Androgens Decrease Plasma Adiponectin, an Insulin-Sensitizing Adipocyte-Derived Protein
Abstract
Adiponectin, an adipose-specific secretory protein, exhibits antidiabetic and antiatherogenic properties. In the present study, we examined the effects of sex hormones on the regulation of adiponectin production. Plasma adiponectin concentrations were significantly lower in 442 men (age, 52.6 ± 11.9 years [mean ± SD]) than in 137 women (53.2 ± 12.0 years) but not different between pre- and postmenopausal women. In mice, ovariectomy did not alter plasma adiponectin levels. In contrast, high levels of plasma adiponectin were found in castrated mice. Testosterone treatment reduced plasma adiponectin concentration in both sham-operated and castrated mice. In 3T3-L1 adipocytes, testosterone reduced adiponectin secretion into the culture media, using pulse-chase study. Castration-induced increase in plasma adiponectin was associated with a significant improvement of insulin sensitivity. Our results indicate that androgens decrease plasma adiponectin and that androgen-induced hypoadiponectinemia may be related to the high risks of insulin resistance and atherosclerosis in men.
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The two major adipokines, leptin and adiponectin, have higher circulating levels in women than men.
“The two major adipokines, leptin and adiponectin, are characterized by higher circulating levels in women than men [14, 15].”
From Sex differences in metabolic homeostasis, diabetes, and obesity (2015) · cites this paper as [15]
Testosterone regulates the secretion of metabolic factors such as adiponectin and leptin.
“Testosterone has been reported to regulate the secretion of metabolic factors such as adiponectin 240 and leptin. 241”
From The role of the androgen receptor in the pathogenesis of obesity and its utility as a target for obesity treatments (2022) · cites this paper as [240]
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“…be modified by various hormonal, nutritional, pharmacological factors, circulating cytokines, inflammatory conditions and disease states (Fasshauer et al., 2002; Maeda et al., 2002; Nishizawa et al., 2002; Combs et al., 2003; Bottner et al., 2004; Tsou et al., 2004; Brochu-Gaudreau et al., 2010).”
BackgroundSex dimorphism and depot differences in adipose tissue function
White, U. A., & Tchoukalova, Y. D. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.05.006 · Cited by 281 · see citing works
Plasma Adiponectin Is an Independent Predictor of Type 2 Diabetes in Asian Indians
Snehalatha, C., Mukesh, B., Simon, M., Viswanathan, V., Haffner, S. M., & Ramachandran, A. (2003) · Diabetes Care · doi:10.2337/diacare.26.12.3226 · Cited by 274 · see citing works
Interorgan communication by exosomes, adipose tissue, and adiponectin in metabolic syndrome
Kita, S., Maeda, N., & Shimomura, I. (2019) · Journal of Clinical Investigation · doi:10.1172/jci129193 · Cited by 269 · see citing works
Self-citationFan, W., Yanase, T., Nomura, M., Okabe, T., Goto, K., Sato, T., Kawano, H., Kato, S., & Nawata, H. (2005) · Diabetes · doi:10.2337/diabetes.54.4.1000 · Cited by 269 · see citing works
“This supports a previous suggestion that testosterone inhibits adiponectin secretion from adipocytes (35,36).”
BackgroundAso, Y., Yamamoto, R., Wakabayashi, S., Uchida, T., Takayanagi, K., Takebayashi, K., Okuno, T., Inoue, T., Node, K., Tobe, T., et al. (2006) · Diabetes · doi:10.2337/db05-1525 · Cited by 264 · see citing works
“ponectin by inhibiting its secretion by adipocytes (27,28).”
BackgroundAdipokines: implications for female fertility and obesity
Mitchell, M., Armstrong, D. T., Robker, R. L., & Norman, R. J. (2005) · Reproduction · doi:10.1530/rep.1.00521 · Cited by 258 · see citing works
“2005) and mice (Nishizawa et al. 2002).”
BackgroundMetabolic function of the CTRP family of hormones
Seldin, M. M., Tan, S. Y., & Wong, G. W. (2013) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-013-9255-7 · Cited by 244 · see citing works
Clinical review: Adiponectin biology and its role in inflammation and critical illness
Robinson, K., Prins, J. B., & Venkatesh, B. (2011) · Critical Care · doi:10.1186/cc10021 · Cited by 238 · see citing works
“Th is sexual dimorphism has been attributed to the eff ect of testosterone on adiponectin secretion [ 8 ].”
