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Effects of glucocorticoids on the gene expression of nutrient transporters in different rabbit intestinal segments

Published online by Cambridge University Press:  09 March 2020

H. Liu
Affiliation:
Department of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural University, No. 61 Daizong Road, Taian, Shandong271018, China
L. Liu
Affiliation:
Department of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural University, No. 61 Daizong Road, Taian, Shandong271018, China
F. Li*
Affiliation:
Department of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural University, No. 61 Daizong Road, Taian, Shandong271018, China
*
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Abstract

Glucocorticoids (GCs) are counterregulatory hormones with broad effects on the digestion and absorption of dietary carbohydrates, lipids and proteins, but the underlying molecular mechanisms of these effects remain unclear. The present experiment was conducted to investigate the main expression sites of nutrient transporters and the effects of GCs on the gene expression of these transporters in the rabbit small intestine. The results showed that peptide transporter 1 (PepT1), facultative amino acid transporter (rBAT), neutral amino acid transporter (B0AT), excitatory amino acid transporter 3 (EAAT3), sodium-glucose transporter 1 (SGLT1) and glucose transporter 5 (GLUT5) were mainly expressed in the distal segment, glucose transporter 2 (GLUT2) and fatty-acid-binding protein 4 (FATP4) were mainly expressed in the proximal segment and cationic amino acid transporter 1 (CAT1) was mainly expressed in the middle segment of the rabbit small intestine. In addition, we analysed the effects of 3 h (short-term) or 7 days (long-term) dexamethasone (DEX) treatment on the gene expression of most nutrient transporters. The results showed that short-term DEX treatment significantly decreased PepT1, B0AT, EAAT3, rBAT and SGLT1 expressions in all small intestinal segments, while it significantly decreased GLUT2 in the duodenum and FATP4 in the duodenum and ileum (P < 0.05). Long-term DEX treatment also significantly decreased PepT1, CAT1, B0AT, EAAT3, rBAT and SGLT1 in all small intestinal segments and significantly decreased GLUT2 in the jejunum and FATP4 in the ileum (P < 0.05). In conclusion, DEX could decrease the gene expression of most nutrient transporters (except GLUT5) and affect the transport of intestinal amino acids, monosaccharides and fatty acids.

Type
Research Article
Copyright
© The Animal Consortium 2020

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Footnotes

*

Co-first authors, these authors contributed the same to this work.

