Work

Hypothalamic tanycytes as mediators of maternally programmed seasonal plasticity

Year: 2024

Type: article

Abstract: In mammals, maternal photoperiodic programming (MPP) provides a means whereby juvenile development can be matched to forthcoming seasonal environmental conditions. 1 1. Horton, T.H. Growth and maturation in Microtus montanus: effects of photoperiods before and after weaning Can. J. Zool. 1984; 62 :1741-1746 Crossref Scopus (30) Google Scholar , 2 2. Horton, T.H. Growth and reproductive development of male Microtus montanus is affected by the prenatal photoperiod Biol. Reprod. 1984; 31 :499-504 Crossref Scopus (84) PubMed Google Scholar , 3 3. Negus, N.C. ∙ Berger, P.J. ∙ Brown, B.W. Microtine population dynamics in a predictable environment Can. J. Zool. 1986; 64 :785-792 Crossref Scopus (41) Google Scholar , 4 4. Negus, N.C. ∙ Berger, P.J. ∙ Forslund, L.G. Reproductive strategy of Microtus montanus J. Mammal. 1977; 58 :347-353 Crossref Scopus (41) PubMed Google Scholar This phenomenon is driven by in utero effects of maternal melatonin 5 5. Weaver, D.R. ∙ Reppert, S.M. Maternal melatonin communicates day length to the fetus in djungarian hamsters Endocrinology. 1986; 119 :2861-2863 Crossref Scopus (84) PubMed Google Scholar , 6 6. Horton, T.H. ∙ Stachecki, S.A. ∙ Stetson, M.H. Maternal transfer of photoperiodic information in Siberian hamsters. IV. Peripubertal reproductive development in the absence of maternal photoperiodic signals during gestation Biol. Reprod. 1990; 42 :441-449 Crossref Scopus (27) PubMed Google Scholar , 7 7. Lee, T.M. ∙ Spears, N. ∙ Tuthill, C.R. ... Maternal melatonin treatment influences rates of neonatal development of meadow vole pups Biol. Reprod. 1989; 40 :495-502 Crossref Scopus (34) PubMed Google Scholar on the production of thyrotropin (TSH) in the fetal pars tuberalis (PT) and consequent TSH receptor-mediated effects on tanycytes lining the 3 rd ventricle of the mediobasal hypothalamus (MBH). 8 8. Saenz de Miera, C. ∙ Bothorel, B. ∙ Jaeger, C. ... Maternal photoperiod programs hypothalamic thyroid status via the fetal pituitary gland Proc. Natl. Acad. Sci. USA. 2017; 114 , 201702943 Crossref Scopus (44) PubMed Google Scholar , 9 9. Sáenz de Miera, C. ∙ Beymer, M. ∙ Routledge, K. ... Photoperiodic regulation in a wild-derived mouse strain J. Exp. Biol. 2020; 223 :jeb217687 Crossref Scopus (9) PubMed Google Scholar , 10 10. van Dalum, J. ∙ Melum, V.J. ∙ Wood, S.H. ... Maternal photoperiodic programming: melatonin and seasonal synchronization before birth Front. Endocrinol. 2019; 10 :901 Crossref Scopus (18) PubMed Google Scholar Here we use LASER capture microdissection and transcriptomic profiling to show that TSH-dependent MPP controls the attributes of the ependymal region of the MBH in juvenile animals. In Siberian hamster pups gestated and raised on a long photoperiod (LP) and thereby committed to a fast trajectory for growth and reproductive maturation, the ependymal region is enriched for tanycytes bearing sensory cilia and receptors implicated in metabolic sensing. Contrastingly, in pups gestated and raised on short photoperiod (SP) and therefore following an over-wintering developmental trajectory with delayed sexual maturation, the ependymal region has fewer sensory tanycytes. Post-weaning transfer of SP-gestated pups to an intermediate photoperiod (IP), which accelerates reproductive maturation, results in a pronounced shift toward a ciliated tanycytic profile and formation of tanycytic processes. We suggest that tanycytic plasticity constitutes a mechanism to tailor metabolic development for extended survival in variable overwintering environments.

Source: Current Biology

DOI: 10.1016/j.cub.2023.12.042