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Published in: Endocrine 3/2017

01-06-2017 | Original Article

Follicle stimulating hormone, its novel association with sex hormone binding globulin in men and postmenopausal women

Authors: Ningjian Wang, Kun Zhang, Bing Han, Qin Li, Yi Chen, Chunfang Zhu, Yingchao Chen, Fangzhen Xia, Hualing Zhai, Boren Jiang, Zhoujun Shen, Yingli Lu

Published in: Endocrine | Issue 3/2017

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Abstract

Purpose

Follicle stimulating hormone plays direct roles in a variety of nongonadal tissues and sex hormone binding globulin is becoming the convergence of the crosstalk among metabolic diseases. However, no studies have explored the association between follicle stimulating hormone and sex hormone binding globulin. We aimed to study this association among men and women.

Methods

SPECT-China is a population-based study conducted since 2014. This study included 4206 men and 2842 postmenopausal women. Collected serum was assayed for gonadotropins, sex hormone binding globulin, sex hormones etc. Regression analyses were performed to assess the relationship between sex hormone binding globulin and follicle stimulating hormone and other variables including metabolic factors, thyroid function and sex hormones. Treatment with follicle stimulating hormone at different concentrations of 0, 5, 50 and 100 IU/L for 24 h was performed in HepG2 cells.

Results

In Spearman correlation, sex hormone binding globulin was significantly correlated with FSH, triglycerides, thyroxins, body mass index and blood pressure in men and postmenopausal women (all P < 0.05). In regression analyses, follicle stimulating hormone was a significant predictor of sex hormone binding globulin in men and postmenopausal women (P < 0.05), independent of above variables. Follicle stimulating hormone induced sex hormone binding globulin expression in a dose-dependent fashion in HepG2 cells.

Conclusion

Serum follicle stimulating hormone levels were positively associated with circulating sex hormone binding globulin levels in men and postmenopausal women. This association is independent of age, insulin resistance, hepatic function, lipid profile, thyroid function, adiposity, blood pressure, and endogenous sex hormones.
Literature
1.
go back to reference Y. Song, E.S. Wang, L.L. Xing, S. Shi, F. Qu, D. Zhang, J.Y. Li, J. Shu, Y. Meng, J.Z. Sheng, J.H. Zhou, H.F. Huang, Follicle-stimulating hormone induces postmenopausal dyslipidemia through inhibiting hepatic cholesterol metabolism. J. Clin. Endocrinol. Metab. 101, 254–263 (2016)CrossRefPubMed Y. Song, E.S. Wang, L.L. Xing, S. Shi, F. Qu, D. Zhang, J.Y. Li, J. Shu, Y. Meng, J.Z. Sheng, J.H. Zhou, H.F. Huang, Follicle-stimulating hormone induces postmenopausal dyslipidemia through inhibiting hepatic cholesterol metabolism. J. Clin. Endocrinol. Metab. 101, 254–263 (2016)CrossRefPubMed
2.
go back to reference H. Cui, G. Zhao, R. Liu, M. Zheng, J. Chen, J. Wen, FSH stimulates lipid biosynthesis in chicken adipose tissue by upregulating the expression of its receptor FSHR. J. Lipid. Res. 53, 909–917 (2012)CrossRefPubMedPubMedCentral H. Cui, G. Zhao, R. Liu, M. Zheng, J. Chen, J. Wen, FSH stimulates lipid biosynthesis in chicken adipose tissue by upregulating the expression of its receptor FSHR. J. Lipid. Res. 53, 909–917 (2012)CrossRefPubMedPubMedCentral
3.
