Circannual variation in thyroid hormone deiodinases in a short-day breeder

Cristina Saenz De Miera, Elodie Aline Hanon, Hugues Dardente, Michael James Birnie, Valerie Simonneaux, Gerald A Lincoln, David Grey Hazlerigg (Corresponding Author)

Research output: Contribution to journalArticle

43 Citations (Scopus)

Abstract

At temperate latitudes, many mammals and birds show internally timed, long-term changes in seasonal physiology, synchronised to the seasons by changing day length (photoperiod). Photoperiodic control of thyroid hormone levels in the hypothalamus dictates the timing. This is effected through reciprocal regulation of thyroid hormone deiodinase gene expression. The local synthesis of type 2 deiodinase (Dio2) promotes triiodothyronine (T3) production and summer biology, whereas type 3 deiodinase (Dio3) promotes T3 degradation and winter biology. In the present study, we investigated the extent to which the hypothalamic expression of Dio2 and Dio3 is circannually regulated in the Soay sheep, a short-day breeding mammal. Male sheep were exposed to a long photoperiod (LP; 16 : 24 h light/dark cycle) or a short photoperiod (SP; 8 : 24 h light/dark cycle), for up to 28 weeks to establish four different endocrine states: (i) LP animals in a spring/summer-like state of reproductive arrest; (ii) LP refractory (LPR) animals showing spontaneous reproductive reactivation; (iii) SP animals showing autumn/winter-like reproductive activation; and (iv) SP refractory (SPR) animals showing spontaneous reproductive arrest. A complex pattern of hypothalamic Dio2 and Dio3 expression was observed, revealing distinctive photoperiod-driven and internally timed effects for both genes. The patterns of expression differed both spatially and temporally, with phases of peak Dio2 expression in the median eminence and tuberoinfundibular sulcus, as well as in the paraventricular zone (PVZ) (maximal under LP), whereas Dio3 expression was always confined to the PVZ (maximal under SP). These effects likely reflect the distinct roles of these enzymes in the localised control of hypothalamic T3 levels. The spontaneous decline in Dio2 and spontaneous increase in Dio3 in LPR animals occurred with a corresponding decline in thyroid-stimulating hormone β expression in the neighbouring pars tuberalis (PT), although this relationship did not hold for the corresponding Dio2 increase/Dio3 decrease seen in SPR animals. We conclude that internally timed and spatially regulated changes in Dio2 and Dio3 expression may drive the cycling between breeding and nonbreeding states in long-lived seasonal species, and may be either PT-dependent or PT-independent at different phases of the circannual cycle.
Original languageEnglish
Pages (from-to)412-421
Number of pages10
JournalJournal of Neuroendocrinology
Volume25
Issue number4
Early online date21 Mar 2013
DOIs
Publication statusPublished - Apr 2013

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Iodide Peroxidase
Photoperiod
Thyroid Hormones
Breeding
Mammals
Sheep
Median Eminence
Triiodothyronine
Thyrotropin
Hypothalamus
Birds
Gene Expression
Enzymes
Genes

Keywords

  • deiodinase
  • TSHb
  • photorefractory
  • circannual
  • tanycyte
  • pars tuberalis

Cite this

Saenz De Miera, C., Hanon, E. A., Dardente, H., Birnie, M. J., Simonneaux, V., Lincoln, G. A., & Hazlerigg, D. G. (2013). Circannual variation in thyroid hormone deiodinases in a short-day breeder. Journal of Neuroendocrinology, 25(4), 412-421. https://doi.org/10.1111/jne.12013

Circannual variation in thyroid hormone deiodinases in a short-day breeder. / Saenz De Miera, Cristina; Hanon, Elodie Aline; Dardente, Hugues; Birnie, Michael James; Simonneaux, Valerie; Lincoln, Gerald A; Hazlerigg, David Grey (Corresponding Author).

In: Journal of Neuroendocrinology, Vol. 25, No. 4, 04.2013, p. 412-421.

Research output: Contribution to journalArticle

Saenz De Miera, C, Hanon, EA, Dardente, H, Birnie, MJ, Simonneaux, V, Lincoln, GA & Hazlerigg, DG 2013, 'Circannual variation in thyroid hormone deiodinases in a short-day breeder', Journal of Neuroendocrinology, vol. 25, no. 4, pp. 412-421. https://doi.org/10.1111/jne.12013
Saenz De Miera C, Hanon EA, Dardente H, Birnie MJ, Simonneaux V, Lincoln GA et al. Circannual variation in thyroid hormone deiodinases in a short-day breeder. Journal of Neuroendocrinology. 2013 Apr;25(4):412-421. https://doi.org/10.1111/jne.12013
Saenz De Miera, Cristina ; Hanon, Elodie Aline ; Dardente, Hugues ; Birnie, Michael James ; Simonneaux, Valerie ; Lincoln, Gerald A ; Hazlerigg, David Grey. / Circannual variation in thyroid hormone deiodinases in a short-day breeder. In: Journal of Neuroendocrinology. 2013 ; Vol. 25, No. 4. pp. 412-421.
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