A molecular switch for photoperiod responsiveness in mammals
Open accessAbstract
Seasonal synchronization based on day length (photoperiod) allows organisms to anticipate environmental change. Photoperiodic decoding relies on circadian clocks, but the underlying molecular pathways have remained elusive [1]. In mammals and birds, photoperiodic responses depend crucially on expression of thyrotrophin β subunit RNA (TSHβ) in the pars tuberalis (PT) of the pituitary gland [2-4]. Now, using our well-characterized Soay sheep model [2], we describe a molecular switch governing TSHβ transcription through the circadian clock. Central to this is a conserved D element in the TSHβ promoter, controlled by the circadian transcription factor thyrotroph embryonic factor (Tef). In the PT, long-day exposure rapidly induces expression of the coactivator eyes absent 3 (Eya3), which synergizes with Tef to maximize TSHβ transcription. The pineal hormone melatonin, secreted nocturnally, sets the phase of rhythmic Eya3 expression in the PT to peak 12 hr after nightfall. Additionally, nocturnal melatonin levels directly suppress Eya3 expression. Together, these effects form a switch triggering a strong morning peak of Eya3 expression under long days. Species variability in the TSHβ D element influences sensitivity to TEF, reflecting species variability in photoperiodic responsiveness. Our findings define a molecular pathway linking the circadian clock to the evolution of seasonal timing in mammals.
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In the sheep pars tuberalis, transcript levels of Eya3 are controlled both by a circadian signal (that licenses eya3 transcription 12 h after night fall) and by acute levels of melatonin (that lead to suppression of eya3 transcription during darkness).
“In the sheep pars tuberalis, transcript levels of the transcription factor Eyes absent 3 (Eya3) are controlled both by a circadian signal (that licenses eya3 transcription 12 h after night fall) and by the acute levels of melatonin (that lead to a suppression of eya3 transcription during darkness).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [56]
The combination of these regulatory mechanisms leads to a specific upregulation of eya3 only under short photoperiod.
“As melatonin levels are suppressed by light, the combination of these regulatory mechanisms leads to a specific upregulation of eya3 only under short photoperiod (56).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [56]
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Whole-genome resequencing reveals loci under selection during chicken domestication
Rubin, C.-J., Zody, M. C., Eriksson, J., Meadows, J. R. S., Sherwood, E., Webster, M. T., Jiang, L., Ingman, M., Sharpe, T., Ka, S., et al. (2010) · Nature · doi:10.1038/nature08832 · Cited by 1,138 · see citing works
Goldman, B. D. (2001) · Journal of Biological Rhythms · doi:10.1177/074873001129001980 · Cited by 771 · see citing works
Li, X., Ohgi, K. A., Zhang, J., Krones, A., Bush, K. T., Glass, C. K., Nigám, S. K., Aggarwal, A. K., Maas, R. L., Rose, D. W., et al. (2003) · Nature · doi:10.1038/nature02083 · Cited by 636 · see citing works
Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds
Yoshimura, T., Yasuo, S., Watanabe, M., Iigo, M., Yamamura, T., Hirunagi, K., & Ebihara, S. (2003) · Nature · doi:10.1038/nature02117 · Cited by 561 · see citing works
Thyrotrophin in the pars tuberalis triggers photoperiodic response
Nakao, N., Ono, H., Yamamura, T., Anraku, T., Takagi, T., Higashi, K., Yasuo, S., Katou, Y., Kageyama, S., Uno, Y., et al. (2008) · Nature · doi:10.1038/nature06738 · Cited by 539 · see citing works
Ancestral TSH Mechanism Signals Summer in a Photoperiodic Mammal
Hanon, É. A., Lincoln, G. A., Fustin, J., Dardente, H., Masson‐Pévet, M., Morgan, P. J., & Hazlerigg, D. G. (2008) · Current Biology · doi:10.1016/j.cub.2008.06.076 · Cited by 400 · see citing works
