Interleukin-17 Induces an Atypical M2-Like Macrophage Subpopulation That Regulates Intestinal Inflammation
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{"title"=>"Interleukin-17 induces an atypical M2-Like macrophage subpopulation that regulates intestinal inflammation", "type"=>"journal", "authors"=>[{"first_name"=>"Kenichiro", "last_name"=>"Nishikawa", "scopus_author_id"=>"35269264300"}, {"first_name"=>"Naohiro", "last_name"=>"Seo", "scopus_author_id"=>"7005678926"}, {"first_name"=>"Mie", "last_name"=>"Torii", "scopus_author_id"=>"23010446800"}, {"first_name"=>"Nei", "last_name"=>"Ma", "scopus_author_id"=>"56372327100"}, {"first_name"=>"Daisuke", "last_name"=>"Muraoka", "scopus_author_id"=>"36966952100"}, {"first_name"=>"Isao", "last_name"=>"Tawara", "scopus_author_id"=>"6603583100"}, {"first_name"=>"Masahiro", "last_name"=>"Masuya", "scopus_author_id"=>"7003603855"}, {"first_name"=>"Kyosuke", "last_name"=>"Tanaka", "scopus_author_id"=>"13906880500"}, {"first_name"=>"Yoshiyuki", "last_name"=>"Takei", "scopus_author_id"=>"7202470579"}, {"first_name"=>"Hiroshi", "last_name"=>"Shiku", "scopus_author_id"=>"35396660100"}, {"first_name"=>"Naoyuki", "last_name"=>"Katayama", "scopus_author_id"=>"7102706400"}, {"first_name"=>"Takuma", "last_name"=>"Kato", "scopus_author_id"=>"7405277298"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84907478536", "sgr"=>"84907478536", "issn"=>"19326203", "isbn"=>"1932-6203", "pmid"=>"25254662", "doi"=>"10.1371/journal.pone.0108494", "pui"=>"600067722"}, "id"=>"9a20b507-68f8-39df-8716-19544b3db0d5", "abstract"=>"Interleukin 17 (IL-17) is a pleiotropic cytokine that acts on both immune and non-immune cells and is generally implicated in inflammatory and autoimmune diseases. Although IL-17 as well as their source, mainly but not limited to Th17 cells, is also abundant in the inflamed intestine, the role of IL-17 in inflammatory bowel disease remains controversial. In the present study, by using IL-17 knockout (KO) mice, we investigated the role of IL-17 in colitis, with special focus on the macrophage subpopulations. Here we show that IL-17KO mice had increased susceptibility to DSS-induced colitis which was associated with decrease in expression of mRNAs implicated in M2 and/or wound healing macrophages, such as IL-10, IL-1 receptor antagonist, arginase 1, cyclooxygenase 2, and indoleamine 2,3-dioxygenase. Lamina propria leukocytes from inflamed colon of IL-17KO mice contained fewer CD11b+Ly6C+MHC Class II+ macrophages, which were derived, at least partly, from blood monocytes, as compared to those of WT mice. FACS-purified CD11b+ cells from WT mice, which were more abundant in Ly6C+MHC Class II+ cells, expressed increased levels of genes associated M2/wound healing macrophages and also M1/proinflammatory macrophages. Depletion of this population by topical administration of clodronate-liposome in the colon of WT mice resulted in the exacerbation of colitis. These results demonstrate that IL-17 confers protection against the development of severe colitis through the induction of an atypical M2-like macrophage subpopulation. Our findings reveal a previously unappreciated mechanism by which IL-17 exerts a protective function in colitis.", "link"=>"http://www.mendeley.com/research/interleukin17-induces-atypical-m2like-macrophage-subpopulation-regulates-intestinal-inflammation", "reader_count"=>50, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>16, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>2, "Student > Master"=>7, "Other"=>4, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>16, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>2, "Student > Master"=>7, "Other"=>4, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>29, "Medicine and Dentistry"=>7, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Computer Science"=>1, "Immunology and Microbiology"=>6}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>6}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>29}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>1}, "group_count"=>3}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1691115"], "description"=>"<p>Monocytes were purified from bone marrow of WT (CD45.1), WT (CD45.2) or IL-17KO (CD45.2), and adaptively transferred into WT (45.2), IL-17KO (CD45.2) or WT (CD45.1) mice (n = 3), respectively, followed by the treatment with DSS. On day 10, colonic LPLs were isolated from pooled colon, stained with anti-CD11b, anti-Ly6C, and anti-MHC Class II together with corresponding anti-CD45 congenic antibody, and subjected to flow cytometry analysis. A representative result from three independent experiments is shown.