IL-34 Induces the Differentiation of Human Monocytes into Immunosuppressive Macrophages. Antagonistic Effects of GM-CSF and IFNγ
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{"title"=>"IL-34 Induces the Differentiation of Human Monocytes into Immunosuppressive Macrophages. Antagonistic Effects of GM-CSF and IFNγ", "type"=>"journal", "authors"=>[{"first_name"=>"Etienne D.", "last_name"=>"Foucher", "scopus_author_id"=>"55587677200"}, {"first_name"=>"Simon", "last_name"=>"Blanchard", "scopus_author_id"=>"12785586200"}, {"first_name"=>"Laurence", "last_name"=>"Preisser", "scopus_author_id"=>"6602447333"}, {"first_name"=>"Erwan", "last_name"=>"Garo", "scopus_author_id"=>"34968061900"}, {"first_name"=>"Norbert", "last_name"=>"Ifrah", "scopus_author_id"=>"35425949100"}, {"first_name"=>"Philippe", "last_name"=>"Guardiola", "scopus_author_id"=>"6701714712"}, {"first_name"=>"Yves", "last_name"=>"Delneste", "scopus_author_id"=>"7003499929"}, {"first_name"=>"Pascale", "last_name"=>"Jeannin", "scopus_author_id"=>"7006740619"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84873659707", "pui"=>"368325891", "doi"=>"10.1371/journal.pone.0056045", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"84873659707", "pmid"=>"23409120"}, "id"=>"e18f453f-27a4-31ef-ad73-0ba5e2f38e48", "abstract"=>"IL-34 is a recently identified cytokine that signals via the M-CSF receptor and promotes monocyte survival. Depending on the environment, monocytes can differentiate into macrophages (Mφ) or dendritic cells (DC). A wide spectrum of Mφ and DC subsets, with distinct phenotypes and functions, has been described. To date, the phenotype of monocytes exposed to IL-34 remains unexplored. We report here that IL-34 induces the differentiation of monocytes into CD14(high) CD163(high) CD1a(-) Mφ (IL-34-Mφ). Upon LPS stimulation, IL-34-Mφ exhibit an IL-10(high) IL-12(low) M2 profile and express low levels of the costimulatory molecules CD80 and CD86. IL-34-Mφ exhibit poor T cell costimulatory properties, and have potent immunosuppressive properties (decrease of TCR-stimulated T cell proliferation). For all the parameters analyzed, IL-34-Mφ are phenotypically and functionally similar to M-CSF-Mφ. IL-34 appears as efficient as M-CSF in inducing the generation of immunosuppressive Mφ. Moreover, the generation of IL-34-Mφ is mediated through the M-CSF receptor, is independent of endogenous M-CSF consumption and is potentiated by IL-6. In an attempt to identify strategies to prevent a deleterious M2 cell accumulation in some pathological situations, we observed that IFNγ and GM-CSF prevent the generation of immunosuppressive Mφ induced by IL-34. IFNγ also switches established IL-34-Mφ into immunostimulatory Mφ. In conclusion, we demonstrate that IL-34 drives the differentiation of monocytes into immunosuppressive M2, in a manner similar to M-CSF, and that IFNγ and GM-CSF prevent this effect.", "link"=>"http://www.mendeley.com/research/il34-induces-differentiation-human-monocytes-immunosuppressive-macrophages-antagonistic-effects-gmcs", "reader_count"=>83, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>19, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>8, "Student > Master"=>17, "Other"=>2, "Student > Bachelor"=>9, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>19, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>8, "Student > Master"=>17, "Other"=>2, "Student > Bachelor"=>9, "Professor"=>3}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>40, "Medicine and Dentistry"=>24, "Neuroscience"=>2, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>7}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>24}, "Neuroscience"=>{"Neuroscience"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>40}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>2, "Japan"=>3, "United Kingdom"=>2, "South Africa"=>1, "Germany"=>2}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/491662"], "description"=>"<p><i>A, IL-34-M</i>φ <i>exhibit a CD14<sup>high</sup> CD163 <sup>high</sup> CD80<sup>low</sup> CD86<sup>low</sup> phenotype.</i> The expression of CD14 and CD163 (before LPS stimulation) and of CD80 and CD86 (after LPS stimulation) was analyzed by flow cytometry on IL-34-Mφ, M-CSF-Mφ, and GM-CSF-Mφ. For each marker, the grey histogram corresponds to isotype control mAb and is similar in the 3 experimental conditions. Results are representative of 1 of 5 experiments. <i>B, IL-34-Mφ polarization results in the maintenance of CD14 and in the acquisition of CD163.</i> The expression of CD14 and CD163 was analyzed by flow cytometry during the 5-day polarization of IL-34-Mφ, M-CSF-Mφ, and GM-CSF-Mφ (left panels). Right panels, flow cytometry histograms of CD14 and CD163 expression by monocytes cultured with IL-34 and analyzed at day 1, day 3, and day5. <i>C, IL-34-Mφ display an IL-10<sup>high</sup> IL-12<sup>low</sup> phenotype.</i> IL-10 and IL-12 were quantified in the supernatants of IL-34-Mφ, M-CSF-Mφ, and GM-CSF-Mφ after LPS stimulation. Results are expressed in pg/ml (IL-12) or ng/ml (IL-10) (mean ± SD, n = 5). * p<0.05, compared to GM-CSF.</p>", "links"=>[], "tags"=>["induces", "monocyte", "differentiation", "m2"], "article_id"=>162170, "categories"=>["Developmental Biology", "Immunology"], "users"=>["Etienne D. Foucher", "Simon Blanchard", "Laurence Preisser", "Erwan Garo", "Norbert Ifrah", "Philippe Guardiola", "Yves Delneste", "Pascale Jeannin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056045.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IL_34_induces_monocyte_differentiation_into_M2_cells_/162170", "title"=>"IL-34 induces monocyte differentiation into M2 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-08 00:36:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/491842"], "description"=>"<p><i>A Three-dimensional projection of PCA of IL-34-Mφ, M-CSF-Mφ and GM-CSF-Mφ</i>. Each dot represents one Mφ subset of one donor, stimulated or not for 6 h with LPS, based on values of all 18 studied chemokines/chemokine receptors. The percentage of variances is depicted on the three axes. <i>B,Two-dimensional unsupervised hierarchical clustering analysis of the chemokines/chemokine receptors expression in the Mφ subset</i>. The normalized values for each chemokine/chemokine receptors from four different donors is depicted according to the color scale, where red and green represent expression above and below the mean, respectively.</p>", "links"=>[], "tags"=>["chemokine", "receptor", "mrna"], "article_id"=>162356, "categories"=>["Developmental Biology", "Immunology"], "users"=>["Etienne D. Foucher", "Simon Blanchard", "Laurence Preisser", "Erwan Garo", "Norbert Ifrah", "Philippe Guardiola", "Yves Delneste", "Pascale Jeannin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056045.g003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_chemokine_and_chemokine_receptor_mRNA_expression_by_macrophages_/162356", "title"=>"Analysis of chemokine and chemokine receptor mRNA expression by macrophages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-08 00:39:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/484235", "https://ndownloader.figshare.com/files/484237", "https://ndownloader.figshare.com/files/484241", "https://ndownloader.figshare.com/files/484244"], "description"=>"<div><p>IL-34 is a recently identified cytokine that signals via the M-CSF receptor and promotes monocyte survival. Depending on the environment, monocytes can differentiate into macrophages (Mφ) or dendritic cells (DC). A wide spectrum of Mφ and DC subsets, with distinct phenotypes and functions, has been described. To date, the phenotype of monocytes exposed to IL-34 remains unexplored. We report here that IL-34 induces the differentiation of monocytes into CD14<sup>high</sup> CD163<sup>high</sup> CD1a<sup>−</sup> Mφ (IL-34-Mφ). Upon LPS stimulation, IL-34-Mφ exhibit an IL-10<sup>high</sup> IL-12<sup>low</sup> M2 profile and express low levels of the costimulatory molecules CD80 and CD86. IL-34-Mφ exhibit poor T cell costimulatory properties, and have potent immunosuppressive properties (decrease of TCR-stimulated T cell proliferation). For all the parameters analyzed, IL-34-Mφ are phenotypically and functionally similar to M-CSF-Mφ. IL-34 appears as