Effects of perinatal stress on the metabolites and lipids in plasma of dairy goats

Yan Huang, Yezi Kong, Bowen Li, Chenxu Zhao, Juan J. Loor, Panpan Tan, Yang Yuan, Fangyuan Zeng, Xiaoyan Zhu, Simeng Qi, Baoyu Zhao, Jianguo Wang

Stress Biology ›› 2023, Vol. 3 ›› Issue (1) : 11. DOI: 10.1007/s44154-023-00088-z
Original Paper

Effects of perinatal stress on the metabolites and lipids in plasma of dairy goats

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Abstract

Dairy goats experience metabolic stress during the peripartal period, and their ability to navigate this stage of lactation is related to the occurrence and development of metabolic diseases. Unlike dairy cows, there is a lack of comprehensive analysis of changes in the plasma profiles of peripartal dairy goats, particularly using high-throughput techniques. A subset of 9 clinically-healthy dairy goats were used from a cohort of 96 primiparous Guanzhong dairy goats (BCS, 2.75 ± 0.15). Blood samples were collected at seven time points around parturition (d 21, 14, 7 before parturition, the day of kidding, and d 7, 14, 21 postpartum), were analyzed using untargeted metabolomics and targeted lipidomics. The orthogonal partial least squares discriminant analysis model revealed a total of 31 differential metabolites including p-cresol sulfate, pyruvic acid, cholic acid, and oxoglutaric acid. The pathway enrichment analysis identified phenylalanine metabolism, aminoacyl-tRNA biosynthesis, and citrate cycle as the top three significantly-altered pathways. The Limma package identified a total of 123 differentially expressed lipids. Phosphatidylserine (PS), free fatty acids (FFA), and acylcarnitines (ACs) were significantly increased on the day of kidding, while diacylglycerols (DAG) and triacylglycerols (TAG) decreased. Ceramides (Cer) and lyso-phosphatidylinositols (LPI) were significantly increased during postpartum period, while PS, FFA, and ACs decreased postpartum and gradually returned to antepartum levels. Individual species of FFA and phosphatidylcholines (PC) were segregated based on the differences in the saturation and length of the carbon chain. Overall, this work generated the largest repository of the plasma lipidome and metabolome in dairy goats across the peripartal period, which contributed to our understanding of the multifaceted adaptations of transition dairy goats.

Keywords

Dairy goat / Transition period / Untargeted metabolomics / Lipidomics

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Yan Huang, Yezi Kong, Bowen Li, Chenxu Zhao, Juan J. Loor, Panpan Tan, Yang Yuan, Fangyuan Zeng, Xiaoyan Zhu, Simeng Qi, Baoyu Zhao, Jianguo Wang. Effects of perinatal stress on the metabolites and lipids in plasma of dairy goats. Stress Biology, 2023, 3(1): 11 https://doi.org/10.1007/s44154-023-00088-z

References

[1]
AdewuyiAA, GruysE, van EerdenburgFJ. Non esterified fatty acids (NEFA) in dairy cattle. A Review Vet Q, 2005, 27(3):117-126
CrossRef Google scholar
[2]
AgazziA, CattaneoD, Dell'OrtoV, MoroniP, BonizziL, PasottoD, BronzoV, SavoiniG. Effect of administration of fish oil on aspects of cell-mediated immune response in periparturient dairy goats. Small Ruminant Res, 2004, 55(1–3):77-83
CrossRef Google scholar
[3]
