Treg-Cell Control of a CXCL5-IL-17 Inflammatory Axis Promotes Hair-Follicle-Stem-Cell Differentiation During Skin-Barrier Repair
Restoration of barrier-tissue integrity after injury is dependent on the function of immune cells and stem cells (SCs) residing in the tissue. In response to skin injury, hair-follicle stem cells (HFSCs), normally poised for hair generation, are recruited to the site of injury and differentiate into...
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| Veröffentlicht in: | Immunity (Cambridge, Mass.) Mass.), 2019-03, Vol.50 (3), p.655-667.e4 |
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| creator | Mathur, Anubhav N. Zirak, Bahar Boothby, Ian C. Tan, Madge Cohen, Jarish N. Mauro, Thea M. Mehta, Pooja Lowe, Margaret M. Abbas, Abul K. Ali, Niwa Rosenblum, Michael D. |
| description | Restoration of barrier-tissue integrity after injury is dependent on the function of immune cells and stem cells (SCs) residing in the tissue. In response to skin injury, hair-follicle stem cells (HFSCs), normally poised for hair generation, are recruited to the site of injury and differentiate into cells that repair damaged epithelium. We used a SC fate-mapping approach to examine the contribution of regulatory T (Treg) cells to epidermal-barrier repair after injury. Depletion of Treg cells impaired skin-barrier regeneration and was associated with a Th17 inflammatory response and failed HFSC differentiation. In this setting, damaged epithelial cells preferentially expressed the neutrophil chemoattractant CXCL5, and blockade of CXCL5 or neutrophil depletion restored barrier function and SC differentiation after epidermal injury. Thus, Treg-cell regulation of localized inflammation enables HFSC differentiation and, thereby, skin-barrier regeneration, with implications for the maintenance and repair of other barrier tissues.
[Display omitted]
•Treg cells promote epidermal regeneration after injury•Treg cells control a CXCL5-IL-17 axis of inflammation during epidermal repair•Treg-cell control of CXCL5 and IL-17 diverts HFSC differentiation toward IFE cells•CXCL5 or IL-17 neutralization restores HFSC differentiation in Treg-depleted mice
In response to skin injury, hair-follicle stem cells (HFSCs) differentiate into epithelial cells that contribute to the repair of damaged epithelium. Mathur et al. show that regulatory T cells facilitate HFSC differentiation via the control of the local inflammatory environment and, specifically, the prevention of an over-exuberant Th17 and neutrophil response mediated by CXCL5. |
| doi_str_mv | 10.1016/j.immuni.2019.02.013 |
| format | Article |
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[Display omitted]
•Treg cells promote epidermal regeneration after injury•Treg cells control a CXCL5-IL-17 axis of inflammation during epidermal repair•Treg-cell control of CXCL5 and IL-17 diverts HFSC differentiation toward IFE cells•CXCL5 or IL-17 neutralization restores HFSC differentiation in Treg-depleted mice
In response to skin injury, hair-follicle stem cells (HFSCs) differentiate into epithelial cells that contribute to the repair of damaged epithelium. Mathur et al. show that regulatory T cells facilitate HFSC differentiation via the control of the local inflammatory environment and, specifically, the prevention of an over-exuberant Th17 and neutrophil response mediated by CXCL5.</description><identifier>ISSN: 1074-7613</identifier><identifier>ISSN: 1097-4180</identifier><identifier>EISSN: 1097-4180</identifier><identifier>DOI: 10.1016/j.immuni.2019.02.013</identifier><identifier>PMID: 30893588</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; barrier repair ; Cell differentiation ; Cell Differentiation - physiology ; Cell fate ; Chemokine CXCL5 - metabolism ; CXCL5 ; Damage ; Data analysis ; Depletion ; Differentiation (biology) ; Epidermal Cells - metabolism ; epidermis ; Epidermis - metabolism ; Epithelial cells ; Epithelial Cells - metabolism ; Epithelium ; Experiments ; Fate maps ; Flow cytometry ; Hair ; Hair - metabolism ; Hair Follicle - metabolism ; hair follicle stem cells ; Helper cells ; Histology ; IL-17 ; Immune system ; Inflammation ; Inflammatory response ; Interleukin 17 ; Interleukin-17 - metabolism ; Ligands ; Lrg5 ; Lymphocytes ; Lymphocytes T ; Mapping ; Mice ; Mice, Inbred C57BL ; Regeneration ; Regeneration - physiology ; regulatory T cell (Treg) ; Repair ; Restoration ; Skin ; Skin injuries ; Software ; Statistical analysis ; stem cell ; Stem cells ; Stem Cells - metabolism ; T-Lymphocytes, Regulatory - metabolism ; Tissues</subject><ispartof>Immunity (Cambridge, Mass.), 2019-03, Vol.50 (3), p.655-667.e4</ispartof><rights>2019 Elsevier Inc.