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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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Cites
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Interleukin‐1 Family Cytokines in Liver Diseases
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BCAP links IL-1R to the PI3K–mTOR pathway and regulates pathogenic Th17 cell differentiation
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Skin tape sampling technique identifies proinflammatory cytokines in atopic dermatitis skin
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Genome Editing Using CRISPR-Cas9 and Autoimmune Diseases: A Comprehensive Review
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“For example, interleukin-36 (IL-36) cytokines (IL-36A, IL-36B, and IL-36G) and members of the IL-1 family can cause pro-inflammatory effects in the skin and other organs [22].”
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BackgroundCCL22 Signaling in the Tumor Environment
Röhrle, N., Knott, M. M. L., & Anz, D. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-36667-4_8 · Cited by 62
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“…interleukin family (Dinarello et al., 2012; Dinarello, 2010), IL‐1, is affecting a wide range of organs and cells with quite a low concentration (Dinarello, 2009), can be divided into IL‐1α and IL‐1β that are from different cells but can combine to the same receptor IL‐1R1 (Garlanda et al., 2013).”
BackgroundThe IL-1 family in tumorigenesis and antitumor immunity
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“Thus, we might state that the host’s inflammatory response is closely regulated by IL-1β since it was shown that it augments this response to both endogenous and exogenous stimuli, also inducing the expression of other cytokines, such as IL-2, IL-6, IL-12 and TNF-α, but also of other pro-inflammatory mediators, among…”
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BackgroundPrediction of sepsis in trauma patients
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“IL-1β, IL-18, IL-33, IL-36α, IL-36β and IL-36γ), three ligands with antagonist activity (IL-1Ra, IL-36Ra and IL-38) and a newly renamed anti-inflammatory cytokine, IL-37 (4-6).”
IL-37 isoform D downregulates pro-inflammatory cytokines expression in a Smad3-dependent manner
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“IL-6 and IL-1b are mainly produced by activated macrophages in the colon (Akira et al, 1993; Garlanda et al, 2013) and IL-1b known to be a potent inducer of IL6 (Tosato & Jones, 1990).”
BackgroundVulnerable Atherosclerotic Plaque: Is There a Molecular Signature?
Chiorescu, R. M., Mocan, M., Inceu, A.-I., Buda, A. P., Blendea, D. C., & Vlaicu, S. I. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113638 · Cited by 59
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“The IL-1 receptor accessory protein (IL-1RAcP, also termed IL-1R3), for example, is critically involved in mediating the functions of not only IL-1α and IL-1β, but also of IL-33 and the different IL-36 cytokines (IL-36α, IL-36β, IL-36γ [40].”
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Cytokines that Modulate the Differentiation of Th17 Cells in Autoimmune Uveitis
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“IL-1β is a member of the IL-1 family, which also includes six proinflammatory agonists (IL-1α, IL-18, IL- 33, IL-36α, IL-36β, and IL-36γ) and four antagonists (IL-1R antagonist [IL-1Ra], IL-36Ra, IL37, and IL-38) [61].”
BackgroundInflammasome Contribution to the Activation of Th1, Th2, and Th17 Immune Responses
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“The IL-1 system is involved in protective host responses in infections and inflammation, as well as in the activation of innate and adaptive lymphoid cells [37,38].”
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“Unlike IL-1b, which is involved in Th17 cell responses, IL-18 has a role in Th1 immunity (40).”
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Mass spectrometry analysis of plasma from amyotrophic lateral sclerosis and control subjects
Xu, Z., Lee, A., Nouwens, A. S., Henderson, R. D., & McCombe, P. (2018) · Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration · doi:10.1080/21678421.2018.1433689 · Cited by 55
“IL-1 is a cytokine that is central to inflammation (77,78).”
BackgroundInflammasomes: Emerging Central Players in Cancer Immunology and Immunotherapy
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“Additionally, the role of IL-1β in angiogenesis, tumor promotion, metastasis, resistance to chemotherapy, and immunosuppression are well-described (39, 40).”
BackgroundA review of innate and adaptive immunity to coccidioidomycosis
Hung, C.-Y., Hsu, A. P., Holland, S. M., & Fierer, J. (2018) · Medical Mycology · doi:10.1093/mmy/myy146 · Cited by 54
Suppression of Inflammasome Activation by IRF8 and IRF4 in cDCs Is Critical for T Cell Priming
McDaniel, M. M., Kottyan, L. C., Singh, H., & Pasare, C. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107604 · Cited by 57
“Although inflammasome products such as the IL-1 family of cytokines are important for adaptive immunity (Ben-Sasson et al., 2009; Garlanda et al., 2013; Jain et al., 2018), release of these cytokines following inflammasome activation is generally concurrent with cell death via pyroptosis.”