AmesBN, CathcartR, SchwiersE, HochsteinP. Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: A hypothesis. Proc Natl Acad Sci U S A, 1981, 78(11):6858-6862
CrossRef Google scholar
[4]
BatistelF, ArroyoJM, GarcesCIM, TrevisiE, ParysC, BallouMA, CardosoFC, LoorJJ. Ethyl-cellulose rumen-protected methionine alleviates inflammation and oxidative stress and improves neutrophil function during the periparturient period and early lactation in Holstein dairy cows. J Dairy Sci, 2018, 101(1):480-490
CrossRef Google scholar
[5]
BellAW. Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. J Anim Sci, 1995, 73(9):2804-2819
CrossRef Google scholar
[6]
BertramHC, YdeCC, ZhangX, KristensenNB. Effect of dietary nitrogen content on the urine metabolite profile of dairy cows assessed by nuclear magnetic resonance (NMR)-based metabolomics. J Agric Food Chem, 2011, 59(23):12499-12505
CrossRef Google scholar
[7]
BobeG, YoungJW, BeitzDC. Invited review: pathology, etiology, prevention, and treatment of fatty liver in dairy cows. J Dairy Sci, 2004, 87(10):3105-3124
CrossRef Google scholar
[8]
CalderPC. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr, 2006, 83(6 Suppl):1505S-1519S
CrossRef Google scholar
[9]
CecilianiF, LecchiC, UrhC, SauerweinH. Proteomics and metabolomics characterizing the pathophysiology of adaptive reactions to the metabolic challenges during the transition from late pregnancy to early lactation in dairy cows. J Proteomics, 2018, 178: 92-106
CrossRef Google scholar
[10]
CeliP, Di TranaA, ClapsS. Effects of perinatal nutrition on lactational performance, metabolic and hormonal profiles of dairy goats and respective kids. Small Ruminant Res, 2008, 79(2–3):129-136
CrossRef Google scholar
[11]
ChandlerTL, WhiteHM. Choline and methionine differentially alter methyl carbon metabolism in bovine neonatal hepatocytes. PLoS One, 2017, 12(2):e0171080
CrossRef Google scholar
[12]
ColeLK, VanceJE, VanceDE. Phosphatidylcholine biosynthesis and lipoprotein metabolism. Biochim Biophys Acta, 2012, 1821(5):754-761
CrossRef Google scholar
[13]
ColemanRA, MashekDG. Mammalian triacylglycerol metabolism: synthesis, lipolysis, and signaling. Chem Rev, 2011, 111(10):6359-6386
CrossRef Google scholar
[14]
da CostaKA, SandersLM, FischerLM, ZeiselSH. Docosahexaenoic acid in plasma phosphatidylcholine may be a potential marker for in vivo phosphatidylethanolamine N-methyltransferase activity in humans. Am J Clin Nutr, 2011, 93(5):968-974
CrossRef Google scholar
[15]
DelaneyJ, NevilleWA, SwainA, MilesA, LeonardMS, WaterfieldCJ. Phenylacetylglycine, a putative biomarker of phospholipidosis: its origins and relevance to phospholipid accumulation using amiodarone treated rats as a model. Biomarkers, 2004, 9(3):271-290
CrossRef Google scholar
[16]
DeLongCJ, ShenYJ, ThomasMJ, CuiZ. Molecular distinction of phosphatidylcholine synthesis between the CDP-choline pathway and phosphatidylethanolamine methylation pathway. J Biol Chem, 1999, 274(42):29683-29688
CrossRef Google scholar
[17]
DervishiE, ZhangG, DunnSM, MandalR, WishartDS, AmetajBN. GC-MS metabolomics identifies metabolite alterations that precede subclinical mastitis in the blood of transition dairy cows. J Proteome Res, 2016, 16(2):433-446
CrossRef Google scholar
[18]
