Asian-Australasian Journal of Animal Sciences

  • 제31권4호
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  • Pages.548-555
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  • 2018
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  • 1011-2367(pISSN)
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  • 1976-5517(eISSN)
아세아태평양축산학회 (Asian Australasian Association of Animal Production Societies)
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The effect of dietary asparagine supplementation on energy metabolism in liver of weaning pigs when challenged with lipopolysaccharide

  • Kang, Ping (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Liu, Yulan (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Zhu, Huiling (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Zhang, Jing (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Shi, Haifeng (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Li, Shuang (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Pi, Dinan (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Leng, Weibo (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Wang, Xiuying (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Wu, Huanting (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Hou, Yongqing (Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University)
  • 투고 : 2017.06.03
  • 심사 : 2017.10.22
  • 발행 : 2018.04.01
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초록

Objective: This experiment was conducted to investigate whether asparagine (Asn) could improve liver energy status in weaning pigs when challenged with lipopolysaccharide. Methods: Forty-eight weaned pigs ($Duroc{\times}Large\;White{\times}Landrace$, $8.12{\pm}0.56kg$) were assigned to four treatments: i) CTRL, piglets received a control diet and injected with sterile 0.9% NaCl solution; ii) lipopolysaccharide challenged control (LPSCC), piglets received the same control diet and injected with Escherichia coli LPS; iii) lipopolysaccharide (LPS)+0.5% Asn, piglets received a 0.5% Asn diet and injected with LPS; and iv) LPS+1.0% Asn, piglets received a 1.0% Asn diet and injected with LPS. All piglets were fed the experimental diets for 19 d. On d 20, the pigs were injected intraperitoneally with Escherichia coli LPS at $100{\mu}g/kg$ body weights or the same volume of 0.9% NaCl solution based on the assigned treatments. Then the pigs were slaughtered at 4 h and 24 h after LPS or saline injection, and the liver samples were collected. Results: At 24 h after LPS challenge, dietary supplementation with 0.5% Asn increased ATP concentration (quadratic, p<0.05), and had a tendency to increase adenylate energy charges and reduce AMP/ATP ratio (quadratic, p<0.1) in liver. In addition, Asn increased the liver mRNA expression of pyruvate kinase, pyruvate dehydrogenase, citrate synthase, and isocitrate dehydrogenase ${\beta}$ (linear, p<0.05; quadratic, p<0.05), and had a tendency to increase the mRNA expression of hexokinase 2 (linear, p<0.1). Moreover, Asn increased liver phosphorylated AMP-activated protein kinase (pAMPK)/total AMP-activated protein kinase (tAMPK) ratio (linear, p<0.05; quadratic, p<0.05). However, at 4 h after LPS challenge, Asn supplementation had no effect on these parameters. Conclusion: The present study indicated that Asn could improve the energy metabolism in injured liver at the late stage of LPS challenge.

