Microbial bile acid metabolites modulate gut RORγ+ regulatory T cell homeostasis
The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules 1 . Primary bile acids (BAs) are synthesized within hepatocytes and released into the duodenum to facilitate absorption of lipids or fat-soluble vitamins 2 . So...
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| Published in | Nature (London) Vol. 577; no. 7790; pp. 410 - 415 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
16.01.2020
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules
1
. Primary bile acids (BAs) are synthesized within hepatocytes and released into the duodenum to facilitate absorption of lipids or fat-soluble vitamins
2
. Some BAs (approximately 5%) escape into the colon, where gut commensal bacteria convert them into various intestinal BAs
2
that are important hormones that regulate host cholesterol metabolism and energy balance via several nuclear receptors and/or G-protein-coupled receptors
3
,
4
. These receptors have pivotal roles in shaping host innate immune responses
1
,
5
. However, the effect of this host–microorganism biliary network on the adaptive immune system remains poorly characterized. Here we report that both dietary and microbial factors influence the composition of the gut BA pool and modulate an important population of colonic FOXP3
+
regulatory T (T
reg
) cells expressing the transcription factor RORγ. Genetic abolition of BA metabolic pathways in individual gut symbionts significantly decreases this T
reg
cell population. Restoration of the intestinal BA pool increases colonic RORγ
+
T
reg
cell counts and ameliorates host susceptibility to inflammatory colitis via BA nuclear receptors. Thus, a pan-genomic biliary network interaction between hosts and their bacterial symbionts can control host immunological homeostasis via the resulting metabolites.
Both dietary and microbial factors influence the composition of the gut bile acid pool, which in turn modulates the frequencies and functionalities of RORγ-expressing colonic FOXP3
+
regulatory T cells, contributing to protection from inflammatory colitis. |
|---|---|
| AbstractList | The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules
1
. Primary bile acids (BAs) are synthesized within hepatocytes and released into the duodenum to facilitate absorption of lipids or fat-soluble vitamins
2
. Some BAs (approximately 5%) escape into the colon, where gut commensal bacteria convert them into various intestinal BAs
2
that are important hormones that regulate host cholesterol metabolism and energy balance via several nuclear receptors and/or G-protein-coupled receptors
3
,
4
. These receptors have pivotal roles in shaping host innate immune responses
1
,
5
. However, the effect of this host–microorganism biliary network on the adaptive immune system remains poorly characterized. Here we report that both dietary and microbial factors influence the composition of the gut BA pool and modulate an important population of colonic FOXP3
+
regulatory T (T
reg
) cells expressing the transcription factor RORγ. Genetic abolition of BA metabolic pathways in individual gut symbionts significantly decreases this T
reg
cell population. Restoration of the intestinal BA pool increases colonic RORγ
+
T
reg
cell counts and ameliorates host susceptibility to inflammatory colitis via BA nuclear receptors. Thus, a pan-genomic biliary network interaction between hosts and their bacterial symbionts can control host immunological homeostasis via the resulting metabolites.
Both dietary and microbial factors influence the composition of the gut bile acid pool, which in turn modulates the frequencies and functionalities of RORγ-expressing colonic FOXP3
+
regulatory T cells, contributing to protection from inflammatory colitis. The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules 1 . Primary bile acids (BAs) are synthesized within hepatocytes and released into the duodenum to facilitate absorption of lipids or fat-soluble vitamins 2 . Some BAs (~5%) escape into the colon, where gut commensal bacteria convert them into a variety of intestinal BAs 2 that are important hormones regulating host cholesterol metabolism and energy balance via several nuclear receptors and/or G protein–coupled receptors 3 , 4 . These receptors play pivotal roles in shaping host innate immune responses 1 , 5 . However, the impact of this host–microbe biliary network on the adaptive immune system remains poorly characterized. Here we report that both dietary and microbial factors influence the composition of the gut BA pool and modulate an important population of colonic Foxp3 + regulatory T cells (Tregs) expressing the transcriptional factor RORγ. Genetic abolition of BA metabolic pathways in individual gut symbionts significantly decreases this Treg population. Restoration of the intestinal BA pool increases colonic RORγ + Treg levels and ameliorates host susceptibility to inflammatory colitis via BA nuclear receptors. Thus, a pan-genomic biliary network interaction between hosts and their bacterial symbionts can control host immunologic homeostasis via the resulting metabolites. The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules. Primary bile acids (BAs) are synthesized within hepatocytes and released into the duodenum to facilitate absorption of lipids or fat-soluble vitamins. Some BAs (approximately 5%) escape into the colon, where gut commensal bacteria convert them into various intestinal BAs2 that are important hormones that regulate host cholesterol metabolism and energy balance via several nuclear receptors and/or G-protein-coupled receptors. These receptors have pivotal roles in shaping host innate immune responses. However, the effect of this host-microorganism biliary network on the adaptive immune system remains