Sex differences in metabolic and adipose tissue responses to juvenile-onset obesity in sheep

Endocrinology

Volumn 154, Issue 10, 2013, Pages 3622-3631

  Bloor, Ian D ^a   Sébert, Sylvain P ^a,d   Saroha, Vivek ^a   Gardner, David S ^b   Keisler, Duane H ^c   Budge, Helen ^a   Symonds, Michael E ^a   Mahajan, Ravi P ^a  

^a NOTTINGHAM UNIVERSITY HOSPITALS NHS TRUST   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF MISSOURI   (United States)

^d UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; 11BETA HYDROXYSTEROID DEHYDROGENASE 2; ADIPONECTIN; ADIPONECTIN RECEPTOR; FATTY ACID; GLUCOCORTICOID; GLUCOSE; HYDROCORTISONE; INSULIN; INTERLEUKIN 6; LEPTIN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN BAX; TOLL LIKE RECEPTOR 4; TRIACYLGLYCEROL;

ABDOMINAL FAT; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; COMORBIDITY; CONTROLLED STUDY; FATTY ACID BLOOD LEVEL; FEMALE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HYDROCORTISONE BLOOD LEVEL; HYPERCORTISOLISM; INSULIN BLOOD LEVEL; MALE; NONHUMAN; OBESITY; OMENTUM; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; TRIACYLGLYCEROL BLOOD LEVEL;

ADIPOSITY; ADRENOCORTICAL HYPERFUNCTION; AGE FACTORS; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANIMALS, INBRED STRAINS; BCL-2-ASSOCIATED X PROTEIN; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; HYPERINSULINISM; INFLAMMATION MEDIATORS; INTRA-ABDOMINAL FAT; LIPID METABOLISM; MALE; OBESITY; RANDOM ALLOCATION; SEX CHARACTERISTICS; SHEEP, DOMESTIC; TOR SERINE-THREONINE KINASES;

EID: 84884696100     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1207     Document Type: Article

References (58)