EvenepoelP, MeijersBK, BammensBR, VerbekeK. Uremic toxins originating from colonic microbial metabolism. Kidney Int Suppl, 2009, 114: S12-19
CrossRef Google scholar
[19]
FahrmannJ, GrapovD, YangJ, HammockB, FiehnO, BellGI, HaraM. Systemic alterations in the metabolome of diabetic NOD mice delineate increased oxidative stress accompanied by reduced inflammation and hypertriglyceremia. Am J Physiol Endocrinol Metab, 2015, 308(11):E978-989
CrossRef Google scholar
[20]
GallWE, BeebeK, LawtonKA, AdamKP, MitchellMW, NakhlePJ, RyalsJA, MilburnMV, NannipieriM, CamastraS, NataliA, FerranniniE, GroupRS. Alpha-hydroxybutyrate is an early biomarker of insulin resistance and glucose intolerance in a nondiabetic population. PLoS One, 2010, 5(5):e10883
CrossRef Google scholar
[21]
GreenfieldRB, CecavaMJ, DonkinSS. Changes in mRNA expression for gluconeogenic enzymes in liver of dairy cattle during the transition to lactation. J Dairy Sci, 2000, 83(6):1228-1236
CrossRef Google scholar
[22]
GrossJJ, SchwarzFJ, EderK, van DorlandHA, BruckmaierRM. Liver fat content and lipid metabolism in dairy cows during early lactation and during a mid-lactation feed restriction. J Dairy Sci, 2013, 96(8):5008-5017
CrossRef Google scholar
[23]
GrzelczykA, Gendaszewska-DarmachE. Novel bioactive glycerol-based lysophospholipids: New data - New insight into their function. Biochimie, 2013, 95(4):667-679
CrossRef Google scholar
[24]
HailemariamD, MandalR, SaleemF, DunnSM, WishartDS, AmetajBN. Identification of predictive biomarkers of disease state in transition dairy cows. J Dairy Sci, 2014, 97(5):2680-2693
CrossRef Google scholar
[25]
HuFB, MansonJE, WillettWC. Types of dietary fat and risk of coronary heart disease: a critical review. J Am Coll Nutr, 2001, 20(1):5-19
CrossRef Google scholar
[26]
HuangY, WenJ, KongY, ZhaoC, LiuS, LiuY, LiL, YangJ, ZhuX, ZhaoB, CaoB, WangJ. Oxidative status in dairy goats: periparturient variation and changes in subclinical hyperketonemia and hypocalcemia. BMC Vet Res, 2021, 17(1):238
CrossRef Google scholar
[27]
ImhaslyS, NaegeliH, BaumannS, von BergenM, LuchA, JungnickelH, PotratzS, GerspachC. Metabolomic biomarkers correlating with hepatic lipidosis in dairy cows. BMC Vet Res, 2014, 10: 122
CrossRef Google scholar
[28]
IsmaeelA, FrancoME, LavadoR, PapoutsiE, CasaleGP, FuglestadM, MietusCJ, HaynatzkiGR, SmithRS, BohannonWT, SawickiI, PipinosII, KoutakisP. Altered metabolomic profile in patients with peripheral artery disease. J Clin Med, 2019, 8(9):1463
CrossRef Google scholar
[29]
KamiguchiH, MurabayashiM, MoriI, HorinouchiA, HigakiK. Biomarker discovery for drug-induced phospholipidosis: phenylacetylglycine to hippuric acid ratio in urine and plasma as potential markers. Biomarkers, 2017, 22(2):178-188
CrossRef Google scholar
[30]
KenezA, DanickeS, Rolle-KampczykU, von BergenM, HuberK. A metabolomics approach to characterize phenotypes of metabolic transition from late pregnancy to early lactation in dairy cows. Metabolomics, 2016, 12(11):165
CrossRef Google scholar
[31]
KesslerEC, GrossJJ, BruckmaierRM, AlbrechtC. Cholesterol metabolism, transport, and hepatic regulation in dairy cows during transition and early lactation. J Dairy Sci, 2014, 97(9):5481-5490
CrossRef Google scholar
[32]
