Influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of Sirtuins in cumulus oocyte complexes in cattle

Sirtuins are of central importance in many cellular functions and promote cell survival under stress. However, little information is available regarding the relationship between sirtuins and female reproductive biology, especially in response to thermal stress. This study investigated the influence...

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Main Authors: Ralf Pöhland, Mirela Brochado Souza-Cáceres, Tirtha Kumar Datta, Jens Vanselow, Wilian Aparecido Leite da Silva, Christopher Junior Tavares Cardoso, Fabiana de Andrade Melo Sterza
Format: Article
Language:English
Published: Universidade Estadual de Londrina 2024-12-01
Series:Semina: Ciências Agrárias
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Online Access:https://ojs.uel.br/revistas/uel/index.php/semagrarias/article/view/51430
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author Ralf Pöhland
Mirela Brochado Souza-Cáceres
Tirtha Kumar Datta
Jens Vanselow
Wilian Aparecido Leite da Silva
Christopher Junior Tavares Cardoso
Fabiana de Andrade Melo Sterza
author_facet Ralf Pöhland
Mirela Brochado Souza-Cáceres
Tirtha Kumar Datta
Jens Vanselow
Wilian Aparecido Leite da Silva
Christopher Junior Tavares Cardoso
Fabiana de Andrade Melo Sterza
author_sort Ralf Pöhland
collection DOAJ
description Sirtuins are of central importance in many cellular functions and promote cell survival under stress. However, little information is available regarding the relationship between sirtuins and female reproductive biology, especially in response to thermal stress. This study investigated the influence of moderately high (40°C) and low (37°C) thermal stress during in vitro maturation on the development competence of bovine oocytes and embryos. The expression and abundance of sirtuins and other proteins involved in stress response were also studied. The cumulus-oocyte complexes (COCs) of Simmental (Bos taurus) cows underwent in vitro maturation (IVM) at different temperatures (37°C, 38.5°C and 40°C). Before maturation, the oocytes were stained with Brilliant Cresyl Blue (BCB) and categorized as labeled (BCB+) or unlabeled (BCB-). Embryo production was analyzed at the different IVM temperatures. Polar body extrusion was evaluated following IVM, and the mRNA and protein abundance of sirtuins and P53 in oocytes and cumulus cells were analyzed. The differing temperatures during IVM did not significantly alter polar body extrusion and cleavage rates; however, significant differences in blastocyst production were observed. COCs matured at 38.5°C (control) had the highest blastocyst rate, in contrast to those matured at 37°C (33.2%) and 40°C (21.5%). In all groups, the blastocyst rates were higher for BCB+ oocytes than for BCB- oocytes. In BCB+ oocytes, the expression of SIRT1, SIRT2, SIRT3, and SIRT5 genes was higher after maturation than that before maturation and in most of the cases, the expression was higher when IVM was performed at 38.5°C. In the cumulus cells of BCB+ COCs, only SIRT2 remained unaffected by the maturation temperature. In summary, the temperature change of ±1.5°C for 24 h during bovine oocyte maturation impaired in vitro embryo development. This lead to several cellular biochemical alterations in oocytes and granulosa cells from COCs with higher developmental competence (BCB+). Thus, SIRT1 is important for in vitro embryonic development and may protect against cold and heat stress.
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spelling doaj-art-b7bd90682f42495da814f44c3741e5f32024-12-17T06:47:46ZengUniversidade Estadual de LondrinaSemina: Ciências Agrárias1676-546X1679-03592024-12-0146110.5433/1679-0359.2025v46n1p149Influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of Sirtuins in cumulus oocyte complexes in cattleRalf Pöhland0https://orcid.org/0000-0003-2521-6126Mirela Brochado Souza-Cáceres1https://orcid.org/0000-0002-7846-7685Tirtha Kumar Datta2Jens Vanselow3Wilian Aparecido Leite da Silva4Christopher Junior Tavares Cardoso5https://orcid.org/0000-0001-7815-3339Fabiana de Andrade Melo Sterza6https://orcid.org/0000-0002-0597-9663Research Institute for Farm Animal BiologyUniversidade Federal de São Carlos National Dairy Research InstituteResearch Institute for Farm Animal BiologyUniversidade Estadual do Mato Grosso do SulUniversidade Federal do Mato Grosso do SulUniversidade Estadual do Mato Grosso do Sul Sirtuins are of central importance in many cellular functions and promote cell survival under stress. However, little information is available regarding the relationship between sirtuins and female reproductive biology, especially in response to thermal stress. This study investigated the influence of moderately high (40°C) and low (37°C) thermal stress during in vitro maturation on the development competence of bovine oocytes and embryos. The expression and abundance of sirtuins and other proteins involved in stress response were also studied. The cumulus-oocyte complexes (COCs) of Simmental (Bos taurus) cows underwent in vitro maturation (IVM) at different temperatures (37°C, 38.5°C and 40°C). Before maturation, the oocytes were stained with Brilliant Cresyl Blue (BCB) and categorized as labeled (BCB+) or unlabeled (BCB-). Embryo production was analyzed at the different IVM temperatures. Polar body extrusion was evaluated following IVM, and the mRNA and protein abundance of sirtuins and P53 in oocytes and cumulus cells were analyzed. The differing temperatures during IVM did not significantly alter polar body extrusion and cleavage rates; however, significant differences in blastocyst production were observed. COCs matured at 38.5°C (control) had the highest blastocyst rate, in contrast to those matured at 37°C (33.2%) and 40°C (21.5%). In all groups, the blastocyst rates were higher for BCB+ oocytes than for BCB- oocytes. In BCB+ oocytes, the expression of SIRT1, SIRT2, SIRT3, and SIRT5 genes was higher after maturation than that before maturation and in most of the cases, the expression was higher when IVM was performed at 38.5°C. In the cumulus cells of BCB+ COCs, only SIRT2 remained unaffected by the maturation temperature. In summary, the temperature change of ±1.5°C for 24 h during bovine oocyte maturation impaired in vitro embryo development. This lead to several cellular biochemical alterations in oocytes and granulosa cells from COCs with higher developmental competence (BCB+). Thus, SIRT1 is important for in vitro embryonic development and may protect against cold and heat stress. https://ojs.uel.br/revistas/uel/index.php/semagrarias/article/view/51430SirtuinsTemperatureIVPBos taurusHeat stress.
spellingShingle Ralf Pöhland
Mirela Brochado Souza-Cáceres
Tirtha Kumar Datta
Jens Vanselow
Wilian Aparecido Leite da Silva
Christopher Junior Tavares Cardoso
Fabiana de Andrade Melo Sterza
Influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of Sirtuins in cumulus oocyte complexes in cattle
Semina: Ciências Agrárias
Sirtuins
Temperature
IVP
Bos taurus
Heat stress.
title Influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of Sirtuins in cumulus oocyte complexes in cattle
title_full Influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of Sirtuins in cumulus oocyte complexes in cattle
title_fullStr Influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of Sirtuins in cumulus oocyte complexes in cattle
title_full_unstemmed Influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of Sirtuins in cumulus oocyte complexes in cattle
title_short Influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of Sirtuins in cumulus oocyte complexes in cattle
title_sort influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of sirtuins in cumulus oocyte complexes in cattle
topic Sirtuins
Temperature
IVP
Bos taurus
Heat stress.
url https://ojs.uel.br/revistas/uel/index.php/semagrarias/article/view/51430
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