Cooperation of Six and Eya in Activation of Their Target Genes through Nuclear Translocation of Eya
Ohto, H., Kamada, S., Tago, K., Tominaga, S., Ozaki, H., Sato, S., & Kawakami, K. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.10.6815 · Cited by 353 · see citing works
Barrett, P., Ebling, F. J. P., Schuhler, S., Wilson, D., Ross, A. W., Warner, A., Jethwa, P., Boelen, A., Visser, T. J., Ozanne, D. M., et al. (2007) · Endocrinology · doi:10.1210/en.2007-0316 · Cited by 286 · see citing works
Involvement of thyrotropin in photoperiodic signal transduction in mice
Ono, H., Hoshino, Y., Yasuo, S., Watanabe, M., Nakane, Y., Murai, A., Ebihara, S., Korf, H., & Yoshimura, T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808952105 · Cited by 279 · see citing works
Kumar, J. P. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8335-4 · Cited by 252 · see citing works
von Gall, C., Garabette, M. L., Kell, C. A., Frenzel, S., Dehghani, F., Schumm‐Draeger, P., Weaver, D. R., Korf, H., Hastings, M. H., & Stehle, J. H. (2002) · Nature Neuroscience · doi:10.1038/nn806 · Cited by 251 · see citing works
Drolet, D. W., Scully, K. M., Simmons, D. M., Wegner, M., Chu, K. T., Swanson, L. W., & Rosenfeld, M. G. (1991) · Genes & Development · doi:10.1101/gad.5.10.1739 · Cited by 245 · see citing works
Photoperiodism in Humans and Other Primates: Evidence and Implications
Wehr, T. A. (2001) · Journal of Biological Rhythms · doi:10.1177/074873001129002060 · Cited by 231 · see citing works
Lincoln, G. A., Messager, S., Andersson, H., & Hazlerigg, D. G. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.212517599 · Cited by 228 · see citing works
Spitz, F., Demignon, J., Porteu, A., Kahn, A., Concordet, J., Daegelen, D., & Maire, P. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.24.14220 · Cited by 218 · see citing works
Decoding photoperiodic time through Per1 and ICER gene amplitude
Messager, S., Ross, A., Barrett, P., & Morgan, P. J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9938 · Cited by 178 · see citing works
Mammalian Seasonal Rhythms: Behavior and Neuroendocrine Substrates
Stevenson, T. J., Prendergast, B. J., & Nelson, R. J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00013-4 · Cited by 169 · see citing works
Fonjallaz, P., Ossipow, V., Wanner, G., & Schibler, U. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00365.x · Cited by 151 · see citing works
Light Directs Zebrafish period2 Expression via Conserved D and E Boxes
Vatine, G. D., Vallone, D., Appelbaum, L., Mracek, P., Ben-Moshe, Z., Lahiri, K., Gothilf, Y., & Foulkes, N. S. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000223 · Cited by 140 · see citing works
New Insights into Ancient Seasonal Life Timers
Hazlerigg, D. G., & Loudon, A. S. I. (2008) · Current Biology · doi:10.1016/j.cub.2008.07.040 · Cited by 138 · see citing works
Jemc, J. C., & Rebay, I. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.052705.164916 · Cited by 133 · see citing works
Klosen, P., Bienvenu, C., Demarteau, O., Dardente, H., Guerrero, H. Y., Pévet, P., & Masson‐Pévet, M. (2002) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215540205001209 · Cited by 127 · see citing works
Dardente, H., Klosen, P., Pévet, P., & Masson‐Pévet, M. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01060.x · Cited by 118 · see citing works
Multiple Effects of Melatonin on Rhythmic Clock Gene Expression in the Mammalian Pars Tuberalis
Johnston, J. D., Tournier, B. B., Andersson, H., Masson‐Pévet, M., Lincoln, G. A., & Hazlerigg, D. G. (2005) · Endocrinology · doi:10.1210/en.2005-1100 · Cited by 114 · see citing works
Bockmann, J., Böckers, T. M., Winter, C., Wittkowski, W., Winterhoff, H., Deufel, T., & Kreutz, M. R. (1997) · Endocrinology · doi:10.1210/endo.138.3.5007 · Cited by 107 · see citing works
Messager, S., Garabette, M. L., Hastings, M. H., & Hazlerigg, D. G. (2001) · Neuroreport · doi:10.1097/00001756-200103050-00029 · Cited by 106 · see citing works