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참고문헌

  1. Crosby LO, Cline TR. Effect of asparagine on growth and protein synthesis in weanling rats. J Anim Sci 1973;37:713-7. https://doi.org/10.2527/jas1973.373713x
  2. Rhoads JM, Argenzio RA, Chen W, Gomez GG. Asparagine stimulates piglet intestinal Cl- secretion by a mechanism requiring a submucosal glutamate receptor and nitric oxide. J Pharmacol Exp Ther 1995;274:404-12.
  3. Kandil HM, Argenzio RA, Chen W, et al. L-glutamine and L-asparagine stimulate ODC activity and proliferation in a porcine jejunal enterocyte line. Am J Physiol 1995;269:G591-9.
  4. Ray RM, Viar MJ, Patel TB, Johnson LR. Interaction of asparagine and EGF in the regulation of ornithine decarboxylase in IEC-6 cells. Am J Physiol 1999;276:G773-80.
  5. Milman HA, Cooney DA, Huang CY. Studies on the mechanism of the glutamine-dependent reaction catalyzed by asparagine synthetase from mouse pancreas. J Biol Chem 1980;255: 1862-6.
  6. Avramis Vi, Panosyan EH. Pharmacokinetic/pharmacodynamic relationships of asparaginase formulations: the past, the present and recommendations for the future. Clin Pharmacokinet 2005;44:367-93. https://doi.org/10.2165/00003088-200544040-00003
  7. Balasubramanian MN, Butterworth EA, Kilberg MS. Asparagine synthetase: regulation by cell stress and involvement in tumor biology. Am J Physiol Endocrinol Metab 2013;304:E789-99. https://doi.org/10.1152/ajpendo.00015.2013
  8. Milman HA, Cooney DA. Partial purification and properties of L-asparagine synthetase from mouse pancreas. Biochem J 1979;181:51-9. https://doi.org/10.1042/bj1810051
  9. Viollet B, Foretz M, Guigas B, et al. Activation of AMP-activated protein kinase in the liver: a new strategy for the management of metabolic hepatic disorders. J Physiol 2006;574:41-53. https://doi.org/10.1113/jphysiol.2006.108506
  10. Masaki T, Chiba S, Tatsukawa H, et al. Adiponectin protects LPS-induced liver injury through modulation of TNF-${\alpha}$ in KK-Ay obese mice. Hepatology 2004;40:177-84.
  11. Alipour M, Omri A, Smith MG, Suntres ZE. Prophylactic effect of liposomal N-acetylcysteine against LPS-induced liver injuries. J Endotoxin Res 2007;13:297-304. https://doi.org/10.1177/0968051907085062
  12. Xu L, Scheenen WJ, Roubos EW, Kozicz T. Peptidergic Edinger- Westphal neurons and the energy-dependent stress response. Gen Comp Endocrinol 2012;177: 296-304. https://doi.org/10.1016/j.ygcen.2011.11.039
  13. Kang P, Liu Y, Zhu H, et al. The effect of aspartate on the energy metabolism in the liver of weanling pigs challenged with lipopolysaccharide. Eur J Nutr 2015;54:581-8. https://doi.org/10.1007/s00394-014-0739-3
  14. Li S, Liu YL, Shi HF, et al Effect of asparagine acid on growth performance, blood cell differential count, and blood biochemical measurements of weaned piglets after lipopolysaccharide challenge. Chinese J Anim Nutr 2012;24:2450-8.
  15. NRC. Nutrient requirements of swine. 11th edition. Washington, DC, USA: National Academic Press; 2012.
  16. Hou Y, Yao K, Wang L, et al. Effects of ${\alpha}$-ketoglutarate on energy status in the intestinal mucosa of weaned piglets chronically challenged with lipopolysaccharide. Br J Nutr 2011;106:357-63. https://doi.org/10.1017/S0007114511000249
  17. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and $2^{-{\Delta}{\Delta}CT}$ method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  18. Zielke HR, Zielke CL, Ozand PT. Glutamine: a major energy source for cultured mammalian cells. Fed Proc 1984;43:121-5.
  19. Scaraffia PY, Wells MA. Proline can be utilized as an energy substrate during flight of Aedes aegypti females. J Insect Physiol 2003;49:591-601. https://doi.org/10.1016/S0022-1910(03)00031-3
  20. Andrade VS, Rojas DB, de Andrade RB, et al. A possible antiinflammatory effect of proline in the brain cortex and cerebellum of rats. Mol Neurobiol 2017 Jun 5 [Epub]. https:/doi.org/10.1007/s12035-017-0626-z
