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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Main Authors: Mª José Izquierdo-Rico, Carla Moros-Nicolás, Míriam Pérez-Crespo, Ricardo Laguna-Barraza, Alfonso Gutiérrez-Adán, Frédéric Veyrunes, José Ballesta, Vincent Laudet, Pascale Chevret, Manuel Avilés
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
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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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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