Kisspeptin and the seasonal control of reproduction in hamsters

Reproduction is a complex and energy demanding function. When internal and external conditions might impair reproductive success (negative energy balance, stress, harsh season) reproductive activity has to be repressed. Recent evidence suggests that these inhibitory mechanisms operate on Kiss1-expressing neurons, which were recently shown to be implicated in the regulation of GnRH release. Hamsters are seasonal rodents which are sexually active in long photoperiod and quiescent in short photoperiod. The photoperiodic information is transmitted to the reproductive system by melatonin, a pineal hormone whose secretion is adjusted to night length. The photoperiodic variation in circulating melatonin has been shown to synchronize reproductive activity with seasons, but the mechanisms involved in this effect of melatonin were so far unknown. Recently we have observed that Kiss1 mRNA level in the arcuate nucleus of the Syrian hamster is lower in short photoperiod, when animals are sexually quiescent. Notably, intracerebroventricular infusion of Kiss1 gene product, kisspeptin, in hamsters kept in short photoperiod is able to override the inhibitory photoperiod and to reactivate sexual activity. The inhibition of Kiss1 expression in short photoperiod is driven by melatonin because pinealectomy prevents decrease in Kiss1 mRNA level in short photoperiod and melatonin injection in long photoperiod down regulates Kiss1 expression. Whether melatonin acts directly on arcuate Kiss1 expressing neurons or mediates its action via interneurons is the subject of the current investigations.     

Phytochrome B mediates the photoperiodic control of tuber formation in potato

To determine whether phytochrome B is involved in the response of potato plants to photoperiod, a potato PHYB cDNA fragment was inserted in the antisense orientation behind the 35S CaMV promoter in Bin19 and this construct was transformed into Solanum tuberosum ssp. andigena plants which normally require short days for tuberization. Two independent transformants were obtained that had much lower levels of PHYB mRNA and protein, and which exhibited phenotypes characteristic of phyB mutants, for example, elongated stems and decreased chlorophyll content. The level of phyA, and of several phytochrome A-controlled responses, was unaffected in these plants. The photoperiodic control of tuberization in these antisense PHYB plants was abolished, the plants tuberizing in short day, long day, or short day plus night break conditions. This result shows that phytochrome B is required for the photoperiodic control of tuberization in potato ( Solanum tuberosum ssp. andigena ) and that it regulates this developmental process by preventing tuber formation in non-inductive photoperiods rather than by promoting tuberization in inductive photoperiods.     

KiSS-1: a likely candidate for the photoperiodic control of reproduction in seasonal breeders

In seasonal species, photoperiod exerts tight regulation of reproduction to ensure that birth occurs at the most favorable time of yr. A distinct photoneuroendocrine circuit composed of the retina, suprachiasmatic nucleus (SCN) of the hypothalamus, and pineal gland transduces daylength into a rhythmic secretion of melatonin. The duration of the night-time rise of this hormone conveys daylength information to the organism. Melatonin is known to mediate the control of seasonal reproduction, but how it modulates sexual activity is far from understood. Recent data indicate that the product of the KiSS-1 gene is a potent stimulator of the hypothalamic-pituitary-gonadal axis and may play, together with its receptor GPR54, a central role in the neuroendocrine regulation of gonadotropin secretion. This article briefly reviews these findings and presents arguments that KiSS-1 could take part in the seasonal control of reproduction.     

Two-step photoperiodic and hormonal control of reproduction in the female beetle, Pterostichus nigrita

The carabid P. nigrita is a short-day/long-day insect. Short days with less than 15.0 hr of light per day induce pre-vitellogenesis. Vitellogenesis only takes place in subsequent long days with more than 13,1 hr of light. In the range from ld 13:11 to ld 16:8 egg production is possible without a change in photoperiod. Pre-vitellogenesis is induced by the corpus allatum hormone. Implantation of active corpora allata or injection of juvenile hormone substitutes for short-day photoperiods. Histological investigations and implantation experiments revealed that for vitellogenesis some neurosecretion is necessary. Ecdysterone cannot replace this neurosecretion.     

