Fetal baboon sex-specific outcomes in adipocyte differentiation at 0.9 gestation in response to moderate maternal nutrient reduction

International Journal of Obesity

Volumn 38, Issue 2, 2014, Pages 224-230

  Tchoukalova, Y D ^a   Krishnapuram, R ^a   White, U A ^a   Burk, D ^a   Fang, X ^b   Nijland, M J ^c   Nathanielsz, P W ^c  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b LOUISIANA DEPARTMENT OF HEALTH AND HOSPITALS   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

adipocyte; adipogenesis; fetal programming; nonhuman primate fetus; preadipocyte; sexual dimorphism

Indexed keywords

ADIPONECTIN; CYTOCHROME C OXIDASE; FATTY ACID BINDING PROTEIN 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX15; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1;

ABDOMINAL SUBCUTANEOUS FAT; ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BABOON; BROWN ADIPOSE TISSUE; CELL COUNT; CELL DIFFERENTIATION; CELL SIZE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FEMALE; FETAL MALNUTRITION; FETUS; GESTATIONAL AGE; GROWTH INHIBITION; HISTOLOGY; HYPERTROPHY; IN VITRO STUDY; MALE; MATERNAL NUTRIENT REDUCTION; MATERNAL NUTRITION; MOTHER; NONHUMAN; OMENTUM; OUTCOME ASSESSMENT; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REDUCTION; SEX DIFFERENCE; STROMA; TISSUE CULTURE; WHITE ADIPOSE TISSUE; ABDOMINAL CIRCUMFERENCE; ADIPOSE TISSUE; BODY WEIGHT; CROWN RUMP LENGTH; GENE EXPRESSION; IMMUNOBLOTTING; MORPHOMETRICS; NUTRIENT AVAILABILITY; SEX; SUBCUTANEOUS TISSUE;

PAPIO; PRIMATES;

ADIPOCYTES; ADIPOGENESIS; ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CELL DIFFERENTIATION; FATTY ACID-BINDING PROTEINS; FEMALE; FETAL DEVELOPMENT; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; HUMANS; IMMUNOBLOTTING; INFANT, NEWBORN; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PAPIO; PPAR ALPHA; PREGNANCY; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; SEX FACTORS;

EID: 84896697927     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2013.106     Document Type: Article

References (50)

