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Am J Physiol Regul Integr Comp Physiol 292: R1315-R1319, 2007. First published November 16, 2006; doi:10.1152/ajpregu.00396.2006 Free Article
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SLEEP AND TEMPERATURE REGULATION

Differential response of type 2 deiodinase gene expression to photoperiod between photoperiodic Fischer 344 and nonphotoperiodic Wistar rats

Shinobu Yasuo,1 Miwa Watanabe,1 Masayuki Iigo,2 Takahiro J. Nakamura,1 Tsuyoshi Watanabe,1 Tsuyoshi Takagi,1 Hiroko Ono,1 Shizufumi Ebihara,1 and Takashi Yoshimura1,3

1Division of Biomodeling, Graduate School of Bioagricultural Sciences and 3Institute for Advanced Research, Nagoya University, Chikusa-ku, Nagoya; and 2Department of Applied Biological Chemistry, Faculty of Agriculture, Utsunomiya University, Mine-machi, Utsunomiya, Tochigi, Japan

Submitted 7 June 2006 ; accepted in final form 14 November 2006


   ABSTRACT
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The molecular basis of seasonal or nonseasonal breeding remains unknown. Although laboratory rats are generally regarded as photoperiod-insensitive species, the testicular weight of the Fischer 344 (F344) strain responds to photoperiod. Recently, it was clarified that photoperiodic regulation of type 2 iodothyronine deiodinase (Dio2) in the mediobasal hypothalamus (MBH) is critical in photoperiodic gonadal regulation. Strain-dependent differences in photoperiod sensitivity may now provide the opportunity to address the regulatory mechanism of seasonality by studying Dio2 expression. Therefore, in the present study, we examined the effect of photoperiod on Dio2 expression in photoperiod-sensitive F344 and photoperiod-insensitive Wistar rats. A statistically significant difference was observed between short and long days in terms of testicular weight and Dio2 expression in the F344 strain, while no difference was observed in the Wistar strain. These results suggest that differential responses of the Dio2 gene to photoperiod may determine the strain-dependent differences in photoperiod sensitivity in laboratory rats.

mediobasal hypothalamus; testicular weight; photoperiodism

FOR MANY SPECIES living in temperate zones, annual changes in photoperiod are the primary factor that regulates the timing of reproduction. The photoperiodic response allows animals to bear their offspring during the food-abundant season to maximize survival. On the other hand, laboratory rats have been bred for many generations to obtain maximal reproductive efficiency under constant temperature and light conditions with ad libitum food availability; this has resulted in the loss of reproductive responsiveness to photoperiod (27). Indeed, the Wistar and Sprague-Dawley inbred rat strains are generally regarded as nonseasonal breeders (23, 28, 36). Nevertheless, some experimental treatments such as neonatal androgen injection, chronic exposure to exogenous testosterone, and olfactory bulbectomy can induce a reproductive responsiveness to photoperiod in these rat strains (23, 28, 34, 36). Extreme lighting conditions, such as constant darkness or blinding, also inhibit gonadal development in Wistar rats (15). These reports indicate that neuroendocrine components that regulate photoperiodic response are still preserved in the Wistar and Sprague-Dawley strains. In contrast, the Fischer 344 (F344) inbred strain of rat exhibits robust photoresponsiveness, even under normal conditions, exhibiting slower gonadal growth on exposure to short days (11, 14). Gonadal development of F344 rats is also inhibited by blinding (17) or by melatonin injection (12). A recent study has also reported that the ACI, PVG, and BUF inbred rat strains are also photoperiod sensitive (6), suggesting that sensitivity to photoperiod varies across different rat strains. However, the underlying mechanism that regulates the variation in photoresponsiveness is not well understood.