</rights><rights>Copyright © 2019 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Mar 19, 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c553t-27010d52f3c866b3511e4d22d71cff806f9bb9bffbfc1cb404f3d1cd68c1284a3</citedby><cites>FETCH-LOGICAL-c553t-27010d52f3c866b3511e4d22d71cff806f9bb9bffbfc1cb404f3d1cd68c1284a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1074761319300809$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30893588$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mathur, Anubhav N.</creatorcontrib><creatorcontrib>Zirak, Bahar</creatorcontrib><creatorcontrib>Boothby, Ian C.</creatorcontrib><creatorcontrib>Tan, Madge</creatorcontrib><creatorcontrib>Cohen, Jarish N.</creatorcontrib><creatorcontrib>Mauro, Thea M.</creatorcontrib><creatorcontrib>Mehta, Pooja</creatorcontrib><creatorcontrib>Lowe, Margaret M.</creatorcontrib><creatorcontrib>Abbas, Abul K.</creatorcontrib><creatorcontrib>Ali, Niwa</creatorcontrib><creatorcontrib>Rosenblum, Michael D.</creatorcontrib><title>Treg-Cell Control of a CXCL5-IL-17 Inflammatory Axis Promotes Hair-Follicle-Stem-Cell Differentiation During Skin-Barrier Repair</title><title>Immunity (Cambridge, Mass.)</title><addtitle>Immunity</addtitle><description>Restoration of barrier-tissue integrity after injury is dependent on the function of immune cells and stem cells (SCs) residing in the tissue. In response to skin injury, hair-follicle stem cells (HFSCs), normally poised for hair generation, are recruited to the site of injury and differentiate into cells that repair damaged epithelium. We used a SC fate-mapping approach to examine the contribution of regulatory T (Treg) cells to epidermal-barrier repair after injury. Depletion of Treg cells impaired skin-barrier regeneration and was associated with a Th17 inflammatory response and failed HFSC differentiation. In this setting, damaged epithelial cells preferentially expressed the neutrophil chemoattractant CXCL5, and blockade of CXCL5 or neutrophil depletion restored barrier function and SC differentiation after epidermal injury. Thus, Treg-cell regulation of localized inflammation enables HFSC differentiation and, thereby, skin-barrier regeneration, with implications for the maintenance and repair of other barrier tissues.
[Display omitted]
•Treg cells promote epidermal regeneration after injury•Treg cells control a CXCL5-IL-17 axis of inflammation during epidermal repair•Treg-cell control of CXCL5 and IL-17 diverts HFSC differentiation toward IFE cells•CXCL5 or IL-17 neutralization restores HFSC differentiation in Treg-depleted mice
In response to skin injury, hair-follicle stem cells (HFSCs) differentiate into epithelial cells that contribute to the repair of damaged epithelium. Mathur et al. show that regulatory T cells facilitate HFSC differentiation via the control of the local inflammatory environment and, specifically, the prevention of an over-exuberant Th17 and neutrophil response mediated by CXCL5.</description><subject>Animals</subject><subject>barrier repair</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - physiology</subject><subject>Cell fate</subject><subject>Chemokine CXCL5 - metabolism</subject><subject>CXCL5</subject><subject>Damage</subject><subject>Data analysis</subject><subject>Depletion</subject><subject>Differentiation (biology)</subject><subject>Epidermal Cells - metabolism</subject><subject>epidermis</subject><subject>Epidermis - metabolism</subject><subject>Epithelial cells</subject><subject>Epithelial Cells - metabolism</subject><subject>Epithelium</subject><subject>Experiments</subject><subject>Fate maps</subject><subject>Flow cytometry</subject><subject>Hair</subject><subject>Hair - metabolism</subject><subject>Hair Follicle - metabolism</subject><subject>hair follicle stem cells</subject><subject>Helper cells</subject><subject>Histology</subject><subject>IL-17</subject><subject>Immune system</subject><subject>Inflammation</subject><subject>Inflammatory response</subject><subject>Interleukin 17</subject><subject>Interleukin-17 - metabolism</subject><subject>Ligands</subject><subject>Lrg5</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Mapping</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Regeneration</subject><subject>Regeneration - physiology</subject><subject>regulatory T cell (Treg)</subject><subject>Repair</subject><subject>Restoration</subject><subject>Skin</subject><subject>Skin injuries</subject><subject>Software</subject><subject>Statistical analysis</subject><subject>stem cell</subject><subject>Stem cells</subject><subject>Stem Cells - metabolism</subject><subject>T-Lymphocytes, Regulatory - metabolism</subject><subject>Tissues</subject><issn>1074-7613</issn><issn>1097-4180</issn><issn>1097-4180</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU1v1DAQhiMEoqXwDxCyxIWLg8d2vi5IJaV0pZVAtEjcLMcZV14Se2sniN746Xi1hQMHTp7D874ezVMUL4GVwKB-uyvdPK_elZxBVzJeMhCPilNgXUMltOzxYW4kbWoQJ8WzlHaMgaw69rQ4EaztRNW2p8Wvm4i3tMdpIn3wSwwTCZZo0n_rtxXdbCk0ZOPtpOdZLyHek_OfLpHPMcxhwUSutIv0MkyTMxPS6wXnY9eFsxYj-sXpxQVPLtbo_C25_u48fa9jdBjJF9zn9PPiidVTwhcP71nx9fLDTX9Ft58-bvrzLTVVJRbKGwZsrLgVpq3rQVQAKEfOxwaMtS2rbTcM3WDtYA2YQTJpxQhmrFsDvJVanBVvjr37GO5WTIuaXTJ5V-0xrElx6CpeSSHqjL7-B92FNfq83YGSrK1l3WRKHikTQ0oRrdpHN-t4r4CpgyG1U0dD6mBIMa6yoRx79VC-DjOOf0N_lGTg3RHAfI0f-VAqGYfe4OgimkWNwf3_h99QcqMD</recordid><startdate>20190319</startdate><enddate>20190319</enddate><creator>Mathur, Anubhav N.</creator><creator>Zirak, Bahar</creator><creator>Boothby, Ian C.</creator><creator>Tan, Madge</creator><creator>Cohen, Jarish N.</creator><creator>Mauro, Thea M.</creator><creator>Mehta, Pooja</creator><creator>Lowe, Margaret M.</creator><creator>Abbas, Abul K.</creator><creator>Ali, Niwa</creator><creator>Rosenblum, Michael D.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7T7</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20190319</creationdate><title>Treg-Cell Control of a CXCL5-IL-17 Inflammatory Axis Promotes Hair-Follicle-Stem-Cell Differentiation During Skin-Barrier Repair</title><author>Mathur, Anubhav N. ; Zirak, Bahar ; Boothby, Ian C. ; Tan, Madge ; Cohen, Jarish N. ; Mauro, Thea M. ; Mehta, Pooja ; Lowe, Margaret M. ; Abbas, Abul K. ; Ali, Niwa ; Rosenblum, Michael D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c553t-27010d52f3c866b3511e4d22d71cff806f9bb9bffbfc1cb404f3d1cd68c1284a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>barrier repair</topic><topic>Cell differentiation</topic><topic>Cell Differentiation - physiology</topic><topic>Cell fate</topic><topic>Chemokine CXCL5 - metabolism</topic><topic>CXCL5</topic><topic>Damage</topic><topic>Data analysis</topic><topic>Depletion</topic><topic>Differentiation (biology)</topic><topic>Epidermal Cells - metabolism</topic><topic>epidermis</topic><topic>Epidermis - metabolism</topic><topic>Epithelial cells</topic><topic>Epithelial Cells - metabolism</topic><topic>Epithelium</topic><topic>Experiments</topic><topic>Fate maps</topic><topic>Flow cytometry</topic><topic>Hair</topic><topic>Hair - metabolism</topic><topic>Hair Follicle - metabolism</topic><topic>hair follicle stem cells</topic><topic>Helper cells</topic><topic>Histology</topic><topic>IL-17</topic><topic>Immune system</topic><topic>Inflammation</topic><topic>Inflammatory response</topic><topic>Interleukin 17</topic><topic>Interleukin-17 - metabolism</topic><topic>Ligands</topic><topic>Lrg5</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>Mapping</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Regeneration</topic><topic>Regeneration - physiology</topic><topic>regulatory T cell (Treg)</topic><topic>Repair</topic><topic>Restoration</topic><topic>Skin</topic><topic>Skin injuries</topic><topic>Software</topic><topic>Statistical analysis</topic><topic>stem cell</topic><topic>Stem cells</topic><topic>Stem Cells - metabolism</topic><topic>T-Lymphocytes, Regulatory - metabolism</topic><topic>Tissues</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mathur, Anubhav N.