The Evolution and Diversity of Interleukin-17 Highlight an Expansion in Marine Invertebrates and Its Conserved Role in Mucosal Immunity

Saco, Amaro; Rey-Campos, Magalí; Rosani, Umberto; Novoa, Beatriz; Figueras, António

doi:10.3389/fimmu.2021.692997

Cited by 23 publications

(21 citation statements)

References 77 publications

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“…The inflammatory IL-17 cytokines are encoded by a diverse gene family leading to expanded IL-17 repertoires in various marine invertebrates. This can be seen, for example, in the study of 16 mussel genomes, which revealed 379 unique IL-17 sequences and 96 unique IL-17 receptor variants (35). Phylogenetic analysis revealed that all detected invertebrate IL-17 genes, from both annelids and mollusks, are clustered into one group, suggesting a common ancestral gene of these invertebrate IL-17s (31) (Table 2).…”

Section: Cytokinesmentioning

confidence: 89%

“…The functional role of these conserved cytokines was indicated by their increased expression in response to bacterial stimuli. Most current information for IL-17 comes from phylogenetic studies, identification of related signaling pathways, and effector mechanisms in models of M. galloprovincialis and C. gigas (33)(34)(35). IL-17 plays a crucial role in mucosal immunity in mussels, just like in vertebrates (35), which was first identified in C. gigas (32) and later on in Pinctada fucata (75).…”

Section: Cytokinesmentioning

confidence: 99%

“…Most current information for IL-17 comes from phylogenetic studies, identification of related signaling pathways, and effector mechanisms in models of M. galloprovincialis and C. gigas (33)(34)(35). IL-17 plays a crucial role in mucosal immunity in mussels, just like in vertebrates (35), which was first identified in C. gigas (32) and later on in Pinctada fucata (75). Further genomic searching found that there were fifteen IL-17 genes in P. fucata martensii, ten in C. gigas, six in M. galloprovincialis, and ten in scallop Mizuhopecten yessoensis (31) (Table 2).…”

Section: Cytokinesmentioning

confidence: 99%

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Soluble mediators of innate immunity in annelids and bivalve mollusks: A mini-review

et al. 2022

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Annelids and mollusks, both in the superphylum of Lophotrochozoa (Bilateria), are important ecological groups, widespread in soil, freshwater, estuarine, and marine ecosystems. Like all invertebrates, they lack adaptive immunity; however, they are endowed with an effective and complex innate immune system (humoral and cellular defenses) similar to vertebrates. The lack of acquired immunity and the capacity to form antibodies does not mean a lack of specificity: invertebrates have evolved genetic mechanisms capable of producing thousands of different proteins from a small number of genes, providing high variability and diversity of immune effector molecules just like their vertebrate counterparts. This diversity allows annelids and mollusks to recognize and eliminate a wide range of pathogens and respond to environmental stressors. Effector molecules can kill invading microbes, reduce their pathogenicity, or regulate the immune response at cellular and systemic levels. Annelids and mollusks are “typical” lophotrochozoan protostome since both groups include aquatic species with trochophore larvae, which unite both taxa in a common ancestry. Moreover, despite their extensive utilization in immunological research, no model systems are available as there are with other invertebrate groups, such as Caenorhabditis elegans or Drosophila melanogaster, and thus, their immune potential is largely unexplored. In this work, we focus on two classes of key soluble mediators of immunity, i.e., antimicrobial peptides (AMPs) and cytokines, in annelids and bivalves, which are the most studied mollusks. The mediators have been of interest from their first identification to recent advances in molecular studies that clarified their role in the immune response.

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Section: Cytokinesmentioning

confidence: 89%

Section: Cytokinesmentioning

confidence: 99%

Section: Cytokinesmentioning

confidence: 99%

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Soluble mediators of innate immunity in annelids and bivalve mollusks: A mini-review

et al. 2022

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“…IL-17 is of very ancient origin and one of the most conserved cytokines throughout evolution. It is present in many mollusks and is associated with inflammation, particularly in the gut, because IL-17 can be produced by mucosal epithelial cells (81,82). The Th1 (IFN-g, IL-12, TNF-a), Th2 (IL-4, IL-5, IL-13), and Th17 (IL-17, IL-22) cytokine genes were already present during the emergence of cartilaginous fishes (83), indicating that T cells could generate sets of responses as diverse as in mammals.…”

Section: Transcription Factors Underlying Innate-like T Cell Developmentmentioning

confidence: 99%

γδ T, NKT, and MAIT Cells During Evolution: Redundancy or Specialized Functions?

