Local Mammary Glucose Supply Regulates Availability and Intracellular Metabolic Pathways of Glucose in the Mammary Gland of Lactating Dairy Goats Under Malnutrition of Energy

Abstract

As glucose is the regulator of both the milk yield and mammary oxidative status, glucose supply is considered to play important nutritional and physiological role on mammary gland (MG) metabolism. However, inconsistent results were observed from different infusion methods to evaluate the effect of glucose on MG glucose metabolism. Thus, precise method should be developed to learn how availability and intracellular metabolic pathways of glucose in the MG are altered by the direct mammary glucose supply. In addition, limited information is available on the role of mammary glucose supply in milk synthesis in lactating ruminants under an energy-deficient diet. Direct glucose supply to the MG was implemented in the current study through the external pudendal artery infusion under an energy-deficient diet. Six doses of glucose (0, 20, 40, 60, 80, and 100 g/d) were infused through the external pudendal arteries, which is the main artery to the MG, to six lactating goats fed with basal diet meeting 81% energy requirement in a 6 × 6 Latin square design. Milk and lactose yields were both quadratically increased with increased glucose infusion, whereas the milk yield changed inconsistently with the increased energy balance (EB), indicating local glucose supply, rather than EB, improved milk production. Glucose fluxes in the MG were significantly increased and correlated with mammary plasma flow. However, the ratio of lactose yield to glucose absorbed by the MG was significantly decreased. The increased glucose fluxes in the MG and changed glucose-related metabolites in milk indicated that the glucose availability and intracellular metabolic pathways was regulated by local mammary glucose. Acute glycolysis consumed the superfluous glucose and induced accumulation of oxygen radicals in the MG during over-supplied glucose conditions. The present study provided insight to optimal glucose supply to the MG during the lactation.

Keywords: glucose supply; lactation; mammary gland; metabolic partition; milk production efficiency.

FIGURE 1

Correlation analysis between infused glucose level (Glucose), energy balance (EB), and milk production (Milk). The upper number within each cell means Pearson Correlation Coefficient. The lower number with the bracket means P-value.

FIGURE 2

Dynamic changes of artery glucose concentration after infusion of different doses of glucose (0–100 g/d) through external pudendal artery. The 0 time in the X axis represents the end time of infusion. “^∗” represents significant difference in the time effect in each treatment, and “^#” represents significant difference in the treatment effect at individual time points (P < 0.05).

FIGURE 3

Effects of increasing mammary glucose supply (0–100 g/d) through the external pudendal artery on mammary plasma flow [MPF, (A)] and the ratio of mammary plasma flow and milk volume (B). Error bar represents mean of standard error.

FIGURE 4

Correlation between mammary plasma flow (MPF) and glucose fluxes. In left square matrix, the deeper color and the higher the saturation of the cells, the greater positive correlation of variables. Meanwhile, in right circle matrix, the filled pie charts from clockwise visualize the positive correlation of variables.

FIGURE 5

Effect of increasing mammary glucose supply through the external pudendal artery on synthesis rate of lactose [the ratio of lactose yield and glucose mammary supply (A) and the ratio of lactose yield and glucose mammary uptake (B)]. Error bar represents mean of standard error.

FIGURE 6

Fitting curves of milk production [milk yield (A) and lactose yield (B)] and glucose utilization [the ratio of lactose yield and glucose mammary supply (C) and the ratio of lactose yield and glucose mammary uptake (D)] when 0–100 g/d of glucose was infused to the mammary gland. Error bar represents standard error.

FIGURE 7

Time-course of artery insulin (A) and glucagon (B) and their ratio (C) when 0–100 g/d of glucose was infused to the mammary gland. The 0 time in the X axis represents the end time of infusion. “^∗” represents significant difference in time effect of each group, and “^#” represents significant difference in treatment effect at individual time points (P < 0.05).

FIGURE 8

Revised quantitative insulin sensitivity check index corrected by β-hydroxybutyric acid (RQUICKI_BHB) in goats with increasing mammary glucose supply through the external pudendal artery. Error bar represents standard error.