Maternal regulation of the vertebrate oocyte-to-embryo transition.
Maternally-loaded factors in the egg accumulate during oogenesis and are essential for the acquisition of oocyte and egg developmental competence to ensure the production of viable embryos. However, their molecular nature and functional importance remain poorly understood. Here, we present a collect...
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2024-07-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1011343 |
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| author | Ricardo Fuentes Florence L Marlow Elliott W Abrams Hong Zhang Manami Kobayashi Tripti Gupta Lee D Kapp Zachary DiNardo Ronald Heller Ruth Cisternas Priscila García-Castro Fabián Segovia-Miranda Felipe Montecinos-Franjola William Vought Charles E Vejnar Antonio J Giraldez Mary C Mullins |
| author_facet | Ricardo Fuentes Florence L Marlow Elliott W Abrams Hong Zhang Manami Kobayashi Tripti Gupta Lee D Kapp Zachary DiNardo Ronald Heller Ruth Cisternas Priscila García-Castro Fabián Segovia-Miranda Felipe Montecinos-Franjola William Vought Charles E Vejnar Antonio J Giraldez Mary C Mullins |
| author_sort | Ricardo Fuentes |
| collection | DOAJ |
| description | Maternally-loaded factors in the egg accumulate during oogenesis and are essential for the acquisition of oocyte and egg developmental competence to ensure the production of viable embryos. However, their molecular nature and functional importance remain poorly understood. Here, we present a collection of 9 recessive maternal-effect mutants identified in a zebrafish forward genetic screen that reveal unique molecular insights into the mechanisms controlling the vertebrate oocyte-to-embryo transition. Four genes, over easy, p33bjta, poached and black caviar, were found to control initial steps in yolk globule sizing and protein cleavage during oocyte maturation that act independently of nuclear maturation. The krang, kazukuram, p28tabj, and spotty genes play distinct roles in egg activation, including cortical granule biology, cytoplasmic segregation, the regulation of microtubule organizing center assembly and microtubule nucleation, and establishing the basic body plan. Furthermore, we cloned two of the mutant genes, identifying the over easy gene as a subunit of the Adaptor Protein complex 5, Ap5m1, which implicates it in regulating intracellular trafficking and yolk vesicle formation. The novel maternal protein Krang/Kiaa0513, highly conserved in metazoans, was discovered and linked to the function of cortical granules during egg activation. These mutant genes represent novel genetic entry points to decipher the molecular mechanisms functioning in the oocyte-to-embryo transition, fertility, and human disease. Additionally, our genetic adult screen not only contributes to the existing knowledge in the field but also sets the basis for future investigations. Thus, the identified maternal genes represent key players in the coordination and execution of events prior to fertilization. |
| format | Article |
| id | doaj-art-7b554f9630d24ed5ab8a433a491aeb11 |
| institution | OA Journals |
| issn | 1553-7390 1553-7404 |
| language | English |
| publishDate | 2024-07-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj-art-7b554f9630d24ed5ab8a433a491aeb112025-08-20T01:49:27ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042024-07-01207e101134310.1371/journal.pgen.1011343Maternal regulation of the vertebrate oocyte-to-embryo transition.Ricardo FuentesFlorence L MarlowElliott W AbramsHong ZhangManami KobayashiTripti GuptaLee D KappZachary DiNardoRonald HellerRuth CisternasPriscila García-CastroFabián Segovia-MirandaFelipe Montecinos-FranjolaWilliam VoughtCharles E VejnarAntonio J GiraldezMary C MullinsMaternally-loaded factors in the egg accumulate during oogenesis and are essential for the acquisition of oocyte and egg developmental competence to ensure the production of viable embryos. However, their molecular nature and functional importance remain poorly understood. Here, we present a collection of 9 recessive maternal-effect mutants identified in a zebrafish forward genetic screen that reveal unique molecular insights into the mechanisms controlling the vertebrate oocyte-to-embryo transition. Four genes, over easy, p33bjta, poached and black caviar, were found to control initial steps in yolk globule sizing and protein cleavage during oocyte maturation that act independently of nuclear maturation. The krang, kazukuram, p28tabj, and spotty genes play distinct roles in egg activation, including cortical granule biology, cytoplasmic segregation, the regulation of microtubule organizing center assembly and microtubule nucleation, and establishing the basic body plan. Furthermore, we cloned two of the mutant genes, identifying the over easy gene as a subunit of the Adaptor Protein complex 5, Ap5m1, which implicates it in regulating intracellular trafficking and yolk vesicle formation. The novel maternal protein Krang/Kiaa0513, highly conserved in metazoans, was discovered and linked to the function of cortical granules during egg activation. These mutant genes represent novel genetic entry points to decipher the molecular mechanisms functioning in the oocyte-to-embryo transition, fertility, and human disease. Additionally, our genetic adult screen not only contributes to the existing knowledge in the field but also sets the basis for future investigations. Thus, the identified maternal genes represent key players in the coordination and execution of events prior to fertilization.https://doi.org/10.1371/journal.pgen.1011343 |
| spellingShingle | Ricardo Fuentes Florence L Marlow Elliott W Abrams Hong Zhang Manami Kobayashi Tripti Gupta Lee D Kapp Zachary DiNardo Ronald Heller Ruth Cisternas Priscila García-Castro Fabián Segovia-Miranda Felipe Montecinos-Franjola William Vought Charles E Vejnar Antonio J Giraldez Mary C Mullins Maternal regulation of the vertebrate oocyte-to-embryo transition. PLoS Genetics |
| title | Maternal regulation of the vertebrate oocyte-to-embryo transition. |
| title_full | Maternal regulation of the vertebrate oocyte-to-embryo transition. |
| title_fullStr | Maternal regulation of the vertebrate oocyte-to-embryo transition. |
| title_full_unstemmed | Maternal regulation of the vertebrate oocyte-to-embryo transition. |
| title_short | Maternal regulation of the vertebrate oocyte-to-embryo transition. |
| title_sort | maternal regulation of the vertebrate oocyte to embryo transition |
| url | https://doi.org/10.1371/journal.pgen.1011343 |
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