DOI QR코드

DOI QR Code

Elevated thyroid hormones caused by high concentrate diets participate in hepatic metabolic disorders in dairy cows

  • Chen, Qu (Key Laboratory of Animal Physiology and Biochemistry, Nanjing Agricultural University) ;
  • Wu, Chen (Key Laboratory of Animal Physiology and Biochemistry, Nanjing Agricultural University) ;
  • Yao, Zhihao (Key Laboratory of Animal Physiology and Biochemistry, Nanjing Agricultural University) ;
  • Cai, Liuping (Key Laboratory of Animal Physiology and Biochemistry, Nanjing Agricultural University) ;
  • Ni, Yingdong (Key Laboratory of Animal Physiology and Biochemistry, Nanjing Agricultural University) ;
  • Mao, Shengyong (Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University)
  • 투고 : 2021.09.02
  • 심사 : 2021.12.17
  • 발행 : 2022.08.01

초록

Objective: High concentrate diets are widely used to satisfy high-yielding dairy cows; however, long-term feeding of high concentrate diets can cause subacute ruminal acidosis (SARA). The endocrine disturbance is one of the important reasons for metabolic disorders caused by SARA. However, there is no current report about thyroid hormones involved in liver metabolic disorders induced by a high concentrate diet. Methods: In this study, 12 mid-lactating dairy cows were randomly assigned to HC (high concentrate) group (60% concentrate of dry matter, n = 6) and LC (low concentrate) group (40% concentrate of dry matter, n = 6). All cows were slaughtered on the 21st day, and the samples of blood and liver were collected to analyze the blood biochemistry, histological changes, thyroid hormones, and the expression of genes and proteins. Results: Compared with LC group, HC group showed decreased serum triglyceride, free fatty acid, total cholesterol, low-density lipoprotein cholesterol, increased hepatic glycogen, and glucose. For glucose metabolism, the gene and protein expression of glucose-6-phosphatase and phosphoenolpyruvate carboxykinase 1 in the liver were significantly up-regulated in HC group. For lipid metabolism, the expression of sterol regulatory element-binding protein 1, long-chain acyl-CoA synthetase 1, and fatty acid synthase in the liver was decreased in HC group, whereas carnitine palmitoyltransferase 1α and peroxisome proliferator activated receptor α were increased. Serum triiodothyronine, thyroxin, free triiodothyronine (FT3), and hepatic FT3 increased in HC group, accompanied by increased expression of thyroid hormone receptor (THR) in the liver. Conclusion: Taken together, thyroid hormones may increase hepatic gluconeogenesis, β-oxidation and reduce fatty acid synthesis through the THR pathway to participate in the metabolic disorders caused by a high concentrate diet.

키워드

과제정보

This study is supported with Fundamental Research Funds for the Central Universities (JCQY201905), National Natural Science Foundation of China (No.32172810), and National Key Research and Development Project (2016YFD0501203).

