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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Experimental atopic dermatitis depends on IL-33R signaling via MyD88 in dendritic cells
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“IL-18 subfamily (IL-18 and IL-37) and IL-36 subfamily (IL-36α/ β/γ, IL-36Ra and IL-38).(13) All IL-1 family members binding to”
Influential
Alarmin cytokines as central regulators of cutaneous immunity
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A Unique Population: Adipose-Resident Regulatory T Cells
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IL-1β expression is increased and regulates GABA transmission following chronic ethanol in mouse central amygdala
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IL-1 family cytokines as drivers and inhibitors of trained immunity
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“…is a potent activator of the inflammasome PGN-induced secretion of IL-1β by macrophages requires stimulation of IL-1β mRNA production, synthesis of pro-IL-1β protein, and activation of the NLRP3 inflammasome to process and release mature IL-1β (Agostini et al., 2004, Garlanda et al., 2013).”
Background
IL-38: A new factor in rheumatoid arthritis
Takenaka, S., Kaieda, S., Kawayama, T., Matsuoka, M., Kaku, Y., Kinoshita, T., Sakazaki, Y., Okamoto, M., Tominaga, M., Kanesaki, K., et al. (2015) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2015.10.015 · Cited by 70
“It is well known that IL-1 family members IL-1β and IL-18 have both inflammatory and anti-inflammatory effects in vivo [18,21].”
The Atypical Ubiquitin E2 Conjugase UBE2L3 Is an Indirect Caspase-1 Target and Controls IL-1β Secretion by Inflammasomes
Eldridge, M. J. G., Sanchez‐Garrido, J., Hoben, G. F., Goddard, P. J., & Shenoy, A. R. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.015 · Cited by 69
“Secreted IL-1b, IL-18, IL-1a, and HMGB1 promote inflammatory and antimicrobial responses (Garlanda et al., 2013; Yanai et al., 2012), and pyroptotic death of infected host cells removes microbial replicative niches.”
Background
IL-33 and ST2 levels in chronic kidney disease: Associations with inflammation, vascular abnormalities, cardiovascular events, and survival
Güngör, Ö., Ünal, H. U., Güçlü, A., Gezer, M., Eyileten, T., Güzel, F. B., Altunören, O., Erken, E., Oğuz, Y., Kocyigit, I. D., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0178939 · Cited by 70
Monocytes and dendritic cells are the primary sources of interleukin 37 in human immune cells
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Role of innate immune system in the pathogenesis of ankylosing spondylitis
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The Tumor Microenvironment in Colorectal Cancer Therapy
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Overexpression of Tear Inflammatory Cytokines as Additional Finding in Keratoconus Patients and Their First Degree Family Members
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“The IL-1 family of cytokines has strong proinflammatory actions and is responsible for the activation of collagenases and metalloproteinases, as well as for the overexpression of IL-6 [25, 26].”
Background
Pyroptosis: The missing puzzle among innate and adaptive immunity crosstalk
Hachim, M. Y., Khalil, B. A., Elemam, N. M., & Maghazachi, A. A. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.3mir0120-625r · Cited by 71
The Therapeutic Prospects of Targeting IL-1R1 for the Modulation of Neuroinflammation in Central Nervous System Disorders
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“IL-1 signaling has been implicated in several inflammatory diseases, prompting the need to find druggable therapeutic targets within the components of the IL-1 inflammatory pathway [4,36].”
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Mechanisms of immunomodulation by mammalian and viral decoy receptors: insights from structures
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Cytokines in oncolytic virotherapy
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Isoliquiritigenin, a potential therapeutic agent for treatment of inflammation-associated diseases
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Lysophospholipid Receptors, as Novel Conditional Danger Receptors and Homeostatic Receptors Modulate Inflammation—Novel Paradigm and Therapeutic Potential
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Expression of LLT1 and its receptor CD161 in lung cancer is associated with better clinical outcome
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“SIGIRR (Single immunoglobulin and toll-interleukin 1 receptor (TIR) domain) is a negative regulator of IL-1 receptor, and was suggested to play a major role in suppression of Th17 differentiation.(35,36) When considering all the Figure 5.”
