Receptor activator of nuclear factor-kappa B ligand-derived microglia healing peptide 1-AcN inhibits osteoarthritis progression in mice

Abstract Background Osteoarthritis (OA) is a degenerative disease characterized by subchondral bone sclerosis, chronic inflammation, and cartilage degradation. Abnormal mechanical stress by meniscal deviation activates osteoclasts and induces the release of transforming growth factor-beta (TGF-β), w...

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Main Authors: Yuji Fukuda, Munehisa Shimamura, Yuki Etani, Takaaki Noguchi, Takuya Kurihara, Atsushi Goshima, Taihei Miura, Makoto Hirao, Nagahiro Ochiai, Nan Ju, Atsushi Sugimoto, Takashi Kanamoto, Ken Nakata, Seiji Okada, Kosuke Ebina
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Arthritis Research & Therapy
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Online Access:https://doi.org/10.1186/s13075-025-03609-5
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author Yuji Fukuda
Munehisa Shimamura
Yuki Etani
Takaaki Noguchi
Takuya Kurihara
Atsushi Goshima
Taihei Miura
Makoto Hirao
Nagahiro Ochiai
Nan Ju
Atsushi Sugimoto
Takashi Kanamoto
Ken Nakata
Seiji Okada
Kosuke Ebina
author_facet Yuji Fukuda
Munehisa Shimamura
Yuki Etani
Takaaki Noguchi
Takuya Kurihara
Atsushi Goshima
Taihei Miura
Makoto Hirao
Nagahiro Ochiai
Nan Ju
Atsushi Sugimoto
Takashi Kanamoto
Ken Nakata
Seiji Okada
Kosuke Ebina
author_sort Yuji Fukuda
collection DOAJ
description Abstract Background Osteoarthritis (OA) is a degenerative disease characterized by subchondral bone sclerosis, chronic inflammation, and cartilage degradation. Abnormal mechanical stress by meniscal deviation activates osteoclasts and induces the release of transforming growth factor-beta (TGF-β), which promotes mesenchymal stem cell (MSC)-mediated type H angiogenesis and osteogenesis, contributing to bone sclerosis and cartilage damage. Subsequently, macrophages recognize cartilage-derived damage-associated molecular patterns (DAMPs) via Toll-like receptor 4 (TLR4), polarizing into the pro-inflammatory M1 phenotype, thereby exacerbating synovitis and cartilage loss. We developed Microglia Healing Peptide 1 with N-terminal acetylation and C-terminal amidation (MHP1-AcN), a modified peptide derived from receptor activator of nuclear factor-kappa B ligand (RANKL), exhibiting both anti-osteoclastic and anti-inflammatory properties. This study aimed to evaluate the therapeutic potential of MHP1-AcN in a murine OA model and elucidate its underlying mechanisms. Methods OA was induced in mice via destabilization of the medial meniscus (DMM) surgery. Mice were randomly assigned to three groups (n = 8/group): Sham (sham surgery + saline), Vehicle (DMM + saline), and MHP1-AcN (DMM + MHP1-AcN). MHP1-AcN (600 µg) was administered intraperitoneally five times per week from a day after surgery. Knee joints were harvested at 2, 4, and 8 weeks post-surgery. In vitro, the effects of MHP1-AcN were assessed on osteoclast differentiation, inflammatory cytokine expression, and M1/M2 macrophage polarization using mouse bone marrow-derived macrophages. Additionally, its effects on TGF-β-induced osteogenic differentiation of bone marrow-derived MSCs (BMMSCs) and angiogenesis of human umbilical vein endothelial cells (HUVECs) were evaluated. Results MHP1-AcN markedly suppressed key pathological features of OA in vivo, including synovial inflammation, osteoclast-driven subchondral bone remodeling, aberrant angiogenesis, and cartilage degeneration. In vitro, MHP1-AcN effectively inhibited TLR4-mediated inflammatory cascades by reducing M1 macrophage polarization and inflammasome activation. Despite being derived from RANKL, MHP1-AcN supressed RANKL-induced osteoclastogenesis through NF-κB pathway suppression. Furthermore, MHP1-AcN attenuated TGF-β-induced osteogenic and angiogenic activities via Smad2 signaling inhibition in BMMSCs and HUVECs. Conclusion MHP1-AcN attenuates OA progression by modulating multi-pathways including aberrant bone remodeling, angiogenesis, and macrophage polarization, representing a promising disease-modifying therapeutic candidate for OA.
