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Intrauterine growth restriction combined with a maternal high-fat diet increased adiposity and serum corticosterone levels in adult rat offspring

Part of: Liggins Institute, New Zealand and the Japanese DOHaD Society

Published online by Cambridge University Press:  05 February 2018

E. K. Zinkhan Open the ORCID record for E. K. Zinkhan [Opens in a new window] ,
B. Yu ,
C. W. Callaway  and
R. A. McKnight
E. K. Zinkhan*
Affiliation:
Department of Pediatrics, Division of Neonatology, University of Utah, Salt Lake City, UT, USA
B. Yu
Affiliation:
Department of Pediatrics, Division of Neonatology, University of Utah, Salt Lake City, UT, USA
C. W. Callaway
Affiliation:
Department of Pediatrics, Division of Neonatology, University of Utah, Salt Lake City, UT, USA
R. A. McKnight
Affiliation:
Department of Pediatrics, Division of Neonatology, University of Utah, Salt Lake City, UT, USA
*
*Author for correspondence: E. K. Zinkhan, Department of Pediatrics, Division of Neonatology, University of Utah, 295 Chipeta Way, Salt Lake City, UT 84108, USA. E-mail [email protected]
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Abstract

Intrauterine growth restriction (IUGR) and fetal exposure to a maternal high-fat diet (HFD) independently increase the risk of developing obesity in adulthood. Excess glucocorticoids increase obesity. We hypothesized that surgically induced IUGR combined with an HFD would increase adiposity and glucocorticoids more than in non-IUGR offspring combined with the same HFD, findings that would persist despite weaning to a regular diet. Non-IUGR (N) and IUGR (I) rat offspring from dams fed either regular rat chow (R) or an HFD (H) were weaned to either a regular rat chow or an HFD. For non-IUGR and IUGR rats, this study design resulted in three diet groups: offspring from dams fed a regular diet and weaned to a regular diet (NRR and IRR), offspring rats from dams fed an HFD and weaned to a regular diet (NHR and IHR) and offspring from dams fed an HFD and weaned to an HFD (NHH and IHH). Magnetic resonance imaging or fasting visceral and subcutaneous adipose tissue collection occurred at postnatal day 60. IHH male rats had greater adiposity than NHH males, findings that were only partly normalized by weaning to a regular chow. IHH male rats had a 10-fold increase in serum corticosterone levels. IHH female rats had increased adiposity and serum triglycerides. We conclude that IUGR combined with an HFD throughout life increased adiposity, glucocorticoids and triglycerides in a sex-specific manner. Our data suggest that one mechanism through which the perinatal environment programs increased adiposity in IHH male rats may be via increased systemic glucocorticoids.

Keywords

glucocorticoidglucocorticoid receptorhigh-fat dietintrauterine growth restrictionobesity
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 3: Themed Issue: NZ-Japan , June 2018 , pp. 315 - 328
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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References

1. Botero, D, Lifshitz, F. Intrauterine growth retardation and long-term effects on growth. Curr Opin Pediatr. 1999; 11, 340–347.Google Scholar
2. Gluckman, PD, Hanson, MA, Pinal, C. The developmental origins of adult disease. Matern Child Nutr. 2005; 1, 130–141.Google Scholar
3. King, JC. Maternal obesity, metabolism, and pregnancy outcomes. Annu Rev Nutr. 2006; 26, 271–291.Google Scholar
