Clinical relevance and therapeutic potential of IL-38 in immune and non-immune-related disorders

Interleukin-38 (IL-38) is the most recent member of the IL-1 family that acts as a natural inflammatory inhibitor by binding to cognate receptors, particularly the IL-36 receptor. In vitro, animal and human studies on autoimmune, metabolic, cardiovascular and allergic diseases, as well sepsis and respiratory viral infections, have shown that IL-38 exerts an anti-inflammatory activity by modulating the generation and function of inflammatory cytokines (e.g. IL-6, IL-8, IL-17 and IL-36) and regulating dendritic cells, M2 macrophages and regulatory T cells (Tregs). Accordingly, IL-38 may possess therapeutic potential for these types of diseases. IL-38 down-regulates CCR3+ eosinophil cells, CRTH2+ Th2 cells, Th17 cells, and innate lymphoid type 2 cells (ILC2), but up-regulates Tregs, and this has influenced the design of immunotherapeutic strategies based on regulatory cells/cytokines for allergic asthma in future studies. In auto-inflammatory diseases, IL-38 alleviates skin inflammation by regulating γδ T cells and limiting the production of IL-17. Due to its ability to suppress IL-1β, IL-6 and IL-36, this cytokine could reduce COVID-19 severity, and might be employed as a therapeutic tool. IL-38 may also influence host immunity and/or the components of the cancer microenvironment, and has been shown to improve the outcome of colorectal cancer, and may participate in tumour progression in lung cancer possibly by modulating CD8 tumour infiltrating T cells and PD-L1 expression. In this review, we first briefly present the biological and immunological functions of IL-38, and then discuss the important roles of IL-38 in various types of diseases, and finally highlight its use in therapeutic strategies.

[1]  G. Palmer,et al.  Multifaceted roles of IL-38 in inflammation and cancer. , 2022, Cytokine.

[2]  E. Fröhlich Acute Respiratory Distress Syndrome: Focus on Viral Origin and Role of Pulmonary Lymphatics , 2021, Biomedicines.

[3]  Zhongxin Lu,et al.  Interleukin-38 Suppresses Cell Migration and Proliferation and Promotes Apoptosis of Colorectal Cancer Cell Through Negatively Regulating Extracellular Signal-Regulated Kinases Signaling. , 2021, Journal of interferon & cytokine research : the official journal of the International Society for Interferon and Cytokine Research.

[4]  W. Jiskoot,et al.  The interleukin-1 cytokine family members: Role in cancer pathogenesis and potential therapeutic applications in cancer immunotherapy. , 2021, Cytokine & growth factor reviews.

[5]  R. Bellomo,et al.  Mast Cell Cytokines IL-1, IL-33, and IL-36 Mediate Skin Inflammation in Psoriasis: A Novel Therapeutic Approach with the Anti-Inflammatory Cytokines IL-37, IL-38, and IL-1Ra , 2021, International journal of molecular sciences.

[6]  Lei Zhao,et al.  The emerging role of Interleukin 37 in bone homeostasis and inflammatory bone diseases. , 2021, International immunopharmacology.

[7]  M. Iannacone,et al.  Immunobiology and pathogenesis of hepatitis B virus infection , 2021, Nature Reviews Immunology.

[8]  Xiaofang Wang,et al.  The Role of IL-36 in Infectious Diseases: Potential Target for COVID-19? , 2021, Frontiers in Immunology.

[9]  W. Xiao,et al.  IL-38 exerts anti-inflammatory and anti-fibrotic effects in thyroid-associated ophthalmopathy. , 2021, The Journal of clinical endocrinology and metabolism.

[10]  D. Wolf,et al.  Inflammatory Cell Recruitment in Cardiovascular Disease , 2021, Frontiers in Cell and Developmental Biology.

[11]  B. Brüne,et al.  IL-38 Ablation Reduces Local Inflammation and Disease Severity in Experimental Autoimmune Encephalomyelitis , 2021, The Journal of Immunology.

[12]  C. Lam,et al.  Interleukin-38 ameliorates poly(I:C) induced lung inflammation: therapeutic implications in respiratory viral infections , 2021, Cell death & disease.

