Sex hormone binding globulin and insulin resistance

Clinical Endocrinology

Volumn 78, Issue 3, 2013, Pages 321-329

  Wallace, Ian R ^a,b   McKinley, Michelle C ^b   Bell, Patrick M ^a   Hunter, Steven J ^a  

^a ROYAL VICTORIA HOSPITAL   (United Kingdom)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SEX HORMONE; SEX HORMONE BINDING GLOBULIN;

CONCENTRATION (PARAMETERS); GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; INSULIN RESISTANCE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; INSULIN RESISTANCE; MALE; SEX HORMONE-BINDING GLOBULIN;

EID: 84872976910     PISSN: 03000664     EISSN: 13652265     Source Type: Journal    
DOI: 10.1111/cen.12086     Document Type: Review

References (68)

1. Ding, E.L., Song, Y., Malik, V.S., et al,. (2006) Sex differences of endogenous sex hormones and risk of type 2 diabetes: a systematic review and meta-analysis. JAMA, 295, 1288-1299.
2. Ding, E.L., Song, Y., Manson, J.E., et al,. (2009) Sex hormone-binding globulin and risk of type 2 diabetes in women and men. New England Journal of Medicine, 361, 1152-1163.
3. Perry, J.R., Weedon, M.N., Langenberg, C., et al,. (2010) Genetic evidence that raised sex hormone binding globulin (SHBG) levels reduce the risk of type 2 diabetes. Human Molecular Genetics, 19, 535-544.
4. DeFronzo, R.A., (2004) Pathogenesis of type 2 diabetes mellitus. Medical Clinics of North America, 88, 787-835.
5. Avvakumov, G.V., Cherkasov, A., Muller, Y.A., et al,. (2010) Structural analyses of sex hormone-binding globulin reveal novel ligands and function. Molecular and Cellular Endocrinology, 316, 13-23.
6. Dunn, J.F., Nisula, B.C., &, Rodbard, D., (1981) Transport of steroid hormones: binding of 21 endogenous steroids to both testosterone-binding globulin and corticosteroid-binding globulin in human plasma. Journal of Clinical Endocrinology and Metabolism, 53, 58-68. (Pubitemid 13245381)
7. Berube, D., Seralini, G.E., Gagne, R., et al,. (1990) Localization of the human sex hormone-binding globulin gene (SHBG) to the short arm of chromosome 17 (17p12-p13). Cytogenetics and Cell Genetics, 54, 65-67.
8. Hammond, G.L., (2011) Diverse roles for sex hormone-binding globulin in reproduction. Biology of Reproduction, 85, 431-441.
9. Edmunds, S.E., Stubbs, A.P., Santos, A.A., et al,. (1990) Estrogen and androgen regulation of sex hormone binding globulin secretion by a human liver cell line. Journal of Steroid Biochemistry and Molecular Biology, 37, 733-739.
10. Strel'chyonok, O.A., Avvakumov, G.V., &, Survilo, L.I., (1984) A recognition system for sex-hormone-binding protein-estradiol complex in human decidual endometrium plasma membranes. Biochimica et Biophysica Acta, 802, 459-466. (Pubitemid 15199805)
11. Rosner, W., Hryb, D.J., Khan, M.S., et al,. (1998) Androgens, estrogens, and second messengers. Steroids, 63, 278-281. (Pubitemid 28265660)
12. Rosner, W., Hryb, D.J., Kahn, S.M., et al,. (2010) Interactions of sex hormone-binding globulin with target cells. Molecular and Cellular Endocrinology, 316, 79-85.
13. Hammes, A., Andreassen, T.K., Spoelgen, R., et al,. (2005) Role of endocytosis in cellular uptake of sex steroids. Cell, 122, 751-762. (Pubitemid 41242639)
14. Willnow, T.E., &, Nykjaer, A., (2010) Cellular uptake of steroid carrier proteins-mechanisms and implications. Molecular and Cellular Endocrinology, 316, 93-102.
15. Rosner, W., Hryb, D.J., Khan, M.S., et al,. (1999) Androgen and estrogen signalling at the cell membrane via G-proteins and cyclic adenosine monophosphate. Steroids, 64, 100-106. (Pubitemid 29168593)
16. Nakhla, A.M., Leonard, J., Hryb, D.J., et al,. (1999) Sex hormone-binding globulin receptor signal transduction proceeds via a G protein. Steroids, 64, 213-216. (Pubitemid 29283674)
17. Mendel, C.M., (1989) The free hormone hypothesis: a physiologically based mathematical model. Endocrine Reviews, 10, 232-274. (Pubitemid 19223060)
