ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction
Mammalian eggs are surrounded by an extracellular matrix called the zona pellucida (ZP). This envelope participates in processes such as acrosome reaction induction, sperm binding, protection of the oviductal embryo, and may be involved in speciation. In eutherian mammals, this coat is formed of thr...
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Frontiers Media S.A.
2021-01-01
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Series: | Frontiers in Cell and Developmental Biology |
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Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2020.626679/full |
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author | Mª José Izquierdo-Rico Mª José Izquierdo-Rico Mª José Izquierdo-Rico Carla Moros-Nicolás Carla Moros-Nicolás Carla Moros-Nicolás Míriam Pérez-Crespo Ricardo Laguna-Barraza Alfonso Gutiérrez-Adán Frédéric Veyrunes José Ballesta José Ballesta José Ballesta Vincent Laudet Pascale Chevret Manuel Avilés Manuel Avilés Manuel Avilés |
author_facet | Mª José Izquierdo-Rico Mª José Izquierdo-Rico Mª José Izquierdo-Rico Carla Moros-Nicolás Carla Moros-Nicolás Carla Moros-Nicolás Míriam Pérez-Crespo Ricardo Laguna-Barraza Alfonso Gutiérrez-Adán Frédéric Veyrunes José Ballesta José Ballesta José Ballesta Vincent Laudet Pascale Chevret Manuel Avilés Manuel Avilés Manuel Avilés |
author_sort | Mª José Izquierdo-Rico |
collection | DOAJ |
description | Mammalian eggs are surrounded by an extracellular matrix called the zona pellucida (ZP). This envelope participates in processes such as acrosome reaction induction, sperm binding, protection of the oviductal embryo, and may be involved in speciation. In eutherian mammals, this coat is formed of three or four glycoproteins (ZP1–ZP4). While Mus musculus has been used as a model to study the ZP for more than 35 years, surprisingly, it is the only eutherian species in which the ZP is formed of three glycoproteins Zp1, Zp2, and Zp3, Zp4 being a pseudogene. Zp4 was lost in the Mus lineage after it diverged from Rattus, although it is not known when precisely this loss occurred. In this work, the status of Zp4 in several murine rodents was tested by phylogenetic, molecular, and proteomic analyses. Additionally, assays of cross in vitro fertilization between three and four ZP rodents were performed to test the effect of the presence of Zp4 in murine ZP and its possible involvement in reproductive isolation. Our results showed that Zp4 pseudogenization is restricted to the subgenus Mus, which diverged around 6 MYA. Heterologous in vitro fertilization assays demonstrate that a ZP formed of four glycoproteins is not a barrier for the spermatozoa of species with a ZP formed of three glycoproteins. This study identifies the existence of several mouse species with four ZPs that can be considered suitable for use as an experimental animal model to understand the structural and functional roles of the four ZP proteins in other species, including human. |
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last_indexed | 2024-12-20T12:56:57Z |
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spelling | doaj.art-f158673f8e804a8986784e0d7c7ea2762022-12-21T19:40:02ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-01-01810.3389/fcell.2020.626679626679ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete InteractionMª José Izquierdo-Rico0Mª José Izquierdo-Rico1Mª José Izquierdo-Rico2Carla Moros-Nicolás3Carla Moros-Nicolás4Carla Moros-Nicolás5Míriam Pérez-Crespo6Ricardo Laguna-Barraza7Alfonso Gutiérrez-Adán8Frédéric Veyrunes9José Ballesta10José Ballesta11José Ballesta12Vincent Laudet13Pascale Chevret14Manuel Avilés15Manuel Avilés16Manuel Avilés17Department of Cell Biology and Histology, Faculty of Medicine, University of Murcia, Murcia, SpainInstitute for Biomedical Research of Murcia (IMIB-Arrixaca), Murcia, SpainInternational Excellence Campus for Higher Education and Research “Campus Mare Nostrum”, Murcia, SpainDepartment of Cell Biology and Histology, Faculty of Medicine, University of Murcia, Murcia, SpainInstitute for Biomedical Research of Murcia (IMIB-Arrixaca), Murcia, SpainInternational Excellence