Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds

Abstract

Reproduction of many temperate zone birds is under photoperiodic control. The Japanese quail is an excellent model for studying the mechanism of photoperiodic time measurement because of its distinct and marked response to changing photoperiods. Studies on this animal have suggested that the mediobasal hypothalamus (MBH) is an important centre controlling photoperiodic time measurement1,2,3,4,5,6,7,8. Here we report that expression in the MBH of the gene encoding type 2 iodothyronine deiodinase (Dio2), which catalyses the intracellular deiodination of thyroxine (T4) prohormone to the active 3,5,3′-triiodothyronine (T3), is induced by light in Japanese quail. Intracerebroventricular administration of T3 mimics the photoperiodic response, whereas the Dio2 inhibitor iopanoic acid prevents gonadal growth. These findings demonstrate that light-induced Dio2 expression in the MBH may be involved in the photoperiodic response of gonads in Japanese quail.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Identification of a gene that controls photoperiodic time measurement.
Figure 2: Locally generated T3 acts on the BTH.
Figure 3: Intracerebroventricular T3 infusion mimics photoperiodically induced testicular growth.

Similar content being viewed by others

References

  1. Sharp, P. J. & Follett, B. K. The effect of hypothalamic lesions on gonadotrophin release in Japanese quail (Coturnix coturnix japonica). Neuroendocrinology 5, 205–218 (1969)

    Article  CAS  Google Scholar 

  2. Davies, D. T. & Follett, B. K. The neuroendocrine control of gonadotrophin release in Japanese quail. I. The role of the tuberal hypothalamus. Proc. R. Soc. Lond. B 191, 303–315 (1975)

    Article  ADS  CAS  Google Scholar 

  3. Ohta, M. & Homma, K. Detection of neural connections to the infundibular complex by partial or complete hypothalamic deafferentation in male quail. Gen. Comp. Endocrinol. 68, 286–292 (1987)

    Article  CAS  Google Scholar 

  4. Juss, T. S. in Avian Endocrinology (ed. Sharp, P. J.) 47–60 (Soc. Endocrinol., Bristol, 1993)

    Google Scholar 

  5. Konishi, H., Foster, R. G. & Follett, B. K. Evidence for a daily rhythmicity in the acute release of LH in response to electrical stimulation in the Japanese quail. J. Comp. Physiol. A 161, 315–319 (1987)

    Article  CAS  Google Scholar 

  6. Ohta, M., Wada, M. & Homma, K. Induction of rapid testicular growth in quail by phasic electrical stimulation of the hypothalamic photosensitive area. J. Comp. Physiol. A 154, 583–589 (1984)

    Article  Google Scholar 

  7. Meddle, S. L. & Follett, B. K. Photoperiodic activation of Fos-like immunoreactive protein in neurons within the tuberal hypothalamus of Japanese quail. J. Comp. Physiol. A 176, 79–89 (1995)

    Article  CAS  Google Scholar 

  8. Meddle, S. L. & Follett, B. K. Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J. Neurosci. 17, 8909–8918 (1997)

    Article  CAS  Google Scholar 

  9. Silver, R. et al. Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res. 253, 189–198 (1988)

    Article  CAS  Google Scholar 

  10. Yasuo, S., Watanabe, M., Okabayashi, N., Ebihara, S. & Yoshimura, T. Circadian clock genes and photoperiodism: Comprehensive analysis of clock genes expression in the mediobasal hypothalamus, the suprachiasmatic nucleus and the pineal gland of Japanese quail under various light schedules. Endocrinology 144, 3742–3748 (2003)

    Article  Google Scholar 

  11. Follett, B. K. & Sharp, P. J. Circadian rhythmicity in photoperiodically induced gonadotrophin release and gonadal growth in the quail. Nature 223, 968–971 (1969)

    Article  ADS  CAS  Google Scholar 

  12. Kuenzel, W. J. & Masson, M. A Stereotaxic Atlas of the Brain of the Chick (Gallus domesticus) (Johns Hopkins Univ. Press, Baltimore, 1988)

