ORIGINAL PAPER
 
KEYWORDS
TOPICS
ABSTRACT
The pars tuberalis (PT) is part of the pituitary that expresses melatonin receptors, therefore it is suggested that PT mediates the effect of melatonin on neuroendocrine functions and may be involved in the photoperiodic regulation of pituitary gland processes. Decoding of the melatonin signalling in the PT is possible thanks to the expression of circadian clock genes in the PT cells. Therefore, the present study was designed to determine circadian and seasonal changes in the expression of biological clock genes in the ewe PT. Two analogical experiments were performed in different photoperiods: 1 month before the summer (long-day photoperiod; LD) and winter (short-day photoperiod; SD) solstice. In each photoperiod, ewes were euthanized after the last blood collection in the middle of the day (n = 6) or night (n = 6). The expression of the basic helix-loop-helix ARNT like 1 (BMAL1), casein kinase 1 epsilon (CK1ε), clock circadian regulator (CLOCK), cryptochrome circadian regulator 2 (CRY2) and period circadian regulator 1 (PER1) genes in the ovine PT was higher (P < 0.05) during the day compared to the night regardless of the season. Only the cryptochrome circadian regulator 1 (CRY1) gene was characterised by a higher (P < 0.05) nocturnal level of expression during both short and long day seasons. The expression of melatonin receptor MTNR1A gene was higher (P < 0.05) during the day in both photoperiodic conditions, and was higher (P < 0.05) during the SD season. It was demonstrated that the direction of circadian changes in the expression of clock genes was relatively constant regardless of the season analysed. However, both diurnal and nocturnal expression of clock genes was higher in the SD season than in the LD photoperiod. This suggests that the protein products of the expression of these genes may exert a more significant effect on the secretory activity of this part of the pituitary gland in the SD season, but elucidating this relationship requires further in-depth research.
FUNDING
This work was supported by the grant from the National Science Centre, Poland No. 2016/23/N/ NZ9/02145.
CONFLICT OF INTEREST
The Authors declare that there is no conflict of interest.
 
REFERENCES (40)
1.
Abo S.M.C., Layton A.T., 2021. Modeling the circadian regulation of the immune system: Sexually dimorphic effects of shift work. PLOS Comput. Biol. 17, e1008514, https://doi.org/10.1371/journa....
 
2.
Ando H., Oshima Y., Yanagihara H., Hayashi Y., Takamura T., Kaneko S., Fujimura A., 2006. Profile of rhythmic gene expression in the livers of obese diabetic KK-Ay mice. Biochem. Biophys. Res. Commun. 346, 1297–1302, https://doi.org/10.1016/j.bbrc....
 
3.
Barrett P., Ebling F.J.P., Schuhler S., et al., 2007. Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology 148, 3608–3617, https://doi.org/10.1210/en.200....
 
4.
Bartlewski P.M., Beard A.P., Rawlings N.C., 2001. Ultrasonographic study of the effects of the corpus luteum on antral follicular development in unilaterally ovulating western white-faced ewes. Anim. Reprod. Sci. 65, 231–244, https://doi.org/10.1016/S0378-....
 
5.
Chu A., Zhu L., Blum I.D., Mai O., Leliavski A., Fahrenkrug J., Oster H., Boehm U., Storch K.-F., 2013. Global but not gonadotropespecific disruption of Bmal1 abolishes the luteinizing hormone surge without affecting ovulation. Endocrinology 154, 2924–2935, https://doi.org/10.1210/en.201....
 
6.
Dardente H., 2007. Does a melatonin-dependent circadian oscillator in the pars tuberalis drive prolactin seasonal rhythmicity? J. Neuroendocrinol. 19, 657–666, https://doi.org/10.1111/j.1365....
 
7.
Fraser S., Cowen P., Franklin M., Franey C., Arendt J., 1983. Direct radioimmunoassay for melatonin in plasma. Clinical Chemistry 29, 396–397, https://doi.org/10.1093/clinch....
 
8.
Goh G.H., Blache D., Mark P.J., Kennington W.J., Maloney S.K., 2021. Daily temperature cycles prolong lifespan and have sex-specific effects on peripheral clock gene expression in Drosophila melanogaster. J. Exp. Biol. 224, jeb233213, https://doi.org/10.1242/jeb.23....
 
9.
Grigsby K., Ledford C., Batish T., et al., 2022. Targeting the maladaptive effects of binge drinking on circadian gene expression. Int. J. Mol. Sci. 23, 11084, https://doi.org/10.3390/ijms23....
 
10.
Hazlerigg D.G., Andersson H., Johnston J.D., Lincoln G., 2004. Molecular characterization of the long-day response in the soay sheep, a seasonal mammal. Curr. Biol. 14, 334–339, https://doi.org/10.1016/j.cub.....
 
11.
Herman A., Romanowicz K., Tomaszewska-Zaremba D., 2010. Effect of LPS on reproductive system at the level of the pituitary of anestrous ewes: Effect of LPS on reproductive system at the pituitary level. Reprod. Domest. Anim. 45, e351–e359, https://doi.org/10.1111/j.1439....
 
12.
Herman A.P., Bochenek J., Skipor J., Król K., Krawczyńska A., Antushevich H., Pawlina B., Marciniak E., Tomaszewska- Zaremba D., 2015. Interleukin-1 β modulates melatonin secretion in ovine pineal gland: ex vivo study. BioMed. Res. Int. 2015, 1–10, https://doi.org/10.1155/2015/5....
 
13.
Herman A.P., Wojtulewicz K., Bochenek J., Krawczyńska A., Antushevich H., Pawlina B., Zielińska-Górska M., Herman A., Romanowicz K., Tomaszewska-Zaremba D., 2017. Endotoxin-induced inflammation disturbs melatonin secretion in ewe. Asian-Australas. J. Anim. Sci. 30, 1784–1795, https://doi.org/10.5713/ajas.1....
 
14.
Hsieh M.-C., Yang S.-C., Tseng H.-L., Hwang L.-L., Chen C.-T., Shieh K.-R., 2010. Abnormal expressions of circadian-clock and circadian clock-controlled genes in the livers and kidneys of long-term, high-fat-diet-treated mice. Int. J. Obes. 34, 227–239, https://doi.org/10.1038/ijo.20....
 
15.
Johnston J.D., Skene D.J., 2015. 60 Years of Neuroendocrinology: Regulation of mammalian neuroendocrine physiology and rhythms by melatonin. J. Endocrinol. 226, T187–T198, https://doi.org/10.1530/JOE-15....
 
16.
Johnston J.D., Tournier B.B., Andersson H., Masson-Pévet M., Lincoln G.A., Hazlerigg D.G., 2006. Multiple effects of melatonin on rhythmic clock gene expression in the mammalian pars tuberalis. Endocrinology 147, 959–965, https://doi.org/10.1210/en.200....
 
17.
Kopycińska K., Wojtulewicz K., Herman A.P., Tomaszewska-Zaremba D., 2022. The effect of photoperiodic conditions on GnRH/LH secretion in ewes. Animals 12, 283, https://doi.org/10.3390/ani120....
 
18.
Król K., Tomaszewska-Zaremba D., Herman A., 2016. Photoperioddependent effect of inflammation on nocturnal gene expression of proinflammatory cytokines and their receptors in pars tuberalis of ewe. J. Anim Feed Sci. 25, 3–11, https://doi.org/10.22358/jafs/....
 
19.
Kumar D., De K., Sejian V., Naqvi S.M.K., 2017. Impact of Climate Change on Sheep Reproduction. In: V. Sejian, R. Bhatta, J. Gaughan, et al. (Editors). Sheep Production Adapting to Climate Change. Springer Singapore, Singapore, pp. 71–93, https://doi.org/10.1007/978-98...
 
20.
Lahiri K., Vallone D., Gondi S.B., Santoriello C., Dickmeis T., Foulkes N.S., 2005. Temperature regulates transcription in the zebrafish circadian clock. PLoS Biol. 3, e351, https://doi.org/10.1371/journa....
 
21.
Lehman M.N., Ladha Z., Coolen L.M., Hileman S.M., Connors J.M., Goodman R.L., 2010. Neuronal plasticity and seasonal reproduction in sheep: Seasonal reproduction in sheep. Eur. J. Neurosci. 32, 2152–2164, https://doi.org/10.1111/j.1460....
 
22.
Lincoln G., Messager S., Andersson H., Hazlerigg D., 2002. Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: Evidence for an internal coincidence timer. Proc. Natl. Acad. Sci. 99, 13890–13895, https://doi.org/10.1073/pnas.2....
 
23.
Long N.M., Tuersunjiang N., George L.A., Lemley C.O., Ma Y., Murdoch W.J., Nathanielsz P.W., Ford S.P., 2013. Maternal nutrient restriction in the ewe from early to midgestation programs reduced steroidogenic enzyme expression and tended to reduce progesterone content of corpora lutea, as well as circulating progesterone in nonpregnant aged female offspring. Reprod. Biol. Endocrinol. 11, 34, https://doi.org/10.1186/1477-7....
 
24.
Nakamura T.J., Sellix M.T., Kudo T., Nakao N., Yoshimura T., Ebihara S., Colwell C.S., Block G.D., 2010. Influence of the estrous cycle on clock gene expression in reproductive tissues: Effects of fluctuating ovarian steroid hormone levels. Steroids 75, 203–212, https://doi.org/10.1016/j.ster....
 
