Alteration in bile acids profile in Large White pigs during chronic heat exposure.

[en] Bile acids (BAs) are critical for cholesterol homeostasis and new roles in metabolism and endocrinology have been demonstrated recently. It remains unknown whether BA metabolism can be affected by heat stress (HS). The objective of this study was to describe the shifts in serum, hepatic and intestinal BA profiles induced by chronic HS. Twenty-seven Large White pigs weighing 40.8+/-2.7kg were assigned to one of the three treatments: a control group (CON, 23 degrees C), a HS group (33 degrees C), or a pair-fed group (PF, 23 degrees C and fed the same amount as HS group) for 21d. The concentrations of taurine-conjugated BAs (TUDCA and THDCA in serum and TCDCA, TUDCA, THDCA and THCA in liver) were decreased in HS and PF pigs. However, in HS pigs, a reduction in taurine-conjugated BAs (TCBA) correlated with decreased liver genes expression of BA synthesis, conjugation and uptake transport. BA regulated-genes (FXR, TGR5 and FGFR4) in HS pigs and TGR5, FGFR4 and KLbeta in PF pigs were down-regulated in liver. In ileum, total BAs and glycoursodeoxycholic acid concentrations were higher in HS pigs than other groups and PF group, respectively (P<0.05). TCBA (P=0.01) and tauroursodeoxycholic acid (P<0.01) were decreased in PF group. BA transporters (OSTalpha and MRP3) were up-regulated in HS pigs compared with CON and PF pigs, respectively (P<0.01). In cecum, ursodeoxycholic acid was higher in HS (P=0.02) group than CON group. The expression of apical sodium-coupled bile acid transporter (P=0.04) was lower in HS pigs than CON pigs, while OSTbeta (P<0.01) was greater in HS group than PF group. These results suggest that chronic HS suppressed liver activity of synthesis and uptake of TCBA, at least in part, which was independent of reduced feed intake.

Disciplines :

Agriculture & agronomy

Author, co-author :

Fang, Wei

Wen, Xiaobin

Meng, Qingshi

Wu, Weida

Everaert, Nadia ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition

Xie, Jingjing

Zhang, Hongfu

Language :

English

Title :

Alteration in bile acids profile in Large White pigs during chronic heat exposure.

Publication date :

2019

Journal title :

Journal of Thermal Biology

ISSN :

0306-4565

eISSN :

1879-0992

Publisher :

Elsevier, United Kingdom

Volume :

Pages :

375-383

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 17 January 2020

Statistics

Number of views

60 (2 by ULiège)