  21. Hristina K, Langerholc T, Trapecar M. Novel metabolic roles of L-arginine in body energy metabolism and possible clinical applications. J Nutr Health Aging 2014;18:213-8. https://doi.org/10.1007/s12603-014-0015-5
  22. Pi D, Liu Y, Shi H, et al. Dietary supplementation of aspartate enhances intestinal integrity and energy status in weanling piglets after lipopolysaccharide challenge. J Nutr Biochem 2014;25:456-62. https://doi.org/10.1016/j.jnutbio.2013.12.006
  23. Yi D, Hou Y, Wang L, et al. Dietary N-acetylcysteine supplementation alleviates liver injury in lipopolysaccharide-challenged piglets. Br J Nutr 2014;111:46-54. https://doi.org/10.1017/S0007114513002171
  24. Ray RM, Viar MJ, Johnson LR. Amino acids regulate expression of antizyme-1 to modulate ornithine decarboxylase activity. J Biol Chem 2012;287:3674-90.
  25. Fausto N. The control of ornithine decarboxylase activity during liver regeneration. Biochim Biophys Acta 1971;238:116-28. https://doi.org/10.1016/0005-2787(71)90015-3
  26. Pirinen E, Kuulasmaa T, Pietila M, et al. Enhanced polyamine catabolism alters homeostatic control of white adipose tissue mass, energy expenditure, and glucose metabolism. Mol Cell Biol 2007;27:4953-67. https://doi.org/10.1128/MCB.02034-06
  27. Soboll S. Regulation of energy metabolism in liver. J Bioenerg Biomembr 1995;27:571-82. https://doi.org/10.1007/BF02111655
  28. Wang J, Li GR, Tan BE, et al. Oral administration of putrescine and proline during the suckling period improves epithelial restitution after early weaning in piglets. J Anim Sci 2015;93: 1679-88.
  29. Furuya E, Uyeda K. An activation factor of liver phosphofructokinase. Proc Nati Acad Sci USA 1980;77:5861-4. https://doi.org/10.1073/pnas.77.10.5861
  30. Reinhart GD, Lardy HA. Rat liver phosphofructokinase: kinetic activity under near-physiological conditions. Biochemistry 1980;19:1477-84. https://doi.org/10.1021/bi00548a034
  31. Zanella A, Fermo E, Bianchi P, Valentini G. Red cell pyruvate kinase deficiency: molecular and clinical aspects. Br J Haematol 2005;130:11-25. https://doi.org/10.1111/j.1365-2141.2005.05527.x
  32. Roy MF, Riendeau N, Bedard C, et al. Pyruvate kinase defi ciency confers susceptibility to Salmonella typhimurium infection in mice. J Exp Med 2007;204:2949-61. https://doi.org/10.1084/jem.20062606
  33. Zhang J, Fan J, Venneti S, et al. Asparagine plays a critical role in regulating cellular adaptation to glutamine depletion. Mol Cell 2014;56:205-18.
  34. Schanbacher FL, Willett LB, Moorhead PD. Ornithine decarboxylase, serum isocitrate dehydrogenase and clinical chemisty changes during thioacetamide-induced hepatotoxicity in a calf. J Anim Sci 1981;53:1658-70. https://doi.org/10.2527/jas1982.5361658x
  35. Kahn BB, Alquier T, Carling D, Hardie DG. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell. Metab 2005;1:15-25. https://doi.org/10.1016/j.cmet.2004.12.003
  36. Stein SC, Woods A, Jones NA, Davison MD, Carling D. The regulation of AMP-activated protein kinase by phosphorylation. Biochem J 2000;345:437-43. https://doi.org/10.1042/bj3450437
  37. Merrill JF, Thomson DM, Hardman SE, et al. Iron deficiency causes a shift in AMP-activated protein kinase (AMPK) subunit composition in rat skeletal muscle. Nutr Metab (Lond) 2012;9:104. https://doi.org/10.1186/1743-7075-9-104
  38. Wang XY, Liu YL, Li S, et al. Asparagine attenuates intestinal injury, improves energy status and inhibits AMP-activated protein kinase signalling pathways in weaned piglets challenged with Escherichia coli lipopolysaccharide. Br J Nutr 2015; 114:553-65. https://doi.org/10.1017/S0007114515001877
  39. Wu HT, Liu YL, Pi DA, et al. Asparagine attenuates hepatic injury caused by lipopolysaccharide in weaned piglets associated with modulation of Toll-like receptor 4 and nucleotidebinding oligomerisation domain protein signalling and their negative regulators. Br J Nutr 2015;114:189-201. https://doi.org/10.1017/S0007114515001476

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