efficient as M-CSF in inducing the generation of immunosuppressive Mφ. Moreover, the generation of IL-34-Mφ is mediated through the M-CSF receptor, is independent of endogenous M-CSF consumption and is potentiated by IL-6. In an attempt to identify strategies to prevent a deleterious M2 cell accumulation in some pathological situations, we observed that IFNγ and GM-CSF prevent the generation of immunosuppressive Mφ induced by IL-34. IFNγ also switches established IL-34-Mφ into immunostimulatory Mφ. In conclusion, we demonstrate that IL-34 drives the differentiation of monocytes into immunosuppressive M2, in a manner similar to M-CSF, and that IFNγ and GM-CSF prevent this effect.</p> </div>", "links"=>[], "tags"=>["il-34", "induces", "differentiation", "monocytes", "immunosuppressive", "antagonistic", "effects", "gm-csf"], "article_id"=>156334, "categories"=>["Developmental Biology", "Immunology"], "users"=>["Etienne D. Foucher", "Simon Blanchard", "Laurence Preisser", "Erwan Garo", "Norbert Ifrah", "Philippe Guardiola", "Yves Delneste", "Pascale Jeannin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0056045.s001", "https://dx.doi.org/10.1371/journal.pone.0056045.s002", "https://dx.doi.org/10.1371/journal.pone.0056045.s003", "https://dx.doi.org/10.1371/journal.pone.0056045.s004"], "stats"=>{"downloads"=>17, "page_views"=>86, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/IL_34_Induces_the_Differentiation_of_Human_Monocytes_into_Immunosuppressive_Macrophages_Antagonistic_Effects_of_GM_CSF_and_IFN__/156334", "title"=>"IL-34 Induces the Differentiation of Human Monocytes into Immunosuppressive Macrophages. Antagonistic Effects of GM-CSF and IFNγ", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-02-08 01:45:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/491998"], "description"=>"<p><i>A–C, GM-CSF and IFNγ prevent the differentiation of monocytes into immunosuppressive IL-34-Mφ.</i> IL-34-Mφ and GM-CSF-Mφ were generated in the absence or presence of GM-CSF or IFNγ before phenotype analysis. <i>D–F, IFNγ skews monocyte differentiation from IL-34-Mφ into immunostimulatory Mφ.</i> IL-34-Mφ and GM-CSF-Mφ were cultured for 3 days in the absence or presence of GM-CSF or IFNγ before phenotype analysis. The expression of CD14 and CD163 (<i>C</i>&<i>F</i>) was analyzed on non-stimulated cells. The production of IL-10 and IL-12 (<i>A</i>&<i>D</i>) and the expression of CD80 and CD86 (<i>B</i>&<i>E</i>) was analyzed after LPS stimulation. Results are expressed in MFI values, in pg/ml (IL-12) or ng/ml (IL-10), or as a percentage of inhibition (mean ± SD, n = 7), (<i>A</i>,<i>B</i>,<i>D</i>&<i>E</i>), * p<0.05, compared to IL-34-Mφ.</p>", "links"=>[], "tags"=>["immunology", "developmental biology"], "article_id"=>162520, "categories"=>["Developmental Biology", "Immunology"], "users"=>["Etienne D. Foucher", "Simon Blanchard", "Laurence Preisser", "Erwan Garo", "Norbert Ifrah", "Philippe Guardiola", "Yves Delneste", "Pascale Jeannin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056045.g005", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GM_CSF_and_IFN_947_prevent_the_generation_of_IL_34_M_966_/162520", "title"=>"GM-CSF and IFNγ prevent the generation of IL-34-Mφ.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-08 00:42:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/491906"], "description"=>"<p><i>A</i>&<i>B, IL-34-Mφ are immunosuppressive.</i> LPS-stimulated IL-34-Mφ, M-CSF-Mφ and GM-CSF-Mφ were cultured with CFDA-SE labeled CD4<sup>+</sup> T cells in MLR experiments (<i>A</i>) or with CFDA-SE labeled memory CD45RO<sup>+</sup> T cells in T cell proliferation assays (<i>B</i>); results are expressed as a percentage of cells depending on the number of cycle division (mean ± SD, n = 4). * p<0.05, compared to GM-CSF-Mφ. Right panels, representative histograms of CFDA-SE labeling from one donor. <i>C</i>&<i>D, IL-34 switches monocytes into M2 in an M-CSF-independent manner.