Campus for Higher Education and Research “Campus Mare Nostrum”, Murcia, SpainDepartment of Animal Reproduction, Instituto Nacional de Investigacion y Tecnologia Agraria y Alimentaria (INIA), Madrid, SpainDepartment of Animal Reproduction, Instituto Nacional de Investigacion y Tecnologia Agraria y Alimentaria (INIA), Madrid, SpainDepartment of Animal Reproduction, Instituto Nacional de Investigacion y Tecnologia Agraria y Alimentaria (INIA), Madrid, SpainInstitut des Sciences de l'Evolution, UMR5554 CNRS/Université Montpellier/IRD/EPHE, Montpellier, FranceDepartment of Cell Biology and Histology, Faculty of Medicine, University of Murcia, Murcia, SpainInstitute for Biomedical Research of Murcia (IMIB-Arrixaca), Murcia, SpainInternational Excellence Campus for Higher Education and Research “Campus Mare Nostrum”, Murcia, SpainMarine Eco-Evo-Devo Unit, Okinawa Institute of Science and Technology, Okinawa, JapanLaboratoire de Biométrie et Biologie Evolutive, UMR5558, CNRS, Université de Lyon, Université Claude Bernard Lyon 1, Villeurbanne, FranceDepartment of Cell Biology and Histology, Faculty of Medicine, University of Murcia, Murcia, SpainInstitute for Biomedical Research of Murcia (IMIB-Arrixaca), Murcia, SpainInternational Excellence Campus for Higher Education and Research “Campus Mare Nostrum”, Murcia, SpainMammalian eggs are surrounded by an extracellular matrix called the zona pellucida (ZP). This envelope participates in processes such as acrosome reaction induction, sperm binding, protection of the oviductal embryo, and may be involved in speciation. In eutherian mammals, this coat is formed of three or four glycoproteins (ZP1–ZP4). While Mus musculus has been used as a model to study the ZP for more than 35 years, surprisingly, it is the only eutherian species in which the ZP is formed of three glycoproteins Zp1, Zp2, and Zp3, Zp4 being a pseudogene. Zp4 was lost in the Mus lineage after it diverged from Rattus, although it is not known when precisely this loss occurred. In this work, the status of Zp4 in several murine rodents was tested by phylogenetic, molecular, and proteomic analyses. Additionally, assays of cross in vitro fertilization between three and four ZP rodents were performed to test the effect of the presence of Zp4 in murine ZP and its possible involvement in reproductive isolation. Our results showed that Zp4 pseudogenization is restricted to the subgenus Mus, which diverged around 6 MYA. Heterologous in vitro fertilization assays demonstrate that a ZP formed of four glycoproteins is not a barrier for the spermatozoa of species with a ZP formed of three glycoproteins. This study identifies the existence of several mouse species with four ZPs that can be considered suitable for use as an experimental animal model to understand the structural and functional roles of the four ZP proteins in other species, including human.https://www.frontiersin.org/articles/10.3389/fcell.2020.626679/fullzona pellucidaZP4Mus musculusmurine phylogenyoocytepseudogene |
spellingShingle | Mª José Izquierdo-Rico Mª José Izquierdo-Rico Mª José Izquierdo-Rico Carla Moros-Nicolás Carla Moros-Nicolás Carla Moros-Nicolás Míriam Pérez-Crespo Ricardo Laguna-Barraza Alfonso Gutiérrez-Adán Frédéric Veyrunes José Ballesta José Ballesta José Ballesta Vincent Laudet Pascale Chevret Manuel Avilés Manuel Avilés Manuel Avilés ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction Frontiers in Cell and Developmental Biology zona pellucida ZP4 Mus musculus murine phylogeny oocyte pseudogene |
title | ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction |
title_full | ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction |
title_fullStr | ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction |
title_full_unstemmed | ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction |
title_short | ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction |
title_sort | zp4 is present in murine zona pellucida and is not responsible for the specific gamete interaction |
topic | zona pellucida ZP4 Mus musculus murine phylogeny oocyte pseudogene |
url | https://www.frontiersin.org/articles/10.3389/fcell.2020.626679/full |
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