Enhanced serum oestrogen levels and highly steroidogenic, luteinized atretic follicles in the ovaries of the Djungarian hamster (Phodopus sungorus) kept under a short photoperiod from birth

Abstract

Enhanced serum oestrogen levels and highly steroidogenic, luteinized atretic follicles in the ovaries of the Djungarian hamster (Phodopus sungorus ) kept under a short photoperiod from birth R van den Hurk, G Dijkstra and F H de Jong AbstractObjective: In contrast to the elaborate information available on the effects of the photoperiod on the testes of hamsters, little is known about the influence on their ovaries. This study aimed to describe the ovarian follicular development and steroid hormone production in Djungarian hamsters kept from birth under a short daylight regime. Design and Methods: Female Djungarian hamsters (Phodopus sungorus ) were kept under two different light regimes: (i) 16 h light:8 h darkness (long daylight; LD) and (ii) 4 h light:20 h darkness (short daylight; SD). They were killed at 28, 56 and 80 days after birth; blood and ovaries were collected. Ovaries were either fixed in Bouin's solution or frozen. Fixed material was dehydrated, embedded in paraffin, serially sectioned at 5 mm and stained with haematoxylin and eosin, whereafter all healthy and atretic follicles were classified and counted. 3b-Hydroxysteroid dehydrogenase (3b-HSD) was histochemically demonstrated in 10 mm sections of frozen ovaries. Serum oestradiol-17b and progesterone levels were determined by RIA. Results: The numbers of healthy preantral and antral follicles were higher in LD than in SD hamsters. Antral follicles did not significantly differ in number during development in LD hamsters, but they were completely absent from 80-day-old SD animals. In LD animals the number of apoptotic preantral follicles dramatically increased with age. In SD animals the numbers of apoptotic antral follicles strongly decreased with age, whereas numerous non-apoptotic follicles with luteinized granulosa cells and a degenerated oocyte appeared, and in increasing numbers with age. During development, moderate 3b-HSD activity was present in interstitial cells, theca cells of healthy follicles, and in both theca and granulosa cells of degenerating follicles. Strong enzyme activity was found in the hypertrophied granulosa cells of luteinized atretic follicles. Mean serum progesterone values varied from 2 to 6 nmol/l and were not different in LD and SD hamsters. Mean serum oestradiol levels varied from 132 to 542 and 325 to 2353 pmol/l in LD and SD hamsters respectively. The highest oestradiol levels were found in SD animals at day 28 of development. Conclusions: Folliculogenesis was dramatically disturbed in Djungarian hamsters raised under a short photoperiod. These animals developed high serum oestradiol levels and numerous luteinized atretic follicles with highly steroidogenic granulosa cells, which appear to be the source of the increased serum oestradiol levels.

Photoperiod-induced differences in uterine growth in Phodopus sungorus are evident at an early age when serum estradiol and uterine estrogen receptor levels are not different

“…When we determined the photoperiod-induced differences in uterine size were evident by 3 wk of age, we then focused our investigation on LD and SD hamsters at 4 wk of age for the following reasons: 1. The highest E2 concentration reported by van den Hurk et al (2002) was in SD females at this age and the LD-SD difference in serum E2 concentration at 4 wk was substantial (approximately 5-fold), and 2. Neither LD nor SD females have matured by this age, as indicated by the lack of vaginal patency (Place et al 2004) and the absence of any signs that ovulations had occurred (van den Hurk et al 2002).…”

“…The highest absolute concentration (~2400 pmol/L or ~ 654 pg/mL) was measured in SD females at 4 wk of age. Given the growth promoting effects of E2 on the uterus (Scotti et al 2007), we found the report of higher E2 in SD hamsters (van den Hurk et al 2002) to be perplexing. Unfortunately, van den Hurk et al (2002) did not report uterine mass data, thus the present study is the first to investigate the apparent mismatch between serum E2 concentrations and uterine growth in P. sungorus .…”

“…Stunted growth of the uterus has been presumed to result from the suppression of gonadotropins in SD (Dodge and Badura 2002) and the associated reduction in the concentrations of estrogens (e.g., estradiol). To our knowledge, this hypothesis has never been formally tested and this conjecture has been called into question by a study that reported significantly higher serum E2 concentrations in SD than in LD hamsters between 4 and 11.4 wk of age (van den Hurk et al 2002). In that study, E2 in SD females was as much as eight-fold higher than in LD hamsters (8 wk of age), and significantly higher concentrations were noted in SD at each of the ages studied (4, 8, and 11.4 wk).…”

Photoperiod-gonadotropin mismatches induced by treatment with acyline or FSH in Siberian hamsters: impacts on ovarian structure and function

“…Specifically, these photoperiodic cues establish and modify the hamster's developmental trajectory via changes in somatic and/or reproductive development. For example, it is well known that photoperiodic information can be transmitted in utero via maternal melatonin secretion, and this prenatal signal can affect postnatal photoperiodic responses (Horton 1985, Stetson et al 1986, Lee et al 1987, Weaver et al 1987, Elliott & Goldman 1989) and the reproductive development of young (Prendergast et al 2000, Kauffman & Zucker 2002, Tuthill et al 2005. More recent studies have shown that perinatal photoperiod can have lasting effects on circadian rhythms expressed by clock neurons, wheel-running behavior (Ciarleglio et al 2011), depressive-and anxiety-like behaviors , and immune responses (Weil et al 2006).…”

Inhibition of matrix metalloproteinases in Siberian hamsters impedes photostimulated recrudescence of ovaries

“…Exposure to 12–14 weeks in short (8h light: 16 h dark per day; SD) photoperiod is sufficient to induce regression of the ovaries, anovulation, and decreased estradiol production (Moffatt-Blue, et al 2006; Salverson et al 2008; Schlatt et al 1993). Reproductively regressed hamsters are characterized by the absence of corpora lutea (CL) in the ovaries, decreases in uterine mass and plasma concentration of estradiol, and the presence of eosiniphilic terminal atretic follicles, structures typically found only in regressed ovaries (van den Hurk et al 2002; Moffatt-Blue, et al 2006; Kabithe & Place 2008). Once transferred to long day photoperiods of 16 hours of light and 8 hours of darkness per 24-hour period (long days; LD), female hamsters will rapidly regain reproductive function (Salverson et al 2008; Shahed & Young 2008).…”