PUBLICATION

Hnf4α integrates AIF and caspase 3/9 signaling to restrict single and coinfecting pathogens in teleosts

Authors
Yan, D., Tao, M.H., Wu, X.M., Zhang, J., Li, M., Chang, M.X.
ID
ZDB-PUB-250909-11
Date
2025
Source
PLoS pathogens   21: e1013491e1013491 (Journal)
Registered Authors
Chang, Mingxian
Keywords
none
MeSH Terms
  • Animals
  • Fish Diseases*/immunology
  • Fish Diseases*/metabolism
  • Fish Diseases*/microbiology
  • Fish Diseases*/virology
  • Reoviridae
  • Zebrafish
  • Coinfection*/immunology
  • Caspase 9*/metabolism
  • Hepatocyte Nuclear Factor 4*/genetics
  • Hepatocyte Nuclear Factor 4*/immunology
  • Hepatocyte Nuclear Factor 4*/metabolism
  • Signal Transduction
  • Carps
  • Reoviridae Infections*/immunology
  • Reoviridae Infections*/metabolism
  • Reoviridae Infections*/veterinary
  • Caspase 3/metabolism
  • Aeromonas salmonicida/immunology
  • Apoptosis
  • Apoptosis Inducing Factor*/metabolism
PubMed
40920830 Full text @ PLoS Pathog.
Abstract
Hepatocyte nuclear factor 4 alpha (Hnf4α), a conserved nuclear receptor central to vertebrate liver development and metabolic regulation, emerges here as a pivotal immune regulator in teleosts against complex infectious threats. While its metabolic roles are well-established, Hnf4α's function in bacterial infection, viral infection, and bacterial-viral coinfection-major challenges in global aquaculture-remained uncharacterized. This study reveals that teleost Hnf4α acts as a dual-functional immune checkpoint, essential for combating Aeromonas salmonicida, grass carp reovirus (GCRV), and their coinfection. In in vivo zebrafish models, hnf4α-deficient larvae showed profound susceptibility, with survival rates reduced by 13.33-40% during infections, whereas gcHnf4α overexpression enhanced larval survival by 17.78-23.33% in single or coinfection scenarios. In vitro analyses in CIK cells demonstrated that gcHnf4α restricts A. salmonicida proliferation and GCRV replication through activation of a mitochondrial apoptotic program. Mechanistically, gcHnf4α forms a nuclear signaling complex with apoptosis-inducing factor (AIF) and caspases 3/9, driving a dual-dependent apoptotic pathway: (1) AIF-mediated caspase-independent nuclear apoptotic processes and (2) caspase 3/9-dependent cytoplasmic apoptotic execution. Confocal microscopy and co-immunoprecipitation validated direct interactions between gcHnf4α and these apoptotic effectors. Pharmacological inhibition of caspases 3/9 or AIF silencing abrogated gcHnf4α's protective effects, while ectopic caspase expression rescued survival deficits in hnf4α-deficient larvae. These findings establish Hnf4α as a conserved molecular nexus linking nuclear receptor signaling to apoptotic immunity, offering a novel strategy for aquacultural disease control. By targeting the AIF-caspase axis, Hnf4α enables efficient pathogen elimination, delineating it as a promising target for developing dual-action immunomodulators.
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Human Disease / Model
Sequence Targeting Reagents
Fish
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Mapping