Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Choline supplementation improves the lipid metabolism of intrauterine-growth-restricted pigs

  • Li, Wei (College of Animal Science and Technology, Nanjing Agricultural University (NJAU)) ;
  • Li, Bo (College of Animal Science and Technology, Nanjing Agricultural University (NJAU)) ;
  • Lv, Jiaqi (College of Animal Science and Technology, Nanjing Agricultural University (NJAU)) ;
  • Dong, Li (College of Animal Science and Technology, Yangzhou University) ;
  • Zhang, Lili (College of Animal Science and Technology, Nanjing Agricultural University (NJAU)) ;
  • Wang, Tian (College of Animal Science and Technology, Nanjing Agricultural University (NJAU))
  • Received : 2015.09.30
  • Accepted : 2016.05.19
  • Published : 2018.05.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: The objective of this study was to investigate the effects of dietary choline supplementation on hepatic lipid metabolism and gene expression in finishing pigs with intrauterine growth retardation (IUGR). Methods: Using a $2{\times}2$ factorial design, eight normal birth weight (NBW) and eight IUGR weaned pigs were fed either a basal diet (NBW pigs fed a basal diet, NC; IUGR pigs fed a basal diet, IC) or a diet supplemented with two times more choline than the basal diet (NBW pigs fed a high-choline diet, NH; IUGR pigs fed a high-choline diet, IH) until 200 d of age. Results: The results showed that the IUGR pigs had reduced body weight compared with the NBW pigs (p<0.05 from birth to d 120; p = 0.07 from d 120 to 200). Increased (p<0.05) free fatty acid (FFA) and triglyceride levels were observed in the IUGR pigs compared with the NBW pigs. Choline supplementation decreased (p<0.05) the levels of FFAs and triglycerides in the serum of the pigs. The activities of malate dehydrogenase and glucose 6-phosphate dehydrogenase were both increased (p<0.05) in the livers of the IUGR pigs. Choline supplementation decreased (p<0.05) malate dehydrogenase activity in the liver of the pigs. Gene expression of fatty acid synthase (FAS) was higher (p<0.05) in the IC group than in the other groups, and choline supplementation decreased (p<0.05) FAS and acetyl-CoA carboxylase ${\alpha}$ expression in the livers of the IUGR pigs. The expression of carnitine palmitoyl transferase 1A (CPT1A) was lower (p<0.05) in the IC group than in the other groups, and choline supplementation increased (p<0.05) the expression of CPT1A in the liver of the IUGR pigs and decreased (p<0.01) the expression of hormone-sensitive lipase in both types of pigs. The gene expression of phosphatidylethanolamine N-methyltransferase (PEMT) was higher (p<0.05) in the IC group than in the other groups, and choline supplementation significantly reduced (p<0.05) PEMT expression in the liver of the IUGR pigs. Conclusion: In conclusion, the lipid metabolism was abnormal in IUGR pigs, but the IUGR pigs consuming twice the normal level of choline had improved circulating lipid parameters, which could be related to the decreased activity of nicotinamide adenine dinucleotide phosphate-generating enzymes or the altered expressions of lipid metabolism-related genes.

