Comparative proteomic analysis of round and elongated spermatids during spermiogenesis in mice

Li, Meining; Li, Huahua; Yang, Hong; Cheng, Rina; Zheng, Pengdou; Guo, Rui

doi:10.1002/bmc.4799

Cited by 6 publications

(5 citation statements)

References 26 publications

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“…Terms related to mRNA processing and DNA replication were kept in the meiotic zone (continuum B) but completed by a chromosome-related process in accordance with meiosis (i.e., nuclear chromosome segregation and the meiotic cell cycle in biological processes; chromosomal region and condensed chromosome in cellular component; homologous recombination and mismatch repair in the wiki pathway). Interestingly, biological processes related to methylation and histone modifications were also retrieved, which could be associated with the establishment of a specific regulation of gene expression during spermatogenesis. − Sphingolipid metabolism was also noticed in wiki pathway and this could be related to male meiotic cytokinesis. , Estrogen signaling was also highlighted, which is in agreement with one of the pioneering works of G. V. Callard on the paracrine function of estrogens during spermatogenesis in a shark species . Proteins associated with spermiogenesis (continuum C and zone D) were unsurprisingly related to the spermatid flagellum development (i.e., for continuum C: cilium organization in biological process; cilium in cellular component; dynein in molecular function) and completed by cilium activity (i.e., for zone D: motile cilium in cellular component; calmodulin and magnesium binding in molecular function; mitochondrial protein import in the reactome pathway and purine metabolism in the wiki pathway).…”

Section: Resultssupporting

confidence: 71%

“…Thirty-one ubiquitin-conjugating enzymes were found with a higher abundance of 11 in zone A, 4 identified only in zone A, and 7 in the zones C and/or D. UBE2G2 and UBE4B were the only two enzymes showing higher abundance in zone B corresponding to cysts with spermatocytes. Their role during spermatogenesis has been little studied, with the exception of publications showing differences in levels of UBE2G2 in subfertile men and overexpression of UBE4b in elongated spermatids in mice . Relatively few E3 ubiquitin ligases were found in the present study, while many isoforms are expressed in the testis. , Of the E3 substrates identified, CUL3 was most abundant in the spermatid zones, which is in agreement with its previously reported profile in mice, while CUL2 appeared to be most abundant only in the early spermatid zone, although its expression has been reported to regulate meiotic entry in the C.…”

Section: Resultsmentioning

confidence: 99%

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Comparative Proteome Analysis of Four Stages of Spermatogenesis in the Small-Spotted Catshark (Scyliorhinus canicula), Using High-Resolution NanoLC-ESI-MS/MS

Jeanne,

Bernay,

Sourdaine

2023

J. Proteome Res.

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Spermatogenesis is a highly specialized process of cell proliferation and differentiation leading to the production of spermatozoa from spermatogonial stem cells. Due to its testicular anatomy, Scyliorhinus canicula is an interesting model to explore stage-based changes in proteins during spermatogenesis. The proteomes of four testicular zones corresponding to the germinative niche and to spermatocysts (cysts) with spermatogonia (zone A), cysts with spermatocytes (zone B), cysts with young spermatids (zone C), and cysts with late spermatids (zone D) have been analyzed by nanoLC-ESI-MS/MS. Gene ontology and KEGG annotations were also performed. A total of 3346 multiple protein groups were identified. Zone-specific protein analyses highlighted RNA-processing, chromosome-related processes, cilium organization, and cilium activity in zones A, D, C, and D, respectively. Analyses of proteins with zone-dependent abundance revealed processes related to cellular stress, ubiquitin-dependent degradation by the proteasome, post-transcriptional regulation, and regulation of cellular homeostasis. Our results also suggest that the roles of some proteins, such as ceruloplasmin, optineurin, the pregnancy zone protein, PA28β or the Culling-RING ligase 5 complex, as well as some uncharacterized proteins, during spermatogenesis could be further explored. Finally, the study of this shark species allows one to integrate these data in an evolutionary context of the regulation of spermatogenesis. Mass spectrometry data are freely accessible via iProX-integrated Proteome resources () for reuse purposes.

