Skip to main content
Top
Published in: Endocrine 1/2014

01-05-2014 | Review

Implications of adiponectin in linking metabolism to testicular function

Author: Luc J. Martin

Published in: Endocrine | Issue 1/2014

Login to get access

Abstract

Obesity is a major health problem, contributing to the development of various diseases with aging. In humans, obesity has been associated with reduced testosterone production and subfertility. Adipose tissue is an important source of hormones having influences on both metabolism and reproduction. Among them, the production and secretion of adiponectin is inversely correlated to the severity of obesity. The purpose of this review of literature is to present the current state of knowledge on adiponectin research to determine whether this hormone affects reproduction in men. Surprisingly, evidences show negative influences of adiponectin on GnRH secretion from the hypothalamus, LH and FSH secretion from the pituitary and testosterone at the testicular level. Thus far, the involvement of adiponectin in the influence of metabolism on reproduction in men is limited. However, adiponectin and its receptors are expressed by different cell types of the male gonad, including Leydig cells, spermatozoa, and epididymis. In addition, actions of adiponectin at the testicular level have been shown to promote spermatogenesis and sperm maturation. Therefore, autocrine/paracrine actions of adiponectin in the testis may contribute to support male reproductive function.
Literature
1.
go back to reference F.X. Pi-Sunyer, The obesity epidemic: pathophysiology and consequences of obesity. Obes. Res. 10(Suppl 2), 97S–104S (2002)PubMed F.X. Pi-Sunyer, The obesity epidemic: pathophysiology and consequences of obesity. Obes. Res. 10(Suppl 2), 97S–104S (2002)PubMed
2.
go back to reference K.M. Flegal, M.D. Carroll, B.K. Kit, C.L. Ogden, Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. J. Am. Med. Assoc. 307, 491–497 (2012) K.M. Flegal, M.D. Carroll, B.K. Kit, C.L. Ogden, Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. J. Am. Med. Assoc. 307, 491–497 (2012)
3.
go back to reference C.A. Derby, S. Zilber, D. Brambilla, K.H. Morales, J.B. McKinlay, Body mass index, waist circumference and waist to hip ratio and change in sex steroid hormones: the Massachusetts Male Ageing Study. Clin. Endocrinol. (Oxf.) 65, 125–131 (2006) C.A. Derby, S. Zilber, D. Brambilla, K.H. Morales, J.B. McKinlay, Body mass index, waist circumference and waist to hip ratio and change in sex steroid hormones: the Massachusetts Male Ageing Study. Clin. Endocrinol. (Oxf.) 65, 125–131 (2006)
4.
go back to reference R.S. Tan, S.J. Pu, Impact of obesity on hypogonadism in the andropause. Int. J. Androl. 25, 195–201 (2002)PubMed R.S. Tan, S.J. Pu, Impact of obesity on hypogonadism in the andropause. Int. J. Androl. 25, 195–201 (2002)PubMed
5.
go back to reference P.M. Mah, G.A. Wittert, Obesity and testicular function. Mol. Cell. Endocrinol. 316, 180–186 (2010)PubMed P.M. Mah, G.A. Wittert, Obesity and testicular function. Mol. Cell. Endocrinol. 316, 180–186 (2010)PubMed
6.
go back to reference D. Landry, F. Cloutier, L.J. Martin, Implications of leptin in neuroendocrine regulation of male reproduction. Reprod. Biol. 13, 1–14 (2013)PubMed D. Landry, F. Cloutier, L.J. Martin, Implications of leptin in neuroendocrine regulation of male reproduction. Reprod. Biol. 13, 1–14 (2013)PubMed
7.
go back to reference M. Pardo, A. Roca-Rivada, L.M. Seoane, F.F. Casanueva, Obesidomics: contribution of adipose tissue secretome analysis to obesity research. Endocrine 41, 374–383 (2012)PubMed M. Pardo, A. Roca-Rivada, L.M. Seoane, F.F. Casanueva, Obesidomics: contribution of adipose tissue secretome analysis to obesity research. Endocrine 41, 374–383 (2012)PubMed
8.
go back to reference K. Marinou, D. Tousoulis, A.S. Antonopoulos, E. Stefanadi, C. Stefanadis, Obesity and cardiovascular disease: from pathophysiology to risk stratification. Int. J. Cardiol. 138, 3–8 (2010)PubMed K. Marinou, D. Tousoulis, A.S. Antonopoulos, E. Stefanadi, C. Stefanadis, Obesity and cardiovascular disease: from pathophysiology to risk stratification. Int. J. Cardiol. 138, 3–8 (2010)PubMed
9.
go back to reference K. Rabe, M. Lehrke, K.G. Parhofer, U.C. Broedl, Adipokines and insulin resistance. Mol. Med. Camb. Mass. 14, 741–751 (2008)PubMedCentralPubMed K. Rabe, M. Lehrke, K.G. Parhofer, U.C. Broedl, Adipokines and insulin resistance. Mol. Med. Camb. Mass. 14, 741–751 (2008)PubMedCentralPubMed
10.
go back to reference P.G. Cohen, Aromatase, adiposity, aging and disease. The hypogonadal–metabolic–atherogenic-disease and aging connection. Med. Hypotheses 56, 702–708 (2001)PubMed P.G. Cohen, Aromatase, adiposity, aging and disease. The hypogonadal–metabolic–atherogenic-disease and aging connection. Med. Hypotheses 56, 702–708 (2001)PubMed
11.
go back to reference A. Vermeulen, Decreased androgen levels and obesity in men. Ann. Med. 28, 13–15 (1996)PubMed A. Vermeulen, Decreased androgen levels and obesity in men. Ann. Med. 28, 13–15 (1996)PubMed
12.
go back to reference A. Vermeulen, J.M. Kaufman, Ageing of the hypothalamo–pituitary–testicular axis in men. Horm. Res. 43, 25–28 (1995)PubMed A. Vermeulen, J.M. Kaufman, Ageing of the hypothalamo–pituitary–testicular axis in men. Horm. Res. 43, 25–28 (1995)PubMed
13.
go back to reference G. Schneider, M.A. Kirschner, R. Berkowitz, N.H. Ertel, Increased estrogen production in obese men. J. Clin. Endocrinol. Metab. 48, 633–638 (1979)PubMed G. Schneider, M.A. Kirschner, R. Berkowitz, N.H. Ertel, Increased estrogen production in obese men. J. Clin. Endocrinol. Metab. 48, 633–638 (1979)PubMed
14.
go back to reference A.M. Corbould, S.J. Judd, R.J. Rodgers, Expression of types 1, 2, and 3 17 beta-hydroxysteroid dehydrogenase in subcutaneous abdominal and intra-abdominal adipose tissue of women. J. Clin. Endocrinol. Metab. 83, 187–194 (1998)PubMed A.M. Corbould, S.J. Judd, R.J. Rodgers, Expression of types 1, 2, and 3 17 beta-hydroxysteroid dehydrogenase in subcutaneous abdominal and intra-abdominal adipose tissue of women. J. Clin. Endocrinol. Metab. 83, 187–194 (1998)PubMed
15.
go back to reference P. Mårin, S. Arver, Androgens and abdominal obesity. Baillières Clin. Endocrinol. Metab. 12, 441–451 (1998)PubMed P. Mårin, S. Arver, Androgens and abdominal obesity. Baillières Clin. Endocrinol. Metab. 12, 441–451 (1998)PubMed
16.
go back to reference P. Mårin, Testosterone and regional fat distribution. Obes. Res. 3(Suppl 4), 609S–612S (1995)PubMed P. Mårin, Testosterone and regional fat distribution. Obes. Res. 3(Suppl 4), 609S–612S (1995)PubMed
17.
go back to reference R. Lazarus, D. Sparrow, S. Weiss, Temporal relations between obesity and insulin: longitudinal data from the normative aging study. Am. J. Epidemiol. 147, 173–179 (1998)PubMed R. Lazarus, D. Sparrow, S. Weiss, Temporal relations between obesity and insulin: longitudinal data from the normative aging study. Am. J. Epidemiol. 147, 173–179 (1998)PubMed
18.
go back to reference D. Goodman-Gruen, E. Barrett-Connor, Sex differences in the association of endogenous sex hormone levels and glucose tolerance status in older men and women. Diabetes Care 23, 912–918 (2000)PubMed D. Goodman-Gruen, E. Barrett-Connor, Sex differences in the association of endogenous sex hormone levels and glucose tolerance status in older men and women. Diabetes Care 23, 912–918 (2000)PubMed
19.
go back to reference E.C. Tsai, E.J. Boyko, D.L. Leonetti, W.Y. Fujimoto, Low serum testosterone level as a predictor of increased visceral fat in Japanese-American men. Int. J. Obes. Relat. Metab. Disord. 24, 485–491 (2000)PubMed E.C. Tsai, E.J. Boyko, D.L. Leonetti, W.Y. Fujimoto, Low serum testosterone level as a predictor of increased visceral fat in Japanese-American men. Int. J. Obes. Relat. Metab. Disord. 24, 485–491 (2000)PubMed
20.
go back to reference V.A. Giagulli, J.M. Kaufman, A. Vermeulen, Pathogenesis of the decreased androgen levels in obese men. J. Clin. Endocrinol. Metab. 79, 997–1000 (1994)PubMed V.A. Giagulli, J.M. Kaufman, A. Vermeulen, Pathogenesis of the decreased androgen levels in obese men. J. Clin. Endocrinol. Metab. 79, 997–1000 (1994)PubMed
21.
go back to reference P.G. Cohen, The hypogonadal-obesity cycle: role of aromatase in modulating the testosterone–estradiol shunt: a major factor in the genesis of morbid obesity. Med. Hypotheses 52, 49–51 (1999)PubMed P.G. Cohen, The hypogonadal-obesity cycle: role of aromatase in modulating the testosterone–estradiol shunt: a major factor in the genesis of morbid obesity. Med. Hypotheses 52, 49–51 (1999)PubMed
22.
go back to reference H.K. Kley, H.G. Solbach, J.C. McKinnan, H.L. Krüskemper, Testosterone decrease and oestrogen increase in male patients with obesity. Acta Endocrinol. (Cph.) 91, 553–563 (1979) H.K. Kley, H.G. Solbach, J.C. McKinnan, H.L. Krüskemper, Testosterone decrease and oestrogen increase in male patients with obesity. Acta Endocrinol. (Cph.) 91, 553–563 (1979)
23.
go back to reference B. Zumoff, G.W. Strain, L.K. Miller, W. Rosner, R. Senie, D.S. Seres, R.S. Rosenfeld, Plasma free and non-sex-hormone-binding-globulin-bound testosterone are decreased in obese men in proportion to their degree of obesity. J. Clin. Endocrinol. Metab. 71, 929–931 (1990)PubMed B. Zumoff, G.W. Strain, L.K. Miller, W. Rosner, R. Senie, D.S. Seres, R.S. Rosenfeld, Plasma free and non-sex-hormone-binding-globulin-bound testosterone are decreased in obese men in proportion to their degree of obesity. J. Clin. Endocrinol. Metab. 71, 929–931 (1990)PubMed
24.
go back to reference T. Kadowaki, T. Yamauchi, Adiponectin and adiponectin receptors. Endocr. Rev. 26, 439–451 (2005)PubMed T. Kadowaki, T. Yamauchi, Adiponectin and adiponectin receptors. Endocr. Rev. 26, 439–451 (2005)PubMed
25.
go back to reference J. Hoffstedt, E. Arvidsson, E. Sjölin, K. Wåhlén, P. Arner, Adipose tissue adiponectin production and adiponectin serum concentration in human obesity and insulin resistance. J. Clin. Endocrinol. Metab. 89, 1391–1396 (2004)PubMed J. Hoffstedt, E. Arvidsson, E. Sjölin, K. Wåhlén, P. Arner, Adipose tissue adiponectin production and adiponectin serum concentration in human obesity and insulin resistance. J. Clin. Endocrinol. Metab. 89, 1391–1396 (2004)PubMed
26.