Role of Thyroid Hormone Deiodination in the Hypothalamus
Lechan, R. M., & Fekete, C. (2005) · Thyroid · doi:10.1089/thy.2005.15.883 · Cited by 104 · see citing works
Proof-by-synthesis of the transcriptional logic of mammalian circadian clocks
Ukai‐Tadenuma, M., Kasukawa, T., & Ueda, H. R. (2008) · Nature Cell Biology · doi:10.1038/ncb1775 · Cited by 101 · see citing works
Identification of Eya3 and TAC1 as Long-Day Signals in the Sheep Pituitary
Dupré, S. M., Miedzinska, K., Duval, C., Yu, L., Goodman, R. L., Lincoln, G. A., Davis, J. R., McNeilly, A. S., Burt, D. W., & Loudon, A. S. I. (2010) · Current Biology · doi:10.1016/j.cub.2010.02.066 · Cited by 82 · see citing works
Molecular Characterization of the Long-Day Response in the Soay Sheep, a Seasonal Mammal
Hazlerigg, D. G., Andersson, H., Johnston, J. D., & Lincoln, G. A. (2004) · Current Biology · doi:10.1016/j.cub.2004.01.057 · Cited by 80 · see citing works
Endocrine Control of the Seasonal Occurrence of Ovulation in Rhesus Monkeys Housed Outdoors*
Walker, M. L., Wilson, M. E., & GORDON, T. P. (1984) · Endocrinology · doi:10.1210/endo-114-4-1074 · Cited by 80 · see citing works
Implication of the F-Box Protein FBXL21 in Circadian Pacemaker Function in Mammals
Dardente, H., Mendoza, J., Fustin, J., Challet, É., & Hazlerigg, D. G. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003530 · Cited by 64 · see citing works
Transcriptional feedback loops in the ovine circadian clock
Dardente, H., Fustin, J., & Hazlerigg, D. G. (2009) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2009.03.016 · Cited by 24 · see citing works
Short or Long Day Light Regimes May Not Affect Reproductive Performance in the Sow
Hälli, O., Tast, A., Heinonen, M., Munsterhjelm, C., Valros, A., & Peltoniemi, O. A. T. (2008) · Reproduction in Domestic Animals · doi:10.1111/j.1439-0531.2007.00976.x · Cited by 11 · see citing works
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1 of the 35 references couldn’t be matched to a known paper.
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Melatonin as a Hormone: New Physiological and Clinical Insights
Cipolla‐Neto, J., & do Amaral, F. G. (2018) · Endocrine Reviews · doi:10.1210/er.2018-00084 · Cited by 653 · see citing works
Melatonin: Both master clock output and internal time-giver in the circadian clocks network
Pévet, P., & Challet, É. (2011) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2011.07.001 · Cited by 372 · see citing works
It's time to swim! Zebrafish and the circadian clock
Vatine, G. D., Vallone, D., Gothilf, Y., & Foulkes, N. S. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.04.007 · Cited by 304 · see citing works
Annual rhythms that underlie phenology: biological time-keeping meets environmental change
Helm, B., Ben‐Shlomo, R., Sheriff, M. J., Hut, R. A., Foster, F., Barnes, B. M., & Dominoni, D. M. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.0016 · Cited by 309 · see citing works
Circadian Entrainment to the Natural Light-Dark Cycle across Seasons and the Weekend
Stothard, E. R., McHill, A. W., Depner, C. M., Birks, B. R., Moehlman, T. M., Ritchie, H. K., Guzzetti, J. R., Chinoy, E. D., LeBourgeois, M. K., Axelsson, J., et al. (2017) · Current Biology · doi:10.1016/j.cub.2016.12.041 · Cited by 303 · see citing works
Seasonal Regulation of Reproduction in Mammals
Hazlerigg, D. G., & Simonneaux, V. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00034-x · Cited by 281 · see citing works
Melatonin feedback on clock genes: a theory involving the proteasome
Vriend, J. P., & Reiter, R. J. (2014) · Journal of Pineal Research · doi:10.1111/jpi.12189 · Cited by 268 · see citing works
Latitudinal clines: an evolutionary view on biological rhythms<sup>,</sup>
Hut, R. A., Paolucci, S., Dor, R., Kyriacou, C. P., & Daan, S. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.0433 · Cited by 241 · see citing works
