Acute Induction of Eya3 by Late-Night Light Stimulation Triggers TSHβ Expression in Photoperiodism
Open accessAbstract
Living organisms detect seasonal changes in day length (photoperiod) [1-3] and alter their physiological functions accordingly to fit seasonal environmental changes. TSHβ, induced in the pars tuberalis (PT), plays a key role in the pathway that regulates vertebrate photoperiodism [4, 5]. However, the upstream inducers of TSHβ expression remain unknown. Here we performed genome-wide expression analysis of the PT under chronic short-day and long-day conditions in melatonin-proficient CBA/N mice, in which the photoperiodic TSHβ expression response is preserved [6]. This analysis identified "short-day" and "long-day" genes, including TSHβ, and further predicted the acute induction of long-day genes by late-night light stimulation. We verified this by advancing and extending the light period by 8 hr, which induced TSHβ expression within one day. In the following genome-wide expression analysis under this acute long-day condition, we searched for candidate upstream genes by looking for expression that preceded TSHβ's, and we identified the Eya3 gene. We demonstrated that Eya3 and its partner Six1 synergistically activate TSHβ expression and that this activation is further enhanced by Tef and Hlf. These results elucidate the comprehensive transcriptional photoperiodic response in the PT, revealing the complex regulation of TSHβ expression and unexpectedly rapid response to light changes in the mammalian photoperiodic system.
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Melatonin-proficient mice appear to possess a similar ability to induce eya3, suggesting that this mechanism could be evolutionarily conserved.
“Melatonin-proficient mice appear to possess a similar ability to induce eya3, suggesting that this mechanism could be evolutionarily conserved (57).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [57]
Cites
Statistical significance for genomewide studies
Storey, J. D., & Tibshirani, R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1530509100 · Cited by 9,692 · see citing works
Summaries of Affymetrix GeneChip probe level data
Irizarry, R. A. (2003) · Nucleic Acids Research · doi:10.1093/nar/gng015 · Cited by 4,906 · see citing works
An Introduction to Systems Biology: Design Principles of Biological Circuits
Alon, U. (2006) · doi:10.1201/9781420011432 · Cited by 2,825 · see citing works
Yoo, S.-H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., Siepka, S. M., Hong, H.-K., Oh, W. J., Yoo, O. J., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308709101 · Cited by 2,329 · see citing works
Photoperiodic Control of Seasonality in Birds
Dawson, A., King, V. M., Bentley, G. E., & Ball, G. F. (2001) · Journal of Biological Rhythms · doi:10.1177/074873001129002079 · Cited by 1,023 · see citing works
The melatonin rhythm: both a clock and a calendar
Reiter, R. J. (1993) · Cellular and Molecular Life Sciences · doi:10.1007/bf01923947 · Cited by 997 · see citing works
Shigeyoshi, Y., Taguchi, K., Yamamoto, S., Takekida, S., Yan, L., Tei, H., Moriya, T., Shibata, S., Loros, J. J., Dunlap, J. C., et al. (1997) · Cell · doi:10.1016/s0092-8674(00)80494-8 · Cited by 891 · 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
Bonini, N. M., Leiserson, W. M., & Benzer, S. (1993) · Cell · doi:10.1016/0092-8674(93)90115-7 · Cited by 559 · 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
Pineal Gland: Influence on Gonads of Male Hamsters
Hoffman, R. A., & Reiter, R. J. (1965) · Science · doi:10.1126/science.148.3677.1609 · Cited by 445 · see citing works
Mueller, C. R., Maire, P., & Schibler, U. (1990) · Cell · doi:10.1016/0092-8674(90)90808-r · Cited by 384 · see citing works
Xu, P., Woo, I., Her, H., Beier, D. R., & Maas, R. L. (1997) · Development · doi:10.1242/dev.124.1.219 · Cited by 331 · see citing works
Fusion of the Leucine Zipper Gene HLF to the E2A Gene in Human Acute B-Lineage Leukemia
