A Meiosis-Specific Form of the APC/C Promotes the Oocyte-to-Embryo Transition by Decreasing Levels of the Polo Kinase Inhibitor Matrimony
Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to meiosis whose levels must be decreased to begin embryogenesis properly? The Drosophila protein Cortex (Cort) is a female, meiosis-specific activ...
Saved in:
| Published in | PLoS biology Vol. 11; no. 9; p. e1001648 |
|---|---|
| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.09.2013
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1545-7885 1544-9173 1545-7885 |
| DOI | 10.1371/journal.pbio.1001648 |
Cover
| Abstract | Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to meiosis whose levels must be decreased to begin embryogenesis properly? The Drosophila protein Cortex (Cort) is a female, meiosis-specific activator of the Anaphase Promoting Complex/Cyclosome (APC/C), an E3 ubiquitin ligase. We performed immunoprecipitation of Cortex followed by mass spectrometry, and identified the Polo kinase inhibitor Matrimony (Mtrm) as a potential interactor with Cort. In vitro binding assays showed Mtrm and Cort can bind directly. We found Mtrm protein levels to be reduced dramatically during the oocyte-to-embryo transition, and this downregulation did not take place in cort mutant eggs, consistent with Mtrm being a substrate of APC(Cort). We showed that Mtrm is subject to APC(Cort)-mediated proteasomal degradation and have identified a putative APC/C recognition motif in Mtrm that when mutated partially stabilized the protein in the embryo. Furthermore, overexpression of Mtrm in the early embryo caused aberrant nuclear divisions and developmental defects, and these were enhanced by decreasing levels of active Polo. These data indicate APC(Cort) ubiquitylates Mtrm at the oocyte-to-embryo transition, thus preventing excessive inhibition of Polo kinase activity due to Mtrm's presence. |
|---|---|
| AbstractList | Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to meiosis whose levels must be decreased to begin embryogenesis properly? The Drosophila protein Cortex (Cort) is a female, meiosis-specific activator of the Anaphase Promoting Complex/Cyclosome (APC/C), an E3 ubiquitin ligase. We performed immunoprecipitation of Cortex followed by mass spectrometry, and identified the Polo kinase inhibitor Matrimony (Mtrm) as a potential interactor with Cort. In vitro binding assays showed Mtrm and Cort can bind directly. We found Mtrm protein levels to be reduced dramatically during the oocyte-to-embryo transition, and this downregulation did not take place in cort mutant eggs, consistent with Mtrm being a substrate of APC(Cort). We showed that Mtrm is subject to APC(Cort)-mediated proteasomal degradation and have identified a putative APC/C recognition motif in Mtrm that when mutated partially stabilized the protein in the embryo. Furthermore, overexpression of Mtrm in the early embryo caused aberrant nuclear divisions and developmental defects, and these were enhanced by decreasing levels of active Polo. These data indicate APC(Cort) ubiquitylates Mtrm at the oocyte-to-embryo transition, thus preventing excessive inhibition of Polo kinase activity due to Mtrm's presence. Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to meiosis whose levels must be decreased to begin embryogenesis properly? The Drosophila protein Cortex (Cort) is a female, meiosis-specific activator of the Anaphase Promoting Complex/Cyclosome (APC/C), an E3 ubiquitin ligase. We performed immunoprecipitation of Cortex followed by mass spectrometry, and identified the Polo kinase inhibitor Matrimony (Mtrm) as a potential interactor with Cort. In vitro binding assays showed Mtrm and Cort can bind directly. We found Mtrm protein levels to be reduced dramatically during the oocyte-to-embryo transition, and this downregulation did not take place in cort mutant eggs, consistent with Mtrm being a substrate of APC(Cort). We showed that Mtrm is subject to APC(Cort)-mediated proteasomal degradation and have identified a putative APC/C recognition motif in Mtrm that when mutated partially stabilized the protein in the embryo. Furthermore, overexpression of Mtrm in the early embryo caused aberrant nuclear divisions and developmental defects, and these were enhanced by decreasing levels of active Polo. These data indicate APC(Cort) ubiquitylates Mtrm at the oocyte-to-embryo transition, thus preventing excessive inhibition of Polo kinase activity due to Mtrm's presence.Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to meiosis whose levels must be decreased to begin embryogenesis properly? The Drosophila protein Cortex (Cort) is a female, meiosis-specific activator of the Anaphase Promoting Complex/Cyclosome (APC/C), an E3 ubiquitin ligase. We performed immunoprecipitation of Cortex followed by mass spectrometry, and identified the Polo kinase inhibitor Matrimony (Mtrm) as a potential interactor with Cort. In vitro binding assays showed Mtrm and Cort can bind directly. We found Mtrm protein levels to be reduced dramatically during the oocyte-to-embryo transition, and this downregulation did not take place in cort mutant eggs, consistent with Mtrm being a substrate of APC(Cort). We showed that Mtrm is subject to APC(Cort)-mediated proteasomal degradation and have identified a putative APC/C recognition motif in Mtrm that when mutated partially stabilized the protein in the embryo. Furthermore, overexpression of Mtrm in the early embryo caused aberrant nuclear divisions and developmental defects, and these were enhanced by decreasing levels of active Polo. These data indicate APC(Cort) ubiquitylates Mtrm at the oocyte-to-embryo transition, thus preventing excessive inhibition of Polo kinase activity due to Mtrm's presence. Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to meiosis whose levels must be decreased to begin embryogenesis properly? The Drosophila protein Cortex (Cort) is a female, meiosis-specific activator of the Anaphase Promoting Complex/Cyclosome (APC/C), an E3 ubiquitin ligase. We performed immunoprecipitation of Cortex followed by mass spectrometry, and identified the Polo kinase inhibitor Matrimony (Mtrm) as a potential interactor with Cort. In vitro binding assays showed Mtrm and Cort can bind directly. We found Mtrm protein levels to be reduced dramatically during the oocyte-to-embryo transition, and this downregulation did not take place in cort mutant eggs, consistent with Mtrm being a substrate of [APC.sup.Cort]. We showed that Mtrm is subject to APC[C.sub.ort]-mediated proteasomal degradation and have identified a putative APC/C recognition motif in Mtrm that when mutated partially stabilized the protein in the embryo. Furthermore, overexpression of Mtrm in the early embryo caused aberrant nuclear divisions and developmental defects, and these were enhanced by decreasing levels of active Polo. These data indicate [APC.sup.Cort] ubiquitylates Mtrm at the oocyte-to-embryo transition, thus preventing excessive inhibition of Polo kinase activity due to Mtrm's presence. Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to meiosis whose levels must be decreased to begin embryogenesis properly? The Drosophila protein Cortex (Cort) is a female, meiosis-specific activator of the Anaphase Promoting Complex/Cyclosome (APC/C), an E3 ubiquitin ligase. We performed immunoprecipitation of Cortex followed by mass spectrometry, and identified the Polo kinase inhibitor Matrimony (Mtrm) as a potential interactor with Cort. In vitro binding assays showed Mtrm and Cort can bind directly. We found Mtrm protein levels to be reduced dramatically during the oocyte-to-embryo transition, and this downregulation did not take place in cort mutant eggs, consistent with Mtrm being a substrate of APCCort. We showed that Mtrm is subject to APCCort-mediated proteasomal degradation and have identified a putative APC/C recognition motif in Mtrm that when mutated partially stabilized the protein in the embryo. Furthermore, overexpression of Mtrm in the early embryo caused aberrant nuclear divisions and developmental defects, and these were enhanced by decreasing levels of active Polo. These data indicate APCCort ubiquitylates Mtrm at the oocyte-to-embryo transition, thus preventing excessive inhibition of Polo kinase activity due to Mtrm's presence. During the oocyte-to-embryo transition in Drosophila, degradation of the Polo kinase inhibitor, Matrimony, depends on Cortex, a meiosis-specific form of the Anaphase Promoting Complex/Cyclosome that is required for the oocyte's normal transition from meiosis to mitosis. Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to meiosis whose levels must be decreased to begin embryogenesis properly? The Drosophila protein Cortex (Cort) is a female, meiosis-specific activator of the Anaphase Promoting Complex/Cyclosome (APC/C), an E3 ubiquitin ligase. We performed immunoprecipitation of Cortex followed by mass spectrometry, and identified the Polo kinase inhibitor Matrimony (Mtrm) as a potential interactor with Cort. In vitro binding assays showed Mtrm and Cort can bind directly. We found Mtrm protein levels to be reduced dramatically during the oocyte-to-embryo transition, and this downregulation did not take place in cort mutant eggs, consistent with Mtrm being a substrate of APC Cort . We showed that Mtrm is subject to APC Cort -mediated proteasomal degradation and have identified a putative APC/C recognition motif in Mtrm that when mutated partially stabilized the protein in the embryo. Furthermore, overexpression of Mtrm in the early embryo caused aberrant nuclear divisions and developmental defects, and these were enhanced by decreasing levels of active Polo. These data indicate APC Cort ubiquitylates Mtrm at the oocyte-to-embryo transition, thus preventing excessive inhibition of Polo kinase activity due to Mtrm's presence. Despite their many differences, the meiotic and mitotic divisions of the early embryo take place within the same cytoplasmic space. The