Maternal photoperiodic history affects offspring development in Syrian hamsters

During the first 7 weeks of postnatal life, short day lengths inhibit the onset of puberty in many photoperiodic rodents, but not in Syrian hamsters. In this species, timing of puberty and fecundity are independent of the early postnatal photoperiod. Gestational day length affects postnatal reproductive development in several rodents; its role in Syrian hamsters has not been assessed. We tested the hypothesis that cumulative effects of pre- and postnatal short day lengths would restrain gonadal development in male Syrian hamsters. Males with prenatal short day exposure were generated by dams transferred to short day lengths 6 weeks, 3 weeks, and 0 weeks prior to mating. Additional groups were gestated in long day lengths and transferred to short days at birth, at 4 weeks of age, or not transferred (control hamsters). In pups of dams exposed to short day treatment throughout gestation, decreased testis growth was apparent by 3 weeks and persisted through 9 weeks of age, at which time maximum testis size was attained. A subset of males (14%), whose dams had been in short days for 3 to 6 weeks prior to mating displayed pronounced delays in testicular development, similar to those of other photoperiodic rodents. This treatment also increased the percentage of male offspring that underwent little or no gonadal regression postnatally (39%). By 19 weeks of age, males housed in short days completed spontaneous gonadal development. After prolonged long day treatment to break refractoriness, hamsters that initially were classified as nonregressors underwent testicular regression in response to a 2nd sequence of short day lengths. The combined action of prenatal and early postnatal short day lengths diminishes testicular growth of prepubertal Syrian hamsters no later than the 3rd week of postnatal life, albeit to a lesser extent than in other photoperiodic rodents.     

Latitude of origin influences photoperiodic control of reproduction of deer mice (Peromyscus maniculatus)

Three subspecies of Peromyscus maniculatus originating from different latitudes were maintained from birth in light dark cycles that provided between 10 and 18 h of light per day. At 50 days of age, Chihuahua, Mexico mice (latitude of origin 27 degrees N) and South Dakota, U.S.A. mice (44 degrees N) kept in the 10L:14D photoperiod had reduced gonadal and seminal vesicle weights and a lower spermatogenic index than corresponding mice kept in a 14L:10D photoperiod. Some Chihuahua and South Dakota mice, apparently constituting nonphotoperiodic subpopulations, developed their gonads while kept in the short-day photoperiod. The critical day length for stimulation of sexual maturation was greater for mice from Manitoba, Canada (55 degrees N) than for mice from the lower latitudes. At 70 days of age, testes and seminal vesicle weights, and the spermatogenic index of Manitoba mice in the 14L:10D photoperiod, were lower than those of animals maintained in 16L:8D and 18L:6D photoperiods. Responsiveness to short day lengths was greater among adult South Dakota than adult Chihuahau mice and melatonin treatment significantly reduced testes weights of South Dakota but not of Chihuahua adult mice. Photoperiodic regulation of the reproductive system varies with latitude of origin. Differences in the critical day length necessary for stimulating development of functional reproductive activity and variations in the percent of photoperiodic animals within each subspecies, appear to contribute to latitudinal gradients in reproduction.     

The thyroid and photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea)

To explore the role of the thyroid gland in the control of seasonal reproduction in obligately photoperiodic American tree sparrows (Spizella arborea), the effects of (1) thyroxine administered in drinking water to thyroid-intact photosensitive or photorefractory birds, and (2) radiothyroidectomy before and after photostimulation and during photorefractoriness were examined. Chronic administration of pharmacological doses of thyroxine induced testicular growth and usually regression in initially photosensitive birds held on short or intermediate daylengths. Some thyroxine-treated birds with regressed testes were absolutely photorefractory, but most remained photosensitive. Exogenous thyroxine never induced testicular growth in photorefractory birds moved to short days, though it often impeded, and sometimes even blocked, the recovery of photosensitivity. Although circumstantial, these effects of exogenous thyroxine are consistent with an hypothesis that assigns to thyroid hormones two roles — one stimulatory and the other inhibitory — in the control of seasonal reproduction. Radiothyroidectomy before photostimulation inhibited (but did not prevent) photoinduced testicular growth, blocked spontaneous testicular regression, suppressed molt, and prevented photorefractoriness. Moreover, as demonstrated by testicular growth after thyroxine replacemnt therapy, radiothyroidectomy during photorefractoriness later restored photosensitivity despite continued photostimulation. Thus, euthyroidism is an essential condition for maximizing (but not for initiating) photoinduced testicular growth and for triggering and maintaining photorefractoriness in photostimulated tree sparrows. However, when performed early during photostimulation, radiothyroidectomy neither immediately induced nor later blocked spontaneous testicular regression. Thus, endogenous thyroid hormones and long days may interact during a critical period to program a sequence of physiological events that plays out as photorefractoriness in chronically photostimulated birds. Such an organizational event cannot be permanent, for seasonal reproduction is episodic and its control mechanism necessarily cyclic. Because thyroidectomy simulated the well-known restorative effect of short days (and exogenous thyroxine impeded it), short days may dissipate photorefractoriness by creating a milieu wherein thyroid hormones are deficient or inactive.Abbreviations ANOVA analysis of variance - bTSH bovine thyroid stimulating hormone - GnRH gonadotropin-releasing hormone - LH luteinizing hormone - nL: nD daily light: dark regime (n is duration in hours) - SEM standard error of the mean - SNK Student-Newman-Keuls test - T₄ thyroxine - TH thyroid hormone - TR thyroid hormone receptor     

