Different Effects of Maternal Low-Isoflavone Soy Protein and Genistein Consumption on Hepatic Lipid Metabolism of 21-Day-Old Male Rat Offspring

Abstract

Amino acid composition and isoflavone are alleged contributors to the beneficial effects of soy protein isolate (SPI) on lipid metabolism. Therefore, we investigated the contributing component(s) of SPI in a maternal diet to the regulation of lipid metabolism in offspring. We also determined serum parameters in dams to investigate specific maternal cues that might be responsible for this regulation. Female rats were fed either a casein (CAS), a low-isoflavone SPI, or a casein plus genistein (GEN, 250 mg/kg) diet for two weeks before mating, as well as during pregnancy and lactation. Male offspring (CAS, SPI and GEN groups) were studied 21 days after birth. The SPI group had lower serum triglyceride levels than the other groups. Serum cholesterol was reduced in both the SPI and GEN groups compared with the CAS group. Expressions of target genes of peroxisome proliferator-activated receptor α were altered in the SPI group. Serum aromatic amino acid levels in dams were associated with serum triglyceride in offspring. In conclusion, the maternal consumption of a low-isoflavone SPI diet or a casein diet containing genistein has different effects on the lipid metabolism of their offspring; however, more profound effects were observed in the SPI group. Therefore, the altered lipid metabolism of offspring may be attributed to amino acid composition in maternal dietary protein sources.

Keywords: PPARα; amino acid; lipid metabolism; maternal diet; offspring liver; soy protein isolate.

Figure 1

Effects of maternal diet on (a) body weight change (n = 14–17) and (b,c) glucose metabolism in male offspring (n = 4). Blood glucose curve and total area under the curve (AUC) in response to a glucose-loading test. Data are means ± standard error of the mean. Means with different superscripts are significantly different at p < 0.05. CAS, offspring of dams fed a casein diet; SPI, offspring of dams fed a low-isoflavone soy protein isolate diet; GEN, offspring of dams fed a casein plus genistein diet.

Figure 2

Effects of maternal diet on lipid metabolism of male offspring. (a) Serum triglyceride, (b) free fatty acid, (c) total cholesterol, (d) high-density lipoprotein (HDL) cholesterol levels, and (e) the ratio of HDL cholesterol to total cholesterol (n = 8–10); (f) Hepatic triglyceride and (g) cholesterol levels (n = 9–11). Data are means ± standard error of the mean. Means with different superscripts are significantly different at p < 0.05.

Figure 3

Effects of maternal diet on hepatic gene expression related to the lipid metabolism of male offspring. (a) Triglyceride metabolism; (b) Cholesterol metabolism. Relative mRNA level of each gene was determined by real-time PCR. Beta-actin was used as an endogenous control. Data are means ± standard error of the mean (n = 4). Means with different superscripts are significantly different at p < 0.05.

Figure 4

Effects of maternal diet on hepatic expressions of peroxisome proliferator-activated receptor alpha (PPARα)-target genes of male offspring. (a) Visualization of gene expression levels as a heat map. Data were Z-score normalized. Each cell represents the individual differentially expressed genes in each offspring liver sample (n = 4). Yellow color represents the up-regulated gene expression and blue color represents the down-regulated gene expression. * p < 0.05 and ** p < 0.01 for maternal diet effect among groups; (b) Serum adiponectin (n = 9) was measured by ELISA; (c,d) Hepatic phosphorylated AMP-activated protein kinase (p-AMPK) protein levels were determined by immunoblotting (n = 4–5). Data are means ± standard error of the mean. Means with different superscripts are significantly different at p < 0.05.

Figure 5

Correlation between (a) serum AAA levels in dams and body weight; (b) serum AAA levels in dams and relative liver weight of offspring; (c) serum AAA levels in dams and serum triglyceride levels in offspring; (d) serum total cholesterol levels in dams and serum total cholesterol levels in offspring; (e) serum high-density lipoprotein (HDL) cholesterol levels in dams and serum total cholesterol levels in offspring AAA, aromatic amino acid. Pearson correlation coefficient, r and p-value are indicated.

Figure 6

Heat map of Pearson correlation coefficients between serum parameters in dams and hepatic expressions of PPARα-target genes in offspring. Yellow color represents positive correlation and blue color represents negative correlation.