Plasma steroid-binding proteins: primary gatekeepers of steroid hormone action

Hammond, Geoffrey L

doi:10.1530/joe-16-0070

Cited by 356Protein Interaction Studies and Fluorescence AnalysisEstrogen and related hormone effectsHormonal and reproductive studies

Plasma steroid-binding proteins: primary gatekeepers of steroid hormone action

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Hammond, Geoffrey L·2016·Journal of Endocrinology

DOI 10.1530/joe-16-0070PMC PMC5064763

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Abstract

Biologically active steroids are transported in the blood by albumin, sex hormone-binding globulin (SHBG), and corticosteroid-binding globulin (CBG). These plasma proteins also regulate the non-protein-bound or 'free' fractions of circulating steroid hormones that are considered to be biologically active; as such, they can be viewed as the 'primary gatekeepers of steroid action'. Albumin binds steroids with limited specificity and low affinity, but its high concentration in blood buffers major fluctuations in steroid concentrations and their free fractions. By contrast, SHBG and CBG play much more dynamic roles in controlling steroid access to target tissues and cells. They bind steroids with high (~nM) affinity and specificity, with SHBG binding androgens and estrogens and CBG binding glucocorticoids and progesterone. Both are glycoproteins that are structurally unrelated, and they function in different ways that extend beyond their transportation or buffering functions in the blood. Plasma SHBG and CBG production by the liver varies during development and different physiological or pathophysiological conditions, and abnormalities in the plasma levels of SHBG and CBG or their abilities to bind steroids are associated with a variety of pathologies. Understanding how the unique structures of SHBG and CBG determine their specialized functions, how changes in their plasma levels are controlled, and how they function outside the blood circulation provides insight into how they control the freedom of steroids to act in health and disease.

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Albumin binds all unconjugated steroids with low affinities (micromolar ranges), but makes a significant contribution to steroid binding due to its high abundance.
“Although albumin binds all unconjugated steroids with low affinities (micromolar ranges), it makes a significant contribution to steroid binding due to its high abundance [45,287].”
From Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review (2019) · cites this paper as [287]
SHBG binds sex steroids (including active androgens and estrogens) with high affinity (nanomolar ranges) and specificity.
“SHBG binds sex steroids (including active androgens and estrogens) with high affinity (nanomolar ranges) and specificity [[285], [286], [287]].”
From Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review (2019) · cites this paper as [287]
Like with androgens, the majority of unconjugated estrogen circulates bound to SHBG with high affinity and albumin with low affinity.
“Like with androgens, the majority of unconjugated estrogen circulates bound to SHBG with high affinity and albumin with low affinity [[285], [286], [287]].”
From Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review (2019) · cites this paper as [287]
During the second and third trimesters of pregnancy placental trophoblasts produce large amounts of progesterone, which displaces glucocorticoids from CBG.
“During the second and third trimesters of pregnancy placental trophoblasts produce large amounts of progesterone, which displaces glucocorticoids from CBG [287,335].”
From Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review (2019) · cites this paper as [287]
Abnormal levels of SHBG and mutations altering the affinity for its ligands are associated with androgen excess and a PCOS phenotype, but have also been implicated in the pathogenesis of cancer and metabolic dysfunction.
“Abnormal levels of SHBG and mutations altering the affinity for its ligands are associated with androgen excess and a PCOS phenotype, but have also been implicated in the pathogenesis of cancer and metabolic dysfunction (Hammond, 2016, Hogeveen et al., 2002).”
From Intracrine androgen biosynthesis, metabolism and action revisited (2018) · cites this paper as Hammond, 2016