4. Kim, SY, Dietz, PM, England, L, Morrow, B, Callaghan, WM. Trends in pre-pregnancy obesity in nine states, 1993-2003. Obesity. 2007; 15, 986–993.Google Scholar
5. Yogev, Y, Catalano, PM. Pregnancy and obesity. Obstet Gynecol Clin North Am. 2009; 36, 285–300, viii.Google Scholar
6. Radulescu, L, Munteanu, O, Popa, F, Cirstoiu, M. The implications and consequences of maternal obesity on fetal intrauterine growth restriction. J Med Life. 2013; 6, 292–298.Google Scholar
7. Deshmukh, VL, Jadhav, M, Yelikar, K. Impact of high BMI on pregnancy: maternal and foetal outcome. J Obstet Gynaecol India. 2016; 66, 192–197.CrossRefGoogle ScholarPubMed
8. Cinar, M, Timur, H, Aksoy, RT, et al. Evaluation of maternal and perinatal outcomes among overweight women who experienced stillbirth. J Matern Fetal Neonatal Med. 2017; 30, 38–42.Google Scholar
9. Demicheva, E, Crispi, F. Long-term follow-up of intrauterine growth restriction: cardiovascular disorders. Fetal Diagn Ther. 2014; 36, 143–153.Google Scholar
10. Rueda-Clausen, CF, Dolinsky, VW, et al. Hypoxia-induced intrauterine growth restriction increases the susceptibility of rats to high-fat diet-induced metabolic syndrome. Diabetes. 2011; 60, 507–516.Google Scholar
11. Liu, J, He, J, Yang, Y, et al. Effects of intrauterine growth retardation and postnatal high-fat diet on hepatic inflammatory response in pigs. Arch Anim Nutr. 2014; 68, 111–125.Google Scholar
12. Boney, CM, Verma, A, Tucker, R, Vohr, BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005; 115, e290–e296.Google Scholar
13. Ravelli, AC, van Der Meulen, JH, Osmond, C, Barker, DJ, Bleker, OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr. 1999; 70, 811–816.Google Scholar
14. Curhan, GC, Willett, WC, Rimm, EB, et al. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation. 1996; 94, 3246–3250.Google Scholar
15. Curhan, GC, Chertow, GM, Willett, WC, et al. Birth weight and adult hypertension and obesity in women. Circulation. 1996; 94, 1310–1315.Google Scholar
16. Fall, CH, Osmond, C, Barker, DJ, et al. Fetal and infant growth and cardiovascular risk factors in women. BMJ. 1995; 310, 428–432.Google Scholar
17. Law, CM, Barker, DJ, Osmond, C, Fall, CH, Simmonds, SJ. Early growth and abdominal fatness in adult life. J Epidemiol Community Health. 1992; 46, 184–186.CrossRefGoogle ScholarPubMed
18. Whitaker, RC. Predicting preschooler obesity at birth: the role of maternal obesity in early pregnancy. Pediatrics. 2004; 114, e29–e36.Google Scholar
19. Rolfe Ede, L, Loos, RJ, Druet, C, et al. Association between birth weight and visceral fat in adults. Am J Clin Nutr. 2010; 92, 347–352.Google Scholar
20. Kim, JY, van de Wall, E, Laplante, M, et al. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J Clin Invest. 2007; 117, 2621–2637.CrossRefGoogle ScholarPubMed
21. Tran, TT, Yamamoto, Y, Gesta, S, Kahn, CR. Beneficial effects of subcutaneous fat transplantation on metabolism. Cell Metab. 2008; 7, 410–420.Google Scholar
22. Despres, JP, Allard, C, Tremblay, A, Talbot, J, Bouchard, C. Evidence for a regional component of body fatness in the association with serum lipids in men and women. Metabolism. 1985; 34, 967–973.Google Scholar
23. Gillum, RF. The association of body fat distribution with hypertension, hypertensive heart disease, coronary heart disease, diabetes and cardiovascular risk factors in men and women aged 18-79 years. J Chronic Dis. 1987; 40, 421–428.Google Scholar
24. Haffner, SM, Fong, D, Hazuda, HP, Pugh, JA, Patterson, JK. Hyperinsulinemia, upper body adiposity, and cardiovascular risk factors in non-diabetics. Metabolism. 1988; 37, 338–345.CrossRefGoogle ScholarPubMed
