IL-27 induces an IFN-like signature in murine macrophages which in turn modulate colonic epithelium

Mucosal delivery of IL-27 has been shown to have a therapeutic benefit in murine models of inflammatory bowel disease (IBD). The IL-27 effect was associated with phosphorylated STAT1 (pSTAT1), a product of IL27 receptor signaling, in bowel tissue. To determine whether IL-27 acted directly on colonic epithelium, murine colonoids and primary intact colonic crypts were shown to be unresponsive to IL-27 in vitro and to lack detectable IL-27 receptors. On the other hand, macrophages, which are present in inflamed colon tissue, were responsive to IL-27 in vitro. IL-27 induced pSTAT1 in macrophages, the transcriptome indicated an IFN-like signature, and supernatants induced pSTAT1 in colonoids. IL-27 induced anti-viral activity in macrophages and MHC Class II induction. We conclude that the effects of mucosal delivery of IL-27 in murine IBD are in part based on the known effects of IL27 inducing immunosuppression of T cells mediated by IL-10. We also conclude that IL-27 has potent effects on macrophages in inflamed colon tissue, generating mediators that in turn act on colonic epithelium.

[1]  H. Ochs,et al.  The clinical, molecular, and therapeutic features of patients with IL10/IL10R deficiency: a systematic review. , 2022, Clinical and experimental immunology.

[2]  S. Durum,et al.  Interleukin-27 Regulates the Function of the Gastrointestinal Epithelial Barrier in a Human Tissue-Derived Organoid Model , 2022, Biology.

[3]  Liling Xiong,et al.  The dual role of IL-27 in CD4+T cells. , 2021, Molecular immunology.

[4]  S. Urcuqui-Inchima,et al.  Interleukin 27 as an inducer of antiviral response against chikungunya virus infection in human macrophages. , 2021, Cellular immunology.

[5]  S. Mehandru,et al.  The intestinal barrier, an arbitrator turned provocateur in IBD , 2020, Nature Reviews Gastroenterology & Hepatology.

[6]  S. Itzkovitz,et al.  Diet Diurnally Regulates Small Intestinal Microbiome-Epithelial-Immune Homeostasis and Enteritis , 2020, Cell.

[7]  Xiaojun Tang,et al.  IL-27 Regulated CD4+IL-10+ T Cells in Experimental Sjögren Syndrome , 2020, Frontiers in Immunology.

[8]  C. Petes,et al.  IL-27 amplifies cytokine responses to Gram-negative bacterial products and Salmonella typhimurium infection , 2018, Scientific Reports.

[9]  S. Durum,et al.  Cytokine Tuning of Intestinal Epithelial Function , 2018, Front. Immunol..

[10]  M. Anver,et al.  Interleukin-27 Is a Potential Rescue Therapy for Acute Severe Colitis Through Interleukin-10–Dependent, T-Cell–Independent Attenuation of Colonic Mucosal Innate Immune Responses , 2017, Inflammatory bowel diseases.

[11]  S. Ferrini,et al.  Dual Roles of IL-27 in Cancer Biology and Immunotherapy , 2017, Mediators of inflammation.

[12]  C. Hunter,et al.  The immunobiology of interleukin-27. , 2015, Annual review of immunology.

[13]  J. Zhong,et al.  Association of IL-27 gene three polymorphisms with Crohn's disease susceptibility in a Chinese Han population. , 2014, International journal of clinical and experimental pathology.

[14]  K. Gee,et al.  Interleukin-27 induces a STAT1/3- and NF-κB-dependent proinflammatory cytokine profile in human monocytes. , 2012, The Journal of Biological Chemistry.

[15]  E. Mohammadi,et al.  Barriers and facilitators related to the implementation of a physiological track and trigger system: A systematic review of the qualitative evidence , 2017, International journal for quality in health care : journal of the International Society for Quality in Health Care.

[16]  S. Brand,et al.  A Novel Role for Interleukin-27 (IL-27) as Mediator of Intestinal Epithelial Barrier Protection Mediated via Differential Signal Transducer and Activator of Transcription (STAT) Protein Signaling and Induction of Antibacterial and Anti-inflammatory Proteins* , 2011, The Journal of Biological Chemistry.

[17]  L. Ivashkiv,et al.  Suppression of TNF-α and IL-1 Signaling Identifies a Mechanism of Homeostatic Regulation of Macrophages by IL-27 , 2010, The Journal of Immunology.

[18]  K. Gee,et al.  Interleukin-27 Induces a STAT1/3- and NF-κB-dependent Proinflammatory Cytokine Profile in Human Monocytes* , 2010, The Journal of Biological Chemistry.

[19]  Johan Van Limbergen,et al.  Common variants at five new loci associated with early-onset inflammatory bowel disease , 2009, Nature Genetics.

[20]  K. Hahm,et al.  Interleukin‐27 polymorphisms are associated with inflammatory bowel diseases in a Korean population , 2009, Journal of gastroenterology and hepatology.

[21]  Xia Zhang,et al.  The Isolation and Characterization of Murine Macrophages , 2008, Current protocols in immunology.

[22]  George D. Kalliolias,et al.  IL-27 Activates Human Monocytes via STAT1 and Suppresses IL-10 Production but the Inflammatory Functions of IL-27 Are Abrogated by TLRs and p381 , 2008, The Journal of Immunology.

[23]  M. Anver,et al.  Oral delivery of IL-27 recombinant bacteria attenuates immune colitis in mice. , 2014, Gastroenterology.

[24]  Hans Clevers,et al.  Primary mouse small intestinal epithelial cell cultures. , 2013, Methods in molecular biology.