Keywords

References

  1. Wang T, Huo YJ, Shi F, Xu RJ, Hutz RJ. Effects of intrauterine growth retardation on development of the gastrointestinal tract in neonatal pigs. Biol Neonate 2005;88:66-72. https://doi.org/10.1159/000084645
  2. Che L, Xuan Y, Hu L, et al. Effect of postnatal nutrition restriction on the oxidative status of neonates with intrauterine growth restriction in a pig model. Neonatology 2015;107:93-9. https://doi.org/10.1159/000368179
  3. Li W, Zhong X, Zhang L, Wang Y, Wang T. Heat shock protein 70 expression is increased in the liver of neonatal intrauterine growth retardation piglets. Asian-Australas J Anim Sci 2012; 25:1096-101. https://doi.org/10.5713/ajas.2012.12058
  4. Liu C, Lin G, Wang X, et al. Intrauterine growth restriction alters the hepatic proteome in fetal pigs. J Nutr Biochem 2013; 24:954-9. https://doi.org/10.1016/j.jnutbio.2012.06.016
  5. Marchesini G, Bugianesi E, Forlani G, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 2003;37:917-23. https://doi.org/10.1053/jhep.2003.50161
  6. Valsamakis G, Kanaka-gantenbein C, Malamitsi-puchner A, Mastorakos G. Causes of intrauterine growth restriction and the postnatal development of the metabolic syndrome. Ann NY Acad Sci 2006;1092:138-47. https://doi.org/10.1196/annals.1365.012
  7. Thamotharan M, Shin BC, Suddirikku DT, et al. Glut4 expression and subcellular localization in the intrauterine growth-restricted adult rat female offspring. Am J Physiol Endocrinol Metab 2005;288:E935-47. https://doi.org/10.1152/ajpendo.00342.2004
  8. Siljander-Rasi H, Peuranen S, Tiihonen K, et al. Effect of equi-molar dietary betaine and choline addition on performance, carcass quality and physiological parameters of pigs. Anim Sci 2003;76:55-62. https://doi.org/10.1017/S1357729800053315
  9. Sidransky H, Farber E. Liver choline oxidase activity in man and in several species of animals. Arch Biochem Biophys 1960; 87:129-33. https://doi.org/10.1016/0003-9861(60)90133-8
  10. He Q, Ren P, Kong X, et al. Intrauterine growth restriction alters the metabonome of the serum and jejunum in piglets. Mol BioSyst 2011;7:2147-55. https://doi.org/10.1039/c1mb05024a
  11. NRC. Nutrient requirements of poultry: National Research Council. Washington, DC, USA: National Academy Press; 1998.
  12. Engel RW. Modified methods for the chemical and biological determination of choline. J Biol Chem 1942;144:701-10.
  13. Noma A, Okabe H, Kita M. A new colorimetric micro-determination of free fatty acids in serum. Clin Chim Acta 1973;43: 317-20. https://doi.org/10.1016/0009-8981(73)90468-3
  14. Reitman S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol 1957;28:56-63. https://doi.org/10.1093/ajcp/28.1.56
  15. Sullivan DR, Kruijswijk Z, West CE, Kohlmeier M, Katan MB. Determination of serum triglycerides by an accurate enzymatic method not affected by free glycerol. Clin Chem 1985;31: 1227-8.
  16. Glock GE, McLean P. Further studies on the properties and assay of glucose 6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase of rat liver. Biochem J 1953;55:400-8. https://doi.org/10.1042/bj0550400
  17. Huang Q, Xu Z, Han X, Li W. Effect of dietary betaine supplementation on lipogenic enzyme activities and fatty acid synthase mrna expression in finishing pigs. Anim Feed Sci Technol 2008;140:365-75. https://doi.org/10.1016/j.anifeedsci.2007.03.007
  18. Xi G, Xu Z, Wu SH, Chen S. Effect of chromium picolinate on growth performance, carcass characteristics, serum metabolites and metabolism of lipid in pigs. Asian-Australas J Anim Sci 2001;14:258-62. https://doi.org/10.5713/ajas.2001.258
  19. MacDonald MJ. Differences between mouse and rat pancreatic islets: Succinate responsiveness, malic enzyme, and anaplerosis. Am J Physiol Endocrin Metabol 2002;283:E302-10. https://doi.org/10.1152/ajpendo.00041.2002
  20. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative pcr and the $2-{{\Delta}{\Delta}CT}$ method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  21. Ueland PM. Choline and betaine in health and disease. J Inherit Metab Dis 2011;34:3-15. https://doi.org/10.1007/s10545-010-9088-4
  22. Rehfeldt C, Lefaucheur L, Block J, et al. Limited and excess protein intake of pregnant gilts differently affects body composition and cellularity of skeletal muscle and subcutaneous adipose tissue of newborn and weanling piglets. Eur J Nutr 2012;51:151-65. https://doi.org/10.1007/s00394-011-0201-8
  23. Attig L, Djiane J, Gertler A, et al. Study of hypothalamic leptin receptor expression in low-birth-weight piglets and effects of leptin supplementation on neonatal growth and development. Am J Physiol Endocrinol Metab 2008;295:E1117-25. https://doi.org/10.1152/ajpendo.90542.2008
  24. Claris O, Beltrand J, Levy-Marchal C. Consequences of intrauterine growth and early neonatal catch-up growth. Semin Perinatol 2010;34:207-10. https://doi.org/10.1053/j.semperi.2010.02.005
  25. Taverne F, Richard C, Couture P, Lamarche B. Abdominal obesity, insulin resistance, metabolic syndrome and cholesterol homeostasis. PharmaNutrition 2013;1:130-6. https://doi.org/10.1016/j.phanu.2013.07.003
  26. Detopoulou P, Panagiotakos DB, Antonopoulou S, Pitsavos C, Stefanadis C. Dietary choline and betaine intakes in relation to concentrations of inflammatory markers in healthy adults: The attica study. Am J Clin Nutr 2008;87:424-30. https://doi.org/10.1093/ajcn/87.2.424
  27. Dalmeijer G, Olthof M, Verhoef P, Bots M, Van der Schouw Y. Prospective study on dietary intakes of folate, betaine, and choline and cardiovascular disease risk in women. Eur J Clin Nutr 2008;62:386-94. https://doi.org/10.1038/sj.ejcn.1602725
  28. Shirakawa T, Nakajima K, Yatsuzuka S, et al. The role of circulating lipoprotein lipase and adiponectin on the particle size of remnant lipoproteins in patients with diabetes mellitus and metabolic syndrome. Clin Chim Acta 2015;440:123-32. https://doi.org/10.1016/j.cca.2014.10.029
  29. Niu Y, Li S, Na L, et al. Mangiferin decreases plasma free fatty acids through promoting its catabolism in liver by activation of ampk. PLoS One 2012;7:e30782. https://doi.org/10.1371/journal.pone.0030782
  30. Turpin S, Hoy A, Brown R, et al. Adipose triacylglycerol lipase is a major regulator of hepatic lipid metabolism but not insulin sensitivity in mice. Diabetologia 2011;54:146-56. https://doi.org/10.1007/s00125-010-1895-5
  31. Reid BN, Ables GP, Otlivanchik OA, et al. Hepatic overexpression of hormone-sensitive lipase and adipose triglyceride lipase promotes fatty acid oxidation, stimulates direct release of free fatty acids, and ameliorates steatosis. J Biol Chem 2008;283: 13087-99. https://doi.org/10.1074/jbc.M800533200
  32. Lane RH, Kelley DE, Gruetzmacher EM, Devaskar SU. Uteroplacental insufficiency alters hepatic fatty acid-metabolizing enzymes in juvenile and adult rats. Am J Physiol Regul Integr Comp Physiol 2001;280:R183-90. https://doi.org/10.1152/ajpregu.2001.280.1.R183
  33. Sachan DS, Hongu N. Increases in $vo_2max$ and metabolic markers of fat oxidation by caffeine, carnitine, and choline supplementation in rats. J Nutr Biochem 2000;11:521-6. https://doi.org/10.1016/S0955-2863(00)00119-4
  34. Zeisel SH, Da Costa KA, Franklin PD, et al. Choline, an essential nutrient for humans. FASEB J 1991;5:2093-8. https://doi.org/10.1096/fasebj.5.7.2010061
  35. Raubenheimer PJ, Nyirenda MJ, Walker BR. A choline-deficient diet exacerbates fatty liver but attenuates insulin resistance and glucose intolerance in mice fed a high-fat diet. Diabetes 2006;55:2015-20. https://doi.org/10.2337/db06-0097
  36. Yan J, Winter L, Burns-Whitmore B, Vermeylen F, Caudill M. Plasma choline metabolites associate with metabolic stress among young overweight men in a genotype-specific manner. Nutr Diabetes 2012;2:e49. https://doi.org/10.1038/nutd.2012.23
  37. Maloney CA, Gosby AK, Phuyal JL, et al. Site-specific changes in the expression of fat-partitioning genes in weanling rats exposed to a low-protein diet in utero. Obes Res 2003;11:461-8. https://doi.org/10.1038/oby.2003.63
  38. Garg M, Thamotharan M, Dai Y, et al. Glucose intolerance and lipid metabolic adaptations in response to intrauterine and postnatal calorie restriction in male adult rats. Endocrinology 2013;154:102-13. https://doi.org/10.1210/en.2012-1640
  39. Koletzko B, Shamir R. Prenatal and postnatal nutrition: impact on child health. Curr Opin Clin Nutr Metab Care 2013;16: 290-1. https://doi.org/10.1097/MCO.0b013e32836051ad

