Corpus luteum proximity alters molecular signature of the small extracellular vesicles and cumulus cells in the bovine ovarian follicle environment

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Rosa, Paola Maria da Silva ; Bridi, Alessandra ; Ferronato, Giuliana de Avila ; Nociti, Ricardo Perecin ; dos Santos, Angelica Camargo ; Cataldi, Thais Regiani ; dos Santos, Gislaine ; Chiaratti, Marcos Roberto ; Silva, Luciano Andrade ; Pugliesi, Guilherme ; Sangalli, Juliano Rodrigues ; Meirelles, Flavio Vieira ; Perecin, Felipe ; da Silveira, Juliano Coelho

• Document type: Journal article
• Source: Molecular and Cellular Endocrinology; v. 592, p. 12-pg., 2024-08-28.

Abstract

Progesterone (P4) is predicted to act as a negative regulatory hormone for oocyte maturation events; however, its local effects during follicular development remain poorly understood in bovine. The complex process of oocyte meiosis progression is dependent on cellular communication among follicular cells. Besides, the breakdown of this communication, mainly between cumulus cells (CC) and oocyte, through the retraction of cumulus projections connecting these cells can impact oocyte maturation. In our study, we observed that follicles from the ovary ipsilateral to the corpus luteum (CL) containing high intrafollicular P4 concentrations enhance the abundance of proteins detected in follicular-derived small extracellular vesicles (sEVs) predicted to be involved in the retraction of membrane projections based on actin filaments, such as transzonal projections (TZPs). Conversely, we found that follicles from the ovary contralateral to the CL, which contained low intrafollicular P4 concentrations, had a high detection of proteins predicted to regulate the maintenance of TZPs. We also performed RNAseq analysis which demonstrated that 177 genes were differentially expressed in CC under the different P4 environments. Bioinformatic analysis points to changes associated to cell metabolism in cells from follicles ipsilateral to the CL in comparison to genes involved in cell communication in CC from follicles contralateral to the CL. Our functional analysis experiment confirmed that supplementation of cumulus-oocyte complexes during in vitro maturation with P4 at concentration similar to ipsilateral follicles reduces the number of TZPs. In summary, our study underscores a direct association between P4 concentration and cumulus-oocyte interaction, with potential consequences for the acquisition of oocyte competence. (AU)

• FAPESP's process: 21/06645-0 - Extracellular vesicles as a platform for diagnostic and manipulation of the in vitro embryo production system: the next generation in animal reproduction
• Grantee: Juliano Coelho da Silveira
• Support Opportunities: Research Grants - Young Investigators Grants - Phase 2
• FAPESP's process: 20/08478-0 - Hormonal influences and body energy reserve on the modulation of the intrafolicular and periconceptional reproductive environment
• Grantee: Juliano Coelho da Silveira
• Support Opportunities: Regular Research Grants
• FAPESP's process: 21/09886-8 - Epigenetic maturation of the oocyte and totipotence: the potential of the oocyte and its relationship with the ovarian follicular niche
• Grantee: Lawrence Charles Smith
• Support Opportunities: Research Projects - SPEC Program