go back to reference K. Hotta, T. Funahashi, Y. Arita, M. Takahashi, M. Matsuda, Y. Okamoto, H. Iwahashi, H. Kuriyama, N. Ouchi, K. Maeda, M. Nishida, S. Kihara, N. Sakai, T. Nakajima, K. Hasegawa, M. Muraguchi, Y. Ohmoto, T. Nakamura, S. Yamashita, T. Hanafusa, Y. Matsuzawa, Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler. Thromb. Vasc. Biol. 20, 1595–1599 (2000)PubMed K. Hotta, T. Funahashi, Y. Arita, M. Takahashi, M. Matsuda, Y. Okamoto, H. Iwahashi, H. Kuriyama, N. Ouchi, K. Maeda, M. Nishida, S. Kihara, N. Sakai, T. Nakajima, K. Hasegawa, M. Muraguchi, Y. Ohmoto, T. Nakamura, S. Yamashita, T. Hanafusa, Y. Matsuzawa, Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler. Thromb. Vasc. Biol. 20, 1595–1599 (2000)PubMed
27.
go back to reference I.J. Neeland, C.R. Ayers, A.K. Rohatgi, A.T. Turer, J.D. Berry, S.R. Das, G.L. Vega, A. Khera, D.K. McGuire, S.M. Grundy, J.A. de Lemos, Associations of visceral and abdominal subcutaneous adipose tissue with markers of cardiac and metabolic risk in obese adults. Obes. Silver Spring Md. 21, E439–E447 (2013) I.J. Neeland, C.R. Ayers, A.K. Rohatgi, A.T. Turer, J.D. Berry, S.R. Das, G.L. Vega, A. Khera, D.K. McGuire, S.M. Grundy, J.A. de Lemos, Associations of visceral and abdominal subcutaneous adipose tissue with markers of cardiac and metabolic risk in obese adults. Obes. Silver Spring Md. 21, E439–E447 (2013)
28.
go back to reference Y. Arita, S. Kihara, N. Ouchi, M. Takahashi, K. Maeda, J. Miyagawa, K. Hotta, I. Shimomura, T. Nakamura, K. Miyaoka, H. Kuriyama, M. Nishida, S. Yamashita, K. Okubo, K. Matsubara, M. Muraguchi, Y. Ohmoto, T. Funahashi, Y. Matsuzawa, Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem. Biophys. Res. Commun. 257, 79–83 (1999)PubMed Y. Arita, S. Kihara, N. Ouchi, M. Takahashi, K. Maeda, J. Miyagawa, K. Hotta, I. Shimomura, T. Nakamura, K. Miyaoka, H. Kuriyama, M. Nishida, S. Yamashita, K. Okubo, K. Matsubara, M. Muraguchi, Y. Ohmoto, T. Funahashi, Y. Matsuzawa, Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem. Biophys. Res. Commun. 257, 79–83 (1999)PubMed
29.
go back to reference M. Cnop, P.J. Havel, K.M. Utzschneider, D.B. Carr, M.K. Sinha, E.J. Boyko, B.M. Retzlaff, R.H. Knopp, J.D. Brunzell, S.E. Kahn, Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex. Diabetologia 46, 459–469 (2003)PubMed M. Cnop, P.J. Havel, K.M. Utzschneider, D.B. Carr, M.K. Sinha, E.J. Boyko, B.M. Retzlaff, R.H. Knopp, J.D. Brunzell, S.E. Kahn, Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex. Diabetologia 46, 459–469 (2003)PubMed
30.
go back to reference F.B. Diamond Jr, D. Cuthbertson, S. Hanna, D. Eichler, Correlates of adiponectin and the leptin/adiponectin ratio in obese and non-obese children. J. Pediatr. Endocrinol. Metab. 17, 1069–1075 (2004)PubMed F.B. Diamond Jr, D. Cuthbertson, S. Hanna, D. Eichler, Correlates of adiponectin and the leptin/adiponectin ratio in obese and non-obese children. J. Pediatr. Endocrinol. Metab. 17, 1069–1075 (2004)PubMed
31.
go back to reference M. Bulló, J. Salas-Salvadó, P. García-Lorda, Adiponectin expression and adipose tissue lipolytic activity in lean and obese women. Obes. Surg. 15, 382–386 (2005)PubMed M. Bulló, J. Salas-Salvadó, P. García-Lorda, Adiponectin expression and adipose tissue lipolytic activity in lean and obese women. Obes. Surg. 15, 382–386 (2005)PubMed
32.
go back to reference S.K. Jacobi, K.M. Ajuwon, T.E. Weber, J.L. Kuske, C.J. Dyer, M.E. Spurlock, Cloning and expression of porcine adiponectin, and its relationship to adiposity, lipogenesis and the acute phase response. J. Endocrinol. 182, 133–144 (2004)PubMed S.K. Jacobi, K.M. Ajuwon, T.E. Weber, J.L. Kuske, C.J. Dyer, M.E. Spurlock, Cloning and expression of porcine adiponectin, and its relationship to adiposity, lipogenesis and the acute phase response. J. Endocrinol. 182, 133–144 (2004)PubMed
33.
go back to reference T. Yamauchi, J. Kamon, H. Waki, Y. Terauchi, N. Kubota, K. Hara, Y. Mori, T. Ide, K. Murakami, N. Tsuboyama-Kasaoka, O. Ezaki, Y. Akanuma, O. Gavrilova, C. Vinson, M.L. Reitman, H. Kagechika, K. Shudo, M. Yoda, Y. Nakano, K. Tobe, R. Nagai, S. Kimura, M. Tomita, P. Froguel, T. Kadowaki, The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 7, 941–946 (2001)PubMed T. Yamauchi, J. Kamon, H. Waki, Y. Terauchi, N. Kubota, K. Hara, Y. Mori, T. Ide, K. Murakami, N. Tsuboyama-Kasaoka, O. Ezaki, Y. Akanuma, O. Gavrilova, C. Vinson, M.L. Reitman, H. Kagechika, K. Shudo, M. Yoda, Y. Nakano, K. Tobe, R. Nagai, S. Kimura, M. Tomita, P. Froguel, T. Kadowaki, The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 7, 941–946 (2001)PubMed
34.
go back to reference E. Hu, P. Liang, B.M. Spiegelman, AdipoQ is a novel adipose-specific gene dysregulated in obesity. J. Biol. Chem. 271, 10697–10703 (1996)PubMed E. Hu, P. Liang, B.M. Spiegelman, AdipoQ is a novel adipose-specific gene dysregulated in obesity. J. Biol. Chem. 271, 10697–10703 (1996)PubMed
35.
go back to reference Kadowaki, T., Yamauchi, T., Kubota, N., Hara, K., Ueki, K.: Adiponectin and adiponectin receptors in obesity-linked insulin resistance. Novartis Found. Symp. 286, 164–176 (2007); discussion 176–182, 200–203 Kadowaki, T., Yamauchi, T., Kubota, N., Hara, K., Ueki, K.: Adiponectin and adiponectin receptors in obesity-linked insulin resistance. Novartis Found. Symp. 286, 164–176 (2007); discussion 176–182, 200–203
36.
go back to reference C. Weyer, T. Funahashi, S. Tanaka, K. Hotta, Y. Matsuzawa, R.E. Pratley, P.A. Tataranni, Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J. Clin. Endocrinol. Metab. 86, 1930–1935 (2001)PubMed C. Weyer, T. Funahashi, S. Tanaka, K. Hotta, Y. Matsuzawa, R.E. Pratley, P.A. Tataranni, Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J. Clin. Endocrinol. Metab. 86, 1930–1935 (2001)PubMed
37.
go back to reference B. Antuna-Puente, B. Feve, S. Fellahi, J.-P. Bastard, Adipokines: the missing link between insulin resistance and obesity. Diabetes Metab. 34, 2–11 (2008)PubMed B. Antuna-Puente, B. Feve, S. Fellahi, J.-P. Bastard, Adipokines: the missing link between insulin resistance and obesity. Diabetes Metab. 34, 2–11 (2008)PubMed
38.
go back to reference L. Sieminska, B. Marek, B. Kos-Kudla, D. Niedziolka, D. Kajdaniuk, M. Nowak, J. Glogowska-Szelag, Serum adiponectin in women with polycystic ovarian syndrome and its relation to clinical, metabolic and endocrine parameters. J. Endocrinol. Invest. 27, 528–534 (2004)PubMed L. Sieminska, B. Marek, B. Kos-Kudla, D. Niedziolka, D. Kajdaniuk, M. Nowak, J. Glogowska-Szelag, Serum adiponectin in women with polycystic ovarian syndrome and its relation to clinical, metabolic and endocrine parameters. J. Endocrinol. Invest. 27, 528–534 (2004)PubMed
39.
go back to reference Y. Okamoto, Adiponectin provides cardiovascular protection in metabolic syndrome. Cardiol. Res. Pract. 2011, 313179 (2011)PubMedCentralPubMed Y. Okamoto, Adiponectin provides cardiovascular protection in metabolic syndrome. Cardiol. Res. Pract. 2011, 313179 (2011)PubMedCentralPubMed
40.
go back to reference H.-S. Kim, J. Jo, J.E. Lim, Y.D. Yun, S.J. Baek, T.-Y. Lee, K.B. Huh, S.H. Jee, Adiponectin as predictor for diabetes among pre-diabetic groups. Endocrine 44, 411–418 (2013)PubMed H.-S. Kim, J. Jo, J.E. Lim, Y.D. Yun, S.J. Baek, T.-Y. Lee, K.B. Huh, S.H. Jee, Adiponectin as predictor for diabetes among pre-diabetic groups. Endocrine 44, 411–418 (2013)PubMed
41.
go back to reference J. Bai, Y. Liu, G.-F. Niu, L.-X. Bai, X.-Y. Xu, G.-Z. Zhang, L.-X. Wang, Relationship between adiponectin and testosterone in patients with type 2 diabetes. Biochem. Medica Časopis Hrvat. Društva Med. Biokem. HDMB 21, 65–70 (2011) J. Bai, Y. Liu, G.-F. Niu, L.-X. Bai, X.-Y. Xu, G.-Z. Zhang, L.-X. Wang, Relationship between adiponectin and testosterone in patients with type 2 diabetes. Biochem. Medica Časopis Hrvat. Društva Med. Biokem. HDMB 21, 65–70 (2011)
42.
go back to reference P.E. Scherer, S. Williams, M. Fogliano, G. Baldini, H.F. Lodish, A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem. 270, 26746–26749 (1995)PubMed P.E. Scherer, S. Williams, M. Fogliano, G. Baldini, H.F. Lodish, A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem. 270, 26746–26749 (1995)PubMed
43.
go back to reference L. Shapiro, P.E. Scherer, The crystal structure of a complement-1q family protein suggests an evolutionary link to tumor necrosis factor. Curr. Biol. 8, 335–338 (1998)PubMed L. Shapiro, P.E. Scherer, The crystal structure of a complement-1q family protein suggests an evolutionary link to tumor necrosis factor. Curr. Biol. 8, 335–338 (1998)PubMed
44.
go back to reference Y. Wang, K.S.L. Lam, M. Yau, A. Xu, Post-translational modifications of adiponectin: mechanisms and functional implications. Biochem. J. 409, 623–633 (2008)PubMed Y. Wang, K.S.L. Lam, M. Yau, A. Xu, Post-translational modifications of adiponectin: mechanisms and functional implications. Biochem. J. 409, 623–633 (2008)PubMed
45.
