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Effects of dietary energy sources on early postmortem muscle metabolism of finishing pigs

  • Li, Yanjiao (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University) ;
  • Yu, Changning (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University) ;
  • Li, Jiaolong (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University) ;
  • Zhang, Lin (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University) ;
  • Gao, Feng (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University) ;
  • Zhou, Guanghong (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Nanjing Agricultural University)
  • Received : 2017.02.11
  • Accepted : 2017.05.22
  • Published : 2017.12.01

Abstract

Objective: This study investigated the effects of different dietary energy sources on early postmortem muscle metabolism of finishing pigs. Methods: Seventy-two barrow ($Duroc{\times}Landrace{\times}Yorkshire$, DLY) pigs ($65.0{\pm}2.0kg$) were allotted to three iso-energetic and iso-nitrogenous diets: A (44.1% starch, 5.9% crude fat, and 12.6% neutral detergent fibre [NDF]), B (37.6% starch, 9.5% crude fat, and 15.4% NDF) or C (30.9% starch, 14.3% crude fat, and 17.8% NDF). After the duration of 28-day feeding experiment, 24 pigs (eight per treatment) were slaughtered and the M. longissimus lumborum (LL) samples at 45 min postmortem were collected. Results: Compared with diet A, diet C resulted in greater adenosine triphosphate and decreased phosphocreatine (PCr) concentrations, greater activity of creatine kinase and reduced percentage bound activities of hexokinase (HK), and pyruvate kinase (PK) in LL muscles (p<0.05). Moreover, diet C decreased the phosphor-AKT level and increased the hydroxy-hypoxia-inducible $factor-1{\alpha}$ ($HIF-1{\alpha}$) level, as well as decreased the bound protein expressions of HK II, PKM2, and lactate dehydrogenase A (p<0.05). Conclusion: Diet C with the lowest level of starch and the highest levels of fat and NDF could enhance the PCr utilization and attenuate glycolysis early postmortem in LL muscle of finishing pigs.

