Arginine nutrition and fetal brown adipose tissue development in diet-induced obese sheep

Amino Acids

Volumn 43, Issue 4, 2012, Pages 1593-1603

  Carey Satterfield, M ^a   Dunlap, Kathrin A ^a   Keisler, Duane H ^b   Bazer, Fuller W ^a   Wu, Guoyao ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Adipose tissue; Arginine; Fetus; Obese; Pregnancy; Sheep

Indexed keywords

ARGININE; GLUCOSE; GLUTAMIC ACID; GLYCINE; INSULIN; LEPTIN; LEUCINE; LIPID; LYSINE; ORNITHINE; PROGESTERONE; SERINE; SODIUM CHLORIDE; THREONINE;

AMNION FLUID; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; BROWN ADIPOSE TISSUE; CARCASS; CONTROLLED STUDY; DIET SUPPLEMENTATION; EMBRYO TRANSFER; EWE; FEMALE; FETAL WELL BEING; FETUS; FETUS DEVELOPMENT; FETUS GROWTH; FETUS WEIGHT; GESTATION PERIOD; MATERNAL NUTRITION; MATERNAL OBESITY; MATERNAL PLASMA; MATERNAL WELFARE; NONHUMAN; PLACENTA; PLACENTA WEIGHT; PRIORITY JOURNAL; PROTEIN CONTENT; SHEEP;

ADIPOSE TISSUE, BROWN; ADMINISTRATION, INTRAVENOUS; ANIMALS; ARGININE; BLOOD GLUCOSE; BODY WEIGHT; DIET; FEMALE; FETAL DEVELOPMENT; FETUS; GESTATIONAL AGE; INSULIN; LEPTIN; NUTRITIONAL STATUS; OBESITY; PREGNANCY; SHEEP, DOMESTIC; SINGLE EMBRYO TRANSFER;

OVIS; OVIS ARIES;

EID: 84867579299     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-012-1235-9     Document Type: Article

References (86)

