Simultaneous free fatty acid elevations and accelerated desaturation in plasma and oocytes in early postpartum dairy cows under intensive feeding management

The fertility of modern high-yielding dairy cows was previously reported to be low [1,2], and one of the leading causes was a malnourished status associated with high milk production after parturition [3,4]. Dry cows show a zero or positive energy balance until the peripartum period, and then enter a negative energy balance concurrently with delivery and the start of lactation [5,6]. The mobilization of fat in adipose tissue to produce energy increases the circulating levels of free fatty acids (FFA). Blood FFA levels start to increase in the peripartum period, peak within the first week of lactation, then decrease, and ultimately return to the basal level after 6–8 weeks of lactation [[7], [8], [9], [10]]. High postpartum blood FFA levels have been reported to induce lipid disorders, such as fatty liver [11], immune malfunction [12], and lipotoxicity [13].

Excessive lipids in cells are converted to triacylglycerol (TAG) and stored in lipid droplets [14]. Lipid droplets serve as an energy source in cells, and function to maintain lipid and protein homeostasis [15]. Furthermore, lipid droplets protect cells from the cytotoxicity of FFA, particularly saturated FFA, by storing lipids in a non-toxic form [14]. This protective mechanism of lipid droplets has been demonstrated in oocytes [16] and cumulus cells [17]. Cumulus cells are in direct contact with follicular fluid and protect oocytes from elevated FFA by converting them to TAG and storing lipid droplets in cumulus cells [17,18]. Lipotoxicity, caused by excessive FFA, may impair the fertility of lactating cows. When FFA levels increase beyond the ability of cells to synthesize TAG from FFA, FFA are incorporated and accumulate in cells, which leads to reactive oxygen species production [19], endoplasmic reticulum stress [20], ceramide accumulation [21], and, ultimately, apoptosis [22]. Oxidative stress was previously reported in the hepatocytes [23] and mammary glands [13] of lactating cows with high circulating levels of FFA. Furthermore, the developmental competence of oocytes matured with supplemental high FFA in culture medium was shown to be impaired due to lipotoxicity [24].

Investigations on FFA and TAG profiles in blood and oocytes by high-resolution liquid chromatography–mass spectrometry (LC/MS) using a small number of oocytes provide insights into lipotoxicity in lactating cows. We recently reported that blood FFA and oocyte TAG were higher in postpartum cows than in heifers [25]. TAG is the intracellular storage form of lipids that comprises three fatty acyls linked to a glycerol backbone and is decomposed to FFA as required for energy production and the synthesis of other lipids [26]. High TAG in the oocytes of postpartum cows indicated that elevated circulating levels of FFA in the 3–6 weeks of the postpartum period increased the amount of FFA reaching cumulus-oocyte complexes (COCs) via follicular fluid [27], and also that TAG synthesis in COCs was accelerated to prevent FFA lipotoxicity. Elevated oocyte TAG indicated that the ability of oocytes to manage lipotoxic FFA was reduced because their storage capacity for TAG was surpassed [28].

Lipid characteristics are important for oocyte quality. Among the FFA present in bovine oocytes, including 16:0, 16:1, 18:0, and 18:1 FFA [25], saturated FFA (FFA 16:0 and 18:0) are more cytotoxic, while monounsaturated FFA (FFA 18:1) are less cytotoxic [16]. Monounsaturated FFA are synthesized from saturated FFA, and this desaturation reaction is a key step in the synthesis of TAG from FFA [29]. The conversion of monounsaturated FFA to TAG is one reason for monounsaturated FFA being less cytotoxic [16]. Stearoyl-CoA desaturase (SCD) catalyzes desaturation reactions, and one of the typical markers of its activity is the ratios of FFA 16:1/16:0 and FFA 18:1/18:0 as the product and substrate ratios of desaturation reactions [30]. A previous study demonstrated that the FFA 18:1/18:0 ratio increased in blood and follicular fluid with elevations in blood and follicular fluid FFA concentrations [18,27]. These findings suggested that the increase in FFA transport from blood to follicular fluid, which is attributable to elevation of the blood FFA level, affected the FFA concentration and composition in follicular fluid. The FFA elongation reaction that long-chain fatty acids family member 6 catalyzes also affects intracellular fatty acid profiles, and the activity of the FFA elongation reaction interacts with the activities of desaturation reactions [31]. FFA 18:0/16:0 and 18:1/16:1 ratios, the product and substrate ratios of these elongation reactions, are used as elongase markers [32,33]. Examinations of these desaturase and elongase markers are useful for obtaining information on the status of lipid metabolism in oocytes.

We previously reported the oocyte FFA and TAG profiles of grazed lactating cows with relatively low milk production (∼7700 kg/305 days) [25]. The different livestock farming systems of outdoor grazing or indoor intensive feeding have been shown to alter the content and composition of lipids in animal products, i. e., meat [34,35] and milk [36], which may be attributed to variations in nutrition intake [37], milk production [37], body condition dynamics [[36], [37], [38]], and the lipid compositions of feed [39]. Therefore, the present study investigated the oocyte lipid profiles of cows that were under indoor intensive management and produced milk close to the average level of Japan (9800 kg/305 days, 2020, Dairy Herd Performance Test data statistics, Livestock Improvement Association of Japan, Inc., Tokyo, Japan).

The objective of this study was to obtain insights into lipotoxicity in the oocytes of dairy cows, particularly in the early postpartum period. Therefore, the contents and compositions of the energy metabolism-related lipids (i. e., FFA and TAG) in oocytes at different lactation stages were examined in cows under typical modern intensive management.

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