Inhibition of Nrf2 degradation alleviates age-related osteoporosis induced by 1,25-Dihydroxyvitamin D deficiency

Yang, Renlei; Zhang, Jiao; Li, Jie; Qin, Ran; Chen, Jie; Wang, Rong; Goltzman, David; Miao, Dengshun

doi:10.1016/j.freeradbiomed.2021.12.010

Cited by 68Bone Metabolism and DiseasesGenomics, phytochemicals, and oxidative stressVitamin D Research Studies

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Inhibition of Nrf2 degradation alleviates age-related osteoporosis induced by 1,25-Dihydroxyvitamin D deficiency

Yang, Renlei, Zhang, Jiao, Li, Jie, Qin, Ran, Chen, Jie, Wang, Rong, Goltzman, David, Miao, Dengshun·2022·Free Radical Biology and Medicine

DOI 10.1016/j.freeradbiomed.2021.12.010

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Abstract

Previous studies have shown that 1,25(OH)2 D plays an anti-osteoporosis role by an anti-aging mechanism. Oxidative stress is a key mediator of aging and bone loss; however, whether 1,25(OH)2 D can exert its anti-osteoporosis effect by inhibiting oxidative stress is unclear. In this study, osteoporosis and the bone aging phenotype induced by 1,25(OH)2 D deficiency in male mice were significantly rescued in vivo upon the supplementation of oltipraz, an inhibitor of Nrf2 degradation. Increased oxidative stress, cellular senescence and reduced osteogenesis of BM-MSCs from VDR knockout mice were also significantly rescued when the cells were pre-treated with oltipraz. We found that 1,25(OH)2 D 3 promoted Nrf2 accumulation by inhibiting its ubiquitin-proteasome degradation, thus facilitating Nrf2 activation of its transcriptional targets. Mechanistically, 1,25(OH)2 D 3 enhances VDR-mediated recruitment of Ezh2 and facilitation of H3K27me3 action at the promoter region of Keap1, thus transcriptionally repressing Keap1. To further validate that the Nrf2-Keap1 pathway serves as the key mediator in the anabolic effect of 1,25(OH)2 D 3 on bone, Nrf2-/- mice, or hBM-MSCs with shRNA-mediated Nrf2-knockdown, were treated with 1,25(OH)2 D 3; we found that Nrf2 knockout largely blocked the bone anabolic effect of 1,25(OH)2 D 3 in vivo and ex vivo, and Nrf2 knockdown in hBM-MSCs markedly blocked the role of 1,25(OH)2 D 3 in inhibiting oxidative stress and promoting osteogenic differentiation and bone formation. This study provides insight into the mechanism whereby 1,25(OH)2 D 3 postpones age-related osteoporosis via VDR-mediated activation of Nrf2-antioxidant signaling and inhibition of oxidative stress, and thus provides evidence for oltipraz as a potential reagent for clinical prevention and treatment of age-related osteoporosis.

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The Nrf2 signaling pathway is a central regulatory system of cellular antioxidant defense in bone metabolism.
“Recent discoveries have highlighted the pivotal role of the Nrf2 signaling pathway, a central regulatory system of cellular antioxidant defense, in bone metabolism52,53.”
From Intelligence-responsive wettability switch coating on magnesium implants for treating osteoporotic fracture (2026) · cites this paper as [53]

1 retracted

RETRACTED: 1,25‐Dihydroxyvitamin D exerts an antiaging role by activation of Nrf2‐antioxidant signaling and inactivation of p16/p53‐senescence signaling
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Additional file 2 of Psoralen alleviates radiation-induced bone injury by rescuing skeletal stem cell stemness through AKT-mediated upregulation of GSK-3β and NRF2
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Additional file 1 of Psoralen alleviates radiation-induced bone injury by rescuing skeletal stem cell stemness through AKT-mediated upregulation of GSK-3β and NRF2
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Additional file 3 of Psoralen alleviates radiation-induced bone injury by rescuing skeletal stem cell stemness through AKT-mediated upregulation of GSK-3β and NRF2
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Additional file 5 of Psoralen alleviates radiation-induced bone injury by rescuing skeletal stem cell stemness through AKT-mediated upregulation of GSK-3β and NRF2
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Authors: Yang, R., Zhang, J., Li, J., Qin, R., Chen, J., Wang, R., Goltzman, D., & Miao, D.
Affiliations: State Key Laboratory of Reproductive Medicine (CN)
Central South University (CN)
Research Institute of the McGill University Health Centre (CA)
Corresponding author: Miao, Dengshun
ORCID: Yang, Renlei
Zhang, Jiao
Li, Jie
Chen, Jie
Wang, Rong
Goltzman, David
Miao, Dengshun
Venue: Free Radical Biology and Medicine
Publisher: Elsevier BV
Published: 2022-01
Volume: 178
Pages: 246-261
ISSN: 0891-5849 (ISSN-L)
DOI: 10.1016/j.freeradbiomed.2021.12.010
OpenAlex: W4200084934
Cited by: 67
References: 52
Citations by year: 2026: 12 · 2025: 10 · 2024: 15 · 2023: 12 · 2022: 18
FWCI: 3.53
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Free Radical Biology and Medicine (publishedVersion)
PubMed (publishedVersion)
Funders: National Key Research and Development Program of China (2018YFA0800800)
Canadian Institutes of Health Research (PJT-152963)
National Natural Science Foundation of China (81730066)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics, phytochemicals, and oxidative stress
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Vitamin D Research Studies
Keywords: senile osteoporosis, 1,25-dihydroxyvitamin D, Nrf2, oltipraz, Nrf2/Keap1 pathway, oxidative stress, vitamin D receptor, EZH2, H3K27me3, Keap1, bone aging, bone marrow mesenchymal stem cells, osteogenic differentiation, bone formation, cellular senescence
MeSH terms: Kelch-Like ECH-Associated Protein 1, Animals, Male, Osteogenesis, Osteoporosis, Vitamin D, Receptors, Calcitriol, NF-E2-Related Factor 2, Mice

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Inhibition of Nrf2 degradation alleviates age-related osteoporosis induced by 1,25-Dihydroxyvitamin D deficiency

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