Mitochondrial stress is relayed to the cytosol by an OMA1–DELE1–HRI pathway
In mammalian cells, mitochondrial dysfunction triggers the integrated stress response, in which the phosphorylation of eukaryotic translation initiation factor 2α (eIF2α) results in the induction of the transcription factor ATF4 1 – 3 . However, how mitochondrial stress is relayed to ATF4 is unknown...
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| Published in: | Nature (London) Vol. 579; no. 7799; pp. 427 - 432 |
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| Main Authors: | , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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Nature Publishing Group UK
01-03-2020
Nature Publishing Group |
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| Abstract | In mammalian cells, mitochondrial dysfunction triggers the integrated stress response, in which the phosphorylation of eukaryotic translation initiation factor 2α (eIF2α) results in the induction of the transcription factor ATF4
1
–
3
. However, how mitochondrial stress is relayed to ATF4 is unknown. Here we show that HRI is the eIF2α kinase that is necessary and sufficient for this relay. In a genome-wide CRISPR interference screen, we identified factors upstream of HRI: OMA1, a mitochondrial stress-activated protease; and DELE1, a little-characterized protein that we found was associated with the inner mitochondrial membrane. Mitochondrial stress stimulates OMA1-dependent cleavage of DELE1 and leads to the accumulation of DELE1 in the cytosol, where it interacts with HRI and activates the eIF2α kinase activity of HRI. In addition, DELE1 is required for ATF4 translation downstream of eIF2α phosphorylation. Blockade of the OMA1–DELE1–HRI pathway triggers an alternative response in which specific molecular chaperones are induced. The OMA1–DELE1–HRI pathway therefore represents a potential therapeutic target that could enable fine-tuning of the integrated stress response for beneficial outcomes in diseases that involve mitochondrial dysfunction.
A genome-wide CRISPR interference screen shows that a signalling pathway involving OMA1, DELE1 and the eIF2α kinase HRI relays mitochondrial stress to the cytosol to trigger the integrated stress response. |
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| AbstractList | In mammalian cells, mitochondrial dysfunction triggers the integrated stress response, in which the phosphorylation of eukaryotic translation initiation factor 2[alpha] (eIF2[alpha]) results in the induction of the transcription factor ATF4.sup.1-3. However, how mitochondrial stress is relayed to ATF4 is unknown. Here we show that HRI is the eIF2[alpha] kinase that is necessary and sufficient for this relay. In a genome-wide CRISPR interference screen, we identified factors upstream of HRI: OMA1, a mitochondrial stress-activated protease; and DELE1, a little-characterized protein that we found was associated with the inner mitochondrial membrane. Mitochondrial stress stimulates OMA1-dependent cleavage of DELE1 and leads to the accumulation of DELE1 in the cytosol, where it interacts with HRI and activates the eIF2[alpha] kinase activity of HRI. In addition, DELE1 is required for ATF4 translation downstream of eIF2[alpha] phosphorylation. Blockade of the OMA1-DELE1-HRI pathway triggers an alternative response in which specific molecular chaperones are induced. The OMA1-DELE1-HRI pathway therefore represents a potential therapeutic target that could enable fine-tuning of the integrated stress response for beneficial outcomes in diseases that involve mitochondrial dysfunction. In mammalian cells, mitochondrial dysfunction triggers the integrated stress response (ISR), in which eIF2α phosphorylation induces the transcription factor ATF4 1 - 3 . However, how mitochondrial stress is relayed to ATF4 is unknown. We found that HRI is the eIF2α kinase necessary and sufficient for this relay. In a genome-wide CRISPRi screen, we identified factors upstream of HRI: OMA1, a mitochondrial stress-activated protease, and DELE1, a little-characterized protein we found to be associated with the inner mitochondrial membrane. Mitochondrial stress stimulates OMA1-dependent cleavage of DELE1, leading to its accumulation in the cytosol, where it interacts with HRI and activates its eIF2α kinase activity. Additionally, DELE1 is required for ATF4 translation downstream of eIF2α phosphorylation. Blockade of the OMA1-DELE1-HRI pathway triggers an alternative response inducing specific molecular chaperones. Therefore, this pathway is a potential therapeutic target enabling fine-tuning of the ISR for beneficial outcomes in diseases involving mitochondrial dysfunction. In mammalian cells, mitochondrial dysfunction triggers the integrated stress response, in which the phosphorylation of eukaryotic translation initiation factor 2[alpha] (eIF2[alpha]) results in the induction of the transcription factor ATF4.sup.1-3. However, how mitochondrial stress is relayed to ATF4 is unknown. Here we show that HRI is the eIF2[alpha] kinase that is necessary and sufficient for this relay. In a genome-wide CRISPR interference screen, we identified factors upstream of HRI: OMA1, a mitochondrial stress-activated protease; and DELE1, a little-characterized protein that we found was associated with the inner mitochondrial membrane. Mitochondrial stress stimulates OMA1-dependent cleavage of DELE1 and leads to