Central versus peripheral impact of estradiol on the impaired glucose metabolism in ovariectomized mice on a high-fat diet

American Journal of Physiology - Endocrinology and Metabolism

Volumn 303, Issue 4, 2012, Pages

  Yonezawa, Rika ^a   Wada, Tsutomu ^a   Matsumoto, Natsumi ^a   Morita, Mayuko ^a   Sawakawa, Kanae ^a   Ishii, Yoko ^a   Sasahara, Masakiyo ^a   Tsuneki, Hiroshi ^a   Saito, Shigeru ^a   Sasaoka, Toshiyasu ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

Author keywords

Energy expenditure; Insulin resistance; Postmenopause

Indexed keywords

ESTRADIOL; FATTY ACID SYNTHASE; GLYCOPROTEIN P 15095; LIPOPROTEIN LIPASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CORE TEMPERATURE; ENERGY EXPENDITURE; FEMALE; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTRAABDOMINAL FAT; LIPID DIET; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBCUTANEOUS FAT; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMALS; BODY TEMPERATURE; BODY WEIGHT; DIET, HIGH-FAT; ENERGY METABOLISM; ESTRADIOL; FEMALE; GLUCONEOGENESIS; GLUCOSE; GLUCOSE INTOLERANCE; INSULIN RESISTANCE; LIVER; MACROPHAGES; MICE; MICE, INBRED C57BL; OBESITY; ORGAN SIZE; STEROL ESTERASE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84865151198     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00638.2011     Document Type: Article

References (45)