Number of downloads

3 (2 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Alemi, F., Poole, D.P., Chiu, J., Schoonjans, K., Cattaruzza, F., Grider, J.R., Bunnett, N.W., Corvera, C.U., The receptor TGR5 mediates the prokinetic actions of intestinal bile acids and is required for normal defecation in mice. Gastroenterology 144 (2013), 145–154 https://doi:10.1053/j.gastro.2012.09.055.
Angelin, B., Carlson, L.A., Bile acids and plasma high density lipoproteins: biliary lipid metabolism in fish eye disease. Eur. J. Clin. Investig. 16 (2010), 157–162 https://doi:10.1111/j.1365-2362.1986.tb01323.x.
Baumgard, L.H., Rhoads, R.P. Jr., Effects of heat stress on postabsorptive metabolism and energetics. Annu. Rev. Anim. Biosci. 1 (2013), 311–337 https://doi:10.1146/annurev-animal-031412-103644.
Björkhem, I., Araya, Z., Rudling, M., Angelin, B., Einarsson, C., Wikvall, K., Differences in the regulation of the classical and the alternative pathway for bile acid synthesis in human liver NO coordinate regulation OF CYP7A1 and CYP27A1. J. Biol. Chem. 277 (2002), 26804–26807 https://doi: 10.1074/jbc.M202343200.
Cassol, O.J., Rezin, G.T., Petronilho, F.C., Scaini, G., Gonçalves, C.L., Ferreira, G.K., Roesler, R., Schwartsmann, G., Dal-Pizzol, F., Streck, E.L., Effects of N-acetylcysteine/deferoxamine, taurine and RC-3095 on respiratory chain complexes and creatine kinase activities in rat brain after sepsis. Neurochem. Res. 35 (2010), 515–521 https://doi:10.1007/s11064-009-0089-3.
Chiang, J., Regulation of bile acid synthesis. Front. Biosci. 3 (1998), d176–d193.
Cohen, D.E., Balancing cholesterol synthesis and absorption in the gastrointestinal tract. J. Clin. lipidol. 2 (2008), S1–S3 https://doi:10.1016/j.jacl.2008.01.004.
Contreras-Jodar, A., Nayan, N.H., Hamzaoui, S., Caja, G., Salama, A.A., Heat stress modifies the lactational performances and the urinary metabolomic profile related to gastrointestinal microbiota of dairy goats. PLoS One, 14, 2019, e0202457 https://doi: 10.1371/journal.pone.0202457.
Dawson, P.A., Karpen, S.J., Intestinal transport and metabolism of bile acids. J. Lipid Res. 56 (2015), 1085–1099 https://doi: 10.1194/jlr.R054114.
Fang, W., Zhang, L., Meng, Q., Wu, W., Lee, Y.K., Xie, J., Zhang, H., Effects of dietary pectin on the profile and transport of intestinal bile acids in young pigs. J. Anim. Sci. 96 (2018), 4743–4754 https://doi: 10.1093/jas/sky327.
Frosini, M., Sesti, C., Palmi, M., Valoti, M., Fusi, F., Mantovani, P., Bianchi, L., Corte, L.D., Sgaragli, G., The Possible Role of Taurine and Gaba as Endogenous Cryogens in the Rabbit. 2002, Springer US, 335–344.
Fu, Z.D., Klaassen, C.D., Increased bile acids in enterohepatic circulation by short-term calorie restriction in male mice. Toxicol. Appl. Pharmacol. 273 (2013), 680–690 https://doi: 10.1016/j.taap.2013.10.020.
Gabler, N.K., Koltes, D., Schaumberger, S., Murugesan, G.R., Reisinger, N., Diurnal heat stress reduces pig intestinal integrity and increases endotoxin translocation. Transl. Anim. Sci. 2 (2018), 1–10 https://doi: 10.1093/tas/txx003.
Goodwin, B., Jones, S.A., Price, R.R., Watson, M.A., McKee, D.D., Moore, L.B., Galardi, C., Wilson, J.G., Lewis, M.C., Roth, M.E., A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol. Cell 6 (2000), 517–526 https://doi: 10.1016/S1097-2765(00)00051-4.
Guo, Q., Xu, L., Liu, J., Li, H., Sun, H., Wu, S., Zhou, B., Fibroblast growth factor 21 reverses suppression of adiponectin expression via inhibiting endoplasmic reticulum stress in adipose tissue of obese mice. Exp. Biol. Med. 242 (2017), 441–447 https://doi: 10.1177/1535370216677354.
