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Nonsense-mediated decay controls a negative feedback loop in innate immune sensing.

Simon Boudreault, Yahira Rivera-Lopez, Max B Ferretti

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    Double-stranded RNA (dsRNA) sensing during viral infection inhibits nonsense-mediated decay (NMD). This NMD inhibition creates a negative feedback loop, limiting dsRNA sensing and shaping innate immune responses.

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    Area of Science:

    • Molecular Biology
    • Immunology
    • Virology

    Background:

    • Nonsense-mediated decay (NMD) is a crucial mRNA surveillance pathway that degrades aberrant transcripts.
    • NMD regulates gene expression and isoform abundance under physiological conditions.
    • During viral infections, NMD's role is complex, exhibiting both antiviral and proviral effects, necessitating further investigation.

    Purpose of the Study:

    • To investigate the involvement of NMD in double-stranded RNA (dsRNA) sensing during viral infection.
    • To elucidate the mechanisms by which dsRNA sensing influences NMD activity.
    • To understand how NMD modulation impacts innate immune responses to viral stimuli.

    Main Methods:

    • Utilized EIF4A2 exon 10B inclusion as a model for NMD-related alternative splicing during viral infection.
    • Assessed the impact of dsRNA sensing on NMD activity.
    • Investigated the roles of RNaseL and PKR in NMD inhibition.
    • Quantified IFN-β induction, interferon-stimulated gene expression, and IRF3 activation.
    • Measured dsRNA content and its effect on PKR and RNaseL activation and cell death.

    Main Results:

    • dsRNA sensing inhibits NMD, primarily through translational blockade mediated by RNaseL or PKR.
    • NMD inhibition was found to limit the induction of IFN-β and interferon-stimulated genes, preceding IRF3 nuclear translocation.
    • Inhibition of NMD reduced dsRNA levels, subsequently decreasing PKR and RNaseL activation and inflammasome-mediated cell death.
    • These findings suggest NMD directly influences dsRNA sensing by modulating the dsRNA load.

    Conclusions:

    • dsRNA sensing during viral infection inhibits NMD via translational repression.
    • This inhibition establishes a negative feedback loop that limits dsRNA sensing and prevents excessive activation of antiviral pathways.
    • NMD plays a critical role in regulating innate immunity and inflammation by controlling the dsRNA load and shaping antiviral responses.