In mammals, the photoperiodic response of gonads is regulated by a daily cycle of melatonin secretion from the pineal gland (1, 27). Melatonin synthesis and secretion occur during the night; therefore, in many species, the pattern of melatonin secretion is influenced by day length. For example, the melatonin secretion patterns of hamsters are greatly affected by the photoperiod, exhibiting a longer duration under short-day conditions and a shorter duration under long-day conditions (8, 16). These changes in duration of nocturnal melatonin secretion into the blood are generally accepted to be critical to melatonin's effect on gonadal regulation (2, 5). Although the site at which melatonin acts to induce photoperiodic gonadal response has yet to be elucidated, lesion studies in Syrian hamsters have demonstrated the involvement of several brain regions, including the dorsomedial hypothalamus and the ventromedial hypothalamus of the mediobasal hypothalamus (MBH) (18, 21), the anterior hypothalamic nucleus (10), and the bed nucleus of the stria terminalis (26). Among these regions, the action of melatonin on the MBH seems to be conserved in various species. For example, melatonin microimplants placed in the premammillary hypothalamic area of the MBH produced a short-day effect on luteinizing hormone secretion in sheep, whereas implants located in other brain regions were ineffective (19, 20).

Long-day-induced type 2 iodothyronine deiodinase (Dio2) expression in the MBH is critical in the photoperiodic response of gonads in birds (42). Dio2 catalyzes the conversion of the prohormone thyroxine (T4) to bioactive triiodothyronine (T3) and controls the local thyroid hormone concentration (3, 42). Furthermore, in Japanese quail, T3 administration to the MBH mimics the long-day effect on gonadal regulation (38, 42). In mammals, the Dio2 expressed in the MBH also appears to be involved in the regulation of gonadal growth, since photoperiodic regulation of Dio2 expression is also observed in the MBH of the Djungarian hamster (37), the Syrian hamster (29), and the Saanen goat (39) and subcutaneous injection of T3 under short days mimics the long-day effect on testicular growth in Djungarian hamsters (7). Moreover, Dio2 expression is suppressed in both Djungarian and Syrian hamsters by daily injections of melatonin (29, 37), suggesting that in photoperiodic gonadal regulation Dio2 expression is involved in the pathway between the melatonin signal and the neuroendocrine-gonadal axis.

Therefore, in the present study, we assumed that the different photoresponsiveness among rat strains is determined by Dio2 expressed in the MBH. To test this hypothesis, we examined the effect of short and long days on Dio2 expression in the F344 and Wistar strains.


   MATERIALS AND METHODS
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Animals. All of the male F344 and Wistar-Imamichi 3-wk-old rats used in the present study were obtained from a local dealer and housed in light-tight boxes in which light cycles were provided. The boxes were placed in a room at a temperature of 24 ± 1°C. Since food restriction is known to enhance the suppressive effect of short days on reproductive maturation in F344 rats (13) and deer mice (22), a low-calorie diet (ZF for herbivorous animals; Oriental Yeast, Tokyo, Japan) was provided to both F344 and Wistar rats to maximize the photoperiodic response in this study. Food and water were available ad libitum and were replenished at least twice a week. The present study was approved by the Committee on Animal Experiments of the Graduate School of Bioagricultural Sciences, Nagoya University.

Effect of photoperiod on Dio2 expression. Rats were maintained under 8:16-h light-dark (8L16D) conditions before the experiment. At 7 wk of age, they were randomly divided into two groups; one group was transferred to the long-day conditions (16:8-h light-dark, 16L8D), while the other group was maintained under short-day conditions (8L16D). Rats were killed by decapitation at 9 wk of age, and the brains were collected for in situ hybridization. The brains were collected at midday (8 h after light onset under long-day conditions and 4 h after light onset under short-day conditions).

Daily melatonin injections. Rats were maintained under 14:10-h light-dark cycle (14L10D) throughout the experiment. The melatonin injection was administered according to Heideman et al. (12). At 5 wk of age, a daily subcutaneous injection of melatonin (100 µg of melatonin dissolved in 0.1 ml of 10% ethanol and 0.9% NaCl) or vehicle (0.1 ml of 10% ethanol/saline) was administered 1 h before the initiation of light offset. Injections were carried out for 3 wk followed by brain sampling.

