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Thyroid axis participates in high-temperature-induced male sex reversal through its activation by the stress response

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Abstract

Environmental changes alter the sex fate in about 15% of vertebrate orders, mainly in ectotherms such as fish and reptiles. However, the effects of temperature changes on the endocrine and molecular processes controlling gonadal sex determination are not fully understood. Here, we provide evidence that thyroid hormones (THs) act as co-players in heat-induced masculinization through interactions with the stress axis to promote testicular development. We first demonstrated that the thyroid axis (through thyroid-related genes and T3 levels) is highly active in males during the gonadal development in medaka (Oryzias latipes). Similarly, T3 treatments promoted female-to-male sex reversal in XX embryos. Subsequently, embryonic exposure to temperature-induced stress up-regulated the genes related to the thyroid and stress axes with a final increase in T3 levels. In this context, we show that blocking the stress axis response by the loss of function of the corticotropin-releasing hormone receptors suppresses thyroid-stimulating hormone expression, therefore, heat-induced activation of the thyroid axis. Thus, our data showed that early activation of the stress axis and, in consequence, the TH axis, too, leaves us with that both being important endocrine players in inducing female-to-male reversal, which can help predict possible upcoming physiological impacts of global warming on fish populations.

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Data availability

Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

Abbreviations

amh:

Anti-müllerian hormone

amhrII:

Anti-müllerian hormone receptor type II

ar:

Androgen receptor

BPI:

Brain-pituitary-interrenal

BPT:

Brain-pituitary-thyroid

CRH:

Corticotropin-releasing hormone

crhb:

Corticotropin-releasing hormone b

Crhr2:

Corticotropin-releasing hormone receptor 2

cyp19a1a:

Cytochrome P450, family 19, subfamily A, polypeptide 1a; ovary marker

dio1:

Deiodinase type 1

dio2:

Deiodinase type 2

dio3:

Deiodinase type 3

foxl2:

Forkhead box protein L2

gsdf:

Gonadal soma derived factor; testicular marker

MM:

Methimazole

R:

RU486; mifepristone

T:

Testosterone

T2:

Diiodothyronine; 3,5- diiodotyrosine

T3:

Triiodothyronine; 3, 5, 3´-L-triiodothyronine

T4:

Thyroxine; 3, 5, 3´, 5´-L-tetra-iodothyronine

THs:

Thyroid hormones

TRH:

Thyrotropin-releasing hormone

TSH:

Thyroid-stimulating hormone

thra:

Thyroid hormone receptors a

thrb:

Thyroid hormone receptors b

TRs:

Thyroid receptors

tshba:

Thyroid-stimulating hormone subunit beta a

tshr:

Thyroid-stimulating hormone receptors

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Acknowledgements

We thank Technician Gabriela C. López and Dr. Leandro A. Miranda (INTECH) for helping with histological preparations. We also thank Dr. Tania Rodriguez for technical support and Technician Javier Herdman (INTECH) for fish handling. We thank NBRP Medaka (https://shigen.nig.ac.jp/medaka/) for providing HNI (Strain ID: MT835).

Funding

This work was supported by the Agencia Nacional de Promoción Científica y Tecnológica Grants 2501/15, 1875/18 and 3231/20 (to J.I.F.). VSL holds a Canada Research Chair (950-232235). RHN and IFR were supported by São Paulo Research Foundation (FAPESP), Brazil (grant numbers 14/07620-7; 18/10265-5; 20/15237-0; 21/06742-5). DCCC, AFB and NP were supported by a PhD scholarship from the National Research Council (CONICET). JIF and PHSM are members of the Research Scientist Career at the CONICET.

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Author notes

  1. Diana C. Castañeda-Cortés and Ivana F. Rosa Equal contribution.

Authors and Affiliations

  1. Instituto Tecnológico de Chascomús, INTECH (CONICET-UNSAM), Chascomús, Argentina

    Diana C. Castañeda-Cortés, Agustín F. Boan, Demian Marrone, Natalia Pagliaro, María S. Dodds, Pablo H. Strobl-Mazzulla & Juan I. Fernandino

  2. Escuela de Bio y Nanotecnologías (UNSAM), Chascomús, Argentina

    Diana C. Castañeda-Cortés, Agustín F. Boan, Demian Marrone, Natalia Pagliaro, María S. Dodds, Pablo H. Strobl-Mazzulla & Juan I. Fernandino

  3. Institut National de la Recherche Scientifique (INRS) - Centre Eau Terre Environnement, Québec, QC, Canada

    Diana C. Castañeda-Cortés & Valerie S. Langlois

  4. Reproductive and Molecular Biology Group, Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil

    Ivana F. Rosa, Marcos A. Oliveira, Maira S. Rodrigues, Lucas B. Doretto, Camila Silva, José Tavares-Júnior, Daniel F. Costa & Rafael H. Nóbrega

  5. South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and Hydrobiology, Faculty of Fisheries and Protection of Waters, University of South Bohemia in Ceske Budejovice, Vodňany, Ceske Budejovice, 389 25, Czech Republic

    Rafael H. Nóbrega

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  1. Diana C. Castañeda-Cortés
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DCCC: conceptualization, methodology, visualization and editing; IFR: conceptualization, methodology and editing; AFB: methodology; DM: methodology; NP: methodology; MAO: methodology MSR: methodology; LB: methodology; CS: methodology; JTJ: methodology, DFC: methodology, SD: methodology; PHS: editing; VSL: conceptualization, supervision; writing-reviewing and editing; RHN: conceptualization, investigation, supervision, writing-reviewing and editing, JIF: writing- original draft preparation, funding acquisition, conceptualization, investigation, supervision, writing-reviewing and editing.

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Correspondence to Valerie S. Langlois, Rafael H. Nóbrega or Juan I. Fernandino.

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The authors have no relevant financial or non-financial interests to disclose.

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Fish were handled under the ethical regulations of the institutional committee for the Brazilian legislation regulated by the Ethical Principles in Animal Research (Protocol n. 1868-CEUA) and the Institutional Committee for the Care and Use of Experimental Animals from Universidad de San Martín, Argentina (CICUAE-UNSAM 010/2021).

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Crosstalk Between the Thyroid and Stress Axes in Thermal-Induced Masculinization in Fish.

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Castañeda-Cortés, D.C., Rosa, I.F., Boan, A.F. et al. Thyroid axis participates in high-temperature-induced male sex reversal through its activation by the stress response. Cell. Mol. Life Sci. 80, 253 (2023). https://doi.org/10.1007/s00018-023-04913-6

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