Gutzwiller, J., Göke, B., Drewe, J., Hildebrand, P., Ketterer, S., Handschin, D., Winterhalder, R., Conen, D., Beglinger, C., Glucagon-like peptide-1: a potent regulator of food intake in humans. Gut 44 (1999), 81–86 https://doi: 10.1136/gut.44.1.81.
Hao, Y., Cui, Y., Gu, X., Genome-wide DNA methylation profiles changes associated with constant heat stress in pigs as measured by bisulfite sequencing. Sci. Rep., 6, 2016, 27507 https://doi: 10.1038/srep27507.
Holt, J.A., Luo, G., Billin, A.N., Bisi, J., McNeill, Y.Y., Kozarsky, K.F., Donahee, M., Mansfield, T.A., Kliewer, S.A., Goodwin, B., Definition of a novel growth factor-dependent signal cascade for the suppression of bile acid biosynthesis. Genes Dev. 17 (2003), 1581–1591 https://doi: 10.1101/gad.1083503.
Houten, S.M., Watanabe, M., Auwerx, J., Endocrine functions of bile acids. EMBO J. 25 (2006), 1419–1425 https://doi: 10.1038/sj.emboj.7601049.
Ippolito, D.L., Lewis, J.A., Yu, C., Leon, L.R., Stallings, J.D., Alteration in circulating metabolites during and after heat stress in the conscious rat: potential biomarkers of exposure and organ-specific injury. BMC Physiol., 14, 2014, 14 https://doi: 10.1186/s12899-014-0014-0.
Ishihara, A., Sapon, M.A., Yamauchi, K., Seasonal acclimatization and thermal acclimation induce global histone epigenetic changes in liver of bullfrog (Lithobates catesbeianus) tadpole. Comp. Biochem. Physiol. Mol. Integr. Physiol. 230 (2019), 39–48 https://doi: 10.1016/j.cbpa.2018.12.014.
Jung, D., Elferink, M.G., Stellaard, F., Groothuis, G.M., Analysis of bile acid‐induced regulation of FXR target genes in human liver slices. Liver Int. 27 (2007), 137–144 https://doi: 10.1111/j.1478-3231.2006.01393.x.
Katsuma, S., Hirasawa, A., Tsujimoto, G., Bile acids promote glucagon-like peptide-1 secretion through TGR5 in a murine enteroendocrine cell line STC-1. Biochem. Bioph. Res. Co. 329 (2005), 386–390 https://doi: 10.1016/j.bbrc.2005.01.139.
Kortner, T.M., Gu, J., Krogdahl, Å., Bakke, A.M., Transcriptional regulation of cholesterol and bile acid metabolism after dietary soyabean meal treatment in Atlantic salmon (Salmo salar L.). Br. J. Nutr. 109 (2013), 593–604 https://doi: 10.1017/S0007114512002024.
Lee, Y.Y., Hong, S.H., Lee, Y.J., Chung, S.S., Jung, H.S., Park, S.G., Park, K.S., Tauroursodeoxycholate (TUDCA), chemical chaperone, enhances function of islets by reducing ER stress. BIOCHEM BIOPH RES CO Biochem. Bioph. Res. Co. 397 (2010), 735–739 https://doi: 10.1016/j.bbrc.2010.06.022.
Lefebvre, P., Cariou, B., Lien, F., Kuipers, F., Staels, B., Role of bile acids and bile acid receptors in metabolic regulation. Physiol. Rev. 89 (2009), 147–191 https://doi: 10.1152/physrev.00010.2008.
Liu, F., Cottrell, J.J., Furness, J.B., Rivera, L.R., Kelly, F.W., Wijesiriwardana, U., Pustovit, R.V., Fothergill, L.J., Bravo, D.M., Celi, P., Selenium and vitamin E together improve intestinal epithelial barrier function and alleviate oxidative stress in heat‐stressed pigs. Exp. Physiol. 101 (2016), 801–810 https://doi: 10.1113/EP085746.
Loria, P., Bozzoli, M., Concari, M., Guicciardi, M.E., Carubbi, F., Bertolotti, M., Piani, D., Nistri, A., Angelico, M., Romani, M., Effect of taurohyodeoxycholic acid on biliary lipid secretion in humans. Hepatology 25 (1997), 1306–1314 https://doi: 10.1002/hep.510250601.
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 6 (2000), 507–515 https://doi: 10.1016/S1097-2765(00)00050-2.
Lu, Z., He, X., Ma, B., Zhang, L., Li, J., Jiang, Y., Zhou, G., Gao, F., Dietary taurine supplementation improves breast meat quality in chronic heat‐stressed broilers via activating the Nrf2 pathway and protecting mitochondria from oxidative attack. J. Sci. Food Agric. 99 (2018), 1066–1072 https://doi: 10.1002/jsfa.9273.