In situ hybridization. In situ hybridization was carried out according to Yoshimura et al. (41). Antisense 45-mer oligonucleotide probes for Dio2 (5'-tgcttgagcagaatgaccgagtcatagagcgccaggaagaggcag-3') were labeled with [33P]dATP (NEN Life Science Products, Boston, MA) using terminal deoxyribonucleotidyl transferase (GIBCO BRL, Frederick, MD). Coronal sections (20 µm thick) of the MBH were prepared with 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 with a computed image-analyzing system (MCID; Imaging Research, St. Catherines, ON, Canada) and converted into the radioactive value (nCi) with the 14C standard measurements.


   RESULTS
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Photoperiodic regulation of gonadal growth in F344 strain but not Wistar strain. We measured the testicular weights of F344 and Wistar strains maintained under short- or long-day conditions for 2 wk. The testicular weight of the Wistar strain did not differ between short and long days (Mann-Whitney U-test, P > 0.05), while that of the F344 strain differed significantly (Mann-Whitney U-test, P < 0.01) (Fig. 1). This result was consistent with previous reports that the Wistar strain is a reproductively nonphotoperiodic strain, while the F344 strain is sensitive to photoperiod (11, 12, 14, 17, 28).


Figure 1
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  		Fig. 1. Photoperiodic response of gonads in the Fischer 344 (F344) strain. Effects of short days [SD; 8:16-h light-dark cycle (8L16D)] or long days [LD; 16:8-h light-dark cycle (16L8D)] on the weight of paired testes were examined in Wistar and F344 strains. Animals were raised under short-day conditions, and the long-day group was transferred to LD for 2 wk. A significant difference was observed in the testicular weight of the F344 strain (Mann-Whitney U-test, *P < 0.01). Values are means ± SE (n = 5 or 6).

 
Photoperiodic regulation of Dio2 mRNA in F344 strain but not Wistar strain. We examined Dio2 expression in the MBH of F344 and Wistar strains under short- and long-day conditions. In both strains, Dio2 mRNA was observed in the cell-clear zone overlying the tuberoinfundibular sulcus (TIS), which is localized in the lateral portion of the median eminence, and the ependymal cell layer lining the infralateral walls of the third ventricle (EC), as previously described in rats (9, 33) and the Djungarian hamster (37). When the expression levels of Dio2 in the TIS and EC were compared under short- and long-day conditions, a significant difference was observed in the TIS of the F344 strain (Mann-Whitney U-test, P < 0.05), while no difference was observed in the EC (Fig. 2). In contrast, photoperiodic treatment did not affect Dio2 expression in either regions of the Wistar strain (Mann-Whitney U-test, P > 0.05; Fig. 2).


Figure 2
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  		Fig. 2. Photoperiodic response of type 2 iodothyronine deiodinase (Dio2) expression in the F344 strain. Effects of short days (8L16D) or long days (16L8D) on Dio2 mRNA in the mediobasal hypothalamus (MBH) of Wistar and F344 strains were examined. Representative autoradiograms are shown at top. Dio2 mRNA was observed in the cell-clear zone overlying the tuberoinfundibular sulcus (TIS; arrowheads) and the ependymal cell layer lining the infralateral walls of the third ventricle (EC; arrows). Filled bars, level of Dio2 expression under short-day conditions; open bars, expression under long-day conditions. A significant difference between short and long days was detected in the TIS of the F344 strain (Mann-Whitney U-test, *P < 0.05). Values are means ± SE (n = 5 or 6).

 
Daily melatonin injections suppress Dio2 expression in both strains. Since daily melatonin injections during late afternoon suppress Dio2 expression in the MBH of Djungarian and Syrian hamsters (29, 37), we next examined the effect of daily melatonin injections on Dio2 expression in F344 and Wistar strains under long-day conditions. This experimental design is known to mimic the short-day effect on gonadal growth in the Syrian hamster (32), the Djungarian hamster (31), and the F344 rat (12). As a result, Dio2 expression in the TIS and EC was suppressed in both F344 (Mann-Whitney U-test, P < 0.01) and Wistar (Mann-Whitney U-test, P < 0.01) strains (Fig. 3).