[13]  W. Su,et al.  Elevated IL-38 inhibits IL-23R expression and IL-17A production in thyroid-associated ophthalmopathy. , 2020, International immunopharmacology.

[14]  J. Sabbatinelli,et al.  Plasma levels of interleukin-38 in healthy aging and in type 2 diabetes. , 2020, Diabetes research and clinical practice.

[15]  M. Khan Regulatory T cells mediated immunomodulation during asthma: a therapeutic standpoint , 2020, Journal of translational medicine.

[16]  J. Laffey,et al.  Role of the adaptive immune response in sepsis , 2020, Intensive Care Medicine Experimental.

[17]  S. Smeekens,et al.  Human recombinant interleukin-38 suppresses inflammation in mouse models of local and systemic disease. , 2020, Cytokine.

[18]  M. Nazarinia,et al.  Elevated IL-38 Serum Levels in Newly Diagnosed Multiple Sclerosis and Systemic Sclerosis Patients , 2020, Medical Principles and Practice.

[19]  Xiaoping Zhou,et al.  IL‐38: A novel cytokine in systemic lupus erythematosus pathogenesis , 2020, Journal of cellular and molecular medicine.

[20]  Hongtao Wang,et al.  Blockade of Th17 response by IL-38 in primary Sjögren's syndrome. , 2020, Molecular immunology.

[21]  M. Akiyama,et al.  IL-36 receptor antagonist deficiency resulted in delayed wound healing due to excessive recruitment of immune cells , 2020, Scientific Reports.

[22]  A. Yalcin,et al.  Future perspective: biologic agents in patients with severe COVID-19 , 2020, Immunopharmacology and immunotoxicology.

[23]  Yan Li,et al.  Interleukin‐38 inhibits adipogenesis and inflammatory cytokine production in 3T3‐L1 preadipocytes , 2020, Cell biology international.

[24]  K. Kosai,et al.  Interleukin-38 promotes tumor growth through regulation of CD8+ tumor-infiltrating lymphocytes in lung cancer tumor microenvironment , 2020, Cancer Immunology, Immunotherapy.

[25]  S. Leeman,et al.  IL-38 inhibits microglial inflammatory mediators and is decreased in amygdala of children with autism spectrum disorder , 2020, Proceedings of the National Academy of Sciences.

[26]  Zhiwei Xu,et al.  Interleukin-38 overexpression prevents bleomycin-induced mouse pulmonary fibrosis , 2020, Naunyn-Schmiedeberg's Archives of Pharmacology.

[27]  Yuan Tian,et al.  Interleukin‐36 receptor antagonist attenuates atherosclerosis development by inhibiting NLRP3 inflammasome , 2020, Journal of cellular physiology.

[28]  P. Conti,et al.  Advances in Mast Cell Activation by IL-1 and IL-33 in Sjögren’s Syndrome: Promising Inhibitory Effect of IL-37 , 2020, International journal of molecular sciences.

[29]  Hong Liu,et al.  High Expression of ACE2 on Keratinocytes Reveals Skin as a Potential Target for SARS-CoV-2 , 2020, Journal of Investigative Dermatology.

[30]  B. Lipworth,et al.  Elevated levels of IL-6 and CRP predict the need for mechanical ventilation in COVID-19 , 2020, Journal of Allergy and Clinical Immunology.

[31]  Lei Cheng,et al.  IL-38 alleviates the inflammatory response and the degeneration of nucleus pulposus cells via inhibition of the NF-κB signaling pathway in vitro. , 2020, International immunopharmacology.

[32]  W. Xiao,et al.  IL-38 restrains inflammatory response of collagen-induced arthritis in rats via SIRT1/HIF-1α signaling pathway , 2020, Bioscience reports.

[33]  Zhe Zhu,et al.  Clinical value of immune-inflammatory parameters to assess the severity of coronavirus disease 2019 , 2020, International Journal of Infectious Diseases.

[34]  Fang Liu,et al.  Prognostic value of interleukin-6, C-reactive protein, and procalcitonin in patients with COVID-19 , 2020, Journal of Clinical Virology.