BackgroundObesity and adipokines: effects on sympathetic overactivity
Smith, M. M., & Minson, C. T. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.221036 · Cited by 237 · see citing works
“Furthermore, adiponectin levels are sex specific, favouring production in women (Nishizawa et al. 2002).”
BackgroundKapoor, D., Clarke, S., Stanworth, R. D., Channer, K. S., & Jones, T. H. (2007) · European Journal of Endocrinology · doi:10.1530/eje-06-0737 · Cited by 234 · see citing works
“Testosterone therapy has also been shown to reduce adiponectin concentrations in both sham-operated and castrated mice as well as in cultured adipocytes ( 26 ).”
BackgroundRBP4: a controversial adipokine
Kotnik, P., Fischer-Posovszky, P., & Wabitsch, M. (2011) · European Journal of Endocrinology · doi:10.1530/eje-11-0431 · Cited by 233 · see citing works
Changes in Insulin Resistance and Cardiovascular Risk During Adolescence
Moran, A., Jacobs, D. R., Steinberger, J., Steffen, L. M., Pankow, J. S., Hong, C.-P., & Sinaiko, A. R. (2008) · Circulation · doi:10.1161/circulationaha.107.704569 · Cited by 224 · see citing works
Adiponectin complexes in human cerebrospinal fluid: distinct complex distribution from serum
Kusminski, C. M., McTernan, P. G., Schraw, T., Kos, K., O’Hare, J. P., Ahima, R. S., Kumar, S., & Scherer, P. E. (2007) · Diabetologia · doi:10.1007/s00125-006-0577-9 · Cited by 223 · see citing works
“Sexual dimorphism in terms of total systemic adiponectin, with women having higher levels of adiponectin than men, has been reported [10, 42 , 43].”
ResultAdiponectin: from obesity to cardiovascular disease
Antoniades, C. A., Antonopoulos, A. S., Tousoulis, D., & Stefanadis, C. (2009) · Obesity Reviews · doi:10.1111/j.1467-789x.2009.00571.x · Cited by 217 · see citing works
“Adiponectin levels have been associated with age, gender (lower in men, possibly as a result of androgens effect) (8) and smoking status, while Mediterranean diet and exercise increase its circulating levels (9–11).”
BackgroundOsteocalcin and its endocrine functions
Mizokami, A., Kawakubo‐Yasukochi, T., & Hirata, M. (2017) · Biochemical Pharmacology · doi:10.1016/j.bcp.2017.02.001 · Cited by 209 · see citing works
Adiponectin in Human Cord Blood: Relation to Fetal Birth Weight and Gender
Sivan, E., Mazaki‐Tovi, S., Pariente, C., Efraty, Y., Schiff, E., Hemi, R., & Kanety, H. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031174 · Cited by 202 · see citing works
“The difference between the sexes in adults may reflect an effect of the sex hormones (45, 46) or other mediators that are either inactive, subtle, or absent in newborns.”
BackgroundObesity and low‐grade inflammation: a paediatric perspective
Tam, C. S., Clément, K., Baur, L. A., & Tordjman, J. (2009) · Obesity Reviews · doi:10.1111/j.1467-789x.2009.00674.x · Cited by 200 · see citing works
“Additional evidence for testosterone suppressing adiponectin comes from studies in vitro and in eugonadal and castrated mice treated with testosterone (57).”
