Cellular and epigenetic changes induced by heat stress in bovine preimplantation embryos

Mammalian preimplantation embryos are sensitive to maternal and direct heat stress. However, the mechanisms by which heat stress affects early embryonic development in vivo or in vitro are unknown. This study examined whether heat-stress-induced loss of developmental competence in mouse embryos was mediated by physiological changes in the maternal environment or by high temperatures alone. After fertilization, zygotes at the same stage were heat-stressed at 39.5 degrees C for 12 h either maternally (measured by maternal rectal temperature) or directly in culture. Zygotes in each group were cultured at 37.5 degrees C for a further 84 h to assess their developmental ability. Neither type of heat stress affected the first cleavage rate. However, the proportion of embryos that developed to morulae or blastocysts was significantly lower in the maternally heat-stressed group, but not in the directly heat-stressed group. Moreover, maternal heat stress significantly reduced intracellular glutathione concentrations and enhanced hydrogen peroxide concentrations in both zygotes and two-cell embryos that were recovered immediately after heat stress or 12 h later, respectively. In contrast, direct heat stress had little effect on concentrations of glutathione or hydrogen peroxide in cultured early embryos. These results demonstrate that maternal heat stress at the zygote stage reduces the developmental ability of mouse embryos via physiological changes in the maternal environment that lead to an increase in intracellular oxidative stress on the embryo.

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Early-life epigenetic changes along the corticotropin-releasing hormone (CRH) gene influence resilience or vulnerability to heat stress later in life

Molecular Psychiatry ◽

10.1038/s41380-018-0280-5 ◽

2018 ◽

Vol 24 (7) ◽

pp. 1013-1026 ◽

Cited By ~ 9

Author(s):

Tomer Cramer ◽

Tali Rosenberg ◽

Tatiana Kisliouk ◽

Noam Meiri

Keyword(s):

Heat Stress ◽

Early Life ◽

Epigenetic Changes ◽

Corticotropin Releasing Hormone ◽

Releasing Hormone

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Effects of heat stress on bovine preimplantation embryos produced in vitro

Journal of Reproduction and Development ◽

10.1262/jrd.2017-045 ◽

2017 ◽

Vol 63 (4) ◽

pp. 347-352 ◽

Cited By ~ 14

Author(s):

Miki SAKATANI

Keyword(s):

Heat Stress ◽

Preimplantation Embryos

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The effect of hyperthermia in vitro on vitality of rabbit preimplantation embryos

Physiological Research ◽

10.33549/physiolres.931105 ◽

2007 ◽

pp. 789-796

Author(s):

AV Makarevich ◽

L Olexiková ◽

P Chrenek ◽

E Kubovičová ◽

K Fréharová ◽

...

Keyword(s):

Heat Stress ◽

Elevated Temperatures ◽

De Novo ◽

Cell Number ◽

Total Cell ◽

Preimplantation Embryos ◽

Short Exposure ◽

Total Cell Number ◽

Standard Temperature

The aim of our study was to test the influence of short exposure (6 h) of preimplantation rabbit embryos to elevated temperatures (41.5 degrees C or 42.5 degrees C) in vitro on their developmental capacity. Fertilized eggs recovered from female oviducts at the pronuclear stage (19 hpc) were cultured at standard temperature (37.5 degrees C) until the morula stage (72 hpc). Afterwards, the embryos were divided into two groups, cultured for 6 h either at hyperthermic (41.5 degrees C or 42.5 degrees C) or standard temperature (control 37.5 degrees C), post-incubated overnight (16-20 h) at 37.5 degrees C and then evaluated for developmental stages, apoptosis (TUNEL), proliferation (cell number), actin cytoskeleton and presence of heat-shock proteins Hsp70. It was observed that hyperthermia at 41.5 degrees C did not alter progression of embryos to higher preimplantation stages (expanded and hatching/hatched blastocysts), rate of apoptosis, total cell number of blastocysts and structure of actin filament compared to 37.5 degrees C. Western-blotting revealed the presence of heat stress-induced 72 kDa fraction of Hsp70 proteins in granulosa cells (exposed to 41 degrees C) and embryos (exposed to 41.5 degrees C). Following the elevation of temperature to 42.5 degrees C embryo development was dramatically compromised. The embryos were arrested at the morula or early blastocyst stage, showed an increased rate of apoptosis and decreased total cell number compared to control. The structure of actin filaments in most of blastomeres was damaged and such blastomeres often contained apoptotic nuclei. In this group a presence of heat-stress-induced fraction of Hsp70 proteins had not been confirmed. This is the first report demonstrating a threshold of thermotolerance of rabbit preimplantation embryos to hyperthermic exposure in vitro. A detrimental effect of higher temperature on the embryo is probably associated with the loss of their ability to produce Hsp70 de novo, which leads to cytoskeleton alterations and enhanced apoptosis.