Masuda, N., Deconjugation of bile salts by Bacteroids and Clostridium. Microbiol. Immunol. 25 (2013), 1–11.
Midtvedt, T., Microbial bile acid transformation. Am. J. Clin. Nutr. 27 (1974), 1341–1347 https://doi: 10.1093/ajcn/27.11.1341.
Nakashima, T., Shima, T., Mitsuyoshi, H., Inaba, K., Matsumoto, N., Sakamoto, Y., Kashima, K., Taurine in the liver. The function of taurine conjugated with bile acids. Adv. Exp. Med. Biol. 403 (1996), 85–92.
Özcan, U., Yilmaz, E., Özcan, L., Furuhashi, M., Vaillancourt, E., Smith, R.O., Görgün, C.Z., Hotamisligil, G.S., Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313 (2006), 1137–1140 https://doi: 10.1126/science.1128294 https://doi.org/10.1111/j.1348-0421.1981.tb00001.x.
Pearce, S., Mani, V., Weber, T., Rhoads, R., Patience, J., Baumgard, L., Gabler, N., Heat stress and reduced plane of nutrition decreases intestinal integrity and function in pigs. J. Anim. Sci. 91 (2013), 5183–5193 https://doi: 10.2527/jas.2013-6759.
Pearce, S.C., Gabler, N.K., Ross, J.W., Escobar, J., Patience, J.F., Rhoads, R.P., Baumgard, L.H., The effects of heat stress and plane of nutrition on metabolism in growing pigs. J. Anim. Sci. 91 (2013), 2108–2118 https://doi: 10.2527/jas.2012-5738.
Pollmann, D., Seasonal effects on sow herds: industry experience and management strategies. J. Anim. Sci., 88(Suppl. 3), 2010, 9 (Abstr.).
Puglielli, L., Amigo, L., Arrese, M., Núñez, L., Rigotti, A., Garrido, J., González, S., Mingrone, G., Greco, A.V., Accatino, L., Protective role of biliary cholesterol and phospholipid lamellae against bile acid-induced cell damage. Gastroenterology 107 (1994), 244–254 https://doi: 10.1016/0016-5085(94)90083-3.
Qu, H., Donkin, S.S., Ajuwon, K.M., Heat stress enhances adipogenic differentiation of subcutaneous fat depot-derived porcine stromovascular cells. J. Anim. Sci. 93 (2015), 3832–3842 https://doi: 10.2527/jas.2015-9074.
Ridlon, J.M., Harris, S.C., Bhowmik, S., Kang, D.-J., Hylemon, P.B., Consequences of bile salt biotransformations by intestinal bacteria. Gut Microb. 7 (2016), 22–39 https://doi: 10.1080/19490976.2015.1127483.
Ridlon, J.M., Kang, D.-J., Hylemon, P.B., Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47 (2006), 241–259 https://doi: 10.1194/jlr.R500013-JLR200.
Roti, J.L.R., Cellular responses to hyperthermia (40–46°C): cell killing and molecular events. Int. J. Hyperth. 24 (2008), 3–15 https://doi: 10.1080/02656730701769841.
Russell, D.W., The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 72 (2003), 137–174 https://doi: 10.1146/annurev.biochem.72.121801.161712.
Russell, D.W., Fifty years of advances in bile acid synthesis and metabolism. J. Lipid Res. 50:Suppl. ment (2009), S120–S125 https://doi: 10.1194/jlr.R800026-JLR200.
Russell, D.W., Setchell, K.D., Bile acid biosynthesis. Biochemistry 31 (1992), 4737–4749 https://doi: 10.1021/bi00135a001.
Sanders, S.R., Cole, L.C., Flann, K.L., Baumgard, L.H., Rhoads, R.P., Effects of acute heat stress on skeletal muscle gene expression associated with energy metabolism in rats. FASEB J., 23(Suppl. 1), 2009 (Abstr.).
Sanz Fernandez, M., Stoakes, S.K., Abuajamieh, M., Seibert, J.T., Johnson, J.S., Horst, E.A., Rhoads, R.P., Baumgard, L.H., Heat stress increases insulin sensitivity in pigs. Phys. Rep., 3, 2015, e12478 https://doi: 10.14814/phy2.12478.
Shi, D., Bai, L., Qu, Q., Zhou, S., Yang, M., Guo, S., Li, Q., Liu, C., Impact of gut microbiota sturcture in heat-stressed broilers. Poult. Sci. 0 (2019), 1–9 https://doi: 10.3382/ps/pez026.