KonashiS, TakahashiK, AkibaY. Effects of dietary essential amino acid deficiencies on immunological variables in broiler chickens. Brit J Nutr, 2000, 83(4):449-456
CrossRef Google scholar
[33]
Krajcovicova-KudlackovaM, SimoncicR, BederovaA, BabinskaK, BederI. Correlation of carnitine levels to methionine and lysine intake. Physiol Res, 2000, 49(3):399-402
[34]
LamSM, ZhangC, WangZ, NiZ, ZhangS, YangS, HuangX, MoL, LiJ, LeeB, MeiM, HuangL, ShiM, XuZ, MengFP, CaoWJ, ZhouMJ, ShiL, ChuaGH, LiB, CaoJ, WangJ, BaoS, WangY, SongJW, ZhangF, WangFS, ShuiG. A multi-omics investigation of the composition and function of extracellular vesicles along the temporal trajectory of COVID-19. Nat Metab, 2021, 3(7):909-922
CrossRef Google scholar
[35]
LanaspaMA, Sanchez-LozadaLG, ChoiYJ, CicerchiC, KanbayM, Roncal-JimenezCA, IshimotoT, LiN, MarekG, DuranayM, SchreinerG, Rodriguez-IturbeB, NakagawaT, KangDH, SautinYY, JohnsonRJ. Uric acid induces hepatic steatosis by generation of mitochondrial oxidative stress: potential role in fructose-dependent and -independent fatty liver. J Biol Chem, 2012, 287(48):40732-40744
CrossRef Google scholar
[36]
LemmonMA, SchlessingerJ. Cell signaling by receptor tyrosine kinases. Cell, 2010, 141(7):1117-1134
CrossRef Google scholar
[37]
LiY, XuC, XiaC, ZhangH, SunL, GaoY. Plasma metabolic profiling of dairy cows affected with clinical ketosis using LC/MS technology. Vet Q, 2014, 34(3):152-158
CrossRef Google scholar
[38]
LuoZZ, ShenLH, JiangJ, HuangYX, BaiLP, YuSM, YaoXP, RenZH, YangYX, CaoSZ. Plasma metabolite changes in dairy cows during parturition identified using untargeted metabolomics. J Dairy Sci, 2019, 102(5):4639-4650
CrossRef Google scholar
[39]
MahlaAS, ChaudhariRK, VermaAK, SinghAK, SinghSK, SinghG, SarkarM, DuttaN, KumarH, KrishnaswamyN. Effect of dietary supplementation of omega-3 polyunsaturated fatty acid (PUFA) rich fish oil on reproductive performance of the goat (Capra hircus). Theriogenology, 2017, 99: 79-89
CrossRef Google scholar
[40]
MalekMR, AhmadianS, DehpourAR, Ebrahim-HabibiA, ShafizadehM, Kashani-AminE. Investigating the role of endogenous opioid system in chloroquine-induced phospholipidosis in rat liver by morphological, biochemical and molecular modelling studies. Clin Exp Pharmacol Physiol, 2020, 47(9):1575-1583
CrossRef Google scholar
[41]
ManatTD, ChaudharySS, SinghVK, PatelSB, PuriG. Hematobiochemical profile in Surti goats during post-partum period. Vet World, 2016, 9(1):19-24
CrossRef Google scholar
[42]
MatthewsJG. JohnW, SonsL. The periparturient goat. Diseases of the Goat, Chichester, UK, 2016 41-60
CrossRef Google scholar
[43]
McArtJAA, NydamDV, OetzelGR. Epidemiology of subclinical ketosis in early lactation dairy cattle. J Dairy Sci, 2012, 95(9):5056-5066
CrossRef Google scholar
[44]
McCarthyMM, MannS, NydamDV, OvertonTR, McArtJA. Short communication: Concentrations of nonesterified fatty acids and beta-hydroxybutyrate in dairy cows are not well correlated during the transition period. J Dairy Sci, 2015, 98(9):6284-6290
CrossRef Google scholar
[45]
McFaddenJW. Review: Lipid biology in the periparturient dairy cow: contemporary perspectives. Animal, 2020, 14(S1):s165-s175
CrossRef Google scholar
[46]
