mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos
Because maturing oocytes and early embryos lack appreciable transcription, posttranscriptional regulatory processes control their development. To better understand this control, we profiled translational efficiencies and poly(A)-tail lengths throughout Drosophila oocyte maturation and early embryoni...
| Main Authors: | , , , , , |
|---|---|
| Other Authors: | |
| Format: | Article |
| Language: | en_US |
| Published: |
eLife Sciences Publications, Ltd.
2017
|
| Online Access: | http://hdl.handle.net/1721.1/106506 https://orcid.org/0000-0002-6410-4699 https://orcid.org/0000-0001-5029-5909 https://orcid.org/0000-0002-7934-111X https://orcid.org/0000-0002-3872-2856 |
| _version_ | 1811085392262201344 |
|---|---|
| author | Eichhorn, Stephen William Subtelny, Alexander Orest Orr-Weaver, Terry Bartel, David Kronja, Iva Kwasnieski, Jamie C. |
| author2 | Harvard University--MIT Division of Health Sciences and Technology |
| author_facet | Harvard University--MIT Division of Health Sciences and Technology Eichhorn, Stephen William Subtelny, Alexander Orest Orr-Weaver, Terry Bartel, David Kronja, Iva Kwasnieski, Jamie C. |
| author_sort | Eichhorn, Stephen William |
| collection | MIT |
| description | Because maturing oocytes and early embryos lack appreciable transcription, posttranscriptional regulatory processes control their development. To better understand this control, we profiled translational efficiencies and poly(A)-tail lengths throughout Drosophila oocyte maturation and early embryonic development. The correspondence between translational-efficiency changes and tail-length changes indicated that tail-length changes broadly regulate translation until gastrulation, when this coupling disappears. During egg activation, relative changes in poly(A)-tail length, and thus translational efficiency, were largely retained in the absence of cytoplasmic polyadenylation, which indicated that selective poly(A)-tail shortening primarily specifies these changes. Many translational changes depended on PAN GU and Smaug, and these changes were largely attributable to tail-length changes. Our results also revealed the presence of tail-length–independent mechanisms that maintained translation despite tail-length shortening during oocyte maturation, and prevented essentially all translation of bicoid and several other mRNAs before egg activation. In addition to these fundamental insights, our results provide valuable resources for future studies. |
| first_indexed | 2024-09-23T13:08:51Z |
| format | Article |
| id | mit-1721.1/106506 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T13:08:51Z |
| publishDate | 2017 |
| publisher | eLife Sciences Publications, Ltd. |
| record_format | dspace |
| spelling | mit-1721.1/1065062022-10-01T13:20:00Z mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos Eichhorn, Stephen William Subtelny, Alexander Orest Orr-Weaver, Terry Bartel, David Kronja, Iva Kwasnieski, Jamie C. Harvard University--MIT Division of Health Sciences and Technology Massachusetts Institute of Technology. Department of Biology Whitehead Institute for Biomedical Research Eichhorn, Stephen William Subtelny, Alexander Orest Orr-Weaver, Terry Bartel, David Kronja, Iva Kwasnieski, Jamie C. Because maturing oocytes and early embryos lack appreciable transcription, posttranscriptional regulatory processes control their development. To better understand this control, we profiled translational efficiencies and poly(A)-tail lengths throughout Drosophila oocyte maturation and early embryonic development. The correspondence between translational-efficiency changes and tail-length changes indicated that tail-length changes broadly regulate translation until gastrulation, when this coupling disappears. During egg activation, relative changes in poly(A)-tail length, and thus translational efficiency, were largely retained in the absence of cytoplasmic polyadenylation, which indicated that selective poly(A)-tail shortening primarily specifies these changes. Many translational changes depended on PAN GU and Smaug, and these changes were largely attributable to tail-length changes. Our results also revealed the presence of tail-length–independent mechanisms that maintained translation despite tail-length shortening during oocyte maturation, and prevented essentially all translation of bicoid and several other mRNAs before egg activation. In addition to these fundamental insights, our results provide valuable resources for future studies. Alexander von Humboldt Foundation (Feodor Lynen Postdoctoral Fellowship) National Science Foundation (U.S.) (Grants GM39341, GM118098, and GM067031) National Institutes of Health (U.S.) (Medical Scientist Training Program Fellowship T32GM007753) 2017-01-17T16:03:25Z 2017-01-17T16:03:25Z 2016-07 2016-04 Article http://purl.org/eprint/type/JournalArticle 2050-084X http://hdl.handle.net/1721.1/106506 Eichhorn, Stephen W et al. “mRNA poly(A)-Tail Changes Specified by Deadenylation Broadly Reshape Translation in Drosophila Oocytes and Early Embryos.” eLife 5 (2016): n. pag. https://orcid.org/0000-0002-6410-4699 https://orcid.org/0000-0001-5029-5909 https://orcid.org/0000-0002-7934-111X https://orcid.org/0000-0002-3872-2856 en_US http://dx.doi.org/10.7554/eLife.16955 eLife Creative Commons Attribution 4.0 International License http://creativecommons.org/licenses/by/4.0/ application/pdf eLife Sciences Publications, Ltd. eLife |
| spellingShingle | Eichhorn, Stephen William Subtelny, Alexander Orest Orr-Weaver, Terry Bartel, David Kronja, Iva Kwasnieski, Jamie C. mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos |
| title | mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos |
| title_full | mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos |
| title_fullStr | mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos |
| title_full_unstemmed | mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos |
| title_short | mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos |
| title_sort | mrna poly a tail changes specified by deadenylation broadly reshape translation in drosophila oocytes and early embryos |
| url | http://hdl.handle.net/1721.1/106506 https://orcid.org/0000-0002-6410-4699 https://orcid.org/0000-0001-5029-5909 https://orcid.org/0000-0002-7934-111X https://orcid.org/0000-0002-3872-2856 |
| work_keys_str_mv | AT eichhornstephenwilliam mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos AT subtelnyalexanderorest mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos AT orrweaverterry mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos AT barteldavid mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos AT kronjaiva mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos AT kwasnieskijamiec mrnapolyatailchangesspecifiedbydeadenylationbroadlyreshapetranslationindrosophilaoocytesandearlyembryos |