Running head: Heat affects cholesterol and bile acid alterations in cholesterol and bile acids metabolism in large white pigs during short-term heat exposure
Running head: Heat affects cholesterol and bile acid alterations in cholesterol and bile acids metabolism in large white pigs during short-term heat exposure
Publication date :
2020
Journal title :
Animals
eISSN :
2076-2615
Publisher :
MDPI AG
Volume :
10
Issue :
2
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
Fundamental Research Funds for the Central UniversitiesNational Key Laboratory of Animal Nutrition2016YFD0500501Agricultural Science and Technology Innovation Program, ASTIP: ASTIP-IAS07
St-Pierre, N.; Cobanov, B.; Schnitkey, G. Economic losses from heat stress by US livestock industries1. J. Dairy Sci. 2003, 86, E52–E77. [CrossRef]
Hyun, Y.; Ellis, M.; Riskowski, G.; Johnson, R. Growth performance of pigs subjected to multiple concurrent environmental stressors. J. Anim. Sci. 1998, 76, 721–727. [CrossRef]
Renaudeau, D.; Anais, C.; Tel, L.; Gourdine, J. Effect of temperature on thermal acclimation in growing pigs estimated using a nonlinear function1. J. Anim. Sci. 2010, 88, 3715–3724. [CrossRef] [PubMed]
Collin, A.; van Milgent, J.; Le Dividich, J. Modelling the effect of high, constant temperature on food intake in young growing pigs. Anim. Sci. 2001, 72, 519–527. [CrossRef]
Baumgard, L.H.; Rhoads, R.P., Jr. Effects of heat stress on postabsorptive metabolism and energetics. Annu. Rev. Anim. Biosci. 2013, 1, 311–337. [CrossRef] [PubMed]
Pearce, S.; Gabler, N.; Ross, J.; Escobar, J.; Patience, J.; Rhoads, R.; Baumgard, L. The effects of heat stress and plane of nutrition on metabolism in growing pigs. J. Anim. Sci. 2013, 91, 2108–2118. [CrossRef] [PubMed]
Qu, H.; Donkin, S.; Ajuwon, K. Heat stress enhances adipogenic differentiation of subcutaneous fat depot–derived porcine stromovascular cells. J. Anim. Sci. 2015, 93, 3832–3842. [CrossRef]
Belhadj Slimen, I.; Najar, T.; Ghram, A.; Abdrrabba, M. Heat stress effects on livestock: Molecular, cellular and metabolic aspects, a review. J. Anim. Physiol. Anim. Nutr. 2016, 100, 401–412. [CrossRef]
Kouba, M.; Hermier, D.; Le Dividich, J. Influence of a high ambient temperature on lipid metabolism in the growing pig. J. Anim. Sci. 2001, 79, 81–87. [CrossRef]
Qu, H.; Ajuwon, K. Adipose tissue-specific responses reveal an important role of lipogenesis during heat stress adaptation in pigs. J. Anim. Sci. 2018, 96, 975–989. [CrossRef]
Qu, H.; Ajuwon, K.M. Metabolomics of heat stress response in pig adipose tissue reveals alteration of phospholipid and fatty acid composition during heat stress. J. Anim. Sci. 2018, 96, 3184–3195. [CrossRef] [PubMed]
Vigh, L.; Maresca, B.; Harwood, J.L. Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem. Sci. 1998, 23, 369–374. [CrossRef]
Leach, M.D.; Cowen, L.E. Membrane fluidity and temperature sensing are coupled via circuitry comprised of Ole1, Rsp5, and Hsf1 in Candida albicans. Eukaryot. Cell 2014, 13, 1077–1084. [CrossRef] [PubMed]
Nagy, E.; Balogi, Z.; Gombos, I.; Åkerfelt, M.; Björkbom, A.; Balogh, G.; Török, Z.; Maslyanko, A.; Fiszer-Kierzkowska, A.; Lisowska, K. Hyperfluidization-coupled membrane microdomain reorganization is linked to activation of the heat shock response in a murine melanoma cell line. Proc. Natl. Acad. Sci. USA 2007, 104, 7945–7950. [CrossRef]
Balogh, G.; Péter, M.; Glatz, A.; Gombos, I.; Török, Z.; Horváth, I.; Harwood, J.L.; Vígh, L. Key role of lipids in heat stress management. FEBS Lett. 2013, 587, 1970–1980. [CrossRef]
Sudhof, T.C.; Goldstein, J.L.; Brown, M.S.; Russell, D.W. The LDL receptor gene: A mosaic of exons shared with different proteins. Science 1985, 228, 815–822. [CrossRef]
Lusis, A.; Heinzmann, C.; Sparkes, R.; Scott, J.; Knott, T.; Geller, R.; Sparkes, M.; Mohandas, T. Regional mapping of human chromosome 19: Organization of genes for plasma lipid transport (APOC1,-C2, and-E and LDLR) and the genes C3, PEPD, and GPI. Proc. Natl. Acad. Sci. USA 1986, 83, 3929–3933. [CrossRef]