Cited by

  1. Transcriptome Analyses Reveal Adult Metabolic Syndrome With Intrauterine Growth Restriction in Pig Models vol.9, pp.1664-8021, 2018, https://doi.org/10.3389/fgene.2018.00291
  2. Effects of dietary dihydroartemisinin supplementation on growth performance, hepatic inflammation, and lipid metabolism in weaned piglets with intrauterine growth retardation vol.91, pp.1, 2020, https://doi.org/10.1111/asj.13363
  3. Comparative Proteomics of Milk Fat Globule Membrane (MFGM) Proteome across Species and Lactation Stages and the Potentials of MFGM Fractions in Infant Formula Preparation vol.9, pp.9, 2018, https://doi.org/10.3390/foods9091251
  4. Liver transcriptome profiling and functional analysis of intrauterine growth restriction (IUGR) piglets reveals a genetic correction and sexual-dimorphic gene expression during postnatal development vol.21, pp.1, 2018, https://doi.org/10.1186/s12864-020-07094-9
  5. Degradation kinetics of vitamins in premixes for pig: effects of choline, high concentrations of copper and zinc, and storage time vol.34, pp.4, 2021, https://doi.org/10.5713/ajas.20.0026
  6. Hippocampal neural cell degeneration and memory deficit in high-fat diet-induced postnatal obese rats- exploring the comparable benefits of choline and DHA or environmental enrichment vol.131, pp.11, 2018, https://doi.org/10.1080/00207454.2020.1773819