Membrane and nuclear estrogen receptor a collaborate to suppress adipogenesis but not triglyceride content

FASEB Journal

Volumn 30, Issue 1, 2016, Pages 230-240

  Pedram, Ali ^a   Razandi, Mahnaz ^a   Blumberg, Bruce ^b   Levin, Ellis Robert ^a,b,c  

^a VA LONG BEACH HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adipocyte hypertrophy; BMSCs; ChREBP; Kinase activation; Preadipocytes

Indexed keywords

BINDING PROTEIN; CARBOHYDRATE RESPONSE ELEMENT BINDING PROTEIN ALPHA; CARBOHYDRATE RESPONSE ELEMENT BINDING PROTEIN BETA; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; PHOSPHOTRANSFERASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN;

3T3 CELL LINE; ADIPOCYTE; ADIPOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MEMBRANE; CONTROLLED STUDY; FEMALE; HEMATOPOIETIC STEM CELL; INTRAABDOMINAL FAT; LIPOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; WEIGHT GAIN; ANIMAL; CELL CULTURE; CELL NUCLEUS; DRUG EFFECTS; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM;

ADIPOGENESIS; ANIMALS; CELL MEMBRANE; CELL NUCLEUS; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; MESENCHYMAL STROMAL CELLS; MICE; TRIGLYCERIDES;

EID: 84974824389     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-274878     Document Type: Article

References (39)

