β-hydroxybutyrate deactivates neutrophil NLRP3 inflammasome to relieve gout flares
Open accessAbstract
Aging and lipotoxicity are two major risk factors for gout that are linked by the activation of the NLRP3 inflammasome. Neutrophil-mediated production of interleukin-1β (IL-1β) drives gouty flares that cause joint destruction, intense pain, and fever. However, metabolites that impact neutrophil inflammasome remain unknown. Here, we identified that ketogenic diet (KD) increases β-hydroxybutyrate (BHB) and alleviates urate crystal-induced gout without impairing immune defense against bacterial infection. BHB inhibited NLRP3 inflammasome in S100A9 fibril-primed and urate crystal-activated macrophages, which serve to recruit inflammatory neutrophils in joints. Consistent with reduced gouty flares in rats fed a ketogenic diet, BHB blocked IL-1β in neutrophils in a NLRP3-dependent manner in mice and humans irrespective of age. Mechanistically, BHB inhibited the NLRP3 inflammasome in neutrophils by reducing priming and assembly steps. Collectively, our studies show that BHB, a known alternate metabolic fuel, is also an anti-inflammatory molecule that may serve as a treatment for gout.
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Ketone bodies inhibit the NLRP3 inflammasome and reduce IL-1beta production in monocytes.
“Additionally, increased levels of ketone bodies inhibit the Nod -like receptor pyrin domain-containing protein 3 (NLRP3) inflammasome and reduce production of interleukin-1 b in monocytes (Youm et al., 2015; Goldberg et al., 2017).”
From A kidney perspective on the mechanism of action of sodium glucose co-transporter 2 inhibitors (2021) · cites this paper as Goldberg et al., 2017
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Han, Y., Sun, W., Ren, D., Zhang, J., He, Z., Fedorova, J., Sun, X., Han, F., & Li, J. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101538 · Cited by 133 · see citing works
“The NLRP3 inflammasome has been shown to sense metabolites such as palmitate [24], uric acid [25], and cholesterol crystals [23], and is inhibited by ketone bodies [26] produced during metabolic flux.”
BackgroundPilot study of a ketogenic diet in relapsing-remitting MS
Brenton, J. N., Banwell, B., Bergqvist, A. G. C., Lehner‐Gulotta, D., Gampper, L., Leytham, E., Coleman, R., & Goldman, M. D. (2019) · Neurology Neuroimmunology & Neuroinflammation · doi:10.1212/nxi.0000000000000565 · Cited by 127 · see citing works
Inflammasomes and autoimmune and rheumatic diseases: A comprehensive review
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NLRP3 inflammasome signalling in Alzheimer's disease
McManus, R. M., & Latz, E. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.109941 · Cited by 125 · see citing works
“Due to this, NLRP3 inflammasome activation has been found across many different and seemingly unconnected diseases, from atherosclerosis (Duewell et al., 2010), gout (Goldberg et al., 2017), multiple sclerosis (Coll et al., 2015) and AD (Heneka et al., 2013).”
Ketogenic Diet: A New Light Shining on Old but Gold Biochemistry
Longo, R., Peri, C., Cricrì, D., Coppi, L., Caruso, D., Mitro, N., Fabiani, E. D., & Crestani, M. (2019) · Nutrients · doi:10.3390/nu11102497 · Cited by 117 · see citing works
“KD showed efficacy in gout mouse model of all ages and did not decrease immune host response to infections [84].”
BackgroundAutoinflammatory Features in Gouty Arthritis
Galozzi, P., Bindoli, S., Doria, A., Oliviero, F., & Sfriso, P. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10091880 · Cited by 116 · see citing works
“Beta-hydroxybutyrate (BHB) NA NLRP3, K+ channels [81]”
BackgroundMetabolic Messengers: ketone bodies
Nelson, A. B., Queathem, E. D., Puchalska, P., & Crawford, P. A. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00935-3 · Cited by 115 · see citing works
“While the exact mechanism is not known, βOHB inhibits NLRP3 assembly and interleukin (IL)-1β secretion in myeloid cells in a dose-dependent but chirality-independent manner, and this may ameliorate gout flares 36,134 .”
Stressing out the mitochondria: Mechanistic insights into NLRP3 inflammasome activation
Yabal, M., Calleja, D. J., Simpson, D. S., & Lawlor, K. E. (2018) · Journal of Leukocyte Biology · doi:10.1002/jlb.mr0318-124r · Cited by 109 · see citing works
Cardiovascular protection by SGLT2 inhibitors – Do anti-inflammatory mechanisms play a role?
