Commensal microbiota drive the functional diversification of colon macrophages
Mononuclear phagocytes are a heterogeneous population of leukocytes essential for immune homeostasis that develop tissue-specific functions due to unique transcriptional programs driven by local microenvironmental cues. Single cell RNA sequencing (scRNA-seq) of colonic myeloid cells from specific pa...
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| Veröffentlicht in: | Mucosal immunology 2020-03, Vol.13 (2), p.216-229 |
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| creator | Kang, Byunghyun Alvarado, Luigi J. Kim, Teayong Lehmann, Michael L. Cho, Hyeseon He, Jianping Li, Peng Kim, Bong-Hyun Larochelle, Andre Kelsall, Brian L. |
| description | Mononuclear phagocytes are a heterogeneous population of leukocytes essential for immune homeostasis that develop tissue-specific functions due to unique transcriptional programs driven by local microenvironmental cues. Single cell RNA sequencing (scRNA-seq) of colonic myeloid cells from specific pathogen free (SPF) and germ-free (GF) C57BL/6 mice revealed extensive heterogeneity of both colon macrophages (MPs) and dendritic cells (DCs). Modeling of developmental pathways combined with inference of gene regulatory networks indicate two major trajectories from common CCR2
+
precursors resulting in colon MP populations with unique transcription factors and downstream target genes. Compared to SPF mice, GF mice had decreased numbers of total colon MPs, as well as selective proportional decreases of two major CD11c
+
CD206
int
CD121b
+
and CD11c
−
CD206
hi
CD121b
−
colon MP populations, whereas DC numbers and proportions were not different. Importantly, these two major colon MP populations were clearly distinct from other colon MP populations regarding their gene expression profile, localization within the lamina propria (LP) and ability to phagocytose macromolecules from the blood. These data uncover the diversity of intestinal myeloid cell populations at the molecular level and highlight the importance of microbiota on the unique developmental as well as anatomical and functional fates of colon MPs. |
| doi_str_mv | 10.1038/s41385-019-0228-3 |
| format | Article |
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+
precursors resulting in colon MP populations with unique transcription factors and downstream target genes. Compared to SPF mice, GF mice had decreased numbers of total colon MPs, as well as selective proportional decreases of two major CD11c
+
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CD121b
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and CD11c
−
CD206
hi
CD121b
−
colon MP populations, whereas DC numbers and proportions were not different. Importantly, these two major colon MP populations were clearly distinct from other colon MP populations regarding their gene expression profile, localization within the lamina propria (LP) and ability to phagocytose macromolecules from the blood. These data uncover the diversity of intestinal myeloid cell populations at the molecular level and highlight the importance of microbiota on the unique developmental as well as anatomical and functional fates of colon MPs.</description><identifier>ISSN: 1933-0219</identifier><identifier>EISSN: 1935-3456</identifier><identifier>DOI: 10.1038/s41385-019-0228-3</identifier><identifier>PMID: 31772323</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>Allergology ; Animals ; Antibodies ; Biomedical and Life Sciences ; Biomedicine ; CCR2 protein ; CD11c antigen ; CD11c Antigen - metabolism ; Cell Differentiation ; Cells, Cultured ; Colon ; Colon - immunology ; Dendritic cells ; Dendritic Cells - immunology ; Gastroenterology ; Gene expression ; Gene Ontology ; Gene Regulatory Networks ; Germfree ; Homeostasis ; Immunology ; Intestine ; Lamina propria ; Lectins, C-Type - genetics ; Lectins, C-Type - metabolism ; Leukocytes (mononuclear) ; Localization ; Macromolecules ; Macrophages ; Macrophages - immunology ; Mannose Receptor ; Mannose-Binding Lectins - genetics ; Mannose-Binding Lectins - metabolism ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Microbiota ; Monocyte chemoattractant protein 1 ; Myeloid cells ; Myeloid Cells - physiology ; Phagocytes ; Phagocytosis - genetics ; Phenotype ; Receptors, Cell Surface - genetics ; Receptors, Cell Surface - metabolism ; Ribonucleic acid ; RNA ; Sequence Analysis, RNA ; Single-Cell Analysis ; Specific pathogen free ; Transcription factors ; Transcriptome</subject><ispartof>Mucosal immunology, 2020-03, Vol.13 (2), p.216-229</ispartof><rights>The Author(s) 2019</rights><rights>This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2019. This work is published under https://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c564t-7f47c4e78b0bc8b2183ce7bb2b82a7bc556ea84757edc48c3d339e4d48f39f63</citedby><cites>FETCH-LOGICAL-c564t-7f47c4e78b0bc8b2183ce7bb2b82a7bc556ea84757edc48c3d339e4d48f39f63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/2475058328?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>230,314,780,784,885,27923,27924,64384,64386,64388,72340</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31772323$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kang, Byunghyun</creatorcontrib><creatorcontrib>Alvarado, Luigi J.</creatorcontrib><creatorcontrib>Kim, Teayong</creatorcontrib><creatorcontrib>Lehmann, Michael L.</creatorcontrib><creatorcontrib>Cho, Hyeseon</creatorcontrib><creatorcontrib>He, Jianping</creatorcontrib><creatorcontrib>Li, Peng</creatorcontrib><creatorcontrib>Kim, Bong-Hyun</creatorcontrib><creatorcontrib>Larochelle, Andre</creatorcontrib><creatorcontrib>Kelsall, Brian L.</creatorcontrib><title>Commensal microbiota drive the functional diversification of colon macrophages</title><title>Mucosal immunology</title><addtitle>Mucosal Immunol</addtitle><addtitle>Mucosal Immunol</addtitle><description>Mononuclear phagocytes are a heterogeneous population of leukocytes essential for immune homeostasis that develop tissue-specific functions due to unique transcriptional programs driven by local microenvironmental cues. Single cell RNA sequencing (scRNA-seq) of colonic myeloid cells from specific pathogen free (SPF) and germ-free (GF) C57BL/6 mice revealed extensive heterogeneity of both colon macrophages (MPs) and dendritic cells (DCs). Modeling of developmental pathways combined with inference of gene regulatory networks indicate two major trajectories from common CCR2
+
precursors resulting in colon MP populations with unique transcription factors and downstream target genes. Compared to SPF mice, GF mice had decreased numbers of total colon MPs, as well as selective proportional decreases of two major CD11c
+
CD206
int
CD121b
+
and CD11c
−
CD206
hi
CD121b
−
colon MP populations, whereas DC numbers and proportions were not different. Importantly, these two major colon MP populations were clearly distinct from other colon MP populations regarding their gene expression profile, localization within the lamina propria (LP) and ability to phagocytose macromolecules from the blood. These data uncover the diversity of intestinal myeloid cell populations at the molecular level and highlight the importance of microbiota on the unique developmental as well as anatomical and functional fates of colon MPs.</description><subject>Allergology</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>CCR2 protein</subject><subject>CD11c antigen</subject><subject>CD11c Antigen - metabolism</subject><subject>Cell Differentiation</subject><subject>Cells, Cultured</subject><subject>Colon</subject><subject>Colon - immunology</subject><subject>Dendritic cells</subject><subject>Dendritic Cells - immunology</subject><subject>Gastroenterology</subject><subject>Gene expression</subject><subject>Gene Ontology</subject><subject>Gene Regulatory Networks</subject><subject>Germfree</subject><subject>Homeostasis</subject><subject>Immunology</subject><subject>Intestine</subject><subject>Lamina propria</subject><subject>Lectins, C-Type - genetics</subject><subject>Lectins, C-Type - metabolism</subject><subject>Leukocytes (mononuclear)</subject><subject>Localization</subject><subject>Macromolecules</subject><subject>Macrophages</subject><subject>Macrophages - immunology</subject><subject>Mannose