[35]  Gianpaolo Ronconi,et al.  Induction of pro-inflammatory cytokines (IL-1 and IL-6) and lung inflammation by Coronavirus-19 (COVI-19 or SARS-CoV-2): anti-inflammatory strategies. , 2020 .

[36]  Tao Chen,et al.  Interleukin-38 increases the insulin sensitivity in children with the type 2 diabetes. , 2020, International immunopharmacology.

[37]  Jing Li,et al.  Interleukin-36 receptor antagonist alleviates airway inflammation in asthma via inhibiting the activation of Interleukin-36 pathway. , 2020, International immunopharmacology.

[38]  X. Hou,et al.  Interleukin-38 is elevated in inflammatory bowel diseases and suppresses intestinal inflammation. , 2020, Cytokine.

[39]  M. Jaeger,et al.  Reduced concentrations of the B cell cytokine interleukin 38 are associated with cardiovascular disease risk in overweight subjects , 2019, European journal of immunology.

[40]  Yun Ge,et al.  Interleukin‐38 protects against sepsis by augmenting immunosuppressive activity of CD4+CD25+ regulatory T cells , 2019, Journal of cellular and molecular medicine.

[41]  F. Zhang,et al.  Interleukin-38 in colorectal cancer: a potential role in precision medicine , 2019, Cancer Immunology, Immunotherapy.

[42]  R. Zhu,et al.  Interleukin‐38 alleviates cardiac remodelling after myocardial infarction , 2019, Journal of cellular and molecular medicine.

[43]  Chuanjiang Wang,et al.  IL-38 is a biomarker for acute respiratory distress syndrome in humans and down-regulates Th17 differentiation in vivo. , 2019, Clinical immunology.

[44]  E. Cheung,et al.  Anti-inflammatory mechanisms of the novel cytokine interleukin-38 in allergic asthma , 2019, Cellular & Molecular Immunology.

[45]  S. Zheng,et al.  IL-38: A New Player in Inflammatory Autoimmune Disorders , 2019, Biomolecules.

[46]  Yuxia Zhao,et al.  Molecular mechanisms of interleukin-38 inhibiting inflammatory bowel disease in children by regulating nuclear factor-κB and signal transduction and activator of transcription 3 pathway , 2019 .

[47]  B. Brüne,et al.  IL-38 Ameliorates Skin Inflammation and Limits IL-17 Production from γδ T Cells. , 2019, Cell reports.

[48]  S. Seyedian,et al.  A review of the diagnosis, prevention, and treatment methods of inflammatory bowel disease , 2019, Journal of medicine and life.

[49]  C. Pitzalis,et al.  IL-36, IL-37, and IL-38 Cytokines in Skin and Joint Inflammation: A Comprehensive Review of Their Therapeutic Potential , 2019, International journal of molecular sciences.

[50]  Yong-ming Yao,et al.  Recent advances in the biology of IL-1 family cytokines and their potential roles in development of sepsis. , 2019, Cytokine & growth factor reviews.

[51]  T. Kinoshita,et al.  Attenuated Airway Eosinophilic Inflammations in IL-38 Knockout Mouse Model. , 2018, The Kurume medical journal.

[52]  Yan Li,et al.  Hydrodynamic delivery of IL-38 gene alleviates obesity-induced inflammation and insulin resistance. , 2019, Biochemical and biophysical research communications.

[53]  J. Yamamoto-Furusho,et al.  Differential Expression of IL-36 Family Members and IL-38 by Immune and Nonimmune Cells in Patients with Active Inflammatory Bowel Disease , 2018, BioMed research international.

[54]  E. Eisenmesser,et al.  IL-38 has an anti-inflammatory action in psoriasis and its expression correlates with disease severity and therapeutic response to anti-IL-17A treatment , 2018, Cell Death & Disease.

[55]  L. Su,et al.  Plasma interleukin‐38 in patients with rheumatoid arthritis , 2018, International immunopharmacology.

[56]  Jingyu Yang,et al.  Elevated Interleukin-38 Level Associates with Clinical Response to Atorvastatin in Patients with Hyperlipidemia , 2018, Cellular Physiology and Biochemistry.