Figure 3
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  		Fig. 3. Daily melatonin injections suppress Dio2 mRNA in the MBH of both Wistar and F344 strains. Animals were injected for 3 wk with melatonin or vehicle 1 h before lights off under long-day conditions (14:10 light-dark cycle). Representative autoradiograms are shown at top. Dio2 expression was observed in the TIS (arrowheads) and the EC (arrows). Filled bars, level of Dio2 expression in rats injected with melatonin; open bars expression in rats injected with vehicle. Significant differences were detected in the TIS and the EC of both strains (Mann-Whitney U-test, **P < 0.01). Values are means ± SE (n = 5 or 6).

 

   DISCUSSION
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The photoperiodic regulation of Dio2 in the MBH has been demonstrated to play a critical role in the photoperiodic regulation of gonads (42). In the case of long-day breeders such as the Japanese quail and Djungarian and Syrian hamsters, Dio2 expression in the MBH is higher under long-day conditions than under short-day conditions (29, 37, 40, 42). Similarly, the results of this study demonstrated higher Dio2 expression in the TIS of the photoperiod-sensitive F344 strain under long-day conditions; this was accompanied by an increase in testicular mass. In contrast, Dio2 expression and testicular mass of the Wistar strain were not affected by the photoperiod as recently reported (29). These results support the hypothesis that in rats, reproductive seasonality is also regulated by the photoperiodic regulation of Dio2 expressed in the MBH.

It is well established that patterns of nocturnal melatonin secretion from the pineal gland control the photoperiodic gonadal response (1, 27) and that melatonin acts on the melatonin binding site within the MBH (18, 21). In a previous study, we demonstrated (37) that the Dio2 mRNA expressed in the MBH of Djungarian hamsters is suppressed by daily melatonin injections administered during the late afternoon under long-day conditions. The suppression of Dio2 mRNA by melatonin is also reported in Syrian hamsters (29). Therefore, we assumed that the responsiveness of Dio2 to the melatonin signal might differ between the F344 and Wistar strains. Thus we next examined the effect of daily melatonin injections on the Dio2 expression in the MBH of both strains. Surprisingly, Dio2 expression was suppressed in both strains. Testicular volume was also suppressed in both strains, although a slight individual variation was observed in the Wistar rats (data not shown). Previous research has also demonstrated that daily melatonin injections in the late afternoon under long days or under a 12:12-h light-dark cycle inhibit testicular development in F344 rats (12) and young Wistar rats (30). These results suggest that both strains are capable of responding to melatonin. Although there is a possibility that changes in testosterone level affected the Dio2 mRNA levels as a secondary effect, this does not appear to be the case. Revel et al. (29) reported that castration under long days or implantation of testosterone under short days does not affect Dio2 mRNA levels in Syrian hamsters.

The similar responsiveness of Dio2 mRNA to melatonin injections in both strains suggests that strain differences of reproductive responsiveness to photoperiod would not be caused by the sensitivity of the reproductive axis to melatonin signals. This hypothesis would be distinct from the case of F344 and Sprague-Dawley rats, because the reproductive system and regulatory system for body mass of Sprague-Dawley rats are unresponsive to melatonin signals, even if melatonin patterns are identical in both strains (25). The differences between Wistar and Sprague-Dawley rats are also obvious in the fact that gonadal development of Wistar rats is inhibited by constant darkness or melatonin injections (15, 30), whereas that of Sprague-Dawley rats does not respond to these treatments (25). Instead, our data lead to the possibility that patterns of melatonin secretion under short- and long-day conditions may differ between Wistar and F344 strains. Indeed, our preliminary data obtained from samples collected every 4 h suggest that the amplitude of nocturnal melatonin peak in F344 rats was higher under short-day than long-day conditions, whereas no differences were seen in Wistar rats (data not shown). It is interesting to note that some reports emphasize not only the duration but also the amplitude of the nocturnal melatonin peak as an important seasonal parameter in gonadal regulation in many photoperiodic animals whose melatonin amplitude varies with the seasons (4, 24, 35). To test this hypothesis, it is important to examine the detailed melatonin profile in F344 and Wistar rats in the future.