go back to reference L. Sun, Y. Peng, A.C. Sharrow, J. Iqbal, Z. Zhang, D.J. Papachristou, S. Zaidi, L.L. Zhu, B.B. Yaroslavskiy, H. Zhou, A. Zallone, M.R. Sairam, T.R. Kumar, W. Bo, J. Braun, L. Cardoso-Landa, M.B. Schaffler, B.S. Moonga, H.C. Blair, M. Zaidi, FSH directly regulates bone mass. Cell. 125, 247–260 (2006)CrossRefPubMed L. Sun, Y. Peng, A.C. Sharrow, J. Iqbal, Z. Zhang, D.J. Papachristou, S. Zaidi, L.L. Zhu, B.B. Yaroslavskiy, H. Zhou, A. Zallone, M.R. Sairam, T.R. Kumar, W. Bo, J. Braun, L. Cardoso-Landa, M.B. Schaffler, B.S. Moonga, H.C. Blair, M. Zaidi, FSH directly regulates bone mass. Cell. 125, 247–260 (2006)CrossRefPubMed
4.
go back to reference J.A. Stilley, D.E. Christensen, K.B. Dahlem, R. Guan, D.A. Santillan, S.K. England, A. Al-Hendy, P.A. Kirby, D.L. Segaloff, FSH receptor (FSHR) expression in human extragonadal reproductive tissues and the developing placenta, and the impact of its deletion on pregnancy in mice. Biol. Reprod. 91, 74 (2014)CrossRefPubMedPubMedCentral J.A. Stilley, D.E. Christensen, K.B. Dahlem, R. Guan, D.A. Santillan, S.K. England, A. Al-Hendy, P.A. Kirby, D.L. Segaloff, FSH receptor (FSHR) expression in human extragonadal reproductive tissues and the developing placenta, and the impact of its deletion on pregnancy in mice. Biol. Reprod. 91, 74 (2014)CrossRefPubMedPubMedCentral
5.
go back to reference J.F. Randolph Jr, H. Zheng, M.R. Sowers, C. Crandall, S. Crawford, E.B. Gold, M. Vuga, Change in follicle-stimulating hormone and estradiol across the menopausal transition: effect of age at the final menstrual period. J. Clin. Endocrinol. Metab. 96, 746–754 (2011)CrossRefPubMed J.F. Randolph Jr, H. Zheng, M.R. Sowers, C. Crandall, S. Crawford, E.B. Gold, M. Vuga, Change in follicle-stimulating hormone and estradiol across the menopausal transition: effect of age at the final menstrual period. J. Clin. Endocrinol. Metab. 96, 746–754 (2011)CrossRefPubMed
6.
go back to reference N. Wang, Q. Li, B. Han, Y. Chen, C. Zhu, Y. Chen, F. Xia, M. Lu, Y. Meng, Y. Guo, L. Ye, C. Sui, L. Kuang, D. Lin, Y. Lu, Follicle-stimulating hormone is associated with non-alcoholic fatty liver disease in Chinese women over 55 years old. J. Gastroenterol. Hepatol. 31, 1196–1202 (2016)CrossRefPubMed N. Wang, Q. Li, B. Han, Y. Chen, C. Zhu, Y. Chen, F. Xia, M. Lu, Y. Meng, Y. Guo, L. Ye, C. Sui, L. Kuang, D. Lin, Y. Lu, Follicle-stimulating hormone is associated with non-alcoholic fatty liver disease in Chinese women over 55 years old. J. Gastroenterol. Hepatol. 31, 1196–1202 (2016)CrossRefPubMed
7.
go back to reference N. Wang, L. Kuang, B. Han, Q. Li, Y. Chen, C. Zhu, Y. Chen, F. Xia, Z. Cang, C. Zhu, M. Lu, Y. Meng, H. Guo, C. Chen, D. Lin, Y. Lu, Follicle-stimulating hormone associates with prediabetes and diabetes in postmenopausal women. Acta. Diabetol. 53, 227–236 (2016)CrossRefPubMed N. Wang, L. Kuang, B. Han, Q. Li, Y. Chen, C. Zhu, Y. Chen, F. Xia, Z. Cang, C. Zhu, M. Lu, Y. Meng, H. Guo, C. Chen, D. Lin, Y. Lu, Follicle-stimulating hormone associates with prediabetes and diabetes in postmenopausal women. Acta. Diabetol. 53, 227–236 (2016)CrossRefPubMed
8.
