The Role of Immunometabolism in Autoimmune Mediated and Autoinflammatory Disorders

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Background

Immune cell responses are tightly regulated by environmental factors, including cytokines, hormones, and microbial products, as well as nutrient availability. These events activate metabolic pathways in immune cells, such as glycolysis or fatty acid synthesis to build an efficient immune response, switching to oxidative phosphorylation or fatty acid oxidation metabolism, for instance, to acquire a pro-resolving and regulatory phenotype during the resolution phase.

However, under certain circumstances, immune cells fail to switch from inflammatory to anti-inflammatory states, and inflammatory responses persist over time, leading to breach of immune tolerance and autoimmunity. Recent evidence suggests that aberrant metabolic responses of immune cells are responsible to trigger or maintain autoimmunity and inflammation in certain diseases. Metabolic pathway abnormalities play, in fact, a major role in the pathogenesis of autoimmune disorders such as rheumatoid arthritis (RA), systemic lupus erythematosus (SLE), multiple sclerosis (MS), inflammatory bowel disease (IBD), and type 1 diabetes (T1D), as well as autoinflammatory diseases where a link between metabolism and inflammasome activation has been established. For example, altered glycolysis and mitochondrial metabolism in T cells have been shown to drive autoimmunity in RA, SLE and MS. Metabolic dysregulation in T/B cells, neutrophils and macrophages has been proposed as potential mechanism for the pathogenesis of vasculitis. Dysregulated metabolic reprogramming in macrophages leads to inflammasome-mediated IL1-beta production in autoinflammatory disorders. In addition, targeting glycolytic enzymes in fibroblasts has revealed encouraging results to reduce inflammation in RA.

Several studies have elucidated the physiological and pathogenic roles of metabolism in regulating the functions of immune cells including activation, differentiation, proliferation, as well as in the cellular cross talk between immune and stromal cells. It is now clear that metabolic intermediates like lactate, lipids, succinate etc. function as signalling molecules capable of linking metabolic reprogramming with autoimmune and inflammatory responses. Specifically, studies suggest that lactate, succinate and choline play an important role in the pathogenesis of autoimmune disorders, such as RA, by modulating T cell, macrophage and fibroblast responses.

Beyond the importance of studying metabolic reprogramming to understand the biology of inflammatory and autoimmune diseases, it also has clinical implications. The ability to image metabolism has allowed the identification of metabolic changes in inflamed tissues (i.e. glucose uptake via 18fluoro-2-deoxyglucose positron emission tomography). In addition, metabolomic studies have shown promising results for predicting specific pathogenic pathways altered in autoimmune diseases such as RA, T1D, MS and IBD.

This Research Topic will address the most recent updates on the role of cellular immunometabolism in the regulation of immune responses and will shed light on how dysregulation of these pathways can be responsible for immune impairment and development of autoimmunity. Targeting cell metabolism can provide potential novel therapeutic targets for autoinflammatory and autoimmune diseases. We welcome manuscripts focusing on, but not limited to, the following areas:

• The role of metabolic dysregulation in immune cells in human and/or mouse models of autoimmune disease
• Novel strategies targeting cell metabolism in autoimmune/autoinflammatory diseases
• How the tissue microenvironment (metabolites, nutrients, hormones regulating metabolism) modulates the metabolism of immune cells in autoimmunity
• Signalling pathways regulating cell metabolism in autoimmunity/autoinflammation
• Microbiota derived metabolites in autoimmunity
• The role of adipocytokines and obesity related mediators in the regulation of immune cell functions in autoimmunity
• Metabolomic studies in autoimmunity
• Metabolism and inflammasome activation in autoinflammatory and autoimmune diseases
• Imaging and metabolism in autoimmunity

Dr. Guma receives funding from Novartis and Pfizer in relation to metabolomics in autoimmune disease. Dr. Pucino declares no potential competing interests with regards to the topic theme.

Keywords: immunometabolism, autoimmunity, inflammation, metabolic intermediates, metabolic targets

Important note: All contributions to this Research Topic must be within the scope of the section and journal to which they are submitted, as defined in their mission statements. Frontiers reserves the right to guide an out-of-scope manuscript to a more suitable section or journal at any stage of peer review.

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