</creatorcontrib><creatorcontrib>Zirak, Bahar</creatorcontrib><creatorcontrib>Boothby, Ian C.</creatorcontrib><creatorcontrib>Tan, Madge</creatorcontrib><creatorcontrib>Cohen, Jarish N.</creatorcontrib><creatorcontrib>Mauro, Thea M.</creatorcontrib><creatorcontrib>Mehta, Pooja</creatorcontrib><creatorcontrib>Lowe, Margaret M.</creatorcontrib><creatorcontrib>Abbas, Abul K.</creatorcontrib><creatorcontrib>Ali, Niwa</creatorcontrib><creatorcontrib>Rosenblum, Michael D.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Immunity (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mathur, Anubhav N.</au><au>Zirak, Bahar</au><au>Boothby, Ian C.</au><au>Tan, Madge</au><au>Cohen, Jarish N.</au><au>Mauro, Thea M.</au><au>Mehta, Pooja</au><au>Lowe, Margaret M.</au><au>Abbas, Abul K.</au><au>Ali, Niwa</au><au>Rosenblum, Michael D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Treg-Cell Control of a CXCL5-IL-17 Inflammatory Axis Promotes Hair-Follicle-Stem-Cell Differentiation During Skin-Barrier Repair</atitle><jtitle>Immunity (Cambridge, Mass.)</jtitle><addtitle>Immunity</addtitle><date>2019-03-19</date><risdate>2019</risdate><volume>50</volume><issue>3</issue><spage>655</spage><epage>667.e4</epage><pages>655-667.e4</pages><issn>1074-7613</issn><issn>1097-4180</issn><eissn>1097-4180</eissn><abstract>Restoration of barrier-tissue integrity after injury is dependent on the function of immune cells and stem cells (SCs) residing in the tissue. In response to skin injury, hair-follicle stem cells (HFSCs), normally poised for hair generation, are recruited to the site of injury and differentiate into cells that repair damaged epithelium. We used a SC fate-mapping approach to examine the contribution of regulatory T (Treg) cells to epidermal-barrier repair after injury. Depletion of Treg cells impaired skin-barrier regeneration and was associated with a Th17 inflammatory response and failed HFSC differentiation. In this setting, damaged epithelial cells preferentially expressed the neutrophil chemoattractant CXCL5, and blockade of CXCL5 or neutrophil depletion restored barrier function and SC differentiation after epidermal injury. Thus, Treg-cell regulation of localized inflammation enables HFSC differentiation and, thereby, skin-barrier regeneration, with implications for the maintenance and repair of other barrier tissues.
[Display omitted]
•Treg cells promote epidermal regeneration after injury•Treg cells control a CXCL5-IL-17 axis of inflammation during epidermal repair•Treg-cell control of CXCL5 and IL-17 diverts HFSC differentiation toward IFE cells•CXCL5 or IL-17 neutralization restores HFSC differentiation in Treg-depleted mice
In response to skin injury, hair-follicle stem cells (HFSCs) differentiate into epithelial cells that contribute to the repair of damaged epithelium. Mathur et al. show that regulatory T cells facilitate HFSC differentiation via the control of the local inflammatory environment and, specifically, the prevention of an over-exuberant Th17 and neutrophil response mediated by CXCL5.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>30893588</pmid><doi>10.1016/j.immuni.2019.02.013</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animals barrier repair Cell differentiation Cell Differentiation - physiology Cell fate Chemokine CXCL5 - metabolism CXCL5 Damage Data analysis Depletion Differentiation (biology) Epidermal Cells - metabolism epidermis Epidermis - metabolism Epithelial cells Epithelial Cells - metabolism Epithelium Experiments Fate maps Flow cytometry Hair Hair - metabolism Hair Follicle - metabolism hair follicle stem cells Helper cells Histology IL-17 Immune system Inflammation Inflammatory response Interleukin 17 Interleukin-17 - metabolism Ligands Lrg5 Lymphocytes Lymphocytes T Mapping Mice Mice, Inbred C57BL Regeneration Regeneration - physiology regulatory T cell (Treg) Repair Restoration Skin Skin injuries Software Statistical analysis stem cell Stem cells Stem Cells - metabolism T-Lymphocytes, Regulatory - metabolism Tissues |
| title | Treg-Cell Control of a CXCL5-IL-17 Inflammatory Axis Promotes Hair-Follicle-Stem-Cell Differentiation During Skin-Barrier Repair |
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