Amino Acids

, Volume 46, Issue 2, pp 353–366 | Cite as

Abomasal infusion of arginine stimulates SCD and C/EBPß gene expression, and decreases CPT1ß gene expression in bovine adipose tissue independent of conjugated linoleic acid

  • Seong Ho Choi
  • Tryon A. Wickersham
  • Guoyao Wu
  • L. Anne Gilmore
  • Holly D. Edwards
  • Sung Kwon Park
  • Kyoung Hoon Kim
  • Stephen B. Smith
Original Article


Based on previous research with bovine peadipocytes, we hypothesized that infusion of arginine into the abomasum of Angus steers stimulates stearoyl-CoA desaturase (SCD) gene expression in bovine subcutaneous (s.c.) adipose tissue, and that this would be attenuated by conjugated linoleic acid (CLA). Growing Angus steers were infused abomasally with l-arginine 50 g/day; n = 13; provided as l-arginine HCl) or l-alanine (isonitrogenous control, 100 g/day; n = 11) for 14 days. For the subsequent 14 days, half of the steers in each amino acid group were infused with CLA (100 g/day). Body weight gain and average daily gain were unaffected (P > 0.15) by infusion of arginine or CLA into the abomasum. The plasma concentrations of cis-9, trans-11 and trans-10, cis-12 CLA were increased CLA infusion (P = 0.001) and infusion of arginine increased plasma arginine (P = 0.01). Compared with day 0, fatty acid synthase, glucose-6-phosphate dehydrogenase, and 6-phosphogluconate dehydrogenase enzyme activities in s.c. adipose tissue increased by day 14 in steers infused with either alanine or arginine (all P < 0.01). NADP-MDH activity was higher (P = 0.01) in steers infused with arginine than in steers infused with arginine plus CLA by day 28, but lipid synthesis in vitro from glucose and acetate was unaffected by infusion of either arginine or CLA (P > 0.40). By day 28, C/EBPβ and SCD gene expression was higher, and CPT1β gene expression was lower, in s.c. adipose tissue of steers infused with arginine than in steers infused with alanine (±CLA) (P = 0.05). CLA decreased adipose tissue oleic acid (18:1n-9) in alanine- or arginine-infused steers (P = 0.05), although CLA had no effect on SCD gene expression. The data indicate that supplemental arginine promotes adipogenic gene expression and may promote lipid accumulation in bovine adipose tissue. l-Arginine may beneficially improve beef quality for human consumption.


Adipose tissue Adipogenesis Arginine Beef cattle Conjugated linoleic acid 



AMP-activated protein kinase-α


CCAAT/enhancer-binding protein-β


Conjugated linoleic acid


Carnitine palmitoyltransferase-1ß


Fatty acid methyl esters


Fatty acid synthase


Glucose-6-phosphate dehydrogenase


G-coupled protein receptor-43


NADP-malate dehydrogenase


6-Phosphogluconate dehydrogenase


Peroxisome proliferator-activated receptor-γ


Quantitative real-time polymerase chain reaction


40S ribosomal protein S9


Stearoyl-coenzyme A desaturase





This work was carried out with Korea Research Foundation (KRF-2008-357-F00030), Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ009482), Rural development Administration, Republic of Korea, and the National Research Initiative Competitive Grant no. 2008-35206-18762 from the USDA National Institute of Food and Agriculture.

Conflict of interest

The authors declare that there is no conflict of interest.


