Matrix-Bound PAI-1 Supports Cell Blebbing via RhoA/ROCK1 Signaling
Publication Date
February 21, 2012
Journal
PLOS ONE
Authors
Amandine Cartier Michaud, Michel Malo, Cécile Charrière Bertrand, Gilles Gadea, et al
Volume
7
Issue
2
Pages
e32204
DOI
https://dx.plos.org/10.1371/journal.pone.0032204
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0032204
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22363817
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3283740
Europe PMC
http://europepmc.org/abstract/MED/22363817
Web of Science
000302873700158
Scopus
84857395728
Mendeley
http://www.mendeley.com/research/matrixbound-pai1-supports-cell-blebbing-via-rhoarock1-signaling
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Mendeley | Further Information

{"title"=>"Matrix-bound PAI-1 supports cell blebbing via RhoA/rock1 signaling", "type"=>"journal", "authors"=>[{"first_name"=>"Amandine", "last_name"=>"Cartier-Michaud", "scopus_author_id"=>"26429171300"}, {"first_name"=>"Michel", "last_name"=>"Malo", "scopus_author_id"=>"7003586722"}, {"first_name"=>"Cécile", "last_name"=>"Charrière-Bertrand", "scopus_author_id"=>"6603650991"}, {"first_name"=>"Gilles", "last_name"=>"Gadea", "scopus_author_id"=>"6508032705"}, {"first_name"=>"Christelle", "last_name"=>"Anguille", "scopus_author_id"=>"6507576463"}, {"first_name"=>"Ajitha", "last_name"=>"Supiramaniam", "scopus_author_id"=>"55022672200"}, {"first_name"=>"Annick", "last_name"=>"Lesne", "scopus_author_id"=>"6603442852"}, {"first_name"=>"Franck", "last_name"=>"Delaplace", "scopus_author_id"=>"6506490410"}, {"first_name"=>"Guillaume", "last_name"=>"Hutzler", "scopus_author_id"=>"14021367300"}, {"first_name"=>"Pierre", "last_name"=>"Roux", "scopus_author_id"=>"35876106200"}, {"first_name"=>"Daniel A.", "last_name"=>"Lawrence", "scopus_author_id"=>"7402207276"}, {"first_name"=>"Georgia", "last_name"=>"Barlovatz-Meimon", "scopus_author_id"=>"6701674862"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"364320976", "sgr"=>"84857395728", "pmid"=>"22363817", "scopus"=>"2-s2.0-84857395728", "doi"=>"10.1371/journal.pone.0032204", "issn"=>"19326203"}, "id"=>"b2ed98b8-3e59-316c-b121-fc887cdb36e8", "abstract"=>"The microenvironment of a tumor can influence both the morphology and the behavior of cancer cells which, in turn, can rapidly adapt to environmental changes. Increasing evidence points to the involvement of amoeboid cell migration and thus of cell blebbing in the metastatic process; however, the cues that promote amoeboid cell behavior in physiological and pathological conditions have not yet been clearly identified. Plasminogen Activator Inhibitor type-1 (PAI-1) is found in high amount in the microenvironment of aggressive tumors and is considered as an independent marker of bad prognosis. Here we show by immunoblotting, activity assay and immunofluorescence that, in SW620 human colorectal cancer cells, matrix-associated PAI-1 plays a role in the cell behavior needed for amoeboid migration by maintaining cell blebbing, localizing PDK1 and ROCK1 at the cell membrane and maintaining the RhoA/ROCK1/MLC-P pathway activation. The results obtained by modeling PAI-1 deposition around tumors indicate that matrix-bound PAI-1 is heterogeneously distributed at the tumor periphery and that, at certain spots, the elevated concentrations of matrix-bound PAI-1 needed for cancer cells to undergo the mesenchymal-amoeboid transition can be observed. Matrix-bound PAI-1, as a matricellular protein, could thus represent one of the physiopathological requirements to support metastatic formation.", "link"=>"http://www.mendeley.com/research/matrixbound-pai1-supports-cell-blebbing-via-rhoarock1-signaling", "reader_count"=>20, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>5, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Student > Bachelor"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>5, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Student > Bachelor"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>3, "Medicine and Dentistry"=>2, "Agricultural and Biological Sciences"=>8, "Physics and Astronomy"=>1, "Chemistry"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>8}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"United Kingdom"=>1, "France"=>1}, "group_count"=>0}