1. World Health Organization. Obesity and overweight. World Health Organisation. Fact Sheet number 311; 2011.
2. Martinez JA. Body-weight regulation: causes of obesity. Proc Nutr Soc. 2000;59(3):337-345.
3. National Health Service. Statistics on obesity, physical activity and diet: England, 2010. London: The Information Centre for Health and Social Care; 2010, London, UK.
4. Singh AS, Mulder C, Twisk JW, van Mechelen W, Chinapaw MJ. Tracking of childhood overweight into adulthood: a systematic review of the literature. Obes Rev. 2008;9(5):474-488.
5. Lemieux S, Prud'homme D, Bouchard C, Tremblay A, Despres JP. Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr. 1993;58(4):463-467. (Pubitemid 23307401)
6. Rappelli A. Hypertension and obesity after the menopause. J Hypertens Suppl. 2002;20(2):S26-S28. (Pubitemid 34913763)
7. Ahima RS. Central actions of adipocyte hormones. Trends Endocrinol Metab. 2005;16(7):307-313. (Pubitemid 41206637)
8. Wellen KE, Hotamisligil GS. Obesity-induced inflammatory changes in adipose tissue. J Clin Invest. 2003;112(12):1785-1788. (Pubitemid 38063699)
9. Trayhurn P, Wood IS. Signalling role of adipose tissue: adipokines and inflammation in obesity. Biochem Soc Trans. 2005;33(Pt 5):1078-1081. (Pubitemid 41659117)
10. Mathieu P, Poirier P, Pibarot P, Lemieux I, Despres JP. Visceral obesity: the link among inflammation, hypertension, and cardiovascular disease. Hypertension. 2009;53(4):577-584.
11. Syed AA, Weaver JU. Glucocorticoid sensitivity: the hypothalamic- pituitary-adrenal-tissue axis. Obes Res. 2005;13(7):1131-1133.
12. Stewart PM, Boulton A, Kumar S, Clark PM, Shackleton CH. Cortisol metabolism in human obesity: impaired cortisone->cortisol conversion in subjects with central adiposity. J Clin Endocrinol Metab. 1999;84(3):1022-1027. (Pubitemid 29138237)
13. Dallman MF, Strack AM, Akana SF, et al. Feast and famine: critical role of glucocorticoids with insulin in daily energy flow. Front Neuroendocrinol. 1993;14(4):303-347. (Pubitemid 23321823)
14. Bloor ID, Sebert SP, Mahajan RP, Symonds ME. The influence of sex on early stage markers of kidney dysfunction in response to juvenile obesity. Hypertension. 2012;60(4):991-997.
15. Sharkey D, Gardner DS, Symonds ME, Budge H. Maternal nutrient restriction during early fetal kidney development attenuates the renal innate inflammatory response in obese young adult offspring. Am J Physiol Renal Physiol. 2009;297(5):F1199-F1207.
16. Agricultural and Food Research Council. Technical Committee on Responses to Nutrients, Alderman G, Cottrill BR. Energy and Protein Requirements of Ruminants. Wallingford, UK: CAB International; 1993.
17. Sebert SP, Hyatt MA, Chan LL, et al. Maternal nutrient restriction between early and midgestation and its impact upon appetite regulation after juvenile obesity. Endocrinology. 2009;150(2):634-641.
18. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162(1):156-159. (Pubitemid 17064313)
19. Dodic M, Abouantoun T, O'Connor A, Wintour EM, Moritz KM. Programming effects of short prenatal exposure to dexamethasone in sheep. Hypertension. 2002;40(5):729-734. (Pubitemid 35278611)
20. Williams PJ, Kurlak LO, Perkins AC, et al. Hypertension and impaired renal function accompany juvenile obesity: the effect of prenatal diet. Kidney Int. 2007;72(3):279-289. (Pubitemid 47172368)
21. Sharkey D, Gardner DS, Fainberg HP, et al. Maternal nutrient restriction during pregnancy differentially alters the unfolded protein response in adipose and renal tissue of obese juvenile offspring. FASEB J. 2009;23(5):1314-1324.
22. Sebert SP, Dellschaft NS, Chan LL, et al. Maternal nutrient restriction during late gestation and early postnatal growth in sheep differentially reset the control of energy metabolism in the gastric mucosa. Endocrinology. 2011;152(7):2816-2826.
23. Dunphy J, Horvath A, Barcham G, Balic A, Bischof R, Meeusen E. Isolation, characterisation and expression of mRNAs encoding the ovine CC chemokines, monocyte chemoattractant protein (MCP)-1α and -2. Vet Immunol Immunopathol. 2001;82(3-4):153-164. (Pubitemid 32913115)
24. Garcia-Crespo D, Juste RA, Hurtado A. Differential gene expression in central nervous system tissues of sheep with natural scrapie. Brain Res. 2006;1073-1074:88-92.
25. Robinson TL, Sutherland IA, Sutherland J. Validation of candidate bovine reference genes for use with real-time PCR. Vet Immunol Immunopathol. 2007;115(1-2):160-165. (Pubitemid 44908667)
26. Delavaud C, Bocquier F, Chilliard Y, Keisler DH, Gertler A, Kann G. Plasma leptin determination in ruminants: effect of nutritional status and body fatness on plasma leptin concentration assessed by a specific RIA in sheep. J Endocrinol. 2000;165(2):519-526. (Pubitemid 30341101)
27. Torres SJ, Nowson CA. Relationship between stress, eating behavior, and obesity. Nutrition. 2007;23(11-12):887-894. (Pubitemid 47532398)
28. Gardner DS, Van Bon BW, Dandrea J, et al. Effect of periconceptional undernutrition and gender on hypothalamic-pituitary-adrenal axis function in young adult sheep. J Endocrinol. 2006;190(2):203-212. (Pubitemid 44288359)