poorly characterized. Here we report that both dietary and microbial factors influence the composition of the gut BA pool and modulate an important population of colonic FOXP3+ regulatory T (Treg) cells expressing the transcription factor RORγ. Genetic abolition of BA metabolic pathways in individual gut symbionts significantly decreases this Treg cell population. Restoration of the intestinal BA pool increases colonic RORγ+ Treg cell counts and ameliorates host susceptibility to inflammatory colitis via BA nuclear receptors. Thus, a pan-genomic biliary network interaction between hosts and their bacterial symbionts can control host immunological homeostasis via the resulting metabolites. The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules . Primary bile acids (BAs) are synthesized within hepatocytes and released into the duodenum to facilitate absorption of lipids or fat-soluble vitamins . Some BAs (approximately 5%) escape into the colon, where gut commensal bacteria convert them into various intestinal BAs that are important hormones that regulate host cholesterol metabolism and energy balance via several nuclear receptors and/or G-protein-coupled receptors . These receptors have pivotal roles in shaping host innate immune responses . However, the effect of this host-microorganism biliary network on the adaptive immune system remains poorly characterized. Here we report that both dietary and microbial factors influence the composition of the gut BA pool and modulate an important population of colonic FOXP3 regulatory T (T ) cells expressing the transcription factor RORγ. Genetic abolition of BA metabolic pathways in individual gut symbionts significantly decreases this T cell population. Restoration of the intestinal BA pool increases colonic RORγ T cell counts and ameliorates host susceptibility to inflammatory colitis via BA nuclear receptors. Thus, a pan-genomic biliary network interaction between hosts and their bacterial symbionts can control host immunological homeostasis via the resulting metabolites. |
| Author | Zhang, Yanbo Oh, Sungwhan F. Song, Xinyang Benoist, Christophe Geva-Zatorsky, Naama Mathis, Diane Kasper, Dennis L. Jupp, Ray Sun, Ximei Zheng, Wen Wu, Meng |
| AuthorAffiliation | 3 UCB Pharma, Slough, Berkshire SL1 3WE, UK 1 Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA 2 Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA |
| AuthorAffiliation_xml | – name: 2 Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 3 UCB Pharma, Slough, Berkshire SL1 3WE, UK – name: 1 Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA |
| Author_xml | – sequence: 1 givenname: Xinyang surname: Song fullname: Song, Xinyang organization: Department of Immunology, Blavatnik Institute, Harvard Medical School – sequence: 2 givenname: Ximei surname: Sun fullname: Sun, Ximei organization: Department of Immunology, Blavatnik Institute, Harvard Medical School – sequence: 3 givenname: Sungwhan F. surname: Oh fullname: Oh, Sungwhan F. organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, Harvard Medical School – sequence: 4 givenname: Meng surname: Wu fullname: Wu, Meng organization: Department of Immunology, Blavatnik Institute, Harvard Medical School – sequence: 5 givenname: Yanbo surname: Zhang fullname: Zhang, Yanbo organization: Department of Immunology, Blavatnik Institute, Harvard Medical School – sequence: 6 givenname: Wen surname: Zheng fullname: Zheng, Wen organization: Department of Immunology, Blavatnik Institute, Harvard Medical School – sequence: 7 givenname: Naama surname: Geva-Zatorsky fullname: Geva-Zatorsky, Naama organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Department of Cell Biology and Cancer Science, Rappaport Faculty of Medicine, Technion Integrated Cancer Center, Technion–Israel Institute of Technology – sequence: 8 givenname: Ray surname: Jupp fullname: Jupp, Ray organization: UCB Pharma – sequence: 9 givenname: Diane surname: Mathis fullname: Mathis, Diane organization: Department of Immunology, Blavatnik Institute, Harvard Medical School – sequence: 10 givenname: Christophe surname: Benoist fullname: Benoist, Christophe organization: Department of Immunology, Blavatnik Institute, Harvard Medical School – sequence: 11 givenname: Dennis L. surname: Kasper fullname: Kasper, Dennis L. email: dennis_kasper@hms.harvard.edu organization: Department of Immunology, Blavatnik Institute, Harvard Medical School |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31875848$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this work. D.L.K. and X.S. designed the experiments and wrote the manuscript; X.S., X.S., S.F.O., M.W., Y.Z., W.Z., and N.G.Z. conducted or helped with the experiments; X.S., X.S., and Y.Z. analyzed the data; R.J., D.M., and C.B. were involved in data discussions and edited the manuscript; and D.L.K. supervised the study. Present address: Department of Cell Biology and Cancer Science, Rappaport Faculty of Medicine, Technion Integrated Cancer Center, Technion–Israel Institute of Technology, 1 Efron St. Bat Galim, Haifa, 3525433, Israel Author contributions |
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| Snippet | The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules
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. Primary bile... The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules . Primary bile... The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules. Primary bile acids... The metabolic pathways encoded by the human gut microbiome constantly interact with host gene products through numerous bioactive molecules 1 . Primary bile... |
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| Title | Microbial bile acid metabolites modulate gut RORγ+ regulatory T cell homeostasis |
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