go back to reference F. Simpson, J.P. Whitehead, Adiponectin: it’s all about the modifications. Int. J. Biochem. Cell Biol. 42, 785–788 (2010)PubMed F. Simpson, J.P. Whitehead, Adiponectin: it’s all about the modifications. Int. J. Biochem. Cell Biol. 42, 785–788 (2010)PubMed
46.
go back to reference Y. Wang, A. Xu, C. Knight, L.Y. Xu, G.J.S. Cooper, Hydroxylation and glycosylation of the four conserved lysine residues in the collagenous domain of adiponectin. Potential role in the modulation of its insulin-sensitizing activity. J. Biol. Chem. 277, 19521–19529 (2002)PubMed Y. Wang, A. Xu, C. Knight, L.Y. Xu, G.J.S. Cooper, Hydroxylation and glycosylation of the four conserved lysine residues in the collagenous domain of adiponectin. Potential role in the modulation of its insulin-sensitizing activity. J. Biol. Chem. 277, 19521–19529 (2002)PubMed
47.
go back to reference Y. Wang, K.S.L. Lam, L. Chan, K.W. Chan, J.B.B. Lam, M.C. Lam, R.C.L. Hoo, W.W.N. Mak, G.J.S. Cooper, A. Xu, Post-translational modifications of the four conserved lysine residues within the collagenous domain of adiponectin are required for the formation of its high molecular weight oligomeric complex. J. Biol. Chem. 281, 16391–16400 (2006)PubMed Y. Wang, K.S.L. Lam, L. Chan, K.W. Chan, J.B.B. Lam, M.C. Lam, R.C.L. Hoo, W.W.N. Mak, G.J.S. Cooper, A. Xu, Post-translational modifications of the four conserved lysine residues within the collagenous domain of adiponectin are required for the formation of its high molecular weight oligomeric complex. J. Biol. Chem. 281, 16391–16400 (2006)PubMed
48.
go back to reference A.A. Richards, T. Stephens, H.K. Charlton, A. Jones, G.A. Macdonald, J.B. Prins, J.P. Whitehead, Adiponectin multimerization is dependent on conserved lysines in the collagenous domain: evidence for regulation of multimerization by alterations in posttranslational modifications. Mol. Endocrinol. Baltim. Md. 20, 1673–1687 (2006) A.A. Richards, T. Stephens, H.K. Charlton, A. Jones, G.A. Macdonald, J.B. Prins, J.P. Whitehead, Adiponectin multimerization is dependent on conserved lysines in the collagenous domain: evidence for regulation of multimerization by alterations in posttranslational modifications. Mol. Endocrinol. Baltim. Md. 20, 1673–1687 (2006)
49.
go back to reference T.-S. Tsao, E. Tomas, H.E. Murrey, C. Hug, D.H. Lee, N.B. Ruderman, J.E. Heuser, H.F. Lodish, Role of disulfide bonds in Acrp30/adiponectin structure and signaling specificity. Different oligomers activate different signal transduction pathways. J. Biol. Chem. 278, 50810–50817 (2003)PubMed T.-S. Tsao, E. Tomas, H.E. Murrey, C. Hug, D.H. Lee, N.B. Ruderman, J.E. Heuser, H.F. Lodish, Role of disulfide bonds in Acrp30/adiponectin structure and signaling specificity. Different oligomers activate different signal transduction pathways. J. Biol. Chem. 278, 50810–50817 (2003)PubMed
50.
go back to reference R. Basu, U.B. Pajvani, R.A. Rizza, P.E. Scherer, Selective downregulation of the high molecular weight form of adiponectin in hyperinsulinemia and in type 2 diabetes: differential regulation from nondiabetic subjects. Diabetes 56, 2174–2177 (2007)PubMed R. Basu, U.B. Pajvani, R.A. Rizza, P.E. Scherer, Selective downregulation of the high molecular weight form of adiponectin in hyperinsulinemia and in type 2 diabetes: differential regulation from nondiabetic subjects. Diabetes 56, 2174–2177 (2007)PubMed
51.
go back to reference U.B. Pajvani, M. Hawkins, T.P. Combs, M.W. Rajala, T. Doebber, J.P. Berger, J.A. Wagner, M. Wu, A. Knopps, A.H. Xiang, K.M. Utzschneider, S.E. Kahn, J.M. Olefsky, T.A. Buchanan, P.E. Scherer, Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J. Biol. Chem. 279, 12152–12162 (2004)PubMed U.B. Pajvani, M. Hawkins, T.P. Combs, M.W. Rajala, T. Doebber, J.P. Berger, J.A. Wagner, M. Wu, A. Knopps, A.H. Xiang, K.M. Utzschneider, S.E. Kahn, J.M. Olefsky, T.A. Buchanan, P.E. Scherer, Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J. Biol. Chem. 279, 12152–12162 (2004)PubMed
52.
go back to reference H. Waki, T. Yamauchi, J. Kamon, Y. Ito, S. Uchida, S. Kita, K. Hara, Y. Hada, F. Vasseur, P. Froguel, S. Kimura, R. Nagai, T. Kadowaki, Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J. Biol. Chem. 278, 40352–40363 (2003)PubMed H. Waki, T. Yamauchi, J. Kamon, Y. Ito, S. Uchida, S. Kita, K. Hara, Y. Hada, F. Vasseur, P. Froguel, S. Kimura, R. Nagai, T. Kadowaki, Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J. Biol. Chem. 278, 40352–40363 (2003)PubMed
53.
go back to reference R.B. Ceddia, R. Somwar, A. Maida, X. Fang, G. Bikopoulos, G. Sweeney, Globular adiponectin increases GLUT4 translocation and glucose uptake but reduces glycogen synthesis in rat skeletal muscle cells. Diabetologia 48, 132–139 (2005)PubMed R.B. Ceddia, R. Somwar, A. Maida, X. Fang, G. Bikopoulos, G. Sweeney, Globular adiponectin increases GLUT4 translocation and glucose uptake but reduces glycogen synthesis in rat skeletal muscle cells. Diabetologia 48, 132–139 (2005)PubMed
54.
go back to reference X. Fang, R. Palanivel, X. Zhou, Y. Liu, A. Xu, Y. Wang, G. Sweeney, Hyperglycemia- and hyperinsulinemia-induced alteration of adiponectin receptor expression and adiponectin effects in L6 myoblasts. J. Mol. Endocrinol. 35, 465–476 (2005)PubMed X. Fang, R. Palanivel, X. Zhou, Y. Liu, A. Xu, Y. Wang, G. Sweeney, Hyperglycemia- and hyperinsulinemia-induced alteration of adiponectin receptor expression and adiponectin effects in L6 myoblasts. J. Mol. Endocrinol. 35, 465–476 (2005)PubMed
55.
go back to reference E. Tomas, T.-S. Tsao, A.K. Saha, H.E. Murrey, Cc. Zhang, C. cheng, S.I. Itani, H.F. Lodish, N.B. Ruderman, Enhanced muscle fat oxidation and glucose transport by ACRP30 globular domain: acetyl-CoA carboxylase inhibition and AMP-activated protein kinase activation. Proc. Natl Acad. Sci. USA 99, 16309–16313 (2002)PubMedCentralPubMed E. Tomas, T.-S. Tsao, A.K. Saha, H.E. Murrey, Cc. Zhang, C. cheng, S.I. Itani, H.F. Lodish, N.B. Ruderman, Enhanced muscle fat oxidation and glucose transport by ACRP30 globular domain: acetyl-CoA carboxylase inhibition and AMP-activated protein kinase activation. Proc. Natl Acad. Sci. USA 99, 16309–16313 (2002)PubMedCentralPubMed
56.
go back to reference J. Fruebis, T.S. Tsao, S. Javorschi, D. Ebbets-Reed, M.R. Erickson, F.T. Yen, B.E. Bihain, H.F. Lodish, Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc. Natl Acad. Sci. USA 98, 2005–2010 (2001)PubMedCentralPubMed J. Fruebis, T.S. Tsao, S. Javorschi, D. Ebbets-Reed, M.R. Erickson, F.T. Yen, B.E. Bihain, H.F. Lodish, Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc. Natl Acad. Sci. USA 98, 2005–2010 (2001)PubMedCentralPubMed
57.
go back to reference U.B. Pajvani, X. Du, T.P. Combs, A.H. Berg, M.W. Rajala, T. Schulthess, J. Engel, M. Brownlee, P.E. Scherer, Structure–function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications fpr metabolic regulation and bioactivity. J. Biol. Chem. 278, 9073–9085 (2003)PubMed U.B. Pajvani, X. Du, T.P. Combs, A.H. Berg, M.W. Rajala, T. Schulthess, J. Engel, M. Brownlee, P.E. Scherer, Structure–function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications fpr metabolic regulation and bioactivity. J. Biol. Chem. 278, 9073–9085 (2003)PubMed
58.
go back to reference H. Waki, T. Yamauchi, J. Kamon, S. Kita, Y. Ito, Y. Hada, S. Uchida, A. Tsuchida, S. Takekawa, T. Kadowaki, Generation of globular fragment of adiponectin by leukocyte elastase secreted by monocytic cell line THP-1. Endocrinology 146, 790–796 (2005)PubMed H. Waki, T. Yamauchi, J. Kamon, S. Kita, Y. Ito, Y. Hada, S. Uchida, A. Tsuchida, S. Takekawa, T. Kadowaki, Generation of globular fragment of adiponectin by leukocyte elastase secreted by monocytic cell line THP-1. Endocrinology 146, 790–796 (2005)PubMed
59.
go back to reference C. Chabrolle, L. Tosca, J. Dupont, Regulation of adiponectin and its receptors in rat ovary by human chorionic gonadotrophin treatment and potential involvement of adiponectin in granulosa cell steroidogenesis. Reprod. Camb. Engl. 133, 719–731 (2007) C. Chabrolle, L. Tosca, J. Dupont, Regulation of adiponectin and its receptors in rat ovary by human chorionic gonadotrophin treatment and potential involvement of adiponectin in granulosa cell steroidogenesis. Reprod. Camb. Engl. 133, 719–731 (2007)
60.
go back to reference Z.V. Wang, P.E. Scherer, Adiponectin, cardiovascular function, and hypertension. Hypertension 51, 8–14 (2008)PubMed Z.V. Wang, P.E. Scherer, Adiponectin, cardiovascular function, and hypertension. Hypertension 51, 8–14 (2008)PubMed
61.
go back to reference Luque-Ramírez, M., Martínez-García, M.Á., Montes-Nieto, R., Fernández-Durán, E., Insenser, M., Alpañés, M., Escobar-Morreale, H.F.: Sexual dimorphism in adipose tissue function as evidenced by circulating adipokine concentrations in the fasting state and after an oral glucose challenge. Hum. Reprod. Oxf. Engl. 28, 1908–1918 (2013) Luque-Ramírez, M., Martínez-García, M.Á., Montes-Nieto, R., Fernández-Durán, E., Insenser, M., Alpañés, M., Escobar-Morreale, H.F.: Sexual dimorphism in adipose tissue function as evidenced by circulating adipokine concentrations in the fasting state and after an oral glucose challenge. Hum. Reprod. Oxf. Engl. 28, 1908–1918 (2013)
62.
go back to reference T.P. Combs, A.H. Berg, M.W. Rajala, S. Klebanov, P. Iyengar, J.C. Jimenez-Chillaron, M.E. Patti, S.L. Klein, R.S. Weinstein, P.E. Scherer, Sexual differentiation, pregnancy, calorie restriction, and aging affect the adipocyte-specific secretory protein adiponectin. Diabetes 52, 268–276 (2003)PubMed T.P. Combs, A.H. Berg, M.W. Rajala, S. Klebanov, P. Iyengar, J.C. Jimenez-Chillaron, M.E. Patti, S.L. Klein, R.S. Weinstein, P.E. Scherer, Sexual differentiation, pregnancy, calorie restriction, and aging affect the adipocyte-specific secretory protein adiponectin. Diabetes 52, 268–276 (2003)PubMed
63.
