Oxidative and endoplasmic reticulum stress defense mechanisms of bovine granulosa cells exposed to heat stress

Alemu, Teshome Wondie; Pandey, Hari Om; Salilew‐Wondim, Dessie; Gebremedhn, Samuel; Neuhof, Christiane; Tholen, Ernst; Hölker, Michael; Schellander, K.; Tesfaye, Dawit

doi:10.1016/j.theriogenology.2017.12.042

Cited by 86 publications

(86 citation statements)

References 74 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Our study showed that exposure to 41°C significantly inhibited the IPEC‐J2 cell proliferation, especially S‐phase cells, which was supported by a decrease in the percentage of EdU + cells and the expression of proliferation marker gene PCNA. This result is consistent with previous studies, that is, high temperature (≥41°C) induces cell damage (Alemu et al, 2018; Gao et al, 2015; Homma & Fujii, 2016; Varasteh et al, 2018; Yang, He, & Zheng, 2007). Of note, a proper increase of temperatures, such as 39°C or 40°C, can improve the viability of porcine intestinal epithelial cells, which might be related to the relatively high resting physiologic body temperature of pigs.…”

Section: Discussionsupporting

confidence: 93%

“…However, this dynamic balance is disturbed by exposure to high ambient temperature, which results in small intestinal villi atrophy (Varasteh, Fink-Gremmels, Garssen, & Braber, 2018). Our study showed that exposure to 41°C significantly inhibited with previous studies, that is, high temperature (≥41°C) induces cell damage (Alemu et al, 2018;Gao et al, 2015;Homma & Fujii, 2016;Varasteh et al, 2018;Yang, He, & Zheng, 2007). Of note, a proper increase of temperatures, such as 39°C or 40°C, can improve the viability of porcine intestinal epithelial cells, which might be related to the relatively high resting physiologic body temperature of pigs.…”

Section: Discussionsupporting

confidence: 42%

“…Accumulating evidence indicates that intestinal epithelial cells respond to heat stress (HS) in several ways to increases their survival, such as expression of heat shock protein 70 (HSP70) which participates in the folding and assembly of nascent or stress denatured proteins as a molecular chaperone (Daugaard, Rohde, & Jaattela, 2007; Piri, Kwong, Gu, & Caprioli, 2016; Xu et al, 2017). Interestingly, Alemu et al (2018) found that heat exposure (41°C) triggered endoplasmic reticulum stress (ERS) accompanied by the accumulation of glucose‐regulated protein 78 (GRP78), a member of Hsp70 subfamily. Besides that, ERS blocks the Wnt/β‐catenin pathway by inducing the dissociation between GRP78 and Wnt (Verras, Papandreou, Lim, & Denko, 2008).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Wnt/β‐catenin‐mediated heat exposure inhibits intestinal epithelial cell proliferation and stem cell expansion through endoplasmic reticulum stress

Zhou

Huang

Zhu

et al. 2020

Journal Cellular Physiology

View full text Add to dashboard Cite

Heat stress induced by continuous high ambient temperatures or strenuous exercise in humans and animals leads to intestinal epithelial damage through the induction of intracellular stress response. However, the precise mechanisms involved in the regulation of intestinal epithelial cell injury, especially intestinal stem cells (ISCs), remain unclear. Thereby, in vitro a confluent monolayer of IPEC‐J2 cells was exposed to the high temperatures (39, 40, and 41°C), the IPEC‐J2 cell proliferation, apoptosis, differentiation, and barrier were determined, as well as the expression of GRP78, which is a marker protein of endoplasmic reticulum stress (ERS). The Wnt/β‐catenin pathway‐mediated regenerative response was validated using R‐spondin 1 (Rspo1). And ex‐vivo, three‐dimensional cultured enteroids were developed from piglet jejunal crypt and employed to assess the ISC activity under heat exposure. The results showed that exposure to 41°C for 72 hr, rather than 39°C and 40°C, decreased IPEC‐J2 cell viability, inhibited cell proliferation and differentiation, induced ERS and cell apoptosis, damaged barrier function and restricted the Wnt/β‐catenin pathway. Nevertheless, Wnt/β‐catenin reactivation via Rspo1 protects the intestinal epithelium from heat exposure‐induced injury. Furthermore, exposure to 41°C for 24 hr reduced ISC activity, stimulated crypt‐cell apoptosis, upregulated the expression of GRP78 and caspase‐3, and downregulated the expression of β‐catenin, Lgr5, Bmi1, Ki67, KRT20, ZO‐1, occludin, and claudin‐1. Taken together, we conclude that heat exposure induces ERS and downregulates the Wnt/β‐catenin signaling pathway to disrupt epithelial integrity by inhibiting the intestinal epithelial cell proliferation and stem cell expansion.