BackgroundDecrease in Serum Adiponectin Level Due to Obesity and Visceral Fat Accumulation in Children
Asayama, K., Hayashibe, H., Dobashi, K., Uchida, N., Nakane, T., Kodera, K., Shirahata, A., & Taniyama, M. (2003) · Obesity Research · doi:10.1038/oby.2003.147 · Cited by 199 · see citing works
van Himbergen, T. M. (2012) · Archives of Neurology · doi:10.1001/archneurol.2011.670 · Cited by 198 · see citing works
Adiponectin, an adipocyte-derived protein
Nedvidkova, J., Smitka, K., Kopský, V., & Hainer, V. (2005) · Physiological Research · doi:10.33549/physiolres.930600 · Cited by 195 · see citing works
Weiss, R., Dufour, S., Groszmann, A., Petersen, K. F., Dziura, J. D., Taksali, S. E., Shulman, G. I., & Caprio, S. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021711 · Cited by 193 · see citing works
Adiponectin Induces Periovulatory Changes in Ovarian Follicular Cells
Ledoux, S., Campos, D. B., Lopes, F. L., Dobias-Goff, M., Palin, M., & Murphy, B. D. (2006) · Endocrinology · doi:10.1210/en.2006-0679 · Cited by 188 · see citing works
Jian, M., Kwan, J., Bunting, M., Ng, R. C.-L., & Chan, K. H. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1492-6 · Cited by 191 · see citing works
“Numerous studies have shown that APN plays an important role in glucose and lipid metabolism [28], insulin sensitization [29], vascular protection [30] and exerting anti-atherosclerosis ef-”
BackgroundInfluence of gender, age and renal function on plasma adiponectin level: the Tanno and Sobetsu study
Isobe, T., Saitoh, S., Takagi, S., Takeuchi, H., Chiba, Y., Katoh, N., & Shimamoto, K. (2005) · European Journal of Endocrinology · doi:10.1530/eje.1.01930 · Cited by 186 · see citing works
“On the other hand, it may be because androgen inhibits the production of adiponectin that adiponectin is lower in males than in females ( 37 ).”
BackgroundMethodTsai, P., Yu, C., Hsu, S., Lee, Y., Chiou, C., Hsu, Y., Ho, S., & Chu, C. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02057.x · Cited by 187 · see citing works
“Adiponectin level has been reported to be influenced by gender in both animals and humans (Nishizawa et al., 2002; Yanakoulia et al., 2003); however, other studies have not found any effect of gender on adiponectin (Stefan et al., 2002; Yang et al., 2002b; Weiss et al., 2003).”
ResultGannagé‐Yared, M., Chédid, R., Khalifé, S., Azzi, E., Zoghbi, F., & Halaby, G. (2009) · European Journal of Endocrinology · doi:10.1530/eje-08-0952 · Cited by 182 · see citing works
Musclin, a novel skeletal muscle-derived secretory factor
Nishizawa, H., Matsuda, M., Yamada, Y., Kawai, K., Suzuki, E., Makishima, M., Kitamura, T., & Shimomura, I. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.c400066200 · Cited by 182 · see citing works
Self-citationUnderstanding androgen action in adipose tissue
O’Reilly, M. W., House, P. J., & Tomlinson., J. W. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.04.008 · Cited by 180 · see citing works
Serum adiponectin levels in hypogonadal males: influence of testosterone replacement therapy
Lanfranco, F., Zitzmann, M., Simoni, M., & Nieschlag, E. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02007.x · Cited by 178 · see citing works
“The same authors also described in humans lower plasma adiponectin levels in male in comparison to female subjects (Nishizawa et al., 2002).”
BackgroundResultInfluentialHung, J., McQuillan, B., Thompson, P. L., & Beilby, J. P. (2008) · International Journal of Obesity · doi:10.1038/sj.ijo.0803793 · Cited by 179 · see citing works
Estrogens in adipose tissue physiology and obesity-related dysfunction
Kuryłowicz, A. (2023) · Biomedicines · doi:10.3390/biomedicines11030690 · Cited by 178 · see citing works
Sex differences in type 2 diabetes: focus on disease course and outcomes
Arnetz, L., Rajamand Ekberg, N., & Alvarsson, M. (2014) · Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy · doi:10.2147/dmso.s51301 · Cited by 175 · see citing works
Novel Interactions of Adiponectin with the Endocrine System and Inflammatory Parameters
Fernández‐Real, J. M., López‐Bermejo, A., Casamitjana, R., & Ricart, W. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021583 · Cited by 175 · see citing works
The regulation of adipose tissue health by estrogens
Steiner, B. M., & Berry, D. C. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.889923 · Cited by 171 · see citing works
Adiponectin before and after Weight Loss in Obese Children
Reinehr, T., Roth, C. L., Menke, T., & Andler, W. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031925 · Cited by 171 · see citing works
Smitka, K., & Maresova, D. (2015) · Prague Medical Report · doi:10.14712/23362936.2015.49 · Cited by 170 · see citing works
“However, Nishizawa et al. (2002) documented that testosterone leads to a reduction in plasma adiponectin in men.”
