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Molecular mechanisms of lipid metabolism disorder in livers of ewes with pregnancy toxemia

Published online by Cambridge University Press:  17 August 2018

Y. F. Xue ,
C. Z. Guo ,
F. Hu ,
D. M. Sun ,
J. H. Liu  and
S. Y. Mao Open the ORCID record for S. Y. Mao [Opens in a new window]
Y. F. Xue
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, Jiangsu Province, China
C. Z. Guo
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, Jiangsu Province, China
F. Hu
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, Jiangsu Province, China
D. M. Sun
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, Jiangsu Province, China
J. H. Liu
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, Jiangsu Province, China
S. Y. Mao*
Affiliation:
Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing210095, Jiangsu Province, China
*
†E-mail: [email protected]
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Abstract

Pathogenesis of pregnancy toxemia (PT) is believed to be associated with the disruption of lipid metabolism. The present study aimed to explore the underlying mechanisms of lipid metabolism disorder in the livers of ewes with PT. In total, 10 pregnant ewes were fed normally (control group) whereas another 10 were subjected to 70% level feed restriction for 15 days to establish a pathological model of PT. Results showed that, as compared with the controls, the levels of blood β-hydroxybutyrate (BHBA), non-esterified fatty acids (NEFAs) and cholesterol were greater (P<0.05) and blood glucose level was lower (P<0.05) in PT ewes. The contents of NEFAs, BHBA, cholesterol and triglyceride were higher (P<0.05) and glycerol content was lower (P<0.05) in hepatic tissues of PT ewes than those of the controls. For ewes with PT, excessive fat vacuoles were observed in liver sections stained with hematoxylin–eosin; furthermore, inner structures of hepatocytes including nuclei, mitochondria and endoplasmic reticulum were damaged seriously according to the results of transmission electron microscope. Real-time PCR data showed that compared with the controls, the expression of hepatic genes involved in fatty acid oxidation (FAO) and triglyceride synthesis (TGS) was enhanced (P<0.05) whereas that related to acetyl-CoA metabolism (ACM) was repressed (P<0.05) in PT ewes. Generally, our results showed that negative energy balance altered the expression of genes involved in FAO, ACM and TGS, further caused lipid metabolism disorder in livers, resulting in PT of ewes. Our findings may provide the molecular basis for novel therapeutic strategies against this systemic metabolic disease in sheep.

Keywords

pregnancy toxemiafatty acidβ-hydroxybutyratecholesteroltriglyceride
Type
Research Article
Information
animal , Volume 13 , Issue 5 , May 2019 , pp. 992 - 999
Copyright
© The Animal Consortium 2018 

