Abstract
In the poultry, only less than 5% primordial follicles in the ovary can develop into the prehierarchical follicles (PHFs) leading to progressive development, ovulation, and egg formation. This low rate of recruitment indicates a huge potential for improvement of the laying performance. A great reduction in egg production is caused by aging with extensive follicular atresia. In this study, age-related changes in the laying performance and ovarian status were compared between the peak-lay (D280) and aged (D580) chickens. Subsequently, a cross coculture of PHFs and granulosa cells (GCs) from D280 or D580 hens was adopted to reveal the mechanism of declined follicle development. Results showed that persistent endoplasmic reticulum (ER) stress in GCs of the aged hens was accompanied with intensified apoptosis. Bone morphogenetic protein 4 (BMP4) secreted by GCs of PHFs in D280 hens was capable of relieving ER stress and improving follicular dominance for selection in D580 hens. During this action, BMP4 reduced free calreticulin (CALR, an ER marker) content and attenuated cell apoptosis in PHFs of D580 hens via the PERK-CHOP-BCL2/caspase3 or CALR-Ca2+-BCL2-caspase12 pathway. Furthermore, BMP4 prevented follicular atresia by promoting production of steroid hormones to improve survival of GCs in PHFs from the aged hens. In conclusion, intensified ER stress and apoptosis occurred in GCs of PHFs in aged chickens, while BMP4 secreted by GCs was capable of improving follicular viability by alleviating ER stress to promote follicular development.
Highlights
In the chicken, the rate of egg production decreased markedly around 580 days of age, which seriously reduces the commercial value of egg production
In order to explore the differences during the aging process in the functional left ovaries of hens, we isolated all visible follicles protruding from the surface of ovaries on D280 and D580
The quantitative real-time polymerase chain reaction (qRT-PCR) result showed that expression of follicle-stimulating hormone receptor (FSHR) mRNA was decreased while occludin mRNA was increased in SWFs of D580 hens compared with D280 hens (Figure 1(b, b2))
Summary
The rate of egg production decreased markedly around 580 days of age, which seriously reduces the commercial value of egg production. The rate of egg production is related to the function of ovaries and quality of follicles in laying hens [1, 2]. Few studies have reported the molecular mechanism involved in the decrease of follicular dominance in the aging hens. Insulin-like growth factor I secreted by granulosa cells (GCs), as well as bone morphogenetic protein (BMP) and estrogen, is reported to play crucial roles in the growth and development of follicles [5,6,7]. GCs are destined to undergo apoptosis when these factors are depleted. In the early atretic follicles, GCs are the first cell type to undergo apoptosis [8]. Formulation of the relationship between cytokines and GC apoptosis is extremely important for improving follicular predominance and subsequent efficient follicular development
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