Insulin signaling, inflammation, and lipolysis in subcutaneous adipose tissue of transition dairy cows either overfed energy during the prepartum period or fed a controlled-energy diet

Abstract

Adipose tissue mobilization is a hallmark of the transition period in dairy cows. Cows overfed energy during the dry period have higher concentrations of nonesterified fatty acids (NEFA) and β-hydroxybutyrate (BHB) compared with cows fed a controlled-energy diet prepartum. The reason for an increase in blood NEFA concentrations at the level of adipose tissue in cows overfed energy has not been fully elucidated. One hypothesis is that cows with high BHB concentrations suffer from adipose tissue-specific insulin resistance, leading to higher rates of adipose tissue mobilization in the postpartum period. To test this hypothesis, subcutaneous adipose tissue biopsies of cows overfed energy in excess of predicted requirements by 50% in the dry period, and that had high concentrations of blood BHB postpartum (group H; n=12), were used. Findings were compared with results of biopsies from cows fed a controlled-energy diet and with low BHB concentrations postpartum (group C; n=12) to create the biggest contrast in BHB concentrations. Subcutaneous adipose tissue biopsies were obtained before and 60 min after an intravenous glucose challenge (0.25 g/kg of glucose) at 28 and 10 d before expected calving as well as on d 4 and 21 postpartum. Phosphorylation of protein kinase B, extracellular signal-regulated kinase, and hormone-sensitive lipase was determined before and after glucose infusion by Western blot. Western blot was also used to assess the baseline protein abundance of peroxisome proliferator-activated receptor gamma and insulin receptor β-subunit. In addition, gene expression of fatty acid synthase, adiponectin, monocyte chemoattractant protein 1, and tumor necrosis factor α was determined by real-time quantitative reverse-transcription PCR. Backfat thickness was determined in the thurl area by ultrasonography. Cows in group H showed a greater degree of lipogenesis prepartum, but no differences were found in lipolytic enzyme activity postpartum compared with cows in group C. Baseline plasma insulin concentrations were decreased and serum NEFA concentrations increased postpartum in group H. Insulin signaling through protein kinase B, quantity of insulin receptor, markers of inflammation, and peroxisome proliferator-activated receptor gamma in adipose tissue were not different between the groups, but expression of adiponectin was increased in adipose tissue of cows in group H during the immediate peripartum period. In conclusion, differences in serum concentrations of NEFA between cows overfed energy prepartum and high blood concentrations of BHB are likely due to greater negative energy balance postpartum reflected in lower circulating concentrations of glucose and insulin and an increase in the total amount of mobilized adipose tissue mass rather than due to changes in adipose tissue insulin signaling.