058.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NEDD9_8722_8722_MEFs_have_increased_migration_speed_in_2D_cell_migration_assays_/327866", "title"=>"NEDD9 −/− MEFs have increased migration speed in 2D cell migration assays.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-11 02:11:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/657460"], "description"=>"<p>A. Western blot analysis of cell extracts following treatment with siRNA targeting NEDD9 or control siRNA sequences. Blots were probed with antibodies to NEDD9 which detects 105 kD and 115 kD NEDD9 phospho-forms and cross-reacted with p130Cas as indicated. Probing with anti-tubulin antibodies confirmed equal loading. B. MSD calculated from trajectories of WT MEFs (black squares, average of 3 independent experiments), NEDD9−/− MEFs (white squares, average of 3 independent experiments n>22 cells per experiment), MEFs treated with control siRNA (black circles, average of n = 38 cells) and NEDD9 siRNA (white circles, average of n = 25 cells). Note that identical values were obtained for the WT MEFs and WT MEFs treated with control siRNA; these data points are therefore super-imposed on the graph. C. Cell speed is significantly reduced in NEDD9−/− MEFs and in NEDD9 siRNA treated cells relative to the matched controls. Horizontal bars indicate the average speed for all cells tracked. D. Cell persistence is significantly reduced in NEDD9−/− and NEDD9 siRNA treated MEFs. Histogram shows the average persistence for all cells tracked. *<i>p</i><0.05, ** <i>p</i><0.001, *** <i>p</i><0.0001, Students' <i>t</i>-test.</p>", "links"=>[], "tags"=>["increases", "3d"], "article_id"=>327943, "categories"=>["Biochemistry", "Cell Biology"], "users"=>["Jessie Zhong", "Jaime B. Baquiran", "Navid Bonakdar", "Justin Lees", "Yu Wooi Ching", "Elena Pugacheva", "Ben Fabry", "Geraldine M. O'Neill"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0035058.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NEDD9_increases_3D_migration_speed_/327943", "title"=>"NEDD9 increases 3D migration speed.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-11 02:12:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/657533"], "description"=>"<p>A. Western blot analysis of lysates extracted from WT MEF and NEDD9−/− MEF grown on tissue culture plastic dishes (2D) or in collagen gels (3D). Blots were probed with the indicated antibodies to total proteins and phosphorylated proteins (-p-). Note that total Src was immunoprecipitated (IP) prior to probing with anti-p-Src antibodies. Blots were probed with Hsp70 or tubulin as a loading control. B. Histograms showing densitometric measurements of the level of phosphorylated protein divided by the matching total protein amount and expressed relative to the level in WT MEFs under 2D culture conditions. Data represent the average of triplicate repeats on separate days and error bars show the S.E.M. *<i>p</i><0.05, ** <i>p</i><0.001, NS = not significant, Students' <i>t</i>-test.</p>", "links"=>[], "tags"=>["signalling", "pathways", "differentially", "activated", "2d"], "article_id"=>328013, "categories"=>["Biochemistry", "Cell Biology"], "users"=>["Jessie Zhong", "Jaime B. Baquiran", "Navid Bonakdar", "Justin Lees", "Yu Wooi Ching", "Elena Pugacheva", "Ben Fabry", "Geraldine M. O'Neill"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0035058.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Adhesion_signalling_pathways_are_differentially_activated_in_2D_versus_3D_/328013", "title"=>"Adhesion signalling pathways are differentially activated in 2D versus 3D.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-11 02:13:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/657683"], "description"=>"<p>A. Time-lapse series of WT and NEDD9−/− MEFs showing cellular morphologies in 3D collagen gels. B. Percentage of cells exhibiting a rounded phenotype. ** <i>p</i><0.001, Students' <i>t</i>-test. C. Mitotic events are decreased in NEDD9−/− fibroblasts. The number of cells observed to undergo mitosis in 3D collagen gels during 6 hours of filming were quantified and expressed as a percentage of the total cells analysed. Data shown are the average of two independent experiments.</p>", "links"=>[], "tags"=>["mefs", "rounded"], "article_id"=>328166, "categories"=>["Biochemistry", "Cell Biology"], "users"=>["Jessie Zhong", "Jaime B. Baquiran", "Navid Bonakdar", "Justin Lees", "Yu Wooi Ching", "Elena Pugacheva", "Ben Fabry", "Geraldine M. O'Neill"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0035058.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NEDD9_8722_8722_MEFs_adopt_a_rounded_morphology_/328166", "title"=>"NEDD9 −/− MEFs adopt a rounded morphology.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-11 02:16:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/657766"], "description"=>"<p>A. Surface expression of α5β1 determined by FACs analysis in WT (grey) and NEDD9 −/− (white) MEFs. B. α5β1 distribution in cells grown under 2D conditions. Arrows point to α5β1-positive focal adhesions. C. Fibronectin (FN) staining and Differential Interference Contrast (DIC) images of WT and −/− cells in 3D collagen gels. D. Fraction of detached fibronectin-coated beads versus pulling force. Adhesion strength was lower in NEDD9−/− MEFs (<i>grey circles</i>, n = 91) compared with WT MEFs (<i>black circles</i>, n = 103). E. The level of activated β1 (detected using β1 antibody clone 9EG7) normalized to α5β1 and expressed as fold change relative to the WT control. FACs data are the average ± SEM from 5 experiments repeated on separate days. * <i>p</i><0.05, *** <i>p</i><0.001, Students' <i>t</i>-test.</p>", "links"=>[], "tags"=>["cell biology", "Biochemistry"], "article_id"=>328248, "categories"=>["Biochemistry", "Cell Biology"], "users"=>["Jessie Zhong", "Jaime B. Baquiran", "Navid Bonakdar", "Justin Lees", "Yu Wooi Ching", "Elena Pugacheva", "Ben Fabry", "Geraldine M. O'Neill"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0035058.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Adhesion_strength_is_decreased_in_NEDD9_8722_8722_MEFs_/328248", "title"=>"Adhesion strength is decreased in NEDD9−/− MEFs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-11 02:17:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/657867"], "description"=>"<p>A. Activated β1 integrin (detected using β1 antibody clone 9EG7) and actin (detected with fluorescently-tagged phalloidin) immunostaining of cells grown in 2D conditions. Merged images show colour overlays of β1 (green) and actin (red). Arrows point to examples of active β1 integrin associated with the ends of actin stress fibres. Cells were imaged by wide-field microscopy. B. Activated β1 integrin and actin immunostaining of cells grown in 3D collagen gels. Boxed insets shows magnified regions containing actin stress fibres. Arrow heads point to actin stress fibres. Images represent single confocal z-slices.</p>", "links"=>[], "tags"=>["fibres", "activated", "mefs"], "article_id"=>328352, "categories"=>["Biochemistry", "Cell Biology"], "users"=>["Jessie Zhong", "Jaime B. Baquiran", "Navid Bonakdar", "Justin Lees", "Yu Wooi Ching", "Elena Pugacheva", "Ben Fabry", "Geraldine M. O'Neill"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0035058.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reduced_stress_fibres_and_activated_946_1_in_NEDD9_8722_8722_MEFs_in_3D_/328352", "title"=>"Reduced stress fibres and activated β1 in NEDD9−/− MEFs in 3D.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-11 02:19:12"}

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