25. Thompson, CJ, Ryu, JE, Craven, TE, Kahl, FR, Crouse, JR 3rd. Central adipose distribution is related to coronary atherosclerosis. Arterioscler Thromb. 1991; 11, 327–333.Google Scholar
26. Owens, S, Gutin, B, Ferguson, M, et al. Visceral adipose tissue and cardiovascular risk factors in obese children. J Pediatr. 1998; 133, 41–45.CrossRefGoogle ScholarPubMed
27. Wei, Y, Yang, CR, Wei, YP, et al. Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc Natl Acad Sci U S A. 2014; 111, 1873–1878.Google Scholar
28. Vadlamudi, S, Kalhan, SC, Patel, MS. Persistence of metabolic consequences in the progeny of rats fed a HC formula in their early postnatal life. Am J Physiol. 1995; 269, E731–E738.Google Scholar
29. Rasmussen, KM, Catalano, PM, Yaktine, AL. New guidelines for weight gain during pregnancy: what obstetrician/gynecologists should know. Curr Opin Obstet Gynecol. 2009; 21, 521–526.Google Scholar
30. Rasmussen, T, Stene, LC, Samuelsen, SO, et al. Maternal BMI before pregnancy, maternal weight gain during pregnancy, and risk of persistent positivity for multiple diabetes-associated autoantibodies in children with the high-risk HLA genotype: the MIDIA study. Diabetes Care. 2009; 32, 1904–1906.Google Scholar
31. Kennedy, E, Meyers, L. Dietary reference intakes: development and uses for assessment of micronutrient status of women – a global perspective. Am J Clin Nutr. 2005; 81, 1194S–1197S.Google Scholar
32. Oakley, RH, Cidlowski, JA. The biology of the glucocorticoid receptor: new signaling mechanisms in health and disease. J Allergy Clin Immunol. 2013; 132, 1033–1044.Google Scholar
33. Newell-Price, J, Bertagna, X, Grossman, AB, Nieman, LK. Cushing’s syndrome. Lancet. 2006; 367, 1605–1617.CrossRefGoogle ScholarPubMed
34. Masuzaki, H, Paterson, J, Shinyama, H, et al. A transgenic model of visceral obesity and the metabolic syndrome. Science. 2001; 294, 2166–2170.Google Scholar
35. Tomlinson, JW, Finney, J, Gay, C, et al. Impaired glucose tolerance and insulin resistance are associated with increased adipose 11beta-hydroxysteroid dehydrogenase type 1 expression and elevated hepatic 5alpha-reductase activity. Diabetes. 2008; 57, 2652–2660.Google Scholar
36. Morton, NM. Obesity and corticosteroids: 11beta-hydroxysteroid type 1 as a cause and therapeutic target in metabolic disease. Mol Cell Endocrinol. 2010; 316, 154–164.Google Scholar
37. London, E, Castonguay, TW. High fructose diets increase 11beta-hydroxysteroid dehydrogenase type 1 in liver and visceral adipose in rats within 24-h exposure. Obesity. 2011; 19, 925–932.Google Scholar
38. Staab, CA, Maser, E. 11beta-Hydroxysteroid dehydrogenase type 1 is an important regulator at the interface of obesity and inflammation. J Steroid Biochem Mol Biol. 2010; 119, 56–72.Google Scholar
39. Lee, MJ, Pramyothin, P, Karastergiou, K, Fried, SK. Deconstructing the roles of glucocorticoids in adipose tissue biology and the development of central obesity. Biochim Biophys Acta. 2014; 1842, 473–481.Google Scholar
40. Bamberger, CM, Bamberger, AM, de Castro, M, Chrousos, GP. Glucocorticoid receptor beta, a potential endogenous inhibitor of glucocorticoid action in humans. J Clin Invest. 1995; 95, 2435–2441.Google Scholar
41. Oakley, RH, Jewell, CM, Yudt, MR, Bofetiado, DM, Cidlowski, JA. The dominant negative activity of the human glucocorticoid receptor beta isoform. Specificity and mechanisms of action. J Biol Chem. 1999; 274, 27857–27866.Google Scholar
