Effect of dietary resveratrol on placental function and reproductive performance of late pregnancy sows

Abstract

Placental function is vital to the fetal growth of sows, and resveratrol (RES) can protect cells against oxidative stress, which is one of the major factors impairing placental function. This study aimed to investigate the effect of dietary resveratrol (RES) on placental function and reproductive performance during late pregnancy in a sow model from the aspects of oxidative stress, insulin resistance, and gut microbiota. A total of 26 hybrid pregnant sows (Landrace × Yorkshire) with similar parity were randomly allocated into two groups (n = 13) and fed with a basal diet or a diet containing 200 mg/kg of resveratrol from day 85 of gestation until parturition. The dietary supplementation of RES increased the litter weight at parturition by 12.53% (p = 0.145), with ameliorated insulin resistance (HOMA-IR), increased triglyceride (TG) levels, and decreased interleukin (IL)-1β and IL-6 levels in serum (p < 0.05). Moreover, resveratrol increased the placental vascular density (p < 0.05) with the enhanced expression of nutrient transporter genes (SLC2A1 and SLC2A3) and antioxidant genes, such as superoxide dismutase 2 (SOD2) and heme oxygenase-1 (HO-1) but declined the expression of inflammatory genes, such as IL-1β and IL-6 (p < 0.05). The characterization of the fecal microbiota revealed that resveratrol decreased the relative abundance of the Christensensllaceae R-7 group and Ruminococcaceae UCG-008 (p < 0.05), which had a positive linear correlation with the expression of IL-1β and IL-6 (p < 0.05), but had a negative linear correlation with the expression of SOD2, HO-1, SLC2A1, and SCL2A3 genes (p < 0.05). These data demonstrated that dietary supplementation with resveratrol can improve placental function with ameliorated insulin resistance, oxidative stress, and inflammation potentially by regulating Ruminococcaceae UCG-008 and the Christensensllaceae R-7 group in sows.

Keywords: gut microbiota; placental function; reproductive performance; resveratrol; sow.

Figure 1

The effect of RES on glucose metabolism and lipid metabolism in perinatal sows. (A) Glu, (B) insulin, (C) HOMA-IR and HOMA-IS, (D) TC and TG, and (E) HDL-C and LDL-C. Glu, glucose; HOMA-IR, homeostasis model assessment-insulin resistance; HOMA-IS, homeostasis model assessment-insulin sensitivity; TC, total cholesterol; TG, triglycerides; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; CTL, a basal diet; and RES, a basal diet containing 200 mg/kg resveratrol. Data are expressed as mean ± SD (n = 10); *, p < 0.05; and **, p < 0.01.

Figure 2

Effects of RES on blood inflammatory markers. Serum levels of (A) IL-1β, (B) IL-6, and (C) MCP-1 were measured by using ELISA kits. CTL, a basal diet; and RES, a basal diet containing 200 mg/kg resveratrol. Data are expressed as mean ± SD (n = 10); *, p < 0.05.

Figure 3

The effect of resveratrol on serum hormone levels in perinatal sows. (A) Follicle-stimulating hormone (FSH), (B) prolactin, and (C) progesterone. CTL, a basal diet; and RES, a basal diet containing 200 mg/kg resveratrol. Data are expressed as mean ± SD (n = 10); *, p < 0.05.

Figure 4

The effect of RES on vessel density, nutrient transport, antioxidant, and inflammation mRNA expression in the placental. (A,B) The hematoxylin and eosin method was used to examine blood vessel density in placental tissues, and the black arrows indicate placental blood vessels (bar = 100 μm, n = 12); (C) CD31 mRNA expression; (D) Nutrient transporters SLC2A1, SCL2A3, and SLC7A1 genes expression; (E) Inflammatory factors IL-1β, IL-6, MCP1, and TNF-α genes expression; (F) Antioxidant genes SOD1, SOD2, SOD3, GPX4, and HO-1 expression. CTL, a basal diet; and RES, a basal diet containing 200 mg/kg resveratrol. Data are expressed as mean ± SD (n = 8); *, p < 0.05; and **, p < 0.01.

Figure 5

Modulation of the gut microbiota by RES. The effect of RES on genus-based (n = 6) principal component analysis (PCA) (A), the Chao 1 index (B), the Shannon index (C), the effect of RES on the relative abundance of main microbes at the phylum level (D) and the genera Christensenellaceae R-7 group (E), and Ruminococcaceae UCG-005 (F). CTL, a basal diet; and RES, a basal diet containing 200 mg/kg resveratrol. Data are expressed as mean ± SD (n = 6); and *, p < 0.05.

Figure 6

The correlation analysis of the gut microbiota and placental gene expression. The correlation analysis between the abundance of the top 50 microbial genera and placental gene expression by Spearman's correlation analysis (A), linear regression analyses between genera and placental mRNA expression of inflammatory cytokines (B), mRNA expression of antioxidative genes (C), and expression of genes involved in the regulation of nutrient transport in placenta (D). *, p < 0.05; and **, p < 0.01.