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Bartalena, L., Hammond, G. L., Farsetti, A., et al. (1993) · Endocrinology · doi:10.1210/endo.133.1.8391424 · Cited by 59 · see citing works
Self-citation
Spatial and temporal distribution of corticosteroid-binding globulin and its messenger ribonucleic acid in embryonic and fetal mice
Scrocchi, L. A., Orava, M., Smith, C. S., Han, V. K. M., & Hammond, G. L. (1993) · Endocrinology · doi:10.1210/endo.132.2.7916682 · Cited by 59 · see citing works
Self-citation
Corticosteroid-binding globulin biosynthesis in the mouse liver and kidney during postnatal development
Scrocchi, L. A., Hearn, S., Han, V. K. M., & Hammond, G. L. (1993) · Endocrinology · doi:10.1210/endo.132.2.8425503 · Cited by 55 · see citing works
Self-citation
Human Variant Sex Hormone-Binding Globulin (SHBG) with an Additional Carbohydrate Chain Has a Reduced Clearance Rate in Rabbit
Cousin, P. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.1.235 · Cited by 55 · see citing works
Organization of the Human Corticosteroid Binding Globulin Gene and Analysis of Its 5′-Flanking Region
Underhill, D. A., & Hammond, G. L. (1989) · Molecular Endocrinology · doi:10.1210/mend-3-9-1448 · Cited by 52 · see citing works
Self-citation
Sex hormones, sex hormone binding globulin, and vertebral fractures in older men
Cawthon, P. M., Schousboe, J. T., Harrison, S. L., Ensrud, K. E., Black, D. M., Cauley, J. A., Cummings, S. R., LeBlanc, E. S., Laughlin, G. A., Nielson, C. M., et al. (2016) · Bone · doi:10.1016/j.bone.2016.01.009 · Cited by 51 · see citing works
Novel Corticosteroid-Binding Globulin Variant That Lacks Steroid Binding Activity
Perogamvros, I., Underhill, C., Henley, D., Hadfield, K. D., Newman, W. G., Ray, D. W., Lightman, S. L., Hammond, G. L., & Trainer, P. J. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0746 · Cited by 50 · see citing works
Self-citation
Corticosteroid-Binding Globulin during Inflammation and Burn Injury: Nutritional Modulation and Clinical Implications
Garrel, D. R. (2008) · Hormone Research · doi:10.1159/000184796 · Cited by 49 · see citing works
Sex Hormone Binding Globulin Deficiency Due to a Homozygous Missense Mutation
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Receptor-Mediated Endocytosis of an Extracellular Steroid-Binding Protein (TeBG) in MCF-7 Human Breast Cancer Cells*
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Association of Breast Cancer Risk with a Common Functional Polymorphism (Asp327Asn) in the Sex Hormone–Binding Globulin Gene
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A Leu → His substitution at residue 93 in human corticosteroid binding globulin results in reduced affinity for cortisol
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Self-citation
Naturally Occurring Mutants Inform SHBG Structure and Function
Wu, T.-S., & Hammond, G. L. (2014) · Molecular Endocrinology · doi:10.1210/me.2014-1058 · Cited by 40 · see citing works
Self-citation
Residues in the Human Corticosteroid-binding Globulin Reactive Center Loop That Influence Steroid Binding before and after Elastase Cleavage
Lin, H., Underhill, C., Gardill, B. R., Muller, Y. A., & Hammond, G. L. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807376200 · Cited by 39 · see citing works
Self-citation
Naturally Occurring Mutations of Human Corticosteroid-Binding Globulin
Simard, M., Hill, L. A., Lewis, J. G., & Hammond, G. L. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-3130 · Cited by 38 · see citing works
Self-citation
Genotype–phenotype associations in understanding the role of corticosteroid-binding globulin in health and disease animal models
Moisan, M. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.07.017 · Cited by 37 · see citing works
Corticosteroid-binding globulin (CBG) production by hepatic and extra-hepatic sites in the ovine fetus; effects of CBG on glucocorticoid negative feedback on pituitary cells in vitro
Berdusco, E. T. M., Yang, K., Hammond, G. L., & Challis, J. R. G. (1995) · Journal of Endocrinology · doi:10.1677/joe.0.1460121 · Cited by 37 · see citing works
Self-citation
Corticosteroid-binding globulin Status at the fetomaternal interface during human term Pregnancy1
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Sex hormone-binding globulin polymorphisms in familial and sporadic breast cancer
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The human corticosteroid binding globulin gene is located on chromosome 14q31?q32.1 near two other serine protease inhibitor genes
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Self-citation
Pseudomonas Aeruginosa Elastase Disrupts the Cortisol-Binding Activity of Corticosteroid-Binding Globulin
Simard, M., Hill, L. A., Underhill, C., Keller, B. O., Villanueva, I., Hancock, R. E. W., & Hammond, G. L. (2014) · Endocrinology · doi:10.1210/en.2014-1055 · Cited by 34 · see citing works
Self-citation
Corticosterone binding globulin: an acute phase “negative” protein in the rat
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The reactive centre loop of corticosteroid-binding globulin (CBG) is a protease target for cortisol release
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Electron spin resonance study of human transcortin thiol groups and binding site topography
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Impact of Corticosteroid-Binding Globulin Deficiency on Pregnancy and Neonatal Sex
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Self-citation
PPARγ Variant Influences Angiographic Outcome and 10-Year Cardiovascular Risk in Male Symptomatic Coronary Artery Disease Patients
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Hormonal regulation of corticosteroid-binding globulin biosynthesis in the male rat
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Human Sex Hormone-Binding Globulin Gene Expression in Transgenic Mice
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Identification of a Locus on Distal Mouse Chromosome 12 That Controls Resistance to Tumor Necrosis Factor-Induced Lethal Shock
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Self-citation
Clinical Manifestations of Highly Prevalent Corticosteroid-Binding Globulin Mutations in a Village in Southern Italy
Cizza, G., Bernardi, L., Smirne, N., et al. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1321 · Cited by 30 · see citing works
CBG Santiago: A Novel CBG Mutation
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Effect of pioglitazone on testosterone in eugonadal men with type 2 diabetes mellitus: a randomized double‐blind placebo‐controlled study
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High Frequency ofSERPINA6Polymorphisms that Reduce Plasma Corticosteroid-Binding Globulin Activity in Chinese Subjects
Lin, H., Underhill, C., Lei, J., et al. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-3141 · Cited by 28 · see citing works
Two Different Corticosteroid-Binding Globulin Variants that Lack Cortisol-Binding Activity in a Greek Woman
Hill, L. A., Vassiliadi, D.-A., Simard, M., Pavlaki, A., Perogamvros, I., Hadjidakis, D., & Hammond, G. L. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2467 · Cited by 26 · see citing works
Self-citation
Total and unbound Cortisol‐, progesterone‐, oestrone‐ and transcortin‐binding activities in sera from patients with myocardial infarction: evidence for differential responses of good and bad prognostic cases
Zouaghi, H., Savu, L., Guérot, C., et al. (1985) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1985.tb00286.x · Cited by 25 · see citing works
Three calculations of free cortisol versus measured values in the critically ill
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Colony-Specific Differences in Endocrine and Immune Responses to an Inflammatory Challenge in Female Sprague Dawley Rats.
Bodnar, T. S., Hill, L., Taves, M. D., Yu, W. K., Soma, K., Hammond, G. L., & Weinberg, J. (2015) · Endocrinology · doi:10.1210/en.2015-1497 · Cited by 21 · see citing works
Self-citation
SEX-HORMONE-BINDING GLOBULIN DEFICIENCY
Ahrentsen, O. D., Jensen, H. K., & Johnsen, S. (1982) · The Lancet · doi:10.1016/s0140-6736(82)90560-8 · Cited by 20 · see citing works
The Pro12Ala Polymorphism of the PPAR Gamma 2 Gene Influences Sex Hormone-Binding Globulin Level and its Relationship to the Development of the Metabolic Syndrome in Young Finnish Men
Mousavinasab, F., Tähtinen, T., Jokelainen, J. J., Koskela, P. U., Vanhala, M. J., Oikarinen, J. A., Laakso, M., & Keinanen-Kiukaanniemi, S. M. (2006) · Endocrine · doi:10.1385/endo:30:2:185 · Cited by 18 · see citing works
Selective delivery of sex steroid hormones to tissues by albumin and by sex hormone-binding globulin.
Pardridge, W. M. (1988) · PubMed · Cited by 18 · see citing works
Interleukin-6 inhibits corticosteroid-binding globulin synthesis by human hepatoblastoma-derived (Hep G2) cells
Bartalena, L. (1993) · Endocrinology · doi:10.1210/en.133.1.291 · Cited by 18 · see citing works
Effect of burn injury on corticosteroid‐binding globulin levels in plasma and wound fluid
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Developmental regulation of corticosteroid-binding globulin biosynthesis in the baboon fetus.
Pepe, G. J., Jury, H. H., Hammond, G. L., et al. (1996) · Endocrinology · doi:10.1210/endo.137.8.8754758 · Cited by 12 · see citing works
Self-citation
Response of transcortin and α2u-globulin to turpentine-induced inflammation in the rat: influence of corticosteroids and prolactin
Faict, D., Vandoren, G., MOOR, P. D., et al. (1983) · Journal of Endocrinology · doi:10.1677/joe.0.0990465 · Cited by 11 · see citing works
Corticosteroid-Binding Globulin in Preterm Infants in an Intensive Care Unit
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Human sex hormone–binding globulin variants associated with hyperandrogenism and ovarian dysfunction
Hogeveen, K. N., Cousin, P., PUGEAT, M. M., Dewailly, D., Soudan, B., & Hammond, G. L. (2002) · Journal of Clinical Investigation · doi:10.1172/jci200214060 · Cited by 7 · see citing works
Self-citation
Corticosteroid-Binding Globulin (CBG)
Westphal, U. (1986) · Monographs on endocrinology · doi:10.1007/978-3-642-82486-9_5 · Cited by 5 · see citing works
Developmental regulation of corticosteroid-binding globulin biosynthesis in the baboon fetus
Pepe, G. J. (1996) · Endocrinology · doi:10.1210/en.137.8.3323 · Cited by 4 · see citing works
[The treatment of hirsutism].
Sn, K., & Eg, I. (1995) · PubMed · Cited by 1 · see citing works

