Human gut bacteria produce TH17-modulating bile acid metabolites

The microbiota modulates gut immune homeostasis. Bacteria influence the development and function of host immune cells, including T helper cells expressing interleukin-17A (TH17 cells). We previously reported that the bile acid (BA) metabolite 3-oxolithocholic acid (3-oxoLCA) inhibits TH17 cell diffe...

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Published in:Nature (London) Vol. 603; no. 7903; pp. 907 - 912
Main Authors: Paik, Donggi, Yao, Lina, Zhang, Yancong, Bae, Sena, D’Agostino, Gabriel D., Zhang, Minghao, Kim, Eunha, Franzosa, Eric A., Avila-Pacheco, Julian, Bisanz, Jordan E., Rakowski, Christopher K., Vlamakis, Hera, Xavier, Ramnik J., Turnbaugh, Peter J., Longman, Randy S., Krout, Michael R., Clish, Clary B., Rastinejad, Fraydoon, Huttenhower, Curtis, Huh, Jun R., Devlin, A. Sloan
Format: Journal Article
Language:English
Published: 31.03.2022
ISSN:0028-0836, 1476-4687
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Abstract The microbiota modulates gut immune homeostasis. Bacteria influence the development and function of host immune cells, including T helper cells expressing interleukin-17A (TH17 cells). We previously reported that the bile acid (BA) metabolite 3-oxolithocholic acid (3-oxoLCA) inhibits TH17 cell differentiation1. While it was suggested that gut-residing bacteria produce 3-oxoLCA, the identity of such bacteria was unknown, and it was unclear whether 3-oxoLCA and other immunomodulatory BAs are associated with inflammatory pathologies in humans. Here, we identify human gut bacteria and corresponding enzymes that convert the secondary BA lithocholic acid into 3-oxoLCA as well as the abundant gut metabolite isolithocholic acid (isoLCA). Like 3-oxoLCA, isoLCA suppressed TH17 differentiation by inhibiting RORγt (retinoic acid receptor-related orphan nuclear receptor γt), a key TH17 cell-promoting transcription factor. Levels of both 3-oxoLCA and isoLCA and the 3α-hydroxysteroid dehydrogenase (3α-HSDH) genes required for their biosynthesis were significantly reduced in inflammatory bowel disease (IBD) patients. Moreover, levels of these BAs were inversely correlated with expression of TH17 cell-associated genes. Overall, our data suggest that bacterially produced BAs inhibit TH17 cell function, an activity that may be relevant to the pathophysiology of inflammatory disorders such as IBD.
AbstractList The microbiota modulates gut immune homeostasis. Bacteria influence the development and function of host immune cells, including T helper cells expressing interleukin-17A (TH17 cells). We previously reported that the bile acid (BA) metabolite 3-oxolithocholic acid (3-oxoLCA) inhibits TH17 cell differentiation1. While it was suggested that gut-residing bacteria produce 3-oxoLCA, the identity of such bacteria was unknown, and it was unclear whether 3-oxoLCA and other immunomodulatory BAs are associated with inflammatory pathologies in humans. Here, we identify human gut bacteria and corresponding enzymes that convert the secondary BA lithocholic acid into 3-oxoLCA as well as the abundant gut metabolite isolithocholic acid (isoLCA). Like 3-oxoLCA, isoLCA suppressed TH17 differentiation by inhibiting RORγt (retinoic acid receptor-related orphan nuclear receptor γt), a key TH17 cell-promoting transcription factor. Levels of both 3-oxoLCA and isoLCA and the 3α-hydroxysteroid dehydrogenase (3α-HSDH) genes required for their biosynthesis were significantly reduced in inflammatory bowel disease (IBD) patients. Moreover, levels of these BAs were inversely correlated with expression of TH17 cell-associated genes. Overall, our data suggest that bacterially produced BAs inhibit TH17 cell function, an activity that may be relevant to the pathophysiology of inflammatory disorders such as IBD.
Author Zhang, Yancong
Avila-Pacheco, Julian
Clish, Clary B.
Franzosa, Eric A.
Yao, Lina
Zhang, Minghao
Devlin, A. Sloan
D’Agostino, Gabriel D.
Turnbaugh, Peter J.
Kim, Eunha
Krout, Michael R.
Rastinejad, Fraydoon
Paik, Donggi
Bae, Sena
Xavier, Ramnik J.
Huttenhower, Curtis
Bisanz, Jordan E.
Huh, Jun R.
Rakowski, Christopher K.