Maternal transfer of photoperiodic information influences the photoperiodic response of prepubertal Djungarian hamsters (Phodopus sungorus sungorus)

Daylengths during the spring are repeated in reverse order in the autumn. For some photoperiodic species, a given photoperiod may be stimulatory for reproduction in the spring and inhibitory in the autumn. The mechanisms regulating this type of seasonal response have, until recently, remained a mystery. Horton (1984a) showed in Microtus montanus that the photoperiod experienced by the mother influences the gonadal development of her young after weaning. To determine if this phenomenon is characteristic of other photoperiodic rodents, adult Djungarian hamsters were paired on 16L:8D, 14L:10D, or 12L:12D. Young males born from these pairings were killed at 15, 28, and 34 days of age to assess gonadal development (testes weight). At 15 days testicular development was identical in all groups; by 28 days, however, males raised in 16L:8D or 14L:10D exhibited a greater degree of testicular development than those raised in 12L:12D. Next, females maintained on each of the three photoperiods throughout gestation were transferred, with their offspring, to the other two photoperiods at birth. Postnatal exposure to 14L:10D or 12L:12D inhibited testicular development in young that had been gestated on 16L:8D. Both 16L:8D and 14L:10D stimulated testicular growth in animals that had been gestated on 12L:12D or 14L:10D. Therefore, a) 16L:8D stimulates testicular growth in all animals, b) 12L:12D inhibits testicular growth in all animals, and c) the testicular response to 14L:10D depends on the photoperiod experienced by the mother during pregnancy.(ABSTRACT TRUNCATED AT 250 WORDS)     

Ventromedial hypothalamic mediation of photoperiodic gonadal responses in male Syrian hamsters.

Short day lengths induce testicular regression in seasonally breeding Syrian hamsters. To test whether the ventromedial hypothalamus is necessary to maintain reproductive quiescence once testicular regression has been achieved, photoregressed male hamsters were subjected to lesions of the ventromedial hypothalamus (VMHx), pinealectomy (Pinx), or sham operation (Sham). VMHx hamsters underwent accelerated gonadal recrudescence compared to Pinx and Sham hamsters. Recovery of prolactin concentrations (PRL) to values characteristic of long-day hamsters was hastened in the VMHx animals compared to Sham hamsters. Concentrations of follicle stimulating hormone (FSH) increased prematurely in both the VMHx and Pinx animals, beginning a few weeks after surgery. By the time the gonads had undergone recrudescence and the hamsters were refractory to melatonin, PRL and FSH concentrations had returned to baseline long-day values in all groups; there was no evidence of hypersecretion of either hormone in any of the animals with lesions. Melatonin concentrations of VMHx hamsters did not differ from those of sham-operated animals, but because only a single determination was made, it remains possible that VMH damage altered the duration of nightly melatonin secretion. An intact VMH appears to be essential for the continued maintenance of reproductive suppression induced by exposure to short day lengths; these and earlier findings suggest that the VMH-dorsomedial hypothalamic complex mediates regression of the reproductive apparatus during decreasing day lengths of late summer and early autumn and also is necessary to sustain regression during the winter months.     

Circadian and photoperiodic effects of brief light pulses in male Djungarian hamsters

The effects of brief light pulses (1-60 min in duration) on the circadian rhythm of locomotor activity and/or the neuroendocrine-gonadal axis was investigated in male Djungarian hamsters. Exposure of hamsters free-running in constant darkness to a single 1-h pulse of light induced phase-dependent phase shifts in the rhythm of locomotor activity. The general shape of the "phase-response curve" was similar to that observed in other animals; phase-delays and phase-advances were induced by light pulses delivered in the early and late subjective night, respectively, while light pulses during the subjective day induced little or no phase-shift in the activity rhythm. Animals exposed for 7 days to 1-min of light during the night in animals otherwise exposed to 6L:18D resulted in increased levels of serum FSH and testicular weight. Daily exposure to two 1-h or two 10-min pulses of light (but not two 1-min pulses) for 10 days resulted in stable entrainment of the activity rhythm as well as testicular weight gains and serum FSH increases. When two 10-min pulses of light were presented 8 and 16 h apart, some animals showed a short-day entrainment pattern (i.e., locomotor activity confined to the long period of darkness) while other animals showed a long-day entrainment pattern (i.e., locomotor activity confined to the short period of darkness). Importantly, the stimulatory effects of light on neuroendocrine-gonadal activity were clearly dependent on the phase-relationship between the light pulses and the circadian rhythm of locomotor activity.(ABSTRACT TRUNCATED AT 250 WORDS)     