18. Le, T.N., Nestler, J.E., Strauss, J.F. III, et al,. (2012) Sex hormone-binding globulin and type 2 diabetes mellitus. Trends in Endocrinology and Metabolism, 23, 32-40.
19. Lakshman, K.M., Bhasin, S., &, Araujo, A.B., (2010) Sex hormone-binding globulin as an independent predictor of incident type 2 diabetes mellitus in men. Journals of Gerontology, Series A, Biological Sciences and Medical Sciences, 65, 503-509.
20. Vikan, T., Schirmer, H., Njolstad, I., et al,. (2010) Low testosterone and sex hormone-binding globulin levels and high estradiol levels are independent predictors of type 2 diabetes in men. European Journal of Endocrinology, 162, 747-754.
21. Kupelian, V., Hayes, F.J., Link, C.L., et al,. (2008) Inverse association of testosterone and the metabolic syndrome in men is consistent across race and ethnic groups. Journal of Clinical Endocrinology and Metabolism, 93, 3403-3410.
22. Stumvoll, M., Goldstein, B.J., &, van Haeften, T.W., (2005) Type 2 diabetes: principles of pathogenesis and therapy. Lancet, 365, 1333-1346.
23. Laaksonen, D.E., Niskanen, L., Punnonen, K., et al,. (2003) Sex hormones, inflammation and the metabolic syndrome: a population-based study. European Journal of Endocrinology, 149, 601-608. (Pubitemid 38054707)
24. Chubb, S.A., Hyde, Z., Almeida, O.P., et al,. (2008) Lower sex hormone-binding globulin is more strongly associated with metabolic syndrome than lower total testosterone in older men: the Health in Men Study. European Journal of Endocrinology, 158, 785-792. (Pubitemid 351837366)
25. Bhasin, S., Jasjua, G.K., Pencina, M., et al,. (2011) Sex hormone-binding globulin, but not testosterone, is associated prospectively and independently with incident metabolic syndrome in men: the framingham heart study. Diabetes Care, 34, 2464-2470.
26. Laaksonen, D.E., Niskanen, L., Punnonen, K., et al,. (2004) Testosterone and sex hormone-binding globulin predict the metabolic syndrome and diabetes in middle-aged men. Diabetes Care, 27, 1036-1041. (Pubitemid 38579762)
27. Brand, J.S., Wareham, N.J., Dowsett, M., et al,. (2011) Associations of endogenous testosterone and SHBG with glycated haemoglobin in middle-aged and older men. Clinical Endocrinology (Oxford), 74, 572-578.
28. Page-Wilson, G., Goulart, A.C., &, Rexrode, K.M., (2009) Interrelation between sex hormones and plasma sex hormone-binding globulin and hemoglobin A1c in healthy postmenopausal women. Metabolic Syndrome and Related Disorders, 7, 249-254.
29. Nestler, J.E., Powers, L.P., Matt, D.W., et al,. (1991) A direct effect of hyperinsulinemia on serum sex hormone-binding globulin levels in obese women with the polycystic ovary syndrome. Journal of Clinical Endocrinology and Metabolism, 72, 83-89. (Pubitemid 21921660)
30. Moran, L.J., Misso, M.L., Wild, R.A., et al,. (2010) Impaired glucose tolerance, type 2 diabetes and metabolic syndrome in polycystic ovary syndrome: a systematic review and meta-analysis. Human Reproduction Update, 16, 347-363.
31. Haffner, S.M., Katz, M.S., Stern, M.P., et al,. (1989) Association of decreased sex hormone binding globulin and cardiovascular risk factors. Arteriosclerosis, 9, 136-143. (Pubitemid 19046100)
32. Koshida, H., Takeda, R., &, Miyamori, I., (1998) Lisinopril decreases plasma free testosterone in male hypertensive patients and increases sex hormone binding globulin in female hypertensive patients. Hypertension Research, 21, 279-282. (Pubitemid 29017340)
33. Michos, E.D., Vaidya, D., Gapstur, S.M., et al,. (2008) Sex hormones, sex hormone binding globulin, and abdominal aortic calcification in women and men in the multi-ethnic study of atherosclerosis (MESA). Atherosclerosis, 200, 432-438.
34. Ouyang, P., Vaidya, D., Dobs, A., et al,. (2009) Sex hormone levels and subclinical atherosclerosis in postmenopausal women: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis, 204, 255-261.