1. Utian, W. H. (1987) Overview on menopause. Am. J. Obstet. Gynecol. 156, 1280-1283
2. Haarbo, J., Marslew, U., Gotfredsen, A., and Christiansen, C. (1991) Postmenopausal hormone replacement therapy prevents central distribution of body fat after menopause. Metabolism 40, 1323-1326
3. Gambacciani, M., Ciaponi, M., Cappagli, B., Piaggesi, L., De Simone, L., Orlandi, R., and Genazzani, A. R. (1997) Body weight, body fat distribution, and hormonal replacement therapy in early postmenopausal women. J. Clin. Endocrinol. Metab. 82, 414-417
4. Okura, T., Koda, M., Ando, F., Niino, N., Ohta, S., and Shimokata, H. (2003) Association of polymorphisms in the estrogen receptor alpha gene with body fat distribution. Int. J. Obes. Relat. Metab. Disord. 27, 1020-1027
5. Heine, P. A., Taylor, J. A., Iwamoto, G. A., Lubahn, D. B., and Cooke, P. S. (2000) Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc. Natl. Acad. Sci. USA 97, 12729-12734
6. Xu, Y., Nedungadi, T. P., Zhu, L., Sobhani, N., Irani, B. G., Davis, K. E., Zhang, X., Zou, F., Gent, L. M., Hahner, L. D., Khan, S. A., Elias, C. F., Elmquist, J. K., and Clegg, D. J. (2011) Distinct hypothalamic neurons mediate estrogenic effects on energy homeostasis and reproduction. Cell Metab. 14, 453-465
7. Heim, M., Frank, O., Kampmann, G., Sochocky, N., Pennimpede, T., Fuchs, P., Hunziker, W., Weber, P., Martin, I., and Bendik, I. (2004) The phytoestrogen genistein enhances osteogenesis and represses adipogenic differentiation of human primary bone marrow stromal cells. Endocrinology 145, 848-859
8. Lapid, K., Lim, A., Clegg, D. J., Zeve, D., and Graff, J. M. (2014) Oestrogen signalling in white adipose progenitor cells inhibits differentiation into brown adipose and smooth muscle cells. Nat. Commun. 5, 5196
9. Pedram, A., Razandi, M., Kim, J. K., O'Mahony, F., Lee, E. Y., Luderer, U., and Levin, E. R. (2009) Developmental phenotype of a membrane only estrogen receptor α (MOER) mouse. J. Biol. Chem. 284, 3488-3495
10. Pedram, A., Razandi, M., and Levin, E. R. (2006) Nature of functional estrogen receptors at the plasma membrane. Mol. Endocrinol. 20, 1996-2009
11. Kuiper, G. G., Enmark, E., Pelto-Huikko, M., Nilsson, S., and Gustafsson, J. A. (1996) Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA 93, 5925-5930
12. Seidlová-Wuttke, D., Prelle, K., Fritzemeier, K. H., and Wuttke, W. (2008) Effects of estrogen receptor alpha- and beta-selective substances in the metaphysis of the tibia and on serum parameters of bone and fat tissue metabolism of ovariectomized rats. Bone 43, 849-855
13. Pedram, A., Razandi, M., Lewis, M., Hammes, S., and Levin, E. R. (2014) Membrane-localized estrogen receptor α is required for normal organ development and function. Dev. Cell 29, 482-490
14. Pedram, A., Razandi, M., O'Mahony, F., Harvey, H., Harvey, B. J., and Levin, E. R. (2013) Estrogen reduces lipid content in the liver exclusively from membrane receptor signaling. Sci. Signal. 6, ra36
15. Chamorro-García, R., Sahu, M., Abbey, R. J., Laude, J., Pham, N., and Blumberg, B. (2013) Transgenerational inheritance of increased fat depot size, stem cell reprogramming, and hepatic steatosis elicited by prenatal exposure to the obesogen tributyltin in mice. Environ. Health Perspect. 121, 359-366
16. Trogden, B. G., Kim, S. H., Lee, S., and Katzenellenbogen, J. A. (2009) Tethered indoles as functionalizable ligands for the estrogen receptor. Bioorg. Med. Chem. Lett. 19, 485-488
17. Wong, W. P., Tiano, J. P., Liu, S., Hewitt, S. C., Le May, C., Dalle, S., Katzenellenbogen, J. A., Katzenellenbogen, B. S., Korach, K. S., and Mauvais-Jarvis, F. (2010) Extranuclear estrogen receptor-alpha stimulates NeuroD1 binding to the insulin promoter and favors insulin synthesis. Proc. Natl. Acad. Sci. USA 107, 13057-13062
18. Kirchner, S., Kieu, T., Chow, C., Casey, S., and Blumberg, B. (2010) Prenatal exposure to the environmental obesogen tributyltin predisposes multipotent stem cells to become adipocytes. Mol. Endocrinol. 24, 526-539
19. Levin, E. R. (2014) Extranuclear estrogen receptor's roles in physiology: lessons from mouse models. Am. J. Physiol. Endocrinol. Metab. 307, E133-E140
20. Harris, H. A., Katzenellenbogen, J. A., and Katzenellenbogen, B. S. (2002) Characterization of the biological roles of the estrogen receptors, ERalpha and ERbeta, in estrogen target tissues in vivo through the use of an ERalpha-selective ligand. Endocrinology 143, 4172-4177
21. Meyers, M. J., Sun, J., Carlson, K. E., Marriner, G. A., Katzenellenbogen, B. S., and Katzenellenbogen, J. A. (2001) Estrogen receptor-β potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J. Med. Chem. 44, 4230-4251
22. Razandi, M., Pedram, A., Jordan, V. C., Fuqua, S., and Levin, E. R. (2013) Tamoxifen regulates cell fate through mitochondrial estrogen receptor beta in breast cancer. Oncogene 32, 3274-3285
23. Smemo, S., Tena, J. J., Kim, K.-H., Gamazon, E. R., Sakabe, N. J., Gómez-Marín, C., Aneas, I., Credidio, F. L., Sobreira, D. R., Wasserman, N. F., Lee, J. H., Puviindran, V., Tam, D., Shen, M., Son, J. E., Vakili, N. A., Sung, H. K., Naranjo, S., Acemel, R. D., Manzanares, M., Nagy, A., Cox, N. J., Hui, C. C., Gomez-Skarmeta, J. L., and Nóbrega, M. A. (2014) Obesity-associated variants within FTO form long-range functional connections with IRX3. Nature 507, 371-375
24. Rosen, E. D., and Spiegelman, B. M. (2014) What we talk about when we talk about fat. Cell 156, 20-44DOI:
25. Anderson, L. A., McTernan, P. G., Barnett, A. H., and Kumar, S. (2001) The effects of androgens and estrogens on preadipocyte proliferation in human adipose tissue: influence of gender and site. J. Clin. Endocrinol. Metab. 86, 5045-5051
26. Harrington, W. R., Kim, S. H., Funk, C. C., Madak-Erdogan, Z., Schiff, R., Katzenellenbogen, J. A., and Katzenellenbogen, B. S. (2006) Estrogen dendrimer conjugates that preferentially activate extranuclear, nongenomic versus genomic pathways of estrogen action. Mol. Endocrinol. 20, 491-502
27. Kawaguchi, T., Takenoshita, M., Kabashima, T., and Uyeda, K. (2001) Glucose and cAMP regulate the L-type pyruvate kinase gene by phosphorylation/dephosphorylation of the carbohydrate response element binding protein. Proc. Natl. Acad. Sci. USA 98, 13710-13715
28. Herman, M. A., Peroni, O. D., Villoria, J., Schön, M. R., Abumrad, N. A., Blüher, M., Klein, S., and Kahn, B. B. (2012) A novel ChREBP isoform in adipose tissue regulates systemic glucose metabolism. Nature 484, 333-338
29. Tiano, J. P., and Mauvais-Jarvis, F. (2012) Molecular mechanisms of estrogen receptors' suppression of lipogenesis in pancreatic β-cells. Endocrinology 153, 2997-3005
30. Dentin, R., Benhamed, F., Hainault, I., Fauveau, V., Foufelle, F., Dyck, J. R., Girard, J., and Postic, C. (2006) Liver-specific inhibition of ChREBP improves hepatic steatosis and insulin resistance in ob/ob mice. Diabetes 55,2159-2170
31. Monsénégo, J., Mansouri, A., Akkaoui, M., Lenoir, V., Esnous, C., Fauveau, V., Tavernier, V., Girard, J., and Prip-Buus, C. (2012) Enhancing liver mitochondrial fatty acid oxidation capacity in obese mice improves insulin sensitivity independently of hepatic steatosis. J. Hepatol. 56, 632-639
32. Riant, E., Waget, A., Cogo, H., Arnal, J. F., Burcelin, R., and Gourdy, P. (2009) Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology 150, 2109-2117
33. Kabashima, T., Kawaguchi, T., Wadzinski, B. E., and Uyeda, K. (2003) Xylulose 5-phosphate mediates glucose-induced lipogenesis by xylulose 5-phosphate-activated protein phosphatase in rat liver. Proc. Natl. Acad. Sci. USA 100, 5107-5112
34. Shulman, G. I. (2014) Ectopic fat in insulin resistance, dyslipidemia, and cardiometabolic disease. N. Engl. J. Med. 371, 1131-1141
35. Perry, R. J., Camporez, J. P., Kursawe, R., Titchenell, P. M., Zhang, D., Perry, C. J., Jurczak, M. J., Abudukadier, A., Han, M. S., Zhang, X. M., Ruan, H. B., Yang, X., Caprio, S., Kaech, S. M., Sul, H. S., Birnbaum, M. J., Davis, R. J., Cline, G. W., Petersen, K. F., and Shulman, G. I. (2015) Hepatic acetyl CoA links adipose tissue inflammation to hepatic insulin resistance and type 2 diabetes. Cell 160, 745-758
36. Yonezawa, R., Wada, T., Matsumoto, N., Morita, M., Sawakawa, K., Ishii, Y., Sasahara, M., Tsuneki, H., Saito, S., and Sasaoka, T. (2012) Central versus peripheral impact of estradiol on the impaired glucose metabolism in ovariectomized mice on a high-fat diet. Am. J. Physiol. Endocrinol. Metab. 303, E445-E456
37. Hong, J., Holcomb, V. B., Kushiro, K., and Núñez, N. P. (2011) Estrogen inhibits the effects of obesity and alcohol on mammary tumors and fatty liver. Int. J. Oncol. 39, 1443-1453
38. Pedram, A., Razandi, M., Aitkenhead, M., and Levin, E. R. (2005) Estrogen inhibits cardiomyocyte hypertrophy in vitro: antagonism of calcineurin-related hypertrophy through induction of MCIP1. J. Biol. Chem. 280, 26339-26348
39. Pedram, A., Razandi, M., O'Mahony, F., Lubahn, D., and Levin, E. R. (2010) Estrogen receptor-beta prevents cardiac fibrosis. Mol. Endocrinol. 24, 2152-2165