</p>", "links"=>[], "tags"=>["Th 17 cells", "WT mice", "Ly 6C Class II", "Lamina propria leukocytes", "coliti", "CD 11b Class II", "ko", "Regulates Intestinal Inflammation Interleukin 17", "il", "macrophage"], "article_id"=>1182508, "categories"=>["Biological Sciences"], "users"=>["Kenichiro Nishikawa", "Naohiro Seo", "Mie Torii", "Nei Ma", "Daisuke Muraoka", "Isao Tawara", "Masahiro Masuya", "Kyosuke Tanaka", "Yoshiyuki Takei", "Hiroshi Shiku", "Naoyuki Katayama", "Takuma Kato"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108494.g005", "stats"=>{"downloads"=>2, "page_views"=>295, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Blood_monocytes_are_recruited_into_inflamed_colons_and_differentiate_into_CD11b_Ly6C_MHC_Class_II_macrophages_in_the_presence_of_IL_17_/1182508", "title"=>"Blood monocytes are recruited into inflamed colons and differentiate into CD11b<sup>+</sup>Ly6C<sup>+</sup>MHC Class II<sup>+</sup> macrophages in the presence of IL-17.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-25 03:37:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1691091"], "description"=>"<p>IL-17KO mice and WT controls were given 1.5% DSS in drinking water or water alone for 7 days followed by consumption of water alone. Colitis severity was assessed by weight loss (A), colon length (day 10) (B) and H&E histology (day 0 and 10) (Calibration bar = 200 µm) (C). Colon barrier permeability was assessed on day 10 by detection of FITC-dextran serum (D). The results are expressed as mean values ± SEM for each geneotype in A (n = 5–6), B (n = 10), C (n = 2), and D (n = 5). *p<0.05; **p<0.01.</p>", "links"=>[], "tags"=>["Th 17 cells", "WT mice", "Ly 6C Class II", "Lamina propria leukocytes", "coliti", "CD 11b Class II", "ko", "Regulates Intestinal Inflammation Interleukin 17", "il", "macrophage"], "article_id"=>1182490, "categories"=>["Biological Sciences"], "users"=>["Kenichiro Nishikawa", "Naohiro Seo", "Mie Torii", "Nei Ma", "Daisuke Muraoka", "Isao Tawara", "Masahiro Masuya", "Kyosuke Tanaka", "Yoshiyuki Takei", "Hiroshi Shiku", "Naoyuki Katayama", "Takuma Kato"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108494.g001", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IL_17_deficient_mice_exhibit_more_severe_acute_colitis_following_DSS_administration_/1182490", "title"=>"IL-17 deficient mice exhibit more severe acute colitis following DSS administration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-25 03:37:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1691109"], "description"=>"<p>IL-17KO mice and WT controls (n = 3) were treated with DSS as described in the legend for <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108494#pone-0108494-g001\" target=\"_blank\">Figure 1</a>. Then, LPLs isolated from these mice were further purified into CD11b<sup>+</sup> cell on FACS Aria, from which cDNA were prepared and subjected to real-time PCR analysis. Expression of target mRNA were normalized to the expression of β-actin mRNA for generation of ΔCt values, and relative mRNA expression was quantified with the ΔΔCt method. Data are expressed as mean ± SEM. *p<0.05; **p<0.01.</p>", "links"=>[], "tags"=>["Th 17 cells", "WT mice", "Ly 6C Class II", "Lamina propria leukocytes", "coliti", "CD 11b Class II", "ko", "Regulates Intestinal Inflammation Interleukin 17", "il", "macrophage"], "article_id"=>1182502, "categories"=>["Biological Sciences"], "users"=>["Kenichiro Nishikawa", "Naohiro Seo", "Mie Torii", "Nei Ma", "Daisuke Muraoka", "Isao Tawara", "Masahiro Masuya", "Kyosuke Tanaka", "Yoshiyuki Takei", "Hiroshi Shiku", "Naoyuki Katayama", "Takuma Kato"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108494.g004", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CD11b_cells_from_inflamed_colonic_LPLs_of_KO_mice_express_significantly_lower_levels_of_genes_implicated_in_M2_wound_healing_macrophages_/1182502", "title"=>"CD11b<sup>+</sup> cells from inflamed colonic LPLs of KO mice express significantly lower levels of