go back to reference A. Stefanska, I. Ponikowska, M. Cwiklinska-Jurkowska, G. Sypniewska, Association of FSH with metabolic syndrome in postmenopausal women: A comparison with CRP, adiponectin and leptin. Biomark. Med. 8, 921–930 (2014)CrossRefPubMed A. Stefanska, I. Ponikowska, M. Cwiklinska-Jurkowska, G. Sypniewska, Association of FSH with metabolic syndrome in postmenopausal women: A comparison with CRP, adiponectin and leptin. Biomark. Med. 8, 921–930 (2014)CrossRefPubMed
9.
go back to reference R. Simó, C. Sáez-López, A. Barbosa-Desongles, C. Hernández, D.M. Selva, Novel insights in SHBG regulation and clinical implications. Trends Endocrinol. Metab. 26, 376–383 (2015)CrossRefPubMed R. Simó, C. Sáez-López, A. Barbosa-Desongles, C. Hernández, D.M. Selva, Novel insights in SHBG regulation and clinical implications. Trends Endocrinol. Metab. 26, 376–383 (2015)CrossRefPubMed
11.
go back to reference S. Liedtke, M.E. Schmidt, A. Vrieling, A. Lukanova, S. Becker, R. Kaaks, A.K. Zaineddin, K. Buck, A. Benner, J. Chang-Claude, K. Steindorf, Postmenopausal sex hormones in relation to body fat distribution. Obesity 20, 1088–1095 (2012)CrossRefPubMed S. Liedtke, M.E. Schmidt, A. Vrieling, A. Lukanova, S. Becker, R. Kaaks, A.K. Zaineddin, K. Buck, A. Benner, J. Chang-Claude, K. Steindorf, Postmenopausal sex hormones in relation to body fat distribution. Obesity 20, 1088–1095 (2012)CrossRefPubMed
12.
go back to reference E.L. Ding, Y. Song, J.E. Manson, D.J. Hunter, C.C. Lee, N. Rifai, J.E. Buring, J.M. Gaziano, S. Liu, Sex hormone-binding globulin and risk of type 2 diabetes in women and men. N. Engl. J. Med. 361, 1152–1163 (2009)CrossRefPubMedPubMedCentral E.L. Ding, Y. Song, J.E. Manson, D.J. Hunter, C.C. Lee, N. Rifai, J.E. Buring, J.M. Gaziano, S. Liu, Sex hormone-binding globulin and risk of type 2 diabetes in women and men. N. Engl. J. Med. 361, 1152–1163 (2009)CrossRefPubMedPubMedCentral
13.
go back to reference D.E. Laaksonen, L. Niskanen, K. Punnonen, K. Nyyssönen, T.P. Tuomainen, V.P. Valkonen, R. Salonen, J.T. Salonen, Testosterone and sex hormone-binding globulin predict the metabolic syndrome and diabetes in middle-aged men. Diabetes Care 27, 1036–1041 (2004)CrossRefPubMed D.E. Laaksonen, L. Niskanen, K. Punnonen, K. Nyyssönen, T.P. Tuomainen, V.P. Valkonen, R. Salonen, J.T. Salonen, Testosterone and sex hormone-binding globulin predict the metabolic syndrome and diabetes in middle-aged men. Diabetes Care 27, 1036–1041 (2004)CrossRefPubMed
14.