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S100 family proteins in inflammation and beyond
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Neutrophil: A New Player in Metastatic Cancers
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“Neutrophils have a potential role as therapeutic targets (152).”
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The NLRP3 inflammasome - interleukin 1 pathway as a therapeutic target in gout
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Very‐low‐carbohydrate diet enhances human T‐cell immunity through immunometabolic reprogramming
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“In animal models, BHB has been shown to dampen inappropriate innate immune responses via suppression of the NLRP3 inflammasome, thus ameliorating chronic low-grade inflammation and associated diseases (Youm et al, 2015; Goldberg et al, 2017; Newman et al, 2017).”
BackgroundInfluentialEmerging Urate-Lowering Drugs and Pharmacologic Treatment Strategies for Gout: A Narrative Review
Terkeltaub, R. A. (2023) · Drugs · doi:10.1007/s40265-023-01944-y · Cited by 102 · see citing works
“However, SGLT2 inhibitor anti-inflammatory effects, partly via ketone generation [116, 117], have not been teased out from relatively moderate urate-lowering effects unlikely to get most gout patients to urate target as ULT monotherapy (e.g., mean ~ 08–1.0 mg/dL serum urate decrease in type II…”
BackgroundInfluentialNLRP3 Inflammasome Activation: A Therapeutic Target for Cerebral Ischemia–Reperfusion Injury
Wang, L., Ren, W., Wu, Q., Liu, T., Wei, Y. L., Ding, J., Zhou, C., Xu, H., & Yang, S. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.847440 · Cited by 100 · see citing works
The NLRP3 inflammasome: Role in metabolic disorders and regulation by metabolic pathways
Jiang, D., Chen, S., Sun, R., Zhang, X., & Wang, D. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.01.034 · Cited by 94 · see citing works
β-Hydroxybutyrate protects from alcohol-induced liver injury via a Hcar2-cAMP dependent pathway
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What makes gouty inflammation so variable?
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“Thus, acetate has paradoxical effects on the inflammatory response in experimental gout [26, 27] (Table 1).”
BackgroundChen, S., Zhou, Y., Wang, X., Sun, J., Cao, F., HaiSam, S., Ye, D., & Tian, Y. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104339 · Cited by 86 · see citing works
Role and therapeutic potential of dietary ketone bodies in lymph vessel growth
García‐Caballero, M., Zecchin, A., Souffreau, J., Truong, A.-C. K., Teuwen, L.-A. M. N., Vermaelen, W., Martín‐Pérez, R., de Zeeuw, P., Bouché, A., Vinckier, S., et al. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0087-y · Cited by 80 · see citing works
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“In human disease models, BHB suppressed the synthesis of TNF-α (Yamanashi et al., 2017) and IL-1β (Youm et al., 2015; Goldberg et al., 2017).”
BackgroundInfluentialLiu, Q., Su, L., Sun, C., Jiao, L., Miao, Y., Xu, M., Luo, R., Zuo, X., Zhou, R., Zheng, P., et al. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101560 · Cited by 78 · see citing works
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Involvement of inflammasomes in tumor microenvironment and tumor therapies
Zhang, Z., Li, X., Wang, Y., Wei, Y., & Wei, X. (2023) · Journal of Hematology & Oncology · doi:10.1186/s13045-023-01407-7 · Cited by 79 · see citing works
Investigating Ketone Bodies as Immunometabolic Countermeasures against Respiratory Viral Infections
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“Importantly, in multiple in vitro and animal studies that have utilized both dietary ketosis and exogenous ketone treatment, BHB inhibits NLRP3 activation in peripheral macrophages and neutrophils,38 in the retina,(109) and in the CNS(110) and reduced systemic inflammation in a rat model of gout, which is driven by NL…”
BackgroundSelf-citationThe NLRP3 inflammasome is involved with the pathogenesis of Mayaro virus
de Castro-Jorge, L. A., de Carvalho, R. A., Klein, T. M., Hiroki, C. H., Lopes, A. H., Guimarães, R. M., Fumagalli, M. J., Floriano, V. G., Agostinho, M. R., Slhessarenko, R. D., et al. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007934 · Cited by 76 · see citing works
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A metabolic perspective of the neutrophil life cycle: new avenues in immunometabolism
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Beta-Hydroxybutyrate: A Dual Function Molecular and Immunological Barrier Function Regulator
Qi, J., Gan, L., Fang, J. S., Zhang, J., Yu, X., Guo, H., Cai, D., Cui, H., Gou, L., Deng, J., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.805881 · Cited by 72 · see citing works
“In recent years, elevated blood ketones concentration by endogenous and exogenous interventions has been widely studied in experimental and clinical research, showing great application potential, including applications in relieving epilepsy (14), Parkinson’s disease (15, 16), gout flares (17), respiratory tract influe…”
BackgroundHow Can a Ketogenic Diet Improve Motor Function?