  1. Adams VL, Gilbert CD, Mersmann HJ et al (2005) Conjugated linoleic acid depresses [3H]-thymidine incorporation into stromal-vascular cells of adipose tissue from postweanling pigs. Adipocytes 1:65–72Google Scholar
  2. Adams TH, Walzem RL, Smith DR et al (2010) Hamburger high in total, saturated and trans-fatty acids decreases HDL cholesterol and LDL particle diameter, and increases TAG, in mildly hypercholesterolaemic men. Brit J Nutr 103:91–98PubMedCrossRefGoogle Scholar
  3. Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593–615PubMedCrossRefGoogle Scholar
  4. Archibeque SL, Lunt DK, Tume RK et al (2005) Fatty acid indices of stearoyl Co-A desaturase activity do not reflect actual stearoyl Co-A desaturase enzyme activity in adipose tissues of beef steers finished with corn-, flaxseed-, or sorghum-based diets. J Anim Sci 83:1153–1166PubMedGoogle Scholar
  5. Barnes KM, Winslow NR, Shelton AG et al (2012) Effect of dietary conjugated linoleic acid on marbling and intramuscular adipocytes in pork. J Anim Sci 90:1142–1149PubMedCrossRefGoogle Scholar
  6. Baxa TJ, Hutcheson JP, Miller MF et al (2010) Additive effects of a steroidal implant and zilpaterol hydrochloride on feedlot performance, carcass characteristics, and skeletal muscle messenger ribonucleic acid abundance in finishing steers. J Anim Sci 88:330–337PubMedCrossRefGoogle Scholar
  7. Brooks MA, Choi CW, Lunt DK et al (2011) Subcutaneous and intramuscular adipose tissue stearoyl-CoA desaturase gene expression and fatty acid composition in calf- and yearling-fed Angus steers. J Anim Sci 89:2556–2570PubMedCrossRefGoogle Scholar
  8. Brown AJ, Goldsworthy SM, Barnes AA et al (2003) The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278:11312–11319Google Scholar
  9. Choi Gang GO, Sawyer JE et al (2013) Fatty acid biosynthesis and lipogenic enzyme activities in subcutaneous adipose tissue of feedlot steers fed supplementary palm oil or soybean oil. J Anim Sci 91:2091–2098PubMedCrossRefGoogle Scholar
  10. Chung KY, Choi CB, Kawachi H et al (2006) Trans-10, cis-12 conjugated linoleic acid antagonizes arginine-promoted differentiation of bovine preadipocytes. Adipocytes 2:93–100Google Scholar
  11. Chung KY, Baxa TJ, Parr SL et al (2012) Administration of estradiol, trenbolone acetate, and trenbolone acetate/estradiol implants alters adipogenic and myogenic gene expression in bovine skeletal muscle. J Anim Sci 90:1421–1427PubMedGoogle Scholar
  12. Dai ZL, Wu ZL, Yang Y et al (2013) Nitric oxide and energy metabolism in mammals. BioFactors 39:383–391PubMedCrossRefGoogle Scholar
  13. Demaree SR, Gilbert CD, Mersmann HJ et al (2002) Conjugated linoleic acid differentially modifies fatty acid composition in subcellular fractions of muscle and adipose tissue but not adiposity of postweaning pigs. J Nutr 132:3272–3279PubMedGoogle Scholar
  14. Ding ST, McNeel RL, Mersmann HJ (2002) Modulation of adipocyte determination and differentiation-dependent factor 1 by selected polyunsaturated fatty acids. In Vitro Cell Dev Biol Anim 38:352–357Google Scholar
  15. Dugan MER, Aalhus JL, Schaefer AL et al (1997) The effect of conjugated linoleic acid on fat to lean repartitioning and feed conversion in pig. Can J Anim Sci 77:723–725CrossRefGoogle Scholar
  16. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509PubMedGoogle Scholar
  17. Fu WJ, Haynes TE, Kohli R et al (2005) Dietary l-arginine supplementation reduces fat mass in Zucker diabetic fatty rats. J Nutr 135:714–721PubMedGoogle Scholar
  18. Gilmore LA, Walzem RL, Crouse SF et al (2011) Consumption of high-oleic acid ground beef increases HDL-cholesterol concentration but both high-and low-oleic acid ground beef decrease HDL particle diameter in normocholesterolemic men. J Nutr 141:1188–1194PubMedCrossRefGoogle Scholar
  19. Gilmore LA, Crouse SF, Carbuhn A et al (2013) Exercise attenuates the increase in plasma monounsaturated fatty acids and high-density lipoprotein but not high-density lipoprotein 2b cholesterol caused by high-oleic ground beef in women. Nutr Res (In press)Google Scholar
  20. Go GW, Wu G, Silvey DT, Choi SH et al (2012) Lipid metabolism in pigs fed supplemental conjugated linoleic acid and/or dietary arginine. Amino Acids 43:1713–1726PubMedCrossRefGoogle Scholar
  21. Hanson RW, Ballard FJ (1967) The relative significance of acetate and glucose as precursors for lipid synthesis in liver and adipose tissue from ruminants. J Biochem 105:529–536Google Scholar
