Homeostatic Control of Sebaceous Glands by Innate Lymphoid Cells Regulates Commensal Bacteria Equilibrium
Immune cells and epithelium form sophisticated barrier systems in symbiotic relationships with microbiota. Evidence suggests that immune cells can sense microbes through intact barriers, but regulation of microbial commensalism remain largely unexplored. Here, we uncovered spatial compartmentalizati...
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| Published in: | Cell Vol. 176; no. 5; p. 982 |
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| Format: | Journal Article |
| Language: | English |
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21.02.2019
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| ISSN: | 1097-4172, 1097-4172 |
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| Abstract | Immune cells and epithelium form sophisticated barrier systems in symbiotic relationships with microbiota. Evidence suggests that immune cells can sense microbes through intact barriers, but regulation of microbial commensalism remain largely unexplored. Here, we uncovered spatial compartmentalization of skin-resident innate lymphoid cells (ILCs) and modulation of sebaceous glands by a subset of RORγt
ILCs residing within hair follicles in close proximity to sebaceous glands. Their persistence in skin required IL-7 and thymic stromal lymphopoietin, and localization was dependent on the chemokine receptor CCR6. ILC subsets expressed TNF receptor ligands, which limited sebocyte growth by repressing Notch signaling pathway. Consequently, loss of ILCs resulted in sebaceous hyperplasia with increased production of antimicrobial lipids and restricted commensalism of Gram-positive bacterial communities. Thus, epithelia-derived signals maintain skin-resident ILCs that regulate microbial commensalism through sebaceous gland-mediated tuning of the barrier surface, highlighting an immune-epithelia circuitry that facilitates host-microbe symbiosis. |
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| AbstractList | Immune cells and epithelium form sophisticated barrier systems in symbiotic relationships with microbiota. Evidence suggests that immune cells can sense microbes through intact barriers, but regulation of microbial commensalism remain largely unexplored. Here, we uncovered spatial compartmentalization of skin-resident innate lymphoid cells (ILCs) and modulation of sebaceous glands by a subset of RORγt
ILCs residing within hair follicles in close proximity to sebaceous glands. Their persistence in skin required IL-7 and thymic stromal lymphopoietin, and localization was dependent on the chemokine receptor CCR6. ILC subsets expressed TNF receptor ligands, which limited sebocyte growth by repressing Notch signaling pathway. Consequently, loss of ILCs resulted in sebaceous hyperplasia with increased production of antimicrobial lipids and restricted commensalism of Gram-positive bacterial communities. Thus, epithelia-derived signals maintain skin-resident ILCs that regulate microbial commensalism through sebaceous gland-mediated tuning of the barrier surface, highlighting an immune-epithelia circuitry that facilitates host-microbe symbiosis. Immune cells and epithelium form sophisticated barrier systems in symbiotic relationships with microbiota. Evidence suggests that immune cells can sense microbes through intact barriers, but regulation of microbial commensalism remain largely unexplored. Here, we uncovered spatial compartmentalization of skin-resident innate lymphoid cells (ILCs) and modulation of sebaceous glands by a subset of RORγt+ ILCs residing within hair follicles in close proximity to sebaceous glands. Their persistence in skin required IL-7 and thymic stromal lymphopoietin, and localization was dependent on the chemokine receptor CCR6. ILC subsets expressed TNF receptor ligands, which limited sebocyte growth by repressing Notch signaling pathway. Consequently, loss of ILCs resulted in sebaceous hyperplasia with increased production of antimicrobial lipids and restricted commensalism of Gram-positive bacterial communities. Thus, epithelia-derived signals maintain skin-resident ILCs that regulate microbial commensalism through sebaceous gland-mediated tuning of the barrier surface, highlighting an immune-epithelia circuitry that facilitates host-microbe symbiosis.Immune cells and epithelium form sophisticated barrier systems in symbiotic relationships with microbiota. Evidence suggests that immune cells can sense microbes through intact barriers, but regulation of microbial commensalism remain largely unexplored. Here, we uncovered spatial compartmentalization of skin-resident innate lymphoid cells (ILCs) and modulation of sebaceous glands by a subset of RORγt+ ILCs residing within hair follicles in close proximity to sebaceous glands. Their persistence in skin required IL-7 and thymic stromal lymphopoietin, and localization was dependent on the chemokine receptor CCR6. ILC subsets expressed TNF receptor ligands, which limited sebocyte growth by repressing Notch signaling pathway. Consequently, loss of ILCs resulted in sebaceous hyperplasia with increased production of antimicrobial lipids and restricted commensalism of Gram-positive bacterial communities. Thus, epithelia-derived signals maintain skin-resident ILCs that regulate microbial commensalism through sebaceous gland-mediated tuning of the barrier surface, highlighting an immune-epithelia circuitry that facilitates host-microbe symbiosis. |