oocyte-to-embryo transition is the process by which an oocyte, which initially undergoes meiosis, becomes “adapted” to support the rapid mitotic divisions of embryogenesis. This involves fertilization as well as the stockpiling of proteins and mRNA for the transcriptionally silent early embryo. The Anaphase Promoting Complex/Cyclosome (APC/C) is a large protein complex that is active during both mitosis and meiosis and is responsible for targeting certain proteins for degradation. The discovery of the existence of APC/C activators that are present only during meiosis hinted at the possibility that this complex also functions to regulate protein degradation during the oocyte-to-embryo transition. Here we study Cortex, a female- and meiosis-specific activator of the APC/C in the fruit fly Drosophila melanogaster . We find that Cortex activity is necessary for the degradation of Matrimony, a key regulator of female meiosis in Drosophila. Matrimony itself inhibits Polo kinase, another important regulator of both mitosis and meiosis that also functions in chromosome segregation, centrosome dynamics, and cytokinesis. When excess Matrimony protein is not removed from the early embryo, developmental defects arise. Together our findings demonstrate that the precise regulation of Matrimony levels in the egg is necessary for the switch from meiosis to mitosis. |
| Audience | Academic |
| Author | Orr-Weaver, Terry L. Whitfield, Zachary J. Chisholm, Jennifer Hawley, R. Scott |
| AuthorAffiliation | 2 Stowers Institute for Medical Research, Kansas City, Missouri, United States of America Dana-Farber Cancer Institute, United States of America 1 Whitehead Institute, Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America 3 Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas, United States of America |
| AuthorAffiliation_xml | – name: 3 Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas, United States of America – name: 1 Whitehead Institute, Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – name: Dana-Farber Cancer Institute, United States of America – name: 2 Stowers Institute for Medical Research, Kansas City, Missouri, United States of America |
| Author_xml | – sequence: 1 givenname: Zachary J. surname: Whitfield fullname: Whitfield, Zachary J. – sequence: 2 givenname: Jennifer surname: Chisholm fullname: Chisholm, Jennifer – sequence: 3 givenname: R. Scott surname: Hawley fullname: Hawley, R. Scott – sequence: 4 givenname: Terry L. surname: Orr-Weaver fullname: Orr-Weaver, Terry L. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24019759$$D View this record in MEDLINE/PubMed |
| BookMark | eNqVk11v0zAUhiM0xD7gHyCIxA1cpHMSf6RcIFVlg4qOTmzi1rLd485TYhfbnehP4F_jrC1aEUKgXDg6ft7Xx8fnHGcH1lnIsuclGpQ1K09v3cpb0Q6W0rhBiVBJcfMoOyoJJgVrGnLw4P8wOw7hFqGqGlbNk-ywwqgcMjI8yn6M8gswLphQXC1BGW1Ufu58lzudxxvIR5fj03F-6V3nIoT70MypdYQiuuKsk37t8msvbDDROJvLdf4elAcRjF3kU7iDNuysLl3r8k_GigD5xN4YaaLz-YWI3nTOrp9mj7VoAzzbrifZ9fnZ9fhjMZ19mIxH00JRymIhJamGTNcNYjXBohZUQ02pRloySYXSUlFFgAznUGus51BCjSuCiMSk0qw-yV5ubJetC3xbxMBLjCtcl4j2xGRDzJ245cuUnfBr7oTh9wHnF1z4aFQLXDZYIo0QgWE6iykhm7lkiBHUVJhikrzebU9byQ7mCmz0ot0z3d-x5oYv3B2vGUWM9gavtwbefVtBiLwzQUHbCgtu1eddl7SqCOnzfrVBFyKlZqx2yVH1OB_VmJFEUZqowR-o9M2hMyq1mDYpvid4sydITITvcSFWIfDJ1Zf_YD__Ozv7us--eFjGX_Xb9XEC3m4A5V0IHjRXJoq-JdPtTMtLxPuh2b0374eGb4cmifFv4p3_X2U_AeoSG-4 |
| CitedBy_id | crossref_primary_10_1016_j_devcel_2021_06_019 crossref_primary_10_1016_j_celrep_2014_05_002 crossref_primary_10_1016_j_cub_2023_04_028 crossref_primary_10_13070_mm_ru_2_133 crossref_primary_10_13070_mm_fr_3_175 crossref_primary_10_1016_j_cub_2023_07_055 crossref_primary_10_13070_mm_cn_3_175 crossref_primary_10_13070_mm_en_3_175 crossref_primary_10_1038_nature17951 crossref_primary_10_1073_pnas_1418657111 crossref_primary_10_1074_mcp_RA118_001076 crossref_primary_10_1007_s13277_016_4986_1 crossref_primary_10_1016_j_cub_2019_12_027 crossref_primary_10_1016_j_cbd_2019_03_006 crossref_primary_10_1016_j_semcdb_2018_02_019 crossref_primary_10_1093_molbev_msy197 crossref_primary_10_13070_mm_en_2_133 crossref_primary_10_1093_g3journal_jkae066 crossref_primary_10_13070_mm_en_2_117 crossref_primary_10_1534_genetics_117_300081 crossref_primary_10_13070_mm_cn_2_133 crossref_primary_10_18632_oncotarget_15570 crossref_primary_10_3389_fcell_2021_749654 crossref_primary_10_13070_mm_cn_2_117 crossref_primary_10_1038_s41598_017_13755_9 crossref_primary_10_13070_mm_pt_2_133 crossref_primary_10_1002_bies_202000018 crossref_primary_10_1093_g3journal_jkae273 crossref_primary_10_7554_eLife_63368 crossref_primary_10_1038_srep16816 crossref_primary_10_1007_s00018_018_2750_y crossref_primary_10_13070_mm_fr_2_117 crossref_primary_10_1038_nrm3819 crossref_primary_10_1038_onc_2014_451 crossref_primary_10_1534_genetics_113_160556 crossref_primary_10_13070_mm_fr_2_133 crossref_primary_10_7554_eLife_53889 |