BackgroundGiorgino, F., Laviola, L., & Eriksson, J. W. (2005) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2004.01385.x · Cited by 230 · see citing works
Liu, Y., Schultz, J. J., & Brent, G. A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306120200 · Cited by 165 · see citing works
The relationship between gut and adipose hormones, and reproduction
Comninos, A. N., Jayasena, C. N., & Dhillo, W. S. (2013) · Human Reproduction Update · doi:10.1093/humupd/dmt033 · Cited by 167 · see citing works
“This latter effect is supported by the findings of higher plasma adiponectin levels in castrated mice while testosterone replacement reduces adiponectin levels in both sham-operated and these castrated mice (Nishizawa et al., 2002).”
InfluentialCardiovascular disease in the polycystic ovary syndrome: New insights and perspectives
Cussons, A. J., Stuckey, B. G. A., & Watts, G. F. (2005) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2005.10.007 · Cited by 167 · see citing works
Plasma adiponectin and insulin resistance in women with polycystic ovary syndrome
Ardawi, M. S. M., & Rouzi, A. A. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.11.077 · Cited by 165 · see citing works
Weigert, J., Obermeier, F., Neumeier, M., Wanninger, J., Filarsky, M., Bauer, S., Aslanidis, C., Rogler, G., Ott, C., Schäffler, A., et al. (2009) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21091 · Cited by 163 · see citing works
“Testosterone decreased plasma adiponectin in mice and metronidazole may lower testosterone levels in males and thereby may also contribute to elevated adiponectin concentrations in males.(46,49) Chemerin, however, was significantly elevated only in the serum of female UC patients treated with corticosteroids.”
BackgroundTestosterone Administration Suppresses Adiponectin Levels in Men
Page, S. T., Herbst, K. L., Amory, J. K., Coviello, A. D., Anawalt, B. D., Matsumoto, A. M., & Bremner, W. J. (2005) · Journal of Andrology · doi:10.1002/j.1939-4640.2005.tb02876.x · Cited by 162 · see citing works
Associations of adipokines with asthma, rhinoconjunctivitis, and eczema in German schoolchildren
Nagel, G., Köenig, W., Rapp, K., Wabitsch, M., Zoellner, I., & Weiland, S. K. (2008) · Pediatric Allergy and Immunology · doi:10.1111/j.1399-3038.2008.00740.x · Cited by 160 · see citing works
“4 lg/ml), but clearly lower adiponectin levels are seen in men than in women (13), which can be explained by hormonal status in adults (33).”
BackgroundSex differences in energy metabolism: natural selection, mechanisms and consequences
Mauvais‐Jarvis, F. (2023) · Nature Reviews Nephrology · doi:10.1038/s41581-023-00781-2 · Cited by 159 · see citing works
Sexual Dimorphism and Regulation of Resistin, Adiponectin, and Leptin Expression in the Mouse
Gui, Y., Silha, J. V., & Murphy, L. J. (2004) · Obesity Research · doi:10.1038/oby.2004.185 · Cited by 155 · see citing works
Serum Levels of the Adipokine Vaspin in Relation to Metabolic and Renal Parameters
Seeger, J., Ziegelmeier, M., Bachmann, A., Lössner, U., Kratzsch, J., Blüher, M., Stümvoll, M., & Faßhauer, M. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1853 · Cited by 153 · see citing works
Novel Expression and Direct Effects of Adiponectin in the Rat Testis
Caminos, J. E., Nogueiras, R., Gaytán, F., Pineda, R., González, C. R., Barreiro, M. L., Castano, J. P., Malagón, M. M., Pinilla, L., Toppari, J., et al. (2008) · Endocrinology · doi:10.1210/en.2007-1582 · Cited by 151 · see citing works
“than in males (38) and that androgens inhibit adiponectin secretion (39, 40).”
BackgroundRundek, T., Gardener, H. E., Xu, Q., Goldberg, R. B., Wright, C. B., Boden-Albala, B. M., Disla, N., Paik, M. C., Elkind, M. S. V., & Sacco, R. L. (2010) · Archives of Neurology · doi:10.1001/archneurol.2010.235 · Cited by 148 · see citing works
Adiponectin as a routine clinical biomarker
Kishida, K., Funahashi, T., & Shimomura, I. (2013) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2013.08.006 · Cited by 149 · see citing works
Self-citationEffects of Growth Hormone (GH) on Ghrelin, Leptin, and Adiponectin in GH-Deficient Patients
Engström, B. E., Burman, P., Holdstock, C., & Karlsson, F. A. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030713 · Cited by 146 · see citing works
Bullen, J. W., Blüher, S., Kelesidis, T., & Mantzoros, C. S. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00245.2006 · Cited by 145 · see citing works
“There are sex differences in plasma levels of adiponectin in rodents and in humans, with higher values in females than in males (9, 18, 27).”