[57]  Yibing Yin,et al.  Interleukin 38 Protects Against Lethal Sepsis , 2018, The Journal of infectious diseases.

[58]  G. Palmer,et al.  The severity of imiquimod-induced mouse skin inflammation is independent of endogenous IL-38 expression , 2018, PloS one.

[59]  B. Le Goff,et al.  The enigmatic role of IL-38 in inflammatory diseases. , 2018, Cytokine & growth factor reviews.

[60]  Giou-Teng Yiang,et al.  New Insights into the Immune Molecular Regulation of the Pathogenesis of Acute Respiratory Distress Syndrome , 2018, International journal of molecular sciences.

[61]  C. Gabay,et al.  Regulation and function of interleukin‐36 cytokines , 2018, Immunological reviews.

[62]  L. Joosten,et al.  Biology of IL‐38 and its role in disease , 2018, Immunological reviews.

[63]  C. Dinarello Overview of the IL‐1 family in innate inflammation and acquired immunity , 2018, Immunological reviews.

[64]  Liwei Lu,et al.  IL-36 cytokines in autoimmunity and inflammatory disease , 2017, Oncotarget.

[65]  Jianbing Ma,et al.  Dendritic cells should not be overlooked when studying the effect of IL-38 administration in arthritis , 2017, Annals of the rheumatic diseases.

[66]  Roberto Giacomelli,et al.  Cytokines in the pathogenesis of rheumatoid arthritis: new players and therapeutic targets , 2017, BMC Rheumatology.

[67]  Y. Maehara,et al.  Clinical implications of the novel cytokine IL-38 expressed in lung adenocarcinoma: Possible association with PD-L1 expression , 2017, PloS one.

[68]  Hong-yan Zhou,et al.  The Effect of Interleukin 38 on Angiogenesis in a Model of Oxygen-induced Retinopathy , 2017, Scientific Reports.

[69]  B. Le Goff,et al.  IL-38 overexpression induces anti-inflammatory effects in mice arthritis models and in human macrophages in vitro , 2017, Annals of the rheumatic diseases.

[70]  Jie Dong,et al.  In vivo anti-inflammatory activities of novel cytokine IL-38 in Murphy Roths Large (MRL)/lpr mice. , 2017, Immunobiology.

[71]  S. Razavi,et al.  Multiple Sclerosis: Pathogenesis, Symptoms, Diagnoses and Cell-Based Therapy , 2016, Cell journal.

[72]  Xiuhe Pan,et al.  IL-38 alleviates concanavalin A-induced liver injury in mice. , 2016, International immunopharmacology.

[73]  Norbert Meyer,et al.  Interleukins (from IL-1 to IL-38), interferons, transforming growth factor β, and TNF-α: Receptors, functions, and roles in diseases. , 2016, The Journal of allergy and clinical immunology.

[74]  Renhua Sun,et al.  Resolution acute respiratory distress syndrome through reversing the imbalance of Treg/Th17 by targeting the cAMP signaling pathway. , 2016, Molecular medicine reports.

[75]  G. Wong,et al.  Aberrant Expression of Novel Cytokine IL-38 and Regulatory T Lymphocytes in Childhood Asthma , 2016, Molecules.

[76]  M. Li,et al.  Production of recombinant human interleukin-38 and its inhibitory effect on the expression of proinflammatory cytokines in THP-1 cells , 2016, Molecular Biology.

[77]  J. Ybe,et al.  Structural and Functional Attributes of the Interleukin-36 Receptor* , 2016, The Journal of Biological Chemistry.

[78]  Yan-fang Jiang,et al.  Elevated serum interleukin-38 level at baseline predicts virological response in telbivudine-treated patients with chronic hepatitis B. , 2016, World journal of gastroenterology.

[79]  X. Sun,et al.  Detection of the novel IL-1 family cytokines by QAH-IL1F-1 assay in rheumatoid arthritis. , 2016, Cellular and molecular biology.

[80]  Andrea Schlemmer,et al.  Interleukin-38 is released from apoptotic cells to limit inflammatory macrophage responses. , 2016, Journal of molecular cell biology.

