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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Rodents lack postnatal hepatic expression and secretion of SHBG into circulation, which explains low levels and susceptibility to fluctuation of testosterone in rodents.
“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]
In “Differences in circulating sex steroid physiology” (page unavailable), the review says mice and rats lack circulating SHBG and that this is thought to contribute to their very low, highly fluctuating serum testosterone. It does not establish the more specific claim about postnatal hepatic expression or secretion, and “explains” is stronger than the review’s qualified wording. (LLM, conf=0.86)
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Multistage genome-wide association meta-analyses identified two new loci for bone mineral density
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Female Estrogen Receptor β−/− Mice Are Partially Protected Against Age-Related Trabecular Bone Loss
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Female Mice Lacking Estrogen Receptor-Alpha in Osteoblasts Have Compromised Bone Mass and Strength
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Role of T cells in ovariectomy induced bone loss—revisited
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Estrogen receptor-α in osteocytes is important for trabecular bone formation in male mice
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Self-citationEstimation of Estradiol in Mouse Serum Samples: Evaluation of Commercial Estradiol Immunoassays
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Hormone Replacement Therapy and Physical Function in Healthy Older Men. Time to Talk Hormones?
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Body composition, volumetric and areal bone parameters in male-to-female transsexual persons
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Calculation of Bioavailable and Free Testosterone in Men: A Comparison of 5 Published Algorithms
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How Sex Hormones Promote Skeletal Muscle Regeneration
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Estrogens as regulators of bone health in men
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Self-citationPopulation-Based Fracture Risk Assessment and Osteoporosis Treatment Disparities by Race and Gender
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Longitudinal Changes in BMD and Bone Geometry in a Population-Based Study
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Unique ERα Cistromes Control Cell Type-Specific Gene Regulation
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Osteoporosis in men: a potential role for the sex hormone binding globulin
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Estren Is a Selective Estrogen Receptor Modulator with Transcriptional Activity
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Self-citationAndrogens regulate bone resorption activity of isolated osteoclasts <i>in vitro</i>
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Estrogens and androgens in skeletal physiology and pathophysiology
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Self-citationAndrogen Receptor Structure, Function and Biology: From Bench to Bedside.
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Self-citationA concise review of testosterone and bone health
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Self-citationGonadal steroid–dependent effects on bone turnover and bone mineral density in men
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Self-citationMuscle-bone interactions: From experimental models to the clinic? A critical update
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Aging and the Male Reproductive System
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Sex differences in athletic performance emerge coinciding with the onset of male puberty
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Pubertal growth and epiphyseal fusion
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A Track Record on SHOX: From Basic Research to Complex Models and Therapy
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Bone-Targeted Therapies in Cancer-Induced Bone Disease
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Mini-Puberty, Physiological and Disordered: Consequences, and Potential for Therapeutic Replacement
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Body weight homeostat that regulates fat mass independently of leptin in rats and mice
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Transwomen in elite sport: scientific and ethical considerations
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The practical management of testosterone deficiency in men
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Neuromuscular Diseases and Bone
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Probiotics in Gut-Bone Signaling
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Self-citationThe Endocrine Role of Estrogens on Human Male Skeleton
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The bone-sparing effects of estrogen and WNT16 are independent of each other
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Self-citationNew Insights Into Androgen and Estrogen Receptor Regulation of the Male Skeleton
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Bone Health in the Transgender Population
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Hypertension is associated with osteoporosis: a case-control study in Chinese postmenopausal women
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Testosterone boosts physical activity in male mice via dopaminergic pathways
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Self-citationEndocrine treatment of aging transgender people
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Associations of vitamin D status and vitamin D-related polymorphisms with sex hormones in older men
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Sex-Differences in Skeletal Growth and Aging
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Sex steroids and the kidney: role in renal calcium and phosphate handling
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Self-citationThe androgen receptor has no direct antiresorptive actions in mouse osteoclasts
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- 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 › Genetics › 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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