Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T12:43:33.807Z Has data issue: false hasContentIssue false
  • English
  • Français

Leucine regulates α-amylase and trypsin synthesis in dairy calf pancreatic tissue in vitro via the mammalian target of rapamycin signalling pathway

Published online by Cambridge University Press:  08 January 2019

L. Guo ,
J. H. Yao ,
C. Zheng ,
H. B. Tian ,
Y. L. Liu ,
S. M. Liu ,
C. J. Cai ,
X. R. Xu  and
Y. C. Cao Open the ORCID record for Y. C. Cao [Opens in a new window]
L. Guo
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, People’s Republic of China
J. H. Yao
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, People’s Republic of China
C. Zheng
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, People’s Republic of China
H. B. Tian
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, People’s Republic of China
Y. L. Liu
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, People’s Republic of China
S. M. Liu
Affiliation:
School of Animal Biology, University of Western Australia, Crawley, WA 6009, Australia
C. J. Cai
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, People’s Republic of China
X. R. Xu
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, People’s Republic of China
Y. C. Cao*
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, People’s Republic of China
*
†E-mail: [email protected]
Get access

Abstract

Starch digestion in the small intestines of the dairy cow is low, to a large extent, due to a shortage of syntheses of α-amylase. One strategy to improve the situation is to enhance the synthesis of α-amylase. The mammalian target of rapamycin (mTOR) signalling pathway, which acts as a central regulator of protein synthesis, can be activated by leucine. Our objectives were to investigate the effects of leucine on the mTOR signalling pathway and to define the associations between these signalling activities and the synthesis of pancreatic enzymes using an in vitro model of cultured Holstein dairy calf pancreatic tissue. The pancreatic tissue was incubated in culture medium containing l-leucine for 3 h, and samples were collected hourly, with the control being included but not containing l-leucine. The leucine supplementation increased α-amylase and trypsin activities and the messenger RNA expression of their coding genes (P <0.05), and it enhanced the mTOR synthesis and the phosphorylation of mTOR, ribosomal protein S6 kinase 1 and eukaryotic initiation factor 4E-binding protein 1 (P <0.05). In addition, rapamycin inhibited the mTOR signal pathway factors during leucine treatment. In sum, the leucine regulates α-amylase and trypsin synthesis in dairy calves through the regulation of the mTOR signal pathways.