</i> Analysis of the expression of CD14 and CD163 (<i>C</i>), and of the production of IL-10 and IL-12 (quantified after a 24 h stimulation with LPS) (<i>D</i>) by IL-34-Mφ, M-CSF-Mφ and GM-CSF-Mφ generated in the absence or presence of a neutralizing anti-M-CSF mAb, an isotype control mAb, the kinase inhibitor GW2580, or the drug diluent. Results are expressed in MFI values or in ng/ml (mean ± SD, n = 4). <i>E, Analysis of cell viability.</i> The viability of monocytes cultured with IL-34, M-CSF or GM-CSF, in the absence of presence of a neutralizing anti-M-CSF mAb, an isotype control mAb, the kinase inhibitor GW2580, or the drug diluent, was determined at day 3 by annexinV labeling. Results are expressed as a percentage of living cells (mean ± SD, n = 4). † means >90% of died cells.</p>", "links"=>[], "tags"=>["induces", "immunosuppressive", "m2", "independently"], "article_id"=>162422, "categories"=>["Developmental Biology", "Immunology"], "users"=>["Etienne D. Foucher", "Simon Blanchard", "Laurence Preisser", "Erwan Garo", "Norbert Ifrah", "Philippe Guardiola", "Yves Delneste", "Pascale Jeannin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056045.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IL_34_induces_the_generation_of_immunosuppressive_M2_independently_of_M_CSF_/162422", "title"=>"IL-34 induces the generation of immunosuppressive M2 independently of M-CSF.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-08 00:40:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/492092"], "description"=>"<p>The expression of the indicated markers was analyzed by FACS on IL-34-Mφ, M-CSF-Mφ and GM-CSF-Mφ, stimulated or not for 48 h with 200 ng/ml LPS. Results are expressed as mean fluorescence intensity values (after subtraction of the MFI obtained with the isotype control mAb) and are representative of 4 separate experiments. +++++ indicates MFI greater than 1000; ++++, MFI greater than 400 and less than 1000; +++, MFI greater than 200 and less than 400; ++, MFI greater than 100 and less than 200; +, MFI greater than 20 and less than 100 and, − indicates MFI less than 20.</p>", "links"=>[], "tags"=>["markers", "macrophage"], "article_id"=>162611, "categories"=>["Developmental Biology", "Immunology"], "users"=>["Etienne D. Foucher", "Simon Blanchard", "Laurence Preisser", "Erwan Garo", "Norbert Ifrah", "Philippe Guardiola", "Yves Delneste", "Pascale Jeannin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056045.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_cell_surface_markers_on_macrophage_subsets_/162611", "title"=>"Analysis of cell surface markers on macrophage subsets.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-08 00:43:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/491757"], "description"=>"<p><i>A–E, IL-34 induces monocyte differentiation into M2</i>. Macrophage subsets were generated as described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0056045#s2\" target=\"_blank\">Material & Methods</a> section. The expression of CD14 (<i>A</i>) and CD163 (<i>B</i>) was analyzed by flow cytometry on non stimulated cells. The expression of CD80 (<i>C</i>), CD86 (<i>D</i>) and ILT3 (<i>E</i>) was analyzed by flow cytometry after LPS stimulation. Results are expressed in MFI values (mean ± SD, n = 5). * p<0.05, compared to IL-34; # p<0.05, compared to IL-34+IL-6. <i>F, IL-6 favors IL-34 consumption</i>. IL-34 was quantified at different time-points in the supernatants of monocytes exposed to 50 ng/ml IL-34, without or with 50 ng/ml IL-6. Results are expressed in ng/ml (mean ± SD, n = 4). * p<0.05.</p>", "links"=>[], "tags"=>["induces", "m2"], "article_id"=>162273, "categories"=>["Developmental Biology", "Immunology"], "users"=>["Etienne D. Foucher", "Simon Blanchard", "Laurence Preisser", "Erwan Garo", "Norbert Ifrah", "Philippe Guardiola", "Yves Delneste", "Pascale Jeannin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056045.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IL_34_induces_M2_cell_generation_/162273", "title"=>"IL-34 induces M2 cell generation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-08 00:37:53"}

PMC Usage Stats | Further Information

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Relative Metric

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