Cited by 310Gut microbiota and healthInflammatory Bowel DiseaseInflammasome and immune disorders

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NLRP12 attenuates colon inflammation by maintaining colonic microbial diversity and promoting protective commensal bacterial growth

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Chen, Liang, Wilson, Justin E, Koenigsknecht, Mark J, Chou, Wei-Chun, Montgomery, Stephanie A, Truax, Agnieszka D, Brickey, W June, Packey, Christopher D, Maharshak, Nitsan, Matsushima, Glenn K, Plevy, Scott E, Young, Vincent B, Sartor, R Balfour, Ting, Jenny P-Y·2017·Nature Immunology

DOI 10.1038/ni.3690PMC PMC5395345

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Abstract

Inflammatory bowel diseases involve the dynamic interaction of host genetics, the microbiome and inflammatory responses. Here we found lower expression of NLRP12 (which encodes a negative regulator of innate immunity) in human ulcerative colitis, by comparing monozygotic twins and other patient cohorts. In parallel, Nlrp12 deficiency in mice caused increased basal colonic inflammation, which led to a less-diverse microbiome and loss of protective gut commensal strains (of the family Lachnospiraceae) and a greater abundance of colitogenic strains (of the family Erysipelotrichaceae). Dysbiosis and susceptibility to colitis associated with Nlrp12 deficency were reversed equally by treatment with antibodies targeting inflammatory cytokines and by the administration of beneficial commensal Lachnospiraceae isolates. Fecal transplants from mice reared in specific-pathogen-free conditions into germ-free Nlrp12-deficient mice showed that NLRP12 and the microbiome each contributed to immunological signaling that culminated in colon inflammation. These findings reveal a feed-forward loop in which NLRP12 promotes specific commensals that can reverse gut inflammation, while cytokine blockade during NLRP12 deficiency can reverse dysbiosis.

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BackgroundInfluential
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Authors: Chen, L., Wilson, J. E., Koenigsknecht, M. J., Chou, W.-C., Montgomery, S. A., Truax, A. D., Brickey, W. J., Packey, C. D., Maharshak, N., Matsushima, G. K., Plevy, S. E., Young, V. B., Sartor, R. B., & Ting, J. P.-Y.
Affiliations: University of North Carolina at Chapel Hill (US)
University of Michigan (US)
Columbia University Irving Medical Center (US)
Tel Aviv University (IL)
Janssen (United States) (US)
Corresponding author: Ting, Jenny P-Y
ORCID: Wilson, Justin E
Koenigsknecht, Mark J
Montgomery, Stephanie A
Brickey, W June
Maharshak, Nitsan
Young, Vincent B
Sartor, R Balfour
Ting, Jenny P-Y
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2017-03-13
Volume: 18
Issue: 5
Pages: 541-551
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/ni.3690
PMC: PMC5395345
OpenAlex: W2596103622
Cited by: 310
References: 51
Citations by year: 2026: 18 · 2025: 32 · 2024: 35 · 2023: 34 · 2022: 32 · 2021: 30 · 2020: 39 · 2019: 42 · 2018: 31 · 2017: 16
FWCI: 14.30
Type: journal article
Language: en
Update notices: erratum (2017-08-01)
erratum (2017-10-18)
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
UNC Libraries
Funders: Crohn's and Colitis Foundation of America (P30 DK034987)
North Carolina State University (P30 DK034987)
Crohn's and Colitis Foundation
Multiple Sclerosis Society
National Institutes of Health (DK034987, DK094779, AI029564, AI067798, P40OD010995)
National Cancer Institute (R01CA156330, P30CA016086)
National Institute of Allergy and Infectious Diseases (U19AI090871, R37AI029564, AI-067798, U19AI067798)
National Institute of Diabetes and Digestive and Kidney Diseases (DK094779, F32DK098916, AI067798, P01DK094779, DK 034987, F32DK088417, P30DK034987)
Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill
Center for Gastrointestinal Biology and Disease, School of Medicine, University of North Carolina at Chapel Hill (P30 DK 034987)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Keywords: NLRP12, inflammatory bowel disease, ulcerative colitis, colonic inflammation, gut microbiota, microbial diversity, commensal bacteria, Lachnospiraceae, Erysipelotrichaceae, dysbiosis, innate immunity, cytokine inhibition, fecal microbiota transplantation, germ-free mice, monozygotic twins
MeSH terms: Clostridiales, Eubacteriales, Firmicutes, Bacillota, Animals, Colitis, Ulcerative, Colon, Feces, Humans, Immunity, Innate, Mice, Inbred C57BL, RNA, Ribosomal, 16S, Symbiosis, Twins, Monozygotic, Dextran Sulfate, Mice, Knockout, Biodiversity, Intracellular Signaling Peptides and Proteins, Mice, Gene-Environment Interaction, Microbiota

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NLRP12 attenuates colon inflammation by maintaining colonic microbial diversity and promoting protective commensal bacterial growth

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