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Photoinducible Phase-Specific Light Induction of Cry1 Gene in the Pars Tuberalis of Japanese Quail

Division of Biomodeling (S.Y., M.W., T.T., S.E., T.Y.), Division of Applied Genetics and Physiology (A.T., K.S.), Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601; and Department of Applied Biological Chemistry (M.I.), Faculty of Agriculture, Utsunomiya University, Mine-machi, Utsunomiya, Tochigi 321-8505, Japan

Address all correspondence and requests for reprints to: Takashi Yoshimura, Ph.D., Division of Biomodeling, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan. E-mail: takashiy{at}agr.nagoya-u.ac.jp.

	Abstract

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Prolactin (PRL) secretion is regulated by photoperiod in mammals and birds. In mammals, the pars tuberalis (PT) in the pituitary is involved in the regulation of photoperiodic regulation of PRL secretion. In birds, however, hypothalamic vasoactive intestinal peptide is implicated in PRL secretion, and physiological roles of the avian PT remain unknown. In the present study, we show that PRL secretion increases under long days and short days with a night interruptive schedule, both of which also cause gonadal growth in Japanese quail. We have also found Cry1 gene expression in the PT of Japanese quail. Cry1 expression was rhythmic under long and short photoperiods in the PT, and the peak was phase delayed under a lengthened photoperiod. Moreover, expression of Cry1 gene was induced by a light pulse but only when given during the photoinducible phase. In our previous study, we have shown rhythmic Per2 gene expression with a peak in the PT during the early day under various photoperiods. When taken together with the results from the present study, different phase relationships between Per2 and Cry1 in the Japanese quail PT under different photoperiods may decode photoperiodic information and regulate photoperiodic PRL secretion in a manner similar to that of mammals.

	Introduction

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IN MANY MAMMALIAN and avian species living in temperate latitudes, prolactin (PRL) secretion is photoperiodically controlled (1, 2). In birds, PRL has long been associated with incubation behavior, parental behavior, and the termination of breeding season (3, 4). The mechanism of initial PRL increase in response to a stimulatory photoperiod has been extensively studied in mammals (5, 6, 7), and it has been shown that pineal melatonin conveys photoperiodic information to the pars tuberalis (PT) of the pituitary stalk, where melatonin receptors are densely localized (8). In the PT, an unidentified factor called tuberalin is thought to be secreted, which then stimulates the release of PRL (9, 10). Several groups have examined the expression of circadian clock genes in the PT and have concluded that their different expression patterns under different photoperiods play an important role in the regulation of photoperiodic PRL secretion (7, 11, 12, 13).

In birds, however, the hypothalamic neuropeptide, vasoactive intestinal peptide (VIP), has been identified to be the avian PRL-releasing hormone (14). In the turkey, hypothalamic VIP content seems to be coupled with the photoperiodic state of bird (15, 16), and active immunization against VIP inhibits photo-induced PRL secretion (17, 18). These observations indicated the involvement of VIP in the photoperiodic control of PRL secretion in birds and suggest that the mechanism for photoinduced PRL secretion in birds is different from that of mammals, whose regulation is independent of hypothalamic regulation (7, 19, 20). However, there is a report indicating that PRL secretion during photoinduction or photorefractoriness is not related to the content of VIP in the basal hypothalamus in starlings (21). In addition, although VIP is secreted by neurons that are concentrated within the mediobasal hypothalamus, in an inclusive area referred to as the infundibular nucleus, lesions of infundibular nucleus, which block the photoperiodic response of the gonads, do not affect photoperiodic PRL secretion (22). Therefore, it seems worthwhile to examine the avian PT in relation with photoperiodic PRL release. Surprisingly, however, few studies have thus far been undertaken that examine the avian PT, leaving the physiological function of the avian PT relatively unknown. In our previous study, we reported on the expression of Per2 and E4bp4 genes in the PT of Japanese quail (23), and we now demonstrate the photoinducible phase-specific light induction of Cry1 gene in relation to PRL secretion. This is the first indication of a molecular link between the avian PT and the photoperiodic control of PRL secretion.

	Materials and Methods

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Animals and housing
Four- or 7-wk-old male Japanese quail (Coturnix coturnix japonica) were obtained from a local dealer and housed in light tight-boxes where light cycles were provided. The boxes were placed in a room at a temperature of 24 ± 1 C. Light was supplied by fluorescent lamps, with a light intensity of 200 lux measured at the level of the bird’s head. Food and water were available ad libitum and were replenished at least once a week. Animals were treated in accordance with the guidelines of Nagoya University.