  22. Hardie GD (2007) Biochemistry. Balancing cellular energy. Science 315:1671–1672Google Scholar
  23. Hosseini A, Sauerwein H, Mielenz M (2010) Putative reference genes for gene expression in studies in propionate and ß-hydroxybutyrate treated bovine adipose tissue explants. J Anim Physiol Anim Nutr (Berl) 94:e178–e184CrossRefGoogle Scholar
  24. Janovick-Guretzky NA, Dann HM, Carlson DB et al (2007) Housekeeping gene expression in bovine liver is affected by physiological state, feed intake, and dietary treatment. J Dairy Sci 90:2246–2252PubMedCrossRefGoogle Scholar
  25. Jobgen WS, Fried SK, Fu WJ et al (2006) Regulatory role for the arginine-nitric oxide pathway in metabolism of energy substrates. J Nutr Biochem 17:571–588Google Scholar
  26. Jobgen W, Fu WJ, Gao H et al (2009a) High fat feeding and dietary l-arginine supplementation differentially regulate gene expression in rat white adipose tissue. Amino Acids 37:187–198PubMedCrossRefGoogle Scholar
  27. Jobgen W, Meininger CJ, Jobgen SC et al (2009b) Dietary l-arginine supplementation reduces white fat gain and enhances skeletal muscle and brown fat masses in diet-induced obese rats. J Nutr 139:230–237PubMedCrossRefGoogle Scholar
  28. Khedrara A, Goto T, Morishima M et al (1999) Elevated body fat in rats by the dietary nitric oxide synthase inhibitor, l-N omega nitroarginine. Biosci Biotechnol Biochem 63:698–702CrossRefGoogle Scholar
  29. King DA, Behrends JM, Jenschke BE et al (2004) Positional distribution of fatty acids in triacylglycerols from subcutaneous adipose tissue of pigs fed diets enriched with conjugated linoleic acid, corn oil, or beef tallow. Meat Sci 67:675–681PubMedCrossRefGoogle Scholar
  30. Lira VA, Soltow QA, Long JH et al (2007) Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle. Am J Physiol Endocrinol Metab 293:E1062–E1068Google Scholar
  31. Martin GS, Lunt DK, Britain KG et al (1999) Postnatal development of stearoyl coenzyme A desaturase gene expression and adiposity in bovine subcutaneous adipose tissue. J Anim Sci 77:630–639PubMedGoogle Scholar
  32. McKnight JR, Satterfield MC, Jobgen WS et al (2010) Beneficial effects of l-arginine on reducing obesity: potential mechanisms and important implications for human health. Amino Acids 39:349–357PubMedCrossRefGoogle Scholar
  33. Mersmann HJ, Underwood MC, Brown LJ et al (1973) Adipose tissue composition and lipogenic capacity in developing swine. Am J Physiol 224:1123–1129PubMedGoogle Scholar
  34. Morrison WR, Smith LM (1964) Preparation of fatty acid methyl esters and diethylacetals from lipids with boron fluoride methanol. J Lipid Res 5:600–608PubMedGoogle Scholar
  35. Nall JL, Wu G, Kim KH et al (2009) Dietary supplementation of l-arginine and conjugated linoleic acid reduces retroperitoneal fat mass and increases lean body mass in rats. J Nutr 139:1279–1285PubMedCrossRefGoogle Scholar
  36. Ostrowska E, Muralitharan M, Cross RF et al (1999) Dietary conjugated linoleic acids increase lean tissue and decrease fat deposition in growing pigs. J Nutr 129:2037–2042PubMedGoogle Scholar
  37. Park Y, Albright KJ, Liu W et al (1997) Effect of conjugated linoleic acid on body composition in mice. Lipids 32:853–858PubMedCrossRefGoogle Scholar
  38. Park Y, Storkson JM, Albright KJ et al (1999) Evidence that the trans-10, cis-12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids 34:235–241PubMedCrossRefGoogle Scholar
  39. Park Y, Storkson JM, Ntambi JM et al (2000) Inhibition of hepatic stearoyl-CoA desaturase by trans-10, cis-12 conjugated linoleic acid and its derivatives. Biochem Biophys Acta 1486:285–292PubMedGoogle Scholar
  40. Satory DL, Smith SB (1999) Conjugated linoleic acid inhibits proliferation but stimulates lipid filling of murine 3T3-L1 preadipocytes. J Nutr 129:92–97PubMedGoogle Scholar
  41. Satterfield MC, Dunlap KA, Keisler DH et al (2012) Arginine nutrition and fetal brown adipose tissue development in diet-induced obese sheep. Amino Acids 43:1593–1603CrossRefGoogle Scholar
  42. Schlegel G, Ringseis R, Shibani M et al (2012a) Influence of a rumen-protected conjugated linoleic acid mixture on carcass traits and meat quality in young simmental heifers. J Anim Sci 90:1532–1540PubMedGoogle Scholar