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/347231", "https://ndownloader.figshare.com/files/347297", "https://ndownloader.figshare.com/files/347376", "https://ndownloader.figshare.com/files/347464", "https://ndownloader.figshare.com/files/347546", "https://ndownloader.figshare.com/files/347618", "https://ndownloader.figshare.com/files/347674", "https://ndownloader.figshare.com/files/347720", "https://ndownloader.figshare.com/files/347780", "https://ndownloader.figshare.com/files/347826", "https://ndownloader.figshare.com/files/347937", "https://ndownloader.figshare.com/files/348011", "https://ndownloader.figshare.com/files/348075"], "description"=>"<div><p>The microenvironment of a tumor can influence both the morphology and the behavior of cancer cells which, in turn, can rapidly adapt to environmental changes. Increasing evidence points to the involvement of amoeboid cell migration and thus of cell blebbing in the metastatic process; however, the cues that promote amoeboid cell behavior in physiological and pathological conditions have not yet been clearly identified. Plasminogen Activator Inhibitor type-1 (PAI-1) is found in high amount in the microenvironment of aggressive tumors and is considered as an independent marker of bad prognosis. Here we show by immunoblotting, activity assay and immunofluorescence that, in SW620 human colorectal cancer cells, matrix-associated PAI-1 plays a role in the cell behavior needed for amoeboid migration by maintaining cell blebbing, localizing PDK1 and ROCK1 at the cell membrane and maintaining the RhoA/ROCK1/MLC-P pathway activation. The results obtained by modeling PAI-1 deposition around tumors indicate that matrix-bound PAI-1 is heterogeneously distributed at the tumor periphery and that, at certain spots, the elevated concentrations of matrix-bound PAI-1 needed for cancer cells to undergo the mesenchymal-amoeboid transition can be observed. Matrix-bound PAI-1, as a matricellular protein, could thus represent one of the physiopathological requirements to support metastatic formation.</p> </div>", "links"=>[], "tags"=>["matrix-bound", "pai-1", "supports", "blebbing", "signaling"], "article_id"=>128649, "categories"=>["Information And Computing Sciences"], "users"=>["Amandine Cartier-Michaud", "Michel Malo", "Cécile Charrière-Bertrand", "Gilles Gadea", "Christelle Anguille", "Ajitha Supiramaniam", "Annick Lesne", "Franck Delaplace", "Guillaume Hutzler", "Pierre Roux", "Daniel A. Lawrence", "Georgia Barlovatz-Meimon"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0032204.s001", "https://dx.doi.org/10.1371/journal.pone.0032204.s002", "https://dx.doi.org/10.1371/journal.pone.0032204.s003", "https://dx.doi.org/10.1371/journal.pone.0032204.s004", "https://dx.doi.org/10.1371/journal.pone.0032204.s005", "https://dx.doi.org/10.1371/journal.pone.0032204.s006", "https://dx.doi.org/10.1371/journal.pone.0032204.s007", "https://dx.doi.org/10.1371/journal.pone.0032204.s008", "https://dx.doi.org/10.1371/journal.pone.0032204.s009", "https://dx.doi.org/10.1371/journal.pone.0032204.s010", "https://dx.doi.org/10.1371/journal.pone.0032204.s011", "https://dx.doi.org/10.1371/journal.pone.0032204.s012", "https://dx.doi.org/10.1371/journal.pone.0032204.s013"], "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Matrix_Bound_PAI_1_Supports_Cell_Blebbing_via_RhoA_ROCK1_Signaling/128649", "title"=>"Matrix-Bound PAI-1 Supports Cell Blebbing via RhoA/ROCK1 Signaling", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-02-21 02:24:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/679309"], "description"=>"<p>uPAR can interact with different types of Integrins and participates in the activation of the MEK/ERK and Rac pathways, both leading to mesenchymal migration. Active, matrix-bound PAI-1 blocks the association of Integrin and uPAR with the extracellular matrix and subsequently supports cell blebbing by activating the RhoA pathway. If only matrix-bound PAI-1 is available, as in our experimental model, the RhoA pathway is activated either through biomechanical transmission (implicating an unknown co-actor) or transduction (implicating a transmembrane receptor; altogether these events might lead to amoeboid migration.</p>", "links"=>[], "tags"=>["plasminogen", "activator", "signaling", "mesenchymal", "amoeboid"], "article_id"=>349777, "categories"=>["Information And Computing Sciences"], "users"=>["Amandine Cartier-Michaud", "Michel Malo", "Cécile Charrière-Bertrand", "Gilles Gadea", "Christelle Anguille", "Ajitha Supiramaniam", "Annick Lesne", "Franck Delaplace", "Guillaume Hutzler", "Pierre Roux", "Daniel A. Lawrence", "Georgia Barlovatz-Meimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032204.