Inaba, T., Roberts, W. M., Shapiro, L. H., Jolly, K. W., Raimondi, S. C., Smith, S. D., & Look, A. T. (1992) · Science · doi:10.1126/science.1386162 · Cited by 287 · 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
Genome-wide Transcriptional Orchestration of Circadian Rhythms inDrosophila
Ueda, H. R., Matsumoto, A., Kawamura, M., Iino, M., Tanimura, T., & Hashimoto, S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c100765200 · Cited by 264 · see citing works
Measurement of internal body time by blood metabolomics
Minami, Y., Kasukawa, T., Kakazu, Y., Iigo, M., Sugimoto, M., Ikeda, S., Yasui, A., van der Horst, G. T. J., Soga, T., & Ueda, H. R. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900617106 · Cited by 261 · 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
Clock genes in calendar cells as the basis of annual timekeeping in mammals--a unifying hypothesis
Lincoln, G., Andersson, H., & Loudon, A. S. I. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1790001 · Cited by 231 · 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
Transcriptional Repression by a Novel Member of the bZIP Family of Transcription Factors
Cowell, I. G., Skinner, A., & Hurst, H. C. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.7.3070 · Cited by 192 · see citing works
EYA4, a novel vertebrate gene related to Drosophila eyes absent
Borsani, G. (1999) · Human Molecular Genetics · doi:10.1093/hmg/8.1.11 · Cited by 174 · see citing works
A riot of rhythms: neuronal and glial circadian oscillators in the mediobasal hypothalamus
Guilding, C., Hughes, A. T. L., Brown, T. M., Namvar, S., & Piggins, H. D. (2009) · Molecular Brain · doi:10.1186/1756-6606-2-28 · Cited by 171 · see citing works
Yoshimura, T., & Ebihara, S. (1996) · Journal of Comparative Physiology A · doi:10.1007/bf00225828 · Cited by 140 · see citing works
The regulation of seasonal changes in food intake and body weight
Ebling, F. J. P., & Barrett, P. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01721.x · Cited by 139 · 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
Zhang, W., Zhang, J., Kornuc, M., Kwan, K. W., Frank, R. C., & Nimer, S. D. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.11.6055 · Cited by 134 · see citing works
Bittman, E. L., Karsch, F. J., & Hopkins, J. W. (1983) · Endocrinology · doi:10.1210/endo-113-1-329 · Cited by 132 · see citing works
Ueda, H. R., Chen, W., Minami, Y., Honma, S., Honma, K., Iino, M., & Hashimoto, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401882101 · Cited by 132 · 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
Thyroid hormones and seasonal reproductive neuroendocrine interactions
Nakao, N., Ono, H., & Yoshimura, T. (2008) · Reproduction · doi:10.1530/rep-08-0041 · Cited by 121 · see citing works
Multiple Roles of theeyes absentGene inDrosophila
Bonini, N. M., Leiserson, W. M., & Benzer, S. (1998) · Developmental Biology · doi:10.1006/dbio.1997.8845 · Cited by 114 · see citing works
Ukai, H., Kobayashi, T., Nagano, M., Masumoto, K., Sujino, M., Kondo, T., Yagita, K., Shigeyoshi, Y., & Ueda, H. R. (2007) · Nature Cell Biology · doi:10.1038/ncb1653 · Cited by 113 · see citing works
Six proteins regulate the activation of Myf5 expression in embryonic mouse limbs
Giordani, J., Bajard, L., Demignon, J., Daubas, P., BUCKINGHAM, M. E., & Maire, P. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611299104 · Cited by 109 · see citing works
A compilation of composite regulatory elements affecting gene transcription in vertebrates
Kel, O. V., Romaschenko, A. G., Kel, A. E., Wingender, E., & Kolchanov, N. A. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.20.4097 · Cited by 98 · see citing works
Melatonin Controls Seasonal Breeding by a Network of Hypothalamic Targets
Revel, F. G., Masson‐Pévet, M., Pévet, P., Mikkelsen, J. D., & Simonneaux, V. (2009) · Neuroendocrinology · doi:10.1159/000219588 · Cited by 97 · see citing works
Pauli, T., Seimiya, M., Blanco, J., & Gehring, W. J. (2005) · Development · doi:10.1242/dev.01841 · Cited by 96 · see citing works
