Analysis of ZP1 gene reveals differences in zona pellucida composition in carnivores

Moros-Nicolás, Carla; Leza, A.; Chevret, Pascale; Guillén-Martínez, A.; González-Brusi, Leopoldo; López-Béjar, Manel; Ballesta, José Antonio Camacho; Avilés, Manuel; Izquierdo-Rico, M. J.

doi:10.1071/rd17022

Cited by 7 publications

(19 citation statements)

References 67 publications

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“…Remarkably, the laboratory mouse remain the only mammalian species studied so far where ZP4 is not present in ZP (Moros-Nicolás et al, 2018), and mouse ZP is noticeably softer and more elastic compared to other mammalian ZPs containing ZP4 with or without ZP1 (Yu Sun et al, 2003). Further evidence for the fundamental structural role of ZP4 comes from transgenic mouse models producing humanized ZP: the expression of human ZP4 in mouse ZP was found to be able to recover the thickness and robustness lost following mouse ZP2 ablation (Avella et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…The evolutionary conservation of ZP4 in humans (Hughes and Barratt, 1999; Lefièvre et al, 2004) and many other mammals (Goudet et al, 2008; Hedrick and Wardrip, 1987; Hoodbhoy et al, 2005; Izquierdo-Rico et al, 2009; Moros-Nicolás et al, 2018; Noguchi et al, 1994; Stetson et al, 2012) points towards a conserved role of this protein. In this sense, these results highlight ZP4 mutations as a possible cause for female infertility in both humans and livestock or wild species, and pave the way for the development of contraceptive methods based on ZP4 disruption.…”

Section: Discussionmentioning

confidence: 99%

“…The fourth ZP protein component, ZP4, is absent in mice, which seems to be an exception for mammals, as ZP4 is present in multiple mammalian species including humans (Hughes and Barratt, 1999; Lefièvre et al, 2004), rabbits (Stetson et al, 2012), ungulates (Hedrick and Wardrip, 1987; Noguchi et al, 1994; Topper et al, 1997), carnivores (Moros-Nicolás et al, 2018) and other rodents (Hoodbhoy et al, 2005; Izquierdo-Rico et al, 2009). The lack of ZP4 in laboratory mouse ( Mus musculus ), the only species where KO models were readily available, has precluded the study of the role of this protein by of loss-of-function experiments.…”

Section: Introductionmentioning

confidence: 99%

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ZP4 confers structural properties to the zona pellucida essential for embryo development

Lamas-Toranzo¹,

Balvís²,

Querejeta-Fernández

et al. 2019

eLife

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Zona pellucida (ZP), the extracellular matrix sheltering mammalian oocytes and embryos, is composed by 3 to 4 proteins. The roles of the three proteins present in mice have been elucidated by KO models, but the function of the fourth component (ZP4), present in all other eutherian mammals studied so far, has remained elusive. Herein, we report that ZP4 ablation impairs fertility in female rabbits. Ovulation, fertilization and in vitro development to blastocyst were not affected by ZP4 ablation. However, in vivo development is severely impaired in embryos covered by a ZP4-devoided zona, suggesting a defective ZP protective capacity in the absence of ZP4. ZP4-null ZP was significantly thinner, more permeable, and exhibited a more disorganized and fenestrated structure. The evolutionary conservation of ZP4 in other mammals, including humans, suggests that the structural properties conferred by this protein are required to ensure proper embryo sheltering during in vivo preimplantation development.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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ZP4 confers structural properties to the zona pellucida essential for embryo development

Lamas-Toranzo¹,

Balvís²,

Querejeta-Fernández

et al. 2019

eLife

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“…For example, the loss of most ZP gene subfamilies occurred repeatedly in mammals ( Figs 3 and 5 ). This gene loss has been explained as a progressive process during the evolution of vertebrates due to the presence of pseudogenes of ZP1, ZP4 and ZPAX in certain mammals ( Goudet et al, 2008 ; Moros-Nicolás et al, 2017 ). Similarly, putative pseudogenes of ZPY, ZP3.2 and ZP3.3 were also found in different species ( ; …”

