Dendritic cell-derived hepcidin sequesters iron from the microbiota to promote mucosal healing
Bleeding and altered iron distribution occur in multiple gastrointestinal diseases, but the importance and regulation of these changes remain unclear. We found that hepcidin, the master regulator of systemic iron homeostasis, is required for tissue repair in the mouse intestine after experimental da...
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| Published in | Science (American Association for the Advancement of Science) Vol. 368; no. 6487; pp. 186 - 189 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
10.04.2020
American Association for the Advancement of Science (AAAS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Bleeding and altered iron distribution occur in multiple gastrointestinal diseases, but the importance and regulation of these changes remain unclear. We found that hepcidin, the master regulator of systemic iron homeostasis, is required for tissue repair in the mouse intestine after experimental damage. This effect was independent of hepatocyte-derived hepcidin or systemic iron levels. Rather, we identified conventional dendritic cells (cDCs) as a source of hepcidin that is induced by microbial stimulation in mice, prominent in the inflamed intestine of humans, and essential for tissue repair. cDC-derived hepcidin acted on ferroportin-expressing phagocytes to promote local iron sequestration, which regulated the microbiota and consequently facilitated intestinal repair. Collectively, these results identify a pathway whereby cDC-derived hepcidin promotes mucosal healing in the intestine through means of nutritional immunity. |
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| AbstractList | Anemia is a frequent complication of disorders such as inflammatory bowel disease, occurring in part as a result of increased bleeding into the intestine. Bessman
et al.
show that the peptide hormone hepcidin, which regulates systemic iron homeostasis, is required for intestinal repair in a mouse model of inflammatory bowel disease (see the Perspective by Rescigno). This effect was independent of hepatocyte-produced hepcidin and systemic iron levels. Instead, production of hepcidin by conventional dendritic cells was necessary and sufficient to promote local iron sequestration by macrophages, which in turn modulated the makeup of the gut microbiota to one with a more beneficial distribution of species.
Science
, this issue p.
186
; see also p.
129
Hepcidin, a master regulator of iron homeostasis, is released from immunological dendritic cells and required for intestinal tissue repair.
Bleeding and altered iron distribution occur in multiple gastrointestinal diseases, but the importance and regulation of these changes remain unclear. We found that hepcidin, the master regulator of systemic iron homeostasis, is required for tissue repair in the mouse intestine after experimental damage. This effect was independent of hepatocyte-derived hepcidin or systemic iron levels. Rather, we identified conventional dendritic cells (cDCs) as a source of hepcidin that is induced by microbial stimulation in mice, prominent in the inflamed intestine of humans, and essential for tissue repair. cDC-derived hepcidin acted on ferroportin-expressing phagocytes to promote local iron sequestration, which regulated the microbiota and consequently facilitated intestinal repair. Collectively, these results identify a pathway whereby cDC-derived hepcidin promotes mucosal healing in the intestine through means of nutritional immunity. Ironing out the details of mucosal healing Anemia is a frequent complication of disorders such as inflammatory bowel disease, occurring in part as a result of increased bleeding into the intestine. Bessman et al. show that the peptide hormone hepcidin, which regulates systemic iron homeostasis, is required for intestinal repair in a mouse model of inflammatory bowel disease (see the Perspective by Rescigno). This effect was independent of hepatocyte-produced hepcidin and systemic iron levels. Instead, production of hepcidin by conventional dendritic cells was necessary and sufficient to promote local iron sequestration by macrophages, which in turn modulated the makeup of the gut microbiota to one with a more beneficial distribution of species. Science , this issue p. 186 ; see also p. 129 Bleeding and altered iron distribution occur in multiple gastrointestinal diseases, but the importance and regulation of these changes remain unclear. We found that hepcidin, the master regulator of systemic iron homeostasis, is required for tissue repair in the mouse intestine after experimental damage. This effect was independent of hepatocyte-derived hepcidin or systemic iron levels. Rather, we identified conventional dendritic cells (cDCs) as a source of hepcidin that is induced by microbial stimulation in mice, prominent in the inflamed intestine of humans, and essential for tissue repair. cDC-derived hepcidin acted on ferroportin-expressing phagocytes to promote local iron sequestration, which regulated the microbiota and consequently facilitated intestinal repair. Collectively, these results identify a pathway whereby cDC-derived hepcidin promotes mucosal healing in the intestine through means of nutritional immunity. Ironing out the details of mucosal healingAnemia is a frequent complication of disorders such as inflammatory bowel disease, occurring in part as a result of increased bleeding into the intestine. Bessman et al. show that the peptide hormone hepcidin, which regulates systemic iron homeostasis, is required for intestinal repair in a mouse model of inflammatory bowel disease (see the Perspective by Rescigno). This effect was independent of hepatocyte-produced hepcidin and systemic iron levels. Instead, production of hepcidin by conventional dendritic cells was necessary and sufficient to promote local iron sequestration by macrophages, which in turn modulated the makeup of the gut microbiota to one with a more beneficial distribution of species.Science, this issue p. 186; see also p. 129Bleeding and altered iron