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This work was supported by the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN) (to T. Yoshimura).


   ACKNOWLEDGMENTS
 
We thank the Nagoya University Radioisotope Center for the use of their facilities.

Present address of S. Yasuo: Inst. of Anatomy II, Johann Wolfgang Goethe University, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany.


   FOOTNOTES
 

Address for reprint requests and other correspondence: T. Yoshimura, Div. of Biomodeling, Graduate School of Bioagricultural Sciences, Nagoya Univ., Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan (e-mail: takashiy{at}agr.nagoya-u.ac.jp)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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  1. Arendt J. Melatonin and the Mammalian Pineal Gland. London: Chapman and Hall, 1995.
  2. Bartness TJ, Powers JB, Hastings MH, Bittman EL, Goldman BD. The timed infusion paradigm for melatonin delivery: what has it taught us about the melatonin signal, its reception, and the photoperiodic control of seasonal responses? J Pineal Res 15: 161–190, 1993.[Web of Science][Medline]
  3. Bernal J. Action of thyroid hormone in brain. J Endocrinol Invest 25: 268–288, 2002.[Web of Science][Medline]
  4. Brainard GC, Petterborg LJ, Richardson BA, Reiter RJ. Pineal melatonin in Syrian hamsters: circadian and seasonal rhythms in animals maintained under laboratory and natural conditions. Neuroendocrinology 35: 342–348, 1982.[Web of Science][Medline]
  5. Carter DS, Goldman BD. Antigonadal effects of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): duration is the critical parameter. Endocrinology 113: 1261–1267, 1983.[Abstract/Free Full Text]
  6. Francisco NR, Raymond CM, Heideman PD. Short photoperiod inhibition of growth in body mass and reproduction in ACI, BUF, and PVG inbred rats. Reproduction 128: 857–862, 2004.[Abstract/Free Full Text]
  7. Freeman DA. Exogenous T3 elicits long day reproductive responses in short-day housed Siberian hamsters. In: Abstract Volume of the 10th Meeting of Society for Research on Biological Rhythms, Urbana-Champaign, IL: University of Illinois, p. 123, 2006.
  8. Goldman BD, Hall V, Hollister C, Reppert S, Roychoudhury P, Yellon SM, Tamarkin L. Diurnal changes in pineal melatonin content in four rodent species: relationship to photoperiodism. Biol Reprod 24: 778–783, 1981.[Abstract]
  9. Guadano-Ferraz A, Obregon MJ, St Germain DL, Bernal J. The type 2 iodothyronine deiodinase is expressed primarily in glial cells in the neonatal rat brain. Proc Natl Acad Sci USA 94: 10391–10396, 1997.[Abstract/Free Full Text]
  10. Hastings MH, Roberts AC, Herbert J. Neurotoxic lesions of the anterior hypothalamus disrupt the photoperiod but not the circadian system of the Syrian hamster. Neuroendocrinology 40: 316–324, 1985.[Web of Science][Medline]
  11. Heideman PD, Bierl CK, Galvez ME. Inhibition of reproductive maturation and somatic growth of Fischer 344 rats by photoperiods shorter than L14:D10 and by gradually decreasing photoperiod. Biol Reprod 63: 1525–1530, 2000.[Abstract/Free Full Text]
  12. Heideman PD, Bierl CK, Sylvester CJ. Photoresponsive Fischer 344 rats are reproductively inhibited by melatonin and differ in 2-[125I]iodomelatonin binding from nonphotoresponsive Sprague-Dawley rats. J Neuroendocrinol 13: 223–232, 2001.[CrossRef][Web of Science][Medline]