show abstract

Section: Discussionsupporting

confidence: 93%

Section: Discussionsupporting

confidence: 42%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Wnt/β‐catenin‐mediated heat exposure inhibits intestinal epithelial cell proliferation and stem cell expansion through endoplasmic reticulum stress

Zhou

Huang

Zhu

et al. 2020

Journal Cellular Physiology

View full text Add to dashboard Cite

show abstract

“…In addition, the high expression of HMOX1 gene was observed in the culture of human melanoma cells, confirming the induction of cellular oxidative stress during harmful insults [56]. Similar to our results, the activation of forkhead box O3 (FoxO3) and kelch-like ECH associated protein 1 (KEAP1) under heat stress protects cells from oxidative stress by upregulating antioxidant enzymes superoxide dismutase 2 (SOD2) and catalase (CAT) [57][58][59]. In Saccharomyces cerevisiae and quail, genes from the glutathione peroxidase family were also shown to be induced under heat stress [60,61].…”

Section: Discussionsupporting

confidence: 87%

Evaluation of heat stress effects on cellular and transcriptional adaptation of bovine granulosa cells

Khan

Dou

Wang

et al. 2020

J Animal Sci Biotechnol

View full text Add to dashboard Cite

Background: Heat stress is known to affect follicular dynamics, oocyte maturation, and fertilization by impairing steroidogenic ability and viability of bovine granulosa cell (bGCs). The present study explored the physiological and molecular response of bGCs to different heat stress intensities in-vitro. We exposed the primary bGCs to heat stress (HS) at 39°C, 40°C and 41°C along with control samples (38°C) for 2 h. To evaluate the impact of heat stress on bGCs, several in vitro cellular parameters including cell apoptosis, intracellular reactive oxygen species (ROS) accumulation and HSP70 kinetics were assessed by flow cytometry, florescence microscopy and western blot, respectively. Furthermore, the ELISA was performed to confirm the 17β-estradiol (E 2 ) and progesterone (P 4 ) levels. In addition, the RNA sequencing (RNA-Seq) method was used to get the molecular based response of bGCs to different heat treatments. Results: Our findings revealed that the HS significantly decreased the cell viability, E 2 and P 4 levels in bGCs, whereas, increased the cellular apoptosis and ROS. Moreover, the RNA-Seq experiments showed that all the treatments (39°C, 40°C and 41°C) significantly regulated many differentially expressed genes (DEGs) i.e. BCL2L1, STAR, CYP11A1, CASP3, SOD2, HSPA13, and MAPK8IP1 and pathways associated with heat stress, apoptosis, steroidogenesis, and oxidative stress. Conclusively, our data demonstrated that the impact of 40°C treatment was comparatively detrimental for cell viability, apoptosis and ROS accumulation. Notably, a similar trend of gene expression was reported by RT-qPCR for RNA-seq data. Conclusions:Our study presented a worthy strategy for the first time to characterize the cellular and transcriptomic adaptation of bGCs to heat stress (39, 40 and 41°C) in-vitro. The results infer that these genes and pathways reported in present study could be useful candidates/indicators for heat stress research in dairy cattle. Moreover, the established model of bGCs to heat stress in the current study provides an appropriate platform to understand the mechanism of how heat-stressed bGCs can affect the quality of oocytes and developing embryo.