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Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review
Schiffer, L., Barnard, L., Baranowski, E. S., Gilligan, L. C., Taylor, A. E., Arlt, W., Shackleton, C. H. L., & Storbeck, K.-H. (2019) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2019.105439 · Cited by 450 · see citing works
“Progesterone primarily circulates bound to CBG.”
Influential
A Reappraisal of Testosterone’s Binding in Circulation: Physiological and Clinical Implications
Goldman, A. L., Bhasin, S., Wu, F. C. W., Krishna, M., Matsumoto, A. M., & Jasuja, R. (2017) · Endocrine Reviews · doi:10.1210/er.2017-00025 · Cited by 414 · 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
Intracrine androgen biosynthesis, metabolism and action revisited
Schiffer, L., Arlt, W., & Storbeck, K.-H. (2018) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.08.016 · Cited by 217 · see citing works
“In contrast, SHBG binds sex steroids (including active androgens, oestrogens, precursors and metabolites (Avvakumov et al., 2010; Cherkasov et al., 2008; Dunn et al., 1981; Grishkovskaya et al., 2002)) with high specificity and affinity (nanomolar ranges) (reviewed in (Hammond, 2016)).”
Effect of Sex Hormone-Binding Globulin on Polycystic Ovary Syndrome: Mechanisms, Manifestations, Genetics, and Treatment
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
Role of sex hormone-binding globulin in the free hormone hypothesis and the relevance of free testosterone in androgen physiology
Narinx, 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
Methylome-wide association findings for major depressive disorder overlap in blood and brain and replicate in independent brain samples
Aberg, K. A., Dean, B., Shabalin, A. A., Chan, R. F., Han, L. K. M., Zhao, M., van Grootheest, G., Xie, L. Y., Milaneschi, Y., Clark, S. L., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-018-0247-6 · Cited by 73 · see citing works
The HERITAGE family study: a review of the effects of exercise training on cardiometabolic health, with insights into molecular transducers
SARZYNSKI, M. A., RICE, T. K., DESPRÉS, J.-P., PÉRUSSE, L., TREMBLAY, A., STANFORTH, P. R., TCHERNOF, A., BARBER, J. L., FALCIANI, F., CLISH, C., et al. (2022) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002859 · Cited by 62 · see citing works
Hormones, Metabolism and the Benefits of Exercise
(2017) · Research and Perspectives in Endocrine Interactions · doi:10.1007/978-3-319-72790-5 · Cited by 44 · see citing works
Arrival cortisol measurement in veal calves and its association with body weight, protein fractions, animal health and performance
Masmeijer, C., Deprez, P., van Leenen, K., De Cremer, L., Cox, E., Devriendt, B., & Pardon, B. (2021) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2020.105251 · Cited by 33 · see citing works
The Prenatal Hormone Milieu in Autism Spectrum Disorder
Worsham, W., Dalton, S., & Bilder, D. A. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.655438 · Cited by 29 · 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
Storage stability of five steroids and in dried blood spots for newborn screening and retrospective diagnosis of congenital adrenal hyperplasia
Grecsó, N., Zádori, A., Szécsi, I., Baráth, Á., Galla, Z., Bereczki, C., & Monostori, P. (2020) · PLoS ONE · doi:10.1371/journal.pone.0233724 · Cited by 26 · see citing works

