Circannual Variation in Thyroid Hormone Deiodinases in a Short‐Day Breeder

C. Sáenz de Miera; E. A. Hanon; H. Dardente; M. Birnie; V. Simonneaux; G. A. Lincoln; D. G. Hazlerigg

doi:10.1111/jne.12013

journal article Mar 21, 2013

Circannual Variation in Thyroid Hormone Deiodinases in a Short‐Day Breeder

C. Sáenz de Miera E. A. Hanon H. Dardente M. Birnie V. Simonneaux G. A. Lincoln D. G. Hazlerigg

Journal of Neuroendocrinology Vol. 25 No. 4 pp. 412-421 · Wiley

View at Publisher Save 10.1111/jne.12013

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.

Topics

No keywords indexed for this article. Browse by subject →

References

53

[1]

Mammalian Photoperiodic System: Formal Properties and Neuroendocrine Mechanisms of Photoperiodic Time Measurement

Bruce D. Goldman

Journal of Biological Rhythms 10.1177/074873001129001980

[2]

10.1111/j.1600-079x.1993.tb00903.x

[3]

10.1095/biolreprod31.4.656

[4]

10.1073/pnas.111140398

[5]

10.1002/ar.1091730311

[6]

10.1095/biolreprod41.6.1034

[7]

10.1210/en.2005-0132

[8]

10.1095/biolreprod.107.064394

[9]

Pengelly E (1974)

[10]

10.1002/jez.1402010305

[11]

10.1677/joe.0.0780389

[12]

10.1530/jrf.0.0950325

[13]

10.1111/j.1600-079x.1994.tb00127.x

[14]

10.1007/978-1-4615-1201-1_20

[15]

10.1177/0748730409344502

[16]

10.1677/joe.0.1790001

[17]

10.1073/pnas.232490799

[18]

Photoperiodically‐lnduced Cycles in the Secretion of Prolactin in Hypothalamo‐Pituitary Disconnected Rams: Evidence for Translation of the Melatonin Signal in the Pituitary Gland

G. A. Lincoln, I. J. Clarke

Journal of Neuroendocrinology 10.1111/j.1365-2826.1994.tb00580.x

[19]

Ancestral TSH Mechanism Signals Summer in a Photoperiodic Mammal

Elodie A. Hanon, Gerald A. Lincoln, Jean-Michel Fustin et al.

Current Biology 10.1016/j.cub.2008.06.076

[20]

10.1016/j.cub.2008.07.040

[21]

10.1111/j.1365-2826.1995.tb00798.x

[22]

Nakao N "Thyrotrophin in the pars tuberalis triggers photoperiodic response" Nature (2008)

[23]

10.1210/en.2003-1593

[24]

10.1210/en.2006-0606

[25]

10.1152/ajpregu.00521.2006

[26]

10.1210/en.138.8.3402

[27]

10.1210/en.140.3.1111

[28]

10.1210/endo.143.7.8924

[29]

10.1152/ajpregu.00713.2006

[30]

10.1210/en.2007-0316

[31]

10.1210/en.2011-1249

[32]

10.1016/j.cmet.2006.12.002

[33]

10.1038/nm.2207

[34]

10.1177/0748730411420812

[35]

10.1038/nn.3091

[36]

10.1038/nn.3079

[37]

10.1016/j.cub.2010.02.066

[38]

10.1096/fj.02-0837com

[39]

10.1016/s0960-9822(03)00619-5

[40]

10.1095/biolreprod39.1.66

[41]

10.1530/jrf.0.0730241

[42]

10.1095/biolreprod57.2.460

[43]

10.1210/en.138.10.4101

[44]

10.1016/0031-9384(87)90161-2

[45]

10.1095/biolreprod30.1.143

[46]

Lincoln GA "Neuroendocrine regulation of seasonal gonadotrophin and prolactin rhythms: lessons from the Soay ram model" Reprod Suppl (2002)

[47]

10.1210/endo.138.8.5318

[48]

Tanycyte Pyroglutamyl Peptidase II Contributes to Regulation of the Hypothalamic-Pituitary-Thyroid Axis through Glial-Axonal Associations in the Median Eminence

Edith Sánchez, Miguel Angel Vargas, Praful S. Singru et al.

Endocrinology 10.1210/en.2008-1643

[49]

10.1210/en.2004-0366

[50]

10.1210/en.2011-1039

Showing 50 of 53 references

Metrics

74

Citations

53

References

Details

Published: Mar 21, 2013
Vol/Issue: 25(4)
Pages: 412-421
License: View

Authors

C

C. Sáenz de Miera

School of Biological Sciences University of Aberdeen Aberdeen UK; Département de Neurobiologie des Rythmes Institut des Neurosciences Cellulaires et Intégratives Université de Strasbourg Strasbourg France

E

E. A. Hanon

School of Biological Sciences University of Aberdeen Aberdeen UK; School of Biomedical Sciences University of Edinburgh The Queen's Medical Research Institute Edinburgh UK

H

H. Dardente

School of Biological Sciences University of Aberdeen Aberdeen UK; INRA UMR85 CNRS UMR7247 Université François Rabelais IFCE Nouzilly France

M

M. Birnie

School of Biological Sciences University of Aberdeen Aberdeen UK

V

V. Simonneaux

Département de Neurobiologie des Rythmes Institut des Neurosciences Cellulaires et Intégratives Université de Strasbourg Strasbourg France

G

G. A. Lincoln

School of Biomedical Sciences University of Edinburgh The Queen's Medical Research Institute Edinburgh UK

D

D. G. Hazlerigg

School of Biological Sciences University of Aberdeen Aberdeen UK

Funding

UK Medical Research Council

Cite This Article

C. Sáenz de Miera, E. A. Hanon, H. Dardente, et al. (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

You May Also Like