    Google Scholar 

  13. Bernal, J. Action of thyroid hormone in brain. J. Endocrinol. Invest. 25, 268–288 (2002)

    Article  CAS  Google Scholar 

  14. Prendergast, B. J., Mosinger, B. Jr, Kolattukudy, P. E. & Nelson, R. J. Hypothalamic gene expression in reproductively photoresponsive and photorefractory Siberian hamsters. Proc. Natl Acad. Sci. USA 99, 16291–16296 (2002)

    Article  ADS  CAS  Google Scholar 

  15. Dawson, A., King, V. M., Bentley, G. E. & Ball, G. F. Photoperiodic control of seasonality in birds. J. Biol. Rhythms 16, 365–380 (2001)

    Article  CAS  Google Scholar 

  16. Leonard, J. L. & Visser, T. J. in Thyroid Hormone Metabolism (ed. Hennemann, G.) 189–229 (Marcel Dekker, New York, 1986)

    Google Scholar 

  17. Follett, B. K. & Nicholls, T. J. Acute effect of thyroid hormones in mimicking photoperiodically induced release of gonadotropins in Japanese quail. J. Comp. Physiol. B 157, 837–843 (1988)

    Article  CAS  Google Scholar 

  18. Follett, B. K., Nicholls, T. J. & Mayes, C. R. Thyroxine can mimic photoperiodically induced gonadal growth in Japanese quail. J. Comp. Physiol. B 157, 829–835 (1988)

    Article  CAS  Google Scholar 

  19. Chopra, I. J. et al. Pathways of metabolism of thyroid hormones. Recent Prog. Horm. Res. 34, 521–567 (1978)

    CAS  PubMed  Google Scholar 

  20. Follett, B. K. & Nicholls, T. J. Photorefractoriness in Japanese quail: possible involvement of the thyroid gland. J. Exp. Zool. 232, 573–580 (1984)

    Article  CAS  Google Scholar 

  21. Follett, B. K. & Nicholls, T. J. Influences of thyroidectomy and thyroxine replacement on photoperiodically controlled reproduction in quail. J. Endocrinol. 107, 211–221 (1985)

    Article  CAS  Google Scholar 

  22. Dawson, A. Thyroidectomy progressively renders the reproductive system of starlings (Sturnus vulgaris) unresponsive to changes in daylength. J. Endocrinol. 139, 51–55 (1993)

    Article  CAS  Google Scholar 

  23. Dawson, A. thyroidectomy of house sparrow (Passer domesticus) prevents photo-induced testicular growth but not the increased hypothalamic gonadotrophin-releasing hormone. Gen. Comp. Endocrinol. 110, 196–200 (1998)

    Article  CAS  Google Scholar 

  24. Dawson, A. & Thapliyal, J. P. Avian Endocrinology (eds Dawson, A. & Chaturvedi, C. M.) 141–151 (Narosa, New Delhi, 2001)

    Google Scholar 

  25. Nicholls, T. J., Follett, B. K., Goldsmith, A. R. & Pearson, H. Possible homologies between photorefractoriness in sheep and birds: the effect of thyroidectomy on the length of the ewe's breeding season. Reprod. Nutr. Dev. 28, 375–385 (1988)

    Article  CAS  Google Scholar 

  26. Yoshimura, T. et al. Molecular analysis of avian circadian clock genes. Mol. Brain Res. 78, 207–215 (2000)

    Article  CAS  Google Scholar 

  27. Tagawa, M. & Hirano, T. Presence of thyroxine in eggs and changes in its content during early development of chum salmon, Oncorhynchus keta. Gen. Comp. Endocrinol. 68, 129–135 (1987)

    Article  CAS  Google Scholar 

  28. Ikuta, K., Aida, K., Okumoto, N. & Hanyu, I. Effects of sex steroids on the smoltification of masu salmon, Oncorhynchus masou. Gen. Comp. Endocrinol. 65, 99–110 (1987)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Nagoya University Radioisotope Center for use of its facilities. We also thank K. Aida, M. Tagawa and A. Munakata for providing antiserum, and A. Nishimura for technical assistance. This work was supported by the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN), a Grant-in-Aid for Encouragement of Young Scientists (to T.Yo.), and a Grant-in-Aid for Scientific Research (to S.E.) from the Ministry of Education, Science, Sports and Culture.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takashi Yoshimura.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yoshimura, T., Yasuo, S., Watanabe, M. et al. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426, 178–181 (2003). https://doi.org/10.1038/nature02117

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02117

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing