Termination of the unfolded protein response is guided by ER stress-induced HAC1 mRNA nuclear retention

Laura Matabishi-Bibi, Drice Challal, Mara Barucco, Domenico Libri and Anna Babour ()
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Laura Matabishi-Bibi: Univ Paris Diderot, Sorbonne Paris Cité, INSERM U944, CNRS UMR7212, Hôpital St. Louis 1, Avenue Claude Vellefaux
Drice Challal: Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC)
Mara Barucco: Institut Jacques Monod, Univ Paris Diderot, Sorbonne Paris Cité, CNRS, Bâtiment Buffon
Domenico Libri: Institut de Génétique Moléculaire de Montpellier, Univ Montpellier, CNRS
Anna Babour: Univ Paris Diderot, Sorbonne Paris Cité, INSERM U944, CNRS UMR7212, Hôpital St. Louis 1, Avenue Claude Vellefaux

Nature Communications, 2022, vol. 13, issue 1, 1-16

Abstract: Abstract Cellular homeostasis is maintained by surveillance mechanisms that intervene at virtually every step of gene expression. In the nucleus, the yeast chromatin remodeler Isw1 holds back maturing mRNA ribonucleoparticles to prevent their untimely export, but whether this activity operates beyond quality control of mRNA biogenesis to regulate gene expression is unknown. Here, we identify the mRNA encoding the central effector of the unfolded protein response (UPR) HAC1, as an Isw1 RNA target. The direct binding of Isw1 to the 3’ untranslated region of HAC1 mRNA restricts its nuclear export and is required for accurate UPR abatement. Accordingly, ISW1 inactivation sensitizes cells to endoplasmic reticulum (ER) stress while its overexpression reduces UPR induction. Our results reveal an unsuspected mechanism, in which binding of ER-stress induced Isw1 to HAC1 mRNA limits its nuclear export, providing a feedback loop that fine-tunes UPR attenuation to guarantee homeostatic adaptation to ER stress.

Date: 2022
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DOI: 10.1038/s41467-022-34133-8

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