A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning

Abstract

We examined the effects of a maternal cafeteria diet on skeletal muscle and adipose tissue development in the offspring at weaning. Rats born to mothers fed the cafeteria diet either during gestation alone or during both gestation and lactation exhibited a 25% reduction in muscle cross-sectional area with approximately 20% fewer fibres compared with pups fed a balanced chow diet. Maintaining the cafeteria diet during lactation increased intramuscular lipid content and fat pad weights characterized by adipocyte hypertrophy but not hyperplasia. These pups also had elevated muscle IGF-1, IGF-1 receptor, and PPARgamma mRNA levels, which may indicate an attempt to maintain normal insulin sensitivity. The increased adiposity and elevated IGF-1, IGF-1 receptor and PPARgamma mRNAs were not seen in the pups rehabilitated to the balanced diet during lactation. However, these pups exhibited reduced muscle cell proliferation (PCNA) with reduced insulin receptor and a trend towards reduced glucose transporter (GLUT)-4 mRNAs when compared with pups fed a balanced chow diet, indicating possible alterations in glucose uptake by muscle tissue. Therefore, rats born to mothers fed a cafeteria diet during gestation alone or during both gestation and lactation exhibited impaired skeletal muscle development and metabolic disorders normally associated with insulin resistance as early as the weaning stage.

Figure 1. A maternal cafeteria diet induces adipocyte hypertrophy in the offspring

Histological analyses of perirenal fat pads of 21-day-old rat pups born to mothers fed either chow ad libitum during gestation and lactation (C, □), the cafeteria diet during gestation followed by chow ad libitum during lactation (CDG, ░) or the cafeteria diet during gestation and lactation (CDW, ▒). A, H&E stained 6 μm thick sections from each nutrition group. B, adipocyte area results. C, an estimation of adipocyte numbers. Results are means ±s.e.m., n = 5 litters; different letters indicate statistically significant differences (P < 0.05), by ANOVA followed by Tukey's post hoc analysis. Scale bars are 50 μm.

Figure 2. A maternal cafeteria diet promotes intramuscular fat accumulation in the offspring

Histological analyses (oil red O) of intramuscular (i.m.) lipid accumulation in the semitendinosus muscles of 21-day-old rat pups born to mothers fed either chow ad libitum during gestation and lactation (C, □), the cafeteria diet during gestation followed by chow ad libitum during lactation (CDG, ░) or the cafeteria diet during gestation and lactation (CDW, ▒). A, lipids accumulated within muscle fibres (CDW group). B, lipids accumulated in the connective tissue (C group). C, quantified results from image analyses. Results are means ±s.e.m., n = 6 litters; different letters indicate statistically significant differences (P < 0.05); *0.05 ≤P≤ 0.10, by ANOVA followed by Games-Howell post hoc analysis. Scale bars are 50 μm.

Figure 3. A maternal cafeteria diet impairs skeletal muscle development

Histological analyses of muscle area (A), number of muscle fibres (B) and nuclei per cross sectional area (C) in the semitendinosus muscles of 21-day-old rat pups born to mothers fed either chow ad libitum during gestation and lactation (C, □), the cafeteria diet during gestation followed by chow ad libitum during lactation (CDG, ░) or the cafeteria diet during gestation and lactation (CDW, ▒). Results are means ±s.e.m., n = 6 litters; different letters indicate statistically significant differences (P < 0.05), *0.05 ≤P≤ 0.10 by ANOVA followed by Tukey's post hoc analysis.

Figure 4. A maternal cafeteria diet affects the expression of genes involved in muscle growth and metabolism in the offspring

Relative gene expression analyses using real-time PCR and SyBR green detection in the gastrocnemius muscles of 21-day-old rat pups born to mothers fed either chow ad libitum during gestation and lactation (C, □), the cafeteria diet during gestation followed by chow ad libitum during lactation (CDG, ░) or the cafeteria diet during gestation and lactation (CDW, ▒). Results are means ±s.e.m., n = 6; different letters indicate statistically significant differences (P < 0.05), *0.05 ≤P≤ 0.10 by ANOVA followed by Tukey's post hoc analysis.