McFaddenJW, GirardCL, TaoS, ZhouZ, BernardJK, DuplessisM, WhiteHM. Symposium review: One-carbon metabolism and methyl donor nutrition in the dairy cow. J Dairy Sci, 2020, 103(6):5668-5683
CrossRef Google scholar
[47]
McGarryJD, BrownNF. The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. Eur J Biochem, 1997, 244(1):1-14
CrossRef Google scholar
[48]
MonteiroAPA, BernardJK, GuoJR, WengXS, EmanueleS, DavisR, DahlGE, TaoS. Effects of feeding betaine-containing liquid supplement to transition dairy cows. J Dairy Sci, 2017, 100(2):1063-1071
CrossRef Google scholar
[49]
NRC (2007) National Research Council (NRC) Nutrient Requirements of Small Ruminants National Academic Press, Washington, DC
[50]
OpdebeeckB, D'HaesePC, VerhulstAJT. Molecular and Cellular Mechanisms That Induce Arterial Calcification by Indoxyl Sulfate and P-Cresyl Sulfate. Toxins (Basel), 2020, 12(1):58
CrossRef Google scholar
[51]
PeraldiP, HotamisligilGS, BuurmanWA, WhiteMF, SpiegelmanBM. Tumor necrosis factor (TNF)-alpha inhibits insulin signaling through stimulation of the p55 TNF receptor and activation of sphingomyelinase. J Biol Chem, 1996, 271(22):13018-13022
CrossRef Google scholar
[52]
PinottiL, BaldiA, Dell'OrtoV. Comparative mammalian choline metabolism with emphasis on the high-yielding dairy cow. Nutr Res Rev, 2002, 15(2):315-332
CrossRef Google scholar
[53]
PulinaG, MilanMJ, LavinMP, TheodoridisA, MorinE, CapoteJ, ThomasDL, FrancesconiAHD, CajaG. Invited review: Current production trends, farm structures, and economics of the dairy sheep and goat sectors. J Dairy Sci, 2018, 101(8):6715-6729
CrossRef Google scholar
[54]
RaboissonD, MounieM, MaigneE. Diseases, reproductive performance, and changes in milk production associated with subclinical ketosis in dairy cows: a meta-analysis and review. J Dairy Sci, 2014, 97(12):7547-7563
CrossRef Google scholar
[55]
RibeiroES, LimaFS, GrecoLF, BisinottoRS, MonteiroAP, FavoretoM, AyresH, MarsolaRS, MartinezN, ThatcherWW, SantosJE. Prevalence of periparturient diseases and effects on fertility of seasonally calving grazing dairy cows supplemented with concentrates. J Dairy Sci, 2013, 96(9):5682-5697
CrossRef Google scholar
[56]
RicoJE, BandaruVV, DorskindJM, HaugheyNJ, McFaddenJW. Plasma ceramides are elevated in overweight Holstein dairy cows experiencing greater lipolysis and insulin resistance during the transition from late pregnancy to early lactation. J Dairy Sci, 2015, 98(11):7757-7770
CrossRef Google scholar
[57]
RicoJE, ZangY, HaugheyNJ, RiusAG, McFaddenJW. Short communication: Circulating fatty acylcarnitines are elevated in overweight periparturient dairy cows in association with sphingolipid biomarkers of insulin resistance. J Dairy Sci, 2018, 101(1):812-819
CrossRef Google scholar
[58]
RingseisR, GessnerDK, EderK. Molecular insights into the mechanisms of liver-associated diseases in early-lactating dairy cows: hypothetical role of endoplasmic reticulum stress. J Anim Physiol an N, 2015, 99(4):626-645
CrossRef Google scholar
[59]
RukkwamsukT, KruipTA, MeijerGA, WensingT. Hepatic fatty acid composition in periparturient dairy cows with fatty liver induced by intake of a high energy diet in the dry period. J Dairy Sci, 1999, 82(2):280-287
CrossRef Google scholar
[60]
SadjadianR, SeifiHA, MohriM. Variations of energy biochemical metabolites in periparturient dairy Saanen goats. Comp Clin Pathol, 2013, 22(3):449-456