Receptor</subject><subject>Mannose-Binding Lectins - genetics</subject><subject>Mannose-Binding Lectins - metabolism</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Microbiota</subject><subject>Monocyte chemoattractant protein 1</subject><subject>Myeloid cells</subject><subject>Myeloid Cells - physiology</subject><subject>Phagocytes</subject><subject>Phagocytosis - genetics</subject><subject>Phenotype</subject><subject>Receptors, Cell Surface - genetics</subject><subject>Receptors, Cell Surface - metabolism</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Sequence Analysis, RNA</subject><subject>Single-Cell Analysis</subject><subject>Specific pathogen free</subject><subject>Transcription factors</subject><subject>Transcriptome</subject><issn>1933-0219</issn><issn>1935-3456</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kcFPHCEUxkmjqVb7B_TSTOLFyyjwYIBLk2ZTWxOjF-8EGGaXzcywwoyJ_31Z125bEz3xwvd7H4_3IfSF4AuCQV5mRkDyGhNVY0plDR_QMVHAa2C8OXiuoShEHaFPOa8xbjDm8BEdARGCAoVjdLuIw-DHbPpqCC5FG-JkqjaFR19NK1918-imEMeit-Uu5dAFZ7Y3VewqF_tSDKY0blZm6fMpOuxMn_3nl_ME3V_9uF_8qm_ufl4vvt_UjjdsqkXHhGNeSIutk5YSCc4La6mV1AjrOG-8kUxw4VvHpIMWQHnWMtmB6ho4Qd92tpvZDgXx45RMrzcpDCY96WiC_l8Zw0ov46MWGJTEqhicvxik-DD7POkhZOf73ow-zllTIIoowRpc0LNX6DrOqSykUGVCzCVQ-S4FDaWYUbGlyI4qC8s5-W4_MsF6G6neRapLpHobqYbS8_Xfv-47_mRYALoDcpHGpU9_n37b9TfI_az4</recordid><startdate>20200301</startdate><enddate>20200301</enddate><creator>Kang, Byunghyun</creator><creator>Alvarado, Luigi J.</creator><creator>Kim, Teayong</creator><creator>Lehmann, Michael L.</creator><creator>Cho, Hyeseon</creator><creator>He, Jianping</creator><creator>Li, Peng</creator><creator>Kim, Bong-Hyun</creator><creator>Larochelle, Andre</creator><creator>Kelsall, Brian L.</creator><general>Nature Publishing Group US</general><general>Elsevier Limited</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7T5</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20200301</creationdate><title>Commensal microbiota drive the functional diversification of colon macrophages</title><author>Kang, Byunghyun ; Alvarado, Luigi J. ; Kim, Teayong ; Lehmann, Michael L. ; Cho, Hyeseon ; He, Jianping ; Li, Peng ; Kim, Bong-Hyun ; Larochelle, Andre ; Kelsall, Brian L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c564t-7f47c4e78b0bc8b2183ce7bb2b82a7bc556ea84757edc48c3d339e4d48f39f63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Allergology</topic><topic>Animals</topic><topic>Antibodies</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>CCR2 protein</topic><topic>CD11c antigen</topic><topic>CD11c Antigen - metabolism</topic><topic>Cell Differentiation</topic><topic>Cells, Cultured</topic><topic>Colon</topic><topic>Colon - immunology</topic><topic>Dendritic cells</topic><topic>Dendritic Cells - immunology</topic><topic>Gastroenterology</topic><topic>Gene expression</topic><topic>Gene Ontology</topic><topic>Gene Regulatory Networks</topic><topic>Germfree</topic><topic>Homeostasis</topic><topic>Immunology</topic><topic>Intestine</topic><topic>Lamina propria</topic><topic>Lectins, C-Type - genetics</topic><topic>Lectins, C-Type - metabolism</topic><topic>Leukocytes (mononuclear)</topic><topic>Localization</topic><topic>Macromolecules</topic><topic>Macrophages</topic><topic>Macrophages - immunology</topic><topic>Mannose Receptor</topic><topic>Mannose-Binding Lectins - genetics</topic><topic>Mannose-Binding Lectins - metabolism</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Microbiota</topic><topic>Monocyte chemoattractant protein 1</topic><topic>Myeloid cells</topic><topic>Myeloid Cells - physiology</topic><topic>Phagocytes</topic><topic>Phagocytosis - genetics</topic><topic>Phenotype</topic><topic>Receptors, Cell Surface - genetics</topic><topic>Receptors, Cell Surface - metabolism</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Sequence Analysis, RNA</topic><topic>Single-Cell Analysis</topic><topic>Specific pathogen free</topic><topic>Transcription factors</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kang, Byunghyun</creatorcontrib><creatorcontrib>Alvarado, Luigi J.</creatorcontrib><creatorcontrib>Kim, Teayong</creatorcontrib><creatorcontrib>Lehmann, Michael L.