Maternal Heat Stress Alters Expression of Genes Associated with Nutrient Transport Activity and Metabolism in Female Placentae from Mid-Gestating Pigs

Zhao, Weicheng; Liu, Fan; Marth, C; Green, Mark P.; Le, Hoang Viet; Leury, Brian J; Bell, A. W.; Dunshea, Frank R.; Cottrell, Jeremy J.

doi:10.3390/ijms22084147

Cited by 14 publications

(11 citation statements)

References 49 publications

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“…For example, amino acid transporters and their metabolism in the endometrium are associated with the receptive state of the endometrial tissue at both day 4 and day 7 of pregnancy [51]. Previous studies have shown that maternal HS during early gestation to mid-gestation in pigs decreased the expression of genes associated with the placental amino acid, peptide, and cation transmembrane transport [52]. As a derivative of this amino acid, SLC16A1 is important for fetal and placental development, and its expression was decreased upon hyperosmotic stress [53].…”

Section: Discussionmentioning

confidence: 99%

Heat Stress Impairs Maternal Endometrial Integrity and Results in Embryo Implantation Failure by Regulating Transport-Related Gene Expression in Tongcheng Pigs

et al. 2022

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Heat stress (HS) poses a significant threat to production and survival in the global swine industry. However, the molecular regulatory effects of heat stress on maternal endometrial cells are poorly understood in pigs during early embryo implantation. In this study, we systematically examined morphological changes in the endometrium and the corresponding regulation mechanism in response to HS by combining scanning electron microscopy (SEM), hematoxylin/eosin (H&E) staining, western blot, and RNA-seq analyses. Our results showed that HS led to porcine endometrium damage and endometrial thinness during embryo implantation. The expression levels of cell adhesion-related proteins, including N-cadherin and E-cadherin, in the uterus were significantly lower in the heat stress group (39 ± 1 °C, n = 3) than in the control group (28 ± 1 °C, n = 3). A total of 338 up-regulated genes and 378 down-regulated genes were identified in porcine endometrium under HS. The down-regulated genes were found to be mainly enriched in the pathways related to the microtubule complex, immune system process, and metalloendopeptidase activity, whereas the up-regulated genes were mainly involved in calcium ion binding, the extracellular region, and molecular function regulation. S100A9 was found to be one of the most significant differentially expressed genes (DEGs) in the endometrium under HS, and this gene could promote proliferation of endometrial cells and inhibit their apoptosis. Meanwhile, HS caused endometrial epithelial cell (EEC) damage and inhibited its proliferation. Overall, our results demonstrated that HS induced uterine morphological change and tissue damage by regulating the expression of genes associated with calcium ions and amino acid transport. These findings may provide novel molecular insights into endometrial damage under HS during embryo implantation.

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Section: Discussionmentioning

confidence: 99%

Heat Stress Impairs Maternal Endometrial Integrity and Results in Embryo Implantation Failure by Regulating Transport-Related Gene Expression in Tongcheng Pigs

et al. 2022

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“…The present study has a potential limitation. As known, the previous study mainly focused on the effects of maternal HS on the placental barrier function and nutrient transport activity and metabolism ( Guo et al, 2021 ; Silva et al, 2021 ; Zhao et al, 2021 ). In the present study, the expressions of genes enriched in the placental inflammation response were altered under maternal HS conditions, implying that maternal HS might cause the inflammation response in the placenta.…”

Section: Discussionmentioning

confidence: 99%

Heat Stress Modulates a Placental Immune Response Associated With Alterations in the Development of the Fetal Intestine and Its Innate Immune System in Late Pregnant Mouse

et al. 2022

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The placenta is critical for the regulation of fetal innate immune function. Maternal heat stress (HS) impairs the immune function and the intestinal barrier in the offspring. However, the effects of maternal HS on the placental immune response and the development of the fetal intestine and its innate immune system remain unclear. Fetal mice were divided into the utero control (IUTN) and heat stress (IUHS) groups according to the maternal ambient temperature. Transcriptome analysis revealed that the expressions of placental immune response–related genes such as macrophage antigen CD68 and Fc gamma receptors 1 and 3 (fcgγ1 and fcgγ3) were increased, but the mRNA expression and protein levels of colony-stimulating factor-1 (Csf1) were decreased in the HS group compared with the TN group (p < 0.05). Furthermore, there was no significant difference in the intestinal length normalized to pup weight between the IUTN and IUHS groups. The expression of genes (such as alpi and ttr) involved in fetal duodenum and jejunum development was downregulated by maternal HS, whereas the expression of genes enriched in the cell cycle was increased. The mRNA expression and protein levels of cell division cycle 6 (Cdc6) in the fetal duodenum and jejunum were much higher in the IUHS group than in the IUTN group (p < 0.05). Maternal HS also down-regulated the expression of genes enriched in the innate immune system in the fetal duodenum and jejunum. The mRNA expression and protein levels of interleukin 1 alpha (IL1a) were reduced in the IUHS group compared with the IUTN group (p < 0.05). Taken together, these data demonstrated that maternal HS modulated the expression of genes in the placenta related to the immune response and inhibited the development of the fetal intestine and its innate immune system.

