Cited by 1,945IL-33, ST2, and ILC PathwaysImmune Response and InflammationInflammasome and immune disorders

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The Interleukin-1 Family: Back to the Future

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Garlanda, Cecilia, Dinarello, Charles A., Mantovani, Alberto·2013·Immunity

DOI 10.1016/j.immuni.2013.11.010PMC PMC3933951

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Abstract

Interleukin-1 (IL-1) is a central mediator of innate immunity and inflammation. The IL-1 family includes seven ligands with agonist activity (IL-1α and IL-1β, IL-18, IL-33, IL-36α, IL-36β, IL-36γ), three receptor antagonists (IL-1Ra, IL-36Ra, IL-38), and an anti-inflammatory cytokine (IL-37). Members of the IL-1 Receptor (IL-1R) family include six receptor chains forming four signaling receptor complexes, two decoy receptors (IL-1R2, IL-18BP), and two negative regulators (TIR8 or SIGIRR, IL-1RAcPb). A tight regulation via receptor antagonists, decoy receptors, and signaling inhibitors ensures a balance between amplification of innate immunity and uncontrolled inflammation. All cells of the innate immune system express and/or are affected by IL-1 family members. Moreover, IL-1 family members play a key role in the differentiation and function of polarized innate and adaptive lymphoid cells. Here we will review the key properties of IL-1 family members, with emphasis on pathways of negative regulation and orchestration of innate and adaptive immunity.