| Cites_doi | 10.1101/cshperspect.a005553 10.1091/mbc.E10-04-0360 10.1146/annurev.cellbio.041408.115949 10.1242/dev.117.1.359 10.1371/journal.pgen.0030200 10.1002/dvg.1020130608 10.1242/jcs.109.7.1707 10.1038/ncb2071 10.1371/journal.pgen.1002667 10.1371/journal.pgen.0030202 10.1021/ac0341261 10.1242/jcs.113.18.3341 10.1101/gad.975802 10.1093/genetics/165.2.637 10.1038/nature05696 10.1038/nrc1841 10.1021/ac025747h 10.1016/S0092-8674(03)00202-2 10.1016/j.cub.2004.12.033 10.1002/gene.1017 10.1073/pnas.1301690110 10.1016/j.tcb.2004.07.005 10.1016/j.molcel.2008.02.027 10.1016/j.cell.2012.08.044 10.1073/pnas.172391099 10.1101/gad.989302 10.1038/nature05688 10.1242/dev.116.2.405 10.1038/sj.embor.7400029 10.1083/jcb.201001083 10.1083/jcb.153.4.663 10.1093/genetics/155.4.1831 10.1073/pnas.97.22.11990 10.1016/j.cub.2005.11.063 10.1093/emboj/19.17.4513 10.1038/nrm3132 10.1093/genetics/121.1.101 10.1242/dev.02784 10.1016/j.molcel.2005.04.023 10.1093/genetics/150.1.119 10.1126/science.1228394 10.1074/jbc.M701507200 10.1016/j.molcel.2011.04.022 10.1038/nrm2653 10.1073/pnas.250351297 10.1016/S0960-9822(98)70091-0 10.1016/j.cub.2004.12.020 10.1242/jcs.114.11.2135 10.1083/jcb.200604140 10.1002/j.1460-2075.1994.tb06524.x 10.1002/dvdy.21454 10.1242/dev.124.18.3543 10.1371/journal.pbio.0050323 10.1006/dbio.1994.1256 |
| ContentType | Journal Article |
| Copyright | COPYRIGHT 2013 Public Library of Science 2013 Whitfield et al 2013 Whitfield et al 2013 Whitfield et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Whitfield ZJ, Chisholm J, Hawley RS, Orr-Weaver TL (2013) A Meiosis-Specific Form of the APC/C Promotes the Oocyte-to-Embryo Transition by Decreasing Levels of the Polo Kinase Inhibitor Matrimony. PLoS Biol 11(9): e1001648. doi:10.1371/journal.pbio.1001648 |
| Copyright_xml | – notice: COPYRIGHT 2013 Public Library of Science – notice: 2013 Whitfield et al 2013 Whitfield et al – notice: 2013 Whitfield et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Whitfield ZJ, Chisholm J, Hawley RS, Orr-Weaver TL (2013) A Meiosis-Specific Form of the APC/C Promotes the Oocyte-to-Embryo Transition by Decreasing Levels of the Polo Kinase Inhibitor Matrimony. PLoS Biol 11(9): e1001648. doi:10.1371/journal.pbio.1001648 |
| DBID | AAYXX CITATION CGR CUY CVF ECM EIF NPM IOV ISN ISR 7X8 5PM DOA CZG |
| DOI | 10.1371/journal.pbio.1001648 |
| DatabaseName | CrossRef Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed Gale In Context: Opposing Viewpoints Gale In Context: Canada Gale In Context: Science MEDLINE - Academic PubMed Central (Full Participant titles) DOAJ Directory of Open Access Journals PLoS Biology |
| DatabaseTitle | CrossRef MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) MEDLINE - Academic |
| DatabaseTitleList | MEDLINE MEDLINE - Academic |
| Database_xml | – sequence: 1 dbid: DOA name: DOAJ Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 3 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Biology |
| DocumentTitleAlternate | The APC/C Promotes the Oocyte-to-Embryo Transition |
| EISSN | 1545-7885 |
| ExternalDocumentID | 1442431067 oai_doaj_org_article_b84b0f005e9f4f7cab8db70750824645 PMC3760765 A347522566 24019759 10_1371_journal_pbio_1001648 |
| Genre | Journal Article Research Support, N.I.H., Extramural |
| GeographicLocations | United States |
| GeographicLocations_xml | – name: United States |
| GrantInformation_xml | – fundername: NCI NIH HHS grantid: P30 CA014051 – fundername: NIGMS NIH HHS grantid: GM 39341 – fundername: NIGMS NIH HHS grantid: R01 GM039341 |
| GroupedDBID | --- 123 29O 2WC 36B 53G 5VS 7X7 7XC 88E 8FE 8FH 8FI 8FJ AAFWJ AAUCC AAWOE AAYXX ABDBF ABIVO ABUWG ACGFO ACIHN ACPRK ACUHS ADBBV ADRAZ AEAQA AENEX AEUYN AFKRA AFPKN AFRAH AFXKF AHMBA AKRSQ ALIPV ALMA_UNASSIGNED_HOLDINGS AOIJS ATCPS B0M BAWUL BBNVY BCNDV BENPR BHPHI BPHCQ BVXVI BWKFM CCPQU CITATION CS3 DIK DU5 E3Z EAD EAP EAS EBD EBS EJD EMB EMK EMOBN EPL ESX F5P FPL FYUFA GROUPED_DOAJ GX1 HCIFZ HMCUK HYE IAG IAO IGS IHR IOV ISE ISN ISR ITC KQ8 LK8 M1P M48 M7P O5R O5S OK1 OVT P2P PATMY PHGZM PHGZT PIMPY PQQKQ PROAC PSQYO PYCSY QF4 QN7 RNS RPM SJN SV3 TR2 TUS UKHRP WOW XSB YZZ ~8M .GJ 3V. AGJBV C1A CGR CUY CVF ECM EIF IPNFZ M~E NPM PV9 RIG RZL WOQ YIN PMFND 7X8 PJZUB PPXIY PQGLB PUEGO 5PM AAPBV ABPTK CZG ZA5 |
| ID | FETCH-LOGICAL-c667t-bb5297f3807354a3a6fe366f0fb7b6acfbc6c5e59de3f4fde1e342505b452f73 |
| IEDL.DBID | M48 |
| ISSN | 1545-7885 1544-9173 |
| IngestDate | Sun Oct 01 00:20:31 EDT 2023 Wed Aug 27 01:25:06 EDT 2025 Thu Aug 21 18:20:22 EDT 2025 Fri Sep 05 12:46:57 EDT 2025 Tue Jun 17 22:01:46 EDT 2025 Tue Jun 10 21:02:05 EDT 2025 Fri Jun 27 05:31:34 EDT 2025 Fri Jun 27 05:31:19 EDT 2025 Fri Jun 27 05:30:05 EDT 2025 Wed Feb 19 02:31:15 EST 2025 Thu Apr 24 23:03:23 EDT 2025 Tue Jul 01 00:57:37 EDT 2025 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 9 |
| Keywords | Anaphase-Promoting Complex-Cyclosome Cell Line Drosophila Proteins Down-Regulation Protein-Serine-Threonine Kinases Meiosis Embryonic Development Oocytes Animals Gene Expression Regulation, Developmental Protein Binding Female Cdc20 Proteins Drosophila melanogaster Cell Cycle Proteins |
| Language | English |
