Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition
The onset of development is marked by two major, posttranscriptionally controlled, events: oocyte maturation (release of the prophase I primary arrest) and egg activation (release from the secondary meiotic arrest). Using quantitative mass spectrometry, we previously described proteome remodeling du...
| Main Authors: | , , , , , , |
|---|---|
| Other Authors: | |
| Format: | Article |
| Language: | en_US |
| Published: |
National Academy of Sciences (U.S.)
2015
|
| Online Access: | http://hdl.handle.net/1721.1/96955 https://orcid.org/0000-0002-7934-111X |
| _version_ | 1826188902123175936 |
|---|---|
| author | Kronja, Iva Whitfield, Zachary J. Yuan, Bingbing Dzeyk, Kristina Kirkpatrick, Joanna Krijgsveld, Jeroen Orr-Weaver, Terry |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Kronja, Iva Whitfield, Zachary J. Yuan, Bingbing Dzeyk, Kristina Kirkpatrick, Joanna Krijgsveld, Jeroen Orr-Weaver, Terry |
| author_sort | Kronja, Iva |
| collection | MIT |
| description | The onset of development is marked by two major, posttranscriptionally controlled, events: oocyte maturation (release of the prophase I primary arrest) and egg activation (release from the secondary meiotic arrest). Using quantitative mass spectrometry, we previously described proteome remodeling during Drosophila egg activation. Here, we describe our quantitative mass spectrometry-based analysis of the changes in protein levels during Drosophila oocyte maturation. This study presents the first quantitative survey, to our knowledge, of proteome changes accompanying oocyte maturation in any organism and provides a powerful resource for identifying both key regulators and biological processes driving this critical developmental window. We show that Muskelin, found to be up-regulated during oocyte maturation, is required for timely nurse cell nuclei clearing from mature egg chambers. Other proteins up-regulated at maturation are factors needed not only for late oogenesis but also completion of meiosis and early embryogenesis. Interestingly, the down-regulated proteins are predominantly involved in RNA processing, translation, and RNAi. Integrating datasets on the proteome changes at oocyte maturation and egg activation uncovers dynamics in proteome remodeling during the change from oocyte to embryo. Notably, 66 proteins likely act uniquely during late oogenesis, because they are up-regulated at maturation and down-regulated at activation. We find down-regulation of this class of proteins to be mediated partially by APC/C[superscript CORT], a meiosis-specific form of the E3 ligase anaphase promoting complex/cyclosome (APC/C). |
| first_indexed | 2024-09-23T08:06:46Z |
| format | Article |
| id | mit-1721.1/96955 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T08:06:46Z |
| publishDate | 2015 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/969552022-09-23T10:58:07Z Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition Kronja, Iva Whitfield, Zachary J. Yuan, Bingbing Dzeyk, Kristina Kirkpatrick, Joanna Krijgsveld, Jeroen Orr-Weaver, Terry Massachusetts Institute of Technology. Department of Biology Whitehead Institute for Biomedical Research Whitfield, Zachary J. Orr-Weaver, Terry L. The onset of development is marked by two major, posttranscriptionally controlled, events: oocyte maturation (release of the prophase I primary arrest) and egg activation (release from the secondary meiotic arrest). Using quantitative mass spectrometry, we previously described proteome remodeling during Drosophila egg activation. Here, we describe our quantitative mass spectrometry-based analysis of the changes in protein levels during Drosophila oocyte maturation. This study presents the first quantitative survey, to our knowledge, of proteome changes accompanying oocyte maturation in any organism and provides a powerful resource for identifying both key regulators and biological processes driving this critical developmental window. We show that Muskelin, found to be up-regulated during oocyte maturation, is required for timely nurse cell nuclei clearing from mature egg chambers. Other proteins up-regulated at maturation are factors needed not only for late oogenesis but also completion of meiosis and early embryogenesis. Interestingly, the down-regulated proteins are predominantly involved in RNA processing, translation, and RNAi. Integrating datasets on the proteome changes at oocyte maturation and egg activation uncovers dynamics in proteome remodeling during the change from oocyte to embryo. Notably, 66 proteins likely act uniquely during late oogenesis, because they are up-regulated at maturation and down-regulated at activation. We find down-regulation of this class of proteins to be mediated partially by APC/C[superscript CORT], a meiosis-specific form of the E3 ligase anaphase promoting complex/cyclosome (APC/C). National Institutes of Health (U.S.) (Grant GM39341) 2015-05-11T14:29:37Z 2015-05-11T14:29:37Z 2014-11 2014-07 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/96955 Kronja, Iva, Zachary J. Whitfield, Bingbing Yuan, Kristina Dzeyk, Joanna Kirkpatrick, Jeroen Krijgsveld, and Terry L. Orr-Weaver. “Quantitative Proteomics Reveals the Dynamics of Protein Changes During Drosophila Oocyte Maturation and the Oocyte-to-Embryo Transition.” Proceedings of the National Academy of Sciences 111, no. 45 (October 27, 2014): 16023–16028. https://orcid.org/0000-0002-7934-111X en_US http://dx.doi.org/10.1073/pnas.1418657111 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) National Academy of Sciences (U.S.) |
| spellingShingle | Kronja, Iva Whitfield, Zachary J. Yuan, Bingbing Dzeyk, Kristina Kirkpatrick, Joanna Krijgsveld, Jeroen Orr-Weaver, Terry Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition |
| title | Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition |
| title_full | Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition |
| title_fullStr | Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition |
| title_full_unstemmed | Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition |
| title_short | Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition |
| title_sort | quantitative proteomics reveals the dynamics of protein changes during drosophila oocyte maturation and the oocyte to embryo transition |
| url | http://hdl.handle.net/1721.1/96955 https://orcid.org/0000-0002-7934-111X |
| work_keys_str_mv | AT kronjaiva quantitativeproteomicsrevealsthedynamicsofproteinchangesduringdrosophilaoocytematurationandtheoocytetoembryotransition AT whitfieldzacharyj quantitativeproteomicsrevealsthedynamicsofproteinchangesduringdrosophilaoocytematurationandtheoocytetoembryotransition AT yuanbingbing quantitativeproteomicsrevealsthedynamicsofproteinchangesduringdrosophilaoocytematurationandtheoocytetoembryotransition AT dzeykkristina quantitativeproteomicsrevealsthedynamicsofproteinchangesduringdrosophilaoocytematurationandtheoocytetoembryotransition AT kirkpatrickjoanna quantitativeproteomicsrevealsthedynamicsofproteinchangesduringdrosophilaoocytematurationandtheoocytetoembryotransition AT krijgsveldjeroen quantitativeproteomicsrevealsthedynamicsofproteinchangesduringdrosophilaoocytematurationandtheoocytetoembryotransition AT orrweaverterry quantitativeproteomicsrevealsthedynamicsofproteinchangesduringdrosophilaoocytematurationandtheoocytetoembryotransition |