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Serum IL-1, Pyroptosis and Intracranial Aneurysm Wall Enhancement: Analysis Integrating Radiology, Serum Cytokines and Histology
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Pentachlorophenol mediated regulation of DAMPs and inflammation: In vitro study
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Soluble ST2 is increased in systemic lupus erythematous and is a potential marker of lupus nephritis
Moreau, A., Nicaise, C., Awada, A., & Soyfoo, M. S. (2021) · Clinical and Experimental Rheumatology · doi:10.55563/clinexprheumatol/eg3a2k · Cited by 18
“and to its coreceptor IL-1R accessory protein (IL-1RacP) ensuing activation of NFκB and MAPK 6 pathways and leading to cell-specific downstream effects (12, 14, 15, 17, 18).”
Background
Terminal Phenoxy Group as a Privileged Moiety of the Drug Scaffold—A Short Review of Most Recent Studies 2013–2022
Kozyra, P., & Pitucha, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23168874 · Cited by 21
The innate and T-cell mediated immune response during acute and chronic gammaherpesvirus infection
Rex, V., Zargari, R., Stempel, M., Halle, S., & Brinkmann, M. M. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1146381 · Cited by 19
“The antiviral innate immune response also initiates and shapes the adaptive immune response with its central players, the cytotoxic CD8+ T cells (CTL), CD4+ T helper cells, and B cells (Tomalka et al., 2022).”
BackgroundInfluential
Immune modulation through secretory autophagy
Weigert, A., & Herhaus, L. (2023) · Journal of Cellular Biochemistry · doi:10.1002/jcb.30427 · Cited by 18
“83,84 This question is furthermore relevant when looking at other inflammation ‐ related cargo being released via secretory autophagy.”
Interleukin‐1 family cytokines at the crossroads of microbiome regulation in barrier health and disease
Narros‐Fernández, P., Basavarajappa, S. C., & Walsh, P. T. (2023) · FEBS Journal · doi:10.1111/febs.16888 · Cited by 19
“The two isoforms of IL-1, IL-1 a and IL-1 b , bind to the same transmembrane receptor complex, formed by IL-1R1 and the IL-1R accessory protein (IL-1RAcp) and have similar biological properties, however, they also share some dissimilarities [74 – 76].”
Background
Goat milk extracellular vesicles: immuno-modulation effects on porcine monocyte-derived macrophages in vitro
Franzoni, G., Mecocci, S., Ciucis, C. G. D., Mura, L., Dell’Anno, F., Zinellu, S., Fruscione, F., Paolis, L. D., Carta, T., Anfossi, A. G., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1209898 · Cited by 18
“IL-1 a and IL-1 b are interleukins produced and released at the early stages of infections, characterized by similar biological properties (56).”
Influential
The impact of the P2X7 receptor on the tumor immune microenvironment and its effects on tumor progression
Zou, Y.-T., Li, J., Chai, J.-Y., Hu, Y., Zhang, W., & Zhang, Q. (2024) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.149513 · Cited by 20
IL-1 Contributes to the Anti-Cancer Efficacy of Ingenol Mebutate
Le, T. T., Skak, K., Schroder, K., Schroder, W. A., Boyle, G. M., Pierce, C. J., & Suhrbier, A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0153975 · Cited by 18
“The data so far supports the view that IL-1 promotes the anti-cancer efficacy of ingenol mebu-tate by promoting neutrophil anti-cancer activity, with MyD88 required for IL-1 receptor signal transduction [42].”
Commensal Bacteria-Induced Inflammasome Activation in Mouse and Human Macrophages Is Dependent on Potassium Efflux but Does Not Require Phagocytosis or Bacterial Viability
Chen, K., Shanmugam, N. K. N., Pazos, M. A., Hurley, B. P., & Cherayil, B. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0160937 · Cited by 19
“IL-1ß plays important roles in several aspects of innate and adaptive immune responses and can contribute to the pathology of chronic inflammatory diseases when its production is dysregulated [3,4].”
IL 1A (‐889) gene polymorphism is associated with the effect of diet as a risk factor in Acne Vulgaris
Ibrahim, A. A., Salem, R. M., El-Shimi, O. S., Baghdady, S. M., & Hussein, S. (2018) · Journal of Cosmetic Dermatology · doi:10.1111/jocd.12516 · Cited by 18
“IL-1A is a member of the IL-1 cytokine family which plays a major role in inflammation and fibrosis in multiple tissues.(4) In vitro and in vivo studies demonstrated that keratinocytes secrete IL-1A when stimulated by P.”
Background
Host Defenses to Viruses
Rouse, B. T., & Mueller, S. N. (2019) · Elsevier eBooks · doi:10.1016/b978-0-7020-6896-6.00025-9 · Cited by 18
Red nucleus interleukin‐1β evokes tactile allodynia through activation of JAK/STAT3 and JNK signaling pathways
Guo, Y., Li, H., Ding, C., Han, S., & Wang, J. (2018) · Journal of Neuroscience Research · doi:10.1002/jnr.24324 · Cited by 18
Cytotoxicity analysis of ambient fine particle in BEAS-2B cells on an air-liquid interface (ALI) microfluidics system
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Autoantibodies and Cytokines
Khan, W. A. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.68834 · Cited by 19
Scaffolds for corneal tissue engineering