| License | This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. Creative Commons Attribution License |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c667t-bb5297f3807354a3a6fe366f0fb7b6acfbc6c5e59de3f4fde1e342505b452f73 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: ZJW TOW. Performed the experiments: ZJW JC. Analyzed the data: ZJW TOW. Contributed reagents/materials/analysis tools: RSH. Wrote the paper: ZJW TOW. The authors have declared that no competing interests exist. |
| OpenAccessLink | http://journals.scholarsportal.info/openUrl.xqy?doi=10.1371/journal.pbio.1001648 |
| PMID | 24019759 |
| PQID | 1431622557 |
| PQPubID | 23479 |
| ParticipantIDs | plos_journals_1442431067 doaj_primary_oai_doaj_org_article_b84b0f005e9f4f7cab8db70750824645 pubmedcentral_primary_oai_pubmedcentral_nih_gov_3760765 proquest_miscellaneous_1431622557 gale_infotracmisc_A347522566 gale_infotracacademiconefile_A347522566 gale_incontextgauss_ISR_A347522566 gale_incontextgauss_ISN_A347522566 gale_incontextgauss_IOV_A347522566 pubmed_primary_24019759 crossref_citationtrail_10_1371_journal_pbio_1001648 crossref_primary_10_1371_journal_pbio_1001648 |
| ProviderPackageCode | CITATION AAYXX |
| PublicationCentury | 2000 |
| PublicationDate | 2013-09-01 |
| PublicationDateYYYYMMDD | 2013-09-01 |
| PublicationDate_xml | – month: 09 year: 2013 text: 2013-09-01 day: 01 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: San Francisco, USA |
| PublicationTitle | PLoS biology |
| PublicationTitleAlternate | PLoS Biol |
| PublicationYear | 2013 |
| Publisher | Public Library of Science Public Library of Science (PLoS) |
| Publisher_xml | – name: Public Library of Science – name: Public Library of Science (PLoS) |
| References | MA Blanco (ref22) 2001; 114 ML Stitzel (ref6) 2006; 16 N Furuno (ref13) 1994; 13 M Iwabuchi (ref14) 2000; 19 E Harms (ref34) 2000; 155 AM Bonner (ref38) 2013; 110 R Wolthuis (ref30) 2008; 30 GJ Gutierrez (ref52) 2010; 12 BH Lee (ref11) 2002; 16 GS Tan (ref41) 2011; 22 LA Gross (ref55) 2000; 97 C Courtot (ref45) 1992; 116 T Nishiyama (ref18) 2007; 446 V Archambault (ref37) 2007; 3 JR Von Stetina (ref1) 2011; 3 EF Joyce (ref56) 2012; 8 D Inoue (ref17) 2007; 446 C Kraft (ref29) 2005; 18 T Schupbach (ref33) 1989; 121 T Chu (ref24) 2001; 29 IA Dawson (ref47) 1993; 117 A Swan (ref25) 2007; 134 JA Pesin (ref23) 2007; 3 ref49 BH Reed (ref44) 1997; 124 K Strebhardt (ref40) 2006; 6 M Van Doren (ref48) 1998; 8 MR Dow (ref7) 1998; 150 JA Pesin (ref20) 2008; 24 T Tischer (ref16) 2012; 338 AI Nesvizhskii (ref51) 2003; 75 KF Cooper (ref21) 2000; 97 V Archambault (ref39) 2009; 10 A Williamson (ref54) 2011; 42 BH Lee (ref9) 2004; 14 G Schatten (ref3) 1994; 165 S Quintin (ref5) 2003; 4 JRV Von Stetina (ref32) 2011; 1 MM Donaldson (ref46) 2001; 153 E Okaz (ref42) 2012; 151 C DeRenzo (ref4) 2004; 14 B Di Fiore (ref31) 2010; 190 MA Shonn (ref12) 2002; 16 M Sullivan (ref10) 2007; 282 J Pines (ref19) 2011; 12 S Madgwick (ref15) 2006; 174 VL Katis (ref8) 2004; 14 Y Xiang (ref28) 2007; 5 RS Hawley (ref57) 1992; 13 MG Riparbelli (ref35) 2000; 113 D Harris (ref27) 2003; 165 DW Buster (ref53) 2010; 40 S Takada (ref36) 2003; 113 H Kashevsky (ref43) 2002; 99 A Keller (ref50) 2002; 74 VL Horner (ref2) 2008; 237 AW Page (ref26) 1996; 109 |
| References_xml | – volume: 3 start-page: a005553 year: 2011 ident: ref1 article-title: Developmental control of oocyte maturation and egg activation in metazoan models publication-title: Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a005553 – volume: 22 start-page: 315 year: 2011 ident: ref41 article-title: Ama1p-activated anaphase-promoting complex regulates the destruction of Cdc20p during meiosis II publication-title: Mol Biol Cell doi: 10.1091/mbc.E10-04-0360 – volume: 24 start-page: 475 year: 2008 ident: ref20 article-title: Regulation of APC/C activators in mitosis and meiosis publication-title: Ann Rev Cell Dev Biol doi: 10.1146/annurev.cellbio.041408.115949 – volume: 117 start-page: 359 year: 1993 ident: ref47 article-title: Mutations of the fizzy locus cause metaphase arrest in Drosophila melanogaster embryos publication-title: Development doi: 10.1242/dev.117.1.359 – volume: 3 start-page: e200 year: 2007 ident: ref37 article-title: Mutations in Drosophila Greatwall/Scant reveal its roles in mitosis and meiosis and interdependence with Polo kinase publication-title: PLoS Genetics doi: 10.1371/journal.pgen.0030200 – volume: 13 start-page: 440 year: 1992 ident: ref57 article-title: There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology publication-title: Dev Genet doi: 10.1002/dvg.1020130608 – volume: 109 start-page: 1707 year: 1996 ident: ref26 article-title: The Drosophila genes grauzone and cortex are necessary for proper female meiosis publication-title: J Cell Sci doi: 10.1242/jcs.109.7.1707 – volume: 12 start-page: 686 year: 2010 ident: ref52 article-title: Interplay between Cdh1 and JNK activity during the cell cycle publication-title: Nat Cell Biol doi: 10.1038/ncb2071 – volume: 8 