Vlamakis, Hera
Longman, Randy S.
AuthorAffiliation 3 Broad Institute of MIT and Harvard, Cambridge, MA, USA
4 Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA
1 Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA
8 Department of Chemistry, Bucknell University, Lewisburg, PA, USA
12 Chan Zuckerberg Biohub, San Francisco, CA, USA
6 Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK
13 Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA
2 Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA
10 Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA
9 Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA
11 Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA
14 Evergrande Center for Immunologic Disease
AuthorAffiliation_xml – name: 10 Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA
– name: 12 Chan Zuckerberg Biohub, San Francisco, CA, USA
– name: 13 Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA
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– name: 14 Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– name: 1 Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA
– name: 6 Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK
– name: 8 Department of Chemistry, Bucknell University, Lewisburg, PA, USA
– name: 3 Broad Institute of MIT and Harvard, Cambridge, MA, USA
– name: 4 Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA
– name: 2 Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA
– name: 11 Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA
– name: 5 Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA
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  givenname: Donggi
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  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
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  givenname: Lina
  surname: Yao
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  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
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  givenname: Yancong
  surname: Zhang
  fullname: Zhang, Yancong
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
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  givenname: Sena
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  fullname: Bae, Sena
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 5
  givenname: Gabriel D.
  surname: D’Agostino
  fullname: D’Agostino, Gabriel D.
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
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  givenname: Minghao
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  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
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  givenname: Eric A.
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  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
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  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 11
  givenname: Christopher K.
  surname: Rakowski
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  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
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  givenname: Hera
  surname: Vlamakis
  fullname: Vlamakis, Hera
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
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  givenname: Ramnik J.
  surname: Xavier
  fullname: Xavier, Ramnik J.
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 14
  givenname: Peter J.
  surname: Turnbaugh
  fullname: Turnbaugh, Peter J.
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 15
  givenname: Randy S.
  surname: Longman
  fullname: Longman, Randy S.
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 16
  givenname: Michael R.
  surname: Krout
  fullname: Krout, Michael R.
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 17
  givenname: Clary B.
  surname: Clish
  fullname: Clish, Clary B.
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 18
  givenname: Fraydoon
  surname: Rastinejad
  fullname: Rastinejad, Fraydoon
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 19
  givenname: Curtis
  surname: Huttenhower
  fullname: Huttenhower, Curtis
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 20
  givenname: Jun R.
  surname: Huh
  fullname: Huh, Jun R.
  email: jun_huh@hms.harvard.edu, sloan_devlin@hms.harvard.edu
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
– sequence: 21
  givenname: A. Sloan
  surname: Devlin
  fullname: Devlin, A. Sloan
  email: jun_huh@hms.harvard.edu, sloan_devlin@hms.harvard.edu
  organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Department of Biological Chemistry and Molecular Pharmacology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Department of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, MA, USA. Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA, USA Department of Chemistry, Bucknell University, Lewisburg, PA, USA Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Molecular Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Center for Microbiome Informatics and Therapeutics, MIT, Cambridge, MA, USA Chan Zuckerberg Biohub, San Francisco, CA, USA. Jill Roberts Center for IBD, Weill Cornell Medicine, New York, NY, USA Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA
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Notes J.R.H. and A.S.D. conceptualized the study. D.P., L.Y., J.R.H., and A.S.D. conceived the project and designed the experiments. D.P. performed mouse experiments, in vitro T cell and reporter assays. L.Y. performed human isolate screen, bacterial in vitro culture experiments, and BA profiling. G.D.D. performed HSDH enzyme characterization. Y.Z. and S.B. performed the bioinformatics analyses. E.A.F. and C.H. supervised the computational analyses. J.A.P. and C.C. performed LCA derivative identification in PRISM and HMP2 metabolomics. E.K. performed T cell RNA-Seq analysis. M.Z. and F.R. performed in vitro protein binding assays. J.E.B. performed comparative genomics on E. lenta. C.K.R. and M.R.K. synthesized some of the BA derivatives. J.E.B. and P.J.T., supervised the E. lenta human isolate studies. H.V. and R.J.X. provided bacterial strains and technical support. R.L. provided the patient stool samples. D.P., L.Y., Y.Z., S.B., G.D.D., E.A.F., J.R.H., and A.S.D. wrote the manuscript, with contributions from all authors.
These authors contributed equally: Donggi Paik, Lina Yao
Author contributions
PMID 35296854
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Snippet The microbiota modulates gut immune homeostasis. Bacteria influence the development and function of host immune cells, including T helper cells expressing...
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