distribution occur in multiple gastrointestinal diseases, but the importance and regulation of these changes remain unclear. We found that hepcidin, the master regulator of systemic iron homeostasis, is required for tissue repair in the mouse intestine after experimental damage. This effect was independent of hepatocyte-derived hepcidin or systemic iron levels. Rather, we identified conventional dendritic cells (cDCs) as a source of hepcidin that is induced by microbial stimulation in mice, prominent in the inflamed intestine of humans, and essential for tissue repair. cDC-derived hepcidin acted on ferroportin-expressing phagocytes to promote local iron sequestration, which regulated the microbiota and consequently facilitated intestinal repair. Collectively, these results identify a pathway whereby cDC-derived hepcidin promotes mucosal healing in the intestine through means of nutritional immunity. Bleeding and altered iron distribution occur in multiple gastrointestinal diseases, but the significance or regulation of these changes remains unclear. Here we report that hepcidin, the master regulator of systemic iron homeostasis, is required for tissue repair in the intestine following experimental damage. This effect was independent of hepatocyte-derived hepcidin or systemic iron levels. Rather, we identified that conventional dendritic cells (cDCs) are a source of hepcidin that is induced by microbial stimulation, prominent in the inflamed intestine of humans, and essential for tissue repair. Mechanistically, cDC-derived hepcidin acted on ferroportin-expressing phagocytes to promote local iron sequestration, which regulated the microbiota and subsequently facilitated intestinal repair. Collectively, these results identify a novel pathway whereby cDC-derived hepcidin promotes mucosal healing in the intestine via nutritional immunity. Dendritic cells produce an iron-regulatory factor that modulates the intestinal microbiota to promote mucosal healing. |
| Author | Peyssonnaux, Carole Putzel, Gregory G Sockolow, Robbyn E Mathieu, Jacques R R Sonnenberg, Gregory F Fung, Thomas C Fernandez, Keith C Vaulont, Sophie Louis, Sabine Bessman, Nicholas J Zumerle, Sara Lakhal-Littleton, Samira Ajami, Nadim J Sokol, Harry Arora, Manish Cloonan, Suzanne M Renassia, Cyril Moeller, Jesper B Zhou, Lei Austin, Christine Arvedson, Tara |
| AuthorAffiliation | 11 Department of Pediatrics, Division of Gastroenterology and Nutrition, Weill Cornell Medicine, Cornell University, New York, NY, USA 6 Department of Environmental Medicine and Public Health, Icahn School of Medicine at Mount Sinai, New York, NY 10029, United States 4 Université de Paris, INSERM U1016, Institut Cochin, CNRS UMR8104, 75014, Paris, France 13 Division of Pulmonary and Critical Care Medicine, Weill Cornell Medicine, Cornell University, New York, NY USA 2 Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology and Hepatology, Weill Cornell Medicine, Cornell University, New York, NY USA 5 Laboratory of Excellence GR-Ex, Paris, France 7 Department of Molecular Medicine, University of Southern Denmark, Odense, Denmark 9 Sorbonne Université, Inserm, Centre de Recherche Saint-Antoine, CRSA, AP-HP, Hôpital Saint Antoine, Service de Gastroenterologie, F-75012 Paris, France 12 Department of Physiology, Anatomy and Genetics, University of Oxford, OX1 3PT Oxford, Unit |
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| Copyright | Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works Distributed under a Creative Commons Attribution 4.0 International License |
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| Notes | Author contributions: N.J.B. and G.F.S. conceived the project. N.J.B., L.Z., T.C.F., K.C.F., J.B.M, J.R.R.M., C.R., S.L. and S.Z. performed experiments and analyzed data. S.V. and S.L-L. provided mouse models and expertise. H.S. performed pathological analyses. T.A. provided tools and expertise. C.P. provided mouse models, designed and supervised experiments. N.J.A. and G.G.P. analyzed sequencing data. C.A. and M.A. performed and analyzed iron imaging. R.E.S. provided essential advice and guidance. S.M.C. provided guidance and iron measurements. N.J.B. and G.F.S. wrote the manuscript, with input from all the authors. These authors contributed equally |
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| Snippet | Bleeding and altered iron distribution occur in multiple gastrointestinal diseases, but the importance and regulation of these changes remain unclear. We found... Anemia is a frequent complication of disorders such as inflammatory bowel disease, occurring in part as a result of increased bleeding into the intestine.... Ironing out the details of mucosal healingAnemia is a frequent complication of disorders such as inflammatory bowel disease, occurring in part as a result of... Ironing out the details of mucosal healing Anemia is a frequent complication of disorders such as inflammatory bowel disease, occurring in part as a result of... Bleeding and altered iron distribution occur in multiple gastrointestinal diseases, but the significance or regulation of these changes remains unclear. Here... |
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| SubjectTerms | Anemia Animal tissues Animals Bleeding Cation Transport Proteins - metabolism Dendritic cells Dendritic Cells - metabolism Dendritic structure Drawing and ironing Fecal Microbiota Transplantation Gastrointestinal diseases Gastrointestinal Microbiome Gene Deletion Geographical distribution Healing Hepcidin Hepcidins - genetics Hepcidins - metabolism Homeostasis Inflammatory bowel disease Inflammatory bowel diseases Inflammatory diseases Intestinal Diseases - microbiology Intestinal microflora Intestinal Mucosa - microbiology Intestinal Mucosa - physiology Intestine Iron Iron - metabolism Iron and steel making Life Sciences Macrophages Mice Mice, Mutant Strains Microbiota Microorganisms Mucosa Phagocytes Phagocytes - metabolism Repair |
| Title | Dendritic cell-derived hepcidin sequesters iron from the microbiota to promote mucosal healing |
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