참고문헌

  1. Keunen JE, Plaizier JC, Kyriazakis L, et al. Effects of a subacute ruminal acidosis model on the diet selection of dairy cows. J Dairy Sci 2002;85:3304-13. https://doi.org/10.3168/jds.S0022-0302(02)74419-6
  2. Metre D, Tyler JW, Stehman SM. Diagnosis of enteric disease in small ruminants. Vet Clin North Am Food Anim Pract 2000;16:87-115. https://doi.org/10.1016/S0749-0720(15)30138-9
  3. Enemark J, Jrgensen RJ, Kristensen NB. An evaluation of parameters for the detection of subclinical rumen acidosis in dairy herds. Vet Res Commun 2004;28:687-709. https://doi.org/10.1023/B:VERC.0000045949.31499.20
  4. Plaizier JC, Krause DO, Gozho GN, Mcbride BW. Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences. Vet J 2008;176:21-31. https://doi.org/10.1016/j.tvjl.2007.12.016
  5. Zhao FQ, Keating AF. Expression and regulation of glucose transporters in the bovine mammary gland. J Dairy Sci 2007;90 (Suppl 1):E76-86. https://doi.org/10.3168/jds.2006-470
  6. Al-Trad B, Wittek T, Penner GB, et al. Expression and activity of key hepatic gluconeogenesis enzymes in response to increasing intravenous infusions of glucose in dairy cows. J Anim Sci 2010;88:2998-3008. https://doi.org/10.2527/jas.2009-2463
  7. Dong H, Wang S, Jia Y, et al. Long-term effects of subacute ruminal acidosis (SARA) on milk quality and hepatic gene expression in lactating goats fed a high-concentrate diet. PLoS One 2013;8:e82850. https://doi.org/10.1371/journal.pone.0082850
  8. Phillips CM, Goumidi L, Bertrais S, et al. Gene-nutrient interactions with dietary fat modulate the association between genetic variation of the ACSL1 gene and metabolic syndrome. J Lipid Res 2010;51:1793-800. https://doi.org/10.1194/jlr.M003046
  9. Dong HB, Sun LL, Cong RH, et al. Changes in milk performance and hepatic metabolism in mid-lactating dairy goats after being fed a high concentrate diet for 10 weeks. Animal 2017;11:418-25. https://doi.org/10.1017/S1751731116001701
  10. Dann HM, Drackley JK. Carnitine palmitoyltransferase I in liver of periparturient dairy cows: effects of prepartum intake, postpartum induction of ketosis, and periparturient disorders. J Dairy Sci 2005;88:3851-9. https://doi.org/10.3168/jds.S0022-0302(05)73070-8
  11. Xu T, Tao H, Chang G, Zhang K, Xu L, Shen X. Lipopolysaccharide derived from the rumen down-regulates stearoyl-CoA desaturase 1 expression and alters fatty acid composition in the liver of dairy cows fed a high-concentrate diet. BMC Vet Res 2015;11:52. https://doi.org/10.1186/s12917-015-0360-6
  12. Cronje PB. Ruminant physiology: digestion, metabolism, growth, and reproduction. Oxfordshire, UK: CABI Publishing; 2000.
  13. Jia YY, Wang SQ, Ni YD, Zhang YS, Zhuang S, Shen XZ. High concentrate-induced subacute ruminal acidosis (SARA) increases plasma acute phase proteins (APPs) and cortisol in goats. Animal 2014;8:1433-8. https://doi.org/10.1017/S1751731114001128
  14. Hultquist KM, Clapper JA, Casper DP. Short communication: Feeding a rumen-degradable amino acid affects plasma thyroxine and triiodothyronine concentrations. J Dairy Sci 2019;102:6679-81. https://doi.org/10.3168/jds.2019-16243
  15. Mullur R, Liu YY, Brent GA. Thyroid hormone regulation of metabolism. Physiol Rev 2014;94:355-82. https://doi.org/10.1152/physrev.00030.2013
  16. Arrojo EDR, Fonseca TL, Werneck-de-Castro JP, Bianco AC. Role of the type 2 iodothyronine deiodinase (D2) in the control of thyroid hormone signaling. Biochim Biophys Acta Gen Subj 2013;1830:3956-64. https://doi.org/10.1016/j.bbagen.2012.08.019
  17. Lakshmanan M, Goncalves E, Pontecorvi A, Robbins J. Differential effect of a new thyromimetic on triiodothyronine transport into myoblasts and hepatoma and neuroblastoma cells. Biochim Biophys Acta Mol Cell Res 1992;1133:213-7. https://doi.org/10.1016/0167-4889(92)90071-I
  18. Flamant F, Gauthier K. Thyroid hormone receptors: the challenge of elucidating isotype-specific functions and cell-specific response. Biochim Biophys Acta Gen Subj 2013;1830:3900-7. https://doi.org/10.1016/j.bbagen.2012.06.003