start-page: e1002667 year: 2012 ident: ref56 article-title: Identification of genes that promote or antagonize somatic homolog pairing using a high-throughput FISH-based screen publication-title: PLoS Genet doi: 10.1371/journal.pgen.1002667 – volume: 3 start-page: e202 year: 2007 ident: ref23 article-title: Developmental Role and Regulation of cortex, a Meiosis-Specific Anaphase-Promoting Complex/Cyclosome Activator publication-title: PLoS Genetics doi: 10.1371/journal.pgen.0030202 – volume: 75 start-page: 4646 year: 2003 ident: ref51 article-title: A statistical model for identifying proteins by tandem mass spectrometry publication-title: Anal Chem doi: 10.1021/ac0341261 – volume: 113 start-page: 3341 year: 2000 ident: ref35 article-title: Failure of pronuclear migration and repeated divisions of polar body nuclei associated with MTOC defects in polo eggs of Drosophila publication-title: J Cell Sci doi: 10.1242/jcs.113.18.3341 – volume: 16 start-page: 1659 year: 2002 ident: ref12 article-title: Spo13 protects meiotic cohesin at centromeres in meiosis I publication-title: Genes Dev doi: 10.1101/gad.975802 – volume: 165 start-page: 637 year: 2003 ident: ref27 article-title: A deficiency screen of the major autosomes identifies a gene (matrimony) that is haplo-insufficient for achiasmate segregation in Drosophila oocytes publication-title: Genetics doi: 10.1093/genetics/165.2.637 – volume: 446 start-page: 1096 year: 2007 ident: ref18 article-title: Phosphorylation of Erp1 by p90rsk is required for cytostatic factor arrest in Xenopus laevis eggs publication-title: Nature doi: 10.1038/nature05696 – volume: 6 start-page: 321 year: 2006 ident: ref40 article-title: Targeting polo-like kinase 1 for cancer therapy publication-title: Nat Rev Cancer doi: 10.1038/nrc1841 – volume: 74 start-page: 5383 year: 2002 ident: ref50 article-title: Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search publication-title: Anal Chem doi: 10.1021/ac025747h – volume: 113 start-page: 87 year: 2003 ident: ref36 article-title: Drosophila Checkpoint Kinase 2 couples centrosome function and spindle assembly to genomic integrity publication-title: Cell doi: 10.1016/S0092-8674(03)00202-2 – volume: 14 start-page: 2168 year: 2004 ident: ref9 article-title: Spo13 maintains centromeric cohesion and kinetochore coorientation during meiosis I publication-title: Curr Biol doi: 10.1016/j.cub.2004.12.033 – volume: 40 start-page: e1982 year: 2010 ident: ref53 article-title: Preparation of Drosophila S2 cells for light microscopy publication-title: J Vis Exp – volume: 29 start-page: 141 year: 2001 ident: ref24 article-title: Cortex, a Drosophila gene required to complete oocyte meiosis, is a member of the Cdc20/fizzy protein family publication-title: Genesis doi: 10.1002/gene.1017 – volume: 110 start-page: E1222 year: 2013 ident: ref38 article-title: Binding of Drosophila Polo kinase to its regulator Matrimony is noncanonical and involves two separate functional domains publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.1301690110 – volume: 14 start-page: 420 year: 2004 ident: ref4 article-title: A clean start: degradation of maternal proteins at the oocyte-to-embryo transition publication-title: Trends Cell Biol doi: 10.1016/j.tcb.2004.07.005 – volume: 30 start-page: 290 year: 2008 ident: ref30 article-title: Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A publication-title: Mol Cell doi: 10.1016/j.molcel.2008.02.027 – volume: 151 start-page: 603 year: 2012 ident: ref42 article-title: Meiotic prophase requires proteolysis of M phase regulators mediated by the meiosis-specific APC/C(Ama1) publication-title: Cell doi: 10.1016/j.cell.2012.08.044 – volume: 99 start-page: 11217 year: 2002 ident: ref43 article-title: The anaphase promoting complex/cyclosome is required during development for modified cell cycles publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.172391099 – volume: 16 start-page: 1672 year: 2002 ident: ref11 article-title: Spo13 regulates cohesin cleavage publication-title: Genes Dev doi: 10.1101/gad.989302 – volume: 446 start-page: 1100 year: 2007 ident: ref17 article-title: A direct link of the Mos-MAPK pathway to Erp1/Emi2 in meiotic arrest of Xenopus laevis eggs publication-title: Nature doi: 10.1038/nature05688 – volume: 116 start-page: 405 year: 1992 ident: ref45 article-title: The Drosophila cdc25 homolog twine is required for meiosis publication-title: Development doi: 10.1242/dev.116.2.405 – volume: 4 start-page: 1175 year: 2003 ident: ref5 article-title: The mbk-2 kinase is required for inactivation of MEI-1/katanin in the one-cell Caenorhabditis elegans embryo publication-title: EMBO Rep doi: 10.1038/sj.embor.7400029 – volume: 190 start-page: 501 year: 2010 ident: ref31 article-title: How cyclin A destruction escapes the spindle assembly checkpoint publication-title: J Cell Biol doi: 10.1083/jcb.201001083 – volume: 153 start-page: 663 year: 2001 ident: ref46 article-title: Metaphase arrest with centromere separation in polo