Thyroid Hormone and Seasonal Rhythmicity
Dardente, H., Hazlerigg, D. G., & Ebling, F. J. P. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00019 · Cited by 226 · see citing works
Wood, S. H., & Loudon, A. S. I. (2014) · Journal of Endocrinology · doi:10.1530/joe-14-0141 · Cited by 192 · see citing works
Plikus, M. V., Spyk, E. N. V., Pham, K., Geyfman, M., Kumar, V., Takahashi, J. S., & D, B. A. M. (2015) · Journal of Biological Rhythms · doi:10.1177/0748730414563537 · Cited by 176 · see citing works
Disrupted seasonal biology impacts health, food security and ecosystems
Stevenson, T. J., Visser, M. E., Arnold, W., Barrett, P., Biello, S. M., Dawson, A., Denlinger, D. L., Dominoni, D. M., Ebling, F. J. P., Elton, S., et al. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.1453 · Cited by 168 · see citing works
A Circannual Clock Drives Expression of Genes Central for Seasonal Reproduction
de Miera, C. S., Monecke, S., Bartzen-Sprauer, J., Laran‐Chich, M., Pévet, P., Hazlerigg, D. G., & Simonneaux, V. (2014) · Current Biology · doi:10.1016/j.cub.2014.05.024 · Cited by 156 · see citing works
Molecular pathways involved in seasonal body weight and reproductive responses governed by melatonin
Barrett, P., & Bolborea, M. (2011) · Journal of Pineal Research · doi:10.1111/j.1600-079x.2011.00963.x · Cited by 151 · see citing works
Thyroid hormone and seasonal regulation of reproduction
Yoshimura, T. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.04.002 · Cited by 146 · see citing works
The Eyes Absent proteins in development and disease
Tadjuidje, E., & Hegde, R. S. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1144-9 · Cited by 145 · see citing works
The circadian clock and glucocorticoids – interactions across many time scales
Dickmeis, T., Weger, B. D., & Weger, M. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.05.012 · Cited by 144 · see citing works
Photoperiodic Regulation of Reproduction in Vertebrates
Nakane, Y., & Yoshimura, T. (2018) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-020518-115216 · Cited by 143 · see citing works
Rhythms in the endocrine system of fish: a review
Cowan, M. E., Azpeleta, C., & López‐Olmeda, J. F. (2017) · Journal of Comparative Physiology B · doi:10.1007/s00360-017-1094-5 · Cited by 141 · see citing works
Roles of circadian clock genes in insect photoperiodism
Goto, S. G. (2012) · Entomological Science · doi:10.1111/ens.12000 · Cited by 131 · see citing works
An integrative view of mammalian seasonal neuroendocrinology
Dardente, H., Wood, S. H., Ebling, F. J. P., & de Miera, C. S. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12729 · Cited by 131 · see citing works
Dardente, H. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02250.x · Cited by 128 · see citing works
Wood, S. H., Christian, H., Miedzinska, K., Saer, B., Johnson, M., Paton, B., Yu, L., McNEILLY, J. R., Davis, J. R., McNeilly, A. S., et al. (2015) · Current Biology · doi:10.1016/j.cub.2015.09.014 · Cited by 126 · see citing works
An Overview of Monthly Rhythms and Clocks
Raible, F., Takekata, H., & Tessmar-Raible, K. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00189 · Cited by 121 · see citing works
Seasonal control of gonadotropin-inhibitory hormone (GnIH) in birds and mammals
Kriegsfeld, L. J., Ubuka, T., Bentley, G. E., & Tsutsui, K. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.12.001 · Cited by 117 · see citing works
TSH restores a summer phenotype in photoinhibited mammals via the RF‐amides RFRP3 and kisspeptin
Klosen, P., Sébert, M., Rasri, K., Laran‐Chich, M., & Simonneaux, V. (2013) · The FASEB Journal · doi:10.1096/fj.13-229559 · Cited by 110 · see citing works
Global climate change and invariable photoperiods: A mismatch that jeopardizes animal fitness
Walker, W. H., Meléndez‐Fernández, O. H., Nelson, R. J., & Reiter, R. J. (2019) · Ecology and Evolution · doi:10.1002/ece3.5537 · Cited by 107 · see citing works
