The Immunomodulatory Roles of Adipocytes

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Background

Obesity is increasing in epidemic proportions worldwide. A low-grade inflammation caused by obesity leads to its many inflammation-associated complications, including insulin resistance, type 2 diabetes, accelerated atherosclerosis, nonalcoholic steatohepatitis that can lead to liver cirrhosis, heart failure, cancer, and Alzheimer’s disease. This systemic inflammation is due to profound changes in the adipose tissue microenvironment, at the heart of which is the adipocyte.

Increasing evidence suggests the adipocyte not only stores excess energy, but initiates an escalating pro-inflammatory cascade in adipose tissue during high-fat diet. The adipocyte secretes over 50 cytokines and hormones that both enhance and suppress inflammation, secretes extracellular matrix proteins that impact inflammation, produces and releases toxic lipids that aggravate inflammation, and, more recently, was shown to present antigen to activate CD4+ T cells. Although discovered several decades ago, studies continue to identify pro-inflammatory roles for leptin and anti-inflammatory activities for adiponectin, hormones secreted in large amounts by the adipocyte.

Additionally, extracellular matrix (ECM) proteins secreted by adipocytes not only determine the architecture of the adipose tissue but also have the capacity to promote inflammation and regulate systemic metabolism. Increased ECM production in obesity, results in adipose tissue fibrosis that leads to multiple metabolic derangements. Among ECM proteins, Clusterin (apolipoprotein J), is secreted in increased amounts by the adipocyte in obesity, correlates with all components of the metabolic syndrome, and inhibits hepatic insulin action and expression of apolipoprotein A, a precursor of the high-density lipoprotein cholesterol particle. Moreover, ceramide, a known toxic lipid released by the adipocyte, was recently found to be exported out of the adipocyte through exosomes to promote inflammation in macrophages. New evidence showed that inhibition of ceramide biosynthesis improved insulin resistance.

Adipocytes have also been shown to increase their capacity to present antigens and activate CD4+ Th1 cells leading to increase insulin resistance in obesity. Knockdown of this capacity attenuates defective insulin action in obesity. Finally, recently described “batokines” secreted by brown adipocytes were found to regulate inflammation and systemic metabolism. Thus, in obesity, the adipocyte exerts immunomodulatory functions, using multiple novel mechanisms to regulate inflammation. Understanding this function and how it impacts other adipose tissue immune cells and obesity-related complications is critical in preventing and treating these complications.

The goal of this Research Topic is to define the immune functions of the adipocyte focusing on novel mechanisms by which the adipocyte promotes inflammation and damages target organs. A greater appreciation that the adipocyte assumes the role of an immune cell in obesity is critical to fighting this epidemic. We welcome authors to submit Review and Original Research articles focusing on, but not limited to, the following subtopics:

1. Factors secreted by adipocytes that enhance or suppress inflammation
2. Antigen presentation by adipocytes and CD4 T cell activation
3. Exosomes, a new mode of adipocyte communication
4. Batokines as novel factors regulating inflammation
5. Targeting adipocytes to treat chronic inflammation

Topic Editor Prof. Aimin Xu receives financial support from Servier Laboratories. The other Topic Editors declare no competing interests with regards to the Research Topic theme.

Keywords: Adipocyte, innate & adaptive immune response, Exosomes, Adipokine cytokines, metabolic disease

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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