Melatonin mediates alternation of seasonality in Syrian hamsters

The annual cycle of reproductive activity in the Syrian hamster, Mesocricetus auratus, is the result of interaction between seasonal changes in daylength (photoperiodism) and seasonal changes in responsiveness to daylength (seasonality). The present experiment was designed to investigate the role of the pineal gland and its hormone, melatonin, in the alternation of seasonality (scotosensitivity and scotorefractoriness). Male hamsters were maintained on short daylengths (10L:14D) to establish scotorefractoriness, and then they were transferred to long daylengths (14L:10D) for conversion to scotosensitivity (sensitive to short daylengths). Before transfer to long daylengths, some of the hamsters were pinealectomized and others were sham-operated or unoperated. Some of the pinealectomized hamsters received single daily melatonin or saline injections while on long daylengths. After 14 wk on long daylengths, the hamsters were transferred to short daylengths for 10 wk to test for conversion to scotosensitivity. Pinealectomized hamsters were given three daily melatonin injections while on short daylengths. Such treatment is known to promote gonadal regression in scotosensitive but not in scotorefractory hamsters. Examination of testes after the short daylength interval revealed that exposure of nonpinealectomized hamsters to long daylengths had reestablished scotosensitivity (regressed testes). Pinealectomized hamsters that received no melatonin replacement while on long daylengths remained scotorefractory (enlarged testes), whereas those that received single daily injections of melatonin during long daylengths were found to be scotosensitive. These results indicate that a daily pulse of melatonin during expsoure to long daylengths has an important role in reestablishing responsiveness (scotosensitivity) to short daylengths.     

Maternal transfer of photoperiodic information in Siberian hamsters. IV. Peripubertal reproductive development in the absence of maternal photoperiodic signals during gestation

Peripubertal reproductive development of Siberian hamsters is influenced by photoperiodic information received during gestation; the maternal pineal is important for this process. We observed that in the absence of the maternal pineal, the fetus appears to receive no information about gestational photoperiods. This is not the equivalent of receipt of a long-day signal by the fetus. Pinealectomized and sham-operated pregnant females were exposed to photoperiods of 12L:12D, 14L:10D, 16L:8D, or constant light (LL); young were reared from birth to 28 days of age in LL or 14L:10D. Regardless of the gestational photoperiod, LL-reared male young born to pinealectomized dams had smaller testes than LL-reared young of pineal-intact dams exposed to 16L:8D while pregnant. Thus, pinealectomy did not result in transmission of a long-day signal, nor did young born of pinealectomized dams receive short- or intermediate-day signals. Unlike young of pineal-intact females exposed to 12L:12D or 14L:10D while pregnant, young born of pinealectomized dams had small testes when reared in 14L:10D, irrespective of gestational photoperiod. Uterine weights of female young presented similar patterns of responses. In a second experiment, adult females were entrained to 12L:12D, 14L:10D, or 16L:8D for 3 wk prior to pinealectomy to determine if the effect of maternal pinealectomy would be altered. Entrainment to the new photoperiod prior to surgery did not alter the effects of maternal pinealectomy.     

Changes in social behavior of the male golden hamster accompanying photoperiodic changes in reproduction