Thyroid hormone signalling genes are regulated by photoperiod in the hypothalamus of F344 rats
Ross, A. W., Helfer, G., Russell, L., Darras, V. M., & Morgan, P. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021351 · Cited by 104 · see citing works
Changes of Dietary Fat and Carbohydrate Content Alter Central and Peripheral Clock in Humans
Pivovarova‐Ramich, O., Jürchott, K., Rudovich, N. N., Hornemann, S., Lu, Y., Möckel, S., Murahovschi, V., Kessler, K., Seltmann, A., Maser‐Gluth, C., et al. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-3868 · Cited by 99 · see citing works
Korf, H. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.05.011 · Cited by 98 · see citing works
Kisspeptins and RFRP-3 Act in Concert to Synchronize Rodent Reproduction with Seasons
Simonneaux, V., Ancel, C., Poirel, V., & Gauer, F. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00022 · Cited by 96 · see citing works
Abrieux, A., Xue, Y., Cai, Y. D., Lewald, K. M., Nguyen, H. N., Zhang, Y., & Chiu, J. C. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2004262117 · Cited by 89 · see citing works
Hypothalamic control of seasonal changes in food intake and body weight
Ebling, F. J. P. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.10.003 · Cited by 88 · see citing works
Circadian clocks and the measurement of daylength in seasonal reproduction
Ikegami, K., & Yoshimura, T. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.06.040 · Cited by 86 · see citing works
Minutes, days and years: molecular interactions among different scales of biological timing
Golombek, D. A., Bussi, I. L., & Agostino, P. V. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0465 · Cited by 80 · see citing works
Vilches, N., Spichiger, C., Mendez, N., Abarzua-Catalan, L., Galdames, H. A., Hazlerigg, D. G., Richter, H. G., & Torres-Farfan, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091313 · Cited by 86 · see citing works
Kuenzel, W. J., Kang, S. W., & Zhou, Z. (2014) · Poultry Science · doi:10.3382/ps.2014-04370 · Cited by 87 · see citing works
Circadian clock mechanism driving mammalian photoperiodism
Wood, S. H., Hindle, M., Mizoro, Y., Cheng, Y., Saer, B., Miedzinska, K., Christian, H., Begley, N., McNeilly, J. R., McNeilly, A. S., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18061-z · Cited by 83 · see citing works
A brief history of circannual time
Lincoln, G. A. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12694 · Cited by 82 · see citing works
Philippé, J., & Dibner, C. (2014) · Journal of Biological Rhythms · doi:10.1177/0748730414557634 · Cited by 82 · see citing works
Seasonal breeding in mammals: From basic science to applications and back
Dardente, H., Lomet, D., Robert, V., Decourt, C., Beltramo, M., & Pellicer-Rubio, M.-T. (2016) · Theriogenology · doi:10.1016/j.theriogenology.2016.04.045 · Cited by 79 · see citing works
Diurnal and seasonal variation of the brain serotonin system in healthy male subjects
Matheson, G. J., Schain, M., Almeida, R., Lundberg, J., Cselényi, Z., Borg, J., Varrone, A., Farde, L., & Červenka, S. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.03.007 · Cited by 78 · see citing works
The impact of thyroid hormone in seasonal breeding has a restricted transcriptional signature
Lomet, D., Cognié, J., Chesneau, D., Dubois, E., Hazlerigg, D. G., & Dardente, H. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2667-x · Cited by 78 · see citing works
Hua, P., Liu, W., Chen, D., Zhao, Y., Chen, L., Zhang, N., Wang, C., Guo, S., Wang, L., Xiao, H., et al. (2013) · Journal of Affective Disorders · doi:10.1016/j.jad.2013.11.019 · Cited by 76 · see citing works
Weems, P. W., Goodman, R. L., & Lehman, M. N. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.12.002 · Cited by 75 · see citing works
The pars tuberalis: The site of the circannual clock in mammals?