BackgroundAdiponectin Levels and Genotype: A Potential Regulator of Life Span in Humans
Atzmon, G., Pollin, T. I., Crandall, J. P., Tanner, K., Schechter, C. B., Scherer, P. E., Rincón, M., Siegel, G., Katz, M., Lipton, R. B., et al. (2008) · The Journals of Gerontology Series A · doi:10.1093/gerona/63.5.447 · Cited by 145 · see citing works
Metabolic Actions of Adipocyte Hormones: Focus on Adiponectin
Ahima, R. S. (2006) · Obesity · doi:10.1038/oby.2006.276 · Cited by 145 · see citing works
“Moreover, women have higher proportions of high molecular weight adiponectin than men (24).”
BackgroundInflammation, adiponectin, obesity and cardiovascular risk
Mangge, H., Almer, G., Truschnig-Wilders, M., Schmidt, A., Gasser, R., & Fuchs, D. (2010) · Current Medicinal Chemistry · doi:10.2174/092986710794183006 · Cited by 142 · see citing works
Ageing and plasma adiponectin concentration in apparently healthy males and females
Adamczak, M., Rzepka, E., Chudek, J. T., & Więcek, A. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02182.x · Cited by 141 · see citing works
Kotani, Y., Yokota, I., Kitamura, S., Matsuda, J., Naito, E., & Kuroda, Y. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02041.x · Cited by 149 · see citing works
“It is possible that this difference originates in the difference in the testosterone level, which decreases the plasma adiponectin concentration through its effect on the secretion of adiponectin from adipocytes (Nishizawa et al., 2002).”
BackgroundAssociation of Hypoadiponectinemia With Smoking Habit in Men
Iwashima, Y., Katsuya, T., Ishikawa, K., Kida, I., Ohishi, M., Horio, T., Ouchi, N., Ohashi, K., Kihara, S., Funahashi, T., et al. (2005) · Hypertension · doi:10.1161/01.hyp.0000169444.05588.4c · Cited by 138 · see citing works
Self-citationDiamanti‐Kandarakis, E. (2006) · Endocrine · doi:10.1385/endo:30:1:13 · Cited by 136 · see citing works
Kanazawa, I., Yamaguchi, T., Tada, Y., Yamauchi, M., Yano, S., & Sugimoto, T. (2010) · Bone · doi:10.1016/j.bone.2010.12.020 · Cited by 133 · see citing works
“It has been shown that androgen decreased plasma adiponectin level via its effect on adipocyte in male mice [27].”
Background
- Authors
- Nishizawa, H., Shimomura, I., Kishida, K., Maeda, N., Kuriyama, H., Nagaretani, H., Matsuda, M., Kondo, H., Furuyama, N., Kihara, S., Nakamura, T., Tochino, Y., Funahashi, T., & Matsuzawa, Y.
- Affiliations
- The University of Osaka (JP)
- From the Department of Internal Medicine and Molecular Science, Graduate School of Medicine, Osaka University, Suita, Japan
- ORCID
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2002-09-01
- Volume
- 51
- Issue
- 9
- Pages
- 2734-2741
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- OpenAlex
- W2102610155
- Cited by
- 837
- References
- 44
- Citations by year
- 2026: 13 · 2025: 18 · 2024: 7 · 2023: 32 · 2022: 19 · 2021: 28 · 2020: 25 · 2019: 32 · 2018: 34 · 2017: 24 · 2016: 21 · 2015: 41 · 2014: 46 · 2013: 43 · 2012: 51
- FWCI
- 28.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Keywords
- adiponectin, androgens, testosterone, sex hormones, insulin sensitivity, insulin resistance, atherosclerosis, hypoadiponectinemia, ovariectomy, castration, adipocytes, 3T3-L1 adipocytes, sex differences, menopause
- MeSH terms
- Adult, Androgens, Animals, Female, Humans, Insulin, Male, Mice, Inbred C57BL, Mice, Inbred ICR, Middle Aged, Ovariectomy, Proteins, Sex Characteristics, Testosterone, 3T3 Cells, Adipocytes, Postmenopause, Intercellular Signaling Peptides and Proteins, Mice, Adiponectin
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