Hepatic overexpression of steroid sulfatase ameliorates mouse models of obesity and type 2 diabetes through sex-specific mechanisms

Journal of Biological Chemistry

Volumn 289, Issue 12, 2014, Pages 8086-8097

  Jiang, Mengxi ^a   He, Jinhan ^a   Kucera, Heidi ^b   Gaikwad, Nilesh W ^b   Zhang, Bin ^a   Xu, Meishu ^a   O'Doherty, Robert M ^c   Selcer, Kyle W ^d   Xie, Wen ^a,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d DUQUESNE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE EXPRESSION; MAMMALS; MUSCLE; NUTRITION; PATHOLOGY; SULFUR COMPOUNDS;

ENERGY EXPENDITURE; FUNCTIONAL RELEVANCE; INSULIN SENSITIVITY; METABOLIC FUNCTION; METABOLIC MECHANISM; METABOLIC SYNDROMES; PROTECTIVE EFFECTS; WHITE ADIPOSE TISSUES;

METABOLISM;

ESTROGEN; MESSENGER RNA; STERYL SULFATASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; ENERGY EXPENDITURE; ENERGY METABOLISM; ESTROGEN ACTIVITY; EXPERIMENTAL MOUSE; FATTY LIVER; FEMALE; GENE OVEREXPRESSION; GLUCOSE METABOLISM; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PHASE TRANSITION; PRIORITY JOURNAL; SKELETAL MUSCLE; STS GENE;

DIABETES; ENERGY METABOLISM; ESTROGEN; OBESITY; STEROID HORMONE; TRANSGENIC MICE;

ANIMALS; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; ESTROGENS; FATTY LIVER; FEMALE; INSULIN RESISTANCE; LIVER; MALE; MICE; MICE, TRANSGENIC; OBESITY; STERYL-SULFATASE; UP-REGULATION;

EID: 84896951643     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.535914     Document Type: Article

References (40)

