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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, 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]
In the citing paper
“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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“(45) found that plasma adiponectin concentrations were significantly higher in castrated mice than in sham-operated control mice and that testosterone treatment reduced plasma adiponectin concentrations in both castrated and sham-operated mice.”
BackgroundThe Relationship between Testosterone Deficiency and Men's Health
Tsujimura, A. (2013) · The World Journal of Men s Health · doi:10.5534/wjmh.2013.31.2.126 · Cited by 115
“Worryingly, the serum adiponectin level is inversely related to the testosterone level in rodents.(63) It was reported in a relatively young population that serum adiponectin levels in hypogonadal men are significantly higher than those in eugonadal men and that at 6 months after initiation of TRT, which increased the…”
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Baillargeon, J., & Rose, D. P. (2006) · International Journal of Oncology · doi:10.3892/ijo.28.3.737 · Cited by 110
“Nishizawa et al (95) found in a group of Japanese men that the plasma adiponectin concentration was 34% lower than in women; in parallel experimental studies they showed that castration produced a significant elevation in plasma adiponectin in mature male mice, while the administration of testosterone to both these an…”
BackgroundResultAdiponectin, Adiposity, and Insulin Resistance in Children and Adolescents
Punthakee, Z., DELVIN, E. E., O’Loughlin, J. L., Paradis, G., Levy, E. H., Platt, R. W., & Lambert, M. A. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2346 · Cited by 109
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ResultNandrolone Decanoate: Use, Abuse and Side Effects
Patanè, F. G., Liberto, A., Maglitto, A. N. M., Malandrino, P., Esposito, M., Amico, F., Cocimano, G., Rosi, G. L., Condorelli, D., Nunno, N. R. D., et al. (2020) · Medicina · doi:10.3390/medicina56110606 · Cited by 103
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Adiponectin accounts for gender differences in hepatocellular carcinoma incidence
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Self-citationProspective Study of Serum Adiponectin and Incident Metabolic Syndrome
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Androgen Deficiency Exacerbates High-Fat Diet-Induced Metabolic Alterations in Male Mice
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BackgroundResultAdiponectin circulating levels: A new emerging biomarker of cardiovascular risk
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BackgroundInfluentialSex-Related Differences Between Adiponectin and Insulin Resistance in Schoolchildren
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“In addition to putatitive direct actions, androgens may aggravate insulin resistance through indirect mechanisms, such as the suppression of adiponectin secretion, which is an adipokine known for its insulin-sensitizing properties [35] .”
BackgroundImmunological and Metabolic Causes of Infertility in Polycystic Ovary Syndrome
Kicińska, A. M., Maksym, R., Zabielska-Kaczorowska, M. A., Stachowska, A., & Babińska, A. (2023) · Biomedicines · doi:10.3390/biomedicines11061567 · Cited by 108
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“Experimental studies have proved that androgens have an inhibitory effect on adiponectin secretion (Bottner et al., 2004; Nishizawa et al., 2002).”
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“Indeed, plasma adiponectin levels decrease after androgen replacement in hypogonadal males (28) and experimental models ( 29 ).”
BackgroundAdiponectin Upregulates SHBG Production: Molecular Mechanisms and Potential Implications
Simó, R., Sáez‐López, C., Lecube, A., Hernández, C., Fort, J. M., & Selva, D. M. (2014) · Endocrinology · doi:10.1210/en.2014-1072 · Cited by 86
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Body composition, metabolic syndrome and type 2 diabetes in Klinefelter syndrome
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“Because African Americans enter puberty at an earlier age and because previous studies have found a relationship between increased testosterone and decreased adiponectin concentrations (37,38), we reasoned that higher testosterone among African-American males may account for the lower adiponectin previously reported i…”
BackgroundSex Hormones and Macronutrient Metabolism
Comitato, R., Saba, A., Turrini, A., Arganini, C., & Virgili, F. (2013) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2011.651177 · Cited by 86
“In mice, adiponectin levels dynamically change throughout the sexual maturation (Combs et al., 2003) and correlate with estrogens or testosterone levels (Nishizawa et al., 2002; Combs et al., 2003).”
BackgroundSerum Adiponectin Concentrations in Newborn Infants in Early Postnatal Life
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“The difference between the genders in adults may reflect an effect of the sex hormones (12,13) or other mediators that are inactive, subtle, or absent in newborns (8).”