Keywords

References

  1. Scheffler TL, Gerrard DE. Mechanisms controlling pork quality development: The biochemistry controlling postmortem energy metabolism. Meat Sci 2007;77:7-16. https://doi.org/10.1016/j.meatsci.2007.04.024
  2. Henckel P, Karlsson A, Jensen MT, Oksbjerg N, Petersen JS. Metabolic conditions in porcine longissimus muscle immediately pre-slaughter and its influence on peri-and post mortem energy metabolism. Meat Sci 2002;62:145-55. https://doi.org/10.1016/S0309-1740(01)00239-X
  3. Bendall JR. The shortening of rabbit muscles during rigor mortis: its relation to the breakdown of adenosine triphosphate and creatine phosphate and to muscular contraction. J Physiol 1951;114:71-88.
  4. Parra J, Pette D. Effects of low-frequency stimulation on soluble and structure-bound activities of hexokinase and phosphofructokinase in rat fast-twitch muscle. Biochim Biophys Acta 1995;1251:154-60. https://doi.org/10.1016/0167-4838(95)00084-8
  5. Lushchak VI. Interaction of lactate dehydrogenase with structural cell components: possible physiological significance. Biokhimiia 1992;57:1142-54.
  6. Forlemu NY. Waingeh VF, Ouporov IV, Lowe SL, Thomasson KA. Theoretical study of interactions between muscle aldolase and F‐actin: Insight into different species. Biopolymers 2007;85:60-71. https://doi.org/10.1002/bip.20611
  7. Semenza GL, Roth PH, Fang H-M, Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 1994;269:23757-63.
  8. Mason SD, Howlett RA, Kim MJ, et al. Loss of skeletal muscle HIF-$1{\alpha}$ results in altered exercise endurance. PLoS Biol 2004;2:e288. https://doi.org/10.1371/journal.pbio.0020288
  9. Dekanty A, Lavista-Llanos S, Irisarri M, Oldham S, Wappner P. The insulin-PI3K/TOR pathway induces a HIF-dependent transcriptional response in Drosophila by promoting nuclear localization of HIF-${\alpha}$/Sima. J Cell Sci 2005;118:5431-41. https://doi.org/10.1242/jcs.02648
  10. Jaakkola P, Mole DR, Tian Y-M, et al. Targeting of HIF-${\alpha}$ to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001;292:468-72. https://doi.org/10.1126/science.1059796
  11. Wu R, Smeele KM, Wyatt E, et al. Reduction in hexokinase II levels results in decreased cardiac function and altered remodeling after ischemia/reperfusion InjuryNovelty and significance. Circ Res 2011;108:60-9. https://doi.org/10.1161/CIRCRESAHA.110.223115
  12. Gottlob K, Majewski N, Kennedy S, et al. Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev 2001;15:1406-18. https://doi.org/10.1101/gad.889901
  13. Weidemann A, Breyer J, Rehm M, et al. HIF-$1{\alpha}$ activation results in actin cytoskeleton reorganization and modulation of Rac-1 signaling in endothelial cells. J Cell Commun Signal 2013;11:80. https://doi.org/10.1186/1478-811X-11-80
  14. Bereiter-Hahn J, Stübig C, Heymann V. Cell cycle-related changes in F-actin distribution are correlated with glycolytic activity. Exp Cell Res 1995;218:551-60. https://doi.org/10.1006/excr.1995.1190
  15. Chen JX, Stinnett A. Ang-1 gene therapy inhibits hypoxia-inducible factor-1alpha (HIF-1alpha)-prolyl-4-hydroxylase-2, stabilizes HIF-1alpha expression, and normalizes immature vasculature in db/db mice. Diabetes 2008;57:3335-43. https://doi.org/10.2337/db08-0503
  16. Li Y, Li J, Zhang L, et al. Effects of dietary energy sources on post mortem glycolysis, meat quality and muscle fibre type transformation of finishing pigs. PLoS One 2015;10:e0131958. https://doi.org/10.1371/journal.pone.0131958
  17. Ferguson D, Gerrard D. Regulation of post-mortem glycolysis in ruminant muscle. Anim Prod Sci 2014;54:464-81. https://doi.org/10.1071/AN13088
  18. Committee on Nutrient Requirements of Swine, National Research Council. Nutrient requirements of swine. 11th ed. Washington, DC, USA: National Academy Press; 2012.
  19. Wang S, Li C, Xu X, Zhou G. Effect of fasting on energy metabolism and tenderizing enzymes in chicken breast muscle early postmortem. Meat Sci 2013;93:865-72. https://doi.org/10.1016/j.meatsci.2012.11.053
  20. Zhang L, Yue H, Wu S, et al. Transport stress in broilers. II. Superoxide production, adenosine phosphate concentrations, and mRNA levels of avian uncoupling protein, avian adenine nucleotide translocator, and avian peroxisome proliferator-activated receptor-${\gamma}$ coactivator-$1{\alpha}$ in skeletal muscles. Poult Sci 2010;89:393-400. https://doi.org/10.3382/ps.2009-00281
  21. Liu Y, Li J, Li Y, et al. Effects of dietary supplementation of guanidinoacetic acid and combination of guanidinoacetic acid and betaine on postmortem glycolysis and meat quality of finishing pigs. Anim Feed Sci Technol 2015;205:82-9. https://doi.org/10.1016/j.anifeedsci.2015.03.010
  22. Clarke FM, Shaw FD, Morton DJ. Effect of electrical stimulation post mortem of bovine muscle on the binding of glycolytic enzymes. Biochem J 1980;186:105-9. https://doi.org/10.1042/bj1860105
  23. Lametsch R, Essen-Gustavsson B, Jensen-Waern M, Lundstrom K, Lindahl G. Postmortem changes in phosphorylation of metabolic enzymes in relation to the RN-genotype. In: 55th ICoMST; 2009.
  24. Westerblad H, Bruton JD, Katz A. Skeletal muscle: energy metabolism, fiber types, fatigue and adaptability. Exp Cell Res 2010;316:3093-9. https://doi.org/10.1016/j.yexcr.2010.05.019
  25. Odland LM, Heigenhauser GJ, Wong D, Hollidge-Horvat MG, Spriet LL. Effects of increased fat availability on fat-carbohydrate interaction during prolonged exercise in men. Am J Physiol Regul Integr Comp Physiol 1998;274:R894-R902. https://doi.org/10.1152/ajpregu.1998.274.4.R894
  26. Wilmore JH, Costill DL. Physiology of sport and exercise. 3nd edn. Champaign, IL: Human Kinetics; 2005. pp. 116-45.
  27. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004;4:891-9. https://doi.org/10.1038/nrc1478
  28. Zhao J, Zhao G, Jiang R, et al. Effects of diet-induced differences in growth rate on metabolic, histological, and meat-quality properties of 2 muscles in male chickens of 2 distinct broiler breeds. Poult Sci 2012;91:237-47. https://doi.org/10.3382/ps.2011-01667
  29. Ribeiro W, Valberg S, Pagan J, Gustavsson B. The effect of varying dietary starch and fat content on serum creatine kinase activity and substrate availability in equine polysaccharide storage myopathy. J Vet Intern Med 2004;18:887-94. https://doi.org/10.1111/j.1939-1676.2004.tb02637.x
  30. Van de Moortel L, Speeckaert MM, Fiers T, et al. Low serum creatine kinase activity is associated with worse outcome in critically ill patients. J Crit Care 2014;29:786-90. https://doi.org/10.1016/j.jcrc.2014.03.010
  31. Boden G, Shulman G. Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and ${\beta}$-cell dysfunction. Eur J Clin Invest 2002;32:14-23. https://doi.org/10.1046/j.1365-2362.32.s3.3.x
  32. Yu C, Li Y, Zhang B, et al. Suppression of mTOR signaling pathways in skeletal muscle of finishing pigs by increasing the ratios of ether extract and neutral detergent fiber at the expense of starch in isoenergetic diets. J Agric Food Chem 2016;64:1557-64. https://doi.org/10.1021/acs.jafc.5b06089
  33. Borges P, Valente LM, Veron V, et al. High dietary lipid level is associated with persistent hyperglycaemia and downregulation of muscle Akt-mTOR pathway in Senegalese sole (Solea senegalensis). PLoS One 2014;9:e102196. https://doi.org/10.1371/journal.pone.0102196
  34. Semenza GL. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 2010;29:625-34. https://doi.org/10.1038/onc.2009.441
  35. Silva APP, Alves GG, Araujo AH, Sola-Penna M. Effects of insulin and actin on phosphofructokinase activity and cellular distribution in skeletal muscle. An Acad Bras Cienc 2004;76:541-8. https://doi.org/10.1590/S0001-37652004000300008
  36. Storey KB. Anoxia tolerance in turtles: metabolic regulation and gene expression. Comp Biochem Physiol Part A Mol Integr Physiol 2007;147:263-76. https://doi.org/10.1016/j.cbpa.2006.03.019

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