The pars tuberalis of the pituitary: a gateway for neuroendocrine output
Morgan, P. J. (1996) · Reviews of Reproduction · doi:10.1530/ror.0.0010153 · Cited by 87 · 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
Analysis and synthesis of high-amplitude Cis -elements in the mammalian circadian clock
Kumaki, Y., Ukai‐Tadenuma, M., Uno, K. D., Nishio, J., Masumoto, K., Nagano, M., Komori, T., Shigeyoshi, Y., Hogenesch, J. B., & Ueda, H. R. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802636105 · Cited by 77 · see citing works
Jeong, B., Hong, C. Y., Chattopadhyay, S., Park, J., Gong, E., Kim, H., Chun, S., & Lee, K. (2003) · Molecular Endocrinology · doi:10.1210/me.2003-0065 · Cited by 67 · see citing works
Gordon, J. W., Pagiatakis, C., Salma, J., Du, ., Andreucci, J. J., Zhao, J., Hou, G., Perry, R. L., Dan, Q., Courtman, D. W., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.000539 · Cited by 66 · see citing works
Ikegami, K., Katou, Y., Higashi, K., & Yoshimura, T. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22165 · Cited by 40 · see citing works
Yoshimura, T., Nishio, M., Goto, M., & Ebihara, S. (1994) · Journal of Biological Rhythms · doi:10.1177/074873049400900105 · Cited by 33 · see citing works
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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
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
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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
Human blood metabolite timetable indicates internal body time
Kasukawa, T., Sugimoto, M., Hida, A., Minami, Y., Mori, M., Honma, S., Honma, K.-I., Mishima, K., Soga, T., & Ueda, H. R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207768109 · Cited by 211 · 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
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
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
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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
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
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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
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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
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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
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A photoperiodic molecular response in migratory redheaded bunting exposed to a single long day
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Xu, Z., Kaga, S., Tsubomizu, J., Fujisaki, J., Mochiduki, A., Sakai, T., Tsukamura, H., Maeda, K., Inoue, K., & Adachi, A. A. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.03.020 · Cited by 24 · see citing works
Gergics, P., Christian, H., Choo, M., Ajmal, A., & Camper, S. A. (2016) · Endocrinology · doi:10.1210/en.2016-1183 · Cited by 22 · see citing works
Neuroendocrine correlates of the critical day length response in the Soay sheep
Hazlerigg, D. G., Lomet, D., Lincoln, G. A., & Dardente, H. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12631 · Cited by 23 · see citing works
Pereira, J. C., Hallinan, M. P., & Alves, R. C. (2016) · Medical Hypotheses · doi:10.1016/j.mehy.2016.11.020 · Cited by 24 · see citing works
Dardente, H., Lomet, D., Chesneau, D., Pellicer-Rubio, M.-T., & Hazlerigg, D. G. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12775 · Cited by 22 · see citing works
Naughty Melatonin: How Mothers Tick Off their Fetus
Simonneaux, V. (2011) · Endocrinology · doi:10.1210/en.2011-0226 · Cited by 22 · see citing works
Melatonin and Seasonal Synchrony in Mammals
Hazlerigg, D. G., Simonneaux, V., & Dardente, H. (2024) · Journal of Pineal Research · doi:10.1111/jpi.12996 · Cited by 20 · see citing works
Clocks within the Master Gland
Lin, X., Blum, I. D., & Storch, K.-F. (2015) · Journal of Biological Rhythms · doi:10.1177/0748730415580881 · Cited by 20 · see citing works