Wood, S. H., & Loudon, A. S. I. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.06.029 · Cited by 70 · see citing works
A Kiss to drive rhythms in reproduction
Simonneaux, V. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14287 · Cited by 70 · see citing works
Flexible clock systems: adjusting the temporal programme
van der Veen, D. R., Riede, S., Heideman, P., Hau, M., van der Vinne, V., & Hut, R. (2017) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2016.0254 · Cited by 62 · see citing works
Ikeno, T., Ishikawa, K., Numata, H., & Goto, S. G. (2013) · Physiological Entomology · doi:10.1111/phen.12013 · Cited by 68 · see citing works
Mohamed, A. A. M., Wang, Q., Bembenek, J., Ichihara, N., Hiragaki, S., Suzuki, T., & Takeda, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092680 · Cited by 66 · see citing works
Hazlerigg, D. G., & Lincoln, G. A. (2011) · Journal of Biological Rhythms · doi:10.1177/0748730411420812 · Cited by 65 · see citing works
A unifying hypothesis for control of body weight and reproduction in seasonally breeding mammals
Helfer, G., Barrett, P., & Morgan, P. J. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12680 · Cited by 65 · see citing works
Timing as a sexually selected trait: the right mate at the right moment
Hau, M., Dominoni, D. M., Casagrande, S., Buck, C. L., Wagner, G., Hazlerigg, D. G., Greives, T., & Hut, R. A. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0249 · Cited by 64 · see citing works
Cellular mechanisms and integrative timing of neuroendocrine control of GnRH secretion by kisspeptin
Beltramo, M., Dardente, H., Cayla, X., & Caraty, A. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.10.015 · Cited by 63 · see citing works
Role for Circadian Clock Genes in Seasonal Timing: Testing the Bünning Hypothesis
Pegoraro, M., Gesto, J. S. M., Kyriacou, C. P., & Tauber, E. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004603 · Cited by 62 · see citing works
Dim light at night disrupts the short-day response in Siberian hamsters
Ikeno, T., Weil, Z. M., & Nelson, R. J. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.12.005 · Cited by 62 · see citing works
Clarke, I. J. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.02.005 · Cited by 58 · see citing works
Barberà, M. A., Collantes‐Alegre, J. M., & Martínez-Torres, D. (2017) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2017.02.006 · Cited by 59 · see citing works
Angelopoulou, E., Quignon, C., Kriegsfeld, L. J., & Simonneaux, V. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00183 · Cited by 58 · see citing works
Владимировна, К. Н., Tsyrlin, V. A., Плисс, М. Г., & Galagudza, M. M. (2021) · Chronobiology International · doi:10.1080/07420528.2020.1865394 · Cited by 58 · see citing works
RFRP Neurons – The Doorway to Understanding Seasonal Reproduction in Mammals
Henningsen, J. B., Gauer, F., & Simonneaux, V. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00036 · Cited by 57 · see citing works
Circadian cycles of gene expression in the coral, Acropora millepora
Brady, A. K., Snyder, K. A., & Vize, P. D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025072 · Cited by 56 · see citing works
Stevenson, T. J., & Ball, G. F. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08209.x · Cited by 55 · see citing works
Temporal organization of pineal melatonin signaling in mammals
Gorman, M. R. (2019) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2019.110687 · Cited by 57 · see citing works
Hidalgo, S., Anguiano, M., Tabuloc, C. A., & Chiu, J. C. (2023) · Current Biology · doi:10.1016/j.cub.2023.01.006 · Cited by 53 · see citing works
Photoperiodism: Shall EYA Compare Thee to a Summer's Day?
