Evolutionary, comparative, and functional analyses of STATs and regulation of the JAK-STAT pathway in lumpfish upon bacterial and poly(I:C) exposure

Front Cell Infect Microbiol. 2023 Sep 22:13:1252744. doi: 10.3389/fcimb.2023.1252744. eCollection 2023.

Abstract

Background: The Janus kinase/signal transducers and activators of transcription (JAK-STAT) system regulates several biological processes by affecting transcription of genes as a response to cytokines and growth factors. In the present study, we have characterized the STAT genes in lumpfish (Cyclopterus lumpus L.), belonging to the order Perciformes, and investigated regulation of the JAK-STAT signaling pathway upon exposure to bacteria (Vibrio anguillarum) and poly(I:C), the latter mimicking antiviral responses.

Methods: Characterization and evolutionary analyses of the STATs were performed by phylogeny, protein domain, homology similarity and synteny analyses. Antibacterial and antiviral responses were investigated by performing KEGG pathway analysis.

Results: We observed that lumpfish have stat1a, 2, 3, 4, 5a, 5b, and 6. Transcriptome-wide analyses showed that most components of the JAK-STAT pathway were present in lumpfish. il-6, il-10, il-21, iκBα and stat3 were upregulated 6 hours post exposure (hpe) against bacteria while type I interferons (IFNs), irf1, irf3, irf10, stat1 and 2 were upregulated 24 hpe against poly(I:C).

Conclusions: Our findings shed light on the diversity and evolution of the STATs and the data show that the STAT genes are highly conserved among fish, including lumpfish. The transcriptome-wide analyses lay the groundwork for future research into the functional significance of these genes in regulating critical biological processes and make an important basis for development of prophylactic measure such as vaccination, which is highly needed for lumpfish since it is vulnerable for both bacterial and viral diseases.

Keywords: JAK-STAT; Poly(I:C); Vibrio anguillarum; lumpfish; lumpsucker; transcriptome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antiviral Agents / pharmacology
  • Bacteria / genetics
  • Bacteria / metabolism
  • Janus Kinases* / genetics
  • Janus Kinases* / metabolism
  • Janus Kinases* / pharmacology
  • Perciformes* / metabolism
  • STAT Transcription Factors / genetics
  • STAT Transcription Factors / metabolism
  • STAT Transcription Factors / pharmacology
  • Signal Transduction

Substances

  • Janus Kinases
  • STAT Transcription Factors
  • Antiviral Agents

Grants and funding

This project has received funding from the Research Council of Norway (grant 244148/E40) and the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 101034309 under SEAS programme at UIB.