Cited by 327Bone health and osteoporosis researchEstrogen and related hormone effectsBone Metabolism and Diseases

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Sex Steroid Actions in Male Bone

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Vanderschueren, Dirk, Laurent, Michaël R., Claessens, Frank, Gielen, Evelien, Lagerquist, Marie K., Vandenput, Liesbeth, Börjesson, Anna E., Ohlsson, Claes·2014·Endocrine Reviews

DOI 10.1210/er.2014-1024PMC PMC4234776

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Abstract

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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Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia
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Effect of Vitamin D Supplementation on Testosterone Levels in Men
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Evaluation of an Estrogen Receptor-β Agonist in Animal Models of Human Disease
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Expression of Estrogen Receptor in Rat Bone
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Estrogen Receptors α and β Are Differentially Expressed in Developing Human Bone1
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Bone Structure at the Distal Radius During Adolescent Growth
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Low Free Testosterone Predicts Frailty in Older Men: The Health in Men Study
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“Serum T levels have been associated with lean mass, muscle strength, and frailty in cross-sectional (32) and prospective studies (34, 430).”
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Differential Effects of Androgens and Estrogens on Bone Turnover in Normal Men
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The Estrogen Receptor-α in Osteoclasts Mediates the Protective Effects of Estrogens on Cancellous But Not Cortical Bone
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Older Men With Low Serum Estradiol and High Serum SHBG Have an Increased Risk of Fractures
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Optimal Vitamin D Status: A Critical Analysis on the Basis of Evidence-Based Medicine
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Sclerostin and Its Association with Physical Activity, Age, Gender, Body Composition, and Bone Mineral Content in Healthy Adults
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Wnt/β-Catenin Signaling Is a Component of Osteoblastic Bone Cell Early Responses to Load-bearing and Requires Estrogen Receptor α
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Kinase-mediated regulation of common transcription factors accounts for the bone-protective effects of sex steroids
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Testosterone Use in Men and Its Effects on Bone Health. A Systematic Review and Meta-Analysis of Randomized Placebo-Controlled Trials
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Endogenous Sex Hormones and Incident Fracture Risk in Older Men<subtitle>The Dubbo Osteoporosis Epidemiology Study</subtitle>
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Estrogen receptor-α signaling in osteoblast progenitors stimulates cortical bone accrual
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Sex Hormones and Cognitive Function in Older Men
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Receptor Activator of Nuclear Factor κB Ligand (RANKL) Protein Expression by B Lymphocytes Contributes to Ovariectomy-induced Bone Loss
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Association of vitamin D status with serum androgen levels in men
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Raloxifene to Prevent Gonadotropin-Releasing Hormone Agonist-Induced Bone Loss in Men with Prostate Cancer: A Randomized Controlled Trial
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A Randomized, Placebo-Controlled Study of the Effects of Denosumab for the Treatment of Men with Low Bone Mineral Density
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The effects of serum testosterone, estradiol, and sex hormone binding globulin levels on fracture risk in older men
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Longitudinal Association between Sex Hormone Levels, Bone Loss, and Bone Turnover in Elderly Men
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Sterility and absence of histopathological defects in nonreproductive organs of a mouse ERβ-null mutant
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Diverse roles of androgen receptor (AR) domains in AR-mediated signaling
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Runx2 determines bone maturity and turnover rate in postnatal bone development and is involved in bone loss in estrogen deficiency
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Regulation of circulating sclerostin levels by sex steroids in women and in men
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Genetic determinants of serum testosterone concentrations in men
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Follicle-stimulating hormone stimulates TNF production from immune cells to enhance osteoblast and osteoclast formation
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Older Men With Low Serum Estradiol and High Serum SHBG Have an Increased Risk of Fractures
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Remaining lifetime and absolute 10-year probabilities of osteoporotic fracture in Swiss men and women
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Low Levels of Estradiol Are Associated with Vertebral Fractures in Older Men, But Not Women: The Rancho Bernardo Study
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Conditional Inactivation of Androgen Receptor Gene in the Nervous System: Effects on Male Behavioral and Neuroendocrine Responses
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The epidemiology of fractures in England
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Estrogens in the Nervous System: Mechanisms and Nonreproductive Functions
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Estrogen Receptor α Signaling in T Lymphocytes Is Required for Estradiol-Mediated Inhibition of Th1 and Th17 Cell Differentiation and Protection against Experimental Autoimmune Encephalomyelitis
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Estrogen receptor specificity in the regulation of the skeleton in female mice
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Impaired skeletal muscle development and function in male, but not female, genomic androgen receptor knockout mice
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A functional androgen receptor is not sufficient to allow estradiol to protect bone after gonadectomy in estradiol receptor–deficient mice
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Estrogen and testosterone use different cellular pathways to inhibit osteoclastogenesis and bone resorption.
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Estrogens Are Essential for Male Pubertal Periosteal Bone Expansion
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Comparison of serum testosterone and estradiol measurements in 3174 European men using platform immunoassay and mass spectrometry; relevance for the diagnostics in aging men
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Androgens and skeletal muscle: cellular and molecular action mechanisms underlying the anabolic actions
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Late onset of obesity in male androgen receptor-deficient (AR KO) mice
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Association of hypogonadism with vitamin D status: The European Male Ageing Study
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Bone Has a Sexually Dimorphic Response to Aromatase Deficiency
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Endogenous Testosterone Levels, Physical Performance, and Fall Risk in Older Men
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Estradiol, Testosterone, and the Risk for Hip Fractures in Elderly Men from the Framingham Study
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Relative Impact of Androgen and Estrogen Receptor Activation in the Effects of Androgens on Trabecular and Cortical Bone in Growing Male Mice: A Study in the Androgen Receptor Knockout Mouse Model
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Bicalutamide Monotherapy Versus Leuprolide Monotherapy for Prostate Cancer: Effects on Bone Mineral Density and Body Composition
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Insulin-Like Growth Factor Regulates Peak Bone Mineral Density in Mice by Both Growth Hormone-Dependent and -Independent Mechanisms
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Estrogen receptor specificity for the effects of estrogen in ovariectomized mice
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Update in Male Osteoporosis
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Bioavailable Estradiol and an Aromatase Gene Polymorphism Are Determinants of Bone Mineral Density Changes in Men over 70 Years of Age
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ORIGINAL ARTICLE: Accuracy of calculated free testosterone formulae in men
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Dissecting Physiological Roles of Estrogen Receptor α and β with Potent Selective Ligands from Structure-Based Design
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Bone micro-architecture and determinants of strength in the radius and tibia: age-related changes in a population-based study of normal adults measured with high-resolution pQCT
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Imprinting of Growth Hormone Secretion, Body Growth, and Hepatic Steroid Metabolism by Neonatal Testosterone*
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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: Vanderschueren, Dirk
Laurent, Michaël R.
Claessens, Frank
Gielen, Evelien
Lagerquist, Marie K.
Vandenput, Liesbeth
Ohlsson, Claes
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
DOI: 10.1210/er.2014-1024
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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Sex Steroid Actions in Male Bone

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