42. Phuc, Le P, Friedman, JR, Schug, J, et al. Glucocorticoid receptor-dependent gene regulatory networks. PLoS Genet. 2005; 1, e16.Google Scholar
43. Atanasov, AG, Nashev, LG, Schweizer, RA, Frick, C, Odermatt, A. Hexose-6-phosphate dehydrogenase determines the reaction direction of 11beta-hydroxysteroid dehydrogenase type 1 as an oxoreductase. FEBS Lett. 2004; 571, 129–133.Google Scholar
44. Kotelevtsev, Y, Holmes, MC, Burchell, A, et al. 11beta-hydroxysteroid dehydrogenase type 1 knockout mice show attenuated glucocorticoid-inducible responses and resist hyperglycemia on obesity or stress. Proc Natl Acad Sci U S A. 1997; 94, 14924–14929.Google Scholar
45. Rosen, ED, Hsu, CH, Wang, X, et al. C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev. 2002; 16, 22–26.Google Scholar
46. Yanase, T, Yashiro, T, Takitani, K, et al. Differential expression of PPAR gamma 1 and gamma 2 isoforms in human adipose tissue. Biochem Biophys Res Commun. 1997; 233, 320–324.Google Scholar
47. Kershaw, EE, Schupp, M, Guan, HP, et al. PPARgamma regulates adipose triglyceride lipase in adipocytes in vitro and in vivo. Am J Physiol Endocrinol Metab. 2007; 293, E1736–E1745.CrossRefGoogle ScholarPubMed
48. Imai, T, Takakuwa, R, Marchand, S, et al. Peroxisome proliferator-activated receptor gamma is required in mature white and brown adipocytes for their survival in the mouse. Proc Natl Acad Sci U S A. 2004; 101, 4543–4547.Google Scholar
49. Zinkhan, EK, Zalla, JM, Carpenter, JR, et al. Intrauterine growth restriction combined with a maternal high-fat diet increases hepatic cholesterol and low-density lipoprotein receptor activity in rats. Physiol Rep. 2016; 4, e12862.Google Scholar
50. Wright, JD, Wang, CY, Kennedy-Stephenson, J, Ervin, RB. Dietary intake of ten key nutrients for public health, United States: 1999-2000. Adv Data. 2003; 334, 1–4.Google Scholar
51. Energy and protein requirements. Report of a joint FAO/WHO ad hoc expert committee. Rome, 22 March-2 April 1971. FAO Nutr Meet Rep Ser. 1973; 552, 1–118.Google Scholar
52. Boujendar, S, Reusens, B, Merezak, S, et al. Taurine supplementation to a low protein diet during foetal and early postnatal life restores a normal proliferation and apoptosis of rat pancreatic islets. Diabetologia. 2002; 45, 856–866.Google Scholar
53. Fu, Q, McKnight, RA, Yu, X, Callaway, CW, Lane, RH. Growth retardation alters the epigenetic characteristics of hepatic dual specificity phosphatase 5. FASEB J. 2006; 20, 2127–2129.Google Scholar
54. Hubscher, CH, Brooks, DL, Johnson, JR. A quantitative method for assessing stages of the rat estrous cycle. Biotech Histochem. 2005; 80, 79–87.Google Scholar
55. Joss-Moore, LA, Wang, Y, Campbell, MS, et al. Uteroplacental insufficiency increases visceral adiposity and visceral adipose PPARgamma2 expression in male rat offspring prior to the onset of obesity. Early Hum Dev. 2010; 86, 179–185.Google Scholar
56. Livak, KJ, Schmittgen, TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001; 25, 402–408.Google Scholar
57. Dodson, RB, Miller, TA, Powers, KN, et al. Intrauterine growth restriction influences vascular remodeling and stiffening in the weanling rat more than sex or diet. Am J Physiol Heart Circ Physiol. 2017; 312, H250–H264.Google Scholar
58. Veena, SR, Krishnaveni, GV, Karat, SC, Osmond, C, Fall, CH. Testing the fetal overnutrition hypothesis; the relationship of maternal and paternal adiposity to adiposity, insulin resistance and cardiovascular risk factors in Indian children. Public Health Nutr. 2013; 16, 1656–1666.Google Scholar
