Heat stress on oocyte or zygote compromises embryo development, impairs interferon tau production and increases reactive oxygen species and oxidative stress in bovine embryos produced in vitro

Amaral, Carolina dos Santos; Koch, Juliane; Júnior, Eduardo E. Correa; Bertolin, Kalyne; Mujica, Lady Katerine Serrano; Fiorenza, M. F.; Rosa, Suzan Gonçalves; Nogueira, Cristina Wayne; Comim, Fábio Vasconcellos; Portela, Valério V.M.; Gonçalves, Paulo Bayard Dias; Antoniazzi, Alfredo Q.

doi:10.1002/mrd.23407

Cited by 13 publications

(8 citation statements)

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“…An overexpression of SOD2 [43], but not of CAT, has been associated with higher embryo quality [44]. In fact, SOD2 expression was downregulated in vitrified-thawed blastocysts [45] or blastocysts derived from heat-shock oocytes, which were cultured at 41 • C during IVM [22]. Recent studies revealed that an increase in SOD2 expression, as shown in the present study, can be attributed to an effect of α-tocopherol on the expression of antioxidant genes [46].…”

Section: Discussionsupporting

confidence: 60%

“…Supplementation of IVM medium with α-tocopherol reduced apoptotic rate in rabbit [20] and porcine [21] cumulus cells and improved oocyte developmental competence. However, the expression of genes involved in the processes of heat and oxidative stress response (SOD2, CAT and HSPA1A), pro-and anti-apoptotic activity (BAX and BCL2), and maternal recognition of pregnancy (IFNT2) has not been described in α-tocopherol-treated embryos, and its evaluation can provide insights into its mechanism of action [22].…”

Section: Introductionmentioning

confidence: 99%

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Effect of Ethanol on Parthenogenetic Activation and α-Tocopherol Supplementation during In Vitro Maturation on Developmental Competence of Summer-Collected Bovine Oocytes

Báez

Gómez

Brun

et al. 2021

CIMB

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The use of α-tocopherol during in vitro maturation (IVM) is an alternative to minimize the adverse effects of heat stress on oocyte competence. However, α-tocopherol is diluted in ethanol, which can induce oocyte parthenogenetic activation (PA). This study aimed to evaluate the role of ethanol concentration on PA and the effect of α-tocopherol supplementation during IVM on the developmental competence and the expression of key genes in blastocysts derived from summer-collected oocytes. All in vitro embryo production was conducted at 5% O2, 5% CO2 at 38.5 °C. Experiment 1: oocytes were cultured with or without 0.05% ethanol. As positive PA control matured oocytes were subjected to 3% or 7% ethanol for 7 min. Oocytes from all groups were placed in fertilization medium (22 h) and culture medium (9 days). Ethanol at 0.05% during IVM did not induce oocyte PA, however, 3% and 7% ethanol were effective parthenogenetic inductors. Experiment 2: oocytes were cultured in maturation medium supplemented with 0, 50, 100 and 200 μM α-tocopherol, diluted in 0.05% ethanol. After in vitro fertilization and embryo culture, we assessed blastocyst apoptotic index and the transcription of a panel of genes. The results showed that supplementation with 100 μM α-tocopherol reduced apoptotic index and increased the expression of SOD2. In conclusion, 100 μM α-tocopherol, diluted in 0.05% ethanol, can be used during IVM to embryonic quality.

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Section: Discussionsupporting

confidence: 60%

Section: Introductionmentioning

confidence: 99%

Effect of Ethanol on Parthenogenetic Activation and α-Tocopherol Supplementation during In Vitro Maturation on Developmental Competence of Summer-Collected Bovine Oocytes

Báez

Gómez

Brun

et al. 2021

CIMB

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“…Heat stress increased intracellular reactive oxygen species (ROS) in bovine embryos and affected the development of early embryo 44 . On GD-7, heat stressed in vitro bovine embryos had increased reactive oxygen species and decreased IFNT expression in comparison to the control 45 . Yoon et al (2013) demonstrated that excessive reactive oxygen species (ROS) reduced the embryo development rate and increased the number of apoptotic cells in embryos cultured in vitro 46 .…”

Section: Discussionmentioning

confidence: 86%

Impact of heat stress on embryonic development during first 16 days of gestation in dairy cows

