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Sex Steroid Actions in Male Bone
Open accessAbstract
Sex steroids are chief regulators of gender differences in the skeleton, and male gender is one of the strongest protective factors against osteoporotic fractures.This advantage in bone strength relies mainly on greater cortical bone expansion during pubertal peak bone mass acquisition and superior skeletal maintenance during aging.During both these phases, estrogens acting via estrogen receptor-␣ in osteoblast lineage cells are crucial for male cortical and trabecular bone, as evident from conditional genetic mouse models, epidemiological studies, rare genetic conditions, genome-wide meta-analyses, and recent interventional trials.Genetic mouse models have also demonstrated a direct role for androgens independent of aromatization on trabecular bone via the androgen receptor in osteoblasts and osteocytes, although the target cell for their key effects on periosteal bone formation remains elusive.Low serum estradiol predicts incident fractures, but the highest risk occurs in men with additionally low T and high SHBG.Still, the possible clinical utility of serum sex steroids for fracture prediction is unknown.It is likely that sex steroid actions on male bone metabolism rely also on extraskeletal mechanisms and cross talk with other signaling pathways.We propose that estrogens influence fracture risk in aging men via direct effects on bone, whereas androgens exert an additional antifracture effect mainly via extraskeletal parameters such as muscle mass and propensity to fall.Given the demographic trends of increased longevity and consequent rise of osteoporosis, an increased understanding of how sex steroids influence male bone health remains a high research priority.(Endocrine Reviews 35: 906 -960, 2014) I. Introduction II.Sex Steroid Physiology in Relation to Bone A. Circulating sex steroids and SHBG B. Local sex steroid metabolism in bone tissue C. Classical androgen and estrogen receptor signaling D. Ligand-independent and nongenomic actions E. Rodent models in the study of sex steroids and bone: a critical appraisal III.Structural Basis of Male Bone Strength A. Favorable cortical bone size and trabecular microstructure in young adult men B. Better maintenance of trabecular and cortical bone structure in men across the lifespan IV.Regulation of Skeletal Sexual Dimorphism A. Estrogen receptor ␣: crucial for peak bone mass B. Estrogen receptor  C. ER␣ AF-1 and AF-2 D. Role of the androgen receptor E. Non-genomic signaling F. Independent effects of gonadotropins V. Target Cells of Sex Steroids in Bone A. Osteoclasts B. Osteoblast lineage C. Chondrocytes D. Conclusions from conditional mouse models VI.Direct Skeletal Target Genes of the Androgen and Estrogen Receptor A. Estrogen receptor target genes B. Androgen receptor target genes VII.Interaction of Sex Steroids with Other Signaling Pathways
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“Although rodents express an SHBG homologue locally in the testis, the androgen-binding protein, hepatic expression of SHBG and SHBG secretion into circulation is absent postnatally. This deficit in circulating SHBG explains low levels and susceptibility to fluctuation of T in rodents [46].”
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 [46]
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Estrogen Resistance Caused by a Mutation in the Estrogen-Receptor Gene in a Man
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Identification of late-onset hypogonadism in middle-aged and elderly men
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- Yu, 2012, Hypogonadism with estrogen removal (HER): differential effects of androgens and estrogens on bone microarchitecture in adult men, J Bone Miner Res, 27, S66
- Orwoll, 2012, Lack of value of serum sex steroid measures in the prediction of osteoporosis and fracture risk in community-dwelling, ambulatory older men, J Bone Miner Res, 27, S66
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Estrogens and androgens in skeletal physiology and pathophysiology
Almeida, M., Laurent, M. R., Dubois, V., Claessens, F., O'Brien, C. A., Bouillon, R., Vanderschueren, D., & Manolagas, S. C. (2017) · Physiological Reviews · doi:10.1152/physrev.00033.2015 · Cited by 860
Self-citationAndrogen Receptor Structure, Function and Biology: From Bench to Bedside.
(2016) · Europe PMC (PubMed Central) · Cited by 623
Cooke, P. S., Nanjappa, M. K., Ko, C. J., Prins, G. S., & Hess, R. A. (2017) · Physiological Reviews · doi:10.1152/physrev.00018.2016 · Cited by 489
Nilsson, M., Vandenput, L., Tivesten, Å., Norlén, A., Lagerquist, M. K., Windahl, S. H., Börjesson, A., Farman, H. H., POUTANEN, M. H., Benrick, A., et al. (2015) · Endocrinology · doi:10.1210/en.2014-1890 · Cited by 354
Self-citationA concise review of testosterone and bone health
Mohamad, N.-V., Soelaiman, I. N., & Chin, K. (2016) · Clinical Interventions in Aging · doi:10.2147/cia.s115472 · Cited by 305
Metadata
- Authors
- Vanderschueren, D., Laurent, M. R., Claessens, F., Gielen, E., Lagerquist, M. K., Vandenput, L., Börjesson, A. E., & Ohlsson, C.
- Affiliations
- KU Leuven (BE)
- Laboratory of Molecular Endocrinology, Department of Cellular and Molecular Medicine (M.R.L., F.C.);
- University of Gothenburg (SE)
- Corresponding author
- Vanderschueren, Dirk
- ORCID
- Venue
- Endocrine Reviews
- Publisher
- The Endocrine Society
- Published
- 2014-09-09
- Volume
- 35
- Issue
- 6
- Pages
- 906-960
- ISSN
- 0163-769X (ISSN-L)
- 1945-7189
- PMC
- PMC4234776
- OpenAlex
- W2163690987
- Cited by
- 327
- References
- 459
- Citations by year
- 2026: 23 · 2025: 24 · 2024: 22 · 2023: 21 · 2022: 30 · 2021: 16 · 2020: 37 · 2019: 21 · 2018: 32 · 2017: 34 · 2016: 30 · 2015: 35 · 2014: 1
- FWCI
- 6.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Endocrine Reviews (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Lirias (submittedVersion, other-oa)
- Funders
- Amgen
- European Commission (201865)
- Stiftelsen för Strategisk Forskning
- Fonds Wetenschappelijk Onderzoek (G068412N, G085413N)
- KU Leuven (OT-11-081, B-3000)
- Novo Nordisk
- Vetenskapsrådet
- Novo Nordisk Fonden (NNF14OC0010513, NNF13OC0005785, NNF13OC0004839)
- Servier
- Vlaamse regering
- Topics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Keywords
- sex steroids, male osteoporosis, estrogen receptor alpha, androgen receptor, androgens, estrogen, sex hormone-binding globulin, peak bone mass, cortical bone, trabecular bone, bone microarchitecture, bone formation, bone resorption, osteoblasts, osteocytes, osteoclasts, chondrocytes, gonadotropins, non-genomic steroid action, fracture risk, older men, sex differences in bone, muscle mass
- MeSH terms
- Aging, Androgens, Animals, Bone and Bones, Estrogens, Female, Humans, Male, Osteogenesis, Osteoporosis, Signal Transduction, Mice
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