go back to reference K. Robinson, J. Prins, B. Venkatesh, Clinical review: adiponectin biology and its role in inflammation and critical illness. Crit. Care Lond. Engl. 15, 221 (2011) K. Robinson, J. Prins, B. Venkatesh, Clinical review: adiponectin biology and its role in inflammation and critical illness. Crit. Care Lond. Engl. 15, 221 (2011)
64.
go back to reference K. Brochu-Gaudreau, C. Rehfeldt, R. Blouin, V. Bordignon, B.D. Murphy, M.-F. Palin, Adiponectin action from head to toe. Endocrine 37, 11–32 (2010)PubMed K. Brochu-Gaudreau, C. Rehfeldt, R. Blouin, V. Bordignon, B.D. Murphy, M.-F. Palin, Adiponectin action from head to toe. Endocrine 37, 11–32 (2010)PubMed
65.
go back to reference M. Calvani, A. Scarfone, L. Granato, E.V. Mora, G. Nanni, M. Castagneto, A.V. Greco, M. Manco, G. Mingrone, Restoration of adiponectin pulsatility in severely obese subjects after weight loss. Diabetes 53, 939–947 (2004)PubMed M. Calvani, A. Scarfone, L. Granato, E.V. Mora, G. Nanni, M. Castagneto, A.V. Greco, M. Manco, G. Mingrone, Restoration of adiponectin pulsatility in severely obese subjects after weight loss. Diabetes 53, 939–947 (2004)PubMed
66.
go back to reference L. Fajas, J.C. Fruchart, J. Auwerx, Transcriptional control of adipogenesis. Curr. Opin. Cell Biol. 10, 165–173 (1998)PubMed L. Fajas, J.C. Fruchart, J. Auwerx, Transcriptional control of adipogenesis. Curr. Opin. Cell Biol. 10, 165–173 (1998)PubMed
67.
go back to reference T.F. Osborne, Sterol regulatory element-binding proteins (SREBPs): key regulators of nutritional homeostasis and insulin action. J. Biol. Chem. 275, 32379–32382 (2000)PubMed T.F. Osborne, Sterol regulatory element-binding proteins (SREBPs): key regulators of nutritional homeostasis and insulin action. J. Biol. Chem. 275, 32379–32382 (2000)PubMed
68.
go back to reference M.I. Yilmaz, A. Sonmez, K. Caglar, D.E. Gok, T. Eyileten, M. Yenicesu, C. Acikel, N. Bingol, S. Kilic, Y. Oguz, A. Vural, Peroxisome proliferator-activated receptor gamma (PPAR-gamma) agonist increases plasma adiponectin levels in type 2 diabetic patients with proteinuria. Endocrine 25, 207–214 (2004)PubMed M.I. Yilmaz, A. Sonmez, K. Caglar, D.E. Gok, T. Eyileten, M. Yenicesu, C. Acikel, N. Bingol, S. Kilic, Y. Oguz, A. Vural, Peroxisome proliferator-activated receptor gamma (PPAR-gamma) agonist increases plasma adiponectin levels in type 2 diabetic patients with proteinuria. Endocrine 25, 207–214 (2004)PubMed
69.
go back to reference A.C. Doran, N. Meller, A. Cutchins, H. Deliri, R.P. Slayton, S.N. Oldham, J.B. Kim, S.R. Keller, C.A. McNamara, The helix–loop–helix factors Id3 and E47 are novel regulators of adiponectin. Circ. Res. 103, 624–634 (2008)PubMedCentralPubMed A.C. Doran, N. Meller, A. Cutchins, H. Deliri, R.P. Slayton, S.N. Oldham, J.B. Kim, S.R. Keller, C.A. McNamara, The helix–loop–helix factors Id3 and E47 are novel regulators of adiponectin. Circ. Res. 103, 624–634 (2008)PubMedCentralPubMed
70.
go back to reference N. Maeda, M. Takahashi, T. Funahashi, S. Kihara, H. Nishizawa, K. Kishida, H. Nagaretani, M. Matsuda, R. Komuro, N. Ouchi, H. Kuriyama, K. Hotta, T. Nakamura, I. Shimomura, Y. Matsuzawa, PPAR gamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes 50, 2094–2099 (2001)PubMed N. Maeda, M. Takahashi, T. Funahashi, S. Kihara, H. Nishizawa, K. Kishida, H. Nagaretani, M. Matsuda, R. Komuro, N. Ouchi, H. Kuriyama, K. Hotta, T. Nakamura, I. Shimomura, Y. Matsuzawa, PPAR gamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes 50, 2094–2099 (2001)PubMed
71.
go back to reference M. Iwaki, M. Matsuda, N. Maeda, T. Funahashi, Y. Matsuzawa, M. Makishima, I. Shimomura, Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes 52, 1655–1663 (2003)PubMed M. Iwaki, M. Matsuda, N. Maeda, T. Funahashi, Y. Matsuzawa, M. Makishima, I. Shimomura, Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes 52, 1655–1663 (2003)PubMed
72.
go back to reference K. Thomas, D.-Y. Sung, X. Chen, W. Thompson, Y.E. Chen, J. McCarrey, W. Walker, M. Griswold, Developmental patterns of PPAR and RXR gene expression during spermatogenesis. Front. Biosci. Elite Ed. 3, 1209–1220 (2011)PubMed K. Thomas, D.-Y. Sung, X. Chen, W. Thompson, Y.E. Chen, J. McCarrey, W. Walker, M. Griswold, Developmental patterns of PPAR and RXR gene expression during spermatogenesis. Front. Biosci. Elite Ed. 3, 1209–1220 (2011)PubMed
73.
go back to reference M.P. Kowalewski, M.T. Dyson, P.R. Manna, D.M. Stocco, Involvement of peroxisome proliferator-activated receptor gamma in gonadal steroidogenesis and steroidogenic acute regulatory protein expression. Reprod. Fertil. Dev. 21, 909–922 (2009)PubMed M.P. Kowalewski, M.T. Dyson, P.R. Manna, D.M. Stocco, Involvement of peroxisome proliferator-activated receptor gamma in gonadal steroidogenesis and steroidogenic acute regulatory protein expression. Reprod. Fertil. Dev. 21, 909–922 (2009)PubMed
74.
go back to reference B. El-Asmar, X.C. Giner, J.J. Tremblay, Transcriptional cooperation between NF-kappaB p50 and CCAAT/enhancer binding protein beta regulates Nur77 transcription in Leydig cells. J. Mol. Endocrinol. 42, 131–138 (2009)PubMed B. El-Asmar, X.C. Giner, J.J. Tremblay, Transcriptional cooperation between NF-kappaB p50 and CCAAT/enhancer binding protein beta regulates Nur77 transcription in Leydig cells. J. Mol. Endocrinol. 42, 131–138 (2009)PubMed
75.
go back to reference L.M. Grønning, M.K. Dahle, K.A. Taskén, S. Enerbäck, L. Hedin, K. Taskén, H.K. Knutsen, Isoform-specific regulation of the CCAAT/enhancer-binding protein family of transcription factors by 3′,5′-cyclic adenosine monophosphate in Sertoli cells. Endocrinology 140, 835–843 (1999)PubMed L.M. Grønning, M.K. Dahle, K.A. Taskén, S. Enerbäck, L. Hedin, K. Taskén, H.K. Knutsen, Isoform-specific regulation of the CCAAT/enhancer-binding protein family of transcription factors by 3′,5′-cyclic adenosine monophosphate in Sertoli cells. Endocrinology 140, 835–843 (1999)PubMed
76.
go back to reference H. Wang, F. Liu, C.F. Millette, D.L. Kilpatrick, Expression of a novel, sterol-insensitive form of sterol regulatory element binding protein 2 (SREBP2) in male germ cells suggests important cell- and stage-specific functions for SREBP targets during spermatogenesis. Mol. Cell. Biol. 22, 8478–8490 (2002)PubMedCentralPubMed H. Wang, F. Liu, C.F. Millette, D.L. Kilpatrick, Expression of a novel, sterol-insensitive form of sterol regulatory element binding protein 2 (SREBP2) in male germ cells suggests important cell- and stage-specific functions for SREBP targets during spermatogenesis. Mol. Cell. Biol. 22, 8478–8490 (2002)PubMedCentralPubMed
77.
go back to reference M. Carroll, B. Robaire, Null mutation of the transcription factor inhibitor of DNA binding 3 (ID3) in male mice adversely impacts on fertility and reproductive outcome. J. Androl. 33, 667–674 (2012)PubMed M. Carroll, B. Robaire, Null mutation of the transcription factor inhibitor of DNA binding 3 (ID3) in male mice adversely impacts on fertility and reproductive outcome. J. Androl. 33, 667–674 (2012)PubMed
78.
go back to reference J. Chaudhary, J. Johnson, G. Kim, M.K. Skinner, Hormonal regulation and differential actions of the helix–loop–helix transcriptional inhibitors of differentiation (Id1, Id2, Id3, and Id4) in Sertoli cells. Endocrinology 142, 1727–1736 (2001)PubMed J. Chaudhary, J. Johnson, G. Kim, M.K. Skinner, Hormonal regulation and differential actions of the helix–loop–helix transcriptional inhibitors of differentiation (Id1, Id2, Id3, and Id4) in Sertoli cells. Endocrinology 142, 1727–1736 (2001)PubMed
79.
go back to reference J. Chaudhary, M.K. Skinner, The basic helix–loop–helix E2A gene product E47, not E12, is present in differentiating Sertoli cells. Mol. Reprod. Dev. 52, 1–8 (1999) J. Chaudhary, M.K. Skinner, The basic helix–loop–helix E2A gene product E47, not E12, is present in differentiating Sertoli cells. Mol. Reprod. Dev. 52, 1–8 (1999)
80.
go back to reference T. Yamauchi, J. Kamon, Y. Ito, A. Tsuchida, T. Yokomizo, S. Kita, T. Sugiyama, M. Miyagishi, K. Hara, M. Tsunoda, K. Murakami, T. Ohteki, S. Uchida, S. Takekawa, H. Waki, N.H. Tsuno, Y. Shibata, Y. Terauchi, P. Froguel, K. Tobe, S. Koyasu, K. Taira, T. Kitamura, T. Shimizu, R. Nagai, T. Kadowaki, Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423, 762–769 (2003)PubMed T. Yamauchi, J. Kamon, Y. Ito, A. Tsuchida, T. Yokomizo, S. Kita, T. Sugiyama, M. Miyagishi, K. Hara, M. Tsunoda, K. Murakami, T. Ohteki, S. Uchida, S. Takekawa, H. Waki, N.H. Tsuno, Y. Shibata, Y. Terauchi, P. Froguel, K. Tobe, S. Koyasu, K. Taira, T. Kitamura, T. Shimizu, R. Nagai, T. Kadowaki, Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423, 762–769 (2003)PubMed
81.
go back to reference T. Yamauchi, Y. Nio, T. Maki, M. Kobayashi, T. Takazawa, M. Iwabu, M. Okada-Iwabu, S. Kawamoto, N. Kubota, T. Kubota, Y. Ito, J. Kamon, A. Tsuchida, K. Kumagai, H. Kozono, Y. Hada, H. Ogata, K. Tokuyama, M. Tsunoda, T. Ide, K. Murakami, M. Awazawa, I. Takamoto, P. Froguel, K. Hara, K. Tobe, R. Nagai, K. Ueki, T. Kadowaki, Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med. 13, 332–339 (2007)PubMed T. Yamauchi, Y. Nio, T. Maki, M. Kobayashi, T. Takazawa, M. Iwabu, M. Okada-Iwabu, S. Kawamoto, N. Kubota, T. Kubota, Y. Ito, J. Kamon, A. Tsuchida, K. Kumagai, H. Kozono, Y. Hada, H. Ogata, K. Tokuyama, M. Tsunoda, T. Ide, K. Murakami, M. Awazawa, I. Takamoto, P. Froguel, K. Hara, K. Tobe, R. Nagai, K. Ueki, T. Kadowaki, Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med. 13, 332–339 (2007)PubMed
82.
