Dynamics of cattle sperm sncRNAs during maturation, from testis to ejaculated sperm

Autor: Hélène Kiefer, Andrea Rau, Eli Sellem, Sylvain Marthey, Chrystelle Le Danvic, Aurelie Bonnet, Laurent Schibler, Hélène Jammes, Luc Jouneau, Benoît Guyonnet
Přispěvatelé: Biologie de la Reproduction, Environnement, Epigénétique & Développement (BREED), École nationale vétérinaire - Alfort (ENVA)-Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Allice, Génétique Animale et Biologie Intégrative (GABI), AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Mathématiques et Informatique Appliquées du Génome à l'Environnement [Jouy-En-Josas] (MaIAGE), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Transfrontalière BioEcoAgro - UMR 1158 (BioEcoAgro), Université d'Artois (UA)-Université de Liège-Université de Picardie Jules Verne (UPJV)-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-JUNIA (JUNIA), Université catholique de Lille (UCL)-Université catholique de Lille (UCL), APIS-GENE (SeQuaMol), ANR-14-LAB3-0008,SeQuaMol,Qualité de la semence et fertilité chez les bovins: développement de nouveaux outils moléculaires de diagnostic(2014), École nationale vétérinaire d'Alfort (ENVA)-Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université Paris-Saclay-AgroParisTech-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Transfrontalière BioEcoAgro (Transfrontalière BioEcoAgro), Université d'Artois (UA)-Université de Liège-Université de Picardie Jules Verne (UPJV)-Université du Littoral Côte d'Opale (ULCO)-Université de Lille-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Jazyk: angličtina
Rok vydání: 2021
Předmět:
Male
endocrine system
Piwi-interacting RNA
Semen
Biology
QH426-470
TRFs
RRFs
[SDV.BDLR.RS]Life Sciences [q-bio]/Reproductive Biology/Sexual reproduction
03 medical and health sciences
0302 clinical medicine
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]
Gene expression
Embryonic morphogenesis
Testis
medicine
Genetics
Animals
Testicular parenchyma sperm
Molecular Biology
[SDV.BDD.GAM]Life Sciences [q-bio]/Development Biology/Gametogenesis
reproductive and urinary physiology
030304 developmental biology
Secretome
Epididymis
0303 health sciences
030219 obstetrics & reproductive medicine
urogenital system
Research
PiRNA
Embryogenesis
SncRNAs
[SDV.BDLR]Life Sciences [q-bio]/Reproductive Biology
[SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Molecular biology
Bovine
Epididymis location
Sperm
Spermatozoa
Cell biology
Sperm epigenetics
medicine.anatomical_structure
RNA
Small Untranslated
Cattle
MiRNA
Spermatogenesis
Zdroj: Epigenetics & Chromatin, Vol 14, Iss 1, Pp 1-18 (2021)
Epigenetics & Chromatin
Epigenetics & Chromatin, 2021, 14, pp.2-18. ⟨10.1186/s13072-021-00397-5⟩
Epigenetics & Chromatin, BioMed Central, 2021, 14, pp.2-18. ⟨10.1186/s13072-021-00397-5⟩
ISSN: 1756-8935
DOI: 10.1186/s13072-021-00397-5⟩
Popis: Background During epididymal transit, spermatozoa go through several functional maturation steps, resulting from interactions with epididymal secretomes specific to each region. In particular, the sperm membrane is under constant remodeling, with sequential attachment and shedding of various molecules provided by the epididymal lumen fluid and epididymosomes, which also deliver sncRNA cargo to sperm. As a result, the payload of sperm sncRNAs changes during the transit from the epididymis caput to the cauda. This work was designed to study the dynamics of cattle sperm sncRNAs from spermatogenesis to final maturation. Results Comprehensive catalogues of sperm sncRNAs were obtained from testicular parenchyma, epididymal caput, corpus and cauda, as well as ejaculated semen from three Holstein bulls. The primary cattle sncRNA sperm content is markedly remodeled as sperm mature along the epididymis. Expression of piRNAs, which are abundant in testis parenchyma, decreases dramatically at epididymis. Conversely, sperm progressively acquires miRNAs, rsRNAs, and tsRNAs along epididymis, with regional specificities. For instance, miRNAs and tsRNAs are enriched in epididymis cauda and ejaculated sperm, while rsRNA expression peaks at epididymis corpus. In addition, epididymis corpus contains mainly 20 nt long piRNAs, instead of 30 nt in all other locations. Beyond the bulk differences in abundance of sncRNAs classes, K-means clustering was performed to study their spatiotemporal expression profile, highlighting differences in specific sncRNAs and providing insights into their putative biological role at each maturation stage. For instance, Gene Ontology analyses using miRNA targets highlighted enriched processes such as cell cycle regulation, response to stress and ubiquitination processes in testicular parenchyma, protein metabolism in epididymal sperm, and embryonic morphogenesis in ejaculated sperm. Conclusions Our findings confirm that the sperm sncRNAome does not simply reflect a legacy of spermatogenesis. Instead, sperm sncRNA expression shows a remarkable level of plasticity resulting probably from the combination of multiple factors such as loss of the cytoplasmic droplet, interaction with epididymosomes, and more surprisingly, the putative in situ production and/or modification of sncRNAs by sperm. Given the suggested role of sncRNA in epigenetic trans-generational inheritance, our detailed spatiotemporal analysis may pave the way for a study of sperm sncRNAs role in embryo development.
Databáze: OpenAIRE
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