Yousaf, S., Keshel, S. H., Farzi, G. A., Momeni-Moghadam, M., Ahmadi, E. D., Asencio, Í. O., Mozafari, M., & Sefat, F. (2019) · Elsevier eBooks · doi:10.1016/b978-0-08-102561-1.00026-9 · Cited by 18
MAP3K2 augments Th1 cell differentiation via IL-18 to promote T cell-mediated colitis
Wu, N., Chen, D., Sun, H., Tan, J., Zhang, Y., Zhang, T., Han, Y., Liu, H., Ouyang, X., Yang, X., et al. (2020) · Science China Life Sciences · doi:10.1007/s11427-020-1720-9 · Cited by 18
IL-1β primed mesenchymal stromal cells moderate hemorrhagic shock-induced organ injuries
Aussel, C., Baudry, N., Grosbot, M., Caron, C., Vicaut, É., Banzet, S., & Peltzer, J. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02505-4 · Cited by 18
Bone marrow fat and the decline of B lymphopoiesis in rabbits
Kennedy, D. E., Witte, P. L., & Knight, K. L. (2015) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2015.11.003 · Cited by 18
“IL-1β is expressed as a full length, inactive precursor, and inflammasome activation is required for cleavage of pro-IL1β into its active form by caspase-1 (Garlanda et al., 2013).”
Background
A link between osteomyelitis and IL1RN and IL1B polymorphisms—a study in patients from Northeast Brazil
de Souza, C. A., de Souza, A. Q. A., de Souza, M. D. S. Q. A., Leite, J. A. D., de Morais, M. S., & Rabenhorst, S. H. B. (2017) · Acta Orthopaedica · doi:10.1080/17453674.2017.1348439 · Cited by 18
Japanese GWAS identifies variants for bust-size, dysmenorrhea, and menstrual fever that are eQTLs for relevant protein-coding or long non-coding RNAs
Hirata, T., Koga, K., Johnson, T. A., Morino, R., Nakazono, K., Kamitsuji, S., Akita, M., Kawajiri, M., Kami, A., Hoshi, Y., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-25065-9 · Cited by 18
The ST2/Interleukin-33 Axis in Hematologic Malignancies: The IL-33 Paradox
Allegra, A., Innao, V., Tartarisco, G., Pioggia, G., Casciaro, M., Musolino, C., & Gangemi, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205226 · Cited by 18
“IL-33 is regarded as an “alarmin” able to stimulate several effectors of the immune system, regulating numerous immune responses comprising cancer immune reactions [6,7] (Figure 1).”
Background
Inflammasome activation by Pseudomonas aeruginosa' s ExlA pore‐forming toxin is detrimental for the host
Bouillot, S., Pont, S., Gallet, B., Moriscot, C., Deruelle, V., Attrée, I., & Huber, P. (2020) · Cellular Microbiology · doi:10.1111/cmi.13251 · Cited by 18
“However, extremely low amounts of IL-1β is nevertheless sufficient to induce inflammatory reactions, as previously noted (Garlanda et al., 2013).”
BackgroundInfluential
Cytokines and Chemokines in Tumor Growth and Progression
Mir, M. A., Rashid, M., & Jan, N. (2023) · Springer eBooks · doi:10.1007/978-981-99-4657-0_2 · Cited by 17
An Interleukin-1 Beta-Encoding Retrovirus Exhibits Enhanced Replication In Vivo
Browne, E. P. (2014) · Journal of Virology · doi:10.1128/jvi.02314-14 · Cited by 16
“Since IL-1R1 is broadly expressed in the immune system, IL-1 can affect many different immune lineages (16).”
Background
Increased sputum endotoxin levels are associated with an impaired lung function response to oral steroids in asthmatic patients
McSharry, C. P., Spears, M., Chaudhuri, R., Cameron, E. J., Husi, H., & Thomson, N. C. (2014) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2014.08.022 · Cited by 17
Evaluation of immunogenicity and protection mediated by Lawsonia intracellularis subunit vaccines
Fourie, K. R., Choudhary, P., Ng, S. H., Obradovic, M. R., Brownlie, R. M., Anand, S. K., & Wilson, H. L. (2021) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2021.110256 · Cited by 17
NLRP2 Is Overexpressed in Spinal Astrocytes at the Peak of Mechanical Pain Sensitivity during Complete Freund Adjuvant-Induced Persistent Pain
Ducza, L., Szűcs, P., Hegedűs, K., Bakk, E., Gajtkó, A., Wéber, I., & Holló, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111408 · Cited by 17
Jinwujiangu Capsule Treats Fibroblast-Like Synoviocytes of Rheumatoid Arthritis by Inhibiting Pyroptosis via the NLRP3/CAPSES/GSDMD Pathway
Ling, Y., Xiao, M., Huang, Z., Xu, H. Z., Huang, F., Ren, N., Chen, C., Lu, D. M., Yao, X., Xiao, L.-N., et al. (2021) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2021/4836992 · Cited by 18
“However, they can be transported outside with the assistance of the GSDMD protein related to perforation [28].”
Background
LDC7559 Exerts Neuroprotective Effects by Inhibiting GSDMD-Dependent Pyroptosis of Microglia in Mice with Traumatic Brain Injury
Yu, E., Zhang, E., Lv, X., Lin, Y., Lin, Z., Siaw-Debrah, F., Zhang, Y., Yang, S., Ruan, L., Zhuge, Q., et al. (2022) · Journal of Neurotrauma · doi:10.1089/neu.2021.0318 · Cited by 17
“53 Most cytokines contain a signal sequence that guides their cellular exit via secretory vesicles; however, the IL-1 family (including IL-1 b and IL-18) lacks a signal peptide to guide secretion via the endoplasmic reticulum to the Golgi secretory pathway.”
Influence of intestinal microecology in the development of gout or hyperuricemia and the potential therapeutic targets
Dang, K., Zhang, N., Gao, H., Wang, G., Liang, H., & Xue, M. (2023) · International Journal of Rheumatic Diseases · doi:10.1111/1756-185x.14888 · Cited by 18