Harly

Robert

Legoux

et al. 2022

The Journal of Immunology

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Innate-like T cells display characteristics of both innate lymphoid cells (ILCs) and mainstream αβ T cells, leading to overlapping functions of innate-like T cells with both subsets. In this review, we show that although innate-like T cells are probably present in all vertebrates, their main characteristics are much better known in amphibians and mammals. Innate-like T cells encompass both γδ and αβ T cells. In mammals, γδ TCRs likely coevolved with molecules of the butyrophilin family they interact with, whereas the semi-invariant TCRs of iNKT and mucosal-associated invariant T cells are evolutionarily locked with their restricting MH1b molecules, CD1d and MR1, respectively. The strong conservation of the Ag recognition systems of innate-like T cell subsets despite similar effector potentialities supports that each one fulfills nonredundant roles related to their Ag specificity.

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“…Mussels can use their efficient innate immune system to deal with different pathogenic agents in a specific way (Costa et al, 2009;Balbi et al, 2013). This attribute is supported by the vast genetic variability that characterizes this species, with several expanded immune gene families as immune recognition C1q factors (Gerdol et al, 2011) or pro-inflammatory cytokines as IL-17 (Saco et al, 2021). The recent discovery of mussel genomic organization as a pangenome revealed presence/absence phenomena in the genetic repertoires of these animals, where a core set of genes was accompanied by great amounts of dispensable and variable genes (Gerdol et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Integration of Transcriptomics and Proteomics Improves the Characterization of the Role of Mussel Gills in a Bacterial Waterborne Infection

et al. 2021

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In recent years, the immune response of mussels (Mytilus galloprovincialis) has been studied at the transcriptomic level against several bacterial infections. As a result, different immune mechanisms have been revealed, including both conserved essential innate pathways and particularities of the mussel immune response according to its nature and environment. However, there is often a lack of functional verification because mussels are a non-model species and because transcriptomic and proteomic information is not always well correlated. In the current study, a high-throughput quantitative proteomics study coupled to LC-MS/MS analysis using isobaric tandem mass tags (TMTs) for protein labeling was employed to study the mussel gill immune response to a Vibrio splendidus bath (waterborne) infection at a functional protein level. A total of 4,242 proteins were identified and quantified, of which 226 were differentially expressed (DEPs) after infection, giving to the study a depth that was lacking in previous proteomic studies of the bivalve immune response. Modulated proteins evidenced an important cytoskeletal disruption caused by bacterial infection. A conserved network of associated proteins was modulated, regulating oxidative stress and NF-kB inflammatory responses and leading to innate immunity effectors. Proteomic results were submitted to an integrated analysis with those obtained in a previous transcriptomic approach with the same infection. Half of all the quantified proteins had a concordant transcriptomic expression trend, but this concordance increased when focusing on the DEPs. The correlation was higher within the immune-related DEPs, and the activation of the conserved NF-kB pro-inflammatory pathway was the main response in both approaches. The results of both techniques could be integrated to obtain a more complete vision of the response.

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The Evolution and Diversity of Interleukin-17 Highlight an Expansion in Marine Invertebrates and Its Conserved Role in Mucosal Immunity

Cited by 23 publications

References 77 publications

Soluble mediators of innate immunity in annelids and bivalve mollusks: A mini-review

Soluble mediators of innate immunity in annelids and bivalve mollusks: A mini-review

γδ T, NKT, and MAIT Cells During Evolution: Redundancy or Specialized Functions?

Integration of Transcriptomics and Proteomics Improves the Characterization of the Role of Mussel Gills in a Bacterial Waterborne Infection

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