59. Fante, T, Simino, LA, Reginato, A, et al. Diet-induced maternal obesity alters insulin signalling in male mice offspring rechallenged with a high-fat diet in adulthood. PloS One. 2016; 11, e0160184.Google Scholar
60. Oliveira, LS, Souza, LL, Souza, AF, et al. Perinatal maternal high-fat diet promotes alterations in hepatic lipid metabolism and resistance to the hypolipidemic effect of fish oil in adolescent rat offspring. Mol Nutr Food Res. 2016; 60, 2493–2504.Google Scholar
61. Frihauf, JB, Fekete, EM, Nagy, TR, Levin, BE, Zorrilla, EP. Maternal western diet increases adiposity even in male offspring of obesity-resistant rat dams: early endocrine risk markers. Am J Physiol Regul Integr Comp Physiol. 2016; 311, R1045–R1059.Google Scholar
62. Golay, A, Bobbioni, E. The role of dietary fat in obesity. Int J Obes Relat Metab Disord. 1997; 21(Suppl. 3), S2–S11.Google Scholar
63. Samuelsson, AM, Matthews, PA, Argenton, M, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008; 51, 383–392.Google Scholar
64. Siemelink, M, Verhoef, A, Dormans, JA, Span, PN, Piersma, AH. Dietary fatty acid composition during pregnancy and lactation in the rat programs growth and glucose metabolism in the offspring. Diabetologia. 2002; 45, 1397–1403.Google Scholar
65. Cheng, HS, Ton, SH, Phang, SCW, Tan, JBL, Abdul Kadir, K. Increased susceptibility of post-weaning rats on high-fat diet to metabolic syndrome. J Adv Res. 2017; 8, 743–752.CrossRefGoogle ScholarPubMed
66. Zinkhan, EK, Lang, BY, Yu, B, et al. Maternal tobacco smoke increased visceral adiposity and serum corticosterone levels in adult male rat offspring. Pediatr Res. 2014; 76, 17–23.Google Scholar
67. Poore, KR, Fowden, AL. The effects of birth weight and postnatal growth patterns on fat depth and plasma leptin concentrations in juvenile and adult pigs. J Physiol. 2004; 558, 295–304.Google Scholar
68. De Blasio, MJ, Gatford, KL, Robinson, JS, Owens, JA. Placental restriction of fetal growth reduces size at birth and alters postnatal growth, feeding activity, and adiposity in the young lamb. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R875–R886.Google Scholar
69. Martin, A, Connelly, A, Bland, RM, Reilly, JJ. Health impact of catch-up growth in low-birth weight infants: systematic review, evidence appraisal, and meta-analysis. Matern Child Nutr. 2017; 13.Google Scholar
70. Lee, JH, Lee, H, Lee, SM, et al. Changes of blood pressure, abdominal visceral fat tissue and gene expressions in fetal programming induced rat model after amlodipine-losartan combination treatment. Clin Hypertens. 2016; 22, 12.Google Scholar
71. Bieswal, F, Ahn, MT, Reusens, B, et al. The importance of catch-up growth after early malnutrition for the programming of obesity in male rat. Obesity. 2006; 14, 1330–1343.Google Scholar
72. Bol, VV, Delattre, AI, Reusens, B, Raes, M, Remacle, C. Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice. Am J Physiol Regul Integr Comp Physiol. 2009; 297, R291–R299.Google Scholar
73. Howie, GJ, Sloboda, DM, Kamal, T, Vickers, MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587, 905–915.Google Scholar
74. Laureano, DP, Dalle Molle, R, Alves, MB, et al. Intrauterine growth restriction modifies the hedonic response to sweet taste in newborn pups – role of the accumbal mu-opioid receptors. Neuroscience. 2016; 322, 500–508.Google Scholar
75. Geer, EB, Shen, W, Gallagher, D, et al. MRI assessment of lean and adipose tissue distribution in female patients with Cushing’s disease. Clin Endocrinol. 2010; 73, 469–475.Google Scholar