Kasimanickam

2021

Sci Rep

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Objective was to elucidate the effects of heat stress (HS) on embryo development during first 16 gestational days (GD) and circulating hormone concentrations on GD-16 in lactating Holstein cows. Cows in HS and control (CON) groups were exposed to temperature humidity index (THI) of ≥ 73 and < 73, respectively, for 3 weeks before the experiment. GD-7 (67 vs 49%) and GD-16 (52 vs. 31%) conception rates following single insemination were greater (P < 0.01) for CON compared with HS cows. Control cows produced more GD-7 transferrable embryos following superovulation compared with HS cows (84.8 vs 53.1%; P < 0.001). Mean (± SEM) length (45.2 ± 10.6 vs. 59.2 ± 9.1 mm) and weight (31.4 ± 4.3 vs. 42.4 ± 6.2 mg) of GD-16 conceptus were greater for CON compared with HS cows (P < 0.05). Control cows yielded more filamentous conceptus (≥ 25 mm) compared with HS cows (71 vs 45%; P < 0.05). Progesterone (2.09-fold) was higher, and cortisol (1.86-fold), prolactin (1.60-fold), substance-P (1.55-fold), Isoprostane-8 (1.34-fold) and prostaglandin F metabolites (1.97-fold) were lower in CON compared with HS cows (P < 0.05). Progesterone positively, and substance-P, isoprostane-8 and the THI negatively were associated with GD-16 conceptus length (P < 0.05). In conclusion, altered hormones concentrations in heat-stressed cows plausibly resulted in lower GD-7 and GD-16 conception rates, fewer GD-7 transferable embryos, and stunted GD-16 conceptus elongation.

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“…The environmental conditions seem to affect the maternal recognition of pregnancy signaling. Previous in vitro study from our group, demonstrated the influence of heat stress on oxidative stress and IFNT production [ 44 ]. Heat stressed pregnant cows did not have the same increased expression of interferon stimulated and IFN I pathway genes on Day 18 as it was found in cows in comfort temperature.…”

Section: Discussionmentioning

confidence: 99%

“…This response makes it difficult to accurately use expression of these ISGs to identify early pregnancy. In addition to the effects of HS on IFNT signaling [ 44 ], IFNT has been shown to modulate local and systemic innate immune response, carried out mainly by neutrophils [ 43 , 63 ]. Neutrophils are essential for innate immunity and resistance to pathogens, not only acting as a final effector of an acute inflammatory response, but also secreting factors such as cytokines to activate cells of innate and adaptative immune response.…”

Section: Discussionmentioning

confidence: 99%

Heat stress modulates polymorphonuclear cell response in early pregnancy cows: I. interferon pathway and oxidative stress

et al. 2021

Self Cite

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One of the major causes of early pregnancy loss is heat stress. In ruminants, interferon tau (IFNT) is the embryo signal to the mother. Once the interferon signaling pathway is activated, it drives gene expression for interferon-stimulated genes (ISGs) and alters neutrophils responses. The aim of the present study was to evaluate interferon (IFN) pathway, ISGs and gene expression in polymorphonuclear leukocytes (PMN) and oxidative stress in dairy cows under heat stress. Pregnant cows had their estrous cycle synchronized and randomly assigned to a comfort or heat stress group. Blood samples were collected at artificial insemination (AI) and on Days 10, 14 and 18 following AI. Pregnant cows were pregnancy checked by ultrasound on Day 30 and confirmed on Day 60 post-AI. Results are presented as mean ± SEM. The corpus luteum (CL) diameter was not different between groups of pregnant cows; concentration of progesterone of pregnant cows on Day 18 following AI was greater in comfort group compared to heat stressed group. Comfort pregnant cows had higher expression of all analyzed genes from interferon pathway, except for IFNAR1, on both Days 14 and 18. Conversely, heat stressed cows did not show altered expression of IFNT pathway genes and ISGs between Days 10, 14, and 18 after AI. The oxidative stress, determined as malondialdehyde (MDA) levels, was greater in heat stress group on Days 10, 14 and 18, independent of pregnancy status. Heat stress negatively influences expression of ISGs, IFN pathway gene expression in neutrophils, and oxidative stress. Our data suggest that lower conception rates in cows under heat stress are multifactorial, with the association of interferon pathway activation and the unbalanced oxidative stress being main contributing factors.

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Heat stress on oocyte or zygote compromises embryo development, impairs interferon tau production and increases reactive oxygen species and oxidative stress in bovine embryos produced in vitro

Cited by 13 publications

References 54 publications

Effect of Ethanol on Parthenogenetic Activation and α-Tocopherol Supplementation during In Vitro Maturation on Developmental Competence of Summer-Collected Bovine Oocytes

Effect of Ethanol on Parthenogenetic Activation and α-Tocopherol Supplementation during In Vitro Maturation on Developmental Competence of Summer-Collected Bovine Oocytes

Impact of heat stress on embryonic development during first 16 days of gestation in dairy cows

Heat stress modulates polymorphonuclear cell response in early pregnancy cows: I. interferon pathway and oxidative stress

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