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Negative Regulation of the IL-1 System by IL-1R2 and IL-1R8: Relevance in Pathophysiology and Disease
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Systemic Cytokine Profiles in Strongyloides stercoralis Infection and Alterations following Treatment
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“Finally, other proinflammatory cytokines, including IL-1 and IL-18, are major components driving harmful host inflammation (27).”
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miRNA‐Regulated Key Components of Cytokine Signaling Pathways and Inflammation in Rheumatoid Arthritis
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“…autoimmune, infectious and degenerative diseases, has increased (Sims and Smith, 2010; Dinarello, 2011a,b, 2013; Dinarello and van der Meer, 2013; Garlanda et al., 2013a) The IL-1 family encompasses 11 cytokines/ligands and 10 related receptors (Dinarello et al., 2010; Boraschi and Tagliabue,…”
Background
The enigmatic role of IL-38 in inflammatory diseases
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“Five splice variants, named IL-37a to IL-37e, have been described[3,46].”
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Menopause-Associated Depression: Impact of Oxidative Stress and Neuroinflammation on the Central Nervous System—A Review
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“The biological functions of these in-terleukins have been linked to many disease processes, including MDD [98,99].”
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Pyroptosis in Osteoblasts: A Novel Hypothesis Underlying the Pathogenesis of Osteoporosis
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Therapeutic potential of targeting interleukin‐1 family cytokines in chronic inflammatory skin diseases*
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Clinical chorioamnionitis at term V: umbilical cord plasma cytokine profile in the context of a systemic maternal inflammatory response
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Interleukin-1 is not involved in synovial inflammation and cartilage destruction in collagenase-induced osteoarthritis
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miR-146a-5p plays an essential role in the aberrant epithelial–fibroblast cross-talk in COPD
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“While the importance of IL-1RI/MyD88 signaling in host resistance against A. fumigatus infection is unequivocal (22, 35, 42), the specific roles of IL-1 and IL-1 for the prevention of fungal growth and disease are controversial in the literature (22, 26, 27).”
BackgroundInfluential
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“[16] Garlanda C, Dinarello CA, Mantovani A.”
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“In this regard, a highly speculative hypothesis involves the IL1-receptor antagonist (IL1-RA), a natural competitor for binding to the IL1-receptor (IL1-R), which is synthesized and released by the same cells that produce IL1 (31).”
Influential
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“If present in high enough concentration cytokines may also manifest endocrine-like behaviour, causing inflammation in other body areas [27].”
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Interleukin-1/-33 Signaling Pathways as Therapeutic Targets for Endometriosis
Kato, T., Yasuda, K., Matsushita, K., Ishii, K. J., Hirota, S., Yoshimoto, T., & Shibahara, H. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02021 · Cited by 61
Comparison of Inhibitory Capacities of 6-, 8- and 10-Gingerols/Shogaols on the Canonical NLRP3 Inflammasome-Mediated IL-1β Secretion
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Interleukin-33 in Malignancies: Friends or Foes?
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Biological functions and therapeutic opportunities of soluble cytokine receptors
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Royal Jelly Abrogates Cadmium-Induced Oxidative Challenge in Mouse Testes: Involvement of the Nrf2 Pathway
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“The overproduction of TNF-α in response to pathogens stimulates the release of other pro-inflammatory cytokines, including IL-β, which enhances gene expression associated with inflammation [44].”
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Interleukin 1 is a key driver of inflammatory bowel disease-demonstration in a murine IL-1Ra knockout model
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Atherosclerosis and inflammation. New therapeutic approaches
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Inflammatory Regulation of CNS Barriers After Traumatic Brain Injury: A Tale Directed by Interleukin-1
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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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