Singh, A.B.; Kan, C.F.K.; Shende, V.; Dong, B.; Liu, J. A novel posttranscriptional mechanism for dietary cholesterol-mediated suppression of liver LDL receptor expression. J. Lipid Res. 2014, 55, 1397–1407. [CrossRef]
Horton, J.D.; Goldstein, J.L.; Brown, M.S. SREBPs: Activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Investig. 2002, 109, 1125–1131. [CrossRef]
Lu, T.T.; Makishima, M.; Repa, J.J.; Schoonjans, K.; Kerr, T.A.; Auwerx, J.; Mangelsdorf, D.J. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol. Cell 2000, 6, 507–515. [CrossRef]
Dawson, P.A.; Karpen, S.J. Intestinal Transport and Metabolism of Bile Acids. J. Lipid Res. 2015, 56, 1085–1099. [CrossRef] [PubMed]
Russell, D.W. The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 2003, 72, 137–174. [CrossRef] [PubMed]
Collier, R.J.; Baumgard, L.H.; Zimbelman, R.B.; Xiao, Y. Heat stress: Physiology of acclimation and adaptation. Anim. Front. 2018, 9, 12–19. [CrossRef] [PubMed]
Wen, X.; Wu, W.; Fang, W.; Tang, S.; Xin, H.; Xie, J.; Zhang, H. Effects of long-term heat exposure on cholesterol metabolism and immune responses in growing pigs. Livest. Sci. 2019, 230, 103857. [CrossRef]
Fang, W.; Wen, X.; Meng, Q.; Wu, W.; Everaert, N.; Xie, J.; Zhang, H. Alteration in bile acids profile in Large White pigs during chronic heat exposure. J. Therm. Biol. 2019, 84, 375–383. [CrossRef]
Pearce, S.; Sanz-Fernandez, M.; Hollis, J.; Baumgard, L.H.; Gabler, N.K. Short-term exposure to heat stress attenuates appetite and intestinal integrity in growing pigs. J. Anim. Sci. 2014, 92, 5444–5454. [CrossRef]
Seelenbinder, K.M.; Zhao, L.D.; Hanigan, M.D.; Hulver, M.W.; McMillan, R.P.; Baumgard, L.H.; Selsby, J.T.; Ross, J.W.; Gabler, N.K.; Rhoads, R.P. Effects of heat stress during porcine reproductive and respiratory syndrome virus infection on metabolic responses in growing pigs. J. Anim. Sci. 2018, 96, 1375–1387. [CrossRef]
Konings, A. Membranes as targets for hyperthermic cell killing. In Preclinical Hyperthermia; Springer: Berlin/Heidelberg, Germany, 1988; pp. 9–21.
Crockett, E.L. Cholesterol function in plasma membranes from ectotherms: Membrane-specific roles in adaptation to temperature. Am. Zool. 1998, 38, 291–304. [CrossRef]
Cress, A.E.; Culver, P.S.; Moon, T.E.; Gerner, E.W. Correlation between amounts of cellular membrane components and sensitivity to hyperthermia in a variety of mammalian cell lines in culture. Cancer Res. 1982, 42, 1716–1721.
Cress, A.E.; Gerner, E.W. Cholesterol levels inversely reflect the thermal sensitivity of mammalian cells in culture. Nature 1980, 283, 677. [CrossRef]
Feder, M.E.; Hofmann, G.E. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu. Rev. Physiol. 1999, 61, 243–282. [CrossRef] [PubMed]
Ness, G.C.; Chambers, C.M. Feedback and hormonal regulation of hepatic 3-hydroxy-3-methylglutaryl coenzyme A reductase: The concept of cholesterol buffering capacity. Proc. Soc. Exp. Biol. Med. 2000, 224, 8–19. [CrossRef] [PubMed]
Hardison, W.; Proffitt, J.H. Influence of hepatic taurine concentration on bile acid conjugation with taurine. Am. J. Physiol. Endocrinol. Metab. 1977, 232, E75. [CrossRef] [PubMed]
Hardison, W.G. Hepatic taurine concentration and dietary taurine as regulators of bile acid conjugation with taurine. Gastroenterology 1978, 75, 71–75. [CrossRef]
Sjövall, J. Dietary glycine and taurine on bile acid conjugation in man. Bile acids and steroids 75. Proc. Soc. Exp. Biol. Med. 1959, 100, 676–678. [CrossRef]
Hahn, G. Dynamic responses of cattle to thermal heat loads. J. Anim. Sci. 1999, 77, 10–20. [CrossRef]
Frosini, M.; Sesti, C.; Palmi, M.; Valoti, M.; Fusi, F.; Mantovani, P.; Bianchi, L.; Della Corte, L.; Sgaragli, G. The possible role of taurine and GABA as endogenous cryogens in the rabbit. In Taurine 4; Springer: Berlin/Heidelberg, Germany, 2002; pp. 335–344.