Section: Discussionmentioning

confidence: 99%

Evolution and multiple origins of zona pellucida genes in vertebrates

Feng

Tian

et al. 2018

Biology Open

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Animal egg coats are composed of different glycoproteins collectively named zona pellucida (ZP) proteins. The characterized vertebrate genes encoding ZP proteins have been classified into six subfamilies, and exhibit low similarity to the ZP genes characterized in certain invertebrates. The origin and evolution of the vertebrate ZP genes remain obscure. A search against 97 representative metazoan species revealed various numbers (ranging from three to 33) of different putative egg-coat ZP genes in all 47 vertebrates and several ZP genes in five invertebrate species, but no putative ZP gene was found in the other 45 species. Based on phylogenetic and synteny analyses, all vertebrate egg-coat ZP genes were classified into eight ZP gene subfamilies. Lineage- and species-specific gene duplications and gene losses occurred frequently and represented the main causes of the patchy distribution of the eight ZP gene subfamilies in vertebrates. Thorough phylogenetic analyses revealed that the vertebrate ZP genes could be traced to three independent origins but were not orthologues of the characterized invertebrate ZP genes. Our results suggested that vertebrate egg-coat ZP genes should be classified into eight subfamilies, and a putative evolutionary map is proposed. These findings would aid the functional and evolutionary analyses of these reproductive genes in vertebrates.

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“…The duplication that gave rise to Zp1 and Zp4 occurred during the early evolution of the amniotes (Hughes and Barratt, 1999; Bausek et al, 2000; Goudet et al, 2008) and multiple events of pseudogenization resulted in modern placental mammals whose zona pellucida structure is only composed of three subunits instead of four. Zp1 was lost in some species of the Caniformia suborder, such as dog ( Canis familiaris ), dingo ( Canis lupus dingo ) and fox ( Vulpes vulpes ) (Goudet et al, 2008; Moros-Nicolás et al, 2018a). Zp1 gene was also lost among some Pinnipeds (Moros-Nicolás et al, 2018a) and at least one more pseudogenization of Zp1 took place in the evolution of Cetartiodactyla as many even-toed ungulates and cetaceans lack a functional version of this gene (Goudet et al, 2008; Stetson et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Positive selection in gamete interaction proteins inCarnivora

Pisciottano

Campos

Penna

et al. 2022

Preprint

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The jaguar (Panthera onca) is the most relevant predator in South America and an endangered species in Argentina. Therefore genomic, evolutionary and functional studies of this species are strategic to gain biological insights and support conservation efforts. With the advent of sequencing advances the study of relevant character species evolution has to be revisited. Recent comparative genomic analysis revealed a long history of hybridization among extant big cats, which indicates an absence of inter-specific isolation barriers. We aimed to uncover the molecular basis of this interspecies crossing and the evolution of the functional capacities of pantherine gamete interaction Zona Pellucida proteins (ZP) and JUNO. Hi-C long-range sequencing and chromosome-resolved jaguar genome assembly was used to resolve ZP genes loci and reconstruct the evolutionary history of these proteins. Exploring sequence variability in more that 30 Carnivora species, Feliforme and Caniforme sister groups show significant differences in average sequence identity for all studied proteins except ZP4, always showing Caniformes as a more diverse group than Feliformes. Molecular evolution of ZP isoforms involved in sperm-recognition, ZP3 and ZP2, showed similar phylogenetic histories, displaying signatures of positive selection among Carnivores and Caniformes, but not among Pantherines or Feliformes. On the other hand, structural cross-linking ZP subunits, ZP1 and ZP4, displayed a different evolutionary history. The fusion protein IZUMO1R was found to be highly conserved in all studied phylogenetic groups. These results strengthen the idea that ZPs are proteins more related to specific-specificity isolation than IZUMO1R, which is specialized in fusion events. Altogether, our findings indicate that sperm-oocyte interaction and fusion proteins lack the degree of diversification necessary to establish a prezygotic reproductive isolation barrier between pantherines, which would explain observed reticulated patterns of evolution in this clade.

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Analysis of ZP1 gene reveals differences in zona pellucida composition in carnivores

Cited by 7 publications

References 67 publications

ZP4 confers structural properties to the zona pellucida essential for embryo development

ZP4 confers structural properties to the zona pellucida essential for embryo development

Evolution and multiple origins of zona pellucida genes in vertebrates

Positive selection in gamete interaction proteins inCarnivora

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