go back to reference K. Sutton-Tyrrell, R.P. Wildman, K.A. Matthews, C. Chae, B.L. Lasley, S. Brockwell, R.C. Pasternak, D. Lloyd-Jones, M.F. Sowers, J.I. Torréns; SWAN Investigators: Sex-hormone-binding globulin and the free androgen index are related to cardiovascular risk factors in multiethnic premenopausal and perimenopausal women enrolled in the Study of Women Across the Nation (SWAN). Circulation 111, 1242–1249 (2005)CrossRefPubMed K. Sutton-Tyrrell, R.P. Wildman, K.A. Matthews, C. Chae, B.L. Lasley, S. Brockwell, R.C. Pasternak, D. Lloyd-Jones, M.F. Sowers, J.I. Torréns; SWAN Investigators: Sex-hormone-binding globulin and the free androgen index are related to cardiovascular risk factors in multiethnic premenopausal and perimenopausal women enrolled in the Study of Women Across the Nation (SWAN). Circulation 111, 1242–1249 (2005)CrossRefPubMed
15.
go back to reference A. Peter, K. Kantartzis, J. Machann, F. Schick, H. Staiger, F. Machicao, E. Schleicher, A. Fritsche, H.U. Häring, N. Stefan, Relationships of circulating sex hormone-binding globulin with metabolic traits in humans. Diabetes 59, 3167–3173 (2010)CrossRefPubMedPubMedCentral A. Peter, K. Kantartzis, J. Machann, F. Schick, H. Staiger, F. Machicao, E. Schleicher, A. Fritsche, H.U. Häring, N. Stefan, Relationships of circulating sex hormone-binding globulin with metabolic traits in humans. Diabetes 59, 3167–3173 (2010)CrossRefPubMedPubMedCentral
16.
go back to reference D.M. Selva, G.L. Hammond, Thyroid hormones act indirectly to increase sex hormone-binding globulin production by liver via hepatocyte nuclear factor-4alpha. J. Mol. Endocrinol. 43, 19–27 (2009)CrossRefPubMed D.M. Selva, G.L. Hammond, Thyroid hormones act indirectly to increase sex hormone-binding globulin production by liver via hepatocyte nuclear factor-4alpha. J. Mol. Endocrinol. 43, 19–27 (2009)CrossRefPubMed
17.
go back to reference R. Simó, A. Barbosa-Desongles, A. Lecube, C. Hernandez, D.M. Selva, Potential role of tumor necrosis factor-α in downregulating sex hormone-binding globulin. Diabetes 61, 372–382 (2012)CrossRefPubMedPubMedCentral R. Simó, A. Barbosa-Desongles, A. Lecube, C. Hernandez, D.M. Selva, Potential role of tumor necrosis factor-α in downregulating sex hormone-binding globulin. Diabetes 61, 372–382 (2012)CrossRefPubMedPubMedCentral
18.
go back to reference R. Simó, C. Saez-Lopez, A. Lecube, C. Hernandez, J.M. Fort, D.M. Selva, Adiponectin upregulates SHBG production: Molecular mechanisms and potential implications. Endocrinology 155, 2820–2830 (2014)CrossRefPubMed R. Simó, C. Saez-Lopez, A. Lecube, C. Hernandez, J.M. Fort, D.M. Selva, Adiponectin upregulates SHBG production: Molecular mechanisms and potential implications. Endocrinology 155, 2820–2830 (2014)CrossRefPubMed
19.
go back to reference D.M. Selva, K.N. Hogeveen, S.M. Innis, G.L. Hammond, Monosaccharide-induced lipogenesis regulates the human hepatic sex hormone-binding globulin gene. J. Clin. Invest. 117, 3979–3987 (2007)PubMedPubMedCentral D.M. Selva, K.N. Hogeveen, S.M. Innis, G.L. Hammond, Monosaccharide-induced lipogenesis regulates the human hepatic sex hormone-binding globulin gene. J. Clin. Invest. 117, 3979–3987 (2007)PubMedPubMedCentral
20.
go back to reference C. Sáez-López, F. Soriguer, C. Hernandez, G. Rojo-Martinez, E. Rubio-Martín, R. Simó, D.M. Selva, Oleic acid increases hepatic sex hormone binding globulin production in men. Mol. Nutr. Food Res. 58, 760–767 (2014)CrossRefPubMed C. Sáez-López, F. Soriguer, C. Hernandez, G. Rojo-Martinez, E. Rubio-Martín, R. Simó, D.M. Selva, Oleic acid increases hepatic sex hormone binding globulin production in men. Mol. Nutr. Food Res. 58, 760–767 (2014)CrossRefPubMed
21.
