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Open AccessArticle

Commensal Microbiota Enhance Both Osteoclast and Osteoblast Activities

1
Department of Preventive Dentistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Kita-ku, Okayama 700-8558, Japan
2
Department of Microbiology and Immunology, Columbia University Medical Center, New York, NY 10032, USA
3
Department of Biochemistry and Molecular Dentistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan. 2-5-1 Shikata-cho, Kita-ku, Okayama 700-8525, Japan
4
Department of Molecular Biology and Biochemistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Kita-ku, Okayama 700-8558, Japan
5
Advanced Research Center for Oral and Craniofacial Sciences, Okayama University Dental School, Okayama, Japan 2-5-1 Shikata-cho, Kita-ku, Okayama 700-8558, Japan
*
Author to whom correspondence should be addressed.
Molecules 2018, 23(7), 1517; https://doi.org/10.3390/molecules23071517
Received: 29 May 2018 / Revised: 19 June 2018 / Accepted: 21 June 2018 / Published: 23 June 2018
Recent studies suggest that the commensal microbiota affects not only host energy metabolism and development of immunity but also bone remodeling by positive regulation of osteoclast activity. However, the mechanism of regulation of bone cells by the commensal microbiota has not been elucidated. In this study, 8-week-old specific pathogen-free (SPF) and germ-free (GF) mice were compared in terms of alveolar bones and primary osteoblasts isolated from calvarias. Micro-CT analysis showed that SPF mice had larger body size associated with lower bone mineral density and bone volume fraction in alveolar bones compared with GF mice. Greater numbers of osteoclasts in alveolar bone and higher serum levels of tartrate-resistant acid phosphatase 5b were observed in SPF mice. Tissue extracts from SPF alveolar bone showed higher levels of cathepsin K, indicating higher osteoclast activity. SPF alveolar extracts also showed elevated levels of γ-carboxylated glutamic acid–osteocalcin as a marker of mature osteoblasts compared with GF mice. Polymerase chain reaction (PCR) array analysis of RNA directly isolated from alveolar bone showed that in SPF mice, expression of mRNA of osteocalcin, which also acts as an inhibitor of bone mineralization, was strongly enhanced compared with GF mice. Cultured calvarial osteoblasts from SPF mice showed reduced mineralization but significantly enhanced expression of mRNAs of osteocalcin, alkaline phosphatase, insulin-like growth factor-I/II, and decreased ratio of osteoprotegerin/receptor activator of nuclear factor-kappa B ligand compared with GF mice. Furthermore, PCR array analyses of transcription factors in cultured calvarial osteoblasts showed strongly upregulated expression of Forkhead box g1. In contrast, Gata-binding protein 3 was strongly downregulated in SPF osteoblasts. These results suggest that the commensal microbiota prevents excessive mineralization possibly by stimulating osteocalcin expression in osteoblasts, and enhances both osteoblast and osteoclast activity by regulating specific transcription factors. View Full-Text
Keywords: osteoblast; osteocalcin; Insulin-like growth factor-1; commensal microbiota; bone remodeling osteoblast; osteocalcin; Insulin-like growth factor-1; commensal microbiota; bone remodeling
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Uchida, Y.; Irie, K.; Fukuhara, D.; Kataoka, K.; Hattori, T.; Ono, M.; Ekuni, D.; Kubota, S.; Morita, M. Commensal Microbiota Enhance Both Osteoclast and Osteoblast Activities. Molecules 2018, 23, 1517.

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