1. Balthasar N, Coppari R, McMinn J, Liu SM, Lee CE, Tang V, Kenny CD, McGovern RA, Chua SC Jr, Elmquist JK, Lowell BB. Leptin receptor signaling in POMC neurons is required for normal body weight homeostasis. Neuron 42: 983-991, 2004.
2. Brown LM, Gent L, Davis K, Clegg DJ. Metabolic impact of sex hormones on obesity. Brain Res 1350: 77-85, 2010.
3. Bryzgalova G, Gao H, Ahren B, Zierath JR, Galuska D, Steiler TL, Dahlman-Wright K, Nilsson S, Gustafsson JA, Efendic S, Khan A. Evidence that oestrogen receptorplays an important role in the regulation of glucose homeostasis in mice: insulin sensitivity in the liver. Diabetologia 49: 588-597, 2006.
4. Bryzgalova G, Lundholm L, Portwood N, Gustafsson JA, Khan A, Efendic S, Dahlman-Wright K. Mechanisms of antidiabetogenic and body weight-lowering effects of estrogen in high-fat diet-fed mice. Am J Physiol Endocrinol Metab 295: E904-E912, 2008.
5. Buettner C, Muse ED, Cheng A, Chen L, Scherer T, Pocai A, Su K, Cheng B, Li X, Harvey-White J, Schwartz GJ, Kunos G, Rossetti L. Leptin controls adipose tissue lipogenesis via central, STAT3-independent mechanisms. Nat Med 14: 667-675, 2008.
6. Butera PC, Czaja JA. Intracranial estradiol in ovariectomized guinea pigs: effects on ingestive behaviors and body weight. Brain Res 322: 41-48, 1984.
7. Carr MC. The emergence of the metabolic syndrome with menopause. J Clin Endocrinol Metab 88: 2404-2411, 2003.
8. Clegg DJ, Brown LM, Woods SC, Benoit SC. Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 55: 978-987, 2006.
9. Cooke PS, Naaz A. Role of estrogens in adipocyte development and function. Exp Biol Med (Maywood) 229: 1127-1135, 2004.
10. D'Eon TM, Souza SC, Aronovitz M, Obin MS, Fried SK, Greenberg AS. Estrogen regulation of adiposity and fuel partitioning. Evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J Biol Chem 280: 35983-35991, 2005.
11. Dayspring TD, Pokrywka G. Impact of triglycerides on lipid and lipoprotein biology in women. Gend Med 7: 189-205, 2010.
12. Deng JY, Hsieh PS, Huang JP, Lu LS, Hung LM. Activation of estrogen receptor is crucial for resveratrol-stimulating muscular glucose uptake via both insulin-dependent and-independent pathways. Diabetes 57: 1814-1823, 2008.
13. Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA 287: 356-359, 2002.
14. Fujisaka S, Usui I, Bukhari A, Ikutani M, Oya T, Kanatani Y, Tsuneyama K, Nagai Y, Takatsu K, Urakaze M, Kobayashi M, Tobe K. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 58: 2574-2582, 2009.
15. Gao H, Bryzgalova G, Hedman E, Khan A, Efendic S, Gustafsson JA, Dahlman-Wright K. Long-term administration of estradiol decreases expression of hepatic lipogenic genes and improves insulin sensitivity in ob/ob mice: a possible mechanism is through direct regulation of signal transducer and activator of transcription 3. Mol Endocrinol 20: 1287-1299, 2006.
16. Gao Q, Horvath TL. Cross-talk between estrogen and leptin signaling in the hypothalamus. Am J Physiol Endocrinol Metab 294: E817-E826, 2008.
17. Gao Q, Mezei G, Nie Y, Rao Y, Choi CS, Bechmann I, Leranth C, Toran-Allerand D, Priest CA, Roberts JL, Gao XB, Mobbs C, Shulman GI, Diano S, Horvath TL. Anorectic estrogen mimics leptin's effect on the rewiring of melanocortin cells and Stat3 signaling in obese animals. Nat Med 13: 89-94, 2007.
18. Godsland IF. Oestrogens and insulin secretion. Diabetologia 48: 2213-2220, 2005.
19. Gruber CJ, Tschugguel W, Schneeberger C, Huber JC. Production and actions of estrogens. N Engl J Med 346: 340-352, 2002.
20. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS. Increased adipose tissue in male and female estrogen receptorknockout mice. Proc Natl Acad Sci USA 97: 12729-12734, 2000.
21. Jones ME, Thorburn AW, Britt KL, Hewitt KN, Wreford NG, Proietto J, Oz OK, Leury BJ, Robertson KM, Yao S, Simpson ER. Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity. Proc Natl Acad Sci USA 97: 12735-12740, 2000.
22. Ludgero-Correia A Jr, Aguila MB, Mandarim-de-Lacerda CA, Faria TS. Effects of high-fat diet on plasma lipids, adiposity, and inflammatory markers in ovariectomized C57BL/6 mice. Nutrition 28: 316-323, 2012.
23. Meyer MR, Clegg DJ, Prossnitz ER, Barton M. Obesity, insulin resistance and diabetes: sex differences and role of oestrogen receptors. Acta Physiol (Oxf) 203: 259-269, 2011.