References

Adams, MC 2007. Role of the transcription factor atf4 in the anabolic actions of insulin and the anti-anabolic actions of glucocorticoids. Journal of Biological Chemistry 282, 1674416753.CrossRefGoogle ScholarPubMed
Boudry, G, Cheeseman, CI and Perdue, MH 2007. Psychological stress impairs Na+-dependent glucose absorption and increases GLUT2 expression in the rat jejunal brush-border membrane. American Journal of Physiology Regulatory Integrative & Comparative Physiology 292, R862.CrossRefGoogle ScholarPubMed
Broer, S 2008. Amino acid transport across mammalian intestinal and renal epithelia. Physiological Reviews 88, 249286.CrossRefGoogle ScholarPubMed
Douard, V, Choi, HI, Elshenawy, S, Lagunoff, D and Ferraris, RP 2008. Developmental reprogramming of rat GLUT5 requires glucocorticoid receptor translocation to the nucleus. The Journal of Physiology 586, 36573673.CrossRefGoogle ScholarPubMed
Fu, CY, Liu, L, Gao, Q, Sui, XY and Li, FC 2017. Cloning, molecular characterization, and spatial and developmental expression analysis of GPR41 and GPR43 genes in New Zealand rabbits. Animal 11, 17981806.CrossRefGoogle ScholarPubMed
Fu, C, Liu, L and Li, F 2018 Acetate alters the process of lipid metabolism in rabbits. Animal 12, 18951902.CrossRefGoogle ScholarPubMed
Gilbert, ER, Li, H, Emmerson, DA, Webb, KE and Wong, EA 2007. Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poultry Science 86, 17391753.CrossRefGoogle ScholarPubMed
Herrmann, T, Buchkremer, F, Gosch, I, Hall, AM, Bernlohr, DA and Stremmel, W 2001. Mouse fatty acid transport protein 4 (FATP4): characterization of the gene and functional assessment as a very long chain acyl-CoA synthetase. Gene 270, 3140.CrossRefGoogle ScholarPubMed
Inui, K, Quaroni, A, Tillotson, LG and Isselbacher, KJ 1980. Amino acid and hexose transport by cultured crypt cells from rat small intestine. American Journal of Physiology. Cell physiology 239, C190C196.CrossRefGoogle ScholarPubMed
James, PS, Smith, MW, Tivey, DR and Wilson, TJ 1987. Dexamethasone selectively increases sodium-dependent alanine transport across neonatal piglet intestine. The Journal of Physiology 393, 569582.CrossRefGoogle ScholarPubMed
Lei, L, Hepeng, L, Xianlei, L, Hongchao, J, Hai, L, Sheikhahmadi, A, Yufeng, W and Zhigang, S 2013. Effects of acute heat stress on gene expression of brain-gut neuropeptides in broiler chickens (Gallus gallus domesticus). Journal of Animal Science 91, 51945201.CrossRefGoogle Scholar
Lei, L, Shaohua, X, Xiaojuan, W, Hongchao, J and Hai, L 2016. Peripheral insulin doesn’t alter appetite of broiler chicks. Asian-Australasian Journal of Animal Science 29, 12941299.Google Scholar
Liu, L, Fu, CY and Li, FC 2019b. Acetate affects the process of lipid metabolism in rabbit liver, skeletal muscle and adipose tissue. Animals 9, 799.CrossRefGoogle ScholarPubMed
Liu, L, Liu, H, Ning, L and Li, F 2019a. Rabbit SLC15A1, SLC7A1 and SLC1A1 genes are affected by site of digestion, stage of development and dietary protein content. Animal, 13 326332.CrossRefGoogle ScholarPubMed
Liu, L, Shen, J, Zhao, C, Wang, X, Yao, J, Gong, Y and Yang, X 2015a. Dietary Astragalus polysaccharide alleviated immunological stress in broilers exposed to lipopolysaccharide. International Journal of Biological Macromolecules 72, 624632.CrossRefGoogle ScholarPubMed
Liu, L, Wang, X, Jiao, H, Zhao, J and Lin, H 2015b. Glucocorticoids inhibited hypothalamic target of rapamycin in high fat diet-fed chicks. Poultry Science 94, 22212227.CrossRefGoogle ScholarPubMed
Liu, L, Zhao, XY, Liu, YX, Zhao, H and Li, FC 2019c. Dietary addition of garlic straw improved the intestinal barrier in rabbits. Journal of Animal Science 97, 42484255.CrossRefGoogle Scholar
Liu, L, Zuo, WS and Li, FC 2019d. Dietary addition of Artemisia argyi reduces diarrhea and modulates the gut immune function without affecting growth performances of rabbits after weaning. Journal of Animal Science 97, 16931700.CrossRefGoogle 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, 402408.CrossRefGoogle Scholar
Lutsar, I, Friedland, IR, Jafri, HS, Wubbel, L, Ahmed, A, Trujillo, M, McCoig, CC and McCracken, GH Jr 2003. Factors influencing the anti-inflammatory effect of dexamethasone therapy in experimental pneumococcal meningitis. Journal of Antimicrobial Chemotherapy 52, 651655.CrossRefGoogle ScholarPubMed
Macfarlane, DP, Forbes, S and Walker, BR 2008. Glucocorticoids and fatty acid metabolism in humans: fuelling fat redistribution in the metabolic syndrome. Journal of Endocrinology 197, 189204.CrossRefGoogle ScholarPubMed
Manolescu, AR, Augustin, R, Moley, K and Cheeseman, C 2007. A highly conserved hydrophobic motif in the exofacial vestibule of fructose transporting SLC2A proteins acts as a critical determinant of their substrate selectivity. Molecular Membrane Biology 24, 455463.CrossRefGoogle ScholarPubMed
Miralles, VJ, Martínez-López, I, Zaragozá, R, Borrás, E, García, C, Pallardó, FV and Viña, JR 2001. Na+ dependent glutamate transporters (EAAT1, EAAT2, and EAAT3) in primary astrocyte cultures: effect of oxidative stress. Brain Research 922, 2129.CrossRefGoogle ScholarPubMed
