Vitamin C epigenetically controls osteogenesis and bone mineralization.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
06 10 2022
Historique:
received: 01 10 2020
accepted: 09 08 2022
entrez: 6 10 2022
pubmed: 7 10 2022
medline: 12 10 2022
Statut: epublish

Résumé

Vitamin C deficiency disrupts the integrity of connective tissues including bone. For decades this function has been primarily attributed to Vitamin C as a cofactor for collagen maturation. Here, we demonstrate that Vitamin C epigenetically orchestrates osteogenic differentiation and function by modulating chromatin accessibility and priming transcriptional activity. Vitamin C regulates histone demethylation (H3K9me3 and H3K27me3) and promotes TET-mediated 5hmC DNA hydroxymethylation at promoters, enhancers and super-enhancers near bone-specific genes. This epigenetic circuit licenses osteoblastogenesis by permitting the expression of all major pro-osteogenic genes. Osteogenic cell differentiation is strictly and continuously dependent on Vitamin C, whereas Vitamin C is dispensable for adipogenesis. Importantly, deletion of 5hmC-writers, Tet1 and Tet2, in Vitamin C-sufficient murine bone causes severe skeletal defects which mimic bone phenotypes of Vitamin C-insufficient Gulo knockout mice, a model of Vitamin C deficiency and scurvy. Thus, Vitamin C's epigenetic functions are central to osteoblastogenesis and bone formation and may be leveraged to prevent common bone-degenerating conditions.

Identifiants

pubmed: 36202795
doi: 10.1038/s41467-022-32915-8
pii: 10.1038/s41467-022-32915-8
pmc: PMC9537512
doi:

Substances chimiques

Chromatin 0
Histones 0
DNA 9007-49-2
Ascorbic Acid PQ6CK8PD0R

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

5883

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK131455
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001863
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK126827
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK058185
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR049069
Pays : United States

Informations de copyright

© 2022. The Author(s).

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Auteurs

Roman Thaler (R)

Department of Orthopedic Surgery, Mayo Clinic, Rochester, MN, USA. Thaler.Roman@mayo.edu.
Department of Biochemistry & Molecular Biology, Mayo Clinic, Rochester, MN, USA. Thaler.Roman@mayo.edu.
Center for Regenerative Medicine, Mayo Clinic, Rochester, MN, USA. Thaler.Roman@mayo.edu.

Farzaneh Khani (F)

Department of Orthopedic Surgery, Mayo Clinic, Rochester, MN, USA.

Ines Sturmlechner (I)

Departments of Pediatric and Adolescent Medicine, Mayo Clinic, Rochester, MN, USA.

Sharareh S Dehghani (SS)

Department of Orthopedic Surgery, Mayo Clinic, Rochester, MN, USA.

Janet M Denbeigh (JM)

Department of Orthopedic Surgery, Mayo Clinic, Rochester, MN, USA.

Xianhu Zhou (X)

Department of Orthopedic Surgery, Mayo Clinic, Rochester, MN, USA.

Oksana Pichurin (O)

Department of Orthopedic Surgery, Mayo Clinic, Rochester, MN, USA.

Amel Dudakovic (A)

Department of Orthopedic Surgery, Mayo Clinic, Rochester, MN, USA.
Department of Biochemistry & Molecular Biology, Mayo Clinic, Rochester, MN, USA.

Sofia S Jerez (SS)

Department of Orthopedic Surgery, Mayo Clinic, Rochester, MN, USA.
Department of Biochemistry & Molecular Biology, Mayo Clinic, Rochester, MN, USA.

Jian Zhong (J)

Epigenomics Program, Center for Individualized Medicine, Mayo Clinic, Rochester, MN, USA.

Jeong-Heon Lee (JH)

Department of Biochemistry & Molecular Biology, Mayo Clinic, Rochester, MN, USA.
Epigenomics Program, Center for Individualized Medicine, Mayo Clinic, Rochester, MN, USA.

Ramesh Natarajan (R)

Department of Internal Medicine, Virginia Commonwealth University, Richmond, VA, USA.

Ivo Kalajzic (I)

Department of Reconstructive Sciences, UConn Health, Farmington, CT, USA.

Yong-Hui Jiang (YH)

Department of Genetics, Neuroscience, and Pediatrics, Yale University School of Medicine, New Haven, CT, USA.

David R Deyle (DR)

Department of Clinical Genomics, Mayo Clinic, Rochester, MN, USA.

Eleftherios P Paschalis (EP)

Ludwig Boltzmann Institute of Osteology at Hanusch Hospital of OEGK and AUVA Trauma Centre Meidling, 1st Med. Dept. Hanusch Hospital, Vienna, Austria.

Barbara M Misof (BM)

Ludwig Boltzmann Institute of Osteology at Hanusch Hospital of OEGK and AUVA Trauma Centre Meidling, 1st Med. Dept. Hanusch Hospital, Vienna, Austria.

Tamas Ordog (T)

Epigenomics Program, Center for Individualized Medicine, Mayo Clinic, Rochester, MN, USA.
Department of Physiology and Biomedical Engineering and Division of Gastroenterology and Hepatology, Department of Medicine, Mayo Clinic, Rochester, MN, USA.

Andre J van Wijnen (AJ)

Department of Biochemistry, University of Vermont, Burlington, VT, USA. andre.vanwijnen@uvm.edu.

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