Aizawa, S., Sakai, T., & Sakata, I. (2012) · Journal of Endocrinology · doi:10.1530/joe-11-0388 · Cited by 19 · see citing works
Establishment of TSH β real‐time monitoring system in mammalian photoperiodism
Tsujino, K., Narumi, R., Masumoto, K., Susaki, E. A., Shinohara, Y., Abe, T., Iigo, M., Wada, A., Nagano, M., Shigeyoshi, Y., et al. (2013) · Genes to Cells · doi:10.1111/gtc.12063 · Cited by 19 · see citing works
Evidence for RGS4 Modulation of Melatonin and Thyrotrophin Signalling Pathways in the Pars Tuberalis
Dupré, S. M., Dardente, H., Birnie, M. J., Loudon, A. S. I., Lincoln, G. A., & Hazlerigg, D. G. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02168.x · Cited by 19 · see citing works
Identification of Photoperiod-Induced LncRNAs and mRNAs in Pituitary Pars Tuberalis of Sheep
Xia, Q., Chu, M., He, X., Liu, Q., Zhang, X., Zhang, J., Guo, X., & Di, R. (2021) · Frontiers in Veterinary Science · doi:10.3389/fvets.2021.644474 · Cited by 18 · see citing works
Sur, S., Sharma, A., Malik, I., Bhardwaj, S. K., & Kumar, V. (2021) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2021.111017 · Cited by 18 · see citing works
Du, X., He, X., Liu, Q., Di, R., Liu, Q., & Chu, M. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.816241 · Cited by 17 · see citing works
Thyroid hormone and hypothalamic stem cells in seasonal functions
Dardente, H., & Migaud, M. (2021) · Vitamins and hormones · doi:10.1016/bs.vh.2021.02.005 · Cited by 17 · see citing works
Aubry, L. M., & Williams, C. T. (2022) · Integrative and Comparative Biology · doi:10.1093/icb/icac121 · Cited by 16 · see citing works
Fischer, C., Christ, E., Korf, H., & von Gall, C. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.02.016 · Cited by 15 · see citing works
Biological timekeeping in polar environments: lessons from terrestrial vertebrates
Hazlerigg, D. G., Appenroth, D., Tomotani, B. M., West, A. C., & Wood, S. H. (2023) · Journal of Experimental Biology · doi:10.1242/jeb.246308 · Cited by 14 · see citing works
Gonads or body? Differences in gonadal and somatic photoperiodic growth response in two vole species
van Rosmalen, L., van Dalum, J., Hazlerigg, D. G., & Hut, R. A. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.230987 · Cited by 14 · see citing works
Novel Candidate Regulators and Developmental Trajectory of Pituitary Thyrotropes
Cheung, L., Menage, L., Rizzoti, K., Hamilton, G., Dumontet, T., Basham, K. J., Daly, A. Z., Brinkmeier, M. L., Masser, B. E., Treier, M., et al. (2023) · Endocrinology · doi:10.1210/endocr/bqad076 · Cited by 14 · see citing works
FMR1, circadian genes and depression: suggestive associations or false discovery?
Kripke, D. F., Nievergelt, C. M., Tranah, G. J., Murray, S. S., Rex, K. M., Grizas, A. P., Hahn, E. K., Lee, H., Kelsoe, J. R., & Kline, L. E. (2013) · Journal of Circadian Rhythms · doi:10.1186/1740-3391-11-3 · Cited by 12 · see citing works
Hazlerigg, D. G., Blix, A. S., & Stokkan, K. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.163741 · Cited by 12 · see citing works
Modelling a molecular calendar: The seasonal photoperiodic response in mammals
Ebenhöh, O., & Hazlerigg, D. G. (2012) · Chaos Solitons & Fractals · doi:10.1016/j.chaos.2012.11.007 · Cited by 12 · see citing works
Michel, S. H., & Kervezee, L. (2023) · Journal of Comparative Physiology A · doi:10.1007/s00359-023-01680-4 · Cited by 12 · see citing works
Doyle, A., Cowan, M. E., Migaud, H., Wright, P. J., & Davie, A. (2021) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2021.111000 · Cited by 10 · see citing works
van Rosmalen, L., Riedstra, B., Beemster, N., Dijkstra, C., & Hut, R. A. (2022) · Molecular Ecology · doi:10.1111/mec.16467 · Cited by 10 · see citing works
Goto, M., Matsuo, H., Iigo, M., Furuse, M., Korf, H., & Yasuo, S. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.02.028 · Cited by 10 · see citing works
How can a binary switch within the pars tuberalis control seasonal timing of reproduction?