25.
Nakazawa K., Marubayashi U., McCann S.M., 1991. Mediation of the short-loop negative feedback of luteinizing hormone (LH) on LH-releasing hormone release by melatonin-induced inhibition of LH release from the pars tuberalis. Proc. Natl. Acad. Sci. 88, 7576–7579, https://doi.org/10.1073/pnas.8....
 
26.
Okada K., Yano M., Doki Y., et al., 2008. Injection of LPS causes transient suppression of biological clock genes in rats. J. Surg. Res. 145, 5–12, https://doi.org/10.1016/j.jss.....
 
27.
Pfeffer M., Korf H.-W., Wicht H., 2018. Synchronizing effects of melatonin on diurnal and circadian rhythms. Gen. Comp. Endocrinol. 258, 215–221, https://doi.org/10.1016/j.ygce....
 
28.
Przybył B., Wójcik-Gładysz A., Gajewska A., Szlis M., 2021. Brainderived neurotrophic factor (BDNF) affects somatotrophicaxis activity in sheep. J. Anim. Feed Sci. 30, 329–339, https://doi.org/10.22358/jafs/....
 
29.
Rabearivony A., Li H., Zhang S., Chen S., An X., Liu C., 2020. Housing temperature affects the circadian rhythm of hepatic metabolism and clock genes. J. Endocrinol. 247, 183–195,https://doi.org/10.1530/JOE-20....
 
30.
Satou R., Sato M., Kimura M., Ishizuka Y., Tazaki M., Sugihara N., Shibukawa Y., 2017. Temporal expression patterns of clock genes and aquaporin 5/anoctamin 1 in rat submandibular gland cells. Front. Physiol. 8, 320, https://doi.org/10.3389/fphys.....
 
31.
Sen A., Hoffmann H.M., 2020. Role of core circadian clock genes in hormone release and target tissue sensitivity in the reproductive axis. Mol. Cell. Endocrinol. 501, 110655, https://doi.org/10.1016/j.mce.....
 
32.
Strzetelski J. (Editor), 2009. IZ-PIB-INRA Standards for Ruminant Feeding (in Polish). National Research Institute of Animal Production. Kraków, Poland. ISBN 978-83-7607-072-8.
 
33.
Szczepkowska A., Bochenek J., Wójcik M., Tomaszewska-Zaremba D., Antushevich H., Tomczyk M., Skipor J., Herman A., 2022. Effect of caffeine on adenosine and ryanodine receptorgene expression in the hypothalamus, pituitary, and choroidplexus in ewes under basal and LPS challenge conditions. J. Anim. Feed Sci. 32, 17–25, https://doi.org/10.22358/jafs/....
 
34.
Tournier B.B., Dardente H., Simonneaux V., Vivien-Roels B., Pévet P., Masson-Pévet M., Vuillez P., 2007. Seasonal variations of clock gene expression in the suprachiasmatic nuclei and pars tuberalis of the European hamster (Cricetus cricetus): Photoperiodic regulation of the suprachiasmatic nuclei and pars tuberalis. Eur. J. Neurosci. 25, 1529–1536, https://doi.org/10.1111/j.1460....
 
35.
Von Gall C., Weaver D.R., Moek J., Jilg A., Stehle J.H., Korf H.-W., 2005. Melatonin plays a crucial role in the regulation of rhythmic clock gene expression in the mouse pars tuberalis. Ann. N. Y. Acad. Sci. 1040, 508–511, https://doi.org/10.1196/annals....
 
36.
Wagner G.C., Johnston J.D., Clarke I.J., Lincoln G.A., Hazlerigg D.G., 2008. Redefining the limits of day length responsiveness in a seasonal mammal. Endocrinology 149, 32–39, https://doi.org/10.1210/en.200....
 
37.
Wojtulewicz K., Tomaszewska-Zaremba D., Herman A., 2017. Endotoxin-induced inflammation suppresses the effect of melatonin on the release of LH from the ovine Pars Tuberalis explants—ex vivo study. Molecules 22, 1933, https://doi.org/10.3390/molecu....
 
38.
Wunderer F., Kühne S., Jilg A., Ackermann K., Sebesteny T., Maronde E., Stehle J.H., 2013. Clock gene expression in the human pituitary gland. Endocrinology 154, 2046–2057, https://doi.org/10.1210/en.201....
 
39.
Zhang L., Ptáček L.J., Fu Y.-H., 2013. Diversity of human clock genotypes and consequences. In: D.B. Teplow (Editor). Progress in Molecular Biology and Translational Science. Elsevier, pp. 51–81, https://doi.org/10.1016/B978-0....
 
40.
Zhang R., Lahens N.F., Ballance H.I., Hughes M.E., Hogenesch J.B., 2014. A circadian gene expression atlas in mammals: Implications for biology and medicine. Proc. Natl. Acad. Sci. 111, 16219–16224, https://doi.org/10.1073/pnas.1....
 
 
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