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The Interleukin-1 Family: Back to the Future
Open accessAbstract
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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“In addition, NLRP3 inflammasome activation reduces phagocytosis of Aβ by microglial cells, thus increasing the Aβ depositions and contributing to the pathogenesis of AD (Garlanda et al., 2013; Gold and El Khoury, 2015).”
From The role of microglia in retinal neurodegeneration: Alzheimer’s disease, parkinson, and glaucoma. (2017) · cites this paper as Garlanda et al., 2013
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“Interleukin-18 is a member of the large interleukin-1 family40 that has recently been associated with cytokine storm disorders.”
From Cytokine storm (2020) · cites this paper as [40]
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“In contrast to IL-1a and IL-1b, IL-1Ra will not recruit the second unit of the IL-1 receptor type I (IL-1RacP) needed for signaling (69).”
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“The IL-1 family comprises 11 members and they are either cytokines with agonist activity (IL-1a, IL-1b, IL-18, IL33, IL-36a, IL-36b, IL-36g, and IL-37) or receptor antagonists (IL-1Ra, IL-36Ra, and IL-38) (Garlanda et al., 2013).”
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Targeting cytokines to treat autoinflammatory diseases
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“This family consists of eleven cytokines and includes seven ligands with agonist activity (IL-1α and IL-1β, IL-18, IL-33, IL-36α, IL-36β, and IL-36γ), three receptor antagonists (IL-1Ra, IL-36Ra, and IL-38), and the anti-inflammatory cytokine (IL-37) [58].”
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“IL-1RAcP is a shared subunit among IL-1, IL-33, and IL-36 (2, 3).”
BackgroundThe Role, Involvement and Function(s) of Interleukin-35 and Interleukin-37 in Disease Pathogenesis
Bello, R. O., Chin, V. K., Isnadi, M. F. A. R., Majid, R. A., Abdullah, M. A., Lee, T. Y., Zakaria, Z. A., Hussain, M. K., & Basir, R. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19041149 · Cited by 53
“SIGGIR does not elicit the classical pro-inflammatory signaling cascade that is typical to the IL-1 receptor family, contrariwise, it operates by inhibition of IL-1R and TLR-dependent inflammation [90].”
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“IL-1 is a central mediator of innate immunity and inflammation.(10) Not surprisingly, therefore, IL-1Ra and other IL-1 family members play a role in disease progression in solid and hematological malignancies.”
BackgroundPyroptosis in Steatohepatitis and Liver Diseases
Knorr, J., Wree, A., & Feldstein, A. E. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2021.167271 · Cited by 48
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“Interleukin-1 (IL-1) is a master inflammatory cytokine that regulates all aspects of immunological responses of the host against infection and injury [1].”
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Rao, S., Tsang, L. S., Zhao, M., Shi, W., & Lu, Q. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.881431 · Cited by 51
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“Among the most upregulated genes was IL-36γ (also called IL1F9), a newly characterized cytokine of the IL-1 family [25].”
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“cleavage to gain bioactivity.(109) IL‐18 is a key cytokine implicated in innate and adaptive type 1 responses and plays a crucial role in the interplay between macrophages/ DCs and NK cells.”
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Interleukin-1 in COVID-19 Infection: Immunopathogenesis and Possible Therapeutic Perspective
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“IL-1 a is a bifunctional cytokine and its precursor gene is expressed in several cells such as (26).”
The roles of interleukin‐1 receptor accessory protein in certain inflammatory conditions
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“The last member of this family, IL- 36, contributes to the differentiation of Th1 and Th17 cells and is involved in the pathogenesis of psoriasis [39].”
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“Caspases-3 and -7 inactivate IL-33 by cleaving its C-terminal IL-1 domain [63].”
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“IL-1ra competitively blocks the binding of IL-1b and IL-1a to IL-1 receptor and therefore acts as an anti-inflammatory cytokine released by peripheral blood leukocytes during the inflammatory process.((23)) IL-1ra is also released by hepatocytes, especially during the acute-phase response, and therefore is considered…”
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“IL-1β is a pro-inflammatory cytokine while IL-10, is anti-inflammatory and both are known to be activated by the innate immune system [28,29].”