go back to reference M. Bjursell, A. Ahnmark, M. Bohlooly-Y, L. William-Olsson, M. Rhedin, X.-R. Peng, K. Ploj, A.-K. Gerdin, G. Arnerup, A. Elmgren, A.-L. Berg, J. Oscarsson, D. Lindén, Opposing effects of adiponectin receptors 1 and 2 on energy metabolism. Diabetes 56, 583–593 (2007)PubMed M. Bjursell, A. Ahnmark, M. Bohlooly-Y, L. William-Olsson, M. Rhedin, X.-R. Peng, K. Ploj, A.-K. Gerdin, G. Arnerup, A. Elmgren, A.-L. Berg, J. Oscarsson, D. Lindén, Opposing effects of adiponectin receptors 1 and 2 on energy metabolism. Diabetes 56, 583–593 (2007)PubMed
83.
go back to reference K. Kos, A.L. Harte, N.F. da Silva, A. Tonchev, G. Chaldakov, S. James, D.R. Snead, B. Hoggart, J.P. O’Hare, P.G. McTernan, S. Kumar, Adiponectin and resistin in human cerebrospinal fluid and expression of adiponectin receptors in the human hypothalamus. J. Clin. Endocrinol. Metab. 92, 1129–1136 (2007)PubMed K. Kos, A.L. Harte, N.F. da Silva, A. Tonchev, G. Chaldakov, S. James, D.R. Snead, B. Hoggart, J.P. O’Hare, P.G. McTernan, S. Kumar, Adiponectin and resistin in human cerebrospinal fluid and expression of adiponectin receptors in the human hypothalamus. J. Clin. Endocrinol. Metab. 92, 1129–1136 (2007)PubMed
84.
go back to reference F. Rodriguez-Pacheco, A.J. Martinez-Fuentes, S. Tovar, L. Pinilla, M. Tena-Sempere, C. Dieguez, J.P. Castaño, M.M. Malagon, Regulation of pituitary cell function by adiponectin. Endocrinology 148, 401–410 (2007)PubMed F. Rodriguez-Pacheco, A.J. Martinez-Fuentes, S. Tovar, L. Pinilla, M. Tena-Sempere, C. Dieguez, J.P. Castaño, M.M. Malagon, Regulation of pituitary cell function by adiponectin. Endocrinology 148, 401–410 (2007)PubMed
85.
go back to reference J.E. Caminos, R. Nogueiras, F. Gaytán, R. Pineda, C.R. González, M.L. Barreiro, J.P. Castaño, M.M. Malagón, L. Pinilla, J. Toppari, C. Diéguez, M. Tena-Sempere, Novel expression and direct effects of adiponectin in the rat testis. Endocrinology 149, 3390–3402 (2008)PubMed J.E. Caminos, R. Nogueiras, F. Gaytán, R. Pineda, C.R. González, M.L. Barreiro, J.P. Castaño, M.M. Malagón, L. Pinilla, J. Toppari, C. Diéguez, M. Tena-Sempere, Novel expression and direct effects of adiponectin in the rat testis. Endocrinology 149, 3390–3402 (2008)PubMed
86.
go back to reference E. Lord, S. Ledoux, B.D. Murphy, D. Beaudry, M.F. Palin, Expression of adiponectin and its receptors in swine. J. Anim. Sci. 83, 565–578 (2005)PubMed E. Lord, S. Ledoux, B.D. Murphy, D. Beaudry, M.F. Palin, Expression of adiponectin and its receptors in swine. J. Anim. Sci. 83, 565–578 (2005)PubMed
87.
go back to reference S. Ledoux, D.B. Campos, F.L. Lopes, M. Dobias-Goff, M.-F. Palin, B.D. Murphy, Adiponectin induces periovulatory changes in ovarian follicular cells. Endocrinology 147, 5178–5186 (2006)PubMed S. Ledoux, D.B. Campos, F.L. Lopes, M. Dobias-Goff, M.-F. Palin, B.D. Murphy, Adiponectin induces periovulatory changes in ovarian follicular cells. Endocrinology 147, 5178–5186 (2006)PubMed
88.
go back to reference R. Ramachandran, O.M. Ocón-Grove, S.L. Metzger, Molecular cloning and tissue expression of chicken AdipoR1 and AdipoR2 complementary deoxyribonucleic acids. Domest. Anim. Endocrinol. 33, 19–31 (2007)PubMed R. Ramachandran, O.M. Ocón-Grove, S.L. Metzger, Molecular cloning and tissue expression of chicken AdipoR1 and AdipoR2 complementary deoxyribonucleic acids. Domest. Anim. Endocrinol. 33, 19–31 (2007)PubMed
89.
go back to reference C. Chabrolle, L. Tosca, S. Crochet, S. Tesseraud, J. Dupont, Expression of adiponectin and its receptors (AdipoR1 and AdipoR2) in chicken ovary: potential role in ovarian steroidogenesis. Domest. Anim. Endocrinol. 33, 480–487 (2007)PubMed C. Chabrolle, L. Tosca, S. Crochet, S. Tesseraud, J. Dupont, Expression of adiponectin and its receptors (AdipoR1 and AdipoR2) in chicken ovary: potential role in ovarian steroidogenesis. Domest. Anim. Endocrinol. 33, 480–487 (2007)PubMed
90.
go back to reference A.E. Civitarese, C.P. Jenkinson, D. Richardson, M. Bajaj, K. Cusi, S. Kashyap, R. Berria, R. Belfort, R.A. DeFronzo, L.J. Mandarino, E. Ravussin, Adiponectin receptors gene expression and insulin sensitivity in non-diabetic Mexican Americans with or without a family history of Type 2 diabetes. Diabetologia 47, 816–820 (2004)PubMed A.E. Civitarese, C.P. Jenkinson, D. Richardson, M. Bajaj, K. Cusi, S. Kashyap, R. Berria, R. Belfort, R.A. DeFronzo, L.J. Mandarino, E. Ravussin, Adiponectin receptors gene expression and insulin sensitivity in non-diabetic Mexican Americans with or without a family history of Type 2 diabetes. Diabetologia 47, 816–820 (2004)PubMed
91.
go back to reference C. Hug, J. Wang, N.S. Ahmad, J.S. Bogan, T.-S. Tsao, H.F. Lodish, T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl Acad. Sci. USA 101, 10308–10313 (2004)PubMedCentralPubMed C. Hug, J. Wang, N.S. Ahmad, J.S. Bogan, T.-S. Tsao, H.F. Lodish, T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl Acad. Sci. USA 101, 10308–10313 (2004)PubMedCentralPubMed
92.
go back to reference K. Asada, H. Yoshiji, R. Noguchi, Y. Ikenaka, M. Kitade, K. Kaji, J. Yoshii, K. Yanase, T. Namisaki, M. Yamazaki, T. Tsujimoto, T. Akahane, M. Uemura, H. Fukui, Crosstalk between high-molecular-weight adiponectin and T-cadherin during liver fibrosis development in rats. Int. J. Mol. Med. 20, 725–729 (2007)PubMed K. Asada, H. Yoshiji, R. Noguchi, Y. Ikenaka, M. Kitade, K. Kaji, J. Yoshii, K. Yanase, T. Namisaki, M. Yamazaki, T. Tsujimoto, T. Akahane, M. Uemura, H. Fukui, Crosstalk between high-molecular-weight adiponectin and T-cadherin during liver fibrosis development in rats. Int. J. Mol. Med. 20, 725–729 (2007)PubMed
93.
go back to reference M.S. Denzel, M.-C. Scimia, P.M. Zumstein, K. Walsh, P. Ruiz-Lozano, B. Ranscht, T-cadherin is critical for adiponectin-mediated cardioprotection in mice. J. Clin. Invest. 120, 4342–4352 (2010)PubMedCentralPubMed M.S. Denzel, M.-C. Scimia, P.M. Zumstein, K. Walsh, P. Ruiz-Lozano, B. Ranscht, T-cadherin is critical for adiponectin-mediated cardioprotection in mice. J. Clin. Invest. 120, 4342–4352 (2010)PubMedCentralPubMed
94.
go back to reference T. Takeuchi, Y. Adachi, Y. Ohtsuki, M. Furihata, Adiponectin receptors, with special focus on the role of the third receptor, T-cadherin, in vascular disease. Med. Mol. Morphol. 40, 115–120 (2007)PubMed T. Takeuchi, Y. Adachi, Y. Ohtsuki, M. Furihata, Adiponectin receptors, with special focus on the role of the third receptor, T-cadherin, in vascular disease. Med. Mol. Morphol. 40, 115–120 (2007)PubMed
95.
go back to reference A.V. Andreeva, J. Han, M.A. Kutuzov, J. Profirovic, V.A. Tkachuk, T.A. Voyno-Yasenetskaya, T-cadherin modulates endothelial barrier function. J. Cell. Physiol. 223, 94–102 (2010)PubMed A.V. Andreeva, J. Han, M.A. Kutuzov, J. Profirovic, V.A. Tkachuk, T.A. Voyno-Yasenetskaya, T-cadherin modulates endothelial barrier function. J. Cell. Physiol. 223, 94–102 (2010)PubMed
96.
go back to reference S.B. Munro, O.W. Blaschuk, A comprehensive survey of the cadherins expressed in the testes of fetal, immature, and adult mice utilizing the polymerase chain reaction. Biol. Reprod. 55, 822–827 (1996)PubMed S.B. Munro, O.W. Blaschuk, A comprehensive survey of the cadherins expressed in the testes of fetal, immature, and adult mice utilizing the polymerase chain reaction. Biol. Reprod. 55, 822–827 (1996)PubMed
97.
go back to reference X. Mao, C.K. Kikani, R.A. Riojas, P. Langlais, L. Wang, F.J. Ramos, Q. Fang, C.Y. Christ-Roberts, J.Y. Hong, R.-Y. Kim, F. Liu, L.Q. Dong, APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat. Cell Biol. 8, 516–523 (2006)PubMed X. Mao, C.K. Kikani, R.A. Riojas, P. Langlais, L. Wang, F.J. Ramos, Q. Fang, C.Y. Christ-Roberts, J.Y. Hong, R.-Y. Kim, F. Liu, L.Q. Dong, APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat. Cell Biol. 8, 516–523 (2006)PubMed
98.
go back to reference M.J. Yoon, G.Y. Lee, J–.J. Chung, Y.H. Ahn, S.H. Hong, J.B. Kim, Adiponectin increases fatty acid oxidation in skeletal muscle cells by sequential activation of AMP-activated protein kinase, p38 mitogen-activated protein kinase, and peroxisome proliferator-activated receptor alpha. Diabetes 55, 2562–2570 (2006)PubMed M.J. Yoon, G.Y. Lee, J–.J. Chung, Y.H. Ahn, S.H. Hong, J.B. Kim, Adiponectin increases fatty acid oxidation in skeletal muscle cells by sequential activation of AMP-activated protein kinase, p38 mitogen-activated protein kinase, and peroxisome proliferator-activated receptor alpha. Diabetes 55, 2562–2570 (2006)PubMed
99.
