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

Front Immunol. 2021 Jul 27:12:692997. doi: 10.3389/fimmu.2021.692997. eCollection 2021.

Abstract

The interleukin-17 (IL-17) family consists of proinflammatory cytokines conserved during evolution. A comparative genomics approach was applied to examine IL-17 throughout evolution from poriferans to higher vertebrates. Cnidaria was highlighted as the most ancient diverged phylum, and several evolutionary patterns were revealed. Large expansions of the IL-17 repertoire were observed in marine molluscs and echinoderm species. We further studied this expansion in filter-fed Mytilus galloprovincialis, which is a bivalve with a highly effective innate immune system supported by a variable pangenome. We recovered 379 unique IL-17 sequences and 96 receptors from individual genomes that were classified into 23 and 6 isoforms after phylogenetic analyses. Mussel IL-17 isoforms were conserved among individuals and shared between closely related Mytilidae species. Certain isoforms were specifically implicated in the response to a waterborne infection with Vibrio splendidus in mussel gills. The involvement of IL-17 in mucosal immune responses could be conserved in higher vertebrates from these ancestral lineages.

Keywords: IL-17; comparative genomics; comparative immunology; cytokines; evolution; interleukin; mucosal immunity; mussel.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Evolution, Molecular*
  • Host-Pathogen Interactions
  • Immunity, Mucosal*
  • Interleukin-17 / genetics
  • Interleukin-17 / immunology*
  • Interleukin-17 / metabolism
  • Mytilus / genetics
  • Mytilus / immunology*
  • Mytilus / metabolism
  • Phylogeny
  • Protein Isoforms
  • Receptors, Interleukin-17 / genetics
  • Receptors, Interleukin-17 / immunology*
  • Receptors, Interleukin-17 / metabolism
  • Signal Transduction
  • Species Specificity
  • Vibrio / immunology
  • Vibrio / pathogenicity
  • Vibrio Infections / immunology
  • Vibrio Infections / metabolism
  • Vibrio Infections / microbiology

Substances

  • Interleukin-17
  • Protein Isoforms
  • Receptors, Interleukin-17

Supplementary concepts

  • Vibrio splendidus