Control of PNG kinase, a key regulator of mRNA translation, is coupled to meiosis completion at egg activation
The oocyte-to-embryo transition involves extensive changes in mRNA translation, regulated in Drosophila by the PNG kinase complex whose activity we show here to be under precise developmental control. Despite presence of the catalytic PNG subunit and the PLU and GNU activating subunits in the mature...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2017-05-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/22219 |
| _version_ | 1811201639734837248 |
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| author | Masatoshi Hara Boryana Petrova Terry L Orr-Weaver |
| author_facet | Masatoshi Hara Boryana Petrova Terry L Orr-Weaver |
| author_sort | Masatoshi Hara |
| collection | DOAJ |
| description | The oocyte-to-embryo transition involves extensive changes in mRNA translation, regulated in Drosophila by the PNG kinase complex whose activity we show here to be under precise developmental control. Despite presence of the catalytic PNG subunit and the PLU and GNU activating subunits in the mature oocyte, GNU is phosphorylated at Cyclin B/CDK1sites and unable to bind PNG and PLU. In vitro phosphorylation of GNU by CyclinB/CDK1 blocks activation of PNG. Meiotic completion promotes GNU dephosphorylation and PNG kinase activation to regulate translation. The critical regulatory effect of phosphorylation is shown by replacement in the oocyte with a phosphorylation-resistant form of GNU, which promotes PNG-GNU complex formation, elevation of Cyclin B, and meiotic defects consistent with premature PNG activation. After PNG activation GNU is destabilized, thus inactivating PNG. This short-lived burst in kinase activity links development with maternal mRNA translation and ensures irreversibility of the oocyte-to-embryo transition. |
| first_indexed | 2024-04-12T02:25:13Z |
| format | Article |
| id | doaj.art-23f54ac30eb148bb923e79365f0de6ab |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:25:13Z |
| publishDate | 2017-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-23f54ac30eb148bb923e79365f0de6ab2022-12-22T03:52:01ZengeLife Sciences Publications LtdeLife2050-084X2017-05-01610.7554/eLife.22219Control of PNG kinase, a key regulator of mRNA translation, is coupled to meiosis completion at egg activationMasatoshi Hara0https://orcid.org/0000-0001-8433-1111Boryana Petrova1Terry L Orr-Weaver2https://orcid.org/0000-0002-7934-111XWhitehead Institute and Massachusetts Institute of Technology, Cambridge, United StatesWhitehead Institute and Massachusetts Institute of Technology, Cambridge, United StatesWhitehead Institute and Massachusetts Institute of Technology, Cambridge, United States; Department of Biology, Massachusetts Institute of Technology, Cambridge, United StatesThe oocyte-to-embryo transition involves extensive changes in mRNA translation, regulated in Drosophila by the PNG kinase complex whose activity we show here to be under precise developmental control. Despite presence of the catalytic PNG subunit and the PLU and GNU activating subunits in the mature oocyte, GNU is phosphorylated at Cyclin B/CDK1sites and unable to bind PNG and PLU. In vitro phosphorylation of GNU by CyclinB/CDK1 blocks activation of PNG. Meiotic completion promotes GNU dephosphorylation and PNG kinase activation to regulate translation. The critical regulatory effect of phosphorylation is shown by replacement in the oocyte with a phosphorylation-resistant form of GNU, which promotes PNG-GNU complex formation, elevation of Cyclin B, and meiotic defects consistent with premature PNG activation. After PNG activation GNU is destabilized, thus inactivating PNG. This short-lived burst in kinase activity links development with maternal mRNA translation and ensures irreversibility of the oocyte-to-embryo transition.https://elifesciences.org/articles/22219egg activationmaternal mRNAcell cycleDrosophila |
| spellingShingle | Masatoshi Hara Boryana Petrova Terry L Orr-Weaver Control of PNG kinase, a key regulator of mRNA translation, is coupled to meiosis completion at egg activation eLife egg activation maternal mRNA cell cycle Drosophila |
| title | Control of PNG kinase, a key regulator of mRNA translation, is coupled to meiosis completion at egg activation |
| title_full | Control of PNG kinase, a key regulator of mRNA translation, is coupled to meiosis completion at egg activation |
| title_fullStr | Control of PNG kinase, a key regulator of mRNA translation, is coupled to meiosis completion at egg activation |
| title_full_unstemmed | Control of PNG kinase, a key regulator of mRNA translation, is coupled to meiosis completion at egg activation |
| title_short | Control of PNG kinase, a key regulator of mRNA translation, is coupled to meiosis completion at egg activation |
| title_sort | control of png kinase a key regulator of mrna translation is coupled to meiosis completion at egg activation |
| topic | egg activation maternal mRNA cell cycle Drosophila |
| url | https://elifesciences.org/articles/22219 |
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