go back to reference T. Yamauchi, J. Kamon, Y. Minokoshi, Y. Ito, H. Waki, S. Uchida, S. Yamashita, M. Noda, S. Kita, K. Ueki, K. Eto, Y. Akanuma, P. Froguel, F. Foufelle, P. Ferre, D. Carling, S. Kimura, R. Nagai, B.B. Kahn, T. Kadowaki, Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 8, 1288–1295 (2002)PubMed T. Yamauchi, J. Kamon, Y. Minokoshi, Y. Ito, H. Waki, S. Uchida, S. Yamashita, M. Noda, S. Kita, K. Ueki, K. Eto, Y. Akanuma, P. Froguel, F. Foufelle, P. Ferre, D. Carling, S. Kimura, R. Nagai, B.B. Kahn, T. Kadowaki, Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 8, 1288–1295 (2002)PubMed
100.
go back to reference Y. Li, D.H. Ramdhan, H. Naito, N. Yamagishi, Y. Ito, Y. Hayashi, Y. Yanagiba, A. Okamura, H. Tamada, F.J. Gonzalez, T. Nakajima, Ammonium perfluorooctanoate may cause testosterone reduction by adversely affecting testis in relation to PPARα. Toxicol. Lett. 205, 265–272 (2011)PubMed Y. Li, D.H. Ramdhan, H. Naito, N. Yamagishi, Y. Ito, Y. Hayashi, Y. Yanagiba, A. Okamura, H. Tamada, F.J. Gonzalez, T. Nakajima, Ammonium perfluorooctanoate may cause testosterone reduction by adversely affecting testis in relation to PPARα. Toxicol. Lett. 205, 265–272 (2011)PubMed
101.
go back to reference L. Brion, P.M. Maloberti, N.V. Gomez, C. Poderoso, A.B. Gorostizaga, M.M.M.S. Garcia, A.B. Acquier, M. Cooke, C.F. Mendez, E.J. Podesta, C. Paz, MAPK phosphatase-1 (MKP-1) expression is up-regulated by hCG/cAMP and modulates steroidogenesis in MA-10 Leydig cells. Endocrinology 152, 2665–2677 (2011)PubMed L. Brion, P.M. Maloberti, N.V. Gomez, C. Poderoso, A.B. Gorostizaga, M.M.M.S. Garcia, A.B. Acquier, M. Cooke, C.F. Mendez, E.J. Podesta, C. Paz, MAPK phosphatase-1 (MKP-1) expression is up-regulated by hCG/cAMP and modulates steroidogenesis in MA-10 Leydig cells. Endocrinology 152, 2665–2677 (2011)PubMed
102.
go back to reference S.W. Ahn, G.-T. Gang, S. Tadi, B. Nedumaran, Y.D. Kim, J.H. Park, G.R. Kweon, S.-H. Koo, K. Lee, R.-S. Ahn, Y.-H. Yim, C.-H. Lee, R.A. Harris, H.-S. Choi, Phosphoenolpyruvate carboxykinase and glucose-6-phosphatase are required for steroidogenesis in testicular Leydig cells. J. Biol. Chem. 287, 41875–41887 (2012)PubMedCentralPubMed S.W. Ahn, G.-T. Gang, S. Tadi, B. Nedumaran, Y.D. Kim, J.H. Park, G.R. Kweon, S.-H. Koo, K. Lee, R.-S. Ahn, Y.-H. Yim, C.-H. Lee, R.A. Harris, H.-S. Choi, Phosphoenolpyruvate carboxykinase and glucose-6-phosphatase are required for steroidogenesis in testicular Leydig cells. J. Biol. Chem. 287, 41875–41887 (2012)PubMedCentralPubMed
103.
go back to reference L. Tosca, C. Chabrolle, J. Dupont, AMPK: a link between metabolism and reproduction? Médecine Sci. 24, 297–300 (2008) L. Tosca, C. Chabrolle, J. Dupont, AMPK: a link between metabolism and reproduction? Médecine Sci. 24, 297–300 (2008)
104.
go back to reference L. Tosca, P. Froment, P. Solnais, P. Ferré, F. Foufelle, J. Dupont, Adenosine 5′-monophosphate-activated protein kinase regulates progesterone secretion in rat granulosa cells. Endocrinology 146, 4500–4513 (2005)PubMed L. Tosca, P. Froment, P. Solnais, P. Ferré, F. Foufelle, J. Dupont, Adenosine 5′-monophosphate-activated protein kinase regulates progesterone secretion in rat granulosa cells. Endocrinology 146, 4500–4513 (2005)PubMed
105.
go back to reference L. Tosca, C. Chabrolle, S. Uzbekova, J. Dupont, Effects of metformin on bovine granulosa cells steroidogenesis: possible involvement of adenosine 5′ monophosphate-activated protein kinase (AMPK). Biol. Reprod. 76, 368–378 (2007)PubMed L. Tosca, C. Chabrolle, S. Uzbekova, J. Dupont, Effects of metformin on bovine granulosa cells steroidogenesis: possible involvement of adenosine 5′ monophosphate-activated protein kinase (AMPK). Biol. Reprod. 76, 368–378 (2007)PubMed
106.
go back to reference R. Ouedraogo, X. Wu, S.-Q. Xu, L. Fuchsel, H. Motoshima, K. Mahadev, K. Hough, R. Scalia, B.J. Goldstein, Adiponectin suppression of high-glucose-induced reactive oxygen species in vascular endothelial cells: evidence for involvement of a cAMP signaling pathway. Diabetes 55, 1840–1846 (2006)PubMed R. Ouedraogo, X. Wu, S.-Q. Xu, L. Fuchsel, H. Motoshima, K. Mahadev, K. Hough, R. Scalia, B.J. Goldstein, Adiponectin suppression of high-glucose-induced reactive oxygen species in vascular endothelial cells: evidence for involvement of a cAMP signaling pathway. Diabetes 55, 1840–1846 (2006)PubMed
107.
go back to reference P. Park, H. Huang, M.R. McMullen, K. Bryan, L.E. Nagy, Activation of cyclic-AMP response element binding protein contributes to adiponectin-stimulated interleukin-10 expression in RAW 264.7 macrophages. J. Leukoc. Biol. 83, 1258–1266 (2008)PubMed P. Park, H. Huang, M.R. McMullen, K. Bryan, L.E. Nagy, Activation of cyclic-AMP response element binding protein contributes to adiponectin-stimulated interleukin-10 expression in RAW 264.7 macrophages. J. Leukoc. Biol. 83, 1258–1266 (2008)PubMed
108.
go back to reference J.-P. Wen, W.-S. Lv, J. Yang, A.-F. Nie, X.-B. Cheng, Y. Yang, Y. Ge, X.-Y. Li, G. Ning, Globular adiponectin inhibits GnRH secretion from GT1-7 hypothalamic GnRH neurons by induction of hyperpolarization of membrane potential. Biochem. Biophys. Res. Commun. 371, 756–761 (2008)PubMed J.-P. Wen, W.-S. Lv, J. Yang, A.-F. Nie, X.-B. Cheng, Y. Yang, Y. Ge, X.-Y. Li, G. Ning, Globular adiponectin inhibits GnRH secretion from GT1-7 hypothalamic GnRH neurons by induction of hyperpolarization of membrane potential. Biochem. Biophys. Res. Commun. 371, 756–761 (2008)PubMed
109.
go back to reference N. Kubota, W. Yano, T. Kubota, T. Yamauchi, S. Itoh, H. Kumagai, H. Kozono, I. Takamoto, S. Okamoto, T. Shiuchi, R. Suzuki, H. Satoh, A. Tsuchida, M. Moroi, K. Sugi, T. Noda, H. Ebinuma, Y. Ueta, T. Kondo, E. Araki, O. Ezaki, R. Nagai, K. Tobe, Y. Terauchi, K. Ueki, Y. Minokoshi, T. Kadowaki, Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab. 6, 55–68 (2007)PubMed N. Kubota, W. Yano, T. Kubota, T. Yamauchi, S. Itoh, H. Kumagai, H. Kozono, I. Takamoto, S. Okamoto, T. Shiuchi, R. Suzuki, H. Satoh, A. Tsuchida, M. Moroi, K. Sugi, T. Noda, H. Ebinuma, Y. Ueta, T. Kondo, E. Araki, O. Ezaki, R. Nagai, K. Tobe, Y. Terauchi, K. Ueki, Y. Minokoshi, T. Kadowaki, Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab. 6, 55–68 (2007)PubMed
110.
go back to reference A. Psilopanagioti, H. Papadaki, E.F. Kranioti, T.K. Alexandrides, J.N. Varakis, Expression of adiponectin and adiponectin receptors in human pituitary gland and brain. Neuroendocrinology 89, 38–47 (2009)PubMed A. Psilopanagioti, H. Papadaki, E.F. Kranioti, T.K. Alexandrides, J.N. Varakis, Expression of adiponectin and adiponectin receptors in human pituitary gland and brain. Neuroendocrinology 89, 38–47 (2009)PubMed
111.
go back to reference M. Mitchell, D.T. Armstrong, R.L. Robker, R.J. Norman, Adipokines: implications for female fertility and obesity. Reprod. Camb. Engl. 130, 583–597 (2005) M. Mitchell, D.T. Armstrong, R.L. Robker, R.J. Norman, Adipokines: implications for female fertility and obesity. Reprod. Camb. Engl. 130, 583–597 (2005)
112.
go back to reference T.P. Combs, U.B. Pajvani, A.H. Berg, Y. Lin, L.A. Jelicks, M. Laplante, A.R. Nawrocki, M.W. Rajala, A.F. Parlow, L. Cheeseboro, Y–.Y. Ding, R.G. Russell, D. Lindemann, A. Hartley, G.R.C. Baker, S. Obici, Y. Deshaies, M. Ludgate, L. Rossetti, P.E. Scherer, A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology 145, 367–383 (2004)PubMed T.P. Combs, U.B. Pajvani, A.H. Berg, Y. Lin, L.A. Jelicks, M. Laplante, A.R. Nawrocki, M.W. Rajala, A.F. Parlow, L. Cheeseboro, Y–.Y. Ding, R.G. Russell, D. Lindemann, A. Hartley, G.R.C. Baker, S. Obici, Y. Deshaies, M. Ludgate, L. Rossetti, P.E. Scherer, A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology 145, 367–383 (2004)PubMed
113.
go back to reference N. Kubota, Y. Terauchi, T. Yamauchi, T. Kubota, M. Moroi, J. Matsui, K. Eto, T. Yamashita, J. Kamon, H. Satoh, W. Yano, P. Froguel, R. Nagai, S. Kimura, T. Kadowaki, T. Noda, Disruption of adiponectin causes insulin resistance and neointimal formation. J. Biol. Chem. 277, 25863–25866 (2002)PubMed N. Kubota, Y. Terauchi, T. Yamauchi, T. Kubota, M. Moroi, J. Matsui, K. Eto, T. Yamashita, J. Kamon, H. Satoh, W. Yano, P. Froguel, R. Nagai, S. Kimura, T. Kadowaki, T. Noda, Disruption of adiponectin causes insulin resistance and neointimal formation. J. Biol. Chem. 277, 25863–25866 (2002)PubMed
114.
go back to reference K. Ma, A. Cabrero, P.K. Saha, H. Kojima, L. Li, B.H.-J. Chang, A. Paul, L. Chan, Increased beta-oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J. Biol. Chem. 277, 34658–34661 (2002)PubMed K. Ma, A. Cabrero, P.K. Saha, H. Kojima, L. Li, B.H.-J. Chang, A. Paul, L. Chan, Increased beta-oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J. Biol. Chem. 277, 34658–34661 (2002)PubMed
115.
