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Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes
Open accessAbstract
Interleukin 1β (IL-1β) is an important inflammatory mediator of type 2 diabetes. Here we show that oligomers of islet amyloid polypeptide (IAPP), a protein that forms amyloid deposits in the pancreas during type 2 diabetes, triggered the NLRP3 inflammasome and generated mature IL-1β. One therapy for type 2 diabetes, glyburide, suppressed IAPP-mediated IL-1β production in vitro. Processing of IL-1β initiated by IAPP first required priming, a process that involved glucose metabolism and was facilitated by minimally oxidized low-density lipoprotein. Finally, mice transgenic for human IAPP had more IL-1β in pancreatic islets, which localized together with amyloid and macrophages. Our findings identify previously unknown mechanisms in the pathogenesis of type 2 diabetes and treatment of pathology caused by IAPP.
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“that induce interleukin (IL)-1β release to recruit macrophages and enhance local islet inflammation ( 45 ).”
From β-Cell Failure in Type 2 Diabetes: Postulated Mechanisms and Prospects for Prevention and Treatment (2014) · cites this paper as [45]
Experimental — accuracy not yet measuredIn the citing paper
“A potential role for NLRP3 in promoting elevated levels of IL-1β in type 2 diabetes was also implied by the observation of NLRP3-dependent IL-1β secretion by mouse bone marrow-derived macrophages and dendritic cells in response to islet amyloid polypeptide (IAPP), which is deposited in the pancreas and associated with loss of β-cell function in type 2 diabetes61.”
From Sterile inflammation: sensing and reacting to damage (2010) · cites this paper as [61]
In the citing paper
“Interestingly, the anti-diabetic drug glyburide (Glibenclamide; Roche/Sanofi-Aventis) has been shown to block glucose-mediated secretion of IL-1β by mouse pancreatic islets62, as well as IL-1β production by macrophages in response to IAPP61, and NLRP3-deficient mice were more glucose tolerant than wild-type mice62.”
From Sterile inflammation: sensing and reacting to damage (2010) · cites this paper as [61]
In the citing paper
“In a separate study, no differences in IL-1β secretion were observed between wild-type and TXNIP-deficient bone marrow-derived macrophages in response to several NLRP3 stimuli, including MSU crystals and ATP61.”
From Sterile inflammation: sensing and reacting to damage (2010) · cites this paper as [61]
In the citing paper
“However, the role of TXNIP and ROS in NLRP3 activation has been challenged.”
From Sterile inflammation: sensing and reacting to damage (2010) · cites this paper as [61]
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“Consistent with previous studies, the mRNA expression levels of NLRP3 inflammasome components including NLRP3, pro-IL-1β, and pro-caspase-1 were upregulated [35, 40].”
ResultRole of pattern recognition receptors and microbiota-derived ligands in obesity
Rolland, A., Douard, V., & Lapaque, N. (2024) · Frontiers in Microbiomes · doi:10.3389/frmbi.2024.1324476 · Cited by 18
Sensing sterile injury: Opportunities for pharmacological control
Menezes, G. B., Mansur, D. S., McDonald, B., Kubes, P., & Teixeira, M. M. (2011) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2011.07.002 · Cited by 17
Mwangi, J., & Gitonga, L. K. (2014) · Open Journal of Clinical Diagnostics · doi:10.4236/ojcd.2014.43024 · Cited by 16
“The majority of type 1 diabetes is of the immunemediated nature, where beta cell loss is a cell mediated autoimmune attack [14].”
BackgroundIL-1β Activation as a Response to Metabolic Disturbances
Donath, M. Y., & Böni‐Schnetzler, M. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.10.002 · Cited by 16
“…via the NALP3 inflammasome, for example in amyloid deposits and hyperglycaemia in pancreatic islets, in uric acid crystals in the joint and cholesterol in blood vessels (Dinarello, 2009; Duewell et al., 2010; Maedler et al., 2002; Martinon et al., 2006; Masters et al., 2010; Zhou et al., 2010).”
BackgroundInfluentialResponding to Threats Both Foreign and Domestic: NOD-Like Receptors in Corals
Dimos, B., Butler, C. C., Ricci, C. A., MacKnight, N. J., & Mydlarz, L. D. (2019) · Integrative and Comparative Biology · doi:10.1093/icb/icz111 · Cited by 14
“…a diverse array of signals (Horvath et al. 2011), including lipopolysaccharide (LPS) (Mariathasan et al. 2006), ROS (Martinon et al. 2009), and organelle calcium efflux (Lee et al. 2012) in addition to other signatures of cellular stress (Dostert et al. 2008; Masters et al. 2010; Zhou et al. 2010).”