1. Guo Z, Hensrud DD, Johnson CM, Jensen MD. Regional postprandial fatty acid metabolism in different obesity phenotypes. Diabetes 1999; 48: 1586-1592
2. Despres JP, Nadeau A, Tremblay A, Ferland M, Moorjani S, Lupien PJ et al. Role of deep abdominal fat in the association between regional adipose tissue distribution and glucose tolerance in obese women. Diabetes 1989; 38: 304-309
3. Canoy D, Luben R, Welch A, Bingham S, Wareham N, Day N et al. Fat distribution, body mass index and blood pressure in 22,090 men and women in the Norfolk cohort of the European Prospective Investigation into Cancer and Nutrition (EPIC-Norfolk) study. J Hypertens 2004; 22: 2067-2074
4. Snijder MB, Dekker JM, Visser M, Yudkin JS, Stehouwer CD, Bouter LM et al. Larger thigh and hip circumferences are associated with better glucose tolerance: The Hoorn study. Obes Res 2003; 11: 104-111
5. Heitmann BL, Frederiksen P, Lissner L. Hip circumference and cardiovascular morbidity and mortality in men and women. Obes Res 2004; 12: 482-487
6. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS. Fetal nutrition and cardiovascular disease in adult life. Lancet 1993; 341: 938-941
7. Sarr O, Yang K, Regnault TR. In utero programming of later adiposity: The role of fetal growth restriction. J Pregnancy 2012; 2012: 134758
8. Crandall DL, Hausman GJ, Kral JG. A review of the microcirculation of adipose tissue: Anatomic, metabolic, and angiogenic perspectives. Microcirculation 1997; 4: 211-232
9. Hausman GJ, Richardson RL. Adipose tissue angiogenesis. J Anim Sci 2004; 82: 925-934
10. Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE et al. White fat progenitor cells reside in the adipose vasculature. Science 2008; 322: 583-586
11. Pope M, Budge H, Symonds ME. The developmental transition of ovine adipose tissue through early life. Acta Physiol (Oxf) 2014; 210: 20-30
12. Li C, McDonald TJ, Wu G, Nijland MJ, Nathanielsz PW. Intrauterine growth restriction alters term fetal baboon hypothalamic appetitive peptide balance. J Endocrinol 2013; 217: 275-282
13. Choi J, Li C, McDonald TJ, Comuzzie A, Mattern V, Nathanielsz PW. Emergence of insulin resistance in juvenile baboon offspring of mothers exposed to moderate maternal nutrient reduction. Am J Physiol Regul Integr Comp Physiol 2011; 301: R757-R762
14. Schlabritz-Loutsevitch NE, Howell K, Rice K, Glover EJ, Nevill CH, Jenkins SL et al. Development of a system for individual feeding of baboons maintained in an outdoor group social environment. J Med Primatol 2004; 33: 117-126
15. Cox LA, Nijland MJ, Gilbert JS, Schlabritz-Loutsevitch NE, Hubbard GB, McDonald TJ et al. Effect of 30 per cent maternal nutrient restriction from 0.16 to 0.5 gestation on fetal baboon kidney gene expression. J Physiol 2006; 572(Pt 1): 67-85
16. Schlabritz-Loutsevitch NE, Hubbard GB, Dammann MJ, Jenkins SL, Frost PA, McDonald TJ et al. Normal concentrations of essential and toxic elements in pregnant baboons and fetuses (Papio species). J Med Primatol 2004; 33: 152-162
17. Tchoukalova YD, Nathanielsz PW, Conover CA, Smith SR, Ravussin E. Regional variation in adipogenesis and IGF regulatory proteins in the fetal baboon. Biochem Biophys Res Commun 2009; 380: 679-683
18. Commins SP, Watson PM, Padgett MA, Dudley A, Argyropoulos G, Gettys TW. Induction of uncoupling protein expression in brown and white adipose tissue by leptin. Endocrinology 1999; 140: 292-300
19. Parker AJ, Davies P, Mayho AM, Newton Jr. The ultrasound estimation of sexrelated variations of intrauterine growth. Am J Obstet Gynecol 1984; 149: 665-669
20. Padoan A, Rigano S, Ferrazzi E, Beaty BL, Battaglia FC, Galan HL. Differences in fat and lean mass proportions in normal and growth-restricted fetuses. Am J Obstetr Gynecol 2004; 191: 1459-1464
21. Larciprete G, Valensise H, Di Pierro G, Vasapollo B, Casalino B, Arduini D et al. Intrauterine growth restriction and fetal body composition. Ultrasound Obstetr Gynecol 2005; 26: 258-262
22. Aubert R, Suquet JP, Lemonnier D. Long-Term morphological and metabolic effects of early under-And over-nutrition in mice. J Nutr 1980; 110: 649-661
23. Johnson PR, Stern JS, Greenwood MR, Zucker LM, Hirsch J. Effect of early nutrition on adipose cellularity and pancreatic insulin release in the Zucker rat. J Nutr 1973; 103: 738-743
24. Xue B, Coulter A, Rim JS, Koza RA, Kozak LP. Transcriptional synergy and the regulation of Ucp1 during brown adipocyte induction in white fat depots. Mol Cell Biol 2005; 25: 8311-8322
25. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A coldinducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998; 92: 829-839
26. Nadal-Casellas A, Bauza-Thorbrugge M, Proenza AM, Gianotti M, Llado I. Sex-dependent differences in rat brown adipose tissue mitochondrial biogenesis and insulin signaling parameters in response to an obesogenic diet. Mol Cell Biochem 2013; 373: 125-135