show abstract

“…Notably, P4hα1 had the largest fold change among all 26 DEGs, with an average fold change of 11.44 in the three tissues ( Figure 4C and Table S6); furthermore, it was DEG of the highest fold change in blood ( Figure 4D). Heat stress can induce endoplasmic reticulum (ER) stress in various mammalian cells through disturbing the homeostasis and, consequently, accumulating unfolded or misfolded proteins [69]. It has been shown that P4hα1 was upregulated during ER stress [70], indicating that HS triggered ER stress in our research.…”

Section: Discussionmentioning

confidence: 55%

Heat Stress Impairs the Physiological Responses and Regulates Genes Coding for Extracellular Exosomal Proteins in Rat

Dou

Khan

et al. 2020

Genes

View full text Add to dashboard Cite

Heat stress (HS) is challenging in humans and animals as it is a complicated regulatory mechanism. This prompted us to characterize the physiological and molecular responses of a HS-animal model. In this study, a rat model system was developed by using three temperature treatments (40°C, 42°C, and 43°C) and sixteen biochemical indicators in blood at 42°C for 30 min (H30), 60 min (H60), and 120 min (H120). In addition, transcriptomic profiling was carried out in H120-rats' blood, liver, and adrenal gland samples for detection of the genes of interest. Our findings demonstrated that the adrenocorticotropic hormone, catalase, prolactin, growth hormone, and lactic acid have significant spatiotemporal variation in the H120-rats as compared with the control. Furthermore, through transcriptomic screening, we documented a high ratio of differentially expressed genes (DEGs) in adrenal glands, liver, and blood, respectively. Among them, Nup153, Plxnb2, Stx7, Hspa9, Chordc1, Pde4d, Gm2α, and Rnf125 were associated with the regulation of HS and immune response processes. Notably, 36 and 314 of DEGs in blood and adrenal glands were detected in the composition of the extracellular exosome, respectively. Furthermore, the correlation analysis between gene transcripts and biochemical indicator levels identified the Lgals3, S1006, Fn1, F2, and Kng1l1 as key candidate genes for HS encoding extracellular exosomal proteins. On the basis of our results, it was concluded that the current rat model provides a molecular basis for future research in HS resistance in humans and livestock.Genes 2020, 11, 306 2 of 23 (e.g., crossbreeding), have not achieved long-lasting, cumulative and significant effects [9]. Thus, further molecular mechanisms and physiological consequences of HS using an animal model are highly recommended.Previous studies have shown HS-induced physiological and biochemical variations in many animals, such as rats [10,11], cows [12], and chickens [13]. The HS causes an imbalance of glucocorticoids, the adrenocorticotropic hormone, the growth hormone, and the norepinephrine hormone, resulting in detrimental metabolic changes [10,14,15]. Furthermore, a set of proteins involved in the antioxidant stress response and inflammatory response, including catalase, glutathione peroxidase, and C-reactive protein were affected by HS [16][17][18][19]. Recently, microarray and next-generation sequencing studies have displayed widespread changes in gene expression in response to HS, the exploration of useful indicators to predict and prevent HS in animals has yet to be defined.In the context of the critical effects of HS on human and animal health, the current study was designed to explore the physiological, biochemical, and transcriptomic responses to HS in Sprague Dawley (SD) rats. The current research targets the key biomarkers that are sensitive to HS. In addition, the altered expression of genes related to HS response was detected by performing transcriptomic screening in blood, liver, and adrenal gland tissues post HS. Collectively...

show abstract

Oxidative and endoplasmic reticulum stress defense mechanisms of bovine granulosa cells exposed to heat stress

Cited by 86 publications

References 74 publications

Wnt/β‐catenin‐mediated heat exposure inhibits intestinal epithelial cell proliferation and stem cell expansion through endoplasmic reticulum stress

Wnt/β‐catenin‐mediated heat exposure inhibits intestinal epithelial cell proliferation and stem cell expansion through endoplasmic reticulum stress

Evaluation of heat stress effects on cellular and transcriptional adaptation of bovine granulosa cells

Heat Stress Impairs the Physiological Responses and Regulates Genes Coding for Extracellular Exosomal Proteins in Rat

Contact Info

Product

Resources

About