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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Two previous studies 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.
“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]
The Results section ('TNF and IL-6 cause microbial dysbiosis in Nlrp12−/− mice'; page unavailable) reports that blocking TNF and IL-6 signaling reduced colitis and shifted the mice’s gut microbiota toward that of wild-type mice. This supports a role for inflammation and TNF in microbial composition, but the paper does not compare their influence with age or establish that inflammation is more influential than age. (LLM, conf=0.87)
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Westfall, S., Caracci, F., Estill, M. S., Frolinger, T., Shen, L., & Pasinetti, G. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.670500 · Cited by 142 · see citing works
“Erysipelotrichaceae family members have been identified as “colitogenic strains”, which are heavily coated in IgA antibodies, can transfer colitis-like symptoms through cohousing and associate with inflammasome-mediated intestinal dysbiosis (55, 56).”
BackgroundNeutrophil Recruitment: From Model Systems to Tissue-Specific Patterns
Margraf, A., Ley, K. F., & Zarbock, A. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.04.010 · Cited by 135 · see citing works
Epithelial Cell Inflammasomes in Intestinal Immunity and Inflammation
Lei, A., Murphy, A. G., & Maloy, K. J. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01168 · Cited by 131 · see citing works
Inflammasome biology, molecular pathology and therapeutic implications
Awad, F., Assrawi, E., Louvrier, C., Jumeau, C., Georgin‐Lavialle, S., Grateau, G., Amselem, S., Giurgea, I., & Karabina, S. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.02.011 · Cited by 134 · see citing works
“patientswith active ulcerative colitis, as compared to patientswith inactive ulcerative colitis or healthy controls (Chen et al., 2017).”
BackgroundNovel insights into microbiome in colitis and colorectal cancer
Yang, Y., & Jobin, C. (2017) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000399 · Cited by 129 · see citing works
Abraham, C., Abreu, M. T., & Turner, J. R. (2022) · Gastroenterology · doi:10.1053/j.gastro.2021.12.288 · Cited by 127 · see citing works
Impaired Autophagy in Intestinal Epithelial Cells Alters Gut Microbiota and Host Immune Responses
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“Although the numbers of some organisms (e.g., Akkermansia muciniphila and members of the Lachnospiraceae family) associated with the control of inflammation decreased, those of proinflammationory bacteria (e.g., “Candidatus Arthromitus”) and potential pathogens (the Pasteurellaceae family) increased in Atg5 / mice.”
ResultInfluentialMijan, M. A., & Lim, B. O. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i25.2673 · Cited by 125 · see citing works
Dysbiotic microbiota interactions in Crohn’s disease
Caparrós, E., Wiest, R., Scharl, M. M., Rogler, G., Gutiérrez, A., Yılmaz, B., Wawrzyniak, M., & Francés, R. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1949096 · Cited by 118 · see citing works
Apigenin inhibits colonic inflammation and tumorigenesis by suppressing STAT3-NF-κB signaling
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Self-citationThe Dynamic Changes of Gut Microbiota in Muc2 Deficient Mice
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“Chen et al. found that NLRP12 (which encodes a negative regulator of innate immunity) deficiency in mice led to increased colonic inflammation, causing a loss of protective gut commensal strains (of the family Lachnospiraceae) and a greater abundance of colitogenic strains (of the family Erysipelotrichaceae) [37].”
BackgroundInfluentialInflammasome as a Therapeutic Target for Cancer Prevention and Treatment
Thi, H. T. H., & Hong, S. (2017) · Journal of Cancer Prevention · doi:10.15430/jcp.2017.22.2.62 · Cited by 109 · see citing works
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Pandey, A., Li, Z., Gautam, M., Ghosh, A., & Man, S. M. (2024) · Immunological Reviews · doi:10.1111/imr.13406 · Cited by 113 · see citing works
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Interactions of commensal and pathogenic microorganisms with the mucus layer in the colon
Cai, R., Chen, C., Chen, J., Xu, X., Ding, C., & Gu, B. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1735606 · Cited by 100 · see citing works
“compared monozygotic twins and found that the expression of NLRP12 was downregulated in patients with ulcerative colitis.(70) NLRP12 could attenuate colitis by maintaining colonic microbial diversity and promoting protective commensal bacterial growth.”