Veyrat‐Durebex, C., Reynier, P., Procaccio, V., Hergesheimer, R. C., Corcia, P., Andres, C. R., & Blasco, H. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00015 · Cited by 72 · see citing works
“…pro-inflammatory NF-κB and cytokines, such as IL-6 and TNFα (Cullingford, 2004; Nandivada et al., 2016). βOHB inhibits the NLRP3 inflammasome, which controls the activation of caspase-1 and the release of the pro-inflammatory cytokines, IL-1β and IL-18 (Youm et al., 2015; Goldberg et al., 2017).”
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Shang, S., Wang, L., Zhang, Y., Lü, H., & Lu, X. (2018) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-018-0617-2 · Cited by 71 · see citing works
Genetic and Epigenetic Regulation of the Innate Immune Response to Gout
de Lima, J. D., de Paula, A. G. P., Yuasa, B. S., Smanioto, C. C. S., Silva, M. C. D. C., dos Santos, P. I., Braun-Prado, K., Boldt, A. B. W., & Braga, T. T. (2023) · Immunological Investigations · doi:10.1080/08820139.2023.2168554 · Cited by 70 · see citing works
“The activation of NLRP3 requires two signals (Bauernfeind et al. 2009; Goldberg et al. 2017).”
BackgroundDietary natural products as epigenetic modifiers in aging-associated inflammation and disease
Evans, L. W., Stratton, M. S., & Ferguson, B. S. (2020) · Natural Product Reports · doi:10.1039/c9np00057g · Cited by 70 · see citing works
Ketogenic Diet: An Effective Treatment Approach for Neurodegenerative Diseases
Zhang, H., Tao, Y., & Leng, S. X. (2022) · Current Neuropharmacology · doi:10.2174/1570159x20666220830102628 · Cited by 71 · see citing works
Pyroptosis in defense against intracellular bacteria
Li, L., Dickinson, M. S., Coers, J., & Miao, E. A. (2023) · Seminars in Immunology · doi:10.1016/j.smim.2023.101805 · Cited by 68 · see citing works
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Metabolic regulation of inflammasomes in inflammation
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Wang, C., Iashchishyn, I. A., Pansieri, J., Nyström, S., Klementieva, O. L., Kara, J. A., Horváth, I., Moskalenko, R., Rofougaran, R., Gouras, G. K., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-31141-x · Cited by 64 · see citing works
Self-citationCould very low-calorie ketogenic diets turn off low grade inflammation in obesity? Emerging evidence
Barrea, L., Caprio, M., Watanabe, M., Cammarata, G., Feraco, A., Muscogiuri, G., Verde, L., Colao, A., & Savastano, S. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2054935 · Cited by 65 · see citing works
Microglial NLRP3 inflammasome-mediated neuroinflammation and therapeutic strategies in depression
Han, Q.-Q., Li, W., Chen, P., Wang, L., Bao, X., Huang, R., Liu, G., & Chen, X. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.390964 · Cited by 65 · see citing works
“Goldberg et al. (2017) discovered that a ketogenic diet could elevate BHB levels, which then deactivate the neutrophil NLRP3 inflammasome, providing relief from gout flares induced by uric acid crystals.”
BackgroundThe NLRP3 inflammasome: role in the pathobiology of chronic pain
Chen, C., & Smith, M. T. (2023) · Inflammopharmacology · doi:10.1007/s10787-023-01235-8 · Cited by 63 · see citing works
“Thus, β-hydroxybutyric acid, is an endogenous antiinflammatory molecule with potential as a treatment for gout (Goldberg et al. 2017).”
BackgroundInfluentialQadri, M. M., Jay, G. D., Zhang, L. X., Wong, W., Reginato, A. M., Sun, C., Schmidt, T. A., & Elsaid, K. A. (2018) · Arthritis Research & Therapy · doi:10.1186/s13075-018-1693-x · Cited by 64 · see citing works
“Future study will use a higher dose of MSU crystals, which has been recently optimized [67].”