24. Misso ML, Murata Y, Boon WC, Jones ME, Britt KL, Simpson ER. Cellular and molecular characterization of the adipose phenotype of the aromatase-deficient mouse. Endocrinology 144: 1474-1480, 2003.
25. Murphy AJ, Guyre PM, Pioli PA. Estradiol suppresses NFB activation through coordinated regulation of let-7a and miR-125b in primary human macrophages. J Immunol 184: 5029-5037, 2010.
26. Musatov S, Chen W, Pfaff DW, Mobbs CV, Yang XJ, Clegg DJ, Kaplitt MG, Ogawa S. Silencing of estrogen receptor in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc Natl Acad Sci USA 104: 2501-2506, 2007.
27. Nagira K, Sasaoka T, Wada T, Fukui K, Ikubo M, Hori S, Tsuneki H, Saito S, Kobayashi M. Altered subcellular distribution of estrogen receptor is implicated in estradiol-induced dual regulation of insulin signaling in 3T3-L1 adipocytes. Endocrinology 147: 1020-1028, 2006.
28. Pardridge WM, Mietus LJ. Transport of steroid hormones through the rat blood-brain barrier. Primary role of albumin-bound hormone. J Clin Invest 64: 145-154, 1979.
29. Park CJ, Zhao Z, Glidewell-Kenney C, Lazic M, Chambon P, Krust A, Weiss J, Clegg DJ, Dunaif A, Jameson JL, Levine JE. Genetic rescue of nonclassical ER signaling normalizes energy balance in obese Erα-null mutant mice. J Clin Invest 121: 604-612, 2011.
30. Pocai A, Morgan K, Buettner C, Gutierrez-Juarez R, Obici S, Rossetti L. Central leptin acutely reverses diet-induced hepatic insulin resistance. Diabetes 54: 3182-3189, 2005.
31. Riant E, Waget A, Cogo H, Arnal JF, Burcelin R, Gourdy P. Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology 150: 2109-2117, 2009.
32. Rogers NH, Witczak CA, Hirshman MF, Goodyear LJ, Greenberg AS. Estradiol stimulates Akt, AMP-activated protein kinase (AMPK) and TBC1D1/4, but not glucose uptake in rat soleus. Biochem Biophys Res Commun 382: 646-650, 2009.
33. Ryan EA, Enns L. Role of gestational hormones in the induction of insulin resistance. J Clin Endocrinol Metab 67: 341-347, 1988.
34. Saito M, Minokoshi Y, Shimazu T. Ventromedial hypothalamic stimulation accelerates norepinephrine turnover in brown adipose tissue of rats. Life Sci 41: 193-197, 1987.
35. Salpeter SR, Walsh JM, Ormiston TM, Greyber E, Buckley NS, Salpeter EE. Meta-analysis: effect of hormone-replacement therapy on components of the metabolic syndrome in postmenopausal women. Diabetes Obes Metab 8: 538-554, 2006.
36. Sherwin BB. Estrogen therapy: is time of initiation critical for neuroprotection? Nat Rev Endocrinol 5: 620-627, 2009.
37. Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB, Korach KS. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 331: 1056-1061, 1994.
38. Tentolouris N, Liatis S, Katsilambros N. Sympathetic system activity in obesity and metabolic syndrome. Ann NY Acad Sci 1083: 129-152, 2006.
39. Tremollieres FA, Pouilles JM, Ribot CA. Relative influence of age and menopause on total and regional body composition changes in postmenopausal women. Am J Obstet Gynecol 175: 1594-1600, 1996.
40. Tsuneki H, Murata S, Anzawa Y, Soeda Y, Tokai E, Wada T, Kimura I, Yanagisawa M, Sakurai T, Sasaoka T. Age-related insulin resistance in hypothalamus and peripheral tissues of orexin knockout mice. Diabetologia 51: 657-667, 2008.
41. Wada T, Kenmochi H, Miyashita Y, Sasaki M, Ojima M, Sasahara M, Koya D, Tsuneki H, Sasaoka T. Spironolactone improves glucose and lipid metabolism by ameliorating hepatic steatosis and inflammation and suppressing enhanced gluconeogenesis induced by high-fat and highfructose diet. Endocrinology 151: 2040-2049, 2010.
42. Wada T, Naito M, Kenmochi H, Tsuneki H, Sasaoka T. Chronic nicotine exposure enhances insulin-induced mitogenic signaling via upregulation of 7 nicotinic receptors in isolated rat aortic smooth muscle cells. Endocrinology 148: 790-799, 2007.
43. Wellen KE, Hotamisligil GS. Obesity-induced inflammatory changes in adipose tissue. J Clin Invest 112: 1785-1788, 2003.
44. Xu Y, Nedungadi TP, Zhu L, Sobhani N, Irani BG, Davis KE, Zhang X, Zou F, Gent LM, Hahner LD, Khan SA, Elias CF, Elmquist JK, Clegg DJ. Distinct hypothalamic neurons mediate estrogenic effects on energy homeostasis and reproduction. Cell Metab 14: 453-465, 2011.
45. Zakrzewska KE, Cusin I, Stricker-Krongrad A, Boss O, Ricquier D, Jeanrenaud B, Rohner-Jeanrenaud F. Induction of obesity and hyperleptinemia by central glucocorticoid infusion in the rat. Diabetes 48: 365-370, 1999.