Keywords

leucinemammalian target of rapamycindigestive enzymespancreas
Type
Research Article
Information
animal , Volume 13 , Issue 9 , September 2019 , pp. 1899 - 1906
Copyright
© The Animal Consortium 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anonymous 1976. Adaptive responses of amino acid degrading enzymes to variation of amino acid and protein intake. Nutrition Reviews 34, 343–345.Google Scholar
Appuhamy, JA, Knoebel, NA, Nayananjalie, WA, Escobar, J and Hanigan, MD 2012. Isoleucine and leucine independently regulate mTOR signaling and protein synthesis in MAC-T cells and bovine mammary tissue slices. Journal of Nutrition 142, 484–491.CrossRefGoogle ScholarPubMed
Arriola Apelo, SI, Singer, LM, Lin, XY, McGilliard, ML, St-Pierre, NR and Hanigan, MD 2014. Isoleucine, leucine, methionine, and threonine effects on mammalian target of rapamycin signaling in mammary tissue. Journal of Dairy Science 97, 1047–1056.CrossRefGoogle ScholarPubMed
Averous, J, Lambert-Langlais, S, Carraro, V, Gourbeyre, O, Parry, L, B’Chir, W, Muranishi, Y, Jousse, C, Bruhat, A, Maurin, AC, Proud, CG and Fafournoux, P 2014. Requirement for lysosomal localization of mTOR for its activation differs between leucine and other amino acids. Cell Signal 26, 1918–1927.CrossRefGoogle ScholarPubMed
Brannon, PM 1990. Adaptation of the exocrine pancreas to diet. Annual Review of Nutrition 10, 85–105.CrossRefGoogle Scholar
Budanov, A and Karin, M 2008. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134, 451–460.CrossRefGoogle ScholarPubMed
Byfield, MP, Murray, JT and Backer, JM 2005. hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. Journal of Biological Chemistry 280, 33076–33082.CrossRefGoogle ScholarPubMed
Cao, YC, Yang, XJ, Guo, L, Zheng, C, Wang, DD, Cai, CJ, Liu, SM and Yao, JH 2018. Effects of dietary leucine and phenylalanine on pancreas development, enzyme activity, and relative gene expression in milk-fed Holstein dairy calves. Journal Dairy Science 101, 1–10.CrossRefGoogle ScholarPubMed
Guba, M, von Breitenbuch, P, Steinbauer, M, Koehl, G, Flegel, S, Hornung, M, Bruns, CJ, Zuelke, C, Farkas, S, Anthuber, M, Jauch, KW and Geissler, EK 2002. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor. Nature Medicine 8, 128.CrossRefGoogle ScholarPubMed
Guo, L, Liang, ZQ, Zheng, C, Liu, BL, Yin, QY, Cao, YC and Yao, JH 2018. Leucine affects amylase synthesis through PI3K/Akt-mTOR signaling pathways in pancreatic acinar cells of dairy calves. Journal of Agricultural and Food Chemistry 66, 5149–5156.CrossRefGoogle ScholarPubMed
Harmon, DL 1992. Dietary influences on carbohydrases and small intestinal starch hydrolysis capacity in ruminants. Journal of Nutrition 122, 203–210.CrossRefGoogle ScholarPubMed
Harper, AE, Benton, DA and Elvehjem, CA 1955. l-Leucine, an isoleucine antagonist in the rat. Archives of Biochemistry and Biophysics 57, 1–12.CrossRefGoogle ScholarPubMed
Holz, MK, Ballif, BA, Gygi, SP and Blenis, J 2005. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123, 569–580.CrossRefGoogle ScholarPubMed
Huntington, GB, Harmon, DL and Richards, CJ 2006. Sites, rates, and limits of starch digestion and glucose metabolism in growing cattle. Journal of Animal Science 84, E14–24.CrossRefGoogle ScholarPubMed
Jiang, W, Zhu, Z and Thompson, HJ 2008. Dietary energy restriction modulates the activity of AMPK, Akt, and mTOR in mammary carcinomas, mammary gland, and liver. Cancer Research 68, 5492–5499.CrossRefGoogle ScholarPubMed
Ju, HG and Chang, KK 2015. Effects of different doses of leucine ingestion following eight weeks of resistance exercise on protein synthesis and hypertrophy of skeletal muscle in rats. Journal of Exercise Nutrition & Biochemistry 19, 31–38.Google Scholar
Katoh, K and Tsuda, T 1984. Effects of acetylcholine and shortchain fatty acids on acinar cells of the exocrine pancreas in sheep. Journal of Physiology 356, 479–489.CrossRefGoogle Scholar
Katoh, K and Yajima, T 1989. Effects of butyric acid and analogues on amylase release from pancreatic segments of sheep and goats. Pflugers Archiv-European Journal of Physiology 413, 256–260.CrossRefGoogle ScholarPubMed
Kimball, SR and Jefferson, LS 2004. Regulation of global and specific mRNA translation by oral administration of branched-chain amino acids. Biochemical and Biophysical Research Communications 313, 423–427.CrossRefGoogle ScholarPubMed