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Involvement_of_the_Plasminogen_Activator_system_in_the_signaling_to_regulate_the_transition_between_mesenchymal_and_amoeboid_migration_/349777", "title"=>"Involvement of the Plasminogen Activator system in the signaling to regulate the transition between mesenchymal and amoeboid migration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-21 02:42:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/679010"], "description"=>"<p>(<b>A</b>) Percentage of blebbing SW620 cells seeded on PAI-1 14-1b or collagen in the presence of the ROCK inhibitor Y27632 (Y27) (10 µM) at 19 h time-point after seeding. Data are the mean ± s.e.m. of three independent experiments; **: <i>P</i><0.01. (<b>B</b>) Detection of cleaved Caspase 3 by immunoblotting in SW620 cells seeded on non-coated plates (control), PAI-1 14-1b or collagen 19 h and 24 h after seeding. SW620 cells treated with 1 µM staurosporin (St.) for 24 h were used as positive control. β-Tubulin served as loading control. (<b>C</b>) RhoA activity and proportion of blebbing cells in SW620 cells seeded on PAI-1 14-1b or collagen at different time-points after seeding. Values were normalized to the effects at 3 h for each condition. Data are the mean ± s.e.m. of four independent experiments. (<b>D</b>) Quantification following immunoblotting of active RhoA relative to total RhoA in SW620 cells seeded on PAI-1 14-1b or collagen for 19 h. Data are the mean ± s.e.m. of three independent experiments; ***: <i>P</i><0.001. (<b>E</b>) Quantification following immunoblotting of phosphorylated MLC (MLC-P) relative to β-Tubulin (loading control) expression in SW620 cells seeded on PAI-1 14-1b or collagen for 19 h. Data are the mean ± s.e.m. of three independent experiments; *: <i>P</i><0.05. (<b>F</b>) Percentage of ROCK1 colocalization with PDK1 relative to total ROCK1 expression in blebbing SW620 cells seeded on PAI-1 14-1b or collagen for 30 min. Data are the mean ± s.e.m. of the analysis of ten blebbing cells in each microenvironment; **: <i>P</i><0.01. (<b>G</b>) Expression of PDK1 and ROCK1 in blebbing SW620 cells seeded on PAI-1 14-1b or collagen for 30 min. The colocalization of PDK1 and ROCK1 is shown and their signal distributions are compared. Bar, 5 µm.</p>", "links"=>[], "tags"=>["pai-1", "maintains", "pathway"], "article_id"=>349486, "categories"=>["Information And Computing Sciences"], "users"=>["Amandine Cartier-Michaud", "Michel Malo", "Cécile Charrière-Bertrand", "Gilles Gadea", "Christelle Anguille", "Ajitha Supiramaniam", "Annick Lesne", "Franck Delaplace", "Guillaume Hutzler", "Pierre Roux", "Daniel A. Lawrence", "Georgia Barlovatz-Meimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032204.g002", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immobilized_active_PAI_1_maintains_the_RhoA_ROCK_pathway_activation_/349486", "title"=>"Immobilized, active PAI-1 maintains the RhoA/ROCK pathway activation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-21 02:38:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/679443"], "description"=>"<p>(<b>A</b>) Cellular-automata simulation of PAI-1 secretion, diffusion and deposition (vertical axis) in tumors of different cell size (10, 100 and 500 cells). (<b>B</b>) Detection of endogenous PAI-1 and recombinant PAI-1 14-1b by immunoblotting in SW620 cells seeded on PAI-1 14-1b at different time-points. Signal intensities were normalized to the expression of β-Tubulin. (<b>C</b>) Mathematical modeling of the possible effects of changes in the concentration of matrix-bound PAI-1 in the hysteretic cycle between amoeboid and mesenchymal behavior. (<b>D</b>) Amoeboid pseudopodal migration of a blebbing SW620 cell seeded on PAI-1 14-1b (17 h after seeding). Arrowhead indicates a pseudopod. Speed was evaluated at 0.4 µm/min (see also <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0032204#pone.0032204.s011\" target=\"_blank\">Video S6</a>). (<b>E</b>) Transition between blebbing and spindle-shaped morphology, and back, in blebbing morphology in a SW620 cell (★) seeded on PAI-1 14-1b (7 h after seeding) (see also <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0032204#pone.0032204.s012\" target=\"_blank\">Video S7</a>). Bar, 10 µm.</p>", "links"=>[], "tags"=>["pai-1", "deposition", "simulation", "amoeboid"], "article_id"=>349913, "categories"=>["Information And Computing Sciences"], "users"=>["Amandine Cartier-Michaud", "Michel Malo", "Cécile Charrière-Bertrand", "Gilles Gadea", "Christelle Anguille", "Ajitha Supiramaniam", "Annick Lesne", "Franck Delaplace", "Guillaume Hutzler", "Pierre Roux", "Daniel A. Lawrence", "Georgia Barlovatz-Meimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032204.g005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Modeling_PAI_1_deposition_and_simulation_of_its_possible_effects_on_amoeboid_cell_behavior_/349913", "title"=>"Modeling PAI-1 deposition and simulation of its possible effects on amoeboid cell behavior.