Wood, S. H. (2018) · Journal of Endocrinology · doi:10.1530/joe-18-0177 · Cited by 9 · see citing works
Ji, C., Ou, Y., Yu, W., Lv, J., Zhang, F., Li, H., Gu, Z., Li, J., Zhong, Z., & Wang, H. (2023) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2023.05.015 · Cited by 8 · see citing works
Ecological Genetics of Thyroid Hormone Physiology in Humans and Wild Animals
Ishikawa, A., & Kitano, J. (2012) · InTech eBooks · doi:10.5772/45969 · Cited by 8 · see citing works
Appenroth, D., West, A. C., Wood, S. H., & Hazlerigg, D. G. (2024) · Journal of Comparative Physiology A · doi:10.1007/s00359-024-01716-3 · Cited by 6 · see citing works
Floessner, T., Benetta, E. D., Beersma, D. G. M., & Hut, R. A. (2023) · Journal of Comparative Physiology A · doi:10.1007/s00359-023-01674-2 · Cited by 6 · see citing works
van Rosmalen, L., Schepers, R., Hao, W., Przybylska-Piech, A. S., Herman, J. S., Stojak, J., Wójcik, J. M., van de Zande, L., Searle, J. B., & Hut, R. A. (2023) · Genes · doi:10.3390/genes14020292 · Cited by 5 · see citing works
Du, X., He, X., Liu, Q., Liu, Q., Di, R., & Chu, M. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.888207 · Cited by 5 · see citing works
Non-human primate seasonal transcriptome atlas reveals seasonal changes in physiology and diseases
Chen, J., Okimura, K., Ren, L., Nakane, Y., Nakayama, T., Chen, Y., Fukawa, K., Sugiyama, S., Natsume, T., Suda‐Hashimoto, N., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-57994-1 · Cited by 4 · see citing works
The Pars Tuberalis and Seasonal Timing
Wood, S. H. (2020) · Masterclass in neuroendocrinology · doi:10.1007/978-3-030-55643-3_2 · Cited by 4 · see citing works
van Dalum, M. J., van Rosmalen, L., Appenroth, D., Cázarez‐Márquez, F., Roodenrijs, R. T. M., de Wit, L., Hut, R. A., & Hazlerigg, D. G. (2023) · Journal of Biological Rhythms · doi:10.1177/07487304231190156 · Cited by 4 · see citing works
Photoperiodic physiology of summer breeding birds and a search for the role of eye
Majumdar, G., Yadav, G., & Singh, N. S. (2023) · Photochemical & Photobiological Sciences · doi:10.1007/s43630-023-00505-2 · Cited by 3 · see citing works
Light-induced reproductive responses in white-rumped munia (Lonchura striata)
Lalpekhlui, R., Hnamler, L., & Trivedi, A. K. (2025) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2025.113300 · Cited by 3 · see citing works
Liu, J., Wang, Z., Wang, H., Yu, L., Yu, Y., & Sun, H. (2025) · Journal of Neuroendocrinology · doi:10.1111/jne.70093 · Cited by 3 · see citing works
Hnamler, L., & Trivedi, A. K. (2025) · Journal of Neuroendocrinology · doi:10.1111/jne.70095 · Cited by 3 · see citing works
Nakao, N., Nakagawa, K., Sasaki, A., Yamaguchi, A., Tsushima, N., & Tanaka, M. (2020) · The Journal of Poultry Science · doi:10.2141/jpsa.0190135 · Cited by 3 · see citing works
Khatib, L., Subasi, B. S., Fishman, B., Kapun, M., & Tauber, E. (2023) · Biology · doi:10.3390/biology12060858 · Cited by 3 · see citing works
Kameda, Y. (2023) · The Journal of Comparative Neurology · doi:10.1002/cne.25555 · Cited by 3 · see citing works
Arreaza‐Gil, V., Escobar‐Martínez, I., Soliz‐Rueda, J. R., Suárez, M., Muguerza, B., Schellekens, H., Torres‐Fuentes, C., & Arola‐Arnal, A. (2024) · Scientific Reports · doi:10.1038/s41598-024-73289-9 · Cited by 2 · see citing works
- Authors
- Masumoto, K.-H., Ukai-Tadenuma, M., Kasukawa, T., Nagano, M., Uno, K. D., Tsujino, K., Horikawa, K., Shigeyoshi, Y., & Ueda, H. R.
- Affiliations
- RIKEN (JP)
- Kindai University (JP)
- Kyoto University (JP)
- Corresponding author
- Shigeyoshi, Yasufumi
- Ueda, Hiroki R.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2010-12
- Volume
- 20
- Issue
- 24
- Pages
- 2199-2206
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2079304693
- Cited by
- 118
- References
- 45
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 4 · 2023: 10 · 2022: 5 · 2021: 9 · 2020: 11 · 2019: 4 · 2018: 5 · 2017: 7 · 2016: 4 · 2015: 4 · 2014: 8 · 2013: 11 · 2012: 12
- FWCI
- 5.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- 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
- photoperiodism, EYA3, Six1, pars tuberalis, transcriptional regulation, Eragrostis tef, HLF, melatonin, circadian rhythm
- MeSH terms
- Animals, Circadian Rhythm, DNA-Binding Proteins, Molecular Sequence Data, Photic Stimulation, Promoter Regions, Genetic, Photoperiod, Homeodomain Proteins, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Thyrotropin, beta Subunit, Mice
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