Osteogenic CpG Oligodeoxynucleotide, iSN40, Inhibits Osteoclastogenesis in a TLR9-Dependent Manner

A CpG oligodeoxynucleotide (CpG-ODN), iSN40, was originally identified as promoting the mineralization and differentiation of osteoblasts, independent of Toll-like receptor 9 (TLR9). Since CpG ODNs are often recognized by TLR9 and inhibit osteoclastogenesis, this study investigated the TLR9 dependen...

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Main Authors: Rena Ikeda, Chihaya Kimura, Yuma Nihashi, Koji Umezawa, Takeshi Shimosato, Tomohide Takaya
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Life
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Online Access:https://www.mdpi.com/2075-1729/14/12/1572
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author Rena Ikeda
Chihaya Kimura
Yuma Nihashi
Koji Umezawa
Takeshi Shimosato
Tomohide Takaya
author_facet Rena Ikeda
Chihaya Kimura
Yuma Nihashi
Koji Umezawa
Takeshi Shimosato
Tomohide Takaya
author_sort Rena Ikeda
collection DOAJ
description A CpG oligodeoxynucleotide (CpG-ODN), iSN40, was originally identified as promoting the mineralization and differentiation of osteoblasts, independent of Toll-like receptor 9 (TLR9). Since CpG ODNs are often recognized by TLR9 and inhibit osteoclastogenesis, this study investigated the TLR9 dependence and anti-osteoclastogenic effect of iSN40 to validate its potential as an osteoporosis drug. The murine monocyte/macrophage cell line RAW264.7 was treated with the receptor activator of nuclear factor-κB ligand (RANKL) to induce osteoclast differentiation, then the effect of iSN40 on was quantified by tartrate-resistant acid phosphatase (TRAP) staining and real-time RT-PCR. iSN40 completely inhibited RANKL-induced differentiation into TRAP<sup>+</sup> multinucleated osteoclasts by suppressing osteoclastogenic genes and inducing anti-/non-osteoclastogenic genes. Treatment with a TLR9 inhibitor, E6446, or a mutation in the CpG motif of iSN40 abolished the intracellular uptake and anti-osteoclastogenic effect of iSN40. These results demonstrate that iSN40 is subcellularly internalized and is recognized by TLR9 via its CpG motif, modulates RANKL-dependent osteoclastogenic gene expression, and ultimately inhibits osteoclastogenesis. Finally, iSN40 was confirmed to inhibit the osteoclastogenesis of RAW264.7 cells cocultured with the murine osteoblast cell line MC3T3-E1, presenting a model of bone remodeling. This study demonstrates that iSN40, which exerts both pro-osteogenic and anti-osteoclastogenic effects, may be a promising nucleic acid drug for osteoporosis.