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Epigenetic changes in preimplantation embryos subjected to laser manipulation.

Lasers in Medical Science ◽

10.1007/s10103-017-2334-3 ◽

2017 ◽

Vol 32 (9) ◽

pp. 2081-2087 ◽

Cited By ~ 3

Author(s):

Sachin D. Honguntikar ◽

Sujith Raj Salian ◽

Fiona D’Souza ◽

Shubhashree Uppangala ◽

Guruprasad Kalthur ◽

...

Keyword(s):

Preimplantation Embryos ◽

Epigenetic Changes ◽

Laser Manipulation

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Effects of paternal heat stress on the in vivo development of preimplantation embryos in the mouse

Reproduction Nutrition Development ◽

10.1051/rnd:2004064 ◽

2004 ◽

Vol 44 (6) ◽

pp. 617-629 ◽

Cited By ~ 33

Author(s):

Bi-ke Zhu ◽

Brain P. Setchell

Keyword(s):

Heat Stress ◽

Preimplantation Embryos

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Effect of paternal heat stress on the development in vitro of preimplantation embryos in the mouse

Andrologia ◽

10.1111/j.1439-0272.2004.00635.x ◽

2004 ◽

Vol 36 (6) ◽

pp. 384-394 ◽

Cited By ~ 38

Author(s):

B. Zhu ◽

S. K. Walker ◽

H. Oakey ◽

B. P. Setchell ◽

S. Maddocks

Keyword(s):

Heat Stress ◽

Preimplantation Embryos ◽

Development In Vitro

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137 Randel Lecture: Genetic control of thermotolerance in cattle at the whole-animal and cellular level

Journal of Animal Science ◽

10.1093/jas/skz397.086 ◽

2020 ◽

Vol 98 (Supplement_2) ◽

pp. 37-38

Author(s):

Peter J Hansen

Keyword(s):

Genetic Variation ◽

Heat Stress ◽

Heat Shock ◽

Body Temperature ◽

Rectal Temperature ◽

Receptor Gene ◽

Prolactin Receptor ◽

Subsequent Development ◽

Preimplantation Embryos ◽

Receptor Protein

Abstract Research by Randel and others has revealed the extensive genetic diversity in thermotolerance existing in cattle. Genetic differences in resistance to heat stress involve genes that affect body temperature regulation and that stabilize cellular function during hyperthermia. There are large differences between breeds in ability to regulate body temperature during heat stress. There is also genetic variation in thermoregulatory ability within breeds that arose in cold climates – the estimate of heritability of rectal temperature during heat stress in Holsteins is 0.17. Efforts are underway to identify genes conferring increased thermoregulatory ability in thermotolerant breeds and transfer these to thermosensitive breeds. One such gene is the prolactin receptor gene (PRLR). Several mutations in PRLR exist in criollo-type B. taurus that result in formation of a truncated receptor protein. Cattle with this mutation, which is dominant, have a short sleek hair coat and are referred to as “slick”. The slick mutation has been introduced into Holsteins by crossbreeding with Senepol cattle and in Red Angus by gene editing. Slick Holsteins are less affected by heat stress than wild-type Holsteins with respect to rectal temperature, milk yield and reproduction. Genetic variation also exists in cellular responses to elevated temperature (i.e., heat shock). Exposure of preimplantation embryos to heat shock, for example, causes a greater reduction in subsequent development of Angus, Holstein, Angus x Holstein or Jersey embryos than embryos from Brahman or Nelore (B. indicus) or Romosinuano (criollo). One gene with alleles affecting cellular resistance is the heat shock protein 70 gene HSPA1A. A mutation in the promoter region of HSPA1Ais associated with increased transcription of the encoded protein and enhanced survival of lymphocytes exposed to heat shock. Identification of other genes conferring thermotolerance will result in the increased ability to produce thermotolerant lines of cattle via genetic selection or gene transfer.

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