  13. Heideman PD, Deibler RW, York LM. Food and neonatal androgen interact with photoperiod to inhibit reproductive maturation in Fischer 344 rats. Biol Reprod 59: 358–363, 1998.[Abstract/Free Full Text]
  14. Heideman PD, Sylvester CJ. Reproductive photoresponsiveness in unmanipulated male Fischer 344 laboratory rats. Biol Reprod 57: 134–138, 1997.[Abstract]
  15. Hoffmann J, Kordon C, Benoit J. Effect of different photoperiods and blinding on ovarian and testicular functions in normal and testosterone-treated rats. Gen Comp Endocrinol 10: 109–118, 1968.[CrossRef][Web of Science][Medline]
  16. Illnerova H, Hoffmann K, Vanecek J. Adjustment of pineal melatonin and N-acetyltransferase rhythms to change from long to short photoperiod in the Djungarian hamster Phodopus sungorus. Neuroendocrinology 38: 226–231, 1984.
  17. Leadem CA. Photoperiodic sensitivity of prepubertal female Fischer 344 rats. J Pineal Res 5: 63–70, 1988.[Web of Science][Medline]
  18. Lewis D, Freeman DA, Dark J, Wynne-Edwards KE, Zucker I. Photoperiodic control of oestrous cycles in Syrian hamsters: mediation by the mediobasal hypothalamus. J Neuroendocrinol 14: 294–299, 2002.[CrossRef][Web of Science][Medline]
  19. Lincoln GI, Maeda KI. Reproductive effects of placing micro-implants of melatonin in the mediobasal hypothalamus and preoptic area in rams. J Endocrinol 132: 210–215, 1992.
  20. Malpaux B, Daveau A, Maurice-Mandon F, Duarte G, Chemineau P. Evidence that melatonin acts in the premammillary hypothalamic area to control reproduction in the ewe: presence of binding sites and stimulation of luteinizing hormone secretion by in situ microimplant delivery. Endocrinology 139: 1508–1516, 1998.[Abstract/Free Full Text]
  21. Maywood ES, Hastings MH. Lesions of the iodomelatonin-binding sites of the mediobasal hypothalamus spare the lactotropic, but block the gonadotropic response of male Syrian hamsters to short photoperiod and to melatonin. Endocrinology 136: 144–153, 1995.[Abstract]
  22. Nelson RJ, Marinovic AC, Moffatt CA, Kriegsfeld LJ, Kim S. The effects of photoperiod and food intake on reproductive development in male deer mice (Peromyscus maniculatus). Physiol Behav 62: 945–950, 1997.[CrossRef][Medline]
  23. Nelson RJ, Moffatt CA, Goldman BD. Reproductive and nonreproductive responsiveness to photoperiod in laboratory rats. J Pineal Res 17: 123–131, 1994.[Web of Science][Medline]
  24. Pévet P, Vivien-Roels B, Masson-Pévet M. Annual changes in the daily pattern of melatonin synthesis and release. In: Roles of Melatonin and Pineal Peptides in Neuroimmunomodulation, edited by Fraschini F and Reiter RJ. New York: Plenum, 1991, p. 147–157.
  25. Price MR, Kruse JA, Galvez ME, Lorincz AM, Avigdor M, Heideman PD. Failure to respond to endogenous or exogenous melatonin may cause nonphotoresponsiveness in Harlan Sprague Dawley rats. J Circadian Rhythms 3: 12, 2005.[CrossRef][Medline]
  26. Raitiere MN, Garyfallou VT, Urbanski HF. Lesions in the bed nucleus of the stria terminalis, but not in the lateral septum, inhibit short-photoperiod-induced testicular regression in Syrian hamsters. Brain Res 705: 159–167, 1995.[CrossRef][Web of Science][Medline]
  27. Reiter RJ. The pineal and its hormones in the control of reproduction in mammals. Endocr Rev 1: 109–131, 1980.[Abstract/Free Full Text]
