A Reappraisal of Testosterone’s Binding in Circulation: Physiological and Clinical Implications
Open accessAbstract
In the circulation, testosterone and other sex hormones are bound to binding proteins, which play an important role in regulating their transport, distribution, metabolism, and biological activity. According to the free hormone hypothesis, which has been debated extensively, only the unbound or free fraction is biologically active in target tissues. Consequently, accurate determination of the partitioning of testosterone between bound and free fractions is central to our understanding of how its delivery to the target tissues and biological activity are regulated and consequently to the diagnosis and treatment of androgen disorders in men and women. Here, we present a historical perspective on the evolution of our understanding of the binding of testosterone to circulating binding proteins. On the basis of an appraisal of the literature as well as experimental data, we show that the assumptions of stoichiometry, binding dynamics, and the affinity of the prevailing models of testosterone binding to sex hormone-binding globulin and human serum albumin are not supported by published experimental data and are most likely inaccurate. This review offers some guiding principles for the application of free testosterone measurements in the diagnosis and treatment of patients with androgen disorders. The growing number of testosterone prescriptions and widely recognized problems with the direct measurement as well as the computation of free testosterone concentrations render this critical review timely and clinically relevant.
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Evidence that 'free' testosterone is the biologically active testosterone fraction is lacking.
“as evidence that ' free ' testosterone is the biologically active testosterone fraction is lacking 9 (Expert Opinion).”
From Global Consensus Position Statement on the Use of Testosterone Therapy for Women (2019) · cites this paper as [9]
In “What is the Biologically Active Fraction of Circulating Testosterone?” (page unavailable), the paper explicitly describes experimental support for the free hormone hypothesis and clinical findings that support it. It treats the hypothesis as debated, but does not say evidence for it is lacking. (LLM, conf=0.88)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredAll free T calculation models have respective strengths and intrinsic limitations.
“All these models have respective strengths and intrinsic limitations, as described in an extensive review [5].”
From Role of sex hormone-binding globulin in the free hormone hypothesis and the relevance of free testosterone in androgen physiology (2022) · cites this paper as [5]
Variability and assumptions in binding affinity, stoichiometry, and allosteric interaction produce different quantities of free T in different models.
“Second, concerning the interaction between SHBG and T, variability and assumptions in terms of binding affinity, stoichiometry and allosteric interaction produce different quantities of free T in different models [5, 208].”
From Role of sex hormone-binding globulin in the free hormone hypothesis and the relevance of free testosterone in androgen physiology (2022) · cites this paper as [5]
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Sorted by citations
Testosterone Therapy in Men With Hypogonadism: An Endocrine Society Clinical Practice Guideline.
Bhasin, S., Brito, J. P., Cunningham, G. R., Hayes, F. J., Hodis, H. N., Matsumoto, A. M., Snyder, P. J., Swerdloff, R. S., Wu, F. C., & Yialamas, M. A. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-00229 · Cited by 1,736 · see citing works
Self-citationMartin, K. A., Anderson, R. R., Chang, R. J., Ehrmann, D. A., Lobo, R. A., Murad, M. H., Pugeat, M. M., & Rosenfield, R. L. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-00241 · Cited by 339 · see citing works
Paediatric and adult-onset male hypogonadism
Salonia, A., Rastrelli, G., Hackett, G., Seminara, S. B., Huhtaniemi, I. T., Rey, R. A., Hellstrom, W. J. G., Palmert, M. R., Corona, G., Dohle, G. R., et al. (2019) · Nature Reviews Disease Primers · doi:10.1038/s41572-019-0087-y · Cited by 286 · see citing works
Hormonal Treatments for Major Depressive Disorder: State of the Art
Dwyer, J. B., Aftab, A., Radhakrishnan, R., Widge, A., Rodriguez, C. I., Carpenter, L. L., Nemeroff, C. B., McDonald, W. M., Kalin, N. H., & APA Council of Research Task Force on Novel Biomarkers and Treatments (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.19080848 · Cited by 252 · see citing works
Xing, C., Zhang, J., Zhao, H., & He, B. (2022) · International Journal of Women's Health · doi:10.2147/ijwh.s344542 · Cited by 118 · see citing works
Global Consensus Position Statement on the Use of Testosterone Therapy for Women
Davis, S. R., Baber, R., Panay, N., Bitzer, J., Cerdas Perez, S., Islam, R. M., Kaunitz, A. M., Kingsberg, S. A., Lambrinoudaki, I., Liu, J., et al. (2019) · Climacteric · doi:10.1080/13697137.2019.1637079 · Cited by 113 · see citing works
“h Current research into testosterone physiology and clinical effects should mainly focus on measuring total testosterone as the main biomarker rather than “free” testosterone, as evidence that ‘free testosterone’ is the biologically active testosterone fraction is lacking [9] (Expert Opinion).”