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-21 02:45:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/679160"], "description"=>"<p>(<b>A</b>) Number of stained pixels of the uPAR immunostaining z-profile in SW620 cells seeded on PAI-1 14-1b or collagen for 19 h. Data are the mean ± s.e.m. of the analysis of thirty blebbing cells; *: <i>P</i><0.05, **: <i>P</i><0.01. (<b>B</b>) Expression of F-Actin and PAI-1 in blebbing SW620 cells seeded on PAI-1 14-1b for 19 h. (<b>C</b>) Percentage of blebbing SW620 cells (3 h after seeding) seeded on plates coated with PAI-1 14-1b or non-coated plates (Control) and in which the medium was supplemented with IgG, anti-uPA or anti-uPAR antibodies. Data are the mean ± s.e.m. of three independent experiments; ***: <i>P</i><0.001. (<b>D</b>) Percentage of blebbing SW620 cells seeded on PAI-1 14-1b, PAI-1 R76E or PAI-1 R at the 3 h and 19 h time-points. Data are the mean ± s.e.m. of three independent experiments; *: <i>P</i><0.05, **: <i>P</i><0.01. (<b>E</b>) Percentage of blebbing SW620 cells (3 h after seeding) seeded on plates coated with PAI-1 14-1b or non-coated plates (Control) and in which the medium was supplemented with soluble PAI-1. Data are the mean ± s.e.m. of three independent experiments; **: <i>P</i><0.01, ***: <i>P</i><0.001. (<b>F</b>) Localization of PAI-1 at the membrane (stained with wheat germ agglutinin) in SW620 cells seeded on non-coated plates for 30 min. (<b>G</b>) Flotillin1 and PAI-1 expression in SW620 cells seeded on non-coated plates for 30 min. (<b>H</b>) PDK1 and ROCK1 expression in SW620 cells seeded on PAI-1 14-1b for 30 min. (<b>I</b>) Schematic representation of deposits, which include PAI-1, uPA, PDK1, ROCK1, Flotillin1 and β1 Integrin, of blebbing cells in a 2D microenvironment. Bar, 5 µm.</p>", "links"=>[], "tags"=>["plasminogen", "activator", "influences"], "article_id"=>349637, "categories"=>["Information And Computing Sciences"], "users"=>["Amandine Cartier-Michaud", "Michel Malo", "Cécile Charrière-Bertrand", "Gilles Gadea", "Christelle Anguille", "Ajitha Supiramaniam", "Annick Lesne", "Franck Delaplace", "Guillaume Hutzler", "Pierre Roux", "Daniel A. Lawrence", "Georgia Barlovatz-Meimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032204.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Plasminogen_Activator_system_influences_cell_blebbing_/349637", "title"=>"The Plasminogen Activator system influences cell blebbing.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-21 02:40:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/678850"], "description"=>"<p>(<b>A</b>) When SW620 human colon cancer cells are cultured in the presence of serum they can be classified in three main morphological types: spindle-shaped, blebbing and round. Bar, 10 µm. The percentage of spindle-shaped (<b>B</b>) and blebbing cells (<b>C</b>) is influenced by the length of time SW620 cells have been in contact with immobilized, active PAI-1 14-1b, collagen or the matrix secreted by control cells (seeded on non-coated plates). Data are the mean ± s.e.m. of eight independent experiments; *: <i>P</i><0.05, ** <i>P</i><0.01. (<b>D</b>) Percentage of spindle-shaped, blebbing and round SW620 cells in plates coated with increasing concentrations of PAI-1 14-1b. Data are the mean ± s.e.m. of four independent experiments; *: <i>P</i><0.05, **: <i>P</i><0.01, ***: <i>P</i><0.001. Analysis by immunostaining and 3D reconstruction of the expression of (<b>E</b>) F-Actin and β-Tubulin, (<b>F</b>) F-Actin and β1 Integrin (arrowheads point to β1 Integrin clusters), and (<b>G</b>) F-Actin and Ezrin (arrowheads point to colocalization in blebs) in blebbing SW620 cell seeded on PAI-1 14-1b and spindle-shaped SW620 cell seeded on collagen at the 19 h time-point after seeding. Bar, 5 µm.</p>", "links"=>[], "tags"=>["pai-1", "supports"], "article_id"=>349334, "categories"=>["Information And Computing Sciences"], "users"=>["Amandine Cartier-Michaud", "Michel Malo", "Cécile Charrière-Bertrand", "Gilles Gadea", "Christelle Anguille", "Ajitha Supiramaniam", "Annick Lesne", "Franck Delaplace", "Guillaume Hutzler", "Pierre Roux", "Daniel A. Lawrence", "Georgia Barlovatz-Meimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032204.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immobilized_active_PAI_1_supports_cell_blebbing_/349334", "title"=>"Immobilized, active PAI-1 supports cell blebbing.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-21 02:35:34"}

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