35. Vassilatou, E., Lafoyianni, S., Vryonidou, A., et al,. (2010) Increased androgen bioavailability is associated with non-alcoholic fatty liver disease in women with polycystic ovary syndrome. Human Reproduction, 25, 212-220.
36. Endre, T., Mattiasson, I., Berglund, G., et al,. (1996) Low testosterone and insulin resistance in hypertension-prone men. Journal of Human Hypertension, 10, 755-761. (Pubitemid 27046048)
37. Pitteloud, N., Mootha, V.K., Dwyer, A.A., et al,. (2005) Relationship between testosterone levels, insulin sensitivity, and mitochondrial function in men. Diabetes Care, 28, 1636-1642. (Pubitemid 41340902)
38. DeFronzo, R.A., Tobin, J.D., &, Andres, R., (1979) Glucose clamp technique: a method for quantifying insulin secretion and resistance. American Journal of Physiology, 237, E214-E223. (Pubitemid 9249478)
39. Matthews, D.R., Hosker, J.P., Rudenski, A.S., et al,. (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia, 28, 412-419. (Pubitemid 15018832)
40. Katz, A., Nambi, S.S., Mather, K., et al,. (2000) Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. Journal of Clinical Endocrinology and Metabolism, 85, 2402-2410. (Pubitemid 32269192)
41. Li, C., Ford, E.S., Li, B., et al,. (2010) Association of testosterone and sex hormone-binding globulin with metabolic syndrome and insulin resistance in men. Diabetes Care, 33, 1618-1624.
42. Akin, F., Bastemir, M., &, Alkis, E., (2007) Effect of insulin sensitivity on SHBG levels in premenopausal versus postmenopausal obese women. Advances in Therapy, 24, 1210-1220. (Pubitemid 351612227)
43. Akin, F., Bastemir, M., Alkis, E., et al,. (2009) SHBG levels correlate with insulin resistance in postmenopausal women. European Journal of Internal Medicine, 20, 162-167.
44. Yasui, T., Tomita, J., Miyatani, Y., et al,. (2007) Associations of adiponectin with sex hormone-binding globulin levels in aging male and female populations. Clinica Chimica Acta, 386, 69-75. (Pubitemid 47417965)
45. Davis, S.R., Robinson, P.J., Moufarege, A., et al,. (2011) The contribution of SHBG to the variation in HOMA-IR is not dependent on endogenous oestrogen or androgen levels in postmenopausal women. Clinical Endocrinology (Oxford), 77, 541-547.
46. Reinecke, H., Bogdanski, J., Woltering, A., et al,. (2002) Relation of serum levels of sex hormone binding globulin to coronary heart disease in postmenopausal women. American Journal of Cardiology, 90, 364-368.
47. Gannage-Yared, M.H., Khalife, S., Semaan, M., et al,. (2006) Serum adiponectin and leptin levels in relation to the metabolic syndrome, androgenic profile and somatotropic axis in healthy non-diabetic elderly men. European Journal of Endocrinology, 155, 167-176. (Pubitemid 44103386)
48. Rajala, U.M., Keinanen-Kiukaanniemi, S.M., Hirsso, P.K., et al,. (2007) Associations of total testosterone and sex hormone-binding globulin levels with insulin sensitivity in middle-aged Finnish men. Diabetes Care, 30, e13. (Pubitemid 46556615)
49. Oh, J.Y., Barrett-Connor, E., Wedick, N.M., et al,. (2002) Endogenous sex hormones and the development of type 2 diabetes in older men and women: the Rancho Bernardo study. Diabetes Care, 25, 55-60. (Pubitemid 41070783)
50. Cagnacci, A., Soldani, R., Carriero, P.L., et al,. (1992) Effects of low doses of transdermal 17 beta-estradiol on carbohydrate metabolism in postmenopausal women. Journal of Clinical Endocrinology and Metabolism, 74, 1396-1400.
51. Godsland, I.F., Walton, C., Felton, C., et al,. (1992) Insulin resistance, secretion, and metabolism in users of oral contraceptives. Journal of Clinical Endocrinology and Metabolism, 74, 64-70.
52. Watanabe, R.M., Azen, C.G., Roy, S., et al,. (1994) Defects in carbohydrate metabolism in oral contraceptive users without apparent metabolic risk factors. Journal of Clinical Endocrinology and Metabolism, 79, 1277-1283. (Pubitemid 24369836)