Hut, R. A. (2011) · Current Biology · doi:10.1016/j.cub.2010.11.060 · Cited by 52 · see citing works
Majumdar, G., Rani, S., & Kumar, V. (2014) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.09.020 · Cited by 52 · see citing works
Bolborea, M., Laran‐Chich, M., Rasri, K., Hildebrandt, H., Govitrapong, P., Simonneaux, V., Pévet, P., Steinlechner, S., & Klosen, P. (2011) · Endocrinology · doi:10.1210/en.2011-1039 · Cited by 51 · see citing works
Dardente, H., & Simonneaux, V. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13124 · Cited by 47 · see citing works
Otsuka, T., Goto, M., Kawai, M., Togo, Y., Sato, K., Katoh, K., Furuse, M., & Yasuo, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039090 · Cited by 49 · see citing works
Photoperiodic and circadian bifurcation theories of depression and mania
Kripke, D. F., Elliott, J. A., Welsh, D. K., & Youngstedt, S. D. (2015) · F1000Research · doi:10.12688/f1000research.6444.1 · Cited by 48 · see citing works
Brady, A. K., Willis, B. L., Harder, L. D., & Vize, P. D. (2016) · The Biological Bulletin · doi:10.1086/bblv230n2p130 · Cited by 48 · see citing works
Lee, H., Woo, H. G., Greenwood, T. A., Kripke, D. F., & Kelsoe, J. R. (2012) · Journal of Affective Disorders · doi:10.1016/j.jad.2012.07.032 · Cited by 48 · see citing works
Insulin-like peptides involved in photoperiodism in the aphid Acyrthosiphon pisum
Barberà, M. A., Cañas-Cañas, R., & Martínez-Torres, D. (2019) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2019.103185 · Cited by 47 · see citing works
LACTATION BIOLOGY SYMPOSIUM: Circadian clocks as mediators of the homeorhetic response to lactation1
Casey, T., & Plaut, K. I. (2012) · Journal of Animal Science · doi:10.2527/jas.2011-4590 · Cited by 43 · see citing works
Melatonin and the circadian system: Keys for health with a focus on sleep
Pévet, P., Challet, É., & Felder‐Schmittbuhl, M. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819975-6.00021-2 · Cited by 46 · see citing works
Maternal Photoperiodic Programming: Melatonin and Seasonal Synchronization Before Birth
van Dalum, J., Melum, V. J., Wood, S. H., & Hazlerigg, D. G. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00901 · Cited by 42 · see citing works
Król, E., Douglas, A., Dardente, H., Birnie, M. J., van der Vinne, V., Eijer, W. G., Gerkema, M. P., Hazlerigg, D. G., & Hut, R. A. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.09.004 · Cited by 41 · see citing works
Irachi, S., Hall, D. J., Fleming, M. S., Maugars, G., Björnsson, B. T., Dufour, S., Uchida, K., & McCormick, S. D. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.111056 · Cited by 41 · see citing works
Transcriptome dynamics over a lunar month in a broadcast spawning acroporid coral
Oldach, M. J., Workentine, M., Matz, M. V., Fan, T., & Vize, P. D. (2017) · Molecular Ecology · doi:10.1111/mec.14043 · Cited by 39 · see citing works
Ikegami, K., & Yoshimura, T. (2017) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2017.09.002 · Cited by 40 · see citing works
Hazlerigg, D. G., Wyse, C. A., Dardente, H., Hanon, É. A., & Lincoln, G. A. (2013) · Chronobiology International · doi:10.3109/07420528.2012.754450 · Cited by 40 · see citing works
Menassol, J.-B., Collet, A., Chesneau, D., Malpaux, B., & Scaramuzzi, R. J. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.111.092817 · Cited by 40 · see citing works
Melatonin in the seasonal response of the aphid Acyrthosiphon pisum
Barberà, M. A., Escrivá, L., Collantes‐Alegre, J. M., Meca, G., Rosato, E., & Martínez‐Torres, D. (2018) · Insect Science · doi:10.1111/1744-7917.12652 · Cited by 39 · see citing works
Zhu, H., Shao, X., Chen, Z., Wei, C., Lei, M., Ying, S., Yu, J., & Shi, Z. (2017) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2017.03.009 · Cited by 39 · see citing works
Mishra, I., Singh, D., & Kumar, V. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12469 · Cited by 39 · see citing works
Milesi, S., Simonneaux, V., & Klosen, P. (2017) · Scientific Reports · doi:10.1038/s41598-017-17920-y · Cited by 39 · see citing works
Herrero, M. J., & Lepesant, J. M. J. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.08.002 · Cited by 38 · see citing works
McKinney, G. J., Hale, M. C., Goetz, G., Gribskov, M., Thrower, F. P., & Nichols, K. M. (2015) · Molecular Ecology · doi:10.1111/mec.13143 · Cited by 38 · see citing works
Seasonal Timing: How Does a Hibernator Know When to Stop Hibernating?
