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NLRP12 attenuates colon inflammation by maintaining colonic microbial diversity and promoting protective commensal bacterial growth
Open accessAbstract
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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“Interestingly, two previous studies have indicated that changes in the relative abundance of gut microbiota are more likely to be influenced by inflammation rather than age, with TNF playing a significant role.185,186”
From Inflammation and aging: signaling pathways and intervention therapies (2023) · cites this paper as [185]
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BackgroundSasaki, K., Inoue, J., Sasaki, D., Hoshi, N., Shirai, T., Fukuda, I., Azuma, T., Kondo, A., & Osawa, R. (2019) · Biotechnology Journal · doi:10.1002/biot.201800555 · Cited by 67
Estrogen protection against EAE modulates the microbiota and mucosal-associated regulatory cells
Benedek, G., Zhang, J., Nguyen, H., Kent, G., Seifert, H. A., Davin, S., Stauffer, P., Vandenbark, A. A., Karstens, L., Asquith, M., et al. (2017) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2017.06.007 · Cited by 64
“The authors demonstrated that Nlrp12 deficient mice are susceptible to dysbiosis and colitis and exhibit similar changes to those observed in EAE induction, with a loss of Lachnospiraceae family members and increases in the abundance of the Erysipelotrichaceae spp (Chen et al. , 2017).”
BackgroundGut microbial alterations in arginine metabolism determine bone mechanical adaptation
Wang, D., Cai, J., Pei, Q., Yan, Z., Zhu, F., Zhao, Z., Liu, R., Guo, X., Sun, T., Liu, J., et al. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.04.004 · Cited by 64
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Dietary copper-fructose interactions alter gut microbial activity in male rats
Song, M., Li, X., Zhang, X., Shi, H., Vos, M. B., Wei, X., Wang, Y., Gao, H., Rouchka, E. C., Yin, X., et al. (2017) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00378.2016 · Cited by 64
Interactions between dietary polyphenols and aging gut microbiota: A review
Davinelli, S., & Scapagnini, G. (2021) · BioFactors · doi:10.1002/biof.1785 · Cited by 62
“The abundance of colitogenic strains (Erysipelotrichaceae) was also associated with a decline in SCFAs.53,55,56 Among the many functions, SCFAs produced by gut microbes provide signals that promote immunity and suppress inflammatory responses.”
BackgroundNOD-like Receptor Signaling Pathway in Gastrointestinal Inflammatory Diseases and Cancers
Zhou, Y., Yu, S., & Zhang, W. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914511 · Cited by 64
“NLRP12 gene expression was shown to have a negative correlation with active ulcerative colitis [87].”
Canonical and noncanonical inflammasomes in intestinal epithelial cells
Winsor, N. J., Krustev, C., Bruce, J. K., Philpott, D. J., & Girardin, S. E. (2019) · Cellular Microbiology · doi:10.1111/cmi.13079 · Cited by 64
“However, the effect of NLRP12 in shaping the microbiome appears to be dependent on myeloid rather than epithelial cells, as bone marrow chimeras of myeloid‐specific Nlpr12−/− mice into Nlrp12+/+ animals recapitulate the reduced diversity seen in global Nlrp12−/− animals (L. Chen et al., 2017).”
BackgroundMethodInfluentialHollister, E. B., Cain, K. C., Shulman, R. J., Jarrett, M. E., Burr, R. L., Ko, C. W., Zia, J. K., Han, C. J., & Heitkemper, M. M. (2018) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000001107 · Cited by 61
The microbiome and cytosolic innate immune receptors
Liwinski, T., Zheng, D., & Elinav, E. (2020) · Immunological Reviews · doi:10.1111/imr.12901 · Cited by 61
PANoptosis in cancer: bridging molecular mechanisms to therapeutic innovations
Lin, J., Wang, T., Huang, R., Tan, Y., Chen, D., & Ju, H. (2025) · Cellular and Molecular Immunology · doi:10.1038/s41423-025-01329-z · Cited by 63
NLR and Intestinal Dysbiosis-Associated Inflammatory Illness: Drivers or Dampers?
Elias‐Oliveira, J., Leite, J. A., Pereira, Í. S., Guimarães, J. B., Manso, G. M. D. C., Silva, J. S., Tostes, R. C., & Carlos, D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01810 · Cited by 59
“NOD2 deficiency breaks this homeostatic interaction, resulting in gut dysbiosis, and increased IBD susceptibility (69).”
BackgroundInfluentialChen, G., Huang, B., Fu, S., Li, B., Ran, X., He, D., Jiang, L., Li, Y., Liu, B., Xie, L., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02079 · Cited by 58
“Similar research has revealed that mice deficient in the intestinal inflammatory regulator NLRP12 possess a dysbiotic microbiome and exacerbated colitis (43).”
BackgroundMultigene sequencing reveals heterogeneity of NLRP12-related autoinflammatory disorders
Kostik, M. M., Suspitsin, E. N., Николаевна, Г. М., Levina, A. S., Kazantseva, A. Y., Соколенко, А. П., & Имянитов, Е. Н. (2018) · Rheumatology International · doi:10.1007/s00296-018-4002-8 · Cited by 55
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Of genes and microbes: solving the intricacies in host genomes
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Eisfeld, A. J., Gasper, D. J., Suresh, M., & Kawaoka, Y. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.03307 · Cited by 54
Udden, S. M. N., Kwak, Y.-T., Godfrey, V., Khan, M. A. W., Khan, S., Loof, N., Peng, L., Zhu, H., & Zaki, H. (2019) · eLife · doi:10.7554/elife.40396 · Cited by 49
“Previous studies showed that deficiency of NLRP12 leads to enhanced incidence and faster progression of colorectal tumorigenesis (Allen et al., 2012; Chen et al., 2017; Zaki et al., 2011).”
Li, M., Wang, B., Sun, X., Tang, Y., Wei, X., Ge, B.-Y., Tang, Y., Deng, Y., He, C., Yuan, J., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00824 · Cited by 52
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“…inflammation, and provides energy to the intestinal epithelium, maintains an acidic environment in the intestine and inhibits the growth of harmful acid intolerant flora, while acid- tolerant Lactobacillus, Clostridium and other beneficial bacteria are able to proliferate (Chen et al., 2017).”
BackgroundMicrobial sensing in the intestine
Wan, T., Wang, Y., He, K., & Zhu, S. (2023) · Protein & Cell · doi:10.1093/procel/pwad028 · Cited by 50
Inflammatory cell death in intestinal pathologies
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Metadata
- 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
- Venue
- Nature Immunology
- Published
- 2017-03-13
- Volume
- 18
- Issue
- 5
- Pages
- 541-551
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- 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
- Open access
- green
- www.ncbi.nlm.nih.gov
- 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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