go back to reference N. Maeda, I. Shimomura, K. Kishida, H. Nishizawa, M. Matsuda, H. Nagaretani, N. Furuyama, H. Kondo, M. Takahashi, Y. Arita, R. Komuro, N. Ouchi, S. Kihara, Y. Tochino, K. Okutomi, M. Horie, S. Takeda, T. Aoyama, T. Funahashi, Y. Matsuzawa, Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 8, 731–737 (2002)PubMed N. Maeda, I. Shimomura, K. Kishida, H. Nishizawa, M. Matsuda, H. Nagaretani, N. Furuyama, H. Kondo, M. Takahashi, Y. Arita, R. Komuro, N. Ouchi, S. Kihara, Y. Tochino, K. Okutomi, M. Horie, S. Takeda, T. Aoyama, T. Funahashi, Y. Matsuzawa, Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 8, 731–737 (2002)PubMed
116.
go back to reference W. Pan, H. Tu, A.J. Kastin, Differential BBB interactions of three ingestive peptides: obestatin, ghrelin, and adiponectin. Peptides 27, 911–916 (2006)PubMed W. Pan, H. Tu, A.J. Kastin, Differential BBB interactions of three ingestive peptides: obestatin, ghrelin, and adiponectin. Peptides 27, 911–916 (2006)PubMed
117.
go back to reference J. Spranger, S. Verma, I. Göhring, T. Bobbert, J. Seifert, A.L. Sindler, A. Pfeiffer, S.M. Hileman, M. Tschöp, W.A. Banks, Adiponectin does not cross the blood–brain barrier but modifies cytokine expression of brain endothelial cells. Diabetes 55, 141–147 (2006)PubMed J. Spranger, S. Verma, I. Göhring, T. Bobbert, J. Seifert, A.L. Sindler, A. Pfeiffer, S.M. Hileman, M. Tschöp, W.A. Banks, Adiponectin does not cross the blood–brain barrier but modifies cytokine expression of brain endothelial cells. Diabetes 55, 141–147 (2006)PubMed
118.
go back to reference Y. Qi, N. Takahashi, S.M. Hileman, H.R. Patel, A.H. Berg, U.B. Pajvani, P.E. Scherer, R.S. Ahima, Adiponectin acts in the brain to decrease body weight. Nat. Med. 10, 524–529 (2004)PubMed Y. Qi, N. Takahashi, S.M. Hileman, H.R. Patel, A.H. Berg, U.B. Pajvani, P.E. Scherer, R.S. Ahima, Adiponectin acts in the brain to decrease body weight. Nat. Med. 10, 524–529 (2004)PubMed
119.
go back to reference C.M. Kusminski, P.G. McTernan, T. Schraw, K. Kos, J.P. O’Hare, R. Ahima, S. Kumar, P.E. Scherer, Adiponectin complexes in human cerebrospinal fluid: distinct complex distribution from serum. Diabetologia 50, 634–642 (2007)PubMed C.M. Kusminski, P.G. McTernan, T. Schraw, K. Kos, J.P. O’Hare, R. Ahima, S. Kumar, P.E. Scherer, Adiponectin complexes in human cerebrospinal fluid: distinct complex distribution from serum. Diabetologia 50, 634–642 (2007)PubMed
120.
go back to reference X.-B. Cheng, J.-P. Wen, J. Yang, Y. Yang, G. Ning, X.-Y. Li, GnRH secretion is inhibited by adiponectin through activation of AMP-activated protein kinase and extracellular signal-regulated kinase. Endocrine 39, 6–12 (2011)PubMed X.-B. Cheng, J.-P. Wen, J. Yang, Y. Yang, G. Ning, X.-Y. Li, GnRH secretion is inhibited by adiponectin through activation of AMP-activated protein kinase and extracellular signal-regulated kinase. Endocrine 39, 6–12 (2011)PubMed
121.
go back to reference J.-P. Wen, C. Liu, W.-K. Bi, Y.-T. Hu, Q. Chen, H. Huang, J.-X. Liang, L.-T. Li, L.-X. Lin, G. Chen, Adiponectin inhibits KISS1 gene transcription through AMPK and specificity protein-1 in the hypothalamic GT1-7 neurons. J. Endocrinol. 214, 177–189 (2012)PubMed J.-P. Wen, C. Liu, W.-K. Bi, Y.-T. Hu, Q. Chen, H. Huang, J.-X. Liang, L.-T. Li, L.-X. Lin, G. Chen, Adiponectin inhibits KISS1 gene transcription through AMPK and specificity protein-1 in the hypothalamic GT1-7 neurons. J. Endocrinol. 214, 177–189 (2012)PubMed
122.
go back to reference M. Lu, Q. Tang, J.M. Olefsky, P.L. Mellon, N.J.G. Webster, Adiponectin activates adenosine monophosphate-activated protein kinase and decreases luteinizing hormone secretion in LbetaT2 gonadotropes. Mol. Endocrinol. Baltim. Md. 22, 760–771 (2008) M. Lu, Q. Tang, J.M. Olefsky, P.L. Mellon, N.J.G. Webster, Adiponectin activates adenosine monophosphate-activated protein kinase and decreases luteinizing hormone secretion in LbetaT2 gonadotropes. Mol. Endocrinol. Baltim. Md. 22, 760–771 (2008)
123.
go back to reference O.M. Ocón-Grove, S.M. Krzysik-Walker, S.R. Maddineni, G.L. Hendricks 3rd, R. Ramachandran, Adiponectin and its receptors are expressed in the chicken testis: influence of sexual maturation on testicular ADIPOR1 and ADIPOR2 mRNA abundance. Reprod. Camb. Engl. 136, 627–638 (2008) O.M. Ocón-Grove, S.M. Krzysik-Walker, S.R. Maddineni, G.L. Hendricks 3rd, R. Ramachandran, Adiponectin and its receptors are expressed in the chicken testis: influence of sexual maturation on testicular ADIPOR1 and ADIPOR2 mRNA abundance. Reprod. Camb. Engl. 136, 627–638 (2008)
124.
go back to reference A. Pfaehler, M.K. Nanjappa, E.S. Coleman, M. Mansour, D. Wanders, E.P. Plaisance, R.L. Judd, B.T. Akingbemi, Regulation of adiponectin secretion by soy isoflavones has implication for endocrine function of the testis. Toxicol. Lett. 209, 78–85 (2012)PubMed A. Pfaehler, M.K. Nanjappa, E.S. Coleman, M. Mansour, D. Wanders, E.P. Plaisance, R.L. Judd, B.T. Akingbemi, Regulation of adiponectin secretion by soy isoflavones has implication for endocrine function of the testis. Toxicol. Lett. 209, 78–85 (2012)PubMed
125.
go back to reference J.E. Caminos, R. Nogueiras, R. Gallego, S. Bravo, S. Tovar, T. García-Caballero, F.F. Casanueva, C. Diéguez, Expression and regulation of adiponectin and receptor in human and rat placenta. J. Clin. Endocrinol. Metab. 90, 4276–4286 (2005)PubMed J.E. Caminos, R. Nogueiras, R. Gallego, S. Bravo, S. Tovar, T. García-Caballero, F.F. Casanueva, C. Diéguez, Expression and regulation of adiponectin and receptor in human and rat placenta. J. Clin. Endocrinol. Metab. 90, 4276–4286 (2005)PubMed
126.
go back to reference P. Li, F. Sun, H.-M. Cao, Q.-Y. Ma, C.-M. Pan, J.-H. Ma, X.-N. Zhang, H. Jiang, H.-D. Song, M.-D. Chen, Expression of adiponectin receptors in mouse adrenal glands and the adrenocortical Y-1 cell line: adiponectin regulates steroidogenesis. Biochem. Biophys. Res. Commun. 390, 1208–1213 (2009)PubMed P. Li, F. Sun, H.-M. Cao, Q.-Y. Ma, C.-M. Pan, J.-H. Ma, X.-N. Zhang, H. Jiang, H.-D. Song, M.-D. Chen, Expression of adiponectin receptors in mouse adrenal glands and the adrenocortical Y-1 cell line: adiponectin regulates steroidogenesis. Biochem. Biophys. Res. Commun. 390, 1208–1213 (2009)PubMed
127.
go back to reference K.A. Toulis, D.G. Goulis, D. Farmakiotis, N.A. Georgopoulos, I. Katsikis, B.C. Tarlatzis, I. Papadimas, D. Panidis, Adiponectin levels in women with polycystic ovary syndrome: a systematic review and a meta-analysis. Hum. Reprod. Updat. 15, 297–307 (2009) K.A. Toulis, D.G. Goulis, D. Farmakiotis, N.A. Georgopoulos, I. Katsikis, B.C. Tarlatzis, I. Papadimas, D. Panidis, Adiponectin levels in women with polycystic ovary syndrome: a systematic review and a meta-analysis. Hum. Reprod. Updat. 15, 297–307 (2009)
128.
go back to reference M. Otani, M. Kogo, S. Furukawa, S. Wakisaka, T. Maeda, The adiponectin paralog C1q/TNF-related protein 3 (CTRP3) stimulates testosterone production through the cAMP/PKA signaling pathway. Cytokine 58, 238–244 (2012)PubMed M. Otani, M. Kogo, S. Furukawa, S. Wakisaka, T. Maeda, The adiponectin paralog C1q/TNF-related protein 3 (CTRP3) stimulates testosterone production through the cAMP/PKA signaling pathway. Cytokine 58, 238–244 (2012)PubMed
129.
go back to reference D.V. Lagaly, P.Y. Aad, J.A. Grado-Ahuir, L.B. Hulsey, L.J. Spicer, Role of adiponectin in regulating ovarian theca and granulosa cell function. Mol. Cell. Endocrinol. 284, 38–45 (2008)PubMed D.V. Lagaly, P.Y. Aad, J.A. Grado-Ahuir, L.B. Hulsey, L.J. Spicer, Role of adiponectin in regulating ovarian theca and granulosa cell function. Mol. Cell. Endocrinol. 284, 38–45 (2008)PubMed
130.
go back to reference C. Chabrolle, L. Tosca, C. Ramé, P. Lecomte, D. Royère, J. Dupont, Adiponectin increases insulin-like growth factor I-induced progesterone and estradiol secretion in human granulosa cells. Fertil. Steril. 92, 1988–1996 (2009)PubMed C. Chabrolle, L. Tosca, C. Ramé, P. Lecomte, D. Royère, J. Dupont, Adiponectin increases insulin-like growth factor I-induced progesterone and estradiol secretion in human granulosa cells. Fertil. Steril. 92, 1988–1996 (2009)PubMed
131.
go back to reference J.S. Richards, Z. Liu, T. Kawai, K. Tabata, H. Watanabe, D. Suresh, F.-T. Kuo, M.D. Pisarska, M. Shimada, Adiponectin and its receptors modulate granulosa cell and cumulus cell functions, fertility, and early embryo development in the mouse and human. Fertil. Steril. 98, 471–479 (2012)PubMedCentralPubMed J.S. Richards, Z. Liu, T. Kawai, K. Tabata, H. Watanabe, D. Suresh, F.-T. Kuo, M.D. Pisarska, M. Shimada, Adiponectin and its receptors modulate granulosa cell and cumulus cell functions, fertility, and early embryo development in the mouse and human. Fertil. Steril. 98, 471–479 (2012)PubMedCentralPubMed
132.
go back to reference M.-C.M. Shih, Y.-N. Chiu, M.-C. Hu, I.-C. Guo, B. Chung, Regulation of steroid production: analysis of Cyp11a1 promoter. Mol. Cell. Endocrinol. 336, 80–84 (2011)PubMed M.-C.M. Shih, Y.-N. Chiu, M.-C. Hu, I.-C. Guo, B. Chung, Regulation of steroid production: analysis of Cyp11a1 promoter. Mol. Cell. Endocrinol. 336, 80–84 (2011)PubMed
133.
