Abstract

Simple SummaryThe purple sea urchin (Strongylocentrotus purpuratus) is a marine invertebrate that populates the east side of the Pacific Ocean from Mexico to Alaska, inhabiting intertidal and near-shore subtidal waters. Due to their ancient relationship with vertebrates, sea urchins are an important research model for developmental biology, cell biology, and immunology, as well as for understanding regenerative responses and ageing. This study assessed a specific protein modification called deimination/citrullination, which can alter protein function, allowing proteins to take on multiple and variable roles in different processes related to health and disease. This study also identified how extracellular vesicles, which are lipid blebs released from cells that participate in key processes for cell communication in health and disease, can carry proteins, including such modified protein cargo. This study may furthermore provide a platform for novel biomarker development to assess sea urchin health, which could be further applied, including for the monitoring of environmental changes.The purple sea urchin (Strongylocentrotus purpuratus) is a marine invertebrate of the class Echinoidea that serves as an important research model for developmental biology, cell biology, and immunology, as well as for understanding regenerative responses and ageing. Peptidylarginine deiminases (PADs) are calcium-dependent enzymes that mediate post-translational protein deimination/citrullination. These alterations affect protein function and may also play roles in protein moonlighting. Extracellular vesicles (EVs) are membrane-bound vesicles that are released from cells as a means of cellular communication. Their cargo includes a range of protein and RNA molecules. EVs can be isolated from many body fluids and are therefore used as biomarkers in physiological and pathological responses. This study assessed EVs present in the coelomic fluid of the purple sea urchin (Strongylocentrotus purpuratus), and identified both total protein cargo as well as the deiminated protein cargo. Deiminated proteins in coelomic fluid EVs were compared with the total deiminated proteins identified in coelomic fluid to assess putative differences in deiminated protein targets. Functional protein network analysis for deiminated proteins revealed pathways for immune, metabolic, and gene regulatory functions within both total coelomic fluid and EVs. Key KEGG and GO pathways for total EV protein cargo furthermore showed some overlap with deimination-enriched pathways. The findings presented in this study add to current understanding of how post-translational deimination may shape immunity across the phylogeny tree, including possibly via PAD activity from microbiota symbionts. Furthermore, this study provides a platform for research on EVs as biomarkers in sea urchin models.

Highlights

  • The purple sea urchin (Strongylocentrotus purpuratus) is a marine invertebrate within the phylum Echinodermata

  • The purple sea urchin immune system consists of two defence mechanisms that mirror those in vertebrates: a physical/chemical barrier; and a second barrier made of humoral factors, which triggers a humoral response and a consequent activation of phagocytic cells, antimicrobial factors, and inflammatory responses [6]

  • extracellular vesicles (EVs) were further assessed by transmission electron microscopy (TEM; Figure 1B) and Western blotting showed positive bands for the EV-specific markers CD63 and Flot-1 (Figure 1C), meeting the minimum criteria for the characterisation of EVs as per specifications by the International Society for Extracellular Vesicles [57]

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Summary

Introduction

The purple sea urchin (Strongylocentrotus purpuratus) is a marine invertebrate within the phylum Echinodermata. Echinoderms species show considerable regenerative abilities and significant variation in longevity (life spans range from 5–over 100 years, depending on species) Both longand short-lived sea urchins display negligible markers of cellular senescence and do not fit within the classic understanding of biological ageing [3]. Sea urchins have an ancient complement activation system that resembles the vertebrate complement systems [4,7,8,9], a significantly expanded array of pattern recognition receptors encoded in the genome, and a unique set of immune effector proteins [4,9,10,11]. Roles for phosphorylation, glycosylation, and various other post-translational modifications have been reported [13,14,15,16], but hitherto no studies have assessed putative roles for post-translational deimination, which in chordates is caused by peptidylarginine deiminases (PADs) and/or by PAD homologues (arginine deiminases, ADI) in bacteria, protists, and fungi

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