Abstract
IL17 cytokines are central mediators of mammalian immunity. In vertebrates, these factors derive from diverse cellular sources. Sea urchins share a molecular heritage with chordates that includes the IL17 system. Here, we characterize the role of epithelial expression of IL17 in the larval gut-associated immune response. The purple sea urchin genome encodes 10 IL17 subfamilies (35 genes) and 2 IL17 receptors. Most of these subfamilies are conserved throughout echinoderms. Two IL17 subfamilies are sequentially strongly upregulated and attenuated in the gut epithelium in response to bacterial disturbance. IL17R1 signal perturbation results in reduced expression of several response genes including an IL17 subtype, indicating a potential feedback. A third IL17 subfamily is activated in adult immune cells indicating that expression in immune cells and epithelia is divided among families. The larva provides a tractable model to investigate the regulation and consequences of gut epithelial IL17 expression across the organism.
Highlights
Gut epithelial cells deploy an elaborate suite of signals to transmit information about the state of the gut lumen to the wider organism
Buckley et al identified three types of IL-17 proteins involved in sea urchin immunity: two that are important for the immune response in the gut during the larval stage, and a third that is only present in adults. These findings suggest that IL-17 signaling is an ancient and central element of gut-associated immune response, which even exists in animals that evolved long before humans
Seawater exposure to the marine bacterium V. diazotrophicus (V.d.) induces a distinct cellular response in sea urchin larvae that includes the migration of pigment cells to the gut epithelium, changes in cell behavior and altered gut morphology (Figure 1a,b) (Ch Ho et al, 2016)
Summary
Gut epithelial cells deploy an elaborate suite of signals to transmit information about the state of the gut lumen to the wider organism. As central mediators of the immune response, cytokines are key targets for pathogen mimicry or co-option (Elde and Malik, 2009; Epperson et al, 2012) and are subject to high levels of evolutionary pressure and sequence diversification (Koyanagi et al, 2010). An exception to this trend is the IL17 cytokine family. These proteins are characterized by a cysteine-knot fold structure that is formed through interactions among four conserved cysteine residues (Hymowitz et al, 2001) This structural constraint provides a means to computationally identify IL17 homologs across phyla. IL17 cytokines have been functionally characterized in jawed (Kolls and Linden, 2004) and jawless vertebrates (Smith et al, 2013; Han et al, 2015), and orthologs have been identified in invertebrate deuterostomes
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