Ancestral TSH mechanism signals summer in a photoperiodic mammal.
In mammals, day-length-sensitive (photoperiodic) seasonal breeding cycles depend on the pineal hormone melatonin, which modulates secretion of reproductive hormones by the anterior pituitary gland [1]. It is thought that melatonin acts in the hypothalamus to control reproduction through the release of neurosecretory signals into the pituitary portal blood supply, where they act on pituitary endocrine cells [2]. Contrastingly, we show here that during the reproductive response of Soay sheep exposed to summer day lengths, the reverse applies: Melatonin acts directly on anterior-pituitary cells, and these then relay the photoperiodic message back into the hypothalamus to control neuroendocrine output. The switch to long days causes melatonin-responsive cells in the pars tuberalis (PT) of the anterior pituitary to increase production of thyrotrophin (TSH). This acts locally on TSH-receptor-expressing cells in the adjacent mediobasal hypothalamus, leading to increased expression of type II thyroid hormone deiodinase (DIO2). DIO2 initiates the summer response by increasing hypothalamic tri-iodothyronine (T3) levels. These data and recent findings in quail [3] indicate that the TSH-expressing cells of the PT play an ancestral role in seasonal reproductive control in vertebrates. In mammals this provides the missing link between the pineal melatonin signal and thyroid-dependent seasonal biology.
Hanon
Elodie A
EA
School of Biological Sciences, University of Aberdeen, Aberdeen, Scotland.
Lincoln
Gerald A
GA
Fustin
Jean-Michel
JM
Dardente
Hugues
H
Masson-Pévet
Mireille
M
Morgan
Peter J
PJ
Hazlerigg
David G
DG
D000818:Animals; D005075:Biological Evolution; D005260:Female; D005786:Gene Expression Regulation / Q000187:drug effects; D007031:Hypothalamus / Q000378:metabolism; D007453:Iodide Peroxidase / Q000235:genetics / Q000378:metabolism; D008297:Male; D008550:Melatonin / Q000378:metabolism; D017440:Photoperiod; D010903:Pituitary Gland, Anterior / Q000378:metabolism; D012098:Reproduction / Q000502:physiology; D012621:Seasons; D012726:Sexual Behavior, Animal / Q000502:physiology*; D012756:Sheep / Q000502:physiology*; D015398:Signal Transduction; D013972:Thyrotropin / Q000378:metabolism* / Q000494:pharmacology / Q000502:physiology
D013972:Thyrotropin; D007453:Iodide Peroxidase; D008550:Melatonin