Expression patterns of Cry1 gene under various light cycles
We examined the expression profiles of Cry1 gene under long photoperiods (LP) [light-to-dark ratio (LD)16:8], short photoperiods (SP) (LD8:16), constant light conditions (LL), constant dark conditions (DD), and night interruptive (NI) cycles. All birds were sampled when 9 wk old. In the case of LP, 7-wk-old birds were kept under LD16:8 for 2 wk before sampling. As for SP, birds were raised under LD8:16 from 4 wk old to 9 wk old. In the LL and DD experiments, 7-wk-old birds were kept under LD12:12 for 2 wk and then transferred to LL or DD. Birds were killed in the first day of LL or DD. In NI experiments, 4-wk-old birds were raised under LD4:20 for 4 wk, and 30-min light pulses were given at Zeitgeber time (ZT)7 (NI7), 13 (NI13), or 21 (NI21) for 10 consecutive days. ZT0 represents light onset. Birds were killed on the 11th day.

Effect of a single light pulse on Cry1 gene expressions
We examined the effect of a single light pulse on Cry1 expression in the PT at three different time points. Birds were raised under LD4:20 from 4 wk old until 9 wk old. A 30-min white light pulse (1600 lux of fluorescent lamps) was given at ZT7 or 13 or 21. Birds were killed by decapitation 90 min after the light pulse, and the brains were immediately removed and frozen on dry ice to avoid degradation of mRNA.

In situ hybridization
In situ hybridization was carried out according to Yoshimura et al. (24). Antisense 45-mer oligonucleotide probes of chicken Cry1 (nucleotides 1742–1786 of GenBank accession number AY034432) and Japanese quail GSU (nucleotide 524–568 of S70833) were labeled with [³³P]dATP (NEN Life Science Products, Boston, MA) using terminal deoxyribonucleotidyl transferase (Life Technologies, Inc., Frederick, MD). Coronal sections (20-µm thickness) of PT were prepared using a Cryostat. Hybridization was carried out overnight at 42 C. Two high-stringency posthybridization washes were performed at 55 C. The sections were air-dried and apposed to Biomax-MR film (Kodak, Rochester, NY) for 2 wk. ¹⁴C standards (American Radiolabeled Chemicals, St. Louis, MO) were included in each cassette, and the relative optical density was measured by using a computed image-analyzing system (MCID, Imaging Research, St. Catherines, Ontario, Canada) and converted into the radioactive value (nCi) using the ¹⁴C standard measurements. Data were normalized by subtracting the value at the stratum cellulare internum, which is located in the same section and does not exhibit a hybridization signal.

Plasma PRL content under various light cycles
We examined plasma PRL content under LP, SP, and NI cycles by RIA. Because it is known that there is a daily rhythm in PRL secretion in European quail (25), we measured PRL content at three time points each day under NI cycles. Under LP and SP, we measured only at ZT18 because plasma PRL content is highest in the dark phase (25). For NI experiments, samples were collected at ZT2, 10, and 18, except for NI21. In the case of NI21, serum collected at ZT22, 6, and 14 were considered as the samples at ZT2, 10, and 18, respectively, because locomotor activity of animals under NI21 starts at ZT21 (26). Plasma PRL was measured by a postprecipitation, double-antibody RIA using purified chicken PRL as a standard and an antichicken PRL antibody raised in rabbits (provided by Dr. A. F. Parlow, Pituitary Hormones and Antisera Center, National Hormone and Peptide Program, Harbor-University of California Los Angeles Medical Center, Torrance, CA), according to the previously described method, with modification (27). Duplicate 50-µl aliquots of plasma were measured in a single assay.

The chicken PRL RIA is confirmed to work in several passerine species other than chicken (28) but not in the Japanese quail. Therefore, a parallelism study has been performed for the validation of the RIA. Parallelism of the inhibition curves for serial 2-fold dilution of the pooled Japanese quail plasma and the chicken PRL standard were tested by parallel line assay (2 x 3 points) using a computer program, Jikken Shien Program, kindly provided by Prof. Wakabayashi (Gunma University, Maebashi, Japan). The inhibition curve for serial 2-fold dilution of the quail plasma was parallel to the curve for the chicken PRL standard (supplemental data). The intraassay coefficient of variation was 2.41%.