BackgroundNarinx, N., David, K., Walravens, J., Vermeersch, P., Claessens, F., Fiers, T., Lapauw, B., Antonio, L., & Vanderschueren, D. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04562-1 · Cited by 96 · see citing works
Association between low testosterone levels and sarcopenia in cirrhosis: A cross-sectional study
Moctezuma-Velázquez, C., Low, G., Mourtzakis, M., Ma, M., Burak, K. W., Tandon, P., & Montano-Loza, A. J. (2018) · Annals of Hepatology · doi:10.5604/01.3001.0012.0930 · Cited by 70 · see citing works
Liu, P. Y. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2019-00683 · Cited by 55 · see citing works
Functional hypogonadism among patients with obesity, diabetes, and metabolic syndrome
Louters, M., Pearlman, M., Solsrud, E., & Pearlman, A. (2022) · International Journal of Impotence Research · doi:10.1038/s41443-021-00496-7 · Cited by 32 · see citing works
Shen, C., Lu, J., Xu, Z., Xu, Y., & Yang, Y. (2020) · BMJ Open · doi:10.1136/bmjopen-2020-041384 · Cited by 28 · see citing works
Ageing male (part I): Pathophysiology and diagnosis of functional hypogonadism
Huhtaniemi, I. T., & Wu, F. C. W. (2022) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2022.101622 · Cited by 31 · see citing works
Self-citationVenkatesh, V. S., Grossmann, M., Zajac, J. D., & Davey, R. A. (2022) · Obesity Reviews · doi:10.1111/obr.13429 · Cited by 22 · see citing works
Telgenkamp, I., Kusters, Y. H. A. M., Schalkwijk, C. G., Houben, A. J. H. M., Kooi, M. E., Lindeboom, L., Bons, J. A. P., Schaper, N. C., Joris, P. J., Plat, J., et al. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-02378 · Cited by 18 · see citing works
Rao, A., Clayton, P., & Briskey, D. (2023) · Frontiers in Sports and Active Living · doi:10.3389/fspor.2023.1207013 · Cited by 2 · see citing works
- Authors
- Goldman, A. L., Bhasin, S., Wu, F. C. W., Krishna, M., Matsumoto, A. M., & Jasuja, R.
- Affiliations
- Brigham and Women's Hospital (US)
- University of Manchester (GB)
- University of Washington (US)
- Venue
- Endocrine Reviews
- Publisher
- The Endocrine Society
- Published
- 2017-06-29
- Volume
- 38
- Issue
- 4
- Pages
- 302-324
- ISSN
- 0163-769X (ISSN-L)
- 1945-7189
- PMC
- PMC6287254
- OpenAlex
- W2731671395
- Cited by
- 414
- References
- 226
- Citations by year
- 2026: 42 · 2025: 74 · 2024: 54 · 2023: 51 · 2022: 57 · 2021: 43 · 2020: 32 · 2019: 31 · 2018: 25 · 2017: 2 · 2016: 2
- FWCI
- 3.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Endocrine Reviews (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eli Lilly and Company
- Brigham and Women's Hospital
- Regeneron Pharmaceuticals
- Mereo BioPharma
- National Institutes of Health (5p30ag031679-15)
- National Institute on Aging (R01AG037193, P30-AG031679, R43AG045011)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Interaction Studies and Fluorescence Analysis
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Keywords
- testosterone, sex hormone-binding globulin, human serum albumin, free testosterone, free hormone hypothesis, binding dynamics
- MeSH terms
- Serum Albumin, Human, Humans, Sex Hormone-Binding Globulin, Testosterone, Transcortin
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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