IL-1 interacts with ethanol effects on GABAergic transmission in the mouse central amygdala
Bajo, M., Varodayan, F. P., Madamba, S. G., Robert, A. J., Casal, L. M., Oleata, C. S., Siggins, G. R., & Roberto, M. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00049 · Cited by 55
“After recruitment of the myeloid differentiation primary response gene 88 (MyD88) adaptor to the IL-1R/IL-1RAcpP complex, signaling pathways, including NF-κB, c-Jun N-terminal kinase (JNK) and p38 MAPK, are activated (Garlanda et al., 2013; Krumm et al., 2014).”
Increased expression of IL-18 in the serum and islets of type 1 diabetics
Harms, R. Z., Yarde, D. N., Guinn, Z. P., Lorenzo-Arteaga, K. M., Corley, K. P., Cabrera, M. S., & Sarvetnick, N. (2015) · Molecular Immunology · doi:10.1016/j.molimm.2014.12.012 · Cited by 54
“In addition, IL-18 has also been found to enhance natural killer (NK) cell as well as macrophage activity [7-9].”
BackgroundInterleukin-1 loop model for pathogenesis of Langerhans cell histiocytosis
Murakami, I., Matsushita, M., Iwasaki, T., Kuwamoto, S., Kato, M., Nagata, K., Horie, Y., Hayashi, K., Imamura, T., Morimoto, A., et al. (2015) · Cell Communication and Signaling · doi:10.1186/s12964-015-0092-z · Cited by 53
“A tight regulation via receptor antagonists, decoy receptors, and signaling inhibitors ensures a balance between amplification of innate immunity and uncontrolled inflammation [124].”
BackgroundA Guide to IL ‐1 family cytokines in adjuvanticity
Muñoz‐Wolf, N., & Lavelle, E. C. (2018) · FEBS Journal · doi:10.1111/febs.14467 · Cited by 54
Colonic dysmotility associated with high‐fat diet‐induced obesity: Role of enteric glia
Antonioli, L., D’Antongiovanni, V., Pellegrini, C., Fornai, M., Benvenuti, L., di Carlo, A., van den Wijngaard, R. M., Caputi, V., Cerantola, S., Giron, M. C., et al. (2020) · The FASEB Journal · doi:10.1096/fj.201901844r · Cited by 55
Vitenberga-Verza, Z., Pilmane, M., Šerstņova, K., Melderis, I., Gontar, Ł., Kochański, M., Drutowska, A., Maróti, G., & Prieto‐Simón, B. (2022) · Pathogens · doi:10.3390/pathogens11030372 · Cited by 52
“The interleukin (IL)-1 (IL-1) family is one of the most widely represented groups of cytokines [20].”
BackgroundMicroRNAs as immune regulators and biomarkers in tuberculosis
Wang, L., Xiong, Y., Fu, B., Guo, D. S., Zaky, M. Y., Lin, X., & Wu, H. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1027472 · Cited by 56
“Previous studies have reported that cytokines and receptors of the IL-1 family are potent factors that prime and amplify the immune response, affecting nearly all cells that are involved in the innate immune system (52, 53).”
BackgroundCostas, B., Couto, A., Azeredo, R., Machado, M., Krogdahl, Å., & Oliva‐Teles, A. (2014) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2014.05.032 · Cited by 53
Markowitz, G. J., Yang, P., Fu, J., Michelotti, G. A., Chen, R., Sui, J., Yang, B., Qin, W., Zhang, Z., Wang, F., et al. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-1548 · Cited by 54
“Our earlier experiments had not shown a genotype-specific difference in intratumoral NK cell accumulation, however IL-18 markedly regulates NK cell activity (25).”
InfluentialIL-33-matured dendritic cells promote Th17 cell responses via IL-1β and IL-6
Park, S.-H., Kim, M. S., Lim, H. X., Cho, D., & Kim, T. S. (2017) · Cytokine · doi:10.1016/j.cyto.2017.07.022 · Cited by 52
“IL-33, a member of the IL-1 cytokine family [1], is a proinflammatory cytokine that is expressed in various human tissues, including adipocytes, synovial fibroblasts, and vascular endothelial cells, as well as epithelial cells of the skin, intestinal tract, and lung [2–5].”