	Results

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Plasma PRL content under various light cycles
We examined plasma PRL levels under LP, SP, and NI conditions. A significant increase in PRL concentration was observed under LP compared with SP (Mann-Whitney U test, P < 0.05) (Fig. 1A). Under NI schedule with a 30-min light pulse given at ZT7 (NI7), ZT13 (NI13), or ZT21 (NI21), a significant PRL increase was seen only in birds kept under NI13, and then at all ZTs examined [one-way ANOVA and Fisher’s least-significant-difference (LSD) post hoc test, F(2, 9) = 7.15, P < 0.05 at ZT2; F(2, 9) = 9.59, P < 0.01 at ZT10; F(2, 8) = 13.86, P < 0.01 at ZT18] (Fig. 1B).

View larger version (16K): [in this window] [in a new window]   FIG. 1. Plasma PRL content under (A) LP (LD16:8), SP (LD8:16), and (B) NI cycles, where 30 min of light is given for 10 d at ZT7 (NI7, closed up-pointing triangle) or ZT13 (NI13, open triangle), or ZT21 (NI21, closed down-pointing triangle) under LD4:20 cycles. Serum was collected at ZT18 in LP and SP, and at ZT 2, 10, and 18 in NI experiments. Each value is the mean and SEM (n = 3–5). A, Significant difference was observed between LP and SP (Mann-Whitney U test, P < 0.05). B, Significant differences shown by asterisks (one-way ANOVA, Fisher’s LSD post hoc test; *, P < 0.05; **, P < 0.01).

View larger version (63K): [in this window] [in a new window]   FIG. 2. Expression of Cry1 and GSU in the Japanese quail PT. Representative autoradiograms for Cry1 and GSU expression in the rostral and caudal PT.

View larger version (42K): [in this window] [in a new window]   FIG. 3. Temporal expression profiles of Cry1 mRNA in the PT of Japanese quail under (A) LP (LD16:8), SP (LD8:16), (B) LL, DD, and (C) NI cycles. In NI experiments, a 30-min light pulse was given each day for 10 d at ZT7 (NI7), or (NI13), or ZT21 (NI21) under LD4:20 cycle. Bars at the bottom of each graph represent the light conditions. Representative autoradiograms of PT at ZT2 and ZT14 under each light cycle are shown. IN, Infundibular nucleus; ME, median eminence; IIIV, third ventricle. Each value is the mean ± SEM (n = 3–6). *, Significant difference (Mann-Whitney U test, P < 0.05); **, significant difference (one-way ANOVA, Fisher’s LSD post hoc test, P < 0.01).

Under NI conditions, significant rhythmic expression was observed in birds under NI7 and NI13 conditions [one-way ANOVA, F(5, 18) = 3.303, P < 0.05 for NI7; F(5, 18) = 5.831, P < 0.01 for NI13]. Although the expression profile of the NI21 group was similar to that of the NI7 group, no significant difference was detected in the NI21 group [one-way ANOVA, F(5, 17) = 1.527, P > 0.05]. Under NI13, a photoinducible cycle, a significant increase in expression was observed at ZT14 when compared with those of nonphotoinducible light cycles (NI7 or NI21) [one-way ANOVA, F(2, 8) = 12.37, P < 0.01] (Fig. 3C). The peak time of expression was at ZT14 under NI13, and at ZT10 under NI7 and NI21.

Effect of a single light pulse on Cry1 expression in the PT
To examine the effect of a single light pulse on Cry1 expression in the PT, animals were given a 30-min light pulse at ZT7, 13, and 21 in the dark phase of LD4:20 cycles. Light induction of Cry1 mRNA expression was observed only at ZT13 (Mann-Whitney U test, P < 0.05) (Fig. 4).

View larger version (45K): [in this window] [in a new window]   FIG. 4. Effect of a single light pulse on Cry1 mRNA in the Japanese quail PT given under LD4:20 cycles. Birds exposed to a light pulse (open bar) and control birds (closed bar) were killed 90 min after the light pulse. The bar at the bottom of the graph represents the light condition. Representative autoradiograms of PT are also shown. Each value is the mean and SEM (n = 3–5). *, Significant difference (Mann-Whitney U test, P < 0.05).

	Discussion

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Although the expression of Cry1 was at a very low level under DD, Cry1 expression was rhythmic in other light conditions (i.e. SP, LP, LL). The signal intensity of Cry1 mRNA was increased and the phase of the peak mRNA was delayed under a lengthened photoperiod. Consistent results were also obtained in the NI schedules. We have further shown that light-induced expression of Cry1 gene occurs only at the photoinducible phase. These results suggest that the expression of Cry1 is regulated not only by light, but it is also under the direct control of a circadian clock.

It has been reported that circadian clock genes are expressed in the mammalian PT (7, 11, 12, 13). In ovine PT, activation of Per genes occurs in the early day, whereas activation of Cry genes occurs in the early night. In mammals, the changes in clock gene expression in the PT are caused by pineal melatonin rhythm, because pinealectomy or melatonin receptor (mt1) knockout prevents Per1 mRNA expression (29, 30). Cry1 may also be driven by melatonin, because Cry1 expression is closely linked to the onset of melatonin secretion in Soy ram, and melatonin induces Cry1 expression in rat (7, 31). This temporal association is conserved even in SP and LP, which results in differences in Per-Cry intervals depending on the photoperiod. In mice, protein-protein interactions between PER and CRY affects their stability, nuclear entry, and subsequent gene transcription (32, 33). Therefore, change in the phasing of Per-Cry expression is a potential mechanism by which the long-day and short-day melatonin signals can be decoded. The level of coincidence in turn determines the formation of PER-CRY protein complexes that can control the transcription of other clock genes and downstream genes that dictate the secretory activity of the PRL-releasing factor that drives the lactotrophs to secrete PRL (7). Unlike the situation in mammals, melatonin has no distinct effects on the regulation of photoperiodic time measurement in birds (34). Light directly regulates Cry1 expression, and the temporal expression profiles of Cry1 gene vary, whereas the peak phase of Per2 rhythmicity remains in the early day between LP and SP in the PT of Japanese quail, similar to the situation of the ovine PT (23) (Fig. 5). The factor controlling Cry1 gene expression in the PT is different between sheep (melatonin) and Japanese quail (light); however, it is particularly interesting that the temporal relationship of Per-Cry under LP and SP are conserved between these different species. In mammals, besides Per2 and Cry1, Per1 and Cry2 seem to be involved in the formation of PER-CRY complexes (7, 13). Because the PT is a very small structure, it was difficult to measure the intensity of signals in most of the clock genes, including Cry2 (23). Although we could detect expression of Cry2 in the PT, the signal was extremely weak when compared with Cry1 and Per2, suggesting the dominant role of Cry1 rather than Cry2 (data not shown). In addition, no light induction of Cry2 expression was observed. Although several groups, including ours, tried to isolate Per1 gene in birds, no group has succeeded in isolating it so far, and it may be possible that birds lack functional Per1 gene (24).

View larger version (19K): [in this window] [in a new window]   FIG. 5. Schematic model for the decoding of photoperiodic information in the PT of Japanese quail. Peak Per2 expression occurs in the early day in both LP and SP (23 ). In contrast, light affects Cry1 expression, and the Cry1 peak occurs in the late day under both LP and SP. Thus, the interval between Per2-Cry1 varies depending on the photoperiod. The different Per2-Cry1 association affects the transcription of other circadian clock genes and downstream genes that regulate photoperiodic PRL secretion.

	Acknowledgments

 
We thank Nagoya University Radioisotope Center for use of facilities, Dr. T. Okano (University of Tokyo, Tokyo, Japan) for providing the cCry1 sequence before its availability in GenBank, and Dr. A. F. Parlow for providing the chicken PRL RIA system. We also thank Dr. P. A. Bartell for helpful discussion.

	Footnotes

 
This work was supported by the Program for Promotion of Basic Research Activities for Innovative Biosciences and Grant-in-Aid for Young Scientists from the Ministry of Education, Culture, Sports, Science and Technology (to T.Y.) and for Scientific Research (to S.E.).

Abbreviations: DD, Constant dark conditions; GSU, glycoprotein hormone -subunit; LD, light-to-dark ratio; LL, constant light conditions; LP, long photoperiods; LSD, least-significant-difference; NI, night interruptive; PRL, prolactin; PT, pars tuberalis; SP, short photoperiods; VIP, vasoactive intestinal peptide; ZT, Zeitgeber time.

Received September 25, 2003.

Accepted for publication December 10, 2003.

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