go back to reference N. Wang, X. Wang, B. Han, Q. Li, Y. Chen, C. Zhu, Y. Chen, F. Xia, Z. Cang, C. Zhu, M. Lu, Y. Meng, C. Chen, D. Lin, B. Wang, M.D. Jensen, Y. Lu, Is exposure to famine in childhood and economic development in adulthood associated with diabetes? J. Clin. Endocrinol. Metab. 100, 4514–4523 (2015)CrossRefPubMedPubMedCentral N. Wang, X. Wang, B. Han, Q. Li, Y. Chen, C. Zhu, Y. Chen, F. Xia, Z. Cang, C. Zhu, M. Lu, Y. Meng, C. Chen, D. Lin, B. Wang, M.D. Jensen, Y. Lu, Is exposure to famine in childhood and economic development in adulthood associated with diabetes? J. Clin. Endocrinol. Metab. 100, 4514–4523 (2015)CrossRefPubMedPubMedCentral
22.
go back to reference N. Wang, X. Wang, Q. Li, B. Han, Y. Chen, C. Zhu, Y. Chen, D. Lin, B. Wang, M.D. Jensen, Y. Lu, The famine exposure in early life and metabolic syndrome in adulthood. Clin. Nutr. (2015). doi:10.1016/j.clnu.2015.11.010 N. Wang, X. Wang, Q. Li, B. Han, Y. Chen, C. Zhu, Y. Chen, D. Lin, B. Wang, M.D. Jensen, Y. Lu, The famine exposure in early life and metabolic syndrome in adulthood. Clin. Nutr. (2015). doi:10.​1016/​j.​clnu.​2015.​11.​010
23.
go back to reference N. Wang, J. Cheng, B. Han, Q. Li, Y. Chen, F. Xia, B. Jiang, M.D. Jensen, Y. Lu, Exposure to severe famine in the prenatal or postnatal period and the development of diabetes in adulthood: an observational study. Diabetologia 60, 262–269 (2017)CrossRefPubMed N. Wang, J. Cheng, B. Han, Q. Li, Y. Chen, F. Xia, B. Jiang, M.D. Jensen, Y. Lu, Exposure to severe famine in the prenatal or postnatal period and the development of diabetes in adulthood: an observational study. Diabetologia 60, 262–269 (2017)CrossRefPubMed
24.
go back to reference S.D. Harlow, M. Gass, J.E. Hall, R. Lobo, P. Maki, R.W. Rebar, S. Sherman, P.M. Sluss, T.J. de Villiers; STRAW + 10 collaborative group., Executive summary of the stages of reproductive aging workshop + 10: Addressing the unfinished agenda of staging reproductive aging. J. Clin. Endocrinol. Metab. 97, 1159–1168 (2012)CrossRefPubMedPubMedCentral S.D. Harlow, M. Gass, J.E. Hall, R. Lobo, P. Maki, R.W. Rebar, S. Sherman, P.M. Sluss, T.J. de Villiers; STRAW + 10 collaborative group., Executive summary of the stages of reproductive aging workshop + 10: Addressing the unfinished agenda of staging reproductive aging. J. Clin. Endocrinol. Metab. 97, 1159–1168 (2012)CrossRefPubMedPubMedCentral
25.