Co-delivery of azithromycin and ibuprofen by ROS-responsive polymer nanoparticles synergistically attenuates the acute lung injury
Muhammad, W., Zhang, Y., Zhu, J., Xie, J., Wang, S., Wang, R., Feng, B., Zhou, J., Chen, W., Xu, Y., et al. (2023) · Biomaterials Advances · doi:10.1016/j.bioadv.2023.213621 · Cited by 17
Pipeline Therapies for Gout
Yip, K. H.-K., Braverman, G., Yue, L., & Fields, T. R. (2023) · Current Rheumatology Reports · doi:10.1007/s11926-023-01128-3 · Cited by 17
“…IL-1β is a potent mediator of the innate immune response with pleiotropic effects throughout the body, including induction of fever, stimulation of the hypothalamic-pituitary-adrenal axis, endothelial activation, promotion of neutrophil trafficking, and differentiation of lymphoid cells [40].”
Interleukin-1 regulates follicular T cells during the germinal center reaction
Belbézier, A., Engeroff, P., Fourcade, G., Vantomme, H., Vaineau, R., Gouritin, B., Bellier, B., Brochériou, I., Tchitchek, N., Graff‐Dubois, S., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1393096 · Cited by 15
“Interleukin-1 a and b (IL-1) are mainly known as potent proin ﬂ ammatory cytokines in innate immunity (1 – 3).”
BackgroundInfluential
The TLR4/NF-κB/NLRP3 and Nrf2/HO-1 pathways mediate the neuroprotective effects of alkaloids extracted from Uncaria rhynchophylla in Parkinson's disease
Zhang, C., Zhou, J., Zhuo, L., Zhang, W., Lv, L., Zhu, L., Zhang, J., Feng, F., Liu, W., Han, L., et al. (2024) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2024.118391 · Cited by 18
Mitigating Metabolic Dysfunction-associated Steatotic Liver Disease (MASLD): The Role of Bioactive Phytoconstituents in Indian Culinary Spices
Barbhuiya, P. A., Ahmed, A., Dutta, P. P., Sen, S., & Pathak, M. P. (2025) · Current Nutrition Reports · doi:10.1007/s13668-024-00598-w · Cited by 18
“Furthermore, IL-1β promotes local inflammation by triggering the production of IL-6, which is another cytokine that promotes inflammation [101].”
Serum CD121a (Interleukin 1 Receptor, Type I): A Potential Novel Inflammatory Marker for Coronary Heart Disease
Liu, Z., Zhang, M., Wu, J. S., Zhou, P., Liu, Y., Wu, Y., Yang, Y., & Lü, X. (2015) · PLoS ONE · doi:10.1371/journal.pone.0131086 · Cited by 17
“The binding receptors for IL-1β include CD121a, which is responsible for triggering IL-1-mediated inflammation, and the type II IL-1 receptor, which acts as non-signaling decoy receptor [7].”
Background
Membrane translocation of transient receptor potential ankyrin 1 induced by inflammatory cytokines in lung cancer cells
Takahashi, K., & Ohta, T. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.06.082 · Cited by 17
“The released IL-1a precursor is fully active and functions as a tissue injury alarm molecule, an alarmin [14].”
Background
Intrathecal cytokine profile in neuropathy with anti‐neurofascin 155 antibody
Ogata, H., Zhang, X., Yamasaki, R., Fujii, T., Machida, A., Morimoto, N., Kaida, K., Masuda, T., Ando, Y., Kuwahara, M., et al. (2019) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.50931 · Cited by 17
Helicobacter hepaticus infection-induced IL-33 promotes hepatic inflammation and fibrosis through ST2 signaling pathways in BALB/c mice
Cao, S., Zhu, L., Zhu, C., Feng, J., Yin, J., Jin, L., Xu, Y., Yang, H., Huang, Y., & Zhang, Q. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.02.139 · Cited by 18
The neutrophil inflammasome
Tyrkalska, S. D., Candel, S., & Mulero, V. (2020) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2020.103874 · Cited by 18
Inhibition of interleukin‐1β signalling promotes atherosclerotic lesion remodelling in mice with inflammatory arthritis
Dragoljevic, D., Lee, M. K. S., Louis, C., Shihata, W., Kraakman, M. J., Hansen, J. A., Masters, S. L., Hanaoka, B. Y., Nagareddy, P. R., Lancaster, G. I., et al. (2020) · Clinical & Translational Immunology · doi:10.1002/cti2.1206 · Cited by 17
“In vivo, the biological function of IL-1b is tightly regulated by two natural inhibitors: the decoy receptor IL-1 type 2 receptor (IL-1R2) and the IL-1R antagonist (IL-1Ra) which binds to the membrane-bound IL-1 type 1 receptor (IL-1R1).(6) Human IL-1Ra also binds to murine IL-1R to prevent signalling.”
Background
Identification of Genes Linking Natural Killer Cells to Apoptosis in Acute Myocardial Infarction and Ischemic Stroke
Feng, L., Tian, R.-F., Mu, X., Chen, C., Zhang, Y., Cui, J., Song, Y., Liu, Y., Zhang, M., Shi, L., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.817377 · Cited by 20
“Interleukin 1 beta (IL1b) is a central mediator of innate immunity and inflammation (59) that was first identified as being responsible for resistance against microbes (60).”
Background
C/EBPβ is a transcriptional key regulator of IL-36α in murine macrophages
Nerlich, A. G., Ruangkiattikul, N., Laarmann, K., Janze, N., Dittrich‐Breiholz, O., Kracht, M., & Goethe, R. (2015) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2015.06.002 · Cited by 17
IL-22 Signaling in the Tumor Microenvironment
Jiang, R., & Sun, B. (2021) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-030-55617-4_5 · Cited by 35