1. Mauvais-Jarvis, F., Clegg, D. J., and Hevener, A. L. (2013) The role of estrogens in control of energy balance and glucose homeostasis. Endocr. Rev. 34, 309-338
2. Carr, M. C. (2003) The emergence of the metabolic syndrome with menopause. J. Clin. Endocrinol. Metab. 88, 2404-2411
3. Margolis, K. L., Bonds, D. E., Rodabough, R. J., Tinker, L., Phillips, L. S., Allen, C., Bassford, T., Burke, G., Torrens, J., and Howard, B. V. (2004) Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women. Results from the Women's Health Initiative Hormone Trial. Diabetologia 47, 1175-1187 (Pubitemid 39093314)
4. Zhu, L., Brown, W. C., Cai, Q., Krust, A., Chambon, P., McGuinness, O. P., and Stafford, J. M. (2013) Estrogen treatment after ovariectomy protects against fatty liver and may improve pathway-selective insulin resistance. Diabetes 62, 424-434
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-α knockout mice. Proc. Natl. Acad. Sci. U.S.A. 97, 12729-12734
6. Jones, M. E., Thorburn, A. W., Britt, K. L., Hewitt, K. N., Wreford, N. G., Proietto, J., Oz, O. K., Leury, B. J., Robertson, K. M., Yao, S., and Simpson, E. R. (2000) Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity. Proc. Natl. Acad. Sci. U.S.A. 97, 12735-12740
7. Hewitt, K. N., Pratis, K., Jones, M. E., and Simpson, E. R. (2004) Estrogen replacement reverses the hepatic steatosis phenotype in the male aromatase knockout mouse. Endocrinology 145, 1842-1848 (Pubitemid 38402393)
8. Smith, E. P., Boyd, J., Frank, G. R., Takahashi, H., Cohen, R. M., Specker, B., Williams, T. C., Lubahn, D. B., and Korach, K. S. (1994) Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N. Engl. J. Med. 331, 1056-1061 (Pubitemid 24317698)
9. Morishima, A., Grumbach, M. M., Simpson, E. R., Fisher, C., and Qin, K. (1995) Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J. Clin. Endocrinol. Metab. 80, 3689-3698
10. Friday, K. E., Dong, C., and Fontenot, R. U. (2001) Conjugated equine estrogen improves glycemic control and blood lipoproteins in postmenopausal women with type 2 diabetes. J. Clin. Endocrinol. Metab. 86, 48-52 (Pubitemid 32109774)
11. Billeci, A. M., Paciaroni, M., Caso, V., and Agnelli, G. (2008) Hormone replacement therapy and stroke. Curr. Vasc. Pharmacol. 6, 112-123
12. Falany, C. N. (1997) Enzymology of human cytosolic sulfotransferases. FASEB J. 11, 206-216
13. Reed, M. J., Purohit, A., Woo, L. W., Newman, S. P., and Potter, B. V. (2005) Steroid sulfatase. Molecular biology, regulation, and inhibition. Endocr. Rev. 26, 171-202
14. Hazan, C., Orlow, S. J., and Schaffer, J. V. (2005) X-linked recessive ichthyosis. Dermatol. Online J. 11, 12
15. Gao, J., He, J., Shi, X., Stefanovic-Racic, M., Xu, M., O'Doherty, R. M., Garcia-Ocana, A., and Xie, W. (2012) Sex-specific effect of estrogen sulfotransferase on mouse models of type 2 diabetes. Diabetes 61, 1543-1551
16. Saini, S. P., Sonoda, J., Xu, L., Toma, D., Uppal, H., Mu, Y., Ren, S., Moore, D. D., Evans, R. M., and Xie, W. (2004) A novel constitutive androstane receptor-mediated and CYP3A-independent pathway of bile acid detoxification. Mol. Pharmacol. 65, 292-300 (Pubitemid 38134256)
17. Zhou, J., Zhai, Y., Mu, Y., Gong, H., Uppal, H., Toma, D., Ren, S., Evans, R. M., and Xie, W. (2006) A novel pregnane X receptor-mediated and sterol regulatory element-binding protein-independent lipogenic pathway. J. Biol. Chem. 281, 15013-15020 (Pubitemid 43855205)
18. Borthwick, E. B., Houston, M. P., Coughtrie, M. W., and Burchell, A. (2001) The antihyperglycemic effect of estrone sulfate in genetically obese-diabetic (ob/ob) mice is associated with reduced hepatic glucose-6- phosphatase. Horm. Metab. Res. 33, 721-726 (Pubitemid 34048834)
19. Gao, J., He, J., Zhai, Y., Wada, T., and Xie, W. (2009) The constitutive androstane receptor is an anti-obesity nuclear receptor that improves insulin sensitivity. J. Biol. Chem. 284, 25984-25992
20. Cani, P. D., Knauf, C., Iglesias, M. A., Drucker, D. J., Delzenne, N. M., and Burcelin, R. (2006) Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like peptide 1 receptor. Diabetes 55, 1484-1490 (Pubitemid 44195391)
21. Al-Dosari, M. S., Knapp, J. E., and Liu, D. (2006) Activation of human CYP2C9 promoter and regulation by CAR and PXR in mouse liver. Mol. Pharm. 3, 322-328 (Pubitemid 44021438)