</creatorcontrib><creatorcontrib>Cho, Hyeseon</creatorcontrib><creatorcontrib>He, Jianping</creatorcontrib><creatorcontrib>Li, Peng</creatorcontrib><creatorcontrib>Kim, Bong-Hyun</creatorcontrib><creatorcontrib>Larochelle, Andre</creatorcontrib><creatorcontrib>Kelsall, Brian L.</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Immunology Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Mucosal immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kang, Byunghyun</au><au>Alvarado, Luigi J.</au><au>Kim, Teayong</au><au>Lehmann, Michael L.</au><au>Cho, Hyeseon</au><au>He, Jianping</au><au>Li, Peng</au><au>Kim, Bong-Hyun</au><au>Larochelle, Andre</au><au>Kelsall, Brian L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Commensal microbiota drive the functional diversification of colon macrophages</atitle><jtitle>Mucosal immunology</jtitle><stitle>Mucosal Immunol</stitle><addtitle>Mucosal Immunol</addtitle><date>2020-03-01</date><risdate>2020</risdate><volume>13</volume><issue>2</issue><spage>216</spage><epage>229</epage><pages>216-229</pages><issn>1933-0219</issn><eissn>1935-3456</eissn><abstract>Mononuclear phagocytes are a heterogeneous population of leukocytes essential for immune homeostasis that develop tissue-specific functions due to unique transcriptional programs driven by local microenvironmental cues. Single cell RNA sequencing (scRNA-seq) of colonic myeloid cells from specific pathogen free (SPF) and germ-free (GF) C57BL/6 mice revealed extensive heterogeneity of both colon macrophages (MPs) and dendritic cells (DCs). Modeling of developmental pathways combined with inference of gene regulatory networks indicate two major trajectories from common CCR2
+
precursors resulting in colon MP populations with unique transcription factors and downstream target genes. Compared to SPF mice, GF mice had decreased numbers of total colon MPs, as well as selective proportional decreases of two major CD11c
+
CD206
int
CD121b
+
and CD11c
−
CD206
hi
CD121b
−
colon MP populations, whereas DC numbers and proportions were not different. Importantly, these two major colon MP populations were clearly distinct from other colon MP populations regarding their gene expression profile, localization within the lamina propria (LP) and ability to phagocytose macromolecules from the blood. These data uncover the diversity of intestinal myeloid cell populations at the molecular level and highlight the importance of microbiota on the unique developmental as well as anatomical and functional fates of colon MPs.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>31772323</pmid><doi>10.1038/s41385-019-0228-3</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Mucosal immunology, 2020-03, Vol.13 (2), p.216-229 |
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| language | eng |
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| source | MEDLINE; EZB-FREE-00999 freely available EZB journals; ProQuest Central UK/Ireland; Alma/SFX Local Collection |
| subjects | Allergology Animals Antibodies Biomedical and Life Sciences Biomedicine CCR2 protein CD11c antigen CD11c Antigen - metabolism Cell Differentiation Cells, Cultured Colon Colon - immunology Dendritic cells Dendritic Cells - immunology Gastroenterology Gene expression Gene Ontology Gene Regulatory Networks Germfree Homeostasis Immunology Intestine Lamina propria Lectins, C-Type - genetics Lectins, C-Type - metabolism Leukocytes (mononuclear) Localization Macromolecules Macrophages Macrophages - immunology Mannose Receptor Mannose-Binding Lectins - genetics Mannose-Binding Lectins - metabolism Mice Mice, Inbred C57BL Mice, Knockout Microbiota Monocyte chemoattractant protein 1 Myeloid cells Myeloid Cells - physiology Phagocytes Phagocytosis - genetics Phenotype Receptors, Cell Surface - genetics Receptors, Cell Surface - metabolism Ribonucleic acid RNA Sequence Analysis, RNA Single-Cell Analysis Specific pathogen free Transcription factors Transcriptome |
| title | Commensal microbiota drive the functional diversification of colon macrophages |
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