BackgroundResultAhmad, A., Ansari, M. M., Mishra, R. K., Kumar, A., Vyawahare, A., Verma, R. K., Raza, S. S., & Khan, R. (2020) · Materials Science and Engineering C · doi:10.1016/j.msec.2020.111582 · Cited by 101 · see citing works
NLRP12 Regulates Anti-viral RIG-I Activation via Interaction with TRIM25
Chen, S.-T., Chen, L., Lin, D. S.-C., Chen, S.-Y., Tsao, Y. C., Guo, H., Li, F.-J., Tseng, W.-T., Tam, J. W., Chao, C.-W., et al. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2019.02.013 · Cited by 95 · see citing works
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Inflammasome activation and Th17 responses
Deng, J. P., Yu, X., & Wang, P. (2019) · Molecular Immunology · doi:10.1016/j.molimm.2018.12.024 · Cited by 94 · see citing works
NLR-Dependent Regulation of Inflammation in Multiple Sclerosis
Gharagozloo, M., Gris, K. V., Mahvelati, T. M., Amrani, A., Lukens, J. R., & Gris, D. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2017.02012 · Cited by 91 · see citing works
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“Interestingly, these bacteria belong to family Erysipelotrichaceae, which has been associated with severe colitis in Nlrp12−/− mice [67].”
BackgroundBusnelli, M., Manzini, S., & Chiesa, G. (2019) · Nutrients · doi:10.3390/nu12010079 · Cited by 91 · see citing works
Mucus, commensals, and the immune system
Zhao, Q. S., & Maynard, C. L. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2041342 · Cited by 88 · see citing works
“In support of this theory, transplantation of a randomly selected consortium of 23 Lachnospiraceae organisms enriched from the mouse feces, cecal contents, and cecal tissue was able to repair the dysbiosis observed in NLRP12 inflammasome-deficient mice and limit the severity of the colitis that ensued when the mice we…”
MethodYue, B., Luo, X., Yu, Z., Mani, S., Wang, Z., & Dou, W. (2019) · Microorganisms · doi:10.3390/microorganisms7100440 · Cited by 86 · see citing works
“NLRP12-/- mice also have the same characteristics, reflecting susceptibility to colitis and microbiome dysbiosis, which indicates the key role of NLRP12 in maintaining intestinal homeostasis [166].”
BackgroundSugden, S., Sanderson, D., Ford, K., Stein, L. Y., & Clair, C. C. S. (2020) · Scientific Reports · doi:10.1038/s41598-020-78891-1 · Cited by 87 · see citing works
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Dietary manipulation of the gut microbiome in inflammatory bowel disease patients: Pilot study
Olendzki, B. C., Bucci, V., Cawley, C., Maserati, R., McManus, M. M., Olednzki, E., Madziar, C., Chiang, D., Ward, D. V., Pellish, R. S., et al. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2046244 · Cited by 77 · see citing works
Vujkovic-Cvijin, I., Welles, H. C., Ha, C. W. Y., Huq, L., Mistry, S., Brenchley, J. M., Trinchieri, G., Devkota, S., & Belkaid, Y. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abl3927 · Cited by 76 · see citing works
“Given our observation of IgG targeting of Lachnospiraceae members, which have been associated with protection from colitis (73, 74), possible proinflammatory properties of some IgG-targeted bacteria may be outweighed by their beneficial effects.”