1. Aagaard-Tillery KM, Grove K, Bishop J et al (2008) Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 41:91-102
2. Alarcon-Aguilar FJ, Almanza-Perez J, Blancas G et al (2008) Glycine regulates the production of pro-inflammatory cytokines in lean and monosodium glutamate-obese mice. Eur J Pharmacol 599:152-158
3. Alexander G (1978) Quantitative development of adipose tissue in foetal sheep. Aust J Biol Sci 31:489-503
4. Appaji Rao N, Ambili M, Jala VR et al (2003) Structure-function relationship in serine hydroxymethyltransferase. Biochim Biophys Acta 1647:24-29
5. Armitage JA, Lakasing L, Taylor PD et al (2005) Developmental programming of aortic and renal structure in offspring of rats fed fat-rich diets in pregnancy. J Physiol 565:171-184
6. Asakura H (2004) Fetal and neonatal thermoregulation. J Nippon Med Sch 71:360-370
7. Bispham J, Gopalakrishnan GS, Dandrea J et al (2003) Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology 144:3575-3585
8. Blachier F, Davila AM, Benamouzig R et al (2011) Channelling of arginine in NO and polyamine pathways in colonocytes and consequences. Front Biosci 16:1331-1343
9. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277-359
10. Clarke L, Bryant MJ, Lomax MA et al (1997) Maternal manipulation of brown adipose tissue and liver development in the ovine fetus during late gestation. Br J Nutr 77:871-883
11. Cox J, Williams S, Grove K et al (2009) Amaternal high-fat diet is accompanied by alterations in the fetal primate metabolome. Am J Obstet Gynecol 201:e281-e289
12. Cypess AM, Lehman S, Williams G et al (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360:1509-1517
13. Delavaud C, Bocquier F, Chilliard Y et al (2000) Plasma leptin determination in ruminants: effect of nutritional status and body fatness on plasma leptin concentration assessed by Aspecific RIA in sheep. J Endocrinol 165:519-526
14. Dunn GA, Bale TL (2009) Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 150:4999-5009
15. Eklou-Lawson M, Bernard F, Neveux N et al (2009) Colonic luminal ammonia and portal blood l-glutamine and l-Arginine concentrations: Apossible link between colon mucosa and liver ureagenesis. Amino Acids 37:751-760
16. Enerback S (2010) Human brown adipose tissue. Cell Metab 11:248-252
17. Felig P, Marliss E, Cahill GF Jr (1969) Plasma amino acid levels and insulin secretion in obesity. N Engl J Med 281:811-816
18. Folch J, Lees M, Sloane Stanley GH (1957) Asimple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497-509
19. Ford SP, Zhang L, Zhu M et al (2009) Maternal obesity accelerates fetal pancreatic beta-cell but not alpha-cell development in sheep: prenatal consequences. Am J Physiol Regul Integr Comp Physiol 297:R835-R843
20. Fu WJ, Haynes TE, Kohli R et al (2005) Dietary l-Arginine supplementation reduces fat mass in Zucker diabetic fatty rats. J Nutr 135:714-721
21. Garcia-Macedo R, Sanchez-Munoz F, Almanza-Perez JC et al (2008) Glycine increases mRNA adiponectin and diminishes pro-inflammatory adipokines expression in 3T3-L1 cells. Eur J Pharmacol 587:317-321
22. Gaudiot N, Jaubert AM, Charbonnier E et al (1998) Modulation of white adipose tissue lipolysis by nitric oxide. J Biol Chem 273:13475-13481
23. Geng MM, Li TJ, Kong XF et al (2011) Reduced expression of intestinal N-Acetylglutamate synthase in suckling piglets: Anovel molecular mechanism for arginine as Anutritionally essential amino acid for neonates. Amino Acids 40:1513-1522
24. Gilbert JS, Nijland MJ (2008) Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol Regul Integr Comp Physiol 295:R1941-R1952
25. Gopalakrishnan G, Rhind SM, Stephenson T et al (2001) Effect of maternal nutrient restriction at defined periods in early to mid gestation on placento-fetal, kidney and adipose tissue weights at 110 days gestation in sheep. Early Hum Dev 63:58-59
26. Hayashi TT, Baldridge RC, Olmsted PS et al (1964) Purine nucleotide catabolism in the placenta. Am J Obstet Gynecol 88:470-478
27. Holmes E, Loo RL, Stamler J et al (2008) Human metabolic phenotype diversity and its association with diet and blood pressure. Nature 453:396-400
28. 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 17:571-588
29. 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 37:187-198