go back to reference A. Bjørnerem, B. Straume, M. Midtby, V. Fønnebø, J. Sundsfjord, J. Svartberg, G. Acharya, P. Oian, G.K. Berntsen, Endogenous sex hormones in relation to age, sex, lifestyle factors, and chronic diseases in a general population: The Tromsø study. J. Clin. Endocrinol. Metab. 89, 6039–6047 (2004)CrossRefPubMed A. Bjørnerem, B. Straume, M. Midtby, V. Fønnebø, J. Sundsfjord, J. Svartberg, G. Acharya, P. Oian, G.K. Berntsen, Endogenous sex hormones in relation to age, sex, lifestyle factors, and chronic diseases in a general population: The Tromsø study. J. Clin. Endocrinol. Metab. 89, 6039–6047 (2004)CrossRefPubMed
26.
go back to reference Y. Xu, L. Wang, J. He, Y. Bi, M. Li, T. Wang, L. Wang, Y. Jiang, M. Dai, J. Lu, M. Xu, Y. Li, N. Hu, J. Li, S. Mi, C.S. Chen, G. Li, Y. Mu, J. Zhao, L. Kong, J. Chen, S. Lai, W. Wang, W. Zhao, G. Ning; 2010 China Noncommunicable Disease Surveillance Group., Prevalence and control of diabetes in Chinese adults. JAMA 310, 948–959 (2013)CrossRefPubMed Y. Xu, L. Wang, J. He, Y. Bi, M. Li, T. Wang, L. Wang, Y. Jiang, M. Dai, J. Lu, M. Xu, Y. Li, N. Hu, J. Li, S. Mi, C.S. Chen, G. Li, Y. Mu, J. Zhao, L. Kong, J. Chen, S. Lai, W. Wang, W. Zhao, G. Ning; 2010 China Noncommunicable Disease Surveillance Group., Prevalence and control of diabetes in Chinese adults. JAMA 310, 948–959 (2013)CrossRefPubMed
27.
go back to reference A. Mitra, B. Chakraborty, D. Mukhopadhay, M. Pal, S. Mukherjee, S. Banerjee, K. Chaudhuri, Effect of smoking on semen quality, FSH, testosterone level, and CAG repeat length in androgen receptor gene of infertile men in an Indian city. Syst. Biol. Reprod. Med. 58, 255–262 (2012)CrossRefPubMed A. Mitra, B. Chakraborty, D. Mukhopadhay, M. Pal, S. Mukherjee, S. Banerjee, K. Chaudhuri, Effect of smoking on semen quality, FSH, testosterone level, and CAG repeat length in androgen receptor gene of infertile men in an Indian city. Syst. Biol. Reprod. Med. 58, 255–262 (2012)CrossRefPubMed
28.
go back to reference N. Wang, H. Zhai, B. Han, Q. Li, Y. Chen, Y. Chen, F. Xia, D. Lin, Y. Lu, Visceral fat dysfunction is positively associated with hypogonadism in Chinese men. Sci. Rep 6, 19844 (2016)CrossRefPubMedPubMedCentral N. Wang, H. Zhai, B. Han, Q. Li, Y. Chen, Y. Chen, F. Xia, D. Lin, Y. Lu, Visceral fat dysfunction is positively associated with hypogonadism in Chinese men. Sci. Rep 6, 19844 (2016)CrossRefPubMedPubMedCentral
29.
go back to reference A.A. MacDonald, G.P. Herbison, M. Showell, C.M. Farquhar, The impact of body mass index on semen parameters and reproductive hormones in human males: A systematic review with meta-analysis. Hum. Reprod. Update 16, 293–311 (2010)CrossRefPubMed A.A. MacDonald, G.P. Herbison, M. Showell, C.M. Farquhar, The impact of body mass index on semen parameters and reproductive hormones in human males: A systematic review with meta-analysis. Hum. Reprod. Update 16, 293–311 (2010)CrossRefPubMed
30.
go back to reference L. Niskanen, D.E. Laaksonen, K. Punnonen, P. Mustajoki, J. Kaukua, A. Rissanen, Changes in sex hormone-binding globulin and testosterone during weight loss and weight maintenance in abdominally obese men with the metabolic syndrome. Diabetes Obes. Metab. 6, 208–215 (2004)CrossRefPubMed L. Niskanen, D.E. Laaksonen, K. Punnonen, P. Mustajoki, J. Kaukua, A. Rissanen, Changes in sex hormone-binding globulin and testosterone during weight loss and weight maintenance in abdominally obese men with the metabolic syndrome. Diabetes Obes. Metab. 6, 208–215 (2004)CrossRefPubMed
31.