BackgroundMorse, J. C., Li, P., Ely, K., Shilts, M. H., Wannemuehler, T. J., Huang, L., Sheng, Q., Chowdhury, N. I., Chandra, R. K., Das, S. R., et al. (2018) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2018.10.056 · Cited by 78 · see citing works
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Porcine gut microbiota in mediating host metabolic adaptation to cold stress
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The Role of Lactoferrin in Intestinal Health
Conesa, C., Bellés, A., Grasa, L., & Sánchez, L. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15061569 · Cited by 70 · see citing works
Toxicity, gut microbiota and metabolome effects after copper exposure during early life in SD rats
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Gut microbiota, NLR proteins, and intestinal homeostasis
Guo, H., Gibson, S. A., & Ting, J. P. ‐. (2020) · The Journal of Experimental Medicine · doi:10.1084/jem.20181832 · Cited by 70 · see citing works
Self-citationInflammation, Autoinflammation and Autoimmunity in Inflammatory Bowel Diseases
Padoan, A., Musso, G., Contran, N., & Basso, D. (2023) · Current Issues in Molecular Biology · doi:10.3390/cimb45070350 · Cited by 71 · see citing works
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Dobranowski, P., Tang, C., Sauvé, J. P., Menzies, S. C., & Sly, L. M. (2019) · Gut Microbes · doi:10.1080/19490976.2018.1560767 · Cited by 68 · see citing works
“Other taxa have been shown to protect from intestinal inflammation through the production of anti-inflammatory metabolites.(6,7) Until recently, there has been a paucity of evidence to establish the temporality of microbiome changes in the context of intestinal inflammation.”
BackgroundJi, J., Ge, X., Chen, Y., Zhu, B., Wu, Q., Zhang, J., Shan, J., Cheng, H., & Shi, L. (2019) · The FASEB Journal · doi:10.1096/fj.201802659rr · Cited by 68 · see citing works
“After the digestion, the digested colonic lamina propria (LP) cells were filtered through a 100-mm strainer, centrifuged at 1500 rpm for 5 min at 4°C, and resuspended in 2 ml PBS for flow cytometric analysis (29).”
MethodCrits‐Christoph, A., Bhattacharya, N., Olm, M. R., Song, Y. S., & Banfield, J. F. (2020) · Genome Research · doi:10.1101/gr.268169.120 · Cited by 70 · see citing works
Melatonin in the colon modulates intestinal microbiota in response to stress and sleep deprivation
Park, Y. S., Kim, S. H., Park, J. W., Kho, Y., Seok, P. R., Shin, J.-H., Choi, Y. J., Jun, J.-H., Jung, H. C., & Kim, E. K. (2020) · Intestinal Research · doi:10.5217/ir.2019.00093 · Cited by 67 · see citing works
“Another group reported that the imbalance between Erysipelotrichace ae (family) and Lachnospiraceae is one cause of IBD and the deficiency of a gene controlling the innate immunity mechanism can cause this abnormality.(40) Together, these results suggest that melatonin is related to changes in bacterial population as…”
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 · see citing works
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 · see citing works
“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 · see citing works
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Dietary copper-fructose interactions alter gut microbial activity in male rats
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Interactions between dietary polyphenols and aging gut microbiota: A review
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“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 63 · see citing works
“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 60 · see citing works
“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 59 · see citing works
The microbiome and cytosolic innate immune receptors
Liwinski, T., Zheng, D., & Elinav, E. (2020) · Immunological Reviews · doi:10.1111/imr.12901 · Cited by 57 · see citing works
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 62 · see citing works
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 58 · see citing works
“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 56 · see citing works
“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 · see citing works
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Of genes and microbes: solving the intricacies in host genomes
Wang, J., Chen, L., Zhao, N., Xu, X., Xu, Y., & Zhu, B. (2018) · Protein & Cell · doi:10.1007/s13238-018-0532-9 · Cited by 51 · see citing works
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“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 50 · see citing works
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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
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Inflammatory cell death in intestinal pathologies
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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
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › 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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