BackgroundSiemińśka, L., Marek, B., Kos‐Kudła, B., Niedziolka, D., Kajdaniuk, D., Nowak, M., & Głogowska-Szeląg, J. (2004) · Journal of Endocrinological Investigation · doi:10.1007/bf03347474 · Cited by 85
O’Connor, A. S., Phelan, N., Tun, T. K., Boran, G. P., Gibney, J., & Roche, H. M. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-1557 · Cited by 81
Tokuda, F., Sando, Y., Matsui, H., Koike, H., & Yokoyama, T. (2008) · Internal Medicine · doi:10.2169/internalmedicine.47.1035 · Cited by 82
“On the other hand, several reports have suggested that age is one of the determinants of serum adiponectin (30, 31), Shand et al (32) suggested that the effect of age on serum adiponectin depends on lipid metabolism because older subjects have higher HDL-cholesterol levels than younger subjects.”
BackgroundAdiponectin Is a Negative Regulator of Bone Mineral and Bone Strength in Growing Mice
Ealey, K. N., Kaludjerovic, J., Archer, M. C., & Ward, W. E. (2008) · Experimental Biology and Medicine · doi:10.3181/0806-rm-192 · Cited by 81
“Adiponectin synthesis and secretion are dependent on many factors and its levels in serum are higher in women than in men (10).”
BackgroundOng, K. L., Li, M., Tso, A. W. K., Xu, A., Cherny, S. S., Sham, P. C., Tse, H., Lam, T. H., Cheung, B. M. Y., & Lam, K. S. L. (2010) · European Journal of Endocrinology · doi:10.1530/eje-10-0251 · Cited by 81
Adiponectin and the Control of Female Reproductive Functions
Palin, M., Bordignon, V., & Murphy, B. D. (2012) · Vitamins and hormones · doi:10.1016/b978-0-12-398313-8.00010-5 · Cited by 83
Akishita, M., Fukai, S., Hashimoto, M., Kameyama, Y. U., Nomura, K., Nakamura, T., Ogawa, S., Iijima, K., Eto, M., & Ouchi, Y. (2010) · Hypertension Research · doi:10.1038/hr.2010.43 · Cited by 79
Self-citationAdiponectin Synthesis, Secretion and Extravasation from Circulation to Interstitial Space
Rosa, S. C. D. S., Liu, M., & Sweeney, G. (2021) · Physiology · doi:10.1152/physiol.00031.2020 · Cited by 80
Plasma Adiponectin Levels and Blood Pressures in Nondiabetic Adolescent Females
Huang, K., Chen, C., Chuang, L., Ho, S., Tai, T., & Yang, W. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030158 · Cited by 78
Nohara, K., Waraich, R. S., Liu, S., Ferron, M., Waget, A., Meyers, M. S., Karsenty, G., Burcelin, R., & Mauvais-Jarvis, F. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00620.2012 · Cited by 77
“Similarly, males have reduced concentrations of serum adiponectin that are dependent on serum testosterone concentrations (39).”
BackgroundFatty acid–gene interactions, adipokines and obesity
Stryjecki, C., & Mutch, D. M. (2011) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2010.277 · Cited by 77
“association holds true in men, as adiponectin plasma levels differ significantly between men and women (Nishizawa et al., 2002).”
BackgroundMeasurement of salivary resistin, visfatin and adiponectin levels
Mamali, I., Roupas, N. D., Armeni, A. K., Theodoropoulou, A., Markou, K. B., & Georgopoulos, N. A. (2011) · Peptides · doi:10.1016/j.peptides.2011.11.007 · Cited by 77
Takahashi, K., Yamaguchi, S., Shimoyama, T., Seki, H., Miyokawa, K., Katsuta, H., Tanaka, T., Yoshimoto, K., Ohno, H., Nagamatsu, S., et al. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00131.2007 · Cited by 79
Effect of Drinking on Adiponectin in Healthy Men and Women
Imhof, A., Plamper, I., Maier, S., Trischler, G., & Köenig, W. (2009) · Diabetes Care · doi:10.2337/dc08-1723 · Cited by 77
“5 that sex hormones affect adiponectin concentrations and among healthy males effects of alcohol on sex hormones varied by drinking pattern and between beer and wine indicating a potential explanation for our findings (13-15).”
Obesity, Inflammation, and Lung Injury (OILI): The Good
Wang, C. (2014) · Mediators of Inflammation · doi:10.1155/2014/978463 · Cited by 78
Kotronen, A., Yki‐Järvinen, H., Aminoff, A., Bergholm, R., Pietiläinen, K. H., Westerbacka, J., Talmud, P. J., Humphries, S. E., Hamsten, A., Isomaa, B., et al. (2009) · European Journal of Endocrinology · doi:10.1530/eje-08-0900 · Cited by 77
Sex-dependent depot differences in adipose tissue development and function; role of sex steroids
Lee, M.-J., & Fried, S. K. (2017) · Journal of Obesity & Metabolic Syndrome · doi:10.7570/jomes.2017.26.3.172 · Cited by 72
Bidulescu, A., Liu, J., Hickson, D. A., Hairston, K. G., Fox, E. R., Arnett, D. K., Sumner, A. E., Taylor, H. A., & Gibbons, G. H. (2013) · BMC Cardiovascular Disorders · doi:10.1186/1471-2261-13-9 · Cited by 75
“In addition, a series of studies showed that androgens reduce plasma adiponectin [48], providing insights into the gender differences of the association between VAT and adiponectin.”
