Neural thyroid hormone metabolism integrates seasonal changes in environmental temperature with the neuroendocrine reproductive axis
Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved..
We asked if environmental temperature alters thyroid hormone metabolism within the hypothalamus, thereby providing a neuroendocrine mechanism by which temperature could be integrated with photoperiod to regulate seasonal rhythms. We used immunohistochemistry to assess the effects of low-temperature winter dormancy at 4 °C or 12 °C on thyroid-stimulating hormone (TSH) within the infundibulum of the pituitary as well as deiodinase 2 (Dio2) and 3 (Dio3) within the hypothalamus of red-sided garter snakes (Thamnophis sirtalis). Both the duration and, in males, magnitude of low-temperature dormancy altered deiodinase immunoreactivity within the hypothalamus, increasing the area of Dio2-immunoreactivity in males and females and decreasing the number of Dio3-immunoreactive cells in males after 8-16 weeks. Reciprocal changes in Dio2/3 favor the accumulation of triiodothyronine within the hypothalamus. Whether TSH mediates these effects requires further study, as significant changes in TSH-immunoreactive cell number were not observed. Temporal changes in deiodinase immunoreactivity coincided with an increase in the proportion of males exhibiting courtship behavior as well as changes in the temporal pattern of courtship behavior after emergence. Our findings mirror those of previous studies, in which males require low-temperature exposure for at least 8 weeks before significant changes in gonadotropin-releasing hormone immunoreactivity and sex steroid hormones are observed. Collectively, these data provide evidence that the neuroendocrine pathway regulating the reproductive axis via thyroid hormone metabolism is capable of transducing temperature information. Because all vertebrates can potentially use temperature as a supplementary cue, these results are broadly applicable to understanding how environment-organism interactions mediate seasonally adaptive responses.
| Medienart: |
E-Artikel |
|---|
| Erscheinungsjahr: |
2024 |
|---|---|
| Erschienen: |
2024 |
| Enthalten in: |
Zur Gesamtaufnahme - volume:161 |
|---|---|
| Enthalten in: |
Hormones and behavior - 161(2024) vom: 28. Feb., Seite 105517 |
| Sprache: |
Englisch |
|---|
| Beteiligte Personen: |
Lutterschmidt, Deborah I [VerfasserIn] |
|---|
| Links: |
|---|
| Themen: |
Brumation |
|---|
| Anmerkungen: |
Date Revised 29.02.2024 published: Print-Electronic Citation Status Publisher |
|---|
| doi: |
10.1016/j.yhbeh.2024.105517 |
|---|
| funding: |
|
|---|---|
| Förderinstitution / Projekttitel: |
|
| PPN (Katalog-ID): |
NLM369127617 |
|---|
| LEADER | 01000naa a22002652 4500 | ||
|---|---|---|---|
| 001 | NLM369127617 | ||
| 003 | DE-627 | ||
| 005 | 20240301233136.0 | ||
| 007 | cr uuu---uuuuu | ||
| 008 | 240301s2024 xx |||||o 00| ||eng c | ||
| 024 | 7 | |a 10.1016/j.yhbeh.2024.105517 |2 doi | |
| 028 | 5 | 2 | |a pubmed24n1313.xml |
| 035 | |a (DE-627)NLM369127617 | ||
| 035 | |a (NLM)38422864 | ||
| 035 | |a (PII)S0018-506X(24)00042-4 | ||
| 040 | |a DE-627 |b ger |c DE-627 |e rakwb | ||
| 041 | |a eng | ||
| 100 | 1 | |a Lutterschmidt, Deborah I |e verfasserin |4 aut | |
| 245 | 1 | 0 | |a Neural thyroid hormone metabolism integrates seasonal changes in environmental temperature with the neuroendocrine reproductive axis |
| 264 | 1 | |c 2024 | |
| 336 | |a Text |b txt |2 rdacontent | ||
| 337 | |a ƒaComputermedien |b c |2 rdamedia | ||
| 338 | |a ƒa Online-Ressource |b cr |2 rdacarrier | ||
| 500 | |a Date Revised 29.02.2024 | ||
| 500 | |a published: Print-Electronic | ||
| 500 | |a Citation Status Publisher | ||
| 520 | |a Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved. | ||
| 520 | |a We asked if environmental temperature alters thyroid hormone metabolism within the hypothalamus, thereby providing a neuroendocrine mechanism by which temperature could be integrated with photoperiod to regulate seasonal rhythms. We used immunohistochemistry to assess the effects of low-temperature winter dormancy at 4 °C or 12 °C on thyroid-stimulating hormone (TSH) within the infundibulum of the pituitary as well as deiodinase 2 (Dio2) and 3 (Dio3) within the hypothalamus of red-sided garter snakes (Thamnophis sirtalis). Both the duration and, in males, magnitude of low-temperature dormancy altered deiodinase immunoreactivity within the hypothalamus, increasing the area of Dio2-immunoreactivity in males and females and decreasing the number of Dio3-immunoreactive cells in males after 8-16 weeks. Reciprocal changes in Dio2/3 favor the accumulation of triiodothyronine within the hypothalamus. Whether TSH mediates these effects requires further study, as significant changes in TSH-immunoreactive cell number were not observed. Temporal changes in deiodinase immunoreactivity coincided with an increase in the proportion of males exhibiting courtship behavior as well as changes in the temporal pattern of courtship behavior after emergence. Our findings mirror those of previous studies, in which males require low-temperature exposure for at least 8 weeks before significant changes in gonadotropin-releasing hormone immunoreactivity and sex steroid hormones are observed. Collectively, these data provide evidence that the neuroendocrine pathway regulating the reproductive axis via thyroid hormone metabolism is capable of transducing temperature information. Because all vertebrates can potentially use temperature as a supplementary cue, these results are broadly applicable to understanding how environment-organism interactions mediate seasonally adaptive responses | ||
| 650 | 4 | |a Journal Article | |
| 650 | 4 | |a Brumation | |
| 650 | 4 | |a Courtship behavior | |
| 650 | 4 | |a Deiodinase | |
| 650 | 4 | |a GnRH | |
| 650 | 4 | |a Reptile | |
| 650 | 4 | |a Seasonal reproduction | |
| 650 | 4 | |a Snake | |
| 650 | 4 | |a TSH | |
| 650 | 4 | |a Thyrotropin | |
| 650 | 4 | |a Winter dormancy | |
| 700 | 1 | |a Stratton, Kalera |e verfasserin |4 aut | |
| 700 | 1 | |a Winters, Treven J |e verfasserin |4 aut | |
| 700 | 1 | |a Martin, Stephanie |e verfasserin |4 aut | |
| 700 | 1 | |a Merlino, Lauren J |e verfasserin |4 aut | |
| 773 | 0 | 8 | |i Enthalten in |t Hormones and behavior |d 1972 |g 161(2024) vom: 28. Feb., Seite 105517 |w (DE-627)NLM000202312 |x 1095-6867 |7 nnns |
| 773 | 1 | 8 | |g volume:161 |g year:2024 |g day:28 |g month:02 |g pages:105517 |
| 856 | 4 | 0 | |u http://dx.doi.org/10.1016/j.yhbeh.2024.105517 |3 Volltext |
| 912 | |a GBV_USEFLAG_A | ||
| 912 | |a GBV_NLM | ||
| 951 | |a AR | ||
| 952 | |d 161 |j 2024 |b 28 |c 02 |h 105517 | ||