76. Campbell, JE, Peckett, AJ, D’Souza, AM, Hawke, TJ, Riddell, MC. Adipogenic and lipolytic effects of chronic glucocorticoid exposure. Am J Physiol Cell Physiol. 2011; 300, C198–C209.Google Scholar
77. Rebuffe-Scrive, M, Walsh, UA, McEwen, B, Rodin, J. Effect of chronic stress and exogenous glucocorticoids on regional fat distribution and metabolism. Physiol Behav. 1992; 52, 583–590.Google Scholar
78. Lukaszewski, MA, Mayeur, S, Fajardy, I, et al. Maternal prenatal undernutrition programs adipose tissue gene expression in adult male rat offspring under high-fat diet. Am J Physiol Endocrinol Metabol. 2011; 301, E548–E559.Google Scholar
79. He, Z, Lv, F, Ding, Y, et al. High-fat diet and chronic stress aggravate adrenal function abnormality induced by prenatal caffeine exposure in male offspring rats. Sci Rep. 2017; 7, 14825.Google Scholar
80. Shen, Y, Roh, HC, Kumari, M, Rosen, ED. Adipocyte glucocorticoid receptor is important in lipolysis and insulin resistance due to exogenous steroids, but not insulin resistance caused by high fat feeding. Mol Metab. 2017; 6, 1150–1160.Google Scholar
81. Desai, M, Jellyman, JK, Han, G, Lane, RH, Ross, MG. Programmed regulation of rat offspring adipogenic transcription factor (PPARgamma) by maternal nutrition. J Dev Orig Health Dis. 2015; 6, 530–538.Google Scholar
82. Pan, S, Yang, X, Jia, Y, et al. Intravenous injection of microvesicle-delivery miR-130b alleviates high-fat diet-induced obesity in C57BL/6 mice through translational repression of PPAR-gamma. J Biomed Sci. 2015; 22, 86.Google Scholar
83. Fountain, ED, Mao, J, Whyte, JJ, et al. Effects of diets enriched in omega-3 and omega-6 polyunsaturated fatty acids on offspring sex-ratio and maternal behavior in mice. Biol Reprod. 2008; 78, 211–217.Google Scholar
84. Gharagozlou, F, Youssefi, R, Akbarinejad, V. Effects of diets supplemented by fish oil on sex ratio of pups in bitch. Vet Res Forum. 2016; 7, 105–110.Google Scholar
85. Rosenfeld, CS, Grimm, KM, Livingston, KA, et al. Striking variation in the sex ratio of pups born to mice according to whether maternal diet is high in fat or carbohydrate. Proc Natl Acad Sci U S A. 2003; 100, 4628–4632.Google Scholar
86. Hansen, D, Moller, H, Olsen, J. Severe periconceptional life events and the sex ratio in offspring: follow up study based on five national registers. BMJ. 1999; 319, 548–549.Google Scholar
87. Ideta, A, Hayama, K, Kawashima, C, et al. Subjecting holstein heifers to stress during the follicular phase following superovulatory treatment may increase the female sex ratio of embryos. J Reprod Dev. 2009; 55, 529–533.Google Scholar
88. Obel, C, Henriksen, TB, Secher, NJ, Eskenazi, B, Hedegaard, M. Psychological distress during early gestation and offspring sex ratio. Hum Reprod. 2007; 22, 3009–3012.CrossRefGoogle ScholarPubMed
89. Chin, EH, Schmidt, KL, Martel, KM, et al. A maternal high-fat, high-sucrose diet has sex-specific effects on fetal glucocorticoids with little consequence for offspring metabolism and voluntary locomotor activity in mice. PloS One. 2017; 12, e0174030.Google Scholar
90. Pelleymounter, MA, Cullen, MJ, Baker, MB, et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science. 1995; 269, 540–543.Google Scholar
91. Aoki, N, Kawada, T, Sugimoto, E. Level of preadipocyte growth factor in rat adipose tissue which specifically permits the proliferation of preadipocytes is affected by restricted energy intake. Obes Res. 1993; 1, 126–131.Google Scholar
