Optineurin deficiency impairs autophagy to cause interferon beta overproduction and increased survival of mice following viral infection

PLoS One. 2023 Jun 23;18(6):e0287545. doi: 10.1371/journal.pone.0287545. eCollection 2023.

Abstract

Background: Optineurin (OPTN) is associated with several human diseases, including amyotrophic lateral sclerosis (ALS), and is involved in various cellular processes, including autophagy. Optineurin regulates the expression of interferon beta (IFNβ), which plays a central role in the innate immune response to viral infection. However, the role of optineurin in response to viral infection has not been fully clarified. It is known that optineurin-deficient cells produce more IFNβ than wild-type cells following viral infection. In this study, we investigate the reasons for, and effects of, IFNβ overproduction during optineurin deficiency both in vitro and in vivo.

Methods: To investigate the mechanism of IFNβ overproduction, viral nucleic acids in infected cells were quantified by RT-qPCR and the autophagic activity of optineurin-deficient cells was determined to understand the basis for the intracellular accumulation of viral nucleic acids. Moreover, viral infection experiments using optineurin-disrupted (Optn-KO) animals were performed with several viruses.

Results: IFNβ overproduction following viral infection was observed not only in several types of optineurin-deficient cell lines but also in Optn-KO mice and human ALS patient cells carrying mutations in OPTN. IFNβ overproduction in Optn-KO cells was revealed to be caused by excessive accumulation of viral nucleic acids, which was a consequence of reduced autophagic activity caused by the loss of optineurin. Additionally, IFNβ overproduction in Optn-KO mice suppressed viral proliferation, resulting in increased mouse survival following viral challenge.

Conclusion: Our findings indicate that the combination of optineurin deficiency and viral infection leads to IFNβ overproduction in vitro and in vivo. The effects of optineurin deficiency are elicited by viral infection, therefore, viral infection may be implicated in the development of optineurin-related diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyotrophic Lateral Sclerosis* / genetics
  • Animals
  • Autophagy / genetics
  • Cell Cycle Proteins* / genetics
  • Humans
  • Immunity, Innate
  • Interferon-beta / genetics
  • Membrane Transport Proteins* / genetics
  • Mice
  • Mice, Knockout
  • Transcription Factor TFIIIA / genetics
  • Transcription Factor TFIIIA / metabolism
  • Virus Diseases*

Substances

  • Cell Cycle Proteins
  • Interferon-beta
  • Transcription Factor TFIIIA
  • OPTN protein, human
  • Optn protein, mouse
  • Membrane Transport Proteins

Grants and funding

This study was supported by JSPS KAKENHI Grant Numbers 16K08812, 25460568, 26242085, 19K22968, 26830035 and 21K07461, and by the Tsuchiya Memorial Medical Foundation, the Program for Promotion of Basic and Applied Research for Innovations in Biooriented Industry (BRAIN), and the Takeda Science Foundation. This study was partially supported by the NIBB Individual Collaborative Research Program (ID: 12-361 and 12-340) and the Program of the Network-type Joint Usage/Research Center for Radiation Disaster Medical Science. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.