| Author | Kim, Do Young Cui, Chang-Yi Leonard, Warren J Sakamoto, Keiko Moro, Kazuyo Zhu, Jinfang Horiuchi, Keisuke Voisin, Benjamin Schlessinger, David Nagao, Keisuke Kobayashi, Tetsuro Kennedy, Elizabeth A Shih, Han-Yu Doebel, Thomas Jo, Jay-Hyun Nakae, Susumu Kong, Heidi H Truong, Amanda |
| Author_xml | – sequence: 1 givenname: Tetsuro surname: Kobayashi fullname: Kobayashi, Tetsuro organization: Cutaneous Leukocyte Biology Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA – sequence: 2 givenname: Benjamin surname: Voisin fullname: Voisin, Benjamin organization: Cutaneous Leukocyte Biology Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA – sequence: 3 givenname: Do Young surname: Kim fullname: Kim, Do Young organization: Cutaneous Leukocyte Biology Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA; Department of Dermatology and Cutaneous Biology Research Institute, Yonsei University College of Medicine, Seoul, Republic of Korea – sequence: 4 givenname: Elizabeth A surname: Kennedy fullname: Kennedy, Elizabeth A organization: Cutaneous Microbiome and Inflammation Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA – sequence: 5 givenname: Jay-Hyun surname: Jo fullname: Jo, Jay-Hyun organization: Cutaneous Microbiome and Inflammation Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA – sequence: 6 givenname: Han-Yu surname: Shih fullname: Shih, Han-Yu organization: Laboratory of Immunology, Molecular Immunology and Inflammation Branch, NIAMS, NIH, Bethesda, MD 20892, USA – sequence: 7 givenname: Amanda surname: Truong fullname: Truong, Amanda organization: Cutaneous Leukocyte Biology Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA – sequence: 8 givenname: Thomas surname: Doebel fullname: Doebel, Thomas organization: Cutaneous Leukocyte Biology Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA – sequence: 9 givenname: Keiko surname: Sakamoto fullname: Sakamoto, Keiko organization: Cutaneous Leukocyte Biology Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA – sequence: 10 givenname: Chang-Yi surname: Cui fullname: Cui, Chang-Yi organization: Human Genetics Section, Laboratory of Genetics and Genomics, NIA, NIH, Baltimore, MD 21224, USA – sequence: 11 givenname: David surname: Schlessinger fullname: Schlessinger, David organization: Human Genetics Section, Laboratory of Genetics and Genomics, NIA, NIH, Baltimore, MD 21224, USA – sequence: 12 givenname: Kazuyo surname: Moro fullname: Moro, Kazuyo organization: Laboratory for Innate Immune Systems, RIKEN Center for Integrative Medical Sciences, Yokohama, 230-0045, Japan – sequence: 13 givenname: Susumu surname: Nakae fullname: Nakae, Susumu organization: Laboratory of Systems Biology, Center for Experimental Medicine and Systems Biology, The Institute of Medical Science, The University of Tokyo, Tokyo, 113-8654, Japan – sequence: 14 givenname: Keisuke surname: Horiuchi fullname: Horiuchi, Keisuke organization: Department of Orthopedic Surgery, National Defense Medical College, Tokorozawa, 359-8513, Japan – sequence: 15 givenname: Jinfang surname: Zhu fullname: Zhu, Jinfang organization: Molecular and Cellular Immunoregulation Section, Laboratory of Immune System Biology, NIAID, NIH, Bethesda, MD 20892, USA – sequence: 16 givenname: Warren J surname: Leonard fullname: Leonard, Warren J organization: Laboratory of Molecular Immunology and Immunology Center, NHLBI, NIH, Bethesda, MD 20892, USA – sequence: 17 givenname: Heidi H surname: Kong fullname: Kong, Heidi H organization: Cutaneous Microbiome and Inflammation Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA – sequence: 18 givenname: Keisuke surname: Nagao fullname: Nagao, Keisuke email: keisuke.nagao@nih.gov organization: Cutaneous Leukocyte Biology Section, Dermatology Branch, NIAMS, NIH, Bethesda, MD 20892, USA. Electronic address: keisuke.nagao@nih.gov |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30712873$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Animals Bacteria - metabolism Cytokines - metabolism Epithelium - immunology Hair Follicle - metabolism Hair Follicle - microbiology Immunity, Innate Interleukin-7 - metabolism Lymphocytes - immunology Lymphocytes - metabolism Male Mice Mice, Inbred C57BL Mice, Knockout Microbiota - immunology Receptors, CCR6 - metabolism Receptors, Notch - metabolism Receptors, Tumor Necrosis Factor - metabolism Sebaceous Glands - immunology Sebaceous Glands - metabolism Sebaceous Glands - microbiology Skin - metabolism Skin Physiological Phenomena Symbiosis Thymic Stromal Lymphopoietin |
| Title | Homeostatic Control of Sebaceous Glands by Innate Lymphoid Cells Regulates Commensal Bacteria Equilibrium |
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