Physiological ER stress caused by amylase production induces regulated Ire1-dependent mRNA decay in Aspergillus oryzae
Abstract Regulated Ire1-dependent decay (RIDD) is a feedback mechanism in which the endoribonuclease Ire1 cleaves endoplasmic reticulum (ER)-localized mRNAs encoding secretory and membrane proteins in eukaryotic cells under ER stress. RIDD is artificially induced by chemicals that generate ER stress...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-10-01
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| Series: | Communications Biology |
| Online Access: | https://doi.org/10.1038/s42003-023-05386-w |
| _version_ | 1797557175278632960 |
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| author | Mizuki Tanaka Silai Zhang Shun Sato Jun-ichi Yokota Yuko Sugiyama Yasuaki Kawarasaki Youhei Yamagata Katsuya Gomi Takahiro Shintani |
| author_facet | Mizuki Tanaka Silai Zhang Shun Sato Jun-ichi Yokota Yuko Sugiyama Yasuaki Kawarasaki Youhei Yamagata Katsuya Gomi Takahiro Shintani |
| author_sort | Mizuki Tanaka |
| collection | DOAJ |
| description | Abstract Regulated Ire1-dependent decay (RIDD) is a feedback mechanism in which the endoribonuclease Ire1 cleaves endoplasmic reticulum (ER)-localized mRNAs encoding secretory and membrane proteins in eukaryotic cells under ER stress. RIDD is artificially induced by chemicals that generate ER stress; however, its importance under physiological conditions remains unclear. Here, we demonstrate the occurrence of RIDD in filamentous fungus using Aspergillus oryzae as a model, which secretes copious amounts of amylases. α-Amylase mRNA was rapidly degraded by IreA, an Ire1 ortholog, depending on its ER-associated translation when mycelia were treated with dithiothreitol, an ER-stress inducer. The mRNA encoding maltose permease MalP, a prerequisite for the induction of amylolytic genes, was also identified as an RIDD target. Importantly, RIDD of malP mRNA is triggered by inducing amylase production without any artificial ER stress inducer. Our data provide the evidence that RIDD occurs in eukaryotic microorganisms under physiological ER stress. |
| first_indexed | 2024-03-10T17:13:37Z |
| format | Article |
| id | doaj.art-de1f9481ffd44c5682eb105af5dd5795 |
| institution | Directory Open Access Journal |
| issn | 2399-3642 |
| language | English |
| last_indexed | 2024-03-10T17:13:37Z |
| publishDate | 2023-10-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Communications Biology |
| spelling | doaj.art-de1f9481ffd44c5682eb105af5dd57952023-11-20T10:36:08ZengNature PortfolioCommunications Biology2399-36422023-10-01611910.1038/s42003-023-05386-wPhysiological ER stress caused by amylase production induces regulated Ire1-dependent mRNA decay in Aspergillus oryzaeMizuki Tanaka0Silai Zhang1Shun Sato2Jun-ichi Yokota3Yuko Sugiyama4Yasuaki Kawarasaki5Youhei Yamagata6Katsuya Gomi7Takahiro Shintani8Department of Applied Biological Chemistry, Graduate School of Agriculture, Tokyo University of Agriculture and TechnologyDepartment of Agricultural Chemistry, Graduate School of Agricultural Science, Tohoku UniversityDepartment of Agricultural Chemistry, Graduate School of Agricultural Science, Tohoku UniversityDepartment of Agricultural Chemistry, Graduate School of Agricultural Science, Tohoku UniversityDepartment of Agricultural Chemistry, Graduate School of Agricultural Science, Tohoku UniversityBiomolecular Engineering Laboratory, School of Food and Nutritional Science, University of ShizuokaDepartment of Applied Biological Chemistry, Graduate School of Agriculture, Tokyo University of Agriculture and TechnologyDepartment of Agricultural Chemistry, Graduate School of Agricultural Science, Tohoku UniversityDepartment of Agricultural Chemistry, Graduate School of Agricultural Science, Tohoku UniversityAbstract Regulated Ire1-dependent decay (RIDD) is a feedback mechanism in which the endoribonuclease Ire1 cleaves endoplasmic reticulum (ER)-localized mRNAs encoding secretory and membrane proteins in eukaryotic cells under ER stress. RIDD is artificially induced by chemicals that generate ER stress; however, its importance under physiological conditions remains unclear. Here, we demonstrate the occurrence of RIDD in filamentous fungus using Aspergillus oryzae as a model, which secretes copious amounts of amylases. α-Amylase mRNA was rapidly degraded by IreA, an Ire1 ortholog, depending on its ER-associated translation when mycelia were treated with dithiothreitol, an ER-stress inducer. The mRNA encoding maltose permease MalP, a prerequisite for the induction of amylolytic genes, was also identified as an RIDD target. Importantly, RIDD of malP mRNA is triggered by inducing amylase production without any artificial ER stress inducer. Our data provide the evidence that RIDD occurs in eukaryotic microorganisms under physiological ER stress.https://doi.org/10.1038/s42003-023-05386-w |
| spellingShingle | Mizuki Tanaka Silai Zhang Shun Sato Jun-ichi Yokota Yuko Sugiyama Yasuaki Kawarasaki Youhei Yamagata Katsuya Gomi Takahiro Shintani Physiological ER stress caused by amylase production induces regulated Ire1-dependent mRNA decay in Aspergillus oryzae Communications Biology |
| title | Physiological ER stress caused by amylase production induces regulated Ire1-dependent mRNA decay in Aspergillus oryzae |
| title_full | Physiological ER stress caused by amylase production induces regulated Ire1-dependent mRNA decay in Aspergillus oryzae |
| title_fullStr | Physiological ER stress caused by amylase production induces regulated Ire1-dependent mRNA decay in Aspergillus oryzae |
| title_full_unstemmed | Physiological ER stress caused by amylase production induces regulated Ire1-dependent mRNA decay in Aspergillus oryzae |
| title_short | Physiological ER stress caused by amylase production induces regulated Ire1-dependent mRNA decay in Aspergillus oryzae |
| title_sort | physiological er stress caused by amylase production induces regulated ire1 dependent mrna decay in aspergillus oryzae |
| url | https://doi.org/10.1038/s42003-023-05386-w |
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