Oocytes Skipped Spawning Through Atresia Is Regulated by Somatic Cells Revealed by Transcriptome Analysis in Pampus argenteus

Abstract

In teleost, follicle atresia is a common degenerative process that can occur at different stages of ovarian development. In this study, we depicted the cellular morphology of silver pomfret (Pampus argenteus) follicular atresia in detail and divided it into four different stages from Aα to Aδ stages based on the main cellular characteristics. High-throughput RNA sequencing was used to profile follicle atresia from Aα to Aδ stages, and many stage-specific genes were identified. In early atretic ovary, a great number of genes in cytokine-cytokine receptor interaction were obviously downregulated, suggesting that somatic cells might directly induce the follicle atresia by disrupting the normal conservation with germ cells. Meanwhile, the regulatory network of immune cell–related pathways was discovered in the process of atresia. The genes enriched in Th cell differentiation, leukocyte transendothelial migration, cholesterol metabolism, and so on were abundantly expressed, indicating that the immune cells play key roles in the process of in follicle atresia. Moreover, a model was proposed to illustrate how somatic cells mediate the process of follicle atresia. The study provides important insights into the molecular networks underlying follicle atresia in teleost.

Apoptosis and autophagy-related gene transcription during ovarian follicular atresia in European hake (Merluccius merluccius)

“…This would allow the recovery of the energy invested in oogenesis previous to follicle resorption through apoptosis-mediated atresia. Comparatively, apoptosis seems to take the leading role in regulating atresia in mammals while in fish as seen hereby, autophagy also plays an important role, especially in somatic cells surrounding the vitellogenic oocytes (Yang et al, 2022). Nonetheless, recent revision of follicular atresia in mammals points also to an important role of autophagy with special mention to molecular markers such as Beclin-1 as in the present study in hake.…”

“…There is evidence that apoptosis plays a key role in gonad development and reproduction in birds and mammals, but also in fish (Habibi and Andreu-Vieyra, 2007;Janz and Van Der Kraak, 1997;Matsuda et al, 2012;Nozu et al, 2013;Tilly, 1996a;Tiwari et al, 2015;Wood and Van Der Kraak, 2001;Yamamoto et al, 2011;Yang et al, 2022). In birds and mammals, for example, the dominant follicle is normally recruited to the ovulatory pool, while the remaining follicles are eliminated through atresia, mediated by apoptosis initiated within granulosa cells (Andreu-Vieyra and Habibi, 2000;Bhardwaj and Sharma, 2012;Matsuda et al, 2012).…”

“…The upregulation of beclin-1 and ptenb transcripts in atretic follicles, occurred irrespective of their developmental stage, suggesting that autophagy is strongly involved in follicular atresia along the whole process of oogenesis. The upregulation of p53, caspase-3, ctsd and dapk1 transcripts only during atresia affecting vitellogenic follicles, would suggest that vitellogenesis is the moment at which both apoptosis and autophagy are at their highest (Yang et al, 2022). Hereby a set of marker genes for the early estimation of atresia in female European hakes (that could be extended to other fish species) is provided.…”

“…Autophagy recycles nutrients from degraded cell organelles in the follicle, and hence could provide the energy that may be required for future oocyte and egg production in vertebrates (Bhardwaj et al, 2022). Whereas in mammals, apoptosis in cells that form the ovarian follicles is considered the main cellular mechanism mediating early ovarian atresia (Hsueh et al, 1994;Matsuda et al, 2012;Tilly, 1996aTilly, , 1996bTiwari et al, 2015), in fish, apoptosis is accompanied by autophagy at least during the late stages of follicular atresia (Miranda et al, 1999;Morais et al, 2012); thus suggesting the existence of another novel pathway during follicular atresia (Yang et al, 2022).…”

Insulin-like growth factor 1 promotes the gonadal development of Pampus argenteus by regulating energy metabolism

“…As a result, most of the body's energy is used for reproductive processes. Under artificial breeding conditions, we discovered instances of ovarian atresia and asynchronous sperm development in some silver pomfret specimens [33, 34]. Additionally, due to generations of breeding, the gonad development of silver pomfret in artificial culture has been accelerated.…”