Siperstein, M., Jayko, M., Chaikoff, I., Dauben, W., Nature of the metabolic products of C14-cholesterol excreted in bile and feces. Exp. Biol. Med. 81 (1952), 720–724 https://doi:10.3181/00379727-81-19999.
Skibiel, A., Peñagaricano, F., Amorín, R., Ahmed, B., Dahl, G., Laporta, J., In utero heat stress alters the offspring epigenome. Sci. Rep., 8, 2018, 14609, 10.1038/s41598-018-32975-1.
Skibiel, A.L., Zachut, M., do Amaral, B.C., Levin, Y., Dahl, G.E., Liver proteomic analysis of postpartum Holstein cows exposed to heat stress or cooling conditions during the dry period. J. Dairy Sci. 101 (2018), 705–716 https://doi: 10.3168/jds.2017-13258.
Sørensen, J.G., Nielsen, M.M., Kruhøffer, M., Justesen, J., Loeschcke, V., Full genome gene expression analysis of the heat stress response in Drosophila melanogaster. Cell Stress Chaperones 10 (2005), 312–328 https://doi: 10.1379/CSC-128R1.1.
Thomas, A.M., Hart, S.N., Kong, B., Fang, J., Zhong, X. b., Guo, G.L., Genome‐wide tissue‐specific farnesoid X receptor binding in mouse liver and intestine. Hepatology 51 (2010), 1410–1419 https://doi: 10.1002/hep.23450.
Thomas, C., Gioiello, A., Noriega, L., Strehle, A., Oury, J., Rizzo, G., Macchiarulo, A., Yamamoto, H., Mataki, C., Pruzanski, M., TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metabol. 10 (2009), 167–177 https://doi: 10.1016/j.cmet.2009.08.001.
Torlińska, T., Banach, R., Paluszak, J., Gryczkadziadecka, A., Hyperthermia effect on lipolytic processes in rat blood and adipose tissue. Acta Physiol. Pol. 38 (1987), 361–366.
Wang, L., Lee, Y.K., Bundman, D., Han, Y., Thevananther, S., Kim, C.S., Chua, S.S., Wei, P., Heyman, R.A., Karin, M., Redundant pathways for negative feedback regulation of bile acid production. Dev. Cell 2 (2002), 721–731 https://doi: 10.1016/S1534-5807(02)00187-9.
Wang, L., Urriola, P.E., Luo, Z. h., Rambo, Z.J., Wilson, M.E., Torrison, J.L., Shurson, G.C., Chen, C., Metabolomics revealed diurnal heat stress and zinc supplementation‐induced changes in amino acid, lipid, and microbial metabolism. Phys. Rep., 4, 2016, e12676 https://doi: 10.14814/phy2.12676.
Wiegant, F., Surinova, S., Ytsma, E., Langelaar-Makkinje, M., Wikman, G., Post, J., Plant adaptogens increase lifespan and stress resistance in C. elegans. Biogerontology 10:1 (2009), 27–42 https://doi:10.1007/s10522-008-9151-9.
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. 77 (2018), 122–130 https://doi: 10.1016/j.jtherbio.2018.08.008.
Yang, T., Shu, T., Liu, G., Mei, H., Zhu, X., Huang, X., Zhang, L., Jiang, Z., Quantitative profiling of 19 bile acids in rat plasma, liver, bile and different intestinal section contents to investigate bile acid homeostasis and the application of temporal variation of endogenous bile acids. J. Steroid Biochem. 172 (2017), 69–78 https://doi.org/10.1016/j.jsbmb.2017.05.015.
Zachut, M., Kra, G., Livshitz, L., Portnick, Y., Yakoby, S., Friedlander, G., Levin, Y., Seasonal heat stress affects adipose tissue proteome toward enrichment of the Nrf2-mediated oxidative stress response in late-pregnant dairy cows. J. Proteomics. 158 (2017), 52–61 https://doi: 10.1016/j.jprot.2017.02.011.
Zhang, L., Wu, W., Lee, Y.-K., Xie, J., Zhang, H., Spatial heterogeneity and co-occurrence of mucosal and luminal microbiome across swine intestinal tract. Front. Microbiol., 9, 2018, 48 https://doi: 10.3389/fmicb.2018.00048.
Zhu, R., Ou, Z., Ruan, X., Gong, J., Role of liver X receptors in cholesterol efflux and inflammatory signaling. Mol. Med. Rep. 5 (2012), 895–900 https://doi: 10.3892/mmr.2012.758.