Heat stress impairs gap junction communication and cumulus function of bovine oocytes

Campen, Kelly A.; Abbott, Chelsea R.; Rispoli, Louisa A.; Payton, Rebecca R.; Saxton, Arnold M.; Edwards, J. L.

doi:10.1262/jrd.2018-029

Cited by 25 publications

(16 citation statements)

References 50 publications

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“…Oocyte transcriptome analysis indicated a strong difference between heat‐tolerant and heat‐sensitive cow breeds, involving genes that are differentially expressed between breed, temperature and the breed × temperature interaction (Ticianelli et al, ). This is further supported by recent studies in bovine oocytes exposed to HS (41–42°C) during the first 6 hr of IVM that demonstrated alterations in gap junction communications between oocytes and cumulus cells, which, in turn, affected correct cytoplasmic maturation and accelerated the progression of oocyte meiosis (Campen et al, ).…”

Section: The Female Reproductive Tractsupporting

confidence: 60%

Heat stress, a serious threat to reproductive function in animals and humans

Boni

2019

Molecular Reproduction Devel

106

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Global warming represents a major stressful environmental condition that compromises the reproductive efficiency of animals and humans via a rise of body temperature above its physiological homeothermic point (heat stress [HS]). The injuries caused by HS on reproductive function involves both male and female components, fertilization mechanisms as well as the early and late stages of embryofetal development. This occurrence causes great economic damage in livestock, and, in wild animals creates selective pressure towards the advantages of better-adapted genotypes to the detriment of others. Humans undergo several types of stress, including heat, and these represent putative causes of ongoing progressive decay in procreation; an increasing number of remedies in the form of antioxidant preparations are now being proposed to counteract the effects of stress. This review aims to describe the results of the most recent studies that aimed to highlight these effects and to draw information on the mechanisms acting as the basis of this problem from a comparative analysis. K E Y W O R D S follicle, global warming, heat stress, mitochondria, oocyte, reproductive activity, spermatozoa Mol Reprod Dev. 2019;86:1307-1323.wileyonlinelibrary.com/journal/mrd

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Section: The Female Reproductive Tractsupporting

confidence: 60%

Heat stress, a serious threat to reproductive function in animals and humans

Boni

2019

Molecular Reproduction Devel

106

View full text Add to dashboard Cite

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“…Direct exposure of cumulus-oocyte complexes to a physiologically-relevant elevated temperature during the first half of in vitro maturation reduces embryo development [9–12] in a manner consistent with what has been observed after heat-induced hyperthermia occurring in vivo near the time of estrus [8, 13, 14]. Heat stress exposure during the first half of in vitro maturation heightens progesterone production and alters the transcriptome and interconnectedness of the cumulus [15–17] surrounding the maturing oocyte. Heat-induced differences in cumulus function persist despite efforts to mature cumulus-oocyte complexes under thermoneutral conditions for the remainder of maturation [16].…”

Section: Introductionmentioning

confidence: 78%

Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows

et al. 2019

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We hypothesized that heat-induced perturbations in cumulus cells surrounding the maturing oocyte may extend to the mural granulosa of the periovulatory follicle in the heat-stressed cow to subsequently the follicular fluid proteome. Lactating Holsteins were pharmacologically stimulated to have a dominant follicle that was capable of responding to a gonadotropin releasing hormone-induced luteinizing hormone surge. Following gonadotropin releasing hormone administration, cows were maintained at ~67 temperature humidity index (THI; thermoneutral conditions) or exposed to conditions simulating an acute heat stress event (71 to 86 THI; heat stress for ~12 h). Dominant follicle collection was conducted in the periovulatory period ~16 h after gonadotropin releasing hormone. Follicular fluid proteome from thermoneutral (n = 5) and hyperthermic (n = 5) cows was evaluated by quantitative tandem mass spectrometry (nano LC-MS/MS). We identified 35 differentially-abundant proteins. Functional annotation revealed numerous immune-related proteins. Subsequent efforts revealed an increase in levels of the proinflammatory mediator bradykinin in follicular fluid (P = 0.0456) but not in serum (P = 0.9319) of hyperthermic cows. Intrafollicular increases in transferrin (negative acute phase protein) in hyperthermic cows (P = 0.0181) coincided with a tendency for levels to be increased in the circulation (P = 0.0683). Nine out of 15 cytokines evaluated were detected in follicular fluid. Heat stress increased intrafollicular interleukin 6 levels (P = 0.0160). Whether hyperthermia-induced changes in the heat-stressed cow’s follicular fluid milieu reflect changes in mural granulosa, cumulus, other cell types secretions, and/or transudative changes from circulation remains unclear. Regardless of origin, heat stress/hyperthermia related changes in the follicular fluid milieu may have an impact on components important for ovulation and competence of the cumulus-oocyte complex contained within the periovulatory follicle.

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“…They also provide extracellular thermoprotectants or produce regulatory molecules that activate thermoprotective mechanisms within the oocyte ( Edwards and Hansen, 1996 ). In addition, it was demonstrated that the effectiveness of gap junction-communication between cumulus cells and oocytes was reduced after heat stress ( Campen et al., 2018 ). The disturbance of oocyte and embryo development could be due to the lack of HSP70 protection for cumulus cells at 37 °C, a stress temperature only for oocytes.…”

Section: Discussionmentioning

confidence: 99%

Influence of long-term thermal stress on the in vitro maturation on embryo development and Heat Shock Protein abundance in zebu cattle

et al. 2020

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The objective of this study was to investigate the influence of long-term temperature stress during the in vitro maturation (IVM) of oocytes on the in vitro embryo production (IVP) and the abundance of HSP70 and HSP90 in zebu cattle. Viable cumulus-oocyte complexes (COCs) were incubated for 24 h at 37 °C, 38.5 °C, or 40 °C for the low-, physiological, and high-temperature stress treatments, respectively. Thereafter, they were subjected to in vitro fertilization and culture. Temperature did not affect the polar body extrusion. However, IVP was adversely affected when IVM took place at 37 °C and 40 °C. The highest abundance of HSP70 was observed in cumulus cells after maturation of COCs at 40 °C. In contrast, HSP70 was more abundant in oocytes at both 37 °C and 40 °C; however, at 40 °C, the difference to the control group (38.5 °C) was not significant. In contrast, the highest abundance of HSP90 was observed in oocytes and cumulus cells at 37 °C. It appears that HSP70 and HSP90 respond to cold and heat stress in different ways. In conclusion, moderately high (40 °C) and low (37 °C) thermal stress for 24 h during IVM is detrimental to the developmental competence of oocyte and is accompanied by changes in the abundances of HSP70 and HSP90, especially in cumulus cells.

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Heat stress impairs gap junction communication and cumulus function of bovine oocytes

Cited by 25 publications

References 50 publications

Heat stress, a serious threat to reproductive function in animals and humans

Heat stress, a serious threat to reproductive function in animals and humans

Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows

Influence of long-term thermal stress on the in vitro maturation on embryo development and Heat Shock Protein abundance in zebu cattle

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