El Idrissi, A.; Trenkner, E. Growth factors and taurine protect against excitotoxicity by stabilizing calcium homeostasis and energy metabolism. J. Neurosci. 1999, 19, 9459–9468. [CrossRef]
Yang, J.; Zong, X.; Wu, G.; Lin, S.; Feng, Y.; Hu, J. Taurine increases testicular function in aged rats by inhibiting oxidative stress and apoptosis. Amino Acids 2015, 47, 1549–1558. [CrossRef]
Surai, P.; Kochish, I.; Kidd, M. Taurine in poultry nutrition. Anim. Feed Sci. Technol. 2019, 260, 114339. [CrossRef]
Serviddio, G.; Pereda, J.; Pallardó, F.V.; Carretero, J.; Borras, C.; Cutrin, J.; Vendemiale, G.; Poli, G.; Viña, J.; Sastre, J. Ursodeoxycholic acid protects against secondary biliary cirrhosis in rats by preventing mitochondrial oxidative stress. Hepatology 2004, 39, 711–720. [CrossRef] [PubMed]
Rodrigues, C.; Fan, G.; Wong, P.Y.; Kren, B.T.; Steer, C.J. Ursodeoxycholic acid may inhibit deoxycholic acid-induced apoptosis by modulating mitochondrial transmembrane potential and reactive oxygen species production. Mol. Med. 1998, 4, 165. [CrossRef] [PubMed]
Hofmann, A.F. The enterohepatic circulation of bile acids in mammals: Form and functions. Front Biosci. 2009, 14, 2584–2598. [CrossRef] [PubMed]
Watt, S.M.; Simmonds, W.J. Effects of four taurine-conjugated bile acids on mucosal uptake and lymphatic absorption of cholesterol in the rat. J. Lipid Res. 1984, 25, 448–455.
Murakami, S.; Fujita, M.; Nakamura, M.; Sakono, M.; Nishizono, S.; Sato, M.; Imaizumi, K.; Mori, M.; Fukuda, N. Taurine ameliorates cholesterol metabolism by stimulating bile acid production in high-cholesterol-fed rats. Clin. Exp. Pharmacol. Physiol. 2016, 43, 372–378. [CrossRef]
Yu, J.; Yin, P.; Liu, F.; Cheng, G.; Guo, K.; Lu, A.; Zhu, X.; Luan, W.; Xu, J. Effect of heat stress on the porcine small intestine: A morphological and gene expression study. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2010, 156, 119–128. [CrossRef]
Zhang, M.; Bi, L.; Fang, J.; Su, X.; Da, G.; Kuwamori, T.; Kagamimori, S. Beneficial effects of taurine on serum lipids in overweight or obese non-diabetic subjects. Amino Acids 2004, 26, 267–271. [CrossRef]
Yeh, Y.-H.; Chen, M.-H.; Lee, Y.-T.; Hsieh, H.-S.; Hwang, D.-F. Effect of Taurine on Toxicity of Oxidized Cholesterol and Oxidized Fish Oil in Rats. J. Food Drug Anal. 2008, 16, 76–85.
Lu, Z.; He, X.; Ma, B.; Zhang, L.; Li, J.; Jiang, Y.; Zhou, G.; Gao, F. Dietary taurine supplementation decreases fat synthesis by suppressing the liver X receptor α pathway and alleviates lipid accumulation in the liver of chronic heat-stressed broilers. J. Sci. Food Agric. 2019. [CrossRef]
Morales, A.; Cota, S.; Ibarra, N.; Arce, N.; Htoo, J.; Cervantes, M. Effect of heat stress on the serum concentrations of free amino acids and some of their metabolites in growing pigs. J. Anim. Sci. 2016, 94, 2835–2842. [CrossRef]
Sun, X.; Zhang, H.; Sheikhahmadi, A.; Wang, Y.; Jiao, H.; Lin, H.; Song, Z. Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens (Gallus gallus domesticus). Int. J. Biometeorol. 2015, 59, 127–135. [CrossRef] [PubMed]
Xin, H.; Zhang, X.; Sun, D.; Zhang, C.; Hao, Y.; Gu, X. Chronic heat stress increases insulin-like growth factor-1 (IGF-1) but does not affect IGF-binding proteins in growing pigs. J. Therm. Biol. 2018, 77, 122–130. [CrossRef] [PubMed]
Oded, S.; Ru, W.; Wang, T.J.; Catherine, R.; Lewis, G.D.; Vasan, R.S.; Carr, S.A.; Ravi, T.; Gerszten, R.E.; Mootha, V.K. Metabolic profiling of the human response to a glucose challenge reveals distinct axes of insulin sensitivity. Mol. Syst. Biol. 2008, 4, 214.
Fu, Z.D.; Klaassen, C.D. Increased bile acids in enterohepatic circulation by short-term calorie restriction in male mice. Toxicol. Appl. Pharmacol. 2013, 273, 680–690. [CrossRef]