  43. Schlegel G, Ringseis R, Windisch W et al (2012b) Effects of a rumen-protected mixture of conjugated linoleic acids on hepatic expression of genes involved in lipid metabolism in dairy cows. J Dairy Sci 95:3905–3918PubMedCrossRefGoogle Scholar
  44. Sisk MB, Hausman DB, Martin RJ et al (2001) Dietary conjugated linoleic acid reduces adiposity in lean but not obese Zucker rats. J Nutr 131:1668–1674PubMedGoogle Scholar
  45. Smith SB, Crouse JD (1984) Relative contributions of acetate, lactate and glucose to lipogenesis in bovine intramuscular and subcutaneous adipose tissue. J Nutr 114:792–800PubMedGoogle Scholar
  46. Smith SB, Prior RL (1981) Evidence for a functional ATP-citrate lyase:NADP-malate dehydrogenase pathway in bovine adipose tissue: Enzyme and metabolite levels. Arch Biochem Biophys 211:192–201PubMedCrossRefGoogle Scholar
  47. Smith SB, Smith DR (1995) Substrate utilization in ruminant adipose tissue. In: The biology of fat in meat animals. American Society of Animal Science, Champaign, 166–188Google Scholar
  48. Smith SB, Hively TS, Cortese GM et al (2002) Conjugated linoleic acid depresses the Δ9 desaturase index and stearoyl coenzyme A desaturase enzyme activity in porcine subcutaneous adipose tissue. J Anim Sci 80:2110–2115PubMedGoogle Scholar
  49. Smith SB, Wilson TA, Gilbert CD et al (2010) Conjugated linoleic acid and dietary fats differentially affect hepatic ACAT activity and LDL-cholesterol in postweanling pigs fed low-fat diets. J Anim Sci Biotech 1:75–84Google Scholar
  50. Smith SB, Go GW, Johnson BJ et al (2012) Adipogenic gene expression and fatty acid composition in subcutaneous adipose tissue depots of Angus steers between 9 and 16 months of age. J Anim Sci 90:2505–2514PubMedCrossRefGoogle Scholar
  51. Takahashi Y, Kushiro M, Shinohara K et al (2002) Dietary conjugated linoleic acid reduces body fat mass and affects gene expression of proteins regulating energy metabolism in mice. Comp Biochem Physiol B 133:395–404PubMedCrossRefGoogle Scholar
  52. Tan BE, Yin YL, Liu ZQ et al (2009) Dietary l-arginine supplementation increases muscle gain and reduces body fat mass in growing-finishing pigs. Amino Acids 37:169–175PubMedCrossRefGoogle Scholar
  53. Tan BE, Yin YL, Liu ZQ et al (2011) Dietary l-arginine supplementation differentially regulates expression of lipid-metabolic genes in porcine adipose tissue and skeletal muscle. J Nutr Biochem 22:441–445PubMedCrossRefGoogle Scholar
  54. Tan BE, Li XG, Yin YL et al (2012) Regulatory roles for l-arginine in reducing white adipose tissue. Front Biosci 17:2237–2246CrossRefGoogle Scholar
  55. Tang QQ, Lane MD (2012) Adipogenesis: from stem cell to adipocyte. Annu Rev Biochem 81:715–736PubMedCrossRefGoogle Scholar
  56. Tous N, Theil PK, Lauridsen et al (2012) Dietary conjugated linoleic acid modify gene expression in liver, muscles, and fat tissues of finishing pigs. J Anim Sci 90:340–342PubMedCrossRefGoogle Scholar
  57. Wickersham TA, Titgemeyer EC, Cochran RC (2009) Methodology for concurrent determination of urea kinetics and the capture of recycled urea nitrogen by ruminal microbes in cattle. Animal 3:372–379PubMedCrossRefGoogle Scholar
  58. Wiegand BR, Sparks JC, Parrish FC Jr et al (2002) Duration of feeding conjugated linoleic acid influences growth performance, carcass traits, and meat quality of finishing burrows. J Anim Sci 80:637–643Google Scholar
  59. Wu G (2013) Functional amino acids in nutrition and health. Amino Acids 45:407–411PubMedCrossRefGoogle Scholar
  60. Wu G, Bazer FW, Cudd TA et al (2007) Pharmacokinetics and safety of arginine supplementation in animals. J Nutr 137:1673S–1680SPubMedGoogle Scholar
  61. Wu ZL, Satterfield MC, Bazer FW et al (2012) Regulation of brown adipose tissue development and white fat reduction by l-arginine. Curr Opin Clin Metab Care 15:529–538CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2013

Authors and Affiliations

  • Seong Ho Choi
    • 2
  • Tryon A. Wickersham
    • 1
  • Guoyao Wu
    • 1
  • L. Anne Gilmore
    • 1
  • Holly D. Edwards
    • 1
  • Sung Kwon Park
    • 3
  • Kyoung Hoon Kim
    • 3
  • Stephen B. Smith
    • 1
  1. 1.Department of Animal Science, 2471 TAMUTexas A&M UniversityCollege StationUSA
  2. 2.Department of Animal ScienceChungbuk National UniversityCheongjuRepublic of Korea
  3. 3.National Institute of Animal ScienceRural Development AdministrationSuwonRepublic of Korea

Personalised recommendations