go back to reference P. Pena, A.T. Reutens, C. Albanese, M. D’Amico, G. Watanabe, A. Donner, I.W. Shu, T. Williams, R.G. Pestell, Activator protein-2 mediates transcriptional activation of the CYP11A1 gene by interaction with Sp1 rather than binding to DNA. Mol. Endocrinol. Baltim. Md. 13, 1402–1416 (1999) P. Pena, A.T. Reutens, C. Albanese, M. D’Amico, G. Watanabe, A. Donner, I.W. Shu, T. Williams, R.G. Pestell, Activator protein-2 mediates transcriptional activation of the CYP11A1 gene by interaction with Sp1 rather than binding to DNA. Mol. Endocrinol. Baltim. Md. 13, 1402–1416 (1999)
134.
go back to reference T. Sugawara, M. Saito, S. Fujimoto, Sp1 and SF-1 interact and cooperate in the regulation of human steroidogenic acute regulatory protein gene expression. Endocrinology 141, 2895–2903 (2000)PubMed T. Sugawara, M. Saito, S. Fujimoto, Sp1 and SF-1 interact and cooperate in the regulation of human steroidogenic acute regulatory protein gene expression. Endocrinology 141, 2895–2903 (2000)PubMed
135.
go back to reference K. Momoi, M.R. Waterman, E.R. Simpson, U.M. Zanger, 3′,5′-Cyclic adenosine monophosphate-dependent transcription of the CYP11A (cholesterol side chain cleavage cytochrome P450) gene involves a DNA response element containing a putative binding site for transcription factor Sp1. Mol. Endocrinol. Baltim. Md. 6, 1682–1690 (1992) K. Momoi, M.R. Waterman, E.R. Simpson, U.M. Zanger, 3′,5′-Cyclic adenosine monophosphate-dependent transcription of the CYP11A (cholesterol side chain cleavage cytochrome P450) gene involves a DNA response element containing a putative binding site for transcription factor Sp1. Mol. Endocrinol. Baltim. Md. 6, 1682–1690 (1992)
136.
go back to reference H. Lin, C.-H. Yu, C.-Y. Jen, C.-F. Cheng, Y. Chou, C–.C. Chang, S.-H. Juan, Adiponectin-mediated heme oxygenase-1 induction protects against iron-induced liver injury via a PPARα dependent mechanism. Am. J. Pathol. 177, 1697–1709 (2010)PubMedCentralPubMed H. Lin, C.-H. Yu, C.-Y. Jen, C.-F. Cheng, Y. Chou, C–.C. Chang, S.-H. Juan, Adiponectin-mediated heme oxygenase-1 induction protects against iron-induced liver injury via a PPARα dependent mechanism. Am. J. Pathol. 177, 1697–1709 (2010)PubMedCentralPubMed
137.
go back to reference L.-F. Liu, W.-J. Shen, Z.H. Zhang, L.J. Wang, F.B. Kraemer, Adipocytes decrease Runx2 expression in osteoblastic cells: roles of PPARγ and adiponectin. J. Cell. Physiol. 225, 837–845 (2010)PubMed L.-F. Liu, W.-J. Shen, Z.H. Zhang, L.J. Wang, F.B. Kraemer, Adipocytes decrease Runx2 expression in osteoblastic cells: roles of PPARγ and adiponectin. J. Cell. Physiol. 225, 837–845 (2010)PubMed
138.
go back to reference F.-P. Lee, C.-Y. Jen, C–.C. Chang, Y. Chou, H. Lin, C.-M. Chou, S.-H. Juan, Mechanisms of adiponectin-mediated COX-2 induction and protection against iron injury in mouse hepatocytes. J. Cell. Physiol. 224, 837–847 (2010)PubMed F.-P. Lee, C.-Y. Jen, C–.C. Chang, Y. Chou, H. Lin, C.-M. Chou, S.-H. Juan, Mechanisms of adiponectin-mediated COX-2 induction and protection against iron injury in mouse hepatocytes. J. Cell. Physiol. 224, 837–847 (2010)PubMed
139.
go back to reference L. Wu, B. Xu, W. Fan, X. Zhu, G. Wang, A. Zhang, Adiponectin protects Leydig cells against proinflammatory cytokines by suppressing the nuclear factor-κB signaling pathway. FEBS J. 280, 3920–3927 (2013)PubMed L. Wu, B. Xu, W. Fan, X. Zhu, G. Wang, A. Zhang, Adiponectin protects Leydig cells against proinflammatory cytokines by suppressing the nuclear factor-κB signaling pathway. FEBS J. 280, 3920–3927 (2013)PubMed
140.
go back to reference C.Y. Hong, J.H. Park, R.S. Ahn, S.Y. Im, H.-S. Choi, J. Soh, S.H. Mellon, K. Lee, Molecular mechanism of suppression of testicular steroidogenesis by proinflammatory cytokine tumor necrosis factor alpha. Mol. Cell. Biol. 24, 2593–2604 (2004)PubMedCentralPubMed C.Y. Hong, J.H. Park, R.S. Ahn, S.Y. Im, H.-S. Choi, J. Soh, S.H. Mellon, K. Lee, Molecular mechanism of suppression of testicular steroidogenesis by proinflammatory cytokine tumor necrosis factor alpha. Mol. Cell. Biol. 24, 2593–2604 (2004)PubMedCentralPubMed
141.
go back to reference C.D.B. Fernandez, F.F. Bellentani, G.S.A. Fernandes, J.E. Perobelli, A.P.A. Favareto, A.F. Nascimento, A.C. Cicogna, W.D.G. Kempinas, Diet-induced obesity in rats leads to a decrease in sperm motility. Reprod. Biol. Endocrinol. 9, 32 (2011)PubMedCentralPubMed C.D.B. Fernandez, F.F. Bellentani, G.S.A. Fernandes, J.E. Perobelli, A.P.A. Favareto, A.F. Nascimento, A.C. Cicogna, W.D.G. Kempinas, Diet-induced obesity in rats leads to a decrease in sperm motility. Reprod. Biol. Endocrinol. 9, 32 (2011)PubMedCentralPubMed
142.
go back to reference F. Erdemir, D. Atilgan, F. Markoc, O. Boztepe, B. Suha-Parlaktas, S. Sahin, The effect of diet induced obesity on testicular tissue and serum oxidative stress parameters. Actas Urol. Españolas. 36, 153–159 (2012) F. Erdemir, D. Atilgan, F. Markoc, O. Boztepe, B. Suha-Parlaktas, S. Sahin, The effect of diet induced obesity on testicular tissue and serum oxidative stress parameters. Actas Urol. Españolas. 36, 153–159 (2012)
143.
go back to reference Thomas, S., Kratzsch, D., Schaab, M., Scholz, M., Grunewald, S., Thiery, J., Paasch, U., Kratzsch, J.: Seminal plasma adipokine levels are correlated with functional characteristics of spermatozoa. Fertil. Steril. 99, 1256–1263 (2013) Thomas, S., Kratzsch, D., Schaab, M., Scholz, M., Grunewald, S., Thiery, J., Paasch, U., Kratzsch, J.: Seminal plasma adipokine levels are correlated with functional characteristics of spermatozoa. Fertil. Steril. 99, 1256–1263 (2013)
144.
go back to reference Kasimanickam, V.R., Kasimanickam, R.K., Kastelic, J.P., Stevenson, J.S.: Associations of adiponectin and fertility estimates in Holstein bulls. Theriogenology 79, 766–777 (2013) Kasimanickam, V.R., Kasimanickam, R.K., Kastelic, J.P., Stevenson, J.S.: Associations of adiponectin and fertility estimates in Holstein bulls. Theriogenology 79, 766–777 (2013)
145.
go back to reference F. Rahmanifar, M.R. Tabandeh, Adiponectin and its receptors gene expression in the reproductive tract of ram. Small Rumin. Res. 105, 263–267 (2012) F. Rahmanifar, M.R. Tabandeh, Adiponectin and its receptors gene expression in the reproductive tract of ram. Small Rumin. Res. 105, 263–267 (2012)
146.
go back to reference M.H. Dai, T. Xia, G.D. Zhang, X.D. Chen, L. Gan, S.Q. Feng, H. Qiu, Y. Peng, Z.Q. Yang, Cloning, expression and chromosome localization of porcine adiponectin and adiponectin receptors genes. Domest. Anim. Endocrinol. 30, 117–125 (2006)PubMed M.H. Dai, T. Xia, G.D. Zhang, X.D. Chen, L. Gan, S.Q. Feng, H. Qiu, Y. Peng, Z.Q. Yang, Cloning, expression and chromosome localization of porcine adiponectin and adiponectin receptors genes. Domest. Anim. Endocrinol. 30, 117–125 (2006)PubMed
147.
go back to reference M. Archanco, J. Gómez-Ambrosi, M. Tena-Sempere, G. Frühbeck, M.A. Burrell, Expression of leptin and adiponectin in the rat oviduct. J. Histochem. Cytochem. Off. J. Histochem. Soc. 55, 1027–1037 (2007) M. Archanco, J. Gómez-Ambrosi, M. Tena-Sempere, G. Frühbeck, M.A. Burrell, Expression of leptin and adiponectin in the rat oviduct. J. Histochem. Cytochem. Off. J. Histochem. Soc. 55, 1027–1037 (2007)
148.
go back to reference E.R.M. Hofny, M.E. Ali, H.Z. Abdel-Hafez, E.E.-D. Kamal, E.E. Mohamed, H.G. Abd El-Azeem, T. Mostafa, Semen parameters and hormonal profile in obese fertile and infertile males. Fertil. Steril. 94, 581–584 (2010)PubMed E.R.M. Hofny, M.E. Ali, H.Z. Abdel-Hafez, E.E.-D. Kamal, E.E. Mohamed, H.G. Abd El-Azeem, T. Mostafa, Semen parameters and hormonal profile in obese fertile and infertile males. Fertil. Steril. 94, 581–584 (2010)PubMed
150.
go back to reference R. Pasquali, L. Patton, A. Gambineri, Obesity and infertility. Curr. Opin. Endocrinol. Diabetes Obes. 14, 482–487 (2007)PubMed R. Pasquali, L. Patton, A. Gambineri, Obesity and infertility. Curr. Opin. Endocrinol. Diabetes Obes. 14, 482–487 (2007)PubMed
151.
go back to reference R. Ramachandran, S. Maddineni, O. Ocón-Grove, G. Hendricks 3rd, R. Vasilatos-Younken, J.A. Hadley, Expression of adiponectin and its receptors in avian species. Gen. Comp. Endocrinol. 190, 88–95 (2013)PubMed R. Ramachandran, S. Maddineni, O. Ocón-Grove, G. Hendricks 3rd, R. Vasilatos-Younken, J.A. Hadley, Expression of adiponectin and its receptors in avian species. Gen. Comp. Endocrinol. 190, 88–95 (2013)PubMed
152.
go back to reference C. Lee, C.-H. Huang, LASAGNA-Search: an integrated web tool for transcription factor binding site search and visualization. Biotechniques 54, 141–153 (2013)PubMed C. Lee, C.-H. Huang, LASAGNA-Search: an integrated web tool for transcription factor binding site search and visualization. Biotechniques 54, 141–153 (2013)PubMed
153.
go back to reference E. Wingender, P. Dietze, H. Karas, R. Knüppel, TRANSFAC: a database on transcription factors and their DNA binding sites. Nucl. Acids Res. 24, 238–241 (1996)PubMedCentralPubMed E. Wingender, P. Dietze, H. Karas, R. Knüppel, TRANSFAC: a database on transcription factors and their DNA binding sites. Nucl. Acids Res. 24, 238–241 (1996)PubMedCentralPubMed
Metadata
Title
Implications of adiponectin in linking metabolism to testicular function
Author
Luc J. Martin
Publication date
01-05-2014
Publisher
Springer US
Published in
Endocrine / Issue 1/2014
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-013-0102-0

Other articles of this Issue 1/2014

Endocrine 1/2014 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.