go back to reference J. Nielsen, R.B. Jensen, A. Juul, Increased sex hormone-binding globulin levels in children and adolescents with thyrotoxicosis. Horm. Res. Paediatr. 79, 157–161 (2013)CrossRefPubMed J. Nielsen, R.B. Jensen, A. Juul, Increased sex hormone-binding globulin levels in children and adolescents with thyrotoxicosis. Horm. Res. Paediatr. 79, 157–161 (2013)CrossRefPubMed
32.
go back to reference R. Hampl, R. Kancheva, M. Hill, M. Bicíková, K. Vondra, Interpretation of sex hormone-binding globulin levels in thyroid disorders. Thyroid 13, 755–760 (2003)CrossRefPubMed R. Hampl, R. Kancheva, M. Hill, M. Bicíková, K. Vondra, Interpretation of sex hormone-binding globulin levels in thyroid disorders. Thyroid 13, 755–760 (2003)CrossRefPubMed
33.
go back to reference Q. Wang, A.J. Kangas, P. Soininen, M. Tiainen, T. Tynkkynen, K. Puukka, A. Ruokonen, J. Viikari, M. Kähönen, T. Lehtimäki, V. Salomaa, M. Perola, G. Davey Smith, O.T. Raitakari, M.R. Järvelin, P. Würtz, J. Kettunen, M. Ala-Korpela, Sex hormone-binding globulin associations with circulating lipids and metabolites and the risk for type 2 diabetes: Observational and causal effect estimates. Int. J. Epidemiol. 44, 623–637 (2015)CrossRefPubMed Q. Wang, A.J. Kangas, P. Soininen, M. Tiainen, T. Tynkkynen, K. Puukka, A. Ruokonen, J. Viikari, M. Kähönen, T. Lehtimäki, V. Salomaa, M. Perola, G. Davey Smith, O.T. Raitakari, M.R. Järvelin, P. Würtz, J. Kettunen, M. Ala-Korpela, Sex hormone-binding globulin associations with circulating lipids and metabolites and the risk for type 2 diabetes: Observational and causal effect estimates. Int. J. Epidemiol. 44, 623–637 (2015)CrossRefPubMed
34.
go back to reference H. Zhang, Q. Li, H. Lin, Q. Yang, H. Wang, C. Zhu, Role of PPARgamma and its gonadotrophic regulation in rat ovarian granulosa cells in vitro. Neuro. Endocrinol. Lett. 28, 289–294 (2007)PubMed H. Zhang, Q. Li, H. Lin, Q. Yang, H. Wang, C. Zhu, Role of PPARgamma and its gonadotrophic regulation in rat ovarian granulosa cells in vitro. Neuro. Endocrinol. Lett. 28, 289–294 (2007)PubMed
35.
go back to reference R. Pasquali, V. Vicennati, D. Bertazzo, F. Casimirri, G. Pascal, O. Tortelli, A.M. Labate, Determinants of sex hormone-binding globulin blood concentrations in premenopausal and postmenopausal women with different estrogen status. Virgilio-Menopause-Health Group. Metabolism 46, 5–9 (1997)PubMed R. Pasquali, V. Vicennati, D. Bertazzo, F. Casimirri, G. Pascal, O. Tortelli, A.M. Labate, Determinants of sex hormone-binding globulin blood concentrations in premenopausal and postmenopausal women with different estrogen status. Virgilio-Menopause-Health Group. Metabolism 46, 5–9 (1997)PubMed
36.