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spelling doaj-art-e5ce8d46744c41718cce8cb25faa0dd62025-08-20T03:43:01ZengBMCArthritis Research & Therapy1478-63622025-07-0127111510.1186/s13075-025-03609-5Receptor activator of nuclear factor-kappa B ligand-derived microglia healing peptide 1-AcN inhibits osteoarthritis progression in miceYuji Fukuda0Munehisa Shimamura1Yuki Etani2Takaaki Noguchi3Takuya Kurihara4Atsushi Goshima5Taihei Miura6Makoto Hirao7Nagahiro Ochiai8Nan Ju9Atsushi Sugimoto10Takashi Kanamoto11Ken Nakata12Seiji Okada13Kosuke Ebina14Department of Orthopaedic Surgery, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Gene & Stem Cell Regenerative Therapy, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Orthopaedic Surgery, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Orthopaedic Surgery, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Orthopaedic Surgery, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Orthopaedic Surgery, Osaka Rosai HospitalClinical and research institute for foot and ankle surgery, Jujo HospitalDepartment of Orthopaedic Surgery, NHO Osaka Minami Medical CenterDepartment of Musculoskeletal Regenerative Medicine, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Gene & Stem Cell Regenerative Therapy, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Orthopaedic Surgery, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Medicine for Sports and Performing Arts, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Medicine for Sports and Performing Arts, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Orthopaedic Surgery, The University of Osaka Graduate School of Medicine Faculty of MedicineDepartment of Orthopaedic Surgery, The University of Osaka Graduate School of Medicine Faculty of MedicineAbstract Background Osteoarthritis (OA) is a degenerative disease characterized by subchondral bone sclerosis, chronic inflammation, and cartilage degradation. Abnormal mechanical stress by meniscal deviation activates osteoclasts and induces the release of transforming growth factor-beta (TGF-β), which promotes mesenchymal stem cell (MSC)-mediated type H angiogenesis and osteogenesis, contributing to bone sclerosis and cartilage damage. Subsequently, macrophages recognize cartilage-derived damage-associated molecular patterns (DAMPs) via Toll-like receptor 4 (TLR4), polarizing into the pro-inflammatory M1 phenotype, thereby exacerbating synovitis and cartilage loss. We developed Microglia Healing Peptide 1 with N-terminal acetylation and C-terminal amidation (MHP1-AcN), a modified peptide derived from receptor activator of nuclear factor-kappa B ligand (RANKL), exhibiting both anti-osteoclastic and anti-inflammatory properties. This study aimed to evaluate the therapeutic potential of MHP1-AcN in a murine OA model and elucidate its underlying mechanisms. Methods OA was induced in mice via destabilization of the medial meniscus (DMM) surgery. Mice were randomly assigned to three groups (n = 8/group): Sham (sham surgery + saline), Vehicle (DMM + saline), and MHP1-AcN (DMM + MHP1-AcN). MHP1-AcN (600 µg) was administered intraperitoneally five times per week from a day after surgery. Knee joints were harvested at 2, 4, and 8 weeks post-surgery. In vitro, the effects of MHP1-AcN were assessed on osteoclast differentiation, inflammatory cytokine expression, and M1/M2 macrophage polarization using mouse bone marrow-derived macrophages. Additionally, its effects on TGF-β-induced osteogenic differentiation of bone marrow-derived MSCs (BMMSCs) and angiogenesis of human umbilical vein endothelial cells (HUVECs) were evaluated. Results MHP1-AcN markedly suppressed key pathological features of OA in vivo, including synovial inflammation, osteoclast-driven subchondral bone remodeling, aberrant angiogenesis, and cartilage degeneration. In vitro, MHP1-AcN effectively inhibited TLR4-mediated inflammatory cascades by reducing M1 macrophage polarization and inflammasome activation. Despite being derived from RANKL, MHP1-AcN supressed RANKL-induced osteoclastogenesis through NF-κB pathway suppression. Furthermore, MHP1-AcN attenuated TGF-β-induced osteogenic and angiogenic activities via Smad2 signaling inhibition in BMMSCs and HUVECs. Conclusion MHP1-AcN attenuates OA progression by modulating multi-pathways including aberrant bone remodeling, angiogenesis, and macrophage polarization, representing a promising disease-modifying therapeutic candidate for OA.https://doi.org/10.1186/s13075-025-03609-5Destabilization of the medial meniscusMacrophageMicroglia healing peptide 1 with N-terminal acetylation and C-terminal amidationOsteoarthritisOsteoclastReceptor activator of nuclear factor-kappa B ligand
spellingShingle Yuji Fukuda
Munehisa Shimamura
Yuki Etani
Takaaki Noguchi
Takuya Kurihara
Atsushi Goshima
Taihei Miura
Makoto Hirao
Nagahiro Ochiai
Nan Ju
Atsushi Sugimoto
Takashi Kanamoto
Ken Nakata
Seiji Okada
Kosuke Ebina
Receptor activator of nuclear factor-kappa B ligand-derived microglia healing peptide 1-AcN inhibits osteoarthritis progression in mice
Arthritis Research & Therapy
Destabilization of the medial meniscus
Macrophage
Microglia healing peptide 1 with N-terminal acetylation and C-terminal amidation
Osteoarthritis
Osteoclast
Receptor activator of nuclear factor-kappa B ligand
title Receptor activator of nuclear factor-kappa B ligand-derived microglia healing peptide 1-AcN inhibits osteoarthritis progression in mice
title_full Receptor activator of nuclear factor-kappa B ligand-derived microglia healing peptide 1-AcN inhibits osteoarthritis progression in mice
title_fullStr Receptor activator of nuclear factor-kappa B ligand-derived microglia healing peptide 1-AcN inhibits osteoarthritis progression in mice
title_full_unstemmed Receptor activator of nuclear factor-kappa B ligand-derived microglia healing peptide 1-AcN inhibits osteoarthritis progression in mice
title_short Receptor activator of nuclear factor-kappa B ligand-derived microglia healing peptide 1-AcN inhibits osteoarthritis progression in mice
title_sort receptor activator of nuclear factor kappa b ligand derived microglia healing peptide 1 acn inhibits osteoarthritis progression in mice
topic Destabilization of the medial meniscus
Macrophage
Microglia healing peptide 1 with N-terminal acetylation and C-terminal amidation
Osteoarthritis
Osteoclast
Receptor activator of nuclear factor-kappa B ligand
url https://doi.org/10.1186/s13075-025-03609-5
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