Testicular regression and decreased serum testosterone levels result when male hamsters are placed in a short-day photoperiod, and these changes are reversed after reexposure to long-days. The present study was undertaken to determine whether these physiological changes lead to modifications in social behavior in the male hamster. Animals in a nonstimulatory short-day (LD 6:18) or a stimulatory long-day (LD 14:10) photoperiod were observed every 3 weeks for 21 weeks. After 9 weeks, half of the LD 6:18 males were returned to LD 14:10 and showed rapid testicular recrudescence. The other half remained in LD 6:18 and showed a slower rate of testicular recrudescence. Assessment of aggression was accomplished by placing an intruder in the home cage of a test animal and recording latency to attack, decisive encounters, number of attacks, and number of aggressive postures. Dominance was evaluated in a neutral arena with opponents of different weights, using the same parameters. Scent-marking was recorded in response to both bedding from an intact male and bedding from an ovariectomized female in a clean cage. Short-day animals undergoing testicular regression showed heightened levels of aggression and an upward shift in their dominance status. Alteration of the photoperiod did not affect the pattern or number of scent marks. As animals underwent testicular recrudescence, there was a return to lower levels of aggression and to a lower dominance status. Males undergoing rapid testicular recrudescence also showed the most rapid decline in aggressive behaviors. These results suggest that levels of agonistic behavior in the male hamster are inversely related to serum testosterone levels. Scent-marking appears to be unreleated to androgen levels in the male hamster and its role in hamster social behavior remains unclear.     

Testicular recrudescence in intermediate day lengths reflects loss of photoperiodic memory in Siberian hamsters

Siberian hamsters transferred from a long (16 h light/day [16 L]) to an intermediate (13.5 L) day length (DL) undergo testicular regression within 2 months followed approximately 2 months later by "spontaneous" testicular recrudescence. Recovery of gonadal function after prolonged exposure to intermediate DLs is thought to reflect development of neuroendocrine refractoriness to intermediate-duration melatonin signals. The authors tested the alternative hypothesis that testicular recrudescence in 13.5 L occurs when the "memory" for the 16-L photoperiod fades and hamsters can no longer compare the 13.5-L to the prior 16-L day length. Adult hamsters transferred from 16 L to 13.5 L that underwent testicular involution were either maintained continuously in 13.5 L for 41 weeks or given a supplementary 2-week treatment of 16 L before being returned to 13.5 L. The supplementary treatment was administered either after hamsters had been in 13.5 L for 10 weeks and had involuted testes, or after 24 weeks, when the gonads had undergone recrudescence. The authors found that 16 L treatment administered at week 10 delayed final gonadal recrudescence by approximately 12 weeks; similar 16-L treatment at week 24 induced a second gonadal regression when animals were returned to 13.5 L. The most parsimonious hypothesis to account for these findings is that gonadal recrudescence in intermediate DLs reflects fading of the "memory" for prior long DLs rather than induction of refractoriness to melatonin signals generated in intermediate DLs.     

Contrasting types of photoperiodic response in the control of dormancy

Abstract The effect of night-break or day-extension treatments with red (R) and/or far-red (FR) light were examined in the control of dormancy and extension growth in Weigela florida and Picea abies. Dormancy in Weigela (as assessed by the continued production of new leaves) was completely prevented by a 30 min night-break treatment with R: the effect of R was prevented by a subsequent exposure to 30 min FR. A day-extension treatment for 8.25 h with R or with R+FR also completely prevented dormancy, irrespective of whether it was given before or after a short day (SD) in sunlight. There was no significant difference between any dayextension treatment, nor between day-extension treatments and a night-break with R. Dormancy in Picea (as assessed by the maintenance of shoot growth) was also delayed by a night-break with R but less effectively than the most effective day-extension. A day-extension treatment for 9 h with R light was more effective when it preceded than when it followed a SD in sunlight. The addition of FR in the second but not in the first 9 h of a 17 h photoperiod increased its effectiveness. It is concluded that the mechanisms of the control of dormancy must differ in the two species. A day-extension for 16 h with light from tungstenfilament lamps increased stem elongation in Weigela when compared with an R night-break. This resulted from an increase in internode length and there was no significant difference between the two treatments in their effect on leaf production.     

Gibberellins in the control of photoperiodic flower transition in Pharbitis nil

The role of gibberellins in the photoperiodic flower induction of short-day plant Pharbitis nil has been investigated. It has been found that the endogenous content of gibberellins in the cotyledons of P. nil is low before and after a 16-h-long inductive dark period. During the inductive night the content of gibberellins is high at the beginning of darkness and about the middle of the dark period. Exogenous GA₃ when applied to the cotyledons of non-induced plants does not replace the effect of the inductive night but it can stimulate the intensity of flowering in plants cultivated on suboptimal photoperiods. GA₃ could also reverse the inhibitory effect of end-of-day far-red light irradiation on P. nil flowering. 2-Chloroethyltri-methylammonium chloride (CCC) applied to the cotyledons during the inductive night also inhibited flowering. GA₃ could reverse the inhibitory effect of CCC. The obtained results strongly suggest that gibberellins are involved in the phytochrome controlled transition of P. nil to flowering. Their effect could be additive to that of photoperiodic induction.