53. Shifren, J.L., Desindes, S., McIlwain, M., et al,. (2007) A randomized, open-label, crossover study comparing the effects of oral versus transdermal estrogen therapy on serum androgens, thyroid hormones, and adrenal hormones in naturally menopausal women. Menopause, 14, 985-994. (Pubitemid 350098657)
54. de Lauzon-Guillain, B., Fournier, A., Fabre, A., et al,. (2009) Menopausal hormone therapy and new-onset diabetes in the French Etude Epidemiologique de Femmes de la Mutuelle Generale de l'Education Nationale (E3N) cohort. Diabetologia, 52, 2092-2100.
55. Sieminska, L., Wojciechowska, C., Niedziolka, D., et al,. (2005) Effect of postmenopause and hormone replacement therapy on serum adiponectin levels. Metabolism: Clinical and Experimental, 54, 1610-1614. (Pubitemid 41728152)
56. Miller, K.K., Rosner, W., Lee, H., et al,. (2004) Measurement of free testosterone in normal women and women with androgen deficiency: comparison of methods. Journal of Clinical Endocrinology and Metabolism, 89, 525-533. (Pubitemid 38269853)
57. Vermeulen, A., Verdonck, L., &, Kaufman, J.M., (1999) A critical evaluation of simple methods for the estimation of free testosterone in serum. Journal of Clinical Endocrinology and Metabolism, 84, 3666-3672. (Pubitemid 30645223)
58. Ho, C.K., Stoddart, M., Walton, M., et al,. (2006) Calculated free testosterone in men: comparison of four equations and with free androgen index. Annals of Clinical Biochemistry, 43, 389-397. (Pubitemid 44526539)
59. Plymate, S.R., Matej, L.A., Jones, R.E., et al,. (1988) Inhibition of sex hormone-binding globulin production in the human hepatoma (Hep G2) cell line by insulin and prolactin. Journal of Clinical Endocrinology and Metabolism, 67, 460-464.
60. Pasquali, R., Casimirri, F., De Iasio, R., et al,. (1995) Insulin regulates testosterone and sex hormone-binding globulin concentrations in adult normal weight and obese men. Journal of Clinical Endocrinology and Metabolism, 80, 654-658.
61. Crave, J.C., Lejeune, H., Brebant, C., et al,. (1995) Differential effects of insulin and insulin-like growth factor I on the production of plasma steroid-binding globulins by human hepatoblastoma-derived (Hep G2) cells. Journal of Clinical Endocrinology and Metabolism, 80, 1283-1289.
62. Haffner, S.M., Katz, M.S., &, Dunn, J.F., (1990) The relationship of insulin sensitivity and metabolic clearance of insulin to adiposity and sex hormone binding globulin. Endocrine Research, 16, 361-376.
63. Selva, D.M., Hogeveen, K.N., Innis, S.M., et al,. (2007) Monosaccharide-induced lipogenesis regulates the human hepatic sex hormone-binding globulin gene. The Journal of Clinical Investigation, 117, 3979-3987. (Pubitemid 350224107)
64. Pasquali, R., Gambineri, A., Biscotti, D., et al,. (2000) Effect of long-term treatment with metformin added to hypocaloric diet on body composition, fat distribution, and androgen and insulin levels in abdominally obese women with and without the polycystic ovary syndrome. Journal of Clinical Endocrinology and Metabolism, 85, 2767-2774. (Pubitemid 32269149)
65. Azziz, R., Ehrmann, D., Legro, R.S., et al,. (2001) Troglitazone improves ovulation and hirsutism in the polycystic ovary syndrome: a multicenter, double blind, placebo-controlled trial. Journal of Clinical Endocrinology and Metabolism, 86, 1626-1632. (Pubitemid 32374915)
66. Selva, D.M., &, Hammond, G.L., (2009) Peroxisome-proliferator receptor gamma represses hepatic sex hormone-binding globulin expression. Endocrinology, 150, 2183-2189.
67. Petra, P.H., (1991) The plasma sex steroid binding protein (SBP or SHBG). A critical review of recent developments on the structure, molecular biology and function. Journal of Steroid Biochemistry and Molecular Biology, 40, 735-753.
68. Khan, M.S., Hryb, D.J., Hashim, G.A., et al,. (1990) Delineation and synthesis of the membrane receptor-binding domain of sex hormone-binding globulin. Journal of Biological Chemistry, 265, 18362-18365.