  28. Reiter RJ, Hoffman JC, Rubin PH. Pineal gland: influence on gonads of male rats treated with androgen 3 days after birth. Science 160: 420–421, 1968.[Abstract/Free Full Text]
  29. Revel FG, Saboureau M, Pévet P, Mikkelsen JD, Simonneaux V. Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology 147: 4680–4687, 2006.[Abstract/Free Full Text]
  30. Sizonenko PC, Lang U, Rivest RW, Aubert ML. The pineal and pubertal development. Ciba Found Symp 117: 208–230, 1985.[Medline]
  31. Stetson MH, Sarafidis E, Rollag MD. Sensitivity of adult male Djungarian hamsters (Phodopus sungorus sungorus) to melatonin injections throughout the day: effects on the reproductive system and the pineal. Biol Reprod 35: 618–623, 1986.[Abstract]
  32. Tamarkin L, Lefebvre NG, Hollister CW, Goldman BD. Effect of melatonin administered during the night on reproductive function in the Syrian hamster. Endocrinology 101: 631–634, 1977.[Abstract/Free Full Text]
  33. Tu HM, Kim SW, Salvatore D, Bartha T, Legradi G, Larsen PR, Lechan RM. Regional distribution of type 2 thyroxine deiodinase messenger ribonucleic acid in rat hypothalamus and pituitary and its regulation by thyroid hormone. Endocrinology 138: 3359–3368, 1997.[Abstract/Free Full Text]
  34. Vanecek J, Illnerova H. Effect of photoperiod on the growth of reproductive organs and on pineal N-acetyltransferase rhythm in male rats treated neonatally with testosterone propionate. Biol Reprod 27: 517–522, 1982.[Abstract]
  35. Vivien-Roels B. Seasonal variations in the amplitude of the daily pattern of melatonin secretion in mammalian and non-mammalian vertebrates: possible physiological consequences. In: Comparative Endocrinology and Reproduction, edited by Joy K, Krishna A, and Haldar C. New Delhi: Narosa, 1999, p. 529–542.
  36. Wallen EP, Turek FW. Photoperiodicity in the male albino laboratory rat. Nature 289: 402–404, 1981.[CrossRef][Medline]
  37. Watanabe M, Yasuo S, Watanabe T, Yamamura T, Nakao N, Ebihara S, Yoshimura T. Photoperiodic regulation of type 2 deiodinase gene in Djungarian hamster: possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology 145: 1546–1549, 2004.[Abstract/Free Full Text]
  38. Yamamura T, Yasuo S, Hirunagi K, Ebihara S, Yoshimura T. T3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell Tissue Res 324: 175–179, 2006.[CrossRef][Web of Science][Medline]
  39. Yasuo S, Nakao N, Ohkura S, Iigo M, Hagiwara S, Goto A, Ando H, Yamamura T, Watanabe M, Watanabe T, Oda SI, Maeda KI, Lincoln G, Okamura H, Ebihara S, Yoshimura T. Long-day suppressed expression of type 2 deiodinase gene in the mediobasal hypothalamus of the Saanen goat, a short-day breeder: implication for seasonal window of thyroid hormone action on reproductive neuroendocrine axis. Endocrinology 147: 432–440, 2005.
  40. Yasuo S, Watanabe M, Nakao N, Takagi T, Follett BK, Ebihara S, Yoshimura T. The reciprocal switching of two thyroid hormone-activating and -inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology 146: 2551–2554, 2005.[Abstract/Free Full Text]
  41. Yoshimura T, Suzuki Y, Makino E, Suzuki T, Kuroiwa A, Matsuda Y, Namikawa T, Ebihara S. Molecular analysis of avian circadian clock genes. Brain Res Mol Brain Res 78: 207–215, 2000.[Medline]
  42. Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K, Ebihara S. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426: 178–181, 2003.[CrossRef][Medline]



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