CrossRef Google scholar
[61]
SaleemF, AmetajBN, BouatraS, MandalR, ZebeliQ, DunnSM, WishartDS. A metabolomics approach to uncover the effects of grain diets on rumen health in dairy cows. J Dairy Sci, 2012, 95(11):6606-6623
CrossRef Google scholar
[62]
SchlegelG, RingseisR, KellerJ, SchwarzFJ, EderK. Changes in the expression of hepatic genes involved in cholesterol homeostasis in dairy cows in the transition period and at different stages of lactation. J Dairy Sci, 2012, 95(7):3826-3836
CrossRef Google scholar
[63]
SchoonemanMG, VazFM, HoutenSM, SoetersMR. Acylcarnitines: reflecting or inflicting insulin resistance?. Diabetes, 2013, 62(1):1-8
CrossRef Google scholar
[64]
SchrenM, SnedecT, RiefkeB, SlopiankaM, KeckM, GruendemannS, WichardJ, BrunnerN, KleinS, TheinertKB. Aspects of transition cow metabolomics—Part I: Effects of a metaphylactic butaphosphan and cyanocobalamin treatment on the metabolome in liver, blood, and urine in cows with different liver metabotypes. J Dairy Sci, 2021, 104(8):9205-9226
CrossRef Google scholar
[65]
Schrimpe-RutledgeAC, CodreanuSG, SherrodSD, McLeanJA. Untargeted metabolomics strategies-challenges and emerging directions. J Am Soc Mass Spectrom, 2016, 27(12):1897-1905
CrossRef Google scholar
[66]
ShahsavariA, D'OcchioMJ, Al JassimR. The role of rumen-protected choline in hepatic function and performance of transition dairy cows. Brit J Nutr, 2016, 116(1):35-44
CrossRef Google scholar
[67]
SimõesJ, GutiérrezC. SimõesJ, GutiérrezC. Nutritional and Metabolic Disorders in Dairy Goats. Sustainable Goat Production in Adverse Environments, 2017 Chan Springer International Publishing 177-194
CrossRef Google scholar
[68]
SongJW, LamSM, FanX, CaoWJ, WangSY, TianH, ChuaGH, ZhangC, MengFP, XuZ, FuJL, HuangL, XiaP, YangT, ZhangS, LiB, JiangTJ, WangR, WangZ, ShiM, ZhangJY, WangFS, ShuiG. Omics-driven systems interrogation of metabolic dysregulation in COVID-19 pathogenesis. Cell Metab, 2020, 32(2):188-202 e185
CrossRef Google scholar
[69]
SordilloLM, RaphaelW. Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders. Vet Clin North Am Food Anim Pract, 2013, 29(2):267-278
CrossRef Google scholar
[70]
Srednicka-ToberD, BaranskiM, SealCJ, SandersonR, BenbrookC, SteinshamnH, Gromadzka-OstrowskaJ, RembialkowskaE, Skwarlo-SontaK, EyreM, CozziG, LarsenMK, JordonT, NiggliU, SakowskiT, CalderPC, BurdgeGC, SotirakiS, StefanakisA, StergiadisS, YolcuH, ChatzidimitriouE, ButlerG, StewartG, LeifertC. Higher PUFA and n-3 PUFA, conjugated linoleic acid, alpha-tocopherol and iron, but lower iodine and selenium concentrations in organic milk: a systematic literature review and meta- and redundancy analyses. Brit J Nutr, 2016, 115(6):1043-1060
CrossRef Google scholar
[71]
StellettaC, GianesellaM, MorganteM. CannasA, PulinaG. Metabolic and nutritional diseases. Dairy goats feeding and nutrition. Bologna, Italy , 2008 263-288
CrossRef Google scholar
[72]
StergiadisS, NorskovNP, PurupS, GivensI, LeeMRF. Comparative nutrient profiling of retail goat and cow milk. Nutrients, 2019, 11(10):2282
CrossRef Google scholar
[73]
TretterL, Adam-ViziV. Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress. Philos Trans R Soc Lond B Biol Sci, 2005, 360(1464):2335-2345