genes implicated in M2/wound healing macrophages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-25 03:37:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1691125"], "description"=>"<p>WT mice were given 1.5% DSS in drinking water for 7 days followed by consumption of water alone for another 3 days, during which the mice were treated with clodronate-liposome or control liposome intrarectally on days −1, 1, 3, and 5 as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108494#s2\" target=\"_blank\">Materials and Methods</a>. (A) Representative FACS plots showing reduced CD11b<sup>+</sup>Ly6C<sup>+</sup>MHC Class II<sup>+</sup> macrophages in colon of clodronate-liposome treated mice. (B) Changes in body weight over time were expressed as a percentage of the original weight. Data represent as mean ± SEM. The experiments were repeated two times with at least three mice per group per experiment.</p>", "links"=>[], "tags"=>["Th 17 cells", "WT mice", "Ly 6C Class II", "Lamina propria leukocytes", "coliti", "CD 11b Class II", "ko", "Regulates Intestinal Inflammation Interleukin 17", "il", "macrophage"], "article_id"=>1182516, "categories"=>["Biological Sciences"], "users"=>["Kenichiro Nishikawa", "Naohiro Seo", "Mie Torii", "Nei Ma", "Daisuke Muraoka", "Isao Tawara", "Masahiro Masuya", "Kyosuke Tanaka", "Yoshiyuki Takei", "Hiroshi Shiku", "Naoyuki Katayama", "Takuma Kato"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108494.g006", "stats"=>{"downloads"=>1, "page_views"=>169, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Depletion_of_CD11b_Ly6C_MHC_Class_II_macrophages_accelerates_colon_inflammation_in_WT_mice_induced_by_DSS_treatment_/1182516", "title"=>"Depletion of CD11b<sup>+</sup>Ly6C<sup>+</sup>MHC Class II<sup>+</sup> macrophages accelerates colon inflammation in WT mice induced by DSS treatment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-25 03:37:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1691166", "https://ndownloader.figshare.com/files/1691167", "https://ndownloader.figshare.com/files/1691168", "https://ndownloader.figshare.com/files/1691169"], "description"=>"<div><p>Interleukin 17 (IL-17) is a pleiotropic cytokine that acts on both immune and non-immune cells and is generally implicated in inflammatory and autoimmune diseases. Although IL-17 as well as their source, mainly but not limited to Th17 cells, is also abundant in the inflamed intestine, the role of IL-17 in inflammatory bowel disease remains controversial. In the present study, by using IL-17 knockout (KO) mice, we investigated the role of IL-17 in colitis, with special focus on the macrophage subpopulations. Here we show that IL-17KO mice had increased susceptibility to DSS-induced colitis which was associated with decrease in expression of mRNAs implicated in M2 and/or wound healing macrophages, such as IL-10, IL-1 receptor antagonist, arginase 1, cyclooxygenase 2, and indoleamine 2,3-dioxygenase. Lamina propria leukocytes from inflamed colon of IL-17KO mice contained fewer CD11b<sup>+</sup>Ly6C<sup>+</sup>MHC Class II<sup>+</sup> macrophages, which were derived, at least partly, from blood monocytes, as compared to those of WT mice. FACS-purified CD11b<sup>+</sup> cells from WT mice, which were more abundant in Ly6C<sup>+</sup>MHC Class II<sup>+</sup> cells, expressed increased levels of genes associated M2/wound healing macrophages and also M1/proinflammatory macrophages. Depletion of this population by topical administration of clodronate-liposome in the colon of WT mice resulted in the exacerbation of colitis. These results demonstrate that IL-17 confers protection against the development of severe colitis through the induction of an atypical M2-like macrophage subpopulation. Our findings reveal a previously unappreciated mechanism by which IL-17 exerts a protective function in colitis.