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Osteoblast-derived vesicles induce a switch from bone-formation to bone-resorption in vivo

Author

Listed:
  • Maki Uenaka

    (Osaka University)

  • Erika Yamashita

    (Osaka University)

  • Junichi Kikuta

    (Osaka University
    Osaka University
    Health and Nutrition)

  • Akito Morimoto

    (Osaka University)

  • Tomoka Ao

    (Osaka University
    Health and Nutrition)

  • Hiroki Mizuno

    (Osaka University
    Osaka University)

  • Masayuki Furuya

    (Osaka University)

  • Tetsuo Hasegawa

    (Osaka University)

  • Hiroyuki Tsukazaki

    (Osaka University)

  • Takao Sudo

    (Osaka University
    Osaka University)

  • Keizo Nishikawa

    (Osaka University
    Osaka University)

  • Daisuke Okuzaki

    (Osaka University)

  • Daisuke Motooka

    (Osaka University)

  • Nobuyoshi Kosaka

    (Tokyo Medical University)

  • Fuminori Sugihara

    (Osaka University)

  • Thomas Boettger

    (Max-Plank-Institute for Heart and Lung Research)

  • Thomas Braun

    (Max-Plank-Institute for Heart and Lung Research)

  • Takahiro Ochiya

    (Tokyo Medical University)

  • Masaru Ishii

    (Osaka University
    Osaka University
    Health and Nutrition)

Abstract

Bone metabolism is regulated by the cooperative activity between bone-forming osteoblasts and bone-resorbing osteoclasts. However, the mechanisms mediating the switch between the osteoblastic and osteoclastic phases have not been fully elucidated. Here, we identify a specific subset of mature osteoblast-derived extracellular vesicles that inhibit bone formation and enhance osteoclastogenesis. Intravital imaging reveals that mature osteoblasts secrete and capture extracellular vesicles, referred to as small osteoblast vesicles (SOVs). Co-culture experiments demonstrate that SOVs suppress osteoblast differentiation and enhance the expression of receptor activator of NF-κB ligand, thereby inducing osteoclast differentiation. We also elucidate that the SOV-enriched microRNA miR-143 inhibits Runt-related transcription factor 2, a master regulator of osteoblastogenesis, by targeting the mRNA expression of its dimerization partner, core-binding factor β. In summary, we identify SOVs as a mode of cell-to-cell communication, controlling the dynamic transition from bone-forming to bone-resorbing phases in vivo.

Suggested Citation

  • Maki Uenaka & Erika Yamashita & Junichi Kikuta & Akito Morimoto & Tomoka Ao & Hiroki Mizuno & Masayuki Furuya & Tetsuo Hasegawa & Hiroyuki Tsukazaki & Takao Sudo & Keizo Nishikawa & Daisuke Okuzaki & , 2022. "Osteoblast-derived vesicles induce a switch from bone-formation to bone-resorption in vivo," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28673-2
    DOI: 10.1038/s41467-022-28673-2
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    References listed on IDEAS

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    1. Yuki Ikebuchi & Shigeki Aoki & Masashi Honma & Madoka Hayashi & Yasutaka Sugamori & Masud Khan & Yoshiaki Kariya & Genki Kato & Yasuhiko Tabata & Josef M. Penninger & Nobuyuki Udagawa & Kazuhiro Aoki , 2018. "Coupling of bone resorption and formation by RANKL reverse signalling," Nature, Nature, vol. 561(7722), pages 195-200, September.
    2. Mikihito Hayashi & Tomoki Nakashima & Masahiko Taniguchi & Tatsuhiko Kodama & Atsushi Kumanogoh & Hiroshi Takayanagi, 2012. "Osteoprotection by semaphorin 3A," Nature, Nature, vol. 485(7396), pages 69-74, May.
    3. Masaru Ishii & Jackson G. Egen & Frederick Klauschen & Martin Meier-Schellersheim & Yukihiko Saeki & Jean Vacher & Richard L. Proia & Ronald N. Germain, 2009. "Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis," Nature, Nature, vol. 458(7237), pages 524-528, March.
    4. Masayuki Furuya & Junichi Kikuta & Sayumi Fujimori & Shigeto Seno & Hiroki Maeda & Mai Shirazaki & Maki Uenaka & Hiroki Mizuno & Yoriko Iwamoto & Akito Morimoto & Kunihiko Hashimoto & Takeshi Ito & Yu, 2018. "Direct cell–cell contact between mature osteoblasts and osteoclasts dynamically controls their functions in vivo," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
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    Cited by:

    1. Yongkuk Park & Tadatoshi Sato & Jungwoo Lee, 2023. "Functional and analytical recapitulation of osteoclast biology on demineralized bone paper," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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