[81]  R. Laubenbacher,et al.  Costimulation Endows Immunotherapeutic CD8 T Cells with IL-36 Responsiveness during Aerobic Glycolysis , 2016, The Journal of Immunology.

[82]  Jiaqi Liu,et al.  Inflammation and Inflammatory Cells in Myocardial Infarction and Reperfusion Injury: A Double-Edged Sword , 2016, Clinical Medicine Insights. Cardiology.

[83]  B. Le Goff,et al.  Distinct expression of interleukin (IL)‐36α, β and γ, their antagonist IL‐36Ra and IL‐38 in psoriasis, rheumatoid arthritis and Crohn's disease , 2015, Clinical and experimental immunology.

[84]  Kunwu Yu,et al.  Elevated Plasma IL-38 Concentrations in Patients with Acute ST-Segment Elevation Myocardial Infarction and Their Dynamics after Reperfusion Treatment , 2015, Mediators of inflammation.

[85]  E. Morand,et al.  Brief Report: Interleukin‐38 Exerts Antiinflammatory Functions and Is Associated With Disease Activity in Systemic Lupus Erythematosus , 2015, Arthritis & rheumatology.

[86]  T. Kinoshita,et al.  IL-38: A new factor in rheumatoid arthritis , 2015, Biochemistry and biophysics reports.

[87]  S. Tokuyama,et al.  Borrelidin Isolated from Streptomyces sp. Inhibited Adipocyte Differentiation in 3T3-L1 Cells via Several Factors Including GATA-Binding Protein 3. , 2015, Biological & pharmaceutical bulletin.

[88]  A. Dart,et al.  Systemic inflammatory response following acute myocardial infarction , 2015, Journal of geriatric cardiology : JGC.

[89]  C. Gabay,et al.  Regulation and function of interleukin‐36 cytokines in homeostasis and pathological conditions , 2015, Journal of leukocyte biology.

[90]  Yong Li,et al.  The ratio of Th17/Treg cells as a risk indicator in early acute respiratory distress syndrome , 2015, Critical Care.

[91]  C. Dinarello Overview of the interleukin-1 family of ligands and receptors. , 2013, Seminars in immunology.

[92]  M. Mishina,et al.  IL1RAPL1 Associated with Mental Retardation and Autism Regulates the Formation and Stabilization of Glutamatergic Synapses of Cortical Neurons through RhoA Signaling Pathway , 2013, PloS one.

[93]  R. Nelson,et al.  Hyperlipidemia as a risk factor for cardiovascular disease. , 2013, Primary care.

[94]  F. Sallusto,et al.  IL-36 signaling amplifies Th1 responses by enhancing proliferation and Th1 polarization of naive CD4+ T cells. , 2012, Blood.

[95]  H. Mühl,et al.  IL-36γ/IL-1F9, an Innate T-bet Target in Myeloid Cells* , 2012, The Journal of Biological Chemistry.

[96]  C. Garlanda,et al.  TIR8/SIGIRR is an Interleukin-1 Receptor/Toll Like Receptor Family Member with Regulatory Functions in Inflammation and Immunity , 2012, Front. Immun..

[97]  Yong-ming Yao,et al.  The role of regulatory T cells in the pathogenesis of sepsis and its clinical implication. , 2012, Journal of interferon & cytokine research : the official journal of the International Society for Interferon and Cytokine Research.

[98]  P. Barrow,et al.  Expression of IL‐1Rrp2 by human myelomonocytic cells is unique to DCs and facilitates DC maturation by IL‐1F8 and IL‐1F9 , 2012, European journal of immunology.

[99]  L. Joosten,et al.  IL-38 binds to the IL-36 receptor and has biological effects on immune cells similar to IL-36 receptor antagonist , 2012, Proceedings of the National Academy of Sciences.

[100]  K. Roeder,et al.  Copy Number Variants for Schizophrenia and Related Psychotic Disorders in Oceanic Palau: Risk and Transmission in Extended Pedigrees , 2011, Biological Psychiatry.

[101]  H. Dinh,et al.  CS16-5. IL-36R Ligands are Potent Regulators of Dendritic and T Cells , 2011 .