27. Giordano A, Frontini A, Murano I, Tonello C, Marino MA, Carruba MO et al. Regional-dependent increase of sympathetic innervation in rat white adipose tissue during prolonged fasting. J Histochem Cytochem 2005; 53: 679-687
28. Lafontan M, Berlan M. Fat cell adrenergic receptors and the control of white and brown fat cell function. J Lipid Res 1993; 34: 1057-1091
29. Kamat A, Nijland MJ, McDonald TJ, Cox LA, Nathanielsz PW, Li C. Moderate global reduction in maternal nutrition has differential stage of gestation specific effects on (beta)1-And (beta)2-Adrenergic receptors in the fetal baboon liver. Reprod Sci 2011; 18: 398-405
30. Monjo M, Pujol E, Roca P. alpha2-To beta3-Adrenoceptor switch in 3T3-L1 preadipocytes and adipocytes: Modulation by testosterone, 17beta-estradiol, and progesterone. Am J Physiol. Endocrinol Metab 2005; 289: E145-E150
31. Rae MT, Rhind SM, Fowler PA, Miller DW, Kyle CE, Brooks AN. Effect of maternal undernutrition on fetal testicular steroidogenesis during the CNS androgenresponsive period in male sheep fetuses. Reproduction 2002; 124: 33-39
32. Fowden AL, Giussani DA, Forhead AJ. Intrauterine programming of physiological systems: Causes and consequences. Physiology (Bethesda) 2006; 21: 29-37
33. Li C, Ramahi E, Nijland MJ, Choi J, Myers DA, Nathanielsz PW et al. Up-regulation of the Fetal baboon hypothalamo-pituitary-Adrenal axis in intrauterine growth restriction: Coincidence with hypothalamic glucocorticoid receptor insensitivity and leptin receptor down-regulation. Endocrinology 2013; 154: 2365-2373
34. Guo C, Li C, Myatt L, Nathanielsz PW, Sun K. Sexually dimorphic effects of maternal nutrient reduction on expression of genes regulating cortisol metabolism in fetal baboon adipose and liver tissues. Diabetes 2013; 62: 1175-1185
35. Yu ZK, Wright JT, Hausman GJ. Preadipocyte recruitment in stromal vascular cultures after depletion of committed preadipocytes by immunocytotoxicity. Obes Res 1997; 5: 9-15
36. Tchoukalova YD, Hausman DB, Dean RG, Hausman GJ. Enhancing effect of troglitazone on porcine adipocyte differentiation in primary culture: A comparison with dexamethasone. Obes Res 2000; 8: 664-672
37. Cantile M, Procino A, D'Armiento M, Cindolo L, Cillo C. HOX gene network is involved in the transcriptional regulation of in vivo human adipogenesis. J Cell Physiol 2003; 194: 225-236
38. Vohl MC, Sladek R, Robitaille J, Gurd S, Marceau P, Richard D et al. A survey of genes differentially expressed in subcutaneous and visceral adipose tissue in men. Obes Res 2004; 12: 1217-1222
39. Gesta S, Bluher M, Yamamoto Y, Norris AW, Berndt J, Kralisch S et al. Evidence for a role of developmental genes in the origin of obesity and body fat distribution. Proc Natl Acad Sci USA 2006; 103: 6676-6681
40. Tchkonia T, Giorgadze N, Pirtskhalava T, Thomou T, DePonte M, Koo A et al. Fat depot-specific characteristics are retained in strains derived from single human preadipocytes. Diabetes 2006; 55: 2571-2578
41. Gburcik V, Cawthorn WP, Nedergaard J, Timmons JA, Cannon B. An essential role for Tbx15 in the differentiation of brown and 'brite' but not white adipocytes. Am J Physiol Endocrinol Metab 2012; 303: E1053-E1060
42. Nookaew I, Svensson PA, Jacobson P, Jernas M, Taube M, Larsson I et al. Adipose tissue resting energy expenditure and expression of genes involved in mitochondrial function are higher in women than in men. J Clin Endocrinol Metab 2013; 98: E370-E378
43. Karastergiou K, Fried SK, Xie H, Lee MJ, Divoux A, Rosencrantz MA et al. Distinct developmental signatures of human abdominal and gluteal subcutaneous adipose tissue depots. J Clin Endocrinol Metab 2013; 98: 362-371
44. Strissel KJ, Stancheva Z, Miyoshi H, Perfield 2nd JW, DeFuria J, Jick Z et al. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 2007; 56: 2910-2918
45. MacKellar J, Cushman SW, Periwal V. Waves of adipose tissue growth in the genetically obese Zucker fatty rat. PLoS One 2010; 5: E8197
46. Gustafson B, Gogg S, Hedjazifar S, Jenndahl L, Hammarstedt A, Smith U. Inflammation and impaired adipogenesis in hypertrophic obesity in man. Am J Physiol Endocrinol Metab 2009; 297: E999-E1003
47. Yanney M, Marlow N. Paediatric consequences of fetal growth restriction. Sem Fetal Neonatal Med 2004; 9: 411-418
48. Sharkey D, Symonds ME, Budge H. Adipose tissue inflammation: Developmental ontogeny and consequences of gestational nutrient restriction in offspring. Endocrinology 2009; 150: 3913-3920
49. Barbatelli G, Murano I, Madsen L, Hao Q, Jimenez M, Kristiansen K et al. The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am J Physiol Endocrinol Metab 2010; 298: E1244-E1253
50. Kozak LP, Koza RA, Anunciado-Koza R. Brown fat thermogenesis and body weight regulation in mice: Relevance to humans. Int J Obes (Lond) 2010; 34(Suppl 1): S23-S27 Development