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A Unique ISR Program Determines Cellular Responses to Chronic Stress

BJ. Guan, V. van Hoef, R. Jobava, O. Elroy-Stein, LS. Valasek, M. Cargnello, XH. Gao, D. Krokowski, WC. Merrick, SR. Kimball, AA. Komar, AE. Koromilas, A. Wynshaw-Boris, I. Topisirovic, O. Larsson, M. Hatzoglou,

. 2017 ; 68 (5) : 885-900.e6.

Language English Country United States

Document type Journal Article

Persistent link   https://www.medvik.cz/link/bmc18016209

The integrated stress response (ISR) is a homeostatic mechanism induced by endoplasmic reticulum (ER) stress. In acute/transient ER stress, decreased global protein synthesis and increased uORF mRNA translation are followed by normalization of protein synthesis. Here, we report a dramatically different response during chronic ER stress. This chronic ISR program is characterized by persistently elevated uORF mRNA translation and concurrent gene expression reprogramming, which permits simultaneous stress sensing and proteostasis. The program includes PERK-dependent switching to an eIF3-dependent translation initiation mechanism, resulting in partial, but not complete, translational recovery, which, together with transcriptional reprogramming, selectively bolsters expression of proteins with ER functions. Coordination of transcriptional and translational reprogramming prevents ER dysfunction and inhibits "foamy cell" development, thus establishing a molecular basis for understanding human diseases associated with ER dysfunction.

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$a The integrated stress response (ISR) is a homeostatic mechanism induced by endoplasmic reticulum (ER) stress. In acute/transient ER stress, decreased global protein synthesis and increased uORF mRNA translation are followed by normalization of protein synthesis. Here, we report a dramatically different response during chronic ER stress. This chronic ISR program is characterized by persistently elevated uORF mRNA translation and concurrent gene expression reprogramming, which permits simultaneous stress sensing and proteostasis. The program includes PERK-dependent switching to an eIF3-dependent translation initiation mechanism, resulting in partial, but not complete, translational recovery, which, together with transcriptional reprogramming, selectively bolsters expression of proteins with ER functions. Coordination of transcriptional and translational reprogramming prevents ER dysfunction and inhibits "foamy cell" development, thus establishing a molecular basis for understanding human diseases associated with ER dysfunction.
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$a van Hoef, Vincent $u Department of Oncology-Pathology, Karolinska Institutet, SciLifeLab, Stockholm 171 76, Sweden.
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$a Jobava, Raul $u Department of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, OH 44106, USA.
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$a Elroy-Stein, Orna $u Department of Cell Research and Immunology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel.
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$a Valasek, Leos S $u Laboratory of Regulation of Gene Expression, Institute of Microbiology AS CR, Prague 142 20, Czech Republic.
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$a Cargnello, Marie $u Lady Davis Institute for Medical Research and Gerald Bronfman, Department of Oncology, Montreal, QC H3T 1E2, Canada.
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$a Gao, Xing-Huang $u Department of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, OH 44106, USA.
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$a Krokowski, Dawid $u Department of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, OH 44106, USA.
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$a Merrick, William C $u Department of Biochemistry, Case Western Reserve University, Cleveland, OH 44106, USA.
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$a Kimball, Scot R $u Department of Cellular and Molecular Physiology, Pennsylvania State University College of Medicine, Hershey, PA 17033, USA.
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$a Komar, Anton A $u Center for Gene Regulation in Health and Disease and Department of Biological, Geological, and Environmental Sciences, Cleveland State University, Cleveland, OH 44115, USA.
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$a Koromilas, Antonis E $u Lady Davis Institute for Medical Research and Gerald Bronfman, Department of Oncology, Montreal, QC H3T 1E2, Canada.
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$a Wynshaw-Boris, Anthony $u Department of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, OH 44106, USA.
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$a Topisirovic, Ivan $u Lady Davis Institute for Medical Research and Gerald Bronfman, Department of Oncology, Montreal, QC H3T 1E2, Canada; Department of Biochemistry, McGill University, Montreal, QC H3T 1E2, Canada. Electronic address: ivan.topisirovic@mcgill.ca.
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$a Larsson, Ola $u Department of Oncology-Pathology, Karolinska Institutet, SciLifeLab, Stockholm 171 76, Sweden. Electronic address: ola.larsson@ki.se.
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$a Hatzoglou, Maria $u Department of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, OH 44106, USA. Electronic address: mxh8@case.edu.
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