[102]  R. Tiwari,et al.  IL-1R–Associated Kinase-1 Mediates Protein Kinase Cδ-Induced IL-1β Production in Monocytes , 2011, The Journal of Immunology.

[103]  M. Iruela-Arispe,et al.  Extracellular matrix, inflammation, and the angiogenic response. , 2010, Cardiovascular research.

[104]  R. Khalil,et al.  Inflammatory cytokines in vascular dysfunction and vascular disease. , 2009, Biochemical pharmacology.

[105]  E. Fombonne,et al.  Mutations in the calcium-related gene IL1RAPL1 are associated with autism. , 2008, Human molecular genetics.

[106]  Hui He,et al.  A study on the correlation between IL1RAPL1 and human cognitive ability , 2008, Neuroscience Letters.

[107]  A. Grainger Difficulties in tracking the long-term global trend in tropical forest area , 2008, Proceedings of the National Academy of Sciences.

[108]  Y. Humeau,et al.  IL1-receptor accessory protein-like 1 (IL1RAPL1), a protein involved in cognitive functions, regulates N-type Ca2+-channel and neurite elongation , 2007, Proceedings of the National Academy of Sciences.

[109]  N. Nishimoto Interleukin-6 in rheumatoid arthritis , 2006, Current opinion in rheumatology.

[110]  J. Khan,et al.  Crystal Structure of the Toll/Interleukin-1 Receptor Domain of Human IL-1RAPL* , 2004, Journal of Biological Chemistry.

[111]  C. Stansberg,et al.  The interleukin 1 receptor family. , 2004, Developmental and comparative immunology.

[112]  J. Sims,et al.  Interleukin (IL)-1F6, IL-1F8, and IL-1F9 Signal through IL-1Rrp2 and IL-1RAcP to Activate the Pathway Leading to NF-κB and MAPKs* , 2004, Journal of Biological Chemistry.

[113]  J. Chelly,et al.  IL1 receptor accessory protein like, a protein involved in X-linked mental retardation, interacts with Neuronal Calcium Sensor-1 and regulates exocytosis. , 2003, Human molecular genetics.

[114]  A. Dunne,et al.  The Interleukin-1 Receptor/Toll-Like Receptor Superfamily: Signal Transduction During Inflammation and Host Defense , 2000, Science's STKE.

[115]  P. Dawson,et al.  Identification of a novel human cytokine gene in the interleukin gene cluster on chromosome 2q12-14. , 2001, Journal of interferon & cytokine research : the official journal of the International Society for Interferon and Cytokine Research.

[116]  J. E. Ford,et al.  Cloning and Characterization of IL-1HY2, a Novel Interleukin-1 Family Member* , 2001, The Journal of Biological Chemistry.

[117]  R. Kastelein,et al.  Computational identification, cloning, and characterization of IL-1R9, a novel interleukin-1 receptor-like gene encoded over an unusually large interval of human chromosome Xq22.2-q22.3. , 2000, Genomics.

[118]  M. Rischmueller,et al.  Inhibitory effects of muscarinic receptor autoantibodies on parasympathetic neurotransmission in Sjögren's syndrome. , 2000, Arthritis and rheumatism.

[119]  F. Muntoni,et al.  Two novel members of the interleukin-1 receptor gene family, one deleted in Xp22.1–Xp21.3 mental retardation , 2000, European Journal of Human Genetics.

[120]  T. Born,et al.  Identification and characterization of two members of a novel class of the interleukin-1 receptor (IL-1R) family. Delineation of a new class of IL-1R-related proteins based on signaling. , 2000, The Journal of biological chemistry.

[121]  Lin Jun,et al.  A new member of the IL-1 receptor family highly expressed in hippocampus and involved in X-linked mental retardation , 1999, Nature Genetics.

[122]  J. Sims,et al.  Identification and characterization of SIGIRR, a molecule representing a novel subtype of the IL-1R superfamily. , 1999, Cytokine.

[123]  C. Janeway,et al.  MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. , 1998, Molecular cell.

[124]  I. M. Neiman,et al.  [Inflammation and cancer]. , 1974, Patologicheskaia fiziologiia i eksperimental'naia terapiia.