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“…Changes in fetal skeletal muscle characteristics are likely underpinned by placental insufficiency [31]. We have previously demonstrated that placentae from the female fetuses exhibited a sexspecific reduction in placental efficiency (fetal/placental weight) in response to maternal HS at mid-gestation, and the placental insufficiency of those female placentae was associated with impaired nutrient transport capacity [15,17]. The current data therefore reinforce and extend our previous findings by demonstrating that HS-induced placental insufficiency can be associated with altered skeletal muscle molecular responses in the fetus.…”

Section: Discussionmentioning

confidence: 99%

“…The sequencing data processing followed the pipeline as previously described [17]. The quality of sequencing reads was verified using FastQC software version 0.11.9 [18].…”

Section: Sequencing Data Processingmentioning

confidence: 99%

Gestational heat stress alters skeletal muscle gene expression profiles and vascularity in fetal pigs in a sexually dimorphic manner

Zhao

Green

Marth

et al. 2022

J Animal Sci Biotechnol

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Background There is evidence that sow heat stress (HS) during gestation affects fetal development with implications for impaired muscle growth. We have previously demonstrated that maternal HS during early to mid-gestation compromised muscle fibre hyperplasia in developing fetal pigs. Thus, we hypothesised these phenotypic changes are associated with a change in expression of genes regulating fetal skeletal muscle development and metabolism. To test this, at d 60 of gestation, RNA sequencing and immunohistochemistry were performed on fetal longissimus dorsi (LD) muscle biopsies collected from pregnant gilts that had experienced either thermoneutral control (CON, 20 °C, n = 7 gilts, 18 LD samples) or controlled HS (cyclic 28 to 33 °C, n = 8 gilts, 23 LD samples) conditions for 3 weeks. Results A total of 282 genes were differentially expressed between the HS and CON groups in female LD muscles (false discovery rate (FDR) ≤ 0.05), whereas no differentially expressed genes were detected in male LD muscles between the two groups (FDR > 0.05). Gestational HS increased the expression of genes associated with transcription corepressor activity, adipogenesis cascades, negative regulation of angiogenesis and pro-inflammatory signalling in female LD muscles. Immunohistochemical analyses revealed a decreased muscle vascularity density in fetuses from HS group for both sexes compared to those from the CON group (P = 0.004). Conclusions These results reveal gilt HS during early to mid-gestation altered gene expression profiles in fetal LD muscles in a sexually dimorphic manner. The molecular responses, including transcription and angiogenesis repressions and enhanced adipogenesis cascades, were exclusively observed in females. However, the associated reductions in muscle vascularity were observed independently of sexes. Collectively this may indicate female fetal pigs are more adaptive to gestational HS in terms of gene expression changes, and/or there may be sexually dimorphic differences with respect to the timing of muscle molecular responses to gestational HS.

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Maternal Heat Stress Alters Expression of Genes Associated with Nutrient Transport Activity and Metabolism in Female Placentae from Mid-Gestating Pigs

Cited by 14 publications

References 49 publications

Heat Stress Impairs Maternal Endometrial Integrity and Results in Embryo Implantation Failure by Regulating Transport-Related Gene Expression in Tongcheng Pigs

Heat Stress Impairs Maternal Endometrial Integrity and Results in Embryo Implantation Failure by Regulating Transport-Related Gene Expression in Tongcheng Pigs

Heat Stress Modulates a Placental Immune Response Associated With Alterations in the Development of the Fetal Intestine and Its Innate Immune System in Late Pregnant Mouse

Gestational heat stress alters skeletal muscle gene expression profiles and vascularity in fetal pigs in a sexually dimorphic manner

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