Shirasuna, K., Karasawa, T., & Takahashi, M. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27475 · Cited by 62 · see citing works
“In addition, elevation of BHB via ketogenic diet blocks NLRP3 inflammasome activation and IL‐1β secretion both in murine macrophages and neutrophils, resulting in protection against acute gout induced by MSU injection (Goldberg et al., 2017).”
BackgroundNasser, S., Solé, T., Véga, N., Thomas, T., Balcerczyk, A., Strigini, M., & Pirola, L. (2022) · Molecular Metabolism · doi:10.1016/j.molmet.2022.101578 · Cited by 61 · see citing works
“The numerous beneficial effects on inflammation [4,5], metabolism [9], and hypertension [35] of the ketogenic diet may be linked to modulation of gene transcription following histone b-hydroxybutyrylation, an histone PTM promoted by BHB [8].”
BackgroundResultChen, L., Song, C., Zhang, Y., Li, Y., Zhao, Y., Lin, F., Han, D., Dai, M., Li, W., & Pan, P. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.175352 · Cited by 61 · see citing works
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Sodium‐glucose cotransporter 2 inhibitors regulate ketone body metabolism via inter‐organ crosstalk
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The fructose survival hypothesis for obesity
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Ketogenic diet restrains aging-induced exacerbation of coronavirus infection in mice
Ryu, S., Shchukina, I., Youm, Y., Qing, H., Hilliard, B. K., Dlugos, T., Zhang, X., Yasumoto, Y., Booth, C. J., Fernandez-Hernando, C. F., et al. (2021) · eLife · doi:10.7554/elife.66522 · Cited by 58 · see citing works
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“BHB suppresses TLR4 stimulus and the assembly of NIC individual proteins (27).”
BackgroundInvited review: Ketone biology—The shifting paradigm of ketones and ketosis in the dairy cow
Rico, J. E., & Barrientos-Blanco, M. A. (2024) · Journal of Dairy Science · doi:10.3168/jds.2023-23904 · Cited by 58 · see citing works
Immune and inflammatory mechanisms and therapeutic targets of gout: An update
Liu, W., Peng, J., Wu, Y., Ye, Z., Zong, Z., Wu, R., & Li, H. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.110466 · Cited by 57 · see citing works
- Authors
- Goldberg, E. L., Asher, J. L., Molony, R. D., Shaw, A. C., Zeiss, C. J., Wang, C., Morozova-Roche, L. A., Herzog, R. I., Iwasaki, A., & Dixit, V. D.
- Affiliations
- Yale University (US)
- Umeå University (SE)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Dixit, Vishwa Deep
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2017-02
- Volume
- 18
- Issue
- 9
- Pages
- 2077-2087
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC5527297
- OpenAlex
- W2594548735
- Cited by
- 370
- References
- 48
- Citations by year
- 2026: 27 · 2025: 27 · 2024: 50 · 2023: 68 · 2022: 51 · 2021: 43 · 2020: 40 · 2019: 31 · 2018: 19 · 2017: 14
- FWCI
- 11.56
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DiVA at Umeå University (Umeå University) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (AG043608, AI105097, AR070811, P01AG051459)
- Diabetes Research Center (UL1-RR- 024139)
- Howard Hughes Medical Institute
- Yale Center for Clinical Investigation, Yale School of Medicine
- National Institute of Diabetes and Digestive and Kidney Diseases (K08 DK082618, R01 DK101984-02)
- American Heart Association (AI007019-38, AI055403, K24 AG042489, P30 AG21342, U19 AI089992)
- American Foundation for Aging Research
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Health Sciences › Medicine › Nephrology › Gout, Hyperuricemia, Uric Acid
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- beta-hydroxybutyrate, NLRP3 inflammasome, gout flares, neutrophils, ketogenic diet, IL-1β, urate crystals, macrophages, lipotoxicity, aging, anti-inflammatory metabolites, joint inflammation
- MeSH terms
- NLR Family, Pyrin Domain-Containing 3 Protein, Adolescent, Adult, Aged, Animals, Female, Gout, Humans, Inflammation, Macrophages, Male, Mice, Inbred C57BL, Middle Aged, Neutrophils, Uric Acid, 3-Hydroxybutyric Acid, Mice, Rats, Interleukin-1beta, Diet, Ketogenic, Young Adult, Inflammasomes
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