BackgroundXu, M., Cheng, Z., Ding, Z., Wang, Y., Guo, Q., & Huang, C. (2018) · Molecular Pain · doi:10.1177/1744806918767549 · Cited by 52
“Although Res cannot suppress upregulation of IL-1b in the dorsal spinal cord, it can block its effect.33,34 Current data suggest that all known actions of IL-1 are mediated via a single cell surface receptor, IL-1R1.”
BackgroundBelizário, J. E., Neyra, J. M., & Rodrigues, M. F. S. D. (2018) · Innate Immunity · doi:10.1177/1753425918800200 · Cited by 53
“Caspase-1 promotes the cleavage of pro-inflammatory cytokines IL-1b and IL-18, which are then released from secretory lysosomes or through cellular membrane leakage.(100,103,106) Murine caspase-11 and its human homologs’ caspase-4 and -5 are activated directly by the binding of bacterial LPS that enter the cytosol of…”
BackgroundFGF2 and IL-1β – explorers of unconventional secretory pathways at a glance
Pallotta, M. T., & Nickel, W. (2020) · Journal of Cell Science · doi:10.1242/jcs.250449 · Cited by 49
Rasheed, M., Battu, A., & Kaur, R. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.813741 · Cited by 51
“The procaspase-1 is cleaved into an active inflammatory cysteine protease caspase-1 following assembly of the inflammasome complex (40).”
BackgroundSabo, M. C., Lehman, D. A., Wang, B., Richardson, B. A., Srinivasan, S., Osborn, L., Matemo, D. N., Kinuthia, J., Fiedler, T. L., Munch, M. M., et al. (2019) · Sexually Transmitted Infections · doi:10.1136/sextrans-2018-053949 · Cited by 51
Tsurutani, N., Mittal, P., Rose, M. S., Ngoi, S. M., Svedova, J., Ménoret, A., Treadway, F. B., Laubenbacher, R., Suarez-Ramirez, J. E., Cauley, L. S., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1501217 · Cited by 51
“IL-18, IL-33, and IL-36 receptors belong to the same family and use similar signaling components that include MyD88 and IL-1R–associated kinase (42).”
BackgroundSikora, J., Mielczarek‐Palacz, A., & Kondera‐Anasz, Z. (2016) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.21944 · Cited by 51
“It consists of the following distinct molecular forms: intercellular IL-1α (IL-1F1), extracellular IL-1β (IL-1F2), IL-1 receptor antagonist (IL-1Ra, IL-1F3), and also IL-18 (IL-1F4), IL-33 (IL-1F11), IL-37 (IL-1F7), and IL-38 (L-1F10) (1, 2).”
BackgroundStrategies to Augment Natural Killer (NK) Cell Activity against Solid Tumors
Chen, Z., Yang, Y., Liu, L. L., & Lundqvist, A. (2019) · Cancers · doi:10.3390/cancers11071040 · Cited by 53
“Interleukin-1 receptor 8 (IL-1R8) is a member of the IL-1 receptor (ILR) family that is involved in negative regulation of ILR and Toll-like receptor (TLR) downstream signaling pathways and orchestrate innate and adaptive immunity [131].”
BackgroundVasanthakumar, A., & Kallies, A. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028506 · Cited by 53
“Thus, expression of IL1 familymembers is tightly regulated at multiple levels, including transcriptional and posttranslational mechanisms as well as the expression of decoy and antagonist receptors (Garlanda et al. 2013).”
BackgroundInfluentialThe Association between TNF-alpha, IL-1 alpha and IL-10 with Alzheimer's Disease
Čuljak, M., Perković, M. N., Uzun, S., Štrac, D. Š., Erjavec, G. N., Leko, M. B., Šimić, G., Tudor, L., Konjevod, M., Kozumplik, O., et al. (2020) · Current Alzheimer Research · doi:10.2174/1567205017666201130092427 · Cited by 52
Mathew, D. J., Newsom, E. M., Guyton, J. M., Tuggle, C. K., Geisert, R. D., & Lucy, M. C. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.114.126128 · Cited by 50
“Juxtapositioning of the IL1RI and IL1RAP toll/interleukin 1 receptor (TIR) domains within the cytoplasm is necessary to initiate a cascade of second-messenger protein interactions.”
