A unifying hypothesis for control of body weight and reproduction in seasonally breeding mammals

Gisela Helfer (Corresponding Author), Perry Barrett, Peter J Morgan

Research output: Contribution to journalReview article

3 Citations (Scopus)

Abstract

Animals have evolved diverse seasonal variations in physiology and reproduction to accommodate yearly changes in environmental and climatic conditions. These changes in physiology are initiated by changes in photoperiod (daylength) and are mediated through melatonin which relays photoperiodic information to the pars tuberalis of the pituitary gland. Melatonin drives thyroid stimulating hormone transcription and synthesis in the pars tuberalis which in turn regulates thyroid hormone and retinoic acid synthesis in the tanycytes lining the third ventricle of the hypothalamus. Seasonal variation in central thyroid hormone signalling is conserved among photoperiodic animals. Despite this, different species adopt divergent phenotypes to cope with the same seasonal changes. A common response amongst different species is increased hypothalamic cell proliferation/neurogenesis in short photoperiod. That cell proliferation/neurogenesis may be important for seasonal timing is based on 1) the neurogenic potential of tanycytes, 2) the fact that they are the locus of striking seasonal morphological changes and 3) the similarities to mechanisms involved in de novo neurogenesis of energy balance neurons. We propose that a fall in hypothalamic thyroid hormone and retinoic acid signalling initiates localised neurodegeneration and apoptosis which leads to a reduction in appetite and body weight. Neurodegeneration induces compensatory cell proliferation from the neurogenic niche in tanycytes and new cells are born under short photoperiod. Since these cells have the potential to differentiate into a number of different neuronal phenotypes, this could provide a mechanistic basis to explain the seasonal regulation of energy balance as well as reproduction. This cycle can be achieved without changes in thyroid hormone/retinoic acid and explains recent data from seasonal animals held in natural conditions. However, thyroid/retinoic acid signalling are required to synchronise the cycles of apoptosis, proliferation and differentiation. Thus, hypothalamic neurogenesis provides a framework to explain diverse photoperiodic responses.

Original languageEnglish
Article numbere12680
JournalJournal of Neuroendocrinology
Volume31
Issue number3
Early online date12 Feb 2019
DOIs
Publication statusPublished - Mar 2019

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Neurogenesis
Tretinoin
Ependymoglial Cells
Thyroid Hormones
Breeding
Reproduction
Mammals
Photoperiod
Body Weight
Cell Proliferation
Melatonin
Hypothalamic Hormones
Apoptosis
Phenotype
Third Ventricle
Appetite
Pituitary Gland
Thyrotropin
Hypothalamus
Thyroid Gland

Keywords

  • photoperiod
  • season
  • pars tuberalis
  • tanycyte
  • melatonin
  • neurogenesis
  • neuroendocrinology
  • thyroid hormone
  • retinoic acid
  • HYPOTHALAMIC GENE-EXPRESSION
  • THYROID-HORMONE
  • FOOD-INTAKE
  • TUBERALIS-SPECIFIC CELLS
  • IODOTHYRONINE DEIODINASE EXPRESSION
  • SIGNAL-TRANSDUCTION
  • AGOUTI-RELATED PROTEIN
  • RETINOIC ACID
  • MELATONIN-RELATED RECEPTOR
  • PARS TUBERALIS

ASJC Scopus subject areas

  • Endocrine and Autonomic Systems
  • Endocrinology
  • Cellular and Molecular Neuroscience
  • Endocrinology, Diabetes and Metabolism

Cite this

A unifying hypothesis for control of body weight and reproduction in seasonally breeding mammals. / Helfer, Gisela (Corresponding Author); Barrett, Perry; Morgan, Peter J.

In: Journal of Neuroendocrinology, Vol. 31, No. 3, e12680, 03.2019.

Research output: Contribution to journalReview article

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abstract = "Animals have evolved diverse seasonal variations in physiology and reproduction to accommodate yearly changes in environmental and climatic conditions. These changes in physiology are initiated by changes in photoperiod (daylength) and are mediated through melatonin which relays photoperiodic information to the pars tuberalis of the pituitary gland. Melatonin drives thyroid stimulating hormone transcription and synthesis in the pars tuberalis which in turn regulates thyroid hormone and retinoic acid synthesis in the tanycytes lining the third ventricle of the hypothalamus. Seasonal variation in central thyroid hormone signalling is conserved among photoperiodic animals. Despite this, different species adopt divergent phenotypes to cope with the same seasonal changes. A common response amongst different species is increased hypothalamic cell proliferation/neurogenesis in short photoperiod. That cell proliferation/neurogenesis may be important for seasonal timing is based on 1) the neurogenic potential of tanycytes, 2) the fact that they are the locus of striking seasonal morphological changes and 3) the similarities to mechanisms involved in de novo neurogenesis of energy balance neurons. We propose that a fall in hypothalamic thyroid hormone and retinoic acid signalling initiates localised neurodegeneration and apoptosis which leads to a reduction in appetite and body weight. Neurodegeneration induces compensatory cell proliferation from the neurogenic niche in tanycytes and new cells are born under short photoperiod. Since these cells have the potential to differentiate into a number of different neuronal phenotypes, this could provide a mechanistic basis to explain the seasonal regulation of energy balance as well as reproduction. This cycle can be achieved without changes in thyroid hormone/retinoic acid and explains recent data from seasonal animals held in natural conditions. However, thyroid/retinoic acid signalling are required to synchronise the cycles of apoptosis, proliferation and differentiation. Thus, hypothalamic neurogenesis provides a framework to explain diverse photoperiodic responses.",
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N2 - Animals have evolved diverse seasonal variations in physiology and reproduction to accommodate yearly changes in environmental and climatic conditions. These changes in physiology are initiated by changes in photoperiod (daylength) and are mediated through melatonin which relays photoperiodic information to the pars tuberalis of the pituitary gland. Melatonin drives thyroid stimulating hormone transcription and synthesis in the pars tuberalis which in turn regulates thyroid hormone and retinoic acid synthesis in the tanycytes lining the third ventricle of the hypothalamus. Seasonal variation in central thyroid hormone signalling is conserved among photoperiodic animals. Despite this, different species adopt divergent phenotypes to cope with the same seasonal changes. A common response amongst different species is increased hypothalamic cell proliferation/neurogenesis in short photoperiod. That cell proliferation/neurogenesis may be important for seasonal timing is based on 1) the neurogenic potential of tanycytes, 2) the fact that they are the locus of striking seasonal morphological changes and 3) the similarities to mechanisms involved in de novo neurogenesis of energy balance neurons. We propose that a fall in hypothalamic thyroid hormone and retinoic acid signalling initiates localised neurodegeneration and apoptosis which leads to a reduction in appetite and body weight. Neurodegeneration induces compensatory cell proliferation from the neurogenic niche in tanycytes and new cells are born under short photoperiod. Since these cells have the potential to differentiate into a number of different neuronal phenotypes, this could provide a mechanistic basis to explain the seasonal regulation of energy balance as well as reproduction. This cycle can be achieved without changes in thyroid hormone/retinoic acid and explains recent data from seasonal animals held in natural conditions. However, thyroid/retinoic acid signalling are required to synchronise the cycles of apoptosis, proliferation and differentiation. Thus, hypothalamic neurogenesis provides a framework to explain diverse photoperiodic responses.

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