BackgroundAmyloids in Site-Specific Autoimmune Reactions and Inflammatory Responses
Huang, Y., Hong, X., Shen, J. X., Geng, L.-J., Pan, Y.-H., Ling, W., & Zhao, H. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02980 · Cited by 16
Despa, F., & Goldstein, L. B. (2021) · Stroke · doi:10.1161/strokeaha.121.034363 · Cited by 16
Bile acid receptors link nutrient sensing to metabolic regulation
Li, J., & Li, T. (2017) · Liver Research · doi:10.1016/j.livres.2017.04.001 · Cited by 16
Kaminiotis, V. V., Agrogiannis, G. D., Konstantopoulos, P. S., Androutsopoulou, V. A., Korou, L. M., Vlachos, I. S., Dontas, I. A., Perrea, D. N., & Iliopoulos, D. (2017) · Lipids in Health and Disease · doi:10.1186/s12944-017-0573-8 · Cited by 16
Short Exposure to Ethanol Diminishes Caspase-1 and ASC Activation in Human HepG2 Cells In Vitro
Hörauf, J.-A., Kany, S., Janicova, A., Xu, B., Vrdoljak, T., Sturm, R., Dunay, I. R., Märtin, L., & Relja, B. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093196 · Cited by 16
“Recent data have indicated that NLRP3 was also involved in the development of globally widespread diseases like diabetes type 2 and Alzheimer’s disease [4,5].”
BackgroundInflammasomes as the molecular hub of cardiovascular-metabolic-immune comorbidity networks
Qian, X., Sun, J. M., Li, F., Li, X., Hu, X., Dong, N., & Li, G. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1690443 · Cited by 18
Genome Damage Sensing Leads to Tissue Homeostasis in Drosophila
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Li, J., Zhang, F., Bian, W., Chen, Y., Liu, J., Liu, Z., Xiong, Y., & Wan, X. H. (2022) · Cell & Bioscience · doi:10.1186/s13578-022-00854-y · Cited by 15
Digital Behavioral Activation Interventions During the Perinatal Period: Scoping Review
Mancinelli, E., Dell’Arciprete, G., Pattarozzi, D., Gabrielli, S., & Salcuni, S. (2023) · JMIR Pediatrics and Parenting · doi:10.2196/40937 · Cited by 20
C4b-binding protein inhibits particulate- and crystalline-induced NLRP3 inflammasome activation
Bierschenk, D., Papac-Miličević, N., Bresch, I. P., Kovacic, V., Bettoni, S., Dziedzic, M., Wetsel, R. A., Eschenburg, S., Binder, C. J., Blom, A. M., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1149822 · Cited by 15
“IAPP oligomers trigger inflammasome activation in pancreatic islets, which contributes to type 2 diabetes pathogenesis (15).”
BackgroundPiotrowska, K., Zgutka, K., Tkacz, M., & Tarnowski, M. (2023) · Antioxidants · doi:10.3390/antiox12081488 · Cited by 18
Mukherjee, N., Contreras, C., Li, L., Colglazier, K. A., Mather, E. G., Kalwat, M. A., Esser, N., Kahn, S. E., & Templin, A. T. (2024) · Molecular Metabolism · doi:10.1016/j.molmet.2024.101877 · Cited by 15
Self-citationLiposome Encapsulation Enhances the Antidiabetic Efficacy of Silibinin
Dinić, S., Јovanović, J. A., Uskoković, A. S., Jovanović, A., Grdović, N., Rajić, J., Đorđević, M., Sarić, A., Bugarski, B., Vidaković, M., et al. (2024) · Pharmaceutics · doi:10.3390/pharmaceutics16060801 · Cited by 15
“Fibrosis, which is known to be a hallmark of chronic inflammation, has also been found in islet sections from T2D patients [5].”
BackgroundZhao, L., Li, J., Xu, X., Zhang, N., He, T., Yuan, Y., Zhang, Y., & Li, H. (2024) · Cell Reports Physical Science · doi:10.1016/j.xcrp.2024.102147 · Cited by 15
Li, Y., Qi, S., Wu, C., Jin, R., Hu, C., Wang, A., Wang, B., Yu, H., Wang, L., Liu, J. L., et al. (2024) · Acta Pharmacologica Sinica · doi:10.1038/s41401-024-01434-1 · Cited by 15
Inflammation, Immunity and Redox Signaling
Jabaut, J., & Ckless, K. (2012) · InTech eBooks · doi:10.5772/27242 · Cited by 15
“…contributing factor in rheumatoid arthritis, gout, multiple sclerosis (in the animal model experimental autoimmune encephalomyelitis), Alzheimer’s Disease, and diabetes (Gris et al.2010 ; Masters et al. 2010 ; Zhou et al. 2010 ; Griffin et al. 2006; Daheshia and Yao 2008; Clutterbuck et al. 2009).”
BackgroundCharacterization and Activation of NLRP3 Inflammasomes in the Renal Medulla in Mice
Xia, M., Abais, J. M., Koka, S., Meng, N., Gehr, T. W. B., Boini, K. M., & Li, P. (2016) · Kidney & Blood Pressure Research · doi:10.1159/000443424 · Cited by 15
Schneider, K. S., Thomas, C. J., & Groß, O. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-523-1_10 · Cited by 15
Inflammasome Activity in Non-Microbial Lung Inflammation
Ather, J. L. (2013) · Journal of Enviromental Immunology and Toxicology · doi:10.7178/jeit.20 · Cited by 15
Pattern Recognition Receptors in Immune Disorders Affecting the Skin
de Koning, H. D., Simon, A., Zeeuwen, P. L. J. M., & Schalkwijk, J. (2012) · Journal of Innate Immunity · doi:10.1159/000335900 · Cited by 16
Potential use of inflammation and early immunological event biomarkers in assessing vaccine safety
Mastelic, B., Lewis, D. J., Golding, H., Gust, I. D., Sheets, R., & Lambert, P. (2012) · Biologicals · doi:10.1016/j.biologicals.2012.10.005 · Cited by 15
“Eicke Latz (Institute of Innate Immunity, University of Bonn, Germany and Division of Infectious Diseases, UMass Med School, USA) described how crystals such as alum, uric acid [8] and amyloid [9], lipids and aggregates could activate the inflammasome via lysosomal swelling and rupture.”
BackgroundLiu, M., Hoskins, A., Verma, N., Bers, D. M., Despa, S. I., & Despa, F. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.10.024 · Cited by 15
Xie, S., Liu, M., Kong, Y., Yang, Y., Chen, R., Wang, Y., Cao, S., & Song, Y. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1549096 · Cited by 15
Bosch, A. J. T., Rohm, T. V., AlAsfoor, S., Low, A. J. Y., Baumann, Z., Parayil, N., Noreen, F., Roux, J., Meier, D. T., & Cavelti‐Weder, C. (2023) · Particle and Fibre Toxicology · doi:10.1186/s12989-023-00536-8 · Cited by 15
Role of the Pancreatic Islet Microvasculature in Health and Disease
Aplin, A. C., Aghazadeh, Y., Mohn, O. G., & Hull, R. L. (2024) · Journal of Histochemistry & Cytochemistry · doi:10.1369/00221554241299862 · Cited by 21
Self-citationLuo, X., Pan, L., Nie, A., Wang, Q., Gu, Y., Li, F., Zhang, H., Li, W., & Li, X. (2013) · Journal of Diabetes · doi:10.1111/1753-0407.12061 · Cited by 14
Metadata
- Authors
- Masters, S. L., Dunne, A., Subramanian, S. L., Hull, R. L., Tannahill, G. M., Sharp, F. A., Becker, C., Franchi, L., Yoshihara, E., Chen, Z., Mullooly, N., Mielke, L. A., Harris, J., Coll, R. C., Mills, K. H. G., Mok, K. H., Newsholme, P., Nuñez, G., Yodoi, J., Kahn, S. E., Lavelle, E. C., & O'Neill, L. A. J.
- Affiliations
- Trinity College Dublin (IE)
- University of Washington (US)
- University of Michigan (US)
- Kyoto University (JP)
- University College Dublin (IE)
- Corresponding author
- Masters, Seth L
- ORCID
- Venue
- Nature Immunology
- Published
- 2010-09-12
- Volume
- 11
- Issue
- 10
- Pages
- 897-904
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- PMC
- PMC3103663
- OpenAlex
- W2034946303
- Cited by
- 1,330
- References
- 55
- Citations by year
- 2026: 58 · 2025: 57 · 2024: 64 · 2023: 75 · 2022: 71 · 2021: 99 · 2020: 100 · 2019: 95 · 2018: 82 · 2017: 83 · 2016: 73 · 2015: 101 · 2014: 95 · 2013: 112 · 2012: 83
- FWCI
- 35.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion, other-oa)
- eSpace (Curtin University) (submittedVersion)
- Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (AI063331, R56AI063331, R01AI063331, R37AI063331)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-75998, R01DK075998)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
- Keywords
- NLRP3 inflammasome, amylin, IL-1β, type 2 diabetes, beta cell destruction, glibenclamide, LDL oxidation, glucose metabolism, inflammasome priming, pancreatic islets, macrophages, amyloid deposition
- MeSH terms
- NLR Family, Pyrin Domain-Containing 3 Protein, Amyloid, Animals, Carrier Proteins, Cells, Cultured, Dendritic Cells, Diabetes Mellitus, Type 2, Glyburide, Humans, Hypoglycemic Agents, Islets of Langerhans, Macrophages, Mice, Inbred C57BL, Mice, Transgenic, Receptors, Cytoplasmic and Nuclear, Mice, Rats, Interleukin-1beta, Islet Amyloid Polypeptide
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