29. Frias JP, Macaraeg GB, Ofrecio J, Yu JG, Olefsky JM, Kruszynska YT. Decreased susceptibility to fatty acid-induced peripheral tissue insulin resistance in women. Diabetes. 2001;50(6):1344-1350. (Pubitemid 32500167)
30. Turgeon JL, Carr MC, Maki PM, Mendelsohn ME, Wise PM. Complex actions of sex steroids in adipose tissue, the cardiovascular system, and brain: Insights from basic science and clinical studies. Endocr Rev. 2006;27(6):575-605. (Pubitemid 44582052)
31. Austin H, Austin JM Jr, Partridge EE, Hatch KD, Shingleton HM. Endometrial cancer, obesity, and body fat distribution. Cancer Res. 1991;51(2):568-572.
32. Seale JV, Wood SA, Atkinson HC, Harbuz MS, Lightman SL. Gonadal steroid replacement reverses gonadectomy-induced changes in the corticosterone pulse profile and stress-induced hypothalamic-pituitary-adrenal axis activity of male and female rats. J Neuroendocrinol. 2004;16(12):989-998. (Pubitemid 40214444)
33. Enzi G, Gasparo M, Biondetti PR, Fiore D, Semisa M, Zurlo F. Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr. 1986;44(6):739-746. (Pubitemid 17208993)
34. Kopelman PG. Obesity as a medical problem. Nature. 2000;404(6778):635- 643. (Pubitemid 30205068)
35. Marin P, Andersson B, Ottosson M, et al. The morphology and metabolism of intraabdominal adipose tissue in men. Metabolism. 1992;41(11):1242-1248.
36. Tchernof A, Belanger C, Morisset AS, et al. Regional differences in adipose tissue metabolism in women: minor effect of obesity and body fat distribution. Diabetes. 2006;55(5):1353-1360. (Pubitemid 44195374)
37. Salehi M, Ferenczi A, Zumoff B. Obesity and cortisol status. Horm Metab Res. 2005;37(4):193-197. (Pubitemid 40756337)
38. Bjorntorp P, Rosmond R. Obesity and cortisol. Nutrition. 2000;16(10):924-936.
39. Strain GW, Zumoff B, Kream J, Strain JJ, Levin J, Fukushima D. Sex difference in the influence of obesity on the 24 hr mean plasma concentration of cortisol. Metabolism. 1982;31(3):209-212. (Pubitemid 12176906)
40. Veilleux A, Laberge PY, Morency J, Noel S, Luu-The V, Tchernof A. Expression of genes related to glucocorticoid action in human subcutaneous and omental adipose tissue. J Steroid Biochem Mol Biol. 2010;122(1-3):28-34.
41. Sebert S, Sharkey D, Budge H, Symonds ME. The early programming of metabolic health: is epigenetic setting the missing link? Am J Clin Nutr. 2011;94(6 Suppl):1953S-1958S.
42. Wake DJ, Rask E, Livingstone DE, Soderberg S, Olsson T, Walker BR. Local and systemic impact of transcriptional up-regulation of 11β-hydroxysteroid dehydrogenase type 1 in adipose tissue in human obesity. J Clin Endocrinol Metab. 2003;88(8):3983-3988. (Pubitemid 37034555)
43. Bjorntorp P. Do stress reactions cause abdominal obesity and comorbidities? Obes Rev. 2001;2(2):73-86. (Pubitemid 33755917)
44. Auphan N, DiDonato JA, Rosette C, Helmberg A, Karin M. Immunosuppression by glucocorticoids: inhibition of NF-κ B activity through induction of I κ B synthesis. Science. 1995;270(5234):286-290.
45. Fain JN, Madan AK, Hiler ML, Cheema P, Bahouth SW. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology. 2004;145(5):2273-2282. (Pubitemid 38535056)
46. Ahima RS. Revisiting leptin's role in obesity and weight loss. J Clin Invest. 2008;118(7):2380-2383. (Pubitemid 351949765)
47. Ren J. Leptin and hyperleptinemia-from friend to foe for cardiovascular function. J Endocrinol. 2004;181(1):1-10. (Pubitemid 38584659)
48. Fruhbeck G, Jebb SA, Prentice AM. Leptin: physiology and pathophysiology. Clin Physiol. 1998;18(5):399-419. (Pubitemid 28451466)
49. Montague CT, Prins JB, Sanders L, Digby JE, O'Rahilly S. Depotand sex-specific differences in human leptin mRNA expression: implications for the control of regional fat distribution. Diabetes. 1997;46(3):342-347. (Pubitemid 27090260)
50. Chilliard Y, Bonnet M, Delavaud C, et al. Leptin in ruminants. Gene expression in adipose tissue and mammary gland, and regulation of plasma concentration. Domest Anim Endocrinol. 2001;21(4):271-295. (Pubitemid 34204089)
51. Sharkey D, Symonds ME, Budge H. Adipose tissue inflammation: developmental ontogeny and consequences of gestational nutrient restriction in offspring. Endocrinology. 2009;150(8):3913-3920.
52. Zhang HM, Chen LL, Wang L, et al. Macrophage infiltrates with high levels of Toll-like receptor 4 expression in white adipose tissues of male Chinese. Nutr Metab Cardiovasc Dis. 2009;19(10):736-743.
53. Kanda H, Tateya S, Tamori Y, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest. 2006;116(6):1494-1505.
54. Gnanalingham MG, Mostyn A, Symonds ME, Stephenson T. Ontogeny and nutritional programming of adiposity in sheep: potential role of glucocorticoid action and uncoupling protein-2. AmJ Physiol Regul Integr Comp Physiol. 2005;289(5):R1407-R1415. (Pubitemid 41507407)
55. Gemmel RT, Alexander G. Ultrastructural development of adipose tissue in foetal sheep. Am J Anat. 1972;31:505-515.
56. Pope M, Budge H, Symonds ME. The developmental transition of ovine adipose tissue through early life [published online January 28, 2013]. Acta Physiol (Oxf). doi:10.1111/apha.12053.
57. Symonds ME, Pope M, Sharkey D, Budge H. Adipose tissue and fetal programming. Diabetologia. 2012;55(6):1597-1606.
58. Labeur M, Holsboer F. Molecular mechanisms of glucocorticoid receptor signaling. Medicina (B Aires).70(5):457-462.