Abstract
Simple SummaryYak, which is the predominant and semi-domesticated livestock on the Qinghai-Tibet Plateau, suffers severe starvation and body weight reduction in the cold season because of the harsh highland environment. Lipids are important energy sources to starvation animals. β-hydroxybutyrate (BHBA) that is derived from lipid decomposition as the primary ketone body is with the function not only to provide energy for animals as energy materials, but also regulate lipid metabolism as signaling molecular. However, the effects of starvation and BHBA on lipid metabolism and its mechanism are still unclear for ruminant animals. Herein, we investigated the effects of starvation and intravenous infusion of BHBA solution on Yak growth, serum biochemistry, hormones, subcutaneous adipocyte morphology, fatty acid composition, activity of enzymes related to lipid metabolism, and signal pathway. The results showed that starvation promoted lipid catabolism and BHBA infusion up-regulated the mRNA expression of receptor GPR109A in subcutaneous adipose tissue, inhibited the Cyclic adenosine monophosphate(cAMP)/Protein kinase A (PKA)/cAMP-responsive element binding protein (CREB) signaling pathway, and inhibited lipolysis. Our study was beneficial for enriching the nutrition regulation theory of yaks and improving their growth potential.Lipid is the chief energy source for starved animals. β-hydroxybutyrate (BHBA) is the main ketone body produced by lipid decomposition. In Chinese hamster ovary (CHO) cell experiment, it was found that BHBA could be used not only as an energy substance, but also as a ligand of GPR109A for regulating lipid metabolism. However, whether BHBA can regulate lipid metabolism of yaks, and its effective concentration and signal pathway are not clear. This study investigated the effects and mechanism of starvation and BHBA on the lipid metabolism of yak. Eighteen male Jiulong yaks were selected and then randomly divided into three groups: normal feeding group (NG), starvation group (SG), and starvation with BHBA infusion group (SBG). The yaks in the NG group were freely fed during the trial, while the yaks in the SG and SBG groups fasted; from 7th to 9th days of the experiment, the NG and SG were infused continuous with 0.9% normal saline and SBG was infused 1.7 mmol/L BHBA solution respectively. The blood samples were collected on the 0th, 1st, 3rd, 5th, 7th, and 9th day of experiment. The subcutaneous adipose tissue of all the yaks in this study were taken from live bodies after infusion. Serum glucose, lipid metabolites, hormone concentrations, and mRNA and protein expressions of key factors of lipid metabolism and signaling pathway in subcutaneous adipose tissue were measured. The results showed that, as compared with NG, starvation significantly reduced the body weight of yak in SG, and significantly increased the concentration of BHBA in serum and the mRNA expression of PKA and CREB1 in subcutaneous adipose tissue, while the mRNA expression of MEK, PKC, ERK1/2, the area of adipocytes, and the proportion of saturated fatty acid were decreased. Whereas, further increase of BHBA concentration through infusion promoted the mRNA expression of GPR109A receptor in the subcutaneous adipose tissue of SBG, inhibited the mRNA expression of AC and PKA, and decreased the phosphorylation protein abundance of CREB1, and significantly increased the diameter and area of adipocytes. These findings suggest that starvation led to enhanced lipid catabolism in yaks. An increasing BHBA concentration could increase the mRNA expression of GPR109A receptor in subcutaneous adipose tissue and inhibit the cAMP/PKA/CREB signaling pathway and lipid decomposition.
Highlights
Yak (Bos grunniens) is the unique bovine that has evolved to adapt to the harsh environment of Qinghai-Tibetan Plateau over 3500 m above sea level
On the ninth day of the experiment, when compared with starvation group (SG), the body weight of yaks with BHBA infusion after starvation did not significantly increase, the weight loss of yaks was reduced from day 7 to day 9 (p < 0.05)
The results found that starvation significantly reduced the mRNA expressions of CCAAT enhancer-binding protein α (C/EBPα), SREBP1, and PPARα in the subcutaneous fat tissues of yaks, and significantly increased FOXO1, which indicated that the differentiation of fat cells in subcutaneous adipose tissue of yak was inhibited and the lipid synthesis decreased after starvation
Summary
Yak (Bos grunniens) is the unique bovine that has evolved to adapt to the harsh environment of Qinghai-Tibetan Plateau over 3500 m above sea level. The Qinghai-Tibet Plateau climate is sharp frost in the long-term cold season from October to May (average temperature 5–15 ◦ C) [1,2]. The plateau grassland has a long-term withered period (October to May of the year) every year when forage is extreme scarce; yaks inevitably suffered from serious starvation in the seasonal cycles, which caused substantial economic losses. Investigating the regulatory mechanisms of nutritional metabolism under starvation is meaningful for yak farming on the Qinghai-Tibetan Plateau. The deposition of adipose tissues is the essential energy storages in the body of yaks for survival under prolonged starvation. The deposition of the triacylglycerol in the fat tissue was mobilized to produce non-esterified fatty acid (NEFA) and glycerol
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