Low temperature-induced circulating triiodothyronine accelerates seasonal testicular regression

Keisuke Ikegami, Yusuke Atsumi, Eriko Yorinaga, Hiroko Ono, Itaru Murayama, Yusuke Nakane, Wataru Ota, Natsumi Arai, Akinori Tega, Masayuki Iigo, Veerle M. Darras, Kazuyoshi Tsutsui, Yoshitaka Hayashi, Shosei Yoshida, Takashi Yoshimura

    Research output: Contribution to journalArticle

    15 Citations (Scopus)

    Abstract

    In temperate zones, animals restrict breeding to specific seasons to maximize the survival of their offspring. Birds have evolved highly sophisticated mechanisms of seasonal regulation, and their testicular mass can change 100-fold within a few weeks. Recent studies on Japanese quail revealed that seasonal gonadal development is regulated by central thyroid hormone activation within the hypothalamus, depending on the photoperiodic changes. By contrast, the mechanisms underlying seasonal testicular regression remain unclear. Here we show the effects of short day and low temperature on testicular regression in quail. Low temperature stimulus accelerated short dayinduced testicular regression by shutting down the hypothalamus-pituitary-gonadal axis and inducing meiotic arrestandgermcell apoptosis. Induction of T3 coincided with the climax of testicular regression. Temporal gene expression analysis over the course of apoptosis revealed the suppression of LH response genes and activation of T3 response genes involved in amphibian metamorphosis within the testis. Daily ip administration of T3 mimicked the effects of low temperature stimulus on germ cell apoptosis and testicular mass. Although type 2 deiodinase, a thyroid hormone- activating enzyme, in the brown adipose tissue generates circulating T3 under low-temperature conditions in mammals, there is no distinct brown adipose tissue in birds. In birds, type 2 deiodinase is induced by low temperature exclusively in the liver, which appears to be caused by increased food consumption. We conclude that birds use low temperature-induced circulating T3 not only for adaptive thermoregulation but also to trigger apoptosis to accelerate seasonal testicular regression.

    Original languageEnglish
    Pages (from-to)647-659
    Number of pages13
    JournalEndocrinology
    Volume156
    Issue number2
    DOIs
    Publication statusPublished - 2015 Feb 1

    Fingerprint

    Triiodothyronine
    Temperature
    Birds
    Apoptosis
    Iodide Peroxidase
    Brown Adipose Tissue
    Thyroid Hormones
    Hypothalamus
    Coturnix
    Quail
    Body Temperature Regulation
    Amphibians
    Germ Cells
    Transcriptional Activation
    Breeding
    Testis
    Mammals
    Gene Expression
    Food
    Liver

    ASJC Scopus subject areas

    • Endocrinology

    Cite this

    Ikegami, K., Atsumi, Y., Yorinaga, E., Ono, H., Murayama, I., Nakane, Y., ... Yoshimura, T. (2015). Low temperature-induced circulating triiodothyronine accelerates seasonal testicular regression. Endocrinology, 156(2), 647-659. https://doi.org/10.1210/en.2014-1741

    Low temperature-induced circulating triiodothyronine accelerates seasonal testicular regression. / Ikegami, Keisuke; Atsumi, Yusuke; Yorinaga, Eriko; Ono, Hiroko; Murayama, Itaru; Nakane, Yusuke; Ota, Wataru; Arai, Natsumi; Tega, Akinori; Iigo, Masayuki; Darras, Veerle M.; Tsutsui, Kazuyoshi; Hayashi, Yoshitaka; Yoshida, Shosei; Yoshimura, Takashi.

    In: Endocrinology, Vol. 156, No. 2, 01.02.2015, p. 647-659.

    Research output: Contribution to journalArticle

    Ikegami, K, Atsumi, Y, Yorinaga, E, Ono, H, Murayama, I, Nakane, Y, Ota, W, Arai, N, Tega, A, Iigo, M, Darras, VM, Tsutsui, K, Hayashi, Y, Yoshida, S & Yoshimura, T 2015, 'Low temperature-induced circulating triiodothyronine accelerates seasonal testicular regression', Endocrinology, vol. 156, no. 2, pp. 647-659. https://doi.org/10.1210/en.2014-1741
    Ikegami K, Atsumi Y, Yorinaga E, Ono H, Murayama I, Nakane Y et al. Low temperature-induced circulating triiodothyronine accelerates seasonal testicular regression. Endocrinology. 2015 Feb 1;156(2):647-659. https://doi.org/10.1210/en.2014-1741
    Ikegami, Keisuke ; Atsumi, Yusuke ; Yorinaga, Eriko ; Ono, Hiroko ; Murayama, Itaru ; Nakane, Yusuke ; Ota, Wataru ; Arai, Natsumi ; Tega, Akinori ; Iigo, Masayuki ; Darras, Veerle M. ; Tsutsui, Kazuyoshi ; Hayashi, Yoshitaka ; Yoshida, Shosei ; Yoshimura, Takashi. / Low temperature-induced circulating triiodothyronine accelerates seasonal testicular regression. In: Endocrinology. 2015 ; Vol. 156, No. 2. pp. 647-659.
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    AU - Murayama, Itaru

    AU - Nakane, Yusuke

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    AU - Arai, Natsumi

    AU - Tega, Akinori

    AU - Iigo, Masayuki

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    AU - Tsutsui, Kazuyoshi

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