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spelling doaj-art-7fb2e5acfc8646979396bf789c3adf642025-08-20T02:53:44ZengMDPI AGLife2075-17292024-11-011412157210.3390/life14121572Osteogenic CpG Oligodeoxynucleotide, iSN40, Inhibits Osteoclastogenesis in a TLR9-Dependent MannerRena Ikeda0Chihaya Kimura1Yuma Nihashi2Koji Umezawa3Takeshi Shimosato4Tomohide Takaya5Department of Agriculture, Graduate School of Science and Technology, Shinshu University, 8304 Minami-minowa, Kami-ina, Nagano 399-4598, JapanDepartment of Agriculture, Graduate School of Science and Technology, Shinshu University, 8304 Minami-minowa, Kami-ina, Nagano 399-4598, JapanDepartment of Science and Technology, Graduate School of Medicine, Science and Technology, Shinshu University, 8304 Minami-minowa, Kami-ina, Nagano 399-4598, JapanDepartment of Science and Technology, Graduate School of Medicine, Science and Technology, Shinshu University, 8304 Minami-minowa, Kami-ina, Nagano 399-4598, JapanDepartment of Agriculture, Graduate School of Science and Technology, Shinshu University, 8304 Minami-minowa, Kami-ina, Nagano 399-4598, JapanDepartment of Agriculture, Graduate School of Science and Technology, Shinshu University, 8304 Minami-minowa, Kami-ina, Nagano 399-4598, JapanA CpG oligodeoxynucleotide (CpG-ODN), iSN40, was originally identified as promoting the mineralization and differentiation of osteoblasts, independent of Toll-like receptor 9 (TLR9). Since CpG ODNs are often recognized by TLR9 and inhibit osteoclastogenesis, this study investigated the TLR9 dependence and anti-osteoclastogenic effect of iSN40 to validate its potential as an osteoporosis drug. The murine monocyte/macrophage cell line RAW264.7 was treated with the receptor activator of nuclear factor-κB ligand (RANKL) to induce osteoclast differentiation, then the effect of iSN40 on was quantified by tartrate-resistant acid phosphatase (TRAP) staining and real-time RT-PCR. iSN40 completely inhibited RANKL-induced differentiation into TRAP<sup>+</sup> multinucleated osteoclasts by suppressing osteoclastogenic genes and inducing anti-/non-osteoclastogenic genes. Treatment with a TLR9 inhibitor, E6446, or a mutation in the CpG motif of iSN40 abolished the intracellular uptake and anti-osteoclastogenic effect of iSN40. These results demonstrate that iSN40 is subcellularly internalized and is recognized by TLR9 via its CpG motif, modulates RANKL-dependent osteoclastogenic gene expression, and ultimately inhibits osteoclastogenesis. Finally, iSN40 was confirmed to inhibit the osteoclastogenesis of RAW264.7 cells cocultured with the murine osteoblast cell line MC3T3-E1, presenting a model of bone remodeling. This study demonstrates that iSN40, which exerts both pro-osteogenic and anti-osteoclastogenic effects, may be a promising nucleic acid drug for osteoporosis.https://www.mdpi.com/2075-1729/14/12/1572CpG oligodeoxynucleotide (CpG-ODN)osteoclastosteoclastogenesisosteogenetic oligodeoxynucleotide (osteoDN)Toll-like receptor 9 (TLR9)
spellingShingle Rena Ikeda
Chihaya Kimura
Yuma Nihashi
Koji Umezawa
Takeshi Shimosato
Tomohide Takaya
Osteogenic CpG Oligodeoxynucleotide, iSN40, Inhibits Osteoclastogenesis in a TLR9-Dependent Manner
Life
CpG oligodeoxynucleotide (CpG-ODN)
osteoclast
osteoclastogenesis
osteogenetic oligodeoxynucleotide (osteoDN)
Toll-like receptor 9 (TLR9)
title Osteogenic CpG Oligodeoxynucleotide, iSN40, Inhibits Osteoclastogenesis in a TLR9-Dependent Manner
title_full Osteogenic CpG Oligodeoxynucleotide, iSN40, Inhibits Osteoclastogenesis in a TLR9-Dependent Manner
title_fullStr Osteogenic CpG Oligodeoxynucleotide, iSN40, Inhibits Osteoclastogenesis in a TLR9-Dependent Manner
title_full_unstemmed Osteogenic CpG Oligodeoxynucleotide, iSN40, Inhibits Osteoclastogenesis in a TLR9-Dependent Manner
title_short Osteogenic CpG Oligodeoxynucleotide, iSN40, Inhibits Osteoclastogenesis in a TLR9-Dependent Manner
title_sort osteogenic cpg oligodeoxynucleotide isn40 inhibits osteoclastogenesis in a tlr9 dependent manner
topic CpG oligodeoxynucleotide (CpG-ODN)
osteoclast
osteoclastogenesis
osteogenetic oligodeoxynucleotide (osteoDN)
Toll-like receptor 9 (TLR9)
url https://www.mdpi.com/2075-1729/14/12/1572
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