  19. Beckett GJ, Russell A, Nicol F, Sahu P, Wolf CR, Arthur JR. Effect of selenium deficiency on hepatic type I 5-iodothyronine deiodinase activity and hepatic thyroid hormone levels in the rat. Biochem J1992;282:483-6. https://doi.org/10.1042/bj2820483
  20. Knegsel ATMv, Brand HVD, Dijkstra J, Tamminga S, Kemp B. Effect of dietary energy source on energy balance, production, metabolic disorders and reproduction in lactating dairy cattle. Reprod Nutr Dev 2005;45:665-88. https://doi.org/10.1051/rnd:2005059
  21. Guo J, Chang G, Zhang K, et al. Rumen-derived lipopolysaccharide provoked inflammatory injury in the liver of dairy cows fed a high-concentrate diet. Oncotarget 2017;8:46769-80. https://doi.org/10.18632/oncotarget.18151
  22. Overton TR, Drackley JK, Ottemann-Abbamonte CJ, Beaulieu AD, Emmert LS, Clark JH. Substrate utilization for hepatic gluconeogenesis is altered by increased glucose demand in ruminants. J Anim Sci 1999;77:1940-51. https://doi.org/10.2527/1999.7771940x
  23. Aschenbach JR, Kristensen NB, Donkin SS, Hammon HM, Penner GB. Gluconeogenesis in dairy cows: the secret of making sweet milk from sour dough. IUBMB Life 2010;62:869-77. https://doi.org/10.1002/iub.400
  24. Xu T, Tao H, Chang G, Zhang K, Xu L, Shen X. Lipopolysaccharide derived from the rumen down-regulates stearoylCoA desaturase 1 expression and alters fatty acid composition in the liver of dairy cows fed a high-concentrate diet. BMC Vet Res 2015;11:52. https://doi.org/10.1186/s12917-015-0360-6
  25. Graugnard DE, Berger LL, Faulkner DB, Loor JJ. High-starch diets induce precocious adipogenic gene network up-regulation in longissimus lumborum of early-weaned Angus cattle. Br J Nutr 2010;103:953-63. https://doi.org/10.1017/S0007114509992789
  26. Suh JH, Sieglaff DH, Zhang A, et al. SIRT1 is a direct coactivator of thyroid hormone receptor beta1 with gene-specific actions. PLoS One 2013;8:e70097. https://doi.org/10.1371/journal.pone.0070097
  27. Park EA, Song S, Vinson C, Roesler WJ. Role of CCAAT enhancer-binding protein beta in the thyroid hormone and cAMP induction of phosphoenolpyruvate carboxykinase gene transcription. J Biol Chem 1999;274:211-7. https://doi.org/10.1074/jbc.274.1.211
  28. Sinha RA, Singh BK, Yen PM. Thyroid hormone regulation of hepatic lipid and carbohydrate metabolism. Trends Endocrinol Metab 2014;25:538-45. https://doi.org/10.1016/j.tem.2014.07.001
  29. Heitzman RJ, Hibbitt KG, Mather I. The effects of thyroxine on hepatic gluconeogenesis and ketogenesis in dairy cows. Eur J Biochem 1971;21:411-5. https://doi.org/10.1111/j.1432-1033.1971.tb01485.x
  30. Tian P, Luo Y, Li X, et al. Negative effects of long-term feeding of high-grain diets to lactating goats on milk fat production and composition by regulating gene expression and DNA methylation in the mammary gland. J Anim Sci Biotechnol 2017;8:74. https://doi.org/10.1186/s40104-017-0204-2
  31. Li L, Cao Y, Xie Z, Zhang Y. A high-concentrate diet induced milk fat decline via glucagon-mediated activation of AMP-activated protein kinase in dairy cows. Sci Rep 2017;7:44217. https://doi.org/10.1038/srep44217
  32. Levesque J, Dion S, Brassard M, Rico D, Gervais R, Chouinard Y. PSXV-24 Dietary strategies to reduce the impact of high-concentrate diet on performance, ruminal fermentation and milk composition of dairy goats. J Anim Sci 2018;96 (suppl_3):474. https://doi.org/10.1093/jas/sky404.1035
  33. Zebeli Q, Dunn SM, Ametaj BN. Perturbations of plasma metabolites correlated with the rise of rumen endotoxin in dairy cows fed diets rich in easily degradable carbohydrates. J Dairy Sci 2011;94:2374-82. https://doi.org/10.3168/jds.2010-3860
  34. Jiang X, Zeng T, Zhang S, Zhang Y. Comparative proteomic and bioinformatic analysis of the effects of a high-grain diet on the hepatic metabolism in lactating dairy goats. Plos One 2013;8:e80698. https://doi.org/10.1371/journal.pone.0080698
  35. Capuco AV, Connor EE, Wood DL. Regulation of mammary gland sensitivity to thyroid hormones during the transition from pregnancy to lactation. Exp Biol Med (Maywood) 2008;233:1309-14. https://doi.org/10.3181/0803-RM-85
  36. Oppenheimer JH. Thyroid hormone action at the nuclear level. Ann Intern Med 1985;102:374-84. https://doi.org/10.7326/0003-4819-102-3-374