92. Chen, S, Wang, J, Yu, G, Liu, W, Pearce, D. Androgen and glucocorticoid receptor heterodimer formation. A possible mechanism for mutual inhibition of transcriptional activity. J Biol Chem. 1997; 272, 14087–14092.Google Scholar
93. Nelson, CC, Hendy, SC, Shukin, RJ, et al. Determinants of DNA sequence specificity of the androgen, progesterone, and glucocorticoid receptors: evidence for differential steroid receptor response elements. Mol Endocrinol. 1999; 13, 2090–2107.Google Scholar
94. Porter, DW, Lincoln, DW, Naylor, AM. Plasma cortisol is increased during the inhibition of LH secretion by central LHRH in the ewe. Neuroendocrinology. 1990; 51, 705–712.Google Scholar
95. Fox, CS, Massaro, JM, Hoffmann, U, et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation. 2007; 116, 39–48.Google Scholar
96. Yatagai, T, Nagasaka, S, Taniguchi, A, et al. Hypoadiponectinemia is associated with visceral fat accumulation and insulin resistance in Japanese men with type 2 diabetes mellitus. Metabolism. 2003; 52, 1274–1278.Google Scholar
97. Saijo, Y, Kiyota, N, Kawasaki, Y, et al. Relationship between C-reactive protein and visceral adipose tissue in healthy Japanese subjects. Diabetes Obes Metab. 2004; 6, 249–258.Google Scholar
98. Kanaya, AM, Harris, T, Goodpaster, BH, et al. Adipocytokines attenuate the association between visceral adiposity and diabetes in older adults. Diabetes Care. 2004; 27, 1375–1380.Google Scholar
99. Lemieux, I, Pascot, A, Prud’homme, D, et al. Elevated C-reactive protein: another component of the atherothrombotic profile of abdominal obesity. Arterioscler Thromb Vasc Biol. 2001; 21, 961–967.Google Scholar
100. Azuma, K, Katsukawa, F, Oguchi, S, et al. Correlation between serum resistin level and adiposity in obese individuals. Obes Res. 2003; 11, 997–1001.Google Scholar
101. Fukuhara, A, Matsuda, M, Nishizawa, M, et al. Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science. 2005; 307, 426–430.Google Scholar
102. Miyazawa-Hoshimoto, S, Takahashi, K, Bujo, H, Hashimoto, N, Saito, Y. Elevated serum vascular endothelial growth factor is associated with visceral fat accumulation in human obese subjects. Diabetologia. 2003; 46, 1483–1488.Google Scholar
103. Giusti, V, Suter, M, Verdumo, C, Gaillard, RC, Burckhardt, P, Pralong, FP. Molecular determinants of human adipose tissue: differences between visceral and subcutaneous compartments in obese women. J Clin Endocrinol Metab. 2004; 89, 1379–1384.Google Scholar
104. Mauriege, P, Joanisse, DR, CasparBauguil, S, et al. Gene expression of different adipose tissues of severely obese women with or without a dysmetabolic profile. J Physiol Biochem. 2015; 71, 719–732.Google Scholar
105. Perrini, S, Laviola, L, Cignarelli, A, et al. Fat depot-related differences in gene expression, adiponectin secretion, and insulin action and signalling in human adipocytes differentiated in vitro from precursor stromal cells. Diabetologia. 2008; 51, 155–164.Google Scholar
106. Han, A, Won, SB, Kwon, YH. Different effects of maternal low-isoflavone soy protein and genistein consumption on hepatic lipid metabolism of 21-day-old male rat offspring. Nutrients. 2017; 9, 9.Google Scholar
107. Xie, L, Zhang, K, Rasmussen, D, et al. Effects of prenatal low protein and postnatal high fat diets on visceral adipose tissue macrophage phenotypes and IL-6 expression in Sprague Dawley rat offspring. PloS One. 2017; 12, e0169581.CrossRefGoogle ScholarPubMed
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