BackgroundInfluentialKang, M., Yoon, C. M., Nam, M., Kim, D., Choi, J., Lee, C. G., & Elias, J. A. (2015) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2014-0366oc · Cited by 48
Bell, S., Mehta, G., Moore, K. P., & Britton, A. R. (2016) · Journal of Internal Medicine · doi:10.1111/joim.12544 · Cited by 52
Inherited human IRAK-1 deficiency selectively impairs TLR signaling in fibroblasts
Mina, E. D., Borghesi, A., Zhou, H., Bougarn, S., Boughorbel, S., Israël, L., Meloni, I., Chrabieh, M., Ling, Y., Itan, Y., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620139114 · Cited by 47
Tomasoni, R., Morini, R., López‐Atalaya, J. P., Corradini, I., Canzi, A., Rasile, M., Mantovani, C., Pozzi, D., Garlanda, C., Mantovani, A., et al. (2017) · eLife · doi:10.7554/elife.21735 · Cited by 52
“IL-1R8 dampens the activation of the TLRs and IL-1R signalling pathways by intracellularly interfering with the association of adaptor molecules to the receptor complexes, including NF-kB and JNK (Riva et al., 2012; Garlanda et al., 2013b).”
BackgroundCritical role of inflammatory mast cell in fibrosis: Potential therapeutic effect of IL ‐37
Conti, P., Caraffa, A., Mastrangelo, F., Tettamanti, L., Ronconi, G., Frydas, I., Kritas, S. K., & Theoharides, T. C. (2018) · Cell Proliferation · doi:10.1111/cpr.12475 · Cited by 51
Cheung, P. H., Ye, Z., Lee, T.-W. T., Chen, H., Chan, C., & Jin, D. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.4ab0420-694r · Cited by 52
Epithelial-interleukin-1 inhibits collagen formation by airway fibroblasts: Implications for asthma
Osei, E. T., Mostaço-Guidolin, L. B., Hsieh, A., Warner, S., Fouadi, M., Wang, M. X., Cole, D. J., Maksym, G. N., Hallstrand, T. S., Timens, W., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-65567-z · Cited by 55
Guo, C., Yang, X., Wang, F., & Ma, X. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2606 · Cited by 49
Structural and Functional Attributes of the Interleukin-36 Receptor
Yi, G., Ybe, J. A., Saha, S. S., Caviness, G. O., Raymond, E. L., Ganesan, R., Mbow, M. L., & Kao, C. C. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.723064 · Cited by 49
“IL-36R is a member of the IL-1 receptor family that contains six receptor proteins that form four signaling complexes: IL-1RI, IL-18R, IL-33R, and IL-36R, and two decoy receptors and two negative regulators (7).”
BackgroundLucinda, N., Figueiredo, M. M., Pessoa, N. L., Santos, B. S. Á. D. S., Lima, G. K., Freitas, A. M., Machado, A. V., Kroon, E. G., Antonelli, L. R. D. V., & Campos, M. A. (2017) · Virology Journal · doi:10.1186/s12985-017-0692-x · Cited by 51
Scholz, H., & Eder, C. (2017) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2017.07.004 · Cited by 49
“It converts biologically inactive precursors of the proinflammatory cytokines interleukin (IL)-1β, IL-18 and IL-33 into their mature, biologically active forms, which play a pivotal role in promoting neuroinflammatory processes (Eder, 2009; Garlanda et al., 2013).”
BackgroundChung, J., Kim, S., Lee, H. A., Park, M. H., Kim, S., Song, Y., & Na, H. S. (2018) · Journal of Periodontology · doi:10.1002/jper.17-0727 · Cited by 49
Mercury and arsenic attenuate canonical and non-canonical NLRP3 inflammasome activation
Ahn, H., Kim, J., Kang, S. G., Yoon, S., Ko, H., Kim, P.-H., Hong, E., An, B., Lee, E., & Lee, G. (2018) · Scientific Reports · doi:10.1038/s41598-018-31717-7 · Cited by 49
Xia, T., Gao, R., Zhou, G., Liu, J., Li, J., & Shen, J. (2019) · BioMed Research International · doi:10.1155/2019/4039472 · Cited by 49
“It is well known that the chondrocyte protective effects mediated by NF-κB activation are connected with the inhibition of the MMP genes [50, 51].”
BackgroundRoles of Inflammasomes in Inflammatory Kidney Diseases
Fan, J., Xie, K., Wang, L., Zheng, N., & Yu, X. (2019) · Mediators of Inflammation · doi:10.1155/2019/2923072 · Cited by 51
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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