CrossRef Google scholar
[74]
Van den TopAM, Van TolA, JansenH, GeelenMJ, BeynenAC. Fatty liver in dairy cows post partum is associated with decreased concentration of plasma triacylglycerols and decreased activity of lipoprotein lipase in adipocytes. J Dairy Res, 2005, 72(2):129-137
CrossRef Google scholar
[75]
VogelL, GnottM, Kroger-KochC, DannenbergerD, TuchschererA, TroscherA, KienbergerH, RychlikM, StarkeA, BachmannL, HammonHM. Effects of abomasal infusion of essential fatty acids together with conjugated linoleic acid in late and early lactation on performance, milk and body composition, and plasma metabolites in dairy cows. J Dairy Sci, 2020, 103(8):7431-7450
CrossRef Google scholar
[76]
WangR, LiB, LamSM, ShuiG. Integration of lipidomics and metabolomics for in-depth understanding of cellular mechanism and disease progression. J Genet Genomics, 2020, 47(2):69-83
CrossRef Google scholar
[77]
XueGP, SnoswellAM. Developmental changes in the activities of enzymes related to methyl group metabolism in sheep tissues. Comp Biochem Physiol B, 1986, 83(1):115-120
CrossRef Google scholar
[78]
YangY, SadriH, PrehnC, AdamskiJ, RehageJ, DanickeS, SaremiB, SauerweinH. Acylcarnitine profiles in serum and muscle of dairy cows receiving conjugated linoleic acids or a control fat supplement during early lactation. J Dairy Sci, 2019, 102(1):754-767
CrossRef Google scholar
[79]
YaoZM, VanceDE. The active synthesis of phosphatidylcholine is required for very low density lipoprotein secretion from rat hepatocytes. J Biol Chem, 1988, 263(6):2998-3004
CrossRef Google scholar
[80]
YoshimiN, FutamuraT, KakumotoK, SalehiAM, SellgrenCM, Holmen-LarssonJ, JakobssonJ, PalssonE, LandenM, HashimotoK. Blood metabolomics analysis identifies abnormalities in the citric acid cycle, urea cycle, and amino acid metabolism in bipolar disorder. BBA Clinical, 2016, 5: 151-158
CrossRef Google scholar
[81]
ZachutM, HonigH, StriemS, ZickY, Boura-HalfonS, MoallemU. Periparturient dairy cows do not exhibit hepatic insulin resistance, yet adipose-specific insulin resistance occurs in cows prone to high weight loss. J Dairy Sci, 2013, 96(9):5656-5669
CrossRef Google scholar
[82]
ZangY, SamiiSS, MyersWA, BaileyHR, DavisAN, GrilliE, McFaddenJW. Methyl donor supplementation suppresses the progression of liver lipid accumulation while modifying the plasma triacylglycerol lipidome in periparturient Holstein dairy cows. J Dairy Sci, 2019, 102(2):1224-1236
CrossRef Google scholar
[83]
ZeiselSH. Choline: an important nutrient in brain development, liver function and carcinogenesis. J Am Coll Nutr, 1992, 11(5):473-481
CrossRef Google scholar
[84]
ZhangHY, WuL, XuC, XiaC, SunLW, ShuS. Plasma metabolomic profiling of dairy cows affected with ketosis using gas chromatography/mass spectrometry. BMC Vet Res, 2013, 26(9):186
CrossRef Google scholar
[85]
ZhouZ, BulgariO, Vailati-RiboniM, TrevisiE, BallouMA, CardosoFC, LuchiniDN, LoorJJ. Rumen-protected methionine compared with rumen-protected choline improves immunometabolic status in dairy cows during the peripartal period. J Dairy Sci, 2016, 99(11):8956-8969
CrossRef Google scholar
Funding
National Natural Science Foundation of China(32102742)

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