22. Gaikwad, N. W. (2013) Ultra performance liquid chromatography-tandem mass spectrometry method for profiling of steroid metabolome in human tissue. Anal. Chem. 85, 4951-4960
23. He, J., Gao, J., Xu, M., Ren, S., Stefanovic-Racic, M., O'Doherty, R. M., and Xie, W. (2013) PXR ablation alleviates diet-induced and genetic obesity and insulin resistance in mice. Diabetes 62, 1876-1887
24. Xie, W., Barwick, J. L., Downes, M., Blumberg, B., Simon, C. M., Nelson, M. C., Neuschwander-Tetri, B. A., Brunt, E. M., Guzelian, P. S., and Evans, R. M. (2000) Humanized xenobiotic response in mice expressing nuclear receptor SXR. Nature 406, 435-439 (Pubitemid 30625566)
25. Lin, X., Yue, P., Chen, Z., and Schonfeld, G. (2005) Hepatic triglyceride contents are genetically determined in mice. Results of a strain survey. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G1179-G1189 (Pubitemid 40741070)
26. Hawkins, R. A., and Oakey, R. E. (1974) Estimation of oestrone sulphate, oestradiol-17β and oestrone in peripheral plasma. Concentrations during the menstrual cycle and in men. J. Endocrinol. 60, 3-17
27. Gao, H., Bryzgalova, G., Hedman, E., Khan, A., Efendic, S., Gustafsson, J. A., and Dahlman-Wright, K. (2006) 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 (Pubitemid 43801232)
28. Bryzgalova, G., Lundholm, L., Portwood, N., Gustafsson, J. A., Khan, A., Efendic, S., and Dahlman-Wright, K. (2008) Mechanisms of antidiabetogenic and body weight-lowering effects of estrogen in high-fat diet-fed mice. Am. J. Physiol. Endocrinol. Metab. 295, E904-E912
29. Leiter, E. H., and Chapman, H. D. (1994) Obesity-induced diabetes (diabesity) in C57BL/KsJ mice produces aberrant trans-regulation of sex steroid sulfotransferase genes. J. Clin. Invest. 93, 2007-2013 (Pubitemid 24143080)
30. 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
31. Tiano, J. P., and Mauvais-Jarvis, F. (2012) Importance of oestrogen receptors to preserve functional beta-cell mass in diabetes. Nat. Rev. Endocrinol. 8, 342-351
32. Finan, B., Yang, B., Ottaway, N., Stemmer, K., Müller, T. D., Yi, C. X., Habegger, K., Schriever, S. C., García-Caceres, C., Kabra, D. G., Hembree, J., Holland, J., Raver, C., Seeley, R. J., Hans, W., Irmler, M., Beckers, J., de Angelis, M. H., Tiano, J. P., Mauvais-Jarvis, F., Perez-Tilve, D., Pfluger, P., Zhang, L., Gelfanov, V., DiMarchi, R. D., and Tschöp, M. H. (2012) Targeted estrogen delivery reverses the metabolic syndrome. Nat. Med. 18, 1847-1856
33. Aoki, K., Nakajima, A., Mukasa, K., Osawa, E., Mori, Y., and Sekihara, H. (2003) Prevention of diabetes, hepatic injury, and colon cancer with dehydroepiandrosterone. J. Steroid Biochem. Mol. Biol. 85, 469-472 (Pubitemid 37011123)
34. Webster, D., France, J. T., Shapiro, L. J., and Weiss, R. (1978) X-linked ichthyosis due to steroid-sulphatase deficiency. Lancet 1, 70-72
35. Brookes, K. J., Hawi, Z., Kirley, A., Barry, E., Gill, M., and Kent, L. (2008) Association of the steroid sulfatase (STS) gene with attention deficit hyperactivity disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 147B, 1531-1535
36. Kent, L., Emerton, J., Bhadravathi, V., Weisblatt, E., Pasco, G., Willatt, L. R., McMahon, R., and Yates, J. R. (2008) X-linked ichthyosis (steroid sulfatase deficiency) is associated with increased risk of attention deficit hyperactivity disorder, autism and social communication deficits. J. Med. Genet. 45, 519-524
37. Maltais, R., and Poirier, D. (2011) Steroid sulfatase inhibitors. A review covering the promising 2000-2010 decade. Steroids 76, 929-948
38. Stanway, S. J., Purohit, A., Woo, L. W., Sufi, S., Vigushin, D., Ward, R., Wilson, R. H., Stanczyk, F. Z., Dobbs, N., Kulinskaya, E., Elliott, M., Potter, B. V., Reed, M. J., and Coombes, R. C. (2006) Phase I study of STX 64 (667 Coumate) in breast cancer patients. The first study of a steroid sulfatase inhibitor. Clin. Cancer Res. 12, 1585-1592
39. Petro, A. E., Cotter, J., Cooper, D. A., Peters, J. C., Surwit, S. J., and Surwit, R. S. (2004) Fat, carbohydrate, and calories in the development of diabetes and obesity in the C57BL/6J mouse. Metabolism 53, 454-457 (Pubitemid 38419187)
40. Schaffer, J. E. (2003) Lipotoxicity. When tissues overeat. Curr. Opin. Lipidol. 14, 281-287