</p></div>", "links"=>[], "tags"=>["Th 17 cells", "WT mice", "Ly 6C Class II", "Lamina propria leukocytes", "coliti", "CD 11b Class II", "ko", "Regulates Intestinal Inflammation Interleukin 17", "il", "macrophage"], "article_id"=>1182543, "categories"=>["Biological Sciences"], "users"=>["Kenichiro Nishikawa", "Naohiro Seo", "Mie Torii", "Nei Ma", "Daisuke Muraoka", "Isao Tawara", "Masahiro Masuya", "Kyosuke Tanaka", "Yoshiyuki Takei", "Hiroshi Shiku", "Naoyuki Katayama", "Takuma Kato"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0108494.s001", "https://dx.doi.org/10.1371/journal.pone.0108494.s002", "https://dx.doi.org/10.1371/journal.pone.0108494.s003", "https://dx.doi.org/10.1371/journal.pone.0108494.s004"], "stats"=>{"downloads"=>15, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interleukin_17_Induces_an_Atypical_M2_Like_Macrophage_Subpopulation_That_Regulates_Intestinal_Inflammation_/1182543", "title"=>"Interleukin-17 Induces an Atypical M2-Like Macrophage Subpopulation That Regulates Intestinal Inflammation", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-09-25 03:37:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1691108"], "description"=>"<p>IL-17KO mice and WT controls were treated with DSS as described in the legend for <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108494#pone-0108494-g001\" target=\"_blank\">Figure 1</a>. (A) LPLs were purified from pooled (n = 2–3) distal colon sections of untreated and DSS-treated mice and subjected to flow cytometry analysis. Gating strategy of live and CD45<sup>+</sup> for CD11b<sup>+</sup> cells was shown in upper panels. Representative data from seven independent experiments are shown. Number denotes frequency of gated cells. (B) The frequency of cells for each subset in A is shown. Graphs represent mean ± SEM of seven independent experiments. *p<0.05. (C) Representative flow cytometry profiles of cell surface molecules implicated in M2/anti-inflammatory macrophages on each subset depicted as in A. Gray histograms represent cells stained with isotype matched control mAbs.</p>", "links"=>[], "tags"=>["Th 17 cells", "WT mice", "Ly 6C Class II", "Lamina propria leukocytes", "coliti", "CD 11b Class II", "ko", "Regulates Intestinal Inflammation Interleukin 17", "il", "macrophage"], "article_id"=>1182501, "categories"=>["Biological Sciences"], "users"=>["Kenichiro Nishikawa", "Naohiro Seo", "Mie Torii", "Nei Ma", "Daisuke Muraoka", "Isao Tawara", "Masahiro Masuya", "Kyosuke Tanaka", "Yoshiyuki Takei", "Hiroshi Shiku", "Naoyuki Katayama", "Takuma Kato"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108494.g003", "stats"=>{"downloads"=>0, "page_views"=>67, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Aggravated_DSS_induced_colitis_in_IL_17KO_mice_is_associated_with_reduced_number_of_CD11b_Ly6C_MHC_Class_II_macrophages_in_the_inflamed_colon_/1182501", "title"=>"Aggravated DSS-induced colitis in IL-17KO mice is associated with reduced number of CD11b<sup>+</sup>Ly6C<sup>+</sup>MHC Class II<sup>+</sup> macrophages in the inflamed colon.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-25 03:37:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/1691096"], "description"=>"<p>IL-17KO mice and WT controls were treated with DSS as described in the legend for <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108494#pone-0108494-g001\" target=\"_blank\">Figure 1</a>. Total RNA were purified from distal colon sections of untreated and DSS-treated individual mice (n = 3) and transcribed into cDNA, which were subsequently subjected for real-time PCR analysis. Expression of target mRNA were normalized to the expression of β-actin mRNA for generation of ΔCt values, and relative mRNA expression was quantified with the ΔΔCt method. Data are expressed as mean ± SEM. *p<0.05; **p<0.01.</p>", "links"=>[], "tags"=>["Th 17 cells", "WT mice", "Ly 6C Class II", "Lamina propria leukocytes", "coliti", "CD 11b Class II", "ko", "Regulates Intestinal Inflammation Interleukin 17", "il", "macrophage"], "article_id"=>1182495, "categories"=>["Biological Sciences"], "users"=>["Kenichiro Nishikawa", "Naohiro Seo", "Mie Torii", "Nei Ma", "Daisuke Muraoka", "Isao Tawara", "Masahiro Masuya", "Kyosuke Tanaka", "Yoshiyuki Takei", "Hiroshi Shiku", "Naoyuki Katayama", "Takuma Kato"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108494.g002", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Colonic_expression_of_mRNA_for_genes_involved_in_inflammation_and_anti_inflammation_/1182495", "title"=>"Colonic expression of mRNA for genes involved in inflammation and anti-inflammation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-25 03:37:45"}

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Relative Metric

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