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Thyrotrophin in the pars tuberalis triggers photoperiodic response

Nature volume 452, pages 317–322 (2008)Cite this article

Abstract

Molecular mechanisms regulating animal seasonal breeding in response to changing photoperiod are not well understood. Rapid induction of gene expression of thyroid-hormone-activating enzyme (type 2 deiodinase, DIO2) in the mediobasal hypothalamus (MBH) of the Japanese quail (Coturnix japonica) is the earliest event yet recorded in the photoperiodic signal transduction pathway. Here we show cascades of gene expression in the quail MBH associated with the initiation of photoinduced secretion of luteinizing hormone. We identified two waves of gene expression. The first was initiated about 14 h after dawn of the first long day and included increased thyrotrophin (TSH) β-subunit expression in the pars tuberalis; the second occurred approximately 4 h later and included increased expression of DIO2. Intracerebroventricular (ICV) administration of TSH to short-day quail stimulated gonadal growth and expression of DIO2 which was shown to be mediated through a TSH receptor–cyclic AMP (cAMP) signalling pathway. Increased TSH in the pars tuberalis therefore seems to trigger long-day photoinduced seasonal breeding.

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Figure 1: Plasma luteinizing hormone and genome-wide analysis of genes expressed in the quail MBH during the first day of photostimulation (time 0 h is dawn of the first long day).
Figure 2: Localization of TSH-β and TSHR in the pars tuberalis and MBH.
Figure 3: Induction of the expression of DIO2 and three other second-wave genes by ICV injection of TSH and inhibition by ICV injection of anti-TSH-β IgG.
Figure 5: Effect of chronic ICV infusion of TSH on MBH DIO2 expression and testicular growth under short-day conditions.
Figure 4: Involvement of a cAMP signalling pathway in TSH induction of DIO2 gene expression.

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GenBank/EMBL/DDBJ

Gene Expression Omnibus

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Acknowledgements

We thank T. Kondo and the Nagoya University Radioisotope Centre for use of facilities. We also thank J. A. Proudman and A. F. Parlow for providing the chicken luteinizing hormone radioimmunoassay kit and the bovine TSH, respectively. This work was done as a part of the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN) and, in part, by Grant-in-Aid for Scientific Research (S), (B), Grant-in-Aid for Young Scientists (S), Grant-in-Aid for JSPS Fellows from the Japanese Society for the Promotion of Science, and a grant of the Genome Network Project from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Author Contributions T.Yo. conceived and directed the work. N.N., H.O., T.Ya., T.A., T.T., K.H., S.Y., Y.K., S.K., Y.U. and T.Yo. performed the microarray analysis and in situ hybridization. N.N., T.K., H.R.U. and T.Yo. analysed the microarray data. N.N. performed the quantitative PCR and promoter assay. M.I. and P.J.S. determined the luteinizing hormone assay. H.O. and M.I. performed the 125I-labelled TSH binding assay. T.Ya. and A.I. performed the immunocytochemistry. T.Ya., T.A. and A.I. examined the ICV injection and infusion. N.N., H.O., Y.S. and S.S. determined transcriptional start sites and genomic DNA sequences. T.Ni. cloned EYA, SIX and DACH family. M.M., T.Na. and S.E. provided laboratory facilities and new materials. All authors discussed the results and commented on the manuscript. T.Yo. and P.J.S. wrote the paper.

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Author notes

  1. Nobuhiro Nakao and Hiroko Ono: These authors contributed equally to this work.

Authors and Affiliations

  1. Division of Biomodelling, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan,

    Nobuhiro Nakao, Hiroko Ono, Takashi Yamamura, Tsubasa Anraku, Tsuyoshi Takagi, Kumiko Higashi, Shinobu Yasuo, Yasuhiro Katou, Saburo Kageyama, Yumiko Uno, Shizufumi Ebihara & Takashi Yoshimura

  2. Functional Genomics Subunit, Centre for Developmental Biology, RIKEN, 2-3-3 Minatojima-minamimachi, Chuo-ku, Kobe 650-0047, Japan,

    Takeya Kasukawa & Hiroki R. Ueda

  3. Department of Applied Biochemistry, Faculty of Agriculture, Utsunomiya University, 350 Mine-machi, Utsunomiya, 321-8505, Japan,

    Masayuki Iigo

  4. Division of Genetics and Genomics, Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Roslin, Midlothian EH25 9PS, UK,

    Peter J. Sharp

  5. Laboratory of Comparative Biochemistry, Graduate School of Applied Biological Sciences, Gifu University, Gifu 501-1193, Japan

    Atsushi Iwasawa

  6. Department of Medical Genome Sciences, Graduate School of Frontier Sciences, University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan,

    Yutaka Suzuki & Sumio Sugano

  7. Division of Biofunctions Development, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan,

    Teruyuki Niimi

  8. Avian Bioscience Research Centre, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan,

    Makoto Mizutani, Takao Namikawa, Shizufumi Ebihara & Takashi Yoshimura

  9. Laboratory for Systems Biology, Centre for Developmental Biology, RIKEN, 2-3-3 Minatojima-minamimachi, Chuo-ku, Kobe 650-0047, Japan,

    Hiroki R. Ueda

  10. Institute for Advanced Research, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan,

    Takashi Yoshimura

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  1. Nobuhiro Nakao
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Corresponding author

Correspondence to Takashi Yoshimura.

Additional information

The microarray data and DNA sequence information have been deposited in NCBI Gene Expression Omnibus (GEO) (GSE8016, GSE8017, GSE8018) and DDBJ/EMBL/GenBank (AB307676, AB307677, AB307678, AB307679, AB307680, AB307681 ), respectively.

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Nakao, N., Ono, H., Yamamura, T. et al. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452, 317–322 (2008). https://doi.org/10.1038/nature06738

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