go back to reference G. Halmenschlager, E.L. Rhoden, C.E. Riedner, The influence of age on bioavailable and free testosterone is independent of body mass index and glucose levels. World J Urol. 29, 541–546 (2011)CrossRefPubMed G. Halmenschlager, E.L. Rhoden, C.E. Riedner, The influence of age on bioavailable and free testosterone is independent of body mass index and glucose levels. World J Urol. 29, 541–546 (2011)CrossRefPubMed
37.
go back to reference H.A. Feldman, C. Longcope, C.A. Derby, C.B. Johannes, A.B. Araujo, A.D. Coviello, W.J. Bremner, J.B. McKinlay, Age trends in the level of serum testosterone and other hormones in middle-aged men: Longitudinal results from the Massachusetts male aging study. J. Clin. Endocrinol. Metab. 87, 589–598 (2002)CrossRefPubMed H.A. Feldman, C. Longcope, C.A. Derby, C.B. Johannes, A.B. Araujo, A.D. Coviello, W.J. Bremner, J.B. McKinlay, Age trends in the level of serum testosterone and other hormones in middle-aged men: Longitudinal results from the Massachusetts male aging study. J. Clin. Endocrinol. Metab. 87, 589–598 (2002)CrossRefPubMed
38.
go back to reference S.H. Golden, A.S. Dobs, D. Vaidya, M. Szklo, S. Gapstur, P. Kopp, K. Liu, P. Ouyang, Endogenous sex hormones and glucose tolerance status in postmenopausal women. J. Clin. Endocrinol. Metab. 92, 1289–1295 (2007)CrossRefPubMed S.H. Golden, A.S. Dobs, D. Vaidya, M. Szklo, S. Gapstur, P. Kopp, K. Liu, P. Ouyang, Endogenous sex hormones and glucose tolerance status in postmenopausal women. J. Clin. Endocrinol. Metab. 92, 1289–1295 (2007)CrossRefPubMed
39.
go back to reference R.R. Kalyani, M. Franco, A.S. Dobs, P. Ouyang, D. Vaidya, A. Bertoni, S.M. Gapstur, S.H. Golden, The association of endogenous sex hormones, adiposity, and insulin resistance with incident diabetes in postmenopausal women. J. Clin. Endocrinol. Metab. 94, 4127–4135 (2009)CrossRefPubMedPubMedCentral R.R. Kalyani, M. Franco, A.S. Dobs, P. Ouyang, D. Vaidya, A. Bertoni, S.M. Gapstur, S.H. Golden, The association of endogenous sex hormones, adiposity, and insulin resistance with incident diabetes in postmenopausal women. J. Clin. Endocrinol. Metab. 94, 4127–4135 (2009)CrossRefPubMedPubMedCentral
40.
go back to reference L. Li, J. Wu, D. Pu, Y. Zhao, C. Wan, L. Sun, C.E. Shen, W. Sun, Z. Yuan, Q. Shen, X. He, J. Jiang, N. Luo, Y. He, Q. Qian, P. Cai, M. Zhang, Factors associated with the age of natural menopause and menopausal symptoms in Chinese women. Maturitas 73, 354–360 (2012)CrossRefPubMed L. Li, J. Wu, D. Pu, Y. Zhao, C. Wan, L. Sun, C.E. Shen, W. Sun, Z. Yuan, Q. Shen, X. He, J. Jiang, N. Luo, Y. He, Q. Qian, P. Cai, M. Zhang, Factors associated with the age of natural menopause and menopausal symptoms in Chinese women. Maturitas 73, 354–360 (2012)CrossRefPubMed
Metadata
Title
Follicle stimulating hormone, its novel association with sex hormone binding globulin in men and postmenopausal women
Authors
Ningjian Wang
Kun Zhang
Bing Han
Qin Li
Yi Chen
Chunfang Zhu
Yingchao Chen
Fangzhen Xia
Hualing Zhai
Boren Jiang
Zhoujun Shen
Yingli Lu
Publication date
01-06-2017
Publisher
Springer US
Published in
Endocrine / Issue 3/2017
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-017-1272-y

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