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Khalid, S. I., Ampie, L., Kelly, R. M., Ladha, S. S., & Dardis, C. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00486 · Cited by 46
“Interleukin 1 is an endogenous pyrogen and a mediator of auto-immune and infectious diseases (26).”
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“Thus, it is possible that HBV antigens activated multiple cellular factors to induce the expression of IL-1 β and perhaps also activate inflammasomes, which are important for the activation of IL-1 β (Garlanda et al., 2013).”
IL‐1β Is an Androgen‐Responsive Target in Macrophages for Immunotherapy of Prostate Cancer
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“Because the IL-1R1 is required for the positive autocrine feedback loop that augments IL-1 β production, 18,19,35,36 loss of IL-1R1 in VF ; IL-1R1 − / − hematopoietic cells prevented the massive overproduction of IL-1 β observed in VF hematopoietic cells.”
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Alternaria extract activates autophagy that induces IL-18 release from airway epithelial cells
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Interleukin-1 and TRAF6-dependent activation of TAK1 in the absence of TAB2 and TAB3
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“GST pulldown was performed as described previously (9).”
BackgroundMethodInfluentialTNF Receptor-Associated Factor (TRAF) Signaling Network in CD4+ T-Lymphocytes
So, T., Nagashima, H., & Ishii, N. (2015) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.236.139 · Cited by 48
Biomarkers for Temporomandibular Disorders: Current Status and Future Directions
Zwiri, A. M. A., Al-Hatamleh, M. A. I., Ahmad, W. M. A. W., Asıf, J. A., Khoo, S. P., Husein, A., Ab‐Ghani, Z., & Kassim, N. K. (2020) · Diagnostics · doi:10.3390/diagnostics10050303 · Cited by 42
“To be specific, IL-1α and IL-1β lead to pro-inflammatory impacts, while IL-1ra prevents the pro-inflammatory functions by playing its role as the competitive receptor inhibitor [85].”
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“tors whereby the majority forms a dimer with the IL1RAP co-receptor.(15) Activation of the IL1 receptor complex activates the MyD88/IRAK1/IRAK4/TRAF6/TAK1 signaling pathway, which in turn results in activation of NFkB and mitogen-activated protein kinases (MAPK), including p38.”
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Ferguson, B. J., Newland, S. A., Gibbs, S. E., Tourlomousis, P., dos Santos, P. F., Patel, M. N., Hall, S. W., Walczak, H., Schramm, G., Haas, H., et al. (2015) · International Journal for Parasitology · doi:10.1016/j.ijpara.2015.08.005 · Cited by 42
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Cytokines as therapeutic targets in skin inflammation
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“The anti-inflammatory cytokine TGFb and to a lesser extent TLR ligands and proinflammatory cytokines (IL-1b, TNF, IL-18) can induce IL-37 production (reviewed in [86]).”
BackgroundRobaszkiewicz, A., Qu, C., Wiśnik, E., Płoszaj, T., Mirsaidi, A., Kunze, F. A., Richards, P. J., Cinelli, P., Mbalaviele, G., & Hottiger, M. O. (2016) · Scientific Reports · doi:10.1038/srep21131 · Cited by 44
Role of Interleukin 36γ in Host Defense Against Tuberculosis
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“cules IL-36α, IL-36β, and IL-36γ and the putative IL-36 receptor antagonist (IL-36RN) [18].”
BackgroundInfluentialDuration of red blood cell storage and inflammatory marker generation.
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Mannan-induced Nos2 in macrophages enhances IL-17–driven psoriatic arthritis by innate lymphocytes
Zhong, J., Scholz, T., Yau, A. C. Y., Guérard, S., Hüffmeier, U., Burkhardt, H., & Holmdahl, R. (2018) · Science Advances · doi:10.1126/sciadv.aas9864 · Cited by 42
“NO is required for IL-17A production of ILC3 It is well known that IL-1R1 is expressed in type 3 innate lymphoid cells (ILC3) and gd T cells, resulting in an IL-1a–triggered feedback loop involving IL-17 production at early phases of sterile inflammation (25).”
