Regulated Formation of an Amyloid-like Translational Repressor Governs Gametogenesis
Message-specific translational control is required for gametogenesis. In yeast, the RNA-binding protein Rim4 mediates translational repression of numerous mRNAs, including the B-type cyclin CLB3, which is essential for establishing the meiotic chromosome segregation pattern. Here, we show that Rim4...
Main Authors: | , , , , , , |
---|---|
Other Authors: | |
Format: | Article |
Language: | en_US |
Published: |
Elsevier
2017
|
Online Access: | http://hdl.handle.net/1721.1/107656 https://orcid.org/0000-0002-3388-7723 https://orcid.org/0000-0003-4363-441X https://orcid.org/0000-0002-7699-9354 https://orcid.org/0000-0003-2807-9657 https://orcid.org/0000-0001-8012-1512 https://orcid.org/0000-0001-9837-0314 |
_version_ | 1826193079775789056 |
---|---|
author | Berchowitz, Luke Edwin Kabachinski, Gregory L. Walker, Margaret R. Carlile Jr, Thomas Marshal Gilbert, Wendy Schwartz, Thomas Amon, Angelika B. |
author2 | Massachusetts Institute of Technology. Department of Biology |
author_facet | Massachusetts Institute of Technology. Department of Biology Berchowitz, Luke Edwin Kabachinski, Gregory L. Walker, Margaret R. Carlile Jr, Thomas Marshal Gilbert, Wendy Schwartz, Thomas Amon, Angelika B. |
author_sort | Berchowitz, Luke Edwin |
collection | MIT |
description | Message-specific translational control is required for gametogenesis. In yeast, the RNA-binding protein Rim4 mediates translational repression of numerous mRNAs, including the B-type cyclin CLB3, which is essential for establishing the meiotic chromosome segregation pattern. Here, we show that Rim4 forms amyloid-like aggregates and that it is the amyloid-like form of Rim4 that is the active, translationally repressive form of the protein. Our data further show that Rim4 aggregation is a developmentally regulated process. Starvation induces the conversion of monomeric Rim4 into amyloid-like aggregates, thereby activating the protein to bring about repression of translation. At the onset of meiosis II, Rim4 aggregates are abruptly degraded allowing translation to commence. Although amyloids are best known for their role in the etiology of diseases such as Alzheimer’s, Parkinson’s, and diabetes by forming toxic protein aggregates, our findings show that cells can utilize amyloid-like protein aggregates to function as central regulators of gametogenesis. |
first_indexed | 2024-09-23T09:33:27Z |
format | Article |
id | mit-1721.1/107656 |
institution | Massachusetts Institute of Technology |
language | en_US |
last_indexed | 2024-09-23T09:33:27Z |
publishDate | 2017 |
publisher | Elsevier |
record_format | dspace |
spelling | mit-1721.1/1076562022-09-26T12:15:30Z Regulated Formation of an Amyloid-like Translational Repressor Governs Gametogenesis Berchowitz, Luke Edwin Kabachinski, Gregory L. Walker, Margaret R. Carlile Jr, Thomas Marshal Gilbert, Wendy Schwartz, Thomas Amon, Angelika B. Massachusetts Institute of Technology. Department of Biology Koch Institute for Integrative Cancer Research at MIT Berchowitz, Luke Edwin Kabachinski, Gregory L. Walker, Margaret R. Carlile Jr, Thomas Marshal Gilbert, Wendy Schwartz, Thomas Amon, Angelika B. Message-specific translational control is required for gametogenesis. In yeast, the RNA-binding protein Rim4 mediates translational repression of numerous mRNAs, including the B-type cyclin CLB3, which is essential for establishing the meiotic chromosome segregation pattern. Here, we show that Rim4 forms amyloid-like aggregates and that it is the amyloid-like form of Rim4 that is the active, translationally repressive form of the protein. Our data further show that Rim4 aggregation is a developmentally regulated process. Starvation induces the conversion of monomeric Rim4 into amyloid-like aggregates, thereby activating the protein to bring about repression of translation. At the onset of meiosis II, Rim4 aggregates are abruptly degraded allowing translation to commence. Although amyloids are best known for their role in the etiology of diseases such as Alzheimer’s, Parkinson’s, and diabetes by forming toxic protein aggregates, our findings show that cells can utilize amyloid-like protein aggregates to function as central regulators of gametogenesis. Charles A. King Trust (Postdoctoral Fellowship) American Cancer Society (Fellowship) National Institutes of Health (U.S.) (Grants GM62207, GM77537, and GM094303) 2017-03-22T19:50:38Z 2017-03-22T19:50:38Z 2015-09 2015-07 Article http://purl.org/eprint/type/JournalArticle 0092-8674 1097-4172 http://hdl.handle.net/1721.1/107656 Berchowitz, Luke E. et al. “Regulated Formation of an Amyloid-like Translational Repressor Governs Gametogenesis.” Cell 163.2 (2015): 406–418. https://orcid.org/0000-0002-3388-7723 https://orcid.org/0000-0003-4363-441X https://orcid.org/0000-0002-7699-9354 https://orcid.org/0000-0003-2807-9657 https://orcid.org/0000-0001-8012-1512 https://orcid.org/0000-0001-9837-0314 en_US http://dx.doi.org/10.1016/j.cell.2015.08.060 Cell Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier PMC |
spellingShingle | Berchowitz, Luke Edwin Kabachinski, Gregory L. Walker, Margaret R. Carlile Jr, Thomas Marshal Gilbert, Wendy Schwartz, Thomas Amon, Angelika B. Regulated Formation of an Amyloid-like Translational Repressor Governs Gametogenesis |
title | Regulated Formation of an Amyloid-like Translational Repressor Governs Gametogenesis |
title_full | Regulated Formation of an Amyloid-like Translational Repressor Governs Gametogenesis |
title_fullStr | Regulated Formation of an Amyloid-like Translational Repressor Governs Gametogenesis |
title_full_unstemmed | Regulated Formation of an Amyloid-like Translational Repressor Governs Gametogenesis |
title_short | Regulated Formation of an Amyloid-like Translational Repressor Governs Gametogenesis |
title_sort | regulated formation of an amyloid like translational repressor governs gametogenesis |
url | http://hdl.handle.net/1721.1/107656 https://orcid.org/0000-0002-3388-7723 https://orcid.org/0000-0003-4363-441X https://orcid.org/0000-0002-7699-9354 https://orcid.org/0000-0003-2807-9657 https://orcid.org/0000-0001-8012-1512 https://orcid.org/0000-0001-9837-0314 |
work_keys_str_mv | AT berchowitzlukeedwin regulatedformationofanamyloidliketranslationalrepressorgovernsgametogenesis AT kabachinskigregoryl regulatedformationofanamyloidliketranslationalrepressorgovernsgametogenesis AT walkermargaretr regulatedformationofanamyloidliketranslationalrepressorgovernsgametogenesis AT carlilejrthomasmarshal regulatedformationofanamyloidliketranslationalrepressorgovernsgametogenesis AT gilbertwendy regulatedformationofanamyloidliketranslationalrepressorgovernsgametogenesis AT schwartzthomas regulatedformationofanamyloidliketranslationalrepressorgovernsgametogenesis AT amonangelikab regulatedformationofanamyloidliketranslationalrepressorgovernsgametogenesis |