Symposium: Binding of upids by proteins conducted Ly The American Oil Chemists舗 Society at its 37tn pall meeting, Minneapolis, Minnesota September 30舑Octoter 2, 1963
Therriault, D. H., Wheeler, D. H., & Chairman, P. (1964) · Journal of the American Oil Chemists Society · doi:10.1007/bf02670028 · Cited by 36 · see citing works
Sex hormone-binding globulin and corticosteroid-binding globulin mRNA levels in infertile women with luteal phase deficiency
Misao, R., Nakanishi, Y., Fujimoto, J., et al. (1995) · Gynecological Endocrinology · doi:10.3109/09513599509160446 · Cited by 7 · see citing works
[Steroid-binding protein levels in breast cancer patients].
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Serum Steroid Binding Proteins and the Bioavailability of Estradiol in Relation to Breast Diseases2
Langley, M. S., Hammond, G. L., Bardsley, A., et al. (1985) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/75.5.823 · Cited by 63 · see citing works
Self-citation
Levels of sex hormone-binding globulin and corticosteroid-binding globulin mRNAs in corpus luteum of human subjects: Correlation with serum steroid hormone levels
Misao, R., Nakanishi, Y., Fujimoto, J., Iwagaki, S., & Tamaya, T. (1999) · Gynecological Endocrinology · doi:10.3109/09513599909167537 · Cited by 11 · see citing works