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Peripheral Inflammatory Hyperalgesia Depends on P2X7 Receptors in Satellite Glial Cells
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Prion Pathogenesis in the Absence of NLRP3/ASC Inflammasomes
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Pathogenetic role and clinical significance of interleukin‐1β in cancer
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“The most important of them are IL1α, IL-1β, IL-1 receptor antagonist (IL-1Ra), IL-18, IL-33, IL-36α, IL-36β, IL36γ and IL-38 [10].”
BackgroundComplex host genetic susceptibility to Staphylococcus aureus infections
Shukla, S. K., Rose, W. E., & Schrodi, S. J. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.05.008 · Cited by 40
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“Interleukin 1 cytokine family members (IL1A, IL1B, IL1R1, www.frontiersin.org May 2014 | Volume 5 | Article 125 | 5 and IL1RL2) are known mediators of immune and inflammatory responses (Garlanda et al., 2013).”
BackgroundFrom proteomics to discovery of first-in-class ST2 inhibitors active in vivo
Ramadan, A. M., Daguindau, É., Rech, J. C., Chinnaswamy, K., Zhang, J., Hura, G. L., Griesenauer, B., Bolten, Z. T., Robida, A. M., Larsen, M. J., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.99208 · Cited by 42
“Both sST2 and ST2 share the same extracellular domain (ECD) (22, 24) that bind with the only known ligand, IL-33 (21).”
BackgroundAutoinflammatory Pathogenesis and Targeted Therapy for Adult-Onset Still’s Disease
Li, S., Zheng, S., Tang, S., Pan, Y., Zhang, S., Fang, H., & Qiao, J. (2019) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-019-08747-8 · Cited by 41
“IL-1β, one of the 11 members of the IL-1 family, is primarily produced by hematopoietic cells, including monocytes, macrophages, dendritic cells, and neutrophils [33].”
BackgroundTseng, H., Kulina, I., Girard, D., Gueguen, J., Vaquette, C., Salga, M., Fleming, W., Jose, B., Millard, S. M., Pettit, A. R., et al. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4482 · Cited by 43
“Because IL-1 comprises two distinct but functionally redundant proteins, namely IL-1α and IL-1β encoded by two distinct genes, which both bind to their common IL-1 receptor IL1R1,((31,32)) we tested the involvement of IL1-mediated signaling in Il1r1 / mice defective for IL1R1.”
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Mesenchymal stem cells in radiation-induced lung injury: From mechanisms to therapeutic potential
Hou, G., Li, J., Liu, W., Wei, J., Xin, Y., & Jiang, X. M. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1100305 · Cited by 43
“IL-1, the main mediator of innate immunity and inflammation, is significantly reduced after MSC treatment (Garlanda et al., 2013).”
BackgroundLiang, Q., Zheng, J., Zuo, H., Li, C., Niu, S., Yang, L., Yan, M., Weng, S., He, J., & Xu, X. (2017) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2017.04.011 · Cited by 40
“cn They play essential roles in regulation of various innate and adaptive immune processes (Garlanda et al., 2013; Huang et al., 2015; Isailovic et al., 2015).”
BackgroundSiddiqui, I., Erreni, M., Kamal, M. A., Porta, C., Marchesi, F., Pesce, S., Pasqualini, F., Schiarea, S., Chiabrando, C., Mantovani, A., et al. (2017) · OncoImmunology · doi:10.1080/2162402x.2017.1388485 · Cited by 40
“Cytokines of the IL-1 family are key inflammatory mediators.(12) The presence of IL-1 at sites of tumor development activates NF-kB and enhances the expression of adhesion molecules on endothelial and malignant cells and promotes early tumor invasiveness, angiogenesis and metastasis.”
Backgroundda Silva, F. R. P., Vasconcelos, A. C. C. G., França, L. F. D. C., Lenardo, D. D., Nascimento, H. M. S., & Vasconcelos, D. F. P. (2018) · Gene · doi:10.1016/j.gene.2018.05.067 · Cited by 40
Herman, F. J., Westfall, S., Brathwaite, J. S., & Pasinetti, G. M. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00867 · Cited by 43
“Upon activation, the caspase-1 domain of the NLRP3 inflammasome cleaves zymogen forms of IL-1β and IL-18 into their functional forms (Garlanda et al., 2013).”