the accumulation of DELE1 in the cytosol, where it interacts with HRI and activates the eIF2[alpha] kinase activity of HRI. In addition, DELE1 is required for ATF4 translation downstream of eIF2[alpha] phosphorylation. Blockade of the OMA1-DELE1-HRI pathway triggers an alternative response in which specific molecular chaperones are induced. The OMA1-DELE1-HRI pathway therefore represents a potential therapeutic target that could enable fine-tuning of the integrated stress response for beneficial outcomes in diseases that involve mitochondrial dysfunction. A genome-wide CRISPR interference screen shows that a signalling pathway involving OMA1, DELE1 and the eIF2[alpha] kinase HRI relays mitochondrial stress to the cytosol to trigger the integrated stress response. In mammalian cells, mitochondrial dysfunction triggers the integrated stress response, in which the phosphorylation of eukaryotic translation initiation factor 2α (eIF2α) results in the induction of the transcription factor ATF4 . However, how mitochondrial stress is relayed to ATF4 is unknown. Here we show that HRI is the eIF2α kinase that is necessary and sufficient for this relay. In a genome-wide CRISPR interference screen, we identified factors upstream of HRI: OMA1, a mitochondrial stress-activated protease; and DELE1, a little-characterized protein that we found was associated with the inner mitochondrial membrane. Mitochondrial stress stimulates OMA1-dependent cleavage of DELE1 and leads to the accumulation of DELE1 in the cytosol, where it interacts with HRI and activates the eIF2α kinase activity of HRI. In addition, DELE1 is required for ATF4 translation downstream of eIF2α phosphorylation. Blockade of the OMA1-DELE1-HRI pathway triggers an alternative response in which specific molecular chaperones are induced. The OMA1-DELE1-HRI pathway therefore represents a potential therapeutic target that could enable fine-tuning of the integrated stress response for beneficial outcomes in diseases that involve mitochondrial dysfunction. In mammalian cells, mitochondrial dysfunction triggers the integrated stress response, in which the phosphorylation of eukaryotic translation initiation factor 2α (eIF2α) results in the induction of the transcription factor ATF4 1 – 3 . However, how mitochondrial stress is relayed to ATF4 is unknown. Here we show that HRI is the eIF2α kinase that is necessary and sufficient for this relay. In a genome-wide CRISPR interference screen, we identified factors upstream of HRI: OMA1, a mitochondrial stress-activated protease; and DELE1, a little-characterized protein that we found was associated with the inner mitochondrial membrane. Mitochondrial stress stimulates OMA1-dependent cleavage of DELE1 and leads to the accumulation of DELE1 in the cytosol, where it interacts with HRI and activates the eIF2α kinase activity of HRI. In addition, DELE1 is required for ATF4 translation downstream of eIF2α phosphorylation. Blockade of the OMA1–DELE1–HRI pathway triggers an alternative response in which specific molecular chaperones are induced. The OMA1–DELE1–HRI pathway therefore represents a potential therapeutic target that could enable fine-tuning of the integrated stress response for beneficial outcomes in diseases that involve mitochondrial dysfunction. A genome-wide CRISPR interference screen shows that a signalling pathway involving OMA1, DELE1 and the eIF2α kinase HRI relays mitochondrial stress to the cytosol to trigger the integrated stress response. In mammalian cells, mitochondrial dysfunction triggers the integrated stress response, in which the phosphorylation of eukaryotic translation initiation factor 2a (eIF2a) results in the induction of the transcription factor ATF41-3. However, how mitochondrial stress is relayed to ATF4 is unknown. Here we show that HRI is the eIF2a kinase that is necessary and sufficient for this relay. In a genome-wide CRISPR interference screen, we identified factors upstream of HRI: OMAI, a mitochondrial stress-activated protease; and DELEI, a little-characterized protein that we found was associated with the inner mitochondrial membrane. Mitochondrial stress stimulates OMAl-dependent cleavage of DELEI and leads to the accumulation of DELEI in the cytosol, where it interacts with HRI and activates the eIF2a kinase activity of HRI. In addition, DELEI is required for ATF4 translation downstream of eIF2a phosphorylation. Blockade of the OMA1-DELE1-HRI pathway triggers an alternative response in which specific molecular chaperones are induced. The OMA1-DELE1-HRI pathway therefore represents a potential therapeutic target that could enable finetuning of the integrated stress response for beneficial outcomes in diseases that involve mitochondrial dysfunction. |
| Audience | Academic |
| Author | Lin, Yu-Hsiu T. Kampmann, Martin Wiita, Arun P. Xu, Ke Guo, Xiaoyan Unger, Bret A. Liu, Yi Aviles, Giovanni Tian, Ruilin Correia, M. Almira |
| AuthorAffiliation | 4 Biophysics Graduate Program, University of California, San Francisco, San Francisco, CA, USA 6 Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA, USA 9 The Liver Center, University of California, San Francisco, San Francisco, CA, USA 7 Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA, USA 10 Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA, USA 1 Institute for Neurodegenerative Disease, University of California, San Francisco, San Francisco, CA, USA 8 Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA, USA 5 Department of Chemistry, University of California, Berkeley, Berkeley, CA, USA 2 Chan Zuckerberg Biohub, San Francisco, CA, USA 3 Department of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA, USA |