Kimball, SR and Jefferson, LS 2006. New functions for amino acid: effects on gene transcription and translation. American Journal of Clinical Nutrition 83, 500–507.CrossRefGoogle ScholarPubMed
Lang, CH, Frost, RA, Deshpande, N, Kumar, V, Vary, TC, Jefferson, LS and Kimball, SR 2003. Alcohol impairs leucine-mediated phosphorylation of 4E-BP1, S6K1, eIF4G, and mTOR in skeletal muscle. American Journal of Physiology-Endocrinology and Metabolism 285, 1205–1215.CrossRefGoogle ScholarPubMed
Layman, DK and Walker, DA 2006. Potential importance of leucine in treatment of obesity and the metabolic syndrome. Journal of Nutrition 136, 319–323.CrossRefGoogle ScholarPubMed
Liu, K, Liu, Y, Liu, SM, Xu, M, Yu, ZP, Wang, X, Cao, YC and Yao, JH 2015. Relationships between leucine and the pancreatic exocrine function for improving starch digestibility in ruminants. Journal of Dairy Science 98, 2576–2582.CrossRefGoogle ScholarPubMed
Mackle, TR, Dwyer, DA, Ingvartsen, KL, Chouinard, PY, Ross, DA and Bauman, DE 2000. Effects of insulin and postruminal supply of protein on use of amino acids by the mammary gland for milk protein synthesis. Journal of Dairy Science 83, 93–105.CrossRefGoogle ScholarPubMed
Meyuhas, O 2000. Synthesis of the translational apparatus is regulated at the translational level. European Journal of Biochemistry 267, 6321–6330.CrossRefGoogle ScholarPubMed
Owens, FN, Zinn, RA and Kim, YK 1986. Limits to starch digestion in the ruminant small intestine. Journal of Animal Science 63, 1634–1648.CrossRefGoogle ScholarPubMed
Phung, TL, Ziv, K, Dabydeen, D, Eyiah-Mensah, G, Riveros, M, Perruzzi, C, Sun, J, Monahan-Earley, RA, Shiojima, I, Nagy, JA, Lin, MI, Walsh, K, Dvorak, AM, Briscoe, DM, Neeman, M, Sessa, WC, Dvorak, HF and Benjamin, LE 2006. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10, 159–170.CrossRefGoogle ScholarPubMed
Raman, N, Nayak, A and Muller, S 2014. mTOR signaling regulates nucleolar targeting of the SUMO-specific isopeptidase SENP3. Molecular & Cellular Biology 34, 4474–4484.CrossRefGoogle ScholarPubMed
Richards, CJ, Branco, AF, Bohnert, DW, Huntington, GB, Macari, M and Harmon, DL 2002. Intestinal starch disappearance increased in steers abomasally infused with starch and protein. Journal of Animal Science 80, 3361–3368.CrossRefGoogle Scholar
Soulard, A and Hall, MN 2007. SnapShot: mTOR signaling. Cell 129, 434.CrossRefGoogle ScholarPubMed
Sugawara, T, Ito, Y, Nishizawa, N and Nagasawa, T 2009. Regulation of muscle protein degradation, not synthesis, by dietary leucine in rats fed a protein-deficient diet. Amino Acids 37, 609–616.CrossRefGoogle Scholar
Swanson, KC, Matthews, JC, Matthews, AD, Howell, JA, Richards, CJ and Harmon, DL 2000. Dietary carbohydrate source and energy intake influence the expression of pancreatic alpha-amylase in lambs. Journal of Nutrition 130, 2157–2165.CrossRefGoogle ScholarPubMed
Swanson, KC, Matthews, JC, Woods, CA and Harmon, DL 2002. Influence of substrate and/or neurohormonal mimic on in vitro pancreatic enzyme release from calves’ postruminally infused with partially hydrolyzed starch and/or casein. Journal of Animal Science 81, 1323–1331.CrossRefGoogle Scholar
Wang, X and Proud, CG. 2006. The mTOR pathway in the control of protein synthesis. Physiology 21, 362–369.CrossRefGoogle ScholarPubMed
Wolfson, RL, Chantranupong, L, Saxton, RA, Shen, K, Scaria, SM, Cantor, JR and Sabatini, DM 2016. Sestrin2 is a leucine sensor for the mTORC1 pathway. Science 351, 43–48.CrossRefGoogle ScholarPubMed
Wu, G 2013. Functional amino acids in nutrition and health. Amino Acids 45, 407–411.CrossRefGoogle ScholarPubMed
Wu, G. 2014. Amino acid nutrition in animals: protein synthesis and beyond. Annual Review of Animal Bioscience 2, 387.CrossRefGoogle ScholarPubMed
Yu, ZP, Xu, M, Liu, K, Yao, JH, Yu, HX and Wang, F. 2014. Leucine markedly regulates pancreatic exocrine secretion in goats. Journal of Animal Physiology and Animal Nutrition 98, 169–177.CrossRefGoogle ScholarPubMed
Supplementary material: File

Guo et al. supplementary material

Guo et al. supplementary material 1

Download Guo et al. supplementary material(File)
File 20.9 KB