Dissociation of the Reproductive and Prolactin Photoperiodic Responses in Male Golden Hamsters

BIOLOGY OF REPRODUCTION 51, 366-372 (1994) Dissociation of the Reproductive and Prolactin Photoperiodic Responses in Male Golden Hamsters' RICHARD S. DONHAM,2 ESTEBAN PALACIO, and MILTON H. STETSON School of Life and Health Sciences, University of Delaware, Newark, Delaware 19716 ABSTRACT INTRODUCTION history, PRL levels reflected the length of the ambient photoperiod irrespective of whether animals had been exposed to a longer or shorter photoperiod previously. Of course, short-day breeders (e.g., sheep) normally have depressed levels of PRL during the period of maximal reproductive activity [13,14]. Thus there is considerable evidence that the release of PRL and that of the gonadotropins are separately regulated despite the dependence of both on the well-known pathway by which photic information reaches the pineal and is translated into a pattern of melatonin secretion [1,2,15]. Herein we compare further the photoperiodic response of PRL to that of the reproductive system in adult and immature hamsters. Gonadal maturation occurs at the same rate in young golden hamsters whether they are raised on long days or short days or even if they are blinded [16,17]. By about 8 wk of age, males have large testes with active spermatogenesis and females display 4-day ovulatory cycles, regardless of photoperiodic treatment. Thereafter, the reproductive system collapses in those animals exposed to short days. However, the question of when juvenile hamsters become photoresponsive is still not completely resolved, since there appears to be considerable latency before photoperiodic effects on the gonads are observable, even in robustly responding adults. It may be that this latency masks a sensitivity to short days in immature hamsters [18, 19]. In any case, an observable response of LH or FSH does not occur before about 7-10 wk of age, regardless of whether or not the animals are sensitive at an earlier age. If the response of PRL to short days is similar to that of the pituitary-testic- Transfer of male golden hamsters (Mesocricetus auratus) to photoperiods of less than 12.5 h of light per 24 h induces morphological and functional regression of the reproductive system. Circulating levels of LH, FSH, prolactin (PRL), and testosterone decrease and the seminiferous tubules dedifferentiate; spermatogenesis ceases and the tubular epithelium consists of only spermatogonia, a few spermatocytes, and Sertoli cells [1-6]. However, prolonged exposure to short day lengths induces photoperiodic refractoriness and LH, FSH, and PRL levels recrudesce, inducing regeneration of the testes [3-6]. Although the photoperiodic regulation of the thyroid gland has received less attention, it is clear that short days similarly decrease the levels of circulating thyroid hormone [7-9]. Although the patterns of response of LH, FSH, and PRL to exposure to short photoperiods are similar, reproductive function and PRL levels may be experimentally dissociated in the golden hamster and other photoperiodic rodents. For example, in the prairie vole (Microtus ochrogaster) [10] and the deer mouse (Peromyscus maniculatus) [11], PRL levels were found to be lower in animals on short days as compared to longer photoperiods, even in animals whose reproductive system failed to respond to the short photoperiod. In the golden hamster, Hastings et al. [12] found that whereas the level of LH was affected by photoperiodic Accepted April 12, 1994. Received October 14, 1993. 'Supported by NSF Research Grant DCB87-14638. 2 Correspondence. FAX: (302) 831-2281. 366 The response of prolactin (PRL) and that of the pituitary-testicular axis to inhibitory photoperiods were compared in immature and young adult hamsters. In the first experiment, 14-day-old hamsters were transferred from 14L:10D to 12L:12D or 8L:16D. At 21, 28, 35, and 49 days of age, body weights, testes weights, and plasma LH were similar in all groups. In contrast, the levels of PRL were lower in animals on 8L:16D or 12L:12D than in those on 14L:1OD at 35 and 49 days of age. In a second experiment, 80-day-old hamsters were transferred from 14L:1OD to either 12L:12D or 8L:16D. At 5-wk intervals, they were weighed and bled by cardiocentesis and the length of the testes was measured. Photoperiods of 12L:12D and 8L:16D induced testicular regression, which was complete by 15 wk. Thereafter, augmented levels of FSH preceded spontaneous recrudescence of the testes in animals on both photoperiods. Serum PRL levels were significantly depressed within 5 wk after transfer t either 8L:16D or 12L:12D. After 15 wk as the testes were increasing in size in both groups, circulating PRL levels increased in animals exposed to 8L:16D, whereas in animals exposed to 12L:12D, PRL remained at or below the sensitivity of the assay. In a final experiment, on the day before parturition, pregnant hamsters were transferred to either 6L:18D, 6L:30D, 6L42D, or 6L:54D or were held on 14L:1OD. There were no differences in testicular weights, plasma LH, or plasma thyroxine (T4) of the pups from these dams at 21, 36, or 48 days of age. On the other hand, PRL levels at these ages were elevated in the 6L:30D and the 6L54D groups as compared to the 6L:18D and the 6L:42D groups. The results suggest that the response of PRL to photoperiod may be experimentally dissociated from that of the hypothalamo-pituitary-testis axis to photoperiod. Like the response of the reproductive system in the adult, the response of PRL incorporates a circadian oscillator in the system that measures day length. PROLACTIN AND PHOTOPERIOD IN HAMSTERS MATERIALS AND METHODS The hamsters were bred and raised at the University of Delaware; they were held in a colony room on a light cycle of 14L:10OD (lights-on from 0600 to 2000 h) until transfer to the experimental photoperiods. Animals were housed several per cage and provided food and water ad libitum. Individuals were identified by variations in pelage color, pattern, and length that characterize golden hamsters in this colony. Experiments Experiment 1. Litters of 14-day-old hamsters were transferred with their mothers from a colony room to ventilated light-sealed boxes (6 cages per box). One third of the animals were exposed to 8L:16D, another one third to 12L:12D, and the remainder to 14L:10D. Photocycles were controlled by electronic timers (ChronTrol Corporation, San Diego, CA). At 21 days, the young were weaned and separated by sex. At 21, 28, 35, and 49 days of age, groups of 8-17 males were killed; trunk blood was collected and the plasma was aspirated and frozen at -20°C until assayed for LH and PRL. Experiment 2. Adult males 80 days of age were transferred to light-sealed boxes and exposed to 8L:16D (n = 20), 12L:12D (n = 20), or 14L:10D (n = 14). At 5-wk intervals, a blood sample was collected by cardiac puncture and the plasma was frozen until it was assayed for PRL, LH, and FSH. After collection of each blood sample, the animals were placed under light ketamine (...truncated)