Siberian hamster reproduction is mediated by photoperiod-induced changes in gonadal activity. However, little is known about how photoperiod induces cellular changes in ovarian function. We hypothesized that exposing female hamsters to short (inhibitory) as opposed to long (control) photoperiods would induce an apoptosis-mediated disruption of ovarian function. Ovaries and plasma from hamsters exposed to either long (LD, 16 h light:8 h darkness) or short (SD, 8 h light:16 h darkness) days were collected during diestrus II after 3, 6, 9 and 12 weeks and processed for histology or RIA respectively. Apoptosis was assessed by in situ TUNEL and active caspase-3 protein immunolabeling. No significant differences were observed among LD hamsters for any parameter; therefore, these control data were pooled. SD exposure induced a decline in preantral follicles (P < 0.05), early antral/antral follicles (P < 0.01) and corpora lutea (P < 0.01) by week 12 as compared with LD. Terminal atretic follicles appeared by SD week 9; by week 12, these had become the predominant ovarian structures. Estradiol concentrations decreased by weeks 9 and 12 SD when compared with both LD and week-3 SD hamsters (P < 0.05); however, no changes were observed for progesterone. TUNEL-positive follicles in SD ovaries increased at week 3 and subsequently declined by week 12 as compared with LD ovaries (P < 0.01). Active capsase-3 protein immunostaining peaked at SD week 3 as compared with all other groups (P < 0.01). TUNEL and capsase-3 immunolabeling were localized to granulosa cells of late-preantral and early-antral/antral follicles. These data indicate that SD exposure rapidly induces follicular apoptosis in Siberian hamsters, which ultimately disrupts both estradiol secretion and folliculogenesis, resulting in the seasonal loss of ovarian function.
IntroductionTo maximize survival when environmental resources are reduced, individuals of many temperate species limit reproductive function seasonally. In mammals, this adaptation is cued primarily by photoperiod-induced alterations in melatonin secretion from the pineal gland. For long-day (LD) seasonal breeders, such as Siberian hamsters (Phodopus sungorus), exposure to long photoperiods (. 12.5 h of light per day; short duration of melatonin release) induces and maintains reproductive function, whereas exposure to short photoperiods (, 12.5 h of light per day; long duration of melatonin release) results in the cessation of reproductive function (Hoffmann 1986, Bronson 1989, Knopper & Boily 2000, Prendergast & Nelson 2001. Extended periods of melatonin secretion negatively affect reproductive activity via inhibition of the hypothalamic-pituitary-gonadal (HPG) axis. In both males and females, short-day (SD) exposure reduces hypothalamic synthesis and secretion of gonadotropin-releasing hormone (GnRH) and, subsequently, the pituitary gonadotropins, follicle-stimulating hormone (FSH) and luteinizing hormone (LH) (Glass 1986, Buchanan & Yellon 1991. Eventually, these endocrine alterations resu...