30. 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 139:230-237
31. Khan IY, Dekou V, Douglas G et al (2005) Ahigh-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol 288:R127-R133
32. Kohli R, Meininger CJ, Haynes TE et al (2004) Dietary l-Arginine supplementation enhances endothelial nitric oxide synthesis in streptozotocin-induced diabetic rats. J Nutr 134:600-608
33. Kwon H, Spencer TE, Bazer FW et al (2003) Developmental changes of amino acids in ovine fetal fluids. Biol Reprod 68:1813-1820
34. Lassala A, Bazer FW, Cudd TA et al (2009) Intravenous administration of l-citrulline to pregnant ewes is more effective than l-Arginine for increasing arginine availability in the fetus. J Nutr 139:660-665
35. Lassala A, Bazer FW, Cudd TA et al (2010) Parenteral administration of l-Arginine prevents fetal growth restriction in undernourished ewes. J Nutr 140:1242-1248
36. Le Gouill E, Jimenez M, Binnert C et al (2007) Endothelial nitric oxide synthase (eNOS) knockout mice have defective mitochondrial beta-oxidation. Diabetes 56:2690-2696
37. Li X, Bazer FW, Gao H et al (2009a) Amino acids and gaseous signaling. Amino Acids 37:65-78
38. Li P, Kim SW, Li XL et al (2009b) Dietary supplementation with cholesterol and docosahexaenoic acid affects concentrations of amino acids in tissues of young pigs. Amino Acids 37:709-716
39. Li X, Rezaei R, Li P et al (2011a) Composition of amino acids in feed ingredients for animal diets. Amino Acids 40:1159-1168
40. Li FN, Yin YL, Tan BE et al (2011b) Leucine nutrition in animals and humans: mTOR signaling and beyond. Amino Acids 41:1185-1193
41. Lucotti P, Setola E, Monti LD et al (2006) Beneficial effects of Along-term oral l-Arginine treatment added to Ahypocaloric diet and exercise training program in obese, insulin-resistant type 2 diabetic patients. Am J Physiol Endocrinol Metab 291:E906-E912
42. March-of-Dimes (2009) PeriStats. http://www.marchofdimes.org
43. McCurdy CE, Bishop JM, Williams SM et al (2009) Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest 119:323-335
44. 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 39:349-357
45. Mendez JD, Balderas F (2001) Regulation of hyperglycemia and dyslipidemia by exogenous l-Arginine in diabetic rats. Biochimie 83:453-458
46. Muhlhausler BS, Duffield JA, McMillen IC (2007a) Increased maternal nutrition increases leptin expression in perirenal and subcutaneous adipose tissue in the postnatal lamb. Endocrinology 148:6157-6163
47. Muhlhausler BS, Duffield JA, McMillen IC (2007b) Increased maternal nutrition stimulates peroxisome proliferator activated receptor-gamma, adiponectin, and leptin messenger ribonucleic acid expression in adipose tissue before birth. Endocrinology 148:878-885
48. National Research Council (NRC) (1985) Nutrient requirements of sheep. National Academy Press, Washington, DC
49. Osgerby JC, Gadd TS, Wathes DC (2003) Effect of maternal body condition on placental and fetal growth and the insulin-like growth factor axis in Dorset ewes. Reproduction 125:717-731
50. Petrovic V, Buzadzic B, Korac Aet al (2010) NO modulates the molecular basis of rat interscapular brown adipose tissue thermogenesis. Comp Biochem Physiol C Toxicol Pharmacol 152:147-159
51. Pfannenberg C, Werner MK, Ripkens S et al (2010) Impact of age on the relationships of brown adipose tissue with sex and adiposity in humans. Diabetes 59:1789-1793
52. Power GG (1989) Biology of temperature: the mammalian fetus. J Dev Physiol 12:295-304
53. Saito M, Okamatsu-Ogura Y, Matsushita M et al (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58:1526-1531
54. Samuelsson AM, Matthews PA, Argenton M et al (2008) Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: Anovel murine model of developmental programming. Hypertension 51:383-392
55. Satterfield MC, Wu G (2011) Brown adipose tissue growth and development: significance and nutritional regulation. Front Biosci 16:1589-1608
56. Satterfield MC, Bazer FW, Spencer TE (2006) Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus. Biol Reprod 75:289-296
57. Satterfield MC, McKnight JR, Li XL et al (2011a) Nutrition, epigenetics, and vascular function. In: Maulik N (ed) Nutrition, epigenetic mechanisms, and human disease. CRC Press, New York, pp 125-139