Mochizuki, K, Takabe, S and Goda, T 2008. Changes on histone H3 modifications on the GLUT5 gene and its expression in Caco-2 cells co-treated with a p44/42 MAPK inhibitor and glucocorticoid hormone. Biochemical and Biophysical Research Communications 371, 324327.CrossRefGoogle ScholarPubMed
Mott, CR, Siegel, PB, Webb, KE Jr and Wong, EA 2008. Gene expression of nutrient transporters in the small intestine of chickens from lines divergently selected for high or low juvenile body weight. Poultry Science 87, 22152224.CrossRefGoogle ScholarPubMed
Munck, LK 1995. Chloride dependent amino acid transport in the human small intestine. Gut 36, 215219.CrossRefGoogle ScholarPubMed
Qu, H, Donkin, SS and Ajuwon, KM 2015. Heat stress enhances adipogenic differentiation of subcutaneous fat depot-derived porcine stromovascular cells. Journal of Animal Science 93, 38323842.CrossRefGoogle ScholarPubMed
Rubio-Aliaga, I and Daniel, H 2008. Peptide transporters and their roles in physiological processes and drug disposition. Xenobiotica 38, 10221042.CrossRefGoogle ScholarPubMed
Santana, P, Akana, SF, Hanson, ES, Strack, AM, Sebastian, RJ and Dallman, MF 1995. Aldosterone and dexamethasone both stimulate energy acquisition whereas only the glucocorticoid alters energy storage. Endocrinology 136, 22142222.CrossRefGoogle ScholarPubMed
Shepherd, EJ, Helliwell, PA, Mace, OJ, Morgan, EL, Patel, N and Kellett, GL 2004. Stress and glucocorticoid inhibit apical GLUT2-trafficking and intestinal glucose absorption in rat small intestine. Journal of Physiology 560, 281290.CrossRefGoogle ScholarPubMed
Solano, JM and Jacobson, L 1999. Glucocorticoids reverse leptin effects on food intake and body fat in mice without increasing NPY mRNA. American Journal of Physiology 277, 708716.Google ScholarPubMed
Song, Z, Yuan, L, Jiao, H, Lin, H 2011. Effect of corticosterone on hypothalamic corticotropin-releasing hormone expression in broiler chicks (Gallus gallus domesticus) fed a high energy diet. Asian-Australasian Journal of Animal Science 24, 17361743.CrossRefGoogle Scholar
Sun, YJ, Ni, ZH, Chen, YL, Zhang, NP and Wang, YJ 2017. Study on distribution of free amino acid and small peptide and the expression of related transporter genes in gastrointestinal tract of sheep. Acta Veterinaria et Zootechnica Sinica 48, 462473.Google Scholar
Sundaram, U, Wisel, S and Coon, S 2007. Neutral Na-amino acid cotransport is differentially regulated by glucocorticoids in the normal and chronically inflamed rabbit small intestine. American Journal of Physiology-Gastrointestinal and Liver Physiology 292, 467474.CrossRefGoogle ScholarPubMed
Sundaram, U, Wisel, S and Fromkes, JJ 1998. Unique mechanism of inhibition of Na+-amino acid, cotransport during chronic ileal inflammation. American Journal of Physiology 275, G483.Google ScholarPubMed
Wang, QW 2015. Effect of vitamin E on oxidative stress environment and placenta fatty acid transport function in GDM mice. Anhui Medical University, Anhui, China.Google Scholar
Wang, XJ, Liu, L, Zhao, JP, Jiao, HC and Lin, H 2017. Stress impairs the reproduction of laying hens: an involvement of energy. World’s Poultry Science Journal 73, 845856.CrossRefGoogle Scholar
Wright, EM, Hirayama, BA and Loo, DF 2007. Active sugar transport in health and disease. Journal of Internal Medicine 261, 3243.CrossRefGoogle ScholarPubMed
Wu, LN 2016. The influence of α-spinasterol on the expression of P-glycoprotein and PepTl on the small intestine of mice. Master thesis, Sichuan Agricultural University, Chengdu, China.Google Scholar
Yang, P, Hao, Y, Feng, J, Lin, H, Feng, Y, Wu, X, Yang, X and Gu, X 2014. The expression of carnosine and its effect on the antioxidant capacity of longissimus dorsi muscle in finishing pigs exposed to constant heat stress. Asian-Australasian Journal of Animal Sciences 27, 17631772.CrossRefGoogle ScholarPubMed
Yin, H, Sumners, LH, Dalloul, RA, Miska, KB, Fetterer, RH, Jenkins, MC, Zhu, Q and Wong, EA 2015. Changes in expression of an antimicrobial peptide, digestive enzymes, and nutrient transporters in the intestine of E. praecox-infected chickens. Poultry Science 94, 15211526.CrossRefGoogle Scholar
Zhang, XH, Jia, N, Zhao, XY, Tang, GK, Guan, LX, Wang, D, Sun, HL, Li, H and Zhu, ZL 2013. Involvement of pGluR1, EAAT2 and EAAT3 in offspring depression induced by prenatal stress. Neuroscience 250, 333341.CrossRefGoogle ScholarPubMed
Zhang, YY, Zhu, SZ, Wang, XP, Wang, CY and Li, FC 2011. The effect of dietary selenium levels on the growth performance, antioxidant capacity and glutathione peroxidase 1 (GSHPx1) mRNA expression in growing meat rabbits. Animal Feed Science and Technology 169, 259264.CrossRefGoogle Scholar
Zhao, JP, Bao, J, Wang, XJ, Jiao, HC, Song, ZG and Lin, H 2012. Altered gene and protein expression of glucose transporter1 underlies dexamethasone inhibition of insulin-stimulated glucose uptake in chicken muscles. Journal of Animal Science 90, 43374345.CrossRefGoogle ScholarPubMed
Zheng, L, Wei, H, Yu, H, Xing, Q, Zou, Y, Zhou, Y and Peng, J 2018. Fish skin gelatin hydrolysate production by ginger powder induces glutathione synthesis to prevent hydrogen peroxide induced intestinal oxidative stress via the Pept1-p62-Nrf2 cascade. Journal of Agricultural and Food Chemistry 66, 1160111611.CrossRefGoogle ScholarPubMed
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