Evolutionary conserved pathway of the innate immune response after a viral insult in Paracentrotus lividus sea urchin

Abstract

Despite the apparent simplicity of the body organization of echinoderms, their immune system is competent to perform a complex innate immune response, which is far from being well understood. The echinoderms represent the most advanced invertebrates that form a bridge with the primitive chordates. In fact, they possess numerous receptors and effectors that are used to obtain a fast immune response. After an infection, the humoral and cellular immune response determines a network in which the main protagonists are membrane and endosomal receptors. The recognition of nonself molecules by specific membrane receptors triggers the immune response, stimulating consecutive intracellular events. We have previously shown how the polyinosinic–polycytidylic acid (polyI:C) that mimics a viral infection is able to induce an immune response in the sea urchin Paracentrotus lividus immune cells. It activates a specific membrane receptor belonging to the Toll‐like receptor (TLR) family. Here, we show the activated expression pattern of some genes involved in the downstream cascade of TLR signalling pathway, such as Pl‐Tbk and Pl‐Irf, whose partial sequence was isolated from P. lividus immune cells. Their mRNA expression increases consequentially to the polyI:C stimulation and in a temporal way. In addition, we analysed the expression of Pl‐NF‐kB and we found that its upregulation was time‐dependent, preceding Pl‐Tbk and Pl‐Irf increase. Protein analysis showed that also some cytokine (TNF‐α and IL‐1α) expression increased after polyI:C insult. Therefore, the purpose of this study was to discover the molecular mechanisms of the innate defence strategies, similarly to vertebrates, implemented by the sea urchins in order to cope with viral infection challenge.

Induced Immune Reaction in the Acorn Worm, Saccoglossus kowalevskii, Informs the Evolution of Antiviral Immunity

“…Both vertebrate NF-κB and IRF signaling act in compensatory regulatory feedback loops which reduce their own expression over time to avoid harmful overstimulation ( Blach-Olszewska and Leszek 2007 ; Dorrington and Fraser 2019 ; Andresen et al 2020 ). Furthermore, targeted expression studies have shown that NF-κB and IRF transcription follows a similar trend in urchin larvae following poly(I:C) exposure ( Pancer et al 1999 ; Chiaramonte et al 2019 ). In light of this evidence, the reduced expression of genes associated with these pathways at 4 hpi suggests NF-κB and IRF activation occurred at an earlier unsampled time point in our experiment.…”

“…Importantly, urchin larval immunity remains one of the most well-characterized immunological systems among invertebrates ( Buckley and Rast 2019 ). With the recent development of experimentally tractable hemichordate larvae in the acorn worm Schizocardium californicum ( Gonzalez et al 2018 ; Bump et al 2022 ), direct comparisons of immune responses between homologous developmental time points will be invaluable for testing hypotheses on the ancestry of immune cell recruitment, inflammatory response, and NF-κB/IRF signaling ( Ho et al 2016 ; Chiaramonte et al 2019 ).…”

De Novo Assembly of the Genome of the Sea Urchin Paracentrotus lividus (Lamarck 1816)

“…The vast majority of sea urchin TLR genes are more similar to each other than to those of other animals, suggesting a gene expansion specific to the sea urchin lineage [28]. The recognition of non-self molecules by specific membrane receptors triggers the immune response, stimulating consecutive intracellular events [30]. An E3 ubiquitin-protein ligase pellino homolog 1 gene was identified, as it has been for S. purpuratus (LOC577851).…”

“…The genome of this sea urchin holds a vast set of at least 222 TLR genes, accompanied by a moderate expansion of downstream adaptors, different from that of chordates [28][29][30]. The abundance of TLRs in sea urchins suggests that this class of receptors plays an important role in the innate immune defence, possibly the case in lower animals as well.…”

Changes in the proteome of sea urchin Paracentrotus lividus coelomocytes in response to LPS injection into the body cavity

“…The coelomocytes, cells that circulate in the coelomic fluid, mediate immune responses through phagocytosis and encapsulation of non-self particles in addition to the production of antimicrobial molecules. These non-self molecules are known as pathogen-associated molecular patterns (PAMPs), and their receptors are called pattern-recognition receptors (PRRs) [6,7]. The PRRs, localised on immune cells and in body fluid as soluble factors, possess a higher numerical variance than those of vertebrate organisms [8][9][10].…”