58. Satterfield MC, Dunlap KA, Keisler DH et al (2011b) Arginine nutrition and fetal brown adipose tissue development in nutrient-restricted sheep. Amino Acids. doi: 10.1007/s00726-011-1168-8
59. Stock MJ, Rothwell NJ (1983) Role of brown adipose tissue thermogenesis in overfeeding: Areview. J Royal Soc Med 76:71-73
60. Stover P, Schirch V (1990) Serine hydroxymethyltransferase catalyzes the hydrolysis of 5,10-methenyltetrahydrofolate to 5-formyltetrahydrofolate. J Biol Chem 265:14227-14233
61. Symonds ME, Lomax MA (1992) Maternal and environmental influences on thermoregulation in the neonate. Proc Nutr Soc 51:165-172
62. Symonds ME, Mostyn A, Pearce S et al (2003) Endocrine and nutritional regulation of fetal adipose tissue development. J Endocrinol 179:293-299
63. Takahashi K, Aoki A, Takimoto T et al (2008) Dietary supplementation of glycine modulates inflammatory response indicators in broiler chickens. Br J Nutr 100:1019-1028
64. Tan B, Yin Y, Liu Z et al (2009) Dietary l-Arginine supplementation increases muscle gain and reduces body fat mass in growing-finishing pigs. Amino Acids 37:169-175
65. Tan B, Yin Y, Liu Z et al (2011) Dietary l-Arginine supplementation differentially regulates expression of lipid-metabolic genes in porcine adipose tissue and skeletal muscle. J Nutr Biochem 22:441-445
66. Taylor PD, McConnell J, Khan IY et al (2005) Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed Afat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol 288:R134-R139
67. Thorburn GD (1991) The placenta, prostaglandins and parturition: Areview. Reprod Fert Dev 3:277-294
68. Vernon RG (1986) The growth and metabolism of adipocytes. In: Buttery PJ, Haynes NB, Lindsay DB (eds) Control and manipulation of animal growth. Butterworths, London, pp 67-83
69. Virtanen KA, Lidell ME, Orava J et al (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518-1525
70. Wallace JM, Milne JS, Aitken RP (2005) The effect of overnourishing singleton-bearing adult ewes on nutrient partitioning to the gravid uterus. Br J Nutr 94:533-539
71. Wang JJ, Wu ZL, Li DF et al (2012) Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal. doi: 10.1089/ars.2011.4381
72. Wei J, Carroll RJ, Harden KK et al (2011) Comparisons of treatment means when factors do not interact in two-factorial studies. Amino Acids. doi: 10.1007/s00726-011-0924-0
73. Williams CL, Gulli MT, Deckelbaum RJ (2001) Prevention and treatment of childhood obesity. Curr Atheroscler Rep 3:486-497
74. Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1-17
75. Wu G (2010) Functional amino acids in growth, reproduction and health. Adv Nutr 1:31-37
76. Wu G, Meininger CJ (2009) Nitric oxide and vascular insulin resistance. BioFactors 35:21-27
77. Wu G, Morris SM Jr (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336:1-17
78. Wu G, Knabe DA, Flynn NE et al (1996) Arginine degradation in developing porcine enterocytes. Am J Physiol Gastrointest Liver Physiol 271:G913-G919
79. Wu G, Davis PK, Flynn NE et al (1997) Endogenous synthesis of arginine plays an important role in maintaining arginine homeostasis in postweaning growing pigs. J Nutr 127:2342-2349
80. Wu G, Ott TL, Knabe DA et al (1999) Amino acid composition of the fetal pig. J Nutr 129:1031-1038
81. Wu G, Collins JK, Perkins-Veazie P et al (2007) Dietary supplementation with watermelon pomace juice enhances arginine availability and ameliorates the metabolic syndrome in Zucker diabetic fatty rats. J Nutr 137:2680-2685
82. Wu G, Bazer FW, Davis TA et al (2009) Arginine metabolism and nutrition in growth, health and disease. Amino Acids 37:153-168
83. Wu G, Bazer FW, Burghardt RC et al (2011) Proline and hydroxyproline metabolism: implications for animal and human nutrition. Amino Acids 40:1053-1063
84. Yoneshiro T, Aita S, Matsushita M et al (2011) Brown adipose tissue, whole-body energy expenditure, and thermogenesis in healthy adult men. Obesity (Silver Spring) 19:13-16
85. Zhu MJ, Han B, Tong J et al (2008) AMP-Activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J Physiol 586:2651-2664
86. Zhu MJ, Du M, Nijland MJ et al (2009) Down-regulation of growth signaling pathways linked to Areduced cotyledonary vascularity in placentomes of over-nourished, obese pregnant ewes. Placenta 30:405-410