Hut, R. A., Dardente, H., & Riede, S. J. (2014) · Current Biology · doi:10.1016/j.cub.2014.05.061 · Cited by 37 · see citing works
The evolutionary physiology of photoperiodism in vertebrates
Hazlerigg, D. G. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59427-3.00023-x · Cited by 37 · see citing works
Photoperiodic induction without light-mediated circadian entrainment in a high arctic resident bird
Appenroth, D., Melum, V. J., West, A. C., Dardente, H., Hazlerigg, D. G., & Wagner, G. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.220699 · Cited by 36 · see citing works
Dunn, I., Wilson, P. W., Shi, Y., Burt, D. W., Loudon, A. S. I., & Sharp, P. J. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12554 · Cited by 36 · see citing works
Reiter, R. J., & Sharma, R. (2020) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2020.113620 · Cited by 36 · see citing works
O’Brien, C. S., Bourdo, R., Bradshaw, W. E., Holzapfel, C. M., & Cresko, W. A. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.03.010 · Cited by 35 · see citing works
Casey, T., & Plaut, K. I. (2022) · Journal of Animal Science · doi:10.1093/jas/skac233 · Cited by 36 · see citing works
Polymorphisms in melatonin synthesis pathways: possible influences on depression
Kripke, D. F., Nievergelt, C. M., Tranah, G. J., Murray, S. S., McCarthy, M. J., Rex, K. M., Parimi, N., & Kelsoe, J. R. (2011) · Journal of Circadian Rhythms · doi:10.1186/1740-3391-9-8 · Cited by 34 · see citing works
Circuit-level analysis identifies target genes of sex steroids in ewe seasonal breeding
Lomet, D., Druart, X., Hazlerigg, D. G., Beltramo, M., & Dardente, H. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110825 · Cited by 34 · see citing works
Kriegsfeld, L. J., Jennings, K. J., Bentley, G. E., & Tsutsui, K. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12597 · Cited by 33 · see citing works
Decourt, C., Caraty, A., Briant, C., Guillaume, D., Lomet, D., Chesneau, D., Lardic, L., Duchamp, G., Reigner, F., Monget, P., et al. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.113.114157 · Cited by 32 · see citing works
- Authors
- Dardente, H., Wyse, C. A., Birnie, M. J., Dupré, S. M., Loudon, A. S. I., Lincoln, G. A., & Hazlerigg, D. G.
- Affiliations
- University of Aberdeen (GB)
- University of Manchester (GB)
- The Queen's Medical Research Institute (GB)
- Corresponding author
- Dardente, Hugues
- Hazlerigg, David G.
- ORCID
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2010-12
- Volume
- 20
- Issue
- 24
- Pages
- 2193-2198
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2062566674
- Cited by
- 291
- References
- 35
- Citations by year
- 2026: 9 · 2025: 16 · 2024: 17 · 2023: 23 · 2022: 17 · 2021: 32 · 2020: 21 · 2019: 9 · 2018: 19 · 2017: 23 · 2016: 6 · 2015: 18 · 2014: 25 · 2013: 21 · 2012: 18
- FWCI
- 8.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- HAL (submittedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/G003033/1)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- photoperiod, circadian clock, pars tuberalis, melatonin, seasonal timing, Soay sheep
- MeSH terms
- Animals, Base Sequence, DNA-Binding Proteins, Humans, Mammals, Melatonin, Molecular Sequence Data, Pituitary Gland, Promoter Regions, Genetic, Seasons, Sheep, Transcription, Genetic, Sequence Alignment, Protein Tyrosine Phosphatases, Photoperiod, Thyrotropin, beta Subunit, Basic-Leucine Zipper Transcription Factors, Circadian Clocks
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