Authors: Garlanda, C., Dinarello, C. A., & Mantovani, A.
Affiliations: Radboud University Medical Center (NL)
University of Milan (IT)
Corresponding author: Mantovani, Alberto
ORCID: Dinarello, Charles A.
Mantovani, Alberto
Venue: Immunity
Publisher: Elsevier BV
Published: 2013-12
Volume: 39
Issue: 6
Pages: 1003-1018
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2013.11.010
PMC: PMC3933951
OpenAlex: W2145866317
Cited by: 1,945
References: 151
Citations by year: 2026: 80 · 2025: 118 · 2024: 136 · 2023: 122 · 2022: 168 · 2021: 172 · 2020: 202 · 2019: 165 · 2018: 194 · 2017: 192 · 2016: 171 · 2015: 156 · 2014: 66 · 2013: 1
FWCI: 11.46
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 376 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Funders: European Research Council
Associazione Italiana per la Ricerca sul Cancro
National Institutes of Health (A115614, AR-45584)
European Commission (FP7-HEALTH-2011- ADITEC 280873)
Topics: Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Keywords: interleukin-1 family, innate immunity, inflammation, IL-1 receptor family, interleukin-1 receptor antagonist, decoy receptor, IL-18, IL-33, IL-36, IL-37, IL-38, IL1RAP, SIGIRR, negative regulation of cytokine signaling, lymphocyte differentiation, innate and adaptive immunity
MeSH terms: Animals, Gene Expression Regulation, Humans, Immunity, Innate, Interleukin-1, Interleukins, Ligands, Receptors, Interleukin-1, Adaptive Immunity

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The Interleukin-1 Family: Back to the Future

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