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Section: Resultssupporting

confidence: 71%

Section: Resultsmentioning

confidence: 99%

Comparative Proteome Analysis of Four Stages of Spermatogenesis in the Small-Spotted Catshark (Scyliorhinus canicula), Using High-Resolution NanoLC-ESI-MS/MS

Jeanne,

Bernay,

Sourdaine

2023

J. Proteome Res.

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“…Early male gametocytes (day 4 – stage II/III) showed highest expression of 579 genes (118 (20%) of unknown function). The predominant processes were related to proteolysis and proteasome complex, consistent with the critical function of proteostasis during metazoan spermatogenesis [ 67 , 68 ]. In the intermediate male gametocytes (day 6 stage III/IV), 694 genes (224 (32%) of unknown function), were found to be highest expressed.…”

Section: Resultsmentioning

confidence: 89%

Plasmodium falciparum gametocytes display global chromatin remodelling during sexual differentiation

et al. 2023

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Background The protozoan malaria parasite Plasmodium falciparum has a complex life cycle during which it needs to differentiate into multiple morphologically distinct life forms. A key process for transmission of the disease is the development of male and female gametocytes in the human blood, yet the mechanisms determining sexual dimorphism in these haploid, genetically identical sexual precursor cells remain largely unknown. To understand the epigenetic program underlying the differentiation of male and female gametocytes, we separated the two sexual forms by flow cytometry and performed RNAseq as well as comprehensive ChIPseq profiling of several histone variants and modifications. Results We show that in female gametocytes the chromatin landscape is globally remodelled with respect to genome-wide patterns and combinatorial usage of histone variants and histone modifications. We identified sex specific differences in heterochromatin distribution, implicating exported proteins and ncRNAs in sex determination. Specifically in female gametocytes, the histone variants H2A.Z/H2B.Z were highly enriched in H3K9me3-associated heterochromatin. H3K27ac occupancy correlated with stage-specific gene expression, but in contrast to asexual parasites this was unlinked to H3K4me3 co-occupancy at promoters in female gametocytes. Conclusions Collectively, we defined novel combinatorial chromatin states differentially organising the genome in gametocytes and asexual parasites and unravelled fundamental, sex-specific differences in the epigenetic code. Our chromatin maps represent an important resource for future understanding of the mechanisms driving sexual differentiation in P. falciparum.

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“…Dramatic morphological changes will occur during spermiogenesis, transforming round spermatids into elongated, tadpole-like spermatozoa with only one-fifth of their original sizes [3]. Thousands of germ cell-specific genes are highly expressed in haploid germ cells and participate in spermiogenesis [4,5]. In the past 15 years, gene knockout studies have identified 20 male germ cell specific genes or gene subtypes that play a crucial role in spermatogenesis [6].…”

Section: Introductionmentioning

confidence: 99%

“…In mammals, the oocyte is characterized by rich microvilli on the membrane surface [7]. Sperm-oocyte binding and fusion mainly occurs in this area, emphasizing its importance for fertilization [4].…”

Section: Introductionmentioning

confidence: 99%

The vertebrate- and testis- specific transmembrane protein C11ORF94 plays a critical role in sperm-oocyte membrane binding

et al. 2022

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Sperm-oocyte membrane fusion is necessary for mammalian fertilization. The factors that determine the fusion of sperm with oocytes are largely unknown. So far, spermatozoon factor IZUMO1 and the IZUMO1 counter-receptor JUNO on the oocyte membrane has been identified as a protein requiring fusion. Some sperm membrane proteins such as FIMP, SPACA6 and TEME95, have been proved not to directly regulate fusion, but their knockout will affect the fusion process of sperm and oocytes. Here, we identified a novel gene C11orf94 encoding a testicular-specific small transmembrane protein that emerges in vertebrates likely acquired via horizontal gene transfer from bacteria and plays an indispensable role in sperm-oocyte binding. We demonstrated that the deletion of C11orf94 dramatically decreased male fertility in mice. Sperm from C11orf94-deficient mice could pass through the zona pellucida, but failed to bind to the oocyte membrane, thus accumulating in the perivitelline space. In consistence, when the sperm of C11orf94-deficient mice were microinjected into the oocyte cytoplasm, fertilized oocytes were obtained and developed normally to blastocysts. Proteomics analysis revealed that C11orf94 influenced the expression of multiple gene products known to be indispensable for sperm-oocyte binding and fusion, including IZUMO1, EQTN and CRISP1. Thus, our study indicated that C11ORF94 is a vertebrate- and testis-specific small transmembrane protein that plays a critical role in sperm binding to the oolemma.

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Comparative proteomic analysis of round and elongated spermatids during spermiogenesis in mice

Cited by 6 publications

References 26 publications

Comparative Proteome Analysis of Four Stages of Spermatogenesis in the Small-Spotted Catshark (Scyliorhinus canicula), Using High-Resolution NanoLC-ESI-MS/MS

Comparative Proteome Analysis of Four Stages of Spermatogenesis in the Small-Spotted Catshark (Scyliorhinus canicula), Using High-Resolution NanoLC-ESI-MS/MS

Plasmodium falciparum gametocytes display global chromatin remodelling during sexual differentiation

The vertebrate- and testis- specific transmembrane protein C11ORF94 plays a critical role in sperm-oocyte membrane binding

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