mutants of Drosophila publication-title: J Cell Biol doi: 10.1083/jcb.153.4.663 – volume: 155 start-page: 1831 year: 2000 ident: ref34 article-title: The only function of Grauzone required for Drosophila oocyte meiosis is transcriptional activation of the cortex gene publication-title: Genetics doi: 10.1093/genetics/155.4.1831 – volume: 97 start-page: 11990 year: 2000 ident: ref55 article-title: The structure of the chromophore within DsRed, a red fluorescent protein from coral publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.97.22.11990 – volume: 16 start-page: 56 year: 2006 ident: ref6 article-title: The C. elegans DYRK kinase MBK-2 marks oocyte proteins for degradation in response to meiotic maturation publication-title: Curr Biol doi: 10.1016/j.cub.2005.11.063 – volume: 19 start-page: 4513 year: 2000 ident: ref14 article-title: Residual Cdc2 activity remaining at meiosis I exit is essential for meiotic M-M transition in Xenopus oocyte extracts publication-title: EMBO J doi: 10.1093/emboj/19.17.4513 – volume: 12 start-page: 427 year: 2011 ident: ref19 article-title: Cubism and the cell cycle: the many faces of the APC/C publication-title: Nature Reviews Mol Cell Biol doi: 10.1038/nrm3132 – volume: 121 start-page: 101 year: 1989 ident: ref33 article-title: Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations publication-title: Genetics doi: 10.1093/genetics/121.1.101 – volume: 134 start-page: 891 year: 2007 ident: ref25 article-title: The Cdc20 (Fzy)/Cdh1-related protein, Cort, cooperates with Fzy in cyclin destruction and anaphase progression in meiosis I and II in Drosophila publication-title: Development doi: 10.1242/dev.02784 – volume: 18 start-page: 543 year: 2005 ident: ref29 article-title: The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates publication-title: Molecular Cell doi: 10.1016/j.molcel.2005.04.023 – volume: 150 start-page: 119 year: 1998 ident: ref7 article-title: Genetic and molecular characterization of the Caenorhabditis elegans gene, mel-26, a postmeiotic negative regulator of MEI-1, a meiotic-specific spindle component publication-title: Genetics doi: 10.1093/genetics/150.1.119 – volume: 338 start-page: 520 year: 2012 ident: ref16 article-title: The APC/C inhibitor XErp1/Emi2 is essential for Xenopus early embryonic divisions publication-title: Science doi: 10.1126/science.1228394 – volume: 282 start-page: 19710 year: 2007 ident: ref10 article-title: A novel destruction sequence targets the meiotic regulator Spo13 for anaphase-promoting complex-dependent degradation in anaphase I publication-title: J Biol Chem doi: 10.1074/jbc.M701507200 – volume: 42 start-page: 744 year: 2011 ident: ref54 article-title: Regulation of ubiquitin chain initiation to control the timing of substrate degradation publication-title: Mol Cell doi: 10.1016/j.molcel.2011.04.022 – volume: 1 start-page: 1 year: 2011 ident: ref32 article-title: A genetic screen for dominant enhancers of the cell-cycle regulator α-endosulfine identifies Matrimony as a strong functional interactor in Drosophila publication-title: G3 – volume: 10 start-page: 265 year: 2009 ident: ref39 article-title: Polo-like kinases: conservation and divergence in their functions and regulation publication-title: Nat Rev Mol Cell Biol doi: 10.1038/nrm2653 – volume: 97 start-page: 14548 year: 2000 ident: ref21 article-title: Ama1p is a meiosis-specific regulator of the anaphase promoting complex/cyclosome in yeast publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.250351297 – volume: 8 start-page: 243 year: 1998 ident: ref48 article-title: Regulation of zygotic gene expression in Drosophila primordial germ cells publication-title: Curr Biol doi: 10.1016/S0960-9822(98)70091-0 – volume: 14 start-page: 2183 year: 2004 ident: ref8 article-title: Spo13 facilitates monopolin recruitment to kinetochores and regulates maintenance of centromeric cohesion during yeast meiosis publication-title: Curr Biol doi: 10.1016/j.cub.2004.12.020 – volume: 114 start-page: 2135 year: 2001 ident: ref22 article-title: Fission yeast mfr1 activates APC and coordinates meiotic nuclear division with sporulation publication-title: J Cell Sci doi: 10.1242/jcs.114.11.2135 – volume: 174 start-page: 791 year: 2006 ident: ref15 article-title: Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis publication-title: J Cell Biol doi: 10.1083/jcb.200604140 – volume: 13 start-page: 2399 year: 1994 ident: ref13 article-title: Suppression of DNA replication via Mos function during meiotic divisions in Xenopus oocytes publication-title: EMBO J doi: 10.1002/j.1460-2075.1994.tb06524.x – ident: ref49 – volume: 237 start-page: 527 year: 2008 ident: ref2 article-title: Transitioning from egg to embryo: triggers and mechanisms of egg activation publication-title: Developmental dynamics doi: 10.1002/dvdy.21454 – volume: 124 start-page: 3543 year: 1997 ident: ref44 article-title: The Drosophila gene morula inhibits mitotic functions in the endo cell cycle and the mitotic cell cycle publication-title: Development doi: 10.1242/dev.124.18.3543 – volume: 5 start-page: e323 year: 2007 ident: ref28 article-title: The inhibition of Polo kinase by Matrimony maintains G2 arrest in the meiotic cell cycle publication-title: PLoS Biology doi: 10.1371/journal.pbio.0050323 – volume: 165 start-page: 299 year: 1994 ident: ref3 article-title: The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization publication-title: Dev Biol doi: 10.1006/dbio.1994.1256 |