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References

Abba, Y, Abdullah, FFJ, Chung, ELT, Sadiq, MA, Mohammed, K, Osman, AY, Rahmat, NRR, Razak, IA, Lila, MAM, Haron, AW and Saharee, AA 2015. Biochemical and pathological findings of pregnancy toxemia in Saanen doe: a case report. Journal of Advanced Veterinary & Animal Research 2, 236–239.10.5455/javar.2015.b78Google Scholar
Brickner, AE, Pires, JAA, Gressley, TF and Grummer, RR 2009. Effects of abomasal lipid infusion on liver triglyceride accumulation and adipose lipolysis during fatty liver induction in dairy cows. Journal of Dairy Science 92, 4954–4961.Google Scholar
Calpereyra, L, Acostadibarrat, J, Benech, A, Silva, SD, Martín, A and González-Montaía, JR 2012. Ewe pregnancy toxemia. Revista Mexicana De Ciencias Pecuarias 3, 247–264.Google Scholar
Calpereyra, L, Benech, A, Gonzálezmontaña, J, Acostadibarrat, J, Da, SS and Martín, A 2015. Changes in the metabolic profile of pregnant ewes to an acute feed restriction in late gestation. New Zealand Veterinary Journal 63, 141–146.Google Scholar
Calpereyra, L, Borteiro, C, Benech, A, Rodas, E, Abreu, MN, Cruz, JC and Gonzálezmontaña, JR 2009. Histological changes of the liver and metabolic correlates in ewes with pregnancy toxemia. Arquivo Brasileiro De Medicina Veterinária E Zootecnia 61, 306–312.Google Scholar
Chomczynski, P and Sacchi, N 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156–159.Google Scholar
Firat, A and Ozpinar, A 2002. Metabolic profile of pre-pregnancy, pregnancy and early lactation in multiple lambing Sakiz ewes. 1. Changes in levels of plasma glucose, 3- hydroxybutyrate and cortisol levels. Annals of Nutrition & Metabolism 46, 57–61.Google Scholar
Graham, C and Simmons, NL 2005. Functional organization of the bovine rumen epithelium. American Journal of Physiology Regulatory Integrative & Comparative Physiology 288, R173–R181.Google Scholar
Grummer, RR 1993. Etiology of lipid-related metabolic disorders in periparturient dairy cows. Journal of Dairy Science 76, 3882–3896.Google Scholar
Ismail, ZA, Almajali, AM, Amireh, F and Alrawashdeh, OF 2008. Metabolic profiles in goat does in late pregnancy with and without subclinical pregnancy toxemia. Veterinary Clinical Pathology 37, 434–437.Google Scholar
Kleppe, BB, Aiello, RJ, Grummer, RR and Armentano, LE 1988. Triglyceride accumulation and very low density lipoprotein secretion by rat and goat hepatocytes in vitro. Journal of Dairy Science 71, 1813–1822.10.3168/jds.S0022-0302(88)79750-7Google Scholar
Lacetera, N, Bernabucci, U, Ronchi, B and Nardone, A 2001. Effects of subclinical pregnancy toxemia on immune responses in sheep. American Journal of Veterinary Research 62, 1020–1024.Google Scholar
Li, P, Li, X, Fu, S, Wu, C, Wang, X, Yu, G, Long, M, Wang, Z and Liu, G 2012. Alterations of fatty acid β-oxidation capability in the liver of ketotic cows. Journal of Dairy Science 95, 1759–1766.10.3168/jds.2011-4580Google Scholar
Li, P, Liu, M, Long, M, Guo, Y, Wang, Z, He, J and Liu, G 2013a. Effect of β-hydroxybutyrate on expression of 3-hydroxy-3-methylglutaryl-CoA synthase in bovine hepatocytes cultured in vitro. Feed Industry 21, 15.Google Scholar
Li, P, Liu, Y, Zhang, Y, Long, M, Guo, Y, Wang, Z, Li, X, Zhang, C, Li, X and He, J 2013b. Effect of non-esterified fatty acids on fatty acid metabolism-related genes in calf hepatocytes cultured in vitro. Cellular Physiology & Biochemistry 32, 1509–1516.Google Scholar
Lima, MS, Pascoal, RA and Stilwell, GT 2012. Glycaemia as a sign of the viability of the foetuses in the last days of gestation in dairy goats with pregnancy toxaemia. Irish veterinary journal 65, 1–6.Google Scholar
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–408.10.1006/meth.2001.1262Google Scholar
Loor, J, Dann, H, Guretzky, N, Everts, R, Oliveira, R, Green, C, Litherland, N, Rodriguez-Zas, S, Lewin, H and Drackley, J 2006. Plane of nutrition prepartum alters hepatic gene expression and function in dairy cows as assessed by longitudinal transcript and metabolic profiling. Physiological Genomics 27, 29–41.10.1152/physiolgenomics.00036.2006Google Scholar
Loor, J, Everts, R, Bionaz, M, Dann, H, Morin, D, Oliveira, R, Rodriguezzas, S, Drackley, JK and Lewin, HA 2007. Nutrition-induced ketosis alters metabolic and signaling gene networks in liver of periparturient dairy cows. Physiological Genomics 32, 105–116.10.1152/physiolgenomics.00188.2007Google Scholar
Louet, JF, Le, MC, Pégorier, JP, Decaux, JF and Girard, J 2001. Regulation of liver carnitine palmitoyltransferase I gene expression by hormones and fatty acids. Biochemical Society Transactions 29, 310–316.Google Scholar
Marteniuk, JV and Herdt, TH 1988. Pregnancy toxemia and ketosis of ewes and does. Veterinary Clinics of North America Food Animal Practice 4, 307–315.Google Scholar
McGarry, J and Foster, D 1980. Regulation of hepatic fatty acid oxidation and ketone body production. Annual review of biochemistry 49, 395–420.Google Scholar
Odongo, N, AlZahal, O, Lindinger, M, Duffield, T, Valdes, E, Terrell, S and McBride, B 2006. Effects of mild heat stress and grain challenge on acid-base balance and rumen tissue histology in lambs. Journal of Animal Science 84, 447–455.10.2527/2006.842447xGoogle Scholar
Rodriguez, JC, Gil-Gómez, G, Hegardt, FG and Haro, D 1994. Peroxisome proliferator-activated receptor mediates induction of the mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase gene by fatty acids. Journal of Biological Chemistry 269, 18767–18772.Google Scholar
Rook, JS and Herdt, TH 2000. Pregnancy toxemia of ewes, does, and beef cows. Veterinary Clinics of North America Food Animal Practice 16, 293–317.Google Scholar
Royo, T, Ayté, J, Albericio, F, Giralt, E, Haro, D and Hegardt, FG 1991. Diurnal rhythm of rat liver cytosolic 3-hydroxy-3-methylglutaryl-CoA synthase. Biochemical Journal 280, 61–64.Google Scholar
Snook, LC 1939. Fatty infiltration of the liver in pregnant ewes. Journal of Physiology 97, 238–249.Google Scholar
Wang, M, Enzhong, LI and Wang, G 2014. Histopathological analysis of liver during pregnancy toxemia in small-tailed han sheep. Agricultral Sciences and Technology 3, 470–473.Google Scholar
West, HJ 1996. Maternal undernutrition during late pregnancy in sheep. Its relationship to maternal condition, gestation length, hepatic physiology and glucose metabolism. British Journal of Nutrition 75, 593–605.Google Scholar
Williamson, DH and Whitelaw, E 1978. Physiological aspects of the regulation of ketogenesis. Biochemical Society Symposium 43, 137–161.Google Scholar
Xu, C, Liu, G, Li, X, Xia, C, Zhang, H and Wang, Z 2010. Decreased complete oxidation capacity of fatty acid in the liver of ketotic cows. Asian Australasian Journal of Animal Sciences 23, 312–317.10.5713/ajas.2010.90416Google Scholar
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