BackgroundUpdated survey of the steroid-converting enzymes in human adipose tissues
Tchernof, A., Mansour, M. F., Pelletier, M., Boulet, M.-M., Nadeau, M., & Luu-The, V. (2015) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.11.011 · Cited by 73
Nakagawa, Y., Kishida, K., Kihara, S., Sonoda, M., Hirata, A., Yasui, A., Nishizawa, H., Nakamura, T., Yoshida, R., Shimomura, I., et al. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00709.2007 · Cited by 73
“The present study demonstrated that exposure to 3%, 5%, 8%, 9%, or 10% hypoxia resulted in suppression of adiponectin mRNA expressions, similar to 1% O2 hypoxia in previous studies (3, 8, 41, 45), and 15% O2 hypoxia suppressed adiponectin production posttranscriptionally, in agreement with a previous report on the reg…”
BackgroundMethodResultInfluentialSelf-citationTranslational value of animal models of obesity—Focus on dogs and cats
Osto, M., & Lutz, T. A. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2015.03.036 · Cited by 79
“…difference may also not be directly attributable to sex hormones, since the levels of testosterone which is known to directly decrease adiponectin levels in humans and rodents (Combs et al., 2003; Nishizawa et al., 2002), are expected to be minimal in neutered male cats (Bjornvad et al., 2014).”
BackgroundMetabolic hormones are integral regulators of female reproductive health and function
Athar, F., Karmani, M., & Templeman, N. M. (2023) · Bioscience Reports · doi:10.1042/bsr20231916 · Cited by 82
“Testosterone also reduces adiponectin secretion [547], which may contribute toward the lower levels in men compared with women [543,544].”
BackgroundHan, L., Wang, Y., Li, J. V., Zhang, X., Bian, C., Wang, H., Du, S., & Suo, L. (2014) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201400088 · Cited by 72
“Greater visceral fat accumulation and lower plasma adiponectin concentrations in men than women contribute to gender differences in insulin sensitivity and higher vulnerability to cardiovascular diseases [31].”
BackgroundDisturbed secretion of mutant adiponectin associated with the metabolic syndrome
Kishida, K., Nagaretani, H., Kondo, H., Kobayashi, H., Tanaka, S., Maeda, N., Nagasawa, A., Hibuse, T., Ohashi, K., Kumada, M., et al. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)00940-9 · Cited by 72
Self-citationKoncarevic, A., Cornwall-Brady, M., Pullen, A., Davies, M., Sako, D., Liu, J., Kumar, R., Tomkinson, K., Baker, T., Umiker, B., et al. (2010) · Endocrinology · doi:10.1210/en.2010-0134 · Cited by 71
Impact of age on leptin and adiponectin independent of adiposity
Schautz, B., Later, W., Heller, M., Peters, A., Müller, M. J., & Bosy‐Westphal, A. (2012) · British Journal Of Nutrition · doi:10.1017/s0007114511005605 · Cited by 73
“to inhibit adiponectin production((38,39)), might have a higher impact on adiponectin than on body fat or fat distribution in women.”
BackgroundHuang, K., Cheng, W., Yen, R., Tsai, K., Tai, T., & Yang, W. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02081.x · Cited by 71
Hypogonadism alters cecal and fecal microbiota in male mice
Harada, N., Hanaoka, R., Hanada, K., Izawa, T., Inui, H., & Yamaji, R. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1239680 · Cited by 67
Capllonch-Amer, G., Lladó, I., Proenza, A. M., García-Palmer, F. J., & Gianotti, M. (2014) · Journal of Molecular Endocrinology · doi:10.1530/jme-13-0201 · Cited by 67
“Indeed, testosterone exerts direct effects on adiponectin secretion, as serum total and high molecular weight adiponectin concentrations are high in castrated rodents and hypogonadal men, and decrease after testosterone therapy (Nishizawa et al. 2002, Xu et al. 2005).”
BackgroundRuscica, M., Baragetti, A., Catapano, A. L., & Norata, G. D. (2016) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2016.12.005 · Cited by 67
Adiponectin: A multitasking player in the field of liver diseases
Silva, T. E., Colombo, G., & Schiavon, L. D. L. (2014) · Diabetes & Metabolism · doi:10.1016/j.diabet.2013.11.004 · Cited by 68
Metadata
- 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 › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Physiology (medical) › 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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