| SSID | ssj0022928 |
| Score | 2.248967 |
| Snippet | Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to... During the oocyte-to-embryo transition in Drosophila, degradation of the Polo kinase inhibitor, Matrimony, depends on Cortex, a meiosis-specific form of the... Oocytes are stockpiled with proteins and mRNA that are required to drive the initial mitotic divisions of embryogenesis. But are there proteins specific to... |
| SourceID | plos doaj pubmedcentral proquest gale pubmed crossref |
| SourceType | Open Website Open Access Repository Aggregation Database Index Database Enrichment Source |
| StartPage | e1001648 |
| SubjectTerms | Anaphase-Promoting Complex-Cyclosome - genetics Anaphase-Promoting Complex-Cyclosome - metabolism Animals Biology Cdc20 Proteins - metabolism Cell cycle Cell Cycle Proteins - biosynthesis Cell Cycle Proteins - metabolism Cell Line Down-Regulation Drosophila melanogaster - embryology Drosophila melanogaster - genetics Drosophila Proteins - antagonists & inhibitors Drosophila Proteins - biosynthesis Drosophila Proteins - metabolism Eggs Embryonic development Embryonic Development - genetics Experiments Female Gene Expression Regulation, Developmental Insects Kinases Mass spectrometry Meiosis Molecular weight Oocytes Oocytes - metabolism Phosphotransferases Physiological aspects Protein Binding Protein-Serine-Threonine Kinases - antagonists & inhibitors Protein-Serine-Threonine Kinases - metabolism Proteins Sperm |
| SummonAdditionalLinks | – databaseName: DOAJ Directory of Open Access Journals dbid: DOA link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Nj9MwELVQJSQuiO8tLMggJE6mSZzY8bFUrBYklhUsaG9RnNi7EW1cNekhP4F_zYyTVg0CLQeuyXOrzkxmnpvxG0Jep6Isg8DkTOmYM9h_WaatDplWxqQ24Tr2p1w_nYnTb_HHy-TyYNQX9oT18sC94WY6jXVgIVaMsrGVRa7TUkssdGmEb-Uw-wYq2G2mhq1WpPxUVZSagcdZ8uHQHJfhbPDR27WunFcgEjj756Aoee3-fYaerJeu-RP9_L2L8qAsndwjdwc-Sef977hPbpn6AbndT5jsHpKfc7oylWuqhuGZSuwLokhTqbMUqB-dny9mC7r2PXmm8ZecK7rWsNYxs9KbztEWy5nv7KK6o6XnmfgPA11iw1Gz-6hz-Er6o6qhLNKqvq405IoNXeEIAAj17hG5OHl_sThlw_QFVgghW6Z1EilpUZCeJ3HOc2ENF8IGVkst8sLqQhSJSVRpOHimNKHhMRIqHSeRlfwxmdSuNkeEGpXnIeTRsMxVHBWRtioNbcFDa0yoknJK-M76WTEok-OAjGXmX7dJ2KH0xszQZ9ngsylh-1XrXpnjBvw7dOwei7ra_gJEWzZEW3ZTtE3JKwyLDJUzamzNucq3TZN9-Pw9m_NYApkFevw30NezfwF9GYHeDCDrwCJFPpyZALuibNcIeTxCQpIoRrePMI53hmlgxxdHwB2Bq0zJy11sZ7gKm-5q47aI4aGA5QlgnvSxvrceEMFQyURNiRw9BSPzju_U1bWXL8c2LCmSp__DH8_IncjPJ8Gmv2MyaTdb8xxYYqtf-ITwC_xHZuA priority: 102 providerName: Directory of Open Access Journals |
| Title | A Meiosis-Specific Form of the APC/C Promotes the Oocyte-to-Embryo Transition by Decreasing Levels of the Polo Kinase Inhibitor Matrimony |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/24019759 https://www.proquest.com/docview/1431622557 https://pubmed.ncbi.nlm.nih.gov/PMC3760765 https://doaj.org/article/b84b0f005e9f4f7cab8db70750824645 http://dx.doi.org/10.1371/journal.pbio.1001648 |
| Volume | 11 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3db9MwELe2Tki8THyvMCqDkHjKaGLHjh8Q6kqrjdGujA31LYode4tUktJ0EvkT-K85u2lF0Cp4yUPyu3ycz-ef4_MdQm8ilqbdrk48ISnxYP5lPGmk70mhdWRCIqnb5Toas5Mr-mkaTnfQumZrrcDyzqmdrSd1tZgd_fxRfYAO_95VbeD-WuhoLrPC5RRiNNpFe27FyAbz0c26QhCIIKo30G2TbAxQLo__xlu35rOivIuK_h1R-ccQNXyA9mtuiXsrY3iIdnT-CN1bVZusHqNfPTzSWVFmpeeqzptM4SFQVlwYDDQQ9yb9d308cfF5unSnzgtVLbW3LLzBd7moCuyGNhflhWWFPzrOaf824M82-Khc32oCj8RnWQ5DJD7NbzIJfmOBR7YcAJh99QRdDgeX_ROvrsTgKcb40pMyDAQ3Njk9CWlCEmY0Ycx0jeSSJcpIxVSoQ5FqYqhJta8JteRK0jAwnDxFrbzI9QHCWiSJDz7VTxNBAxVIIyLfKOIbrX0Rpm1E1tqPVZ2l3BbLmMVu6Y3DbGWlzNi2WVy3WRt5G6n5KkvHP_DHtmE3WJtj250oFtdx3WVjGVHZNeCltIBv4iqRUSq5pVhRYNeD2-i1NYvYZtHIbZjOdXJblvHp-be4RygHYgtUeRvo6_h_QBcN0NsaZArQiErq_ROgV5vCq4E8bCDBYajG5QNrx2vFlDD7owHwSOAtbfRqbduxlbIBeLkubi2G-AzEQ8A8W9n6RntACn3BQ9FGvNELGuptXsmzG5fK3IZkcRY-3_5KL9D9wFUgsWF9h6i1XNzql8ADl7KDdvmUd9De8WA8uei4vylwPPsSdVyn_w2-nWOg |
| linkProvider | Scholars Portal |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=A+Meiosis-Specific+Form+of+the+APC%2FC+Promotes+the+Oocyte-to-Embryo+Transition+by+Decreasing+Levels+of+the+Polo+Kinase+Inhibitor+Matrimony&rft.jtitle=PLoS+biology&rft.au=Whitfield%2C+Zachary&rft.au=Chisholm%2C+Jennifer&rft.au=Hawley%2C+R&rft.au=Orr-Weaver%2C+Terry&rft.date=2013-09-01&rft.pub=Public+Library+of+Science&rft.eissn=1545-7885&rft.volume=11&rft.issue=9&rft_id=info:doi/10.1371%2Fjournal.pbio.1001648&rft.externalDocID=1442431067 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1545-7885&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1545-7885&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1545-7885&client=summon |