Authors: Hammond, G. L.
Affiliations: University of British Columbia (CA)
Corresponding author: Hammond, Geoffrey L
ORCID: Hammond, Geoffrey L
Venue: Journal of Endocrinology
Publisher: Bioscientifica
Published: 2016-07
Volume: 230
Issue: 1
Pages: R13-R25
ISSN: 0022-0795 (ISSN-L)
1479-6805
DOI: 10.1530/joe-16-0070
PMC: PMC5064763
OpenAlex: W2343578093
Cited by: 356
References: 125
Citations by year: 2026: 40 · 2025: 34 · 2024: 32 · 2023: 45 · 2022: 36 · 2021: 44 · 2020: 37 · 2019: 29 · 2018: 31 · 2017: 20 · 2016: 8
FWCI: 2.62
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/3.0/ (unspecified)
Locations: Journal of Endocrinology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: Society for Endocrinology
Canada Research Chairs
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Interaction Studies and Fluorescence Analysis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
Keywords: sex hormone-binding globulin, corticosteroid-binding globulin, albumin, steroid hormone transport, steroid binding affinity, glucocorticoids, androgens, estrogen, progesterone, steroid hormone action
MeSH terms: Animals, Estradiol, Glucocorticoids, Humans, Progesterone, Serum Albumin, Sex Hormone-Binding Globulin, Testosterone, Transcortin

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Plasma steroid-binding proteins: primary gatekeepers of steroid hormone action

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