BackgroundHuo, X., Fan, C., Ai, T., & Su, J. (2020) · Vaccines · doi:10.3390/vaccines8040567 · Cited by 40
“IL-1 is an important early inflammatory cytokine that plays a vital role in regulating defensive and pathological innate immunity responses [38].”
BackgroundInflammasomes in dendritic cells: Friend or foe?
Hatscher, L., Amon, L., Heger, L., & Dudziak, D. (2021) · Immunology Letters · doi:10.1016/j.imlet.2021.04.002 · Cited by 40
Zhao, B., Chen, W., Jiang, R., Zhang, R., Wang, Y., Wang, L., Gordon, L. K., & Chen, L. (2015) · Experimental Eye Research · doi:10.1016/j.exer.2015.06.018 · Cited by 40
Pathomechanisms of bone loss in rheumatoid arthritis
Sakthiswary, R., Veshaaliini, R. U., Chin, K., Das, S., & Sirasanagandla, S. R. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.962969 · Cited by 40
Interleukin-1 Receptor Antagonist as Therapy for Traumatic Brain Injury
Lindblad, C., Rostami, E., & Helmy, A. E. (2023) · Neurotherapeutics · doi:10.1007/s13311-023-01421-0 · Cited by 43
“In addition, the IL-1 family is also composed of proteins with antagonistic effects to IL-1 and IL-1R1 [22, 27].”
BackgroundInfluentialResearch progress on pyroptosis and its effect on the central nervous system
Hao, W., & Feng, C. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106333 · Cited by 42
“IL-1 β could bind to IL-1 receptors on the surface of immune cells and triggering a series of physiological processes, such as fever, vasodilation, hematopoiesis, tissue migration, as well as cytokines and chemokines expression (Garlanda et al., 2013).”
BackgroundMechanism of NLRP3 Inflammasome in Epilepsy and Related Therapeutic Agents
Chen, J., Gao, Y., Liu, N., Hai, D., Wei, W., Liu, Y., Lan, X., Jin, X., Yu, J., & Ma, L. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.03.029 · Cited by 42
Deciphering the crosstalk among IL-1 and IL-10 family cytokines in intestinal immunity
Manzanillo, P. S., Eidenschenk, C., & Ouyang, W. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.06.003 · Cited by 44
In vivo pre-activation of monocytes in patients with axial spondyloarthritis
Conrad, K., Wu, P., Sieper, J., & Syrbe, U. (2015) · Arthritis Research & Therapy · doi:10.1186/s13075-015-0694-2 · Cited by 39
“Proinflammatory responses are tightly controlled by concomitant induction of antiinflammatory mediators, such as IL-1ra, which competes with IL-1 for binding to the IL-1 receptor 1 [6], and IL-10, which is produced by monocytes at later time points after stimulation and downregulates TNFα production [7].”
BackgroundMonogenic autoinflammatory diseases: Cytokinopathies
Moghaddas, F., & Masters, S. L. (2015) · Cytokine · doi:10.1016/j.cyto.2015.02.012 · Cited by 39
“Once released, IL-36 cytokines lead to a number of factors that induce Th1 and Th17 polarisation [4,47].”
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“IL-1ra inhibits signaling by binding to the IL1R1 and preventing the recruitment of IL-1RAcP, which is critical for the initiation of IL-1R1 signaling (Garlanda et al., 2013; Krumm et al., 2014).”
BackgroundAre ILC 2s Jekyll and Hyde in airway inflammation?
Ealey, K. N., Moro, K., & Koyasu, S. (2017) · Immunological Reviews · doi:10.1111/imr.12547 · Cited by 39
Metadata
- Authors
- Garlanda, C., Dinarello, C. A., & Mantovani, A.
- Affiliations
- Radboud University Medical Center (NL)
- University of Milan (IT)
- Corresponding author
- Mantovani, Alberto
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 39
- Issue
- 6
- Pages
- 1003-1018
- ISSN
- 1074-7613 (ISSN-L)
- 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
- 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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