| AuthorAffiliation_xml | – name: 3 Department of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA, USA – name: 9 The Liver Center, University of California, San Francisco, San Francisco, CA, USA – name: 2 Chan Zuckerberg Biohub, San Francisco, CA, USA – name: 4 Biophysics Graduate Program, University of California, San Francisco, San Francisco, CA, USA – name: 1 Institute for Neurodegenerative Disease, University of California, San Francisco, San Francisco, CA, USA – name: 5 Department of Chemistry, University of California, Berkeley, Berkeley, CA, USA – name: 6 Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA, USA – name: 7 Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA, USA – name: 8 Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA, USA – name: 10 Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA, USA |
| Author_xml | – sequence: 1 givenname: Xiaoyan surname: Guo fullname: Guo, Xiaoyan organization: Institute for Neurodegenerative Diseases, University of California, San Francisco, Chan Zuckerberg Biohub – sequence: 2 givenname: Giovanni orcidid: 0000-0002-6768-1985 surname: Aviles fullname: Aviles, Giovanni organization: Institute for Neurodegenerative Diseases, University of California, San Francisco, Chan Zuckerberg Biohub – sequence: 3 givenname: Yi surname: Liu fullname: Liu, Yi organization: Department of Cellular and Molecular Pharmacology, University of California, San Francisco – sequence: 4 givenname: Ruilin surname: Tian fullname: Tian, Ruilin organization: Institute for Neurodegenerative Diseases, University of California, San Francisco, Chan Zuckerberg Biohub, Biophysics Graduate Program, University of California, San Francisco – sequence: 5 givenname: Bret A. surname: Unger fullname: Unger, Bret A. organization: Chan Zuckerberg Biohub, Department of Chemistry, University of California, Berkeley – sequence: 6 givenname: Yu-Hsiu T. orcidid: 0000-0002-7157-4330 surname: Lin fullname: Lin, Yu-Hsiu T. organization: Department of Laboratory Medicine, University of California, San Francisco – sequence: 7 givenname: Arun P. orcidid: 0000-0002-7465-6964 surname: Wiita fullname: Wiita, Arun P. organization: Department of Laboratory Medicine, University of California, San Francisco – sequence: 8 givenname: Ke orcidid: 0000-0002-2788-194X surname: Xu fullname: Xu, Ke organization: Chan Zuckerberg Biohub, Department of Chemistry, University of California, Berkeley – sequence: 9 givenname: M. Almira surname: Correia fullname: Correia, M. Almira organization: Department of Cellular and Molecular Pharmacology, University of California, San Francisco, Department of Pharmaceutical Chemistry, University of California, San Francisco, Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, The Liver Center, University of California, San Francisco – sequence: 10 givenname: Martin orcidid: 0000-0002-3819-7019 surname: Kampmann fullname: Kampmann, Martin email: martin.kampmann@ucsf.edu organization: Institute for Neurodegenerative Diseases, University of California, San Francisco, Chan Zuckerberg Biohub, Department of Biochemistry and Biophysics, University of California, San Francisco |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32132707$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contributions: X.G. and M.K. conceptualized and led the overall project, analyzed results and wrote the manuscript, with input from all co-authors. X.G. and G.A. conducted and analyzed the CRISPRi screen and follow-up experiments. Y.L. and M.A.C. conducted and analyzed experiments with purified proteins. R.T. and M.K. analyzed and visualized RNA-Seq results. B.U. and K.X. conducted and analyzed super-resolution experiments. Y.T.L and A.P.W. conducted and analyzed mass spectrometry experiments. |
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| SubjectTerms | 13 13/106 13/31 14 14/63 38 42 45 45/47 631/80/642/333 631/80/86/2366 82 82/1 82/29 82/51 82/58 82/83 Activating Transcription Factor 4 - biosynthesis Activating Transcription Factor 4 - metabolism Amino acids Cell Line Cell physiology Cellular stress response Chaperones CRISPR CRISPR-Cas Systems Cytosol Cytosol - enzymology Cytosol - metabolism eIF-2 Kinase - metabolism Enzyme Activation Eukaryotic Initiation Factor-2 - metabolism Genetic aspects Genomes Health aspects Humanities and Social Sciences Humans Initiation factor eIF-2 Kinases Localization Male Mammalian cells Metalloendopeptidases - metabolism Mitochondria Mitochondria - metabolism Mitochondria - pathology Mitochondrial Proteins - chemistry Mitochondrial Proteins - metabolism Molecular Chaperones - metabolism multidisciplinary Phosphorylation Physiological aspects Physiological research Protein Binding Proteins Science Science (multidisciplinary) Stress (Physiology) Stress, Physiological Therapeutic applications |
| Title | Mitochondrial stress is relayed to the cytosol by an OMA1–DELE1–HRI pathway |
| URI | https://link.springer.com/article/10.1038/s41586-020-2078-2 https://www.ncbi.nlm.nih.gov/pubmed/32132707 https://www.proquest.com/docview/2384222771 https://search.proquest.com/docview/2371851077 https://pubmed.ncbi.nlm.nih.gov/PMC7147832 |
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