Oviductal extracellular vesicles interact with the spermatozoon’s head and mid-piece and improves its motility and fertilizing ability in the domestic cat

Abstract

Fertilization and early embryo development are regulated by a unique maternal-gamete/embryo cross-talk within the oviduct. Recent studies have shown that extracellular vesicles (EVs) within the oviduct play important roles in mediating this developmental process. Here, we examined the influence of oviductal EVs on sperm function in the domestic cat. We demonstrated that (1) EVs are enriched in proteins related to energy metabolism, membrane modification, and reproductive function; (2) EVs bound and fused with the membranes of the acrosome and mid piece; and (3) incubating sperm with EVs improved motility, fertilizing capacity of cat spermatozoa and prevented acrosomal exocytosis in vitro . These findings indicated that oviductal EVs mediate sperm function and fertilization in the cat and provides new insights to improve sperm cryopreservation and in vitro fertilization in the domestic and wild felids and human.

Metabolomic Profile of Oviductal Extracellular Vesicles across the Estrous Cycle in Cattle

“…As spermatozoa and preimplantation embryos are able to uptake oEVs [5,6,8], oEV-metabolites at the pre-and post-ovulatory stages may contribute to their continuous supply of amino acids and energy substrates for the success of early reproductive events. In this sense, we would like to point out that the three most abundant metabolites identified in oEVs (i.e., myoinositol, lactate, and glycine, may have a higher impact on gametes and embryos.…”

“…In the female genital tract, EVs have been isolated from follicular, uterine, and oviductal fluids (OF) [2][3][4][5]. EVs from the OF (oEVs), also known as oviductosomes, have gained growing attention in recent years as they may 2 of 17 act as natural cargos, bringing key components from the maternal compartment into gametes and embryos for the establishment of pregnancy [5][6][7][8][9]. Oviductal EVs are released by oviductal epithelial cells (OECs), as shown from in vitro studies [5,7], and may originate from the pre-ovulatory follicle at ovulation.…”

“…Previous studies in mice showed that incubation of spermatozoa with oEVs activates a Ca2+ efflux pomp, PMCA4, which is important for the acquisition of sperm hyperactivated motility and fertilizing competence [6]. In the feline species, oEVs were shown to fuse with the sperm membrane, to improve sperm motility and fertilizing ability, and to prevent premature acrosome reaction in vitro [8].…”

Composing the Early Embryonic Microenvironment: Physiology and Regulation of Oviductal Secretions

“…Recently, using mass spectrometry, more than 50 OF proteins, including oviductin, several annexins, alpha-2-macroglobulin, and galectin-3, were shown to interact with the cattle embryo [49]. Interestingly, a majority of these embryo-interacting proteins was also identified in bovine and feline oviductal exosomes [45,50], supporting the idea of an embryo-maternal dialog mediated by EVs in the oviduct.…”

“…Alternatively, cytoplasmic proteins detected in the lumen may derive from the apocrine secretory pathway or be secreted via non-classical mechanisms [41,43], as known for annexins (ANXAs), heat shock protein 70 (HSP70), and interleukin 1-beta (IL-1β). Additionally, a majority of proteins identified in OF was also found in EV fractions isolated from the OF of cattle and cat [45]. This is the case for OVGP1, heat shock proteins (HSPA8, HSP70), annexins (ANXA1-5), and several intracytoplasmic enzymes (e.g., fatty acid synthase (FASN) and glycogen phosphorylase (PYG)), among others.…”