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Periosteum contains skeletal stem cells with high bone regenerative potential controlled by Periostin

Author

Listed:
  • Oriane Duchamp de Lageneste

    (Paris Descartes University)

  • Anaïs Julien

    (Paris Descartes University)

  • Rana Abou-Khalil

    (Paris Descartes University)

  • Giulia Frangi

    (Paris Descartes University)

  • Caroline Carvalho

    (Paris Descartes University)

  • Nicolas Cagnard

    (Paris-Descartes Bioinformatics Platform)

  • Corinne Cordier

    (Paris Descartes University)

  • Simon J. Conway

    (Indiana University School of Medicine)

  • Céline Colnot

    (Paris Descartes University)

Abstract

Bone regeneration relies on the activation of skeletal stem cells (SSCs) that still remain poorly characterized. Here, we show that periosteum contains SSCs with high bone regenerative potential compared to bone marrow stromal cells/skeletal stem cells (BMSCs) in mice. Although periosteal cells (PCs) and BMSCs are derived from a common embryonic mesenchymal lineage, postnatally PCs exhibit greater clonogenicity, growth and differentiation capacity than BMSCs. During bone repair, PCs can efficiently contribute to cartilage and bone, and integrate long-term after transplantation. Molecular profiling uncovers genes encoding Periostin and other extracellular matrix molecules associated with the enhanced response to injury of PCs. Periostin gene deletion impairs PC functions and fracture consolidation. Periostin-deficient periosteum cannot reconstitute a pool of PCs after injury demonstrating the presence of SSCs within periosteum and the requirement of Periostin in maintaining this pool. Overall our results highlight the importance of analyzing periosteum and PCs to understand bone phenotypes.

Suggested Citation

  • Oriane Duchamp de Lageneste & Anaïs Julien & Rana Abou-Khalil & Giulia Frangi & Caroline Carvalho & Nicolas Cagnard & Corinne Cordier & Simon J. Conway & Céline Colnot, 2018. "Periosteum contains skeletal stem cells with high bone regenerative potential controlled by Periostin," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-03124-z
    DOI: 10.1038/s41467-018-03124-z
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    Cited by:

    1. Xianzhu Zhang & Wei Jiang & Chang Xie & Xinyu Wu & Qian Ren & Fei Wang & Xilin Shen & Yi Hong & Hongwei Wu & Youguo Liao & Yi Zhang & Renjie Liang & Wei Sun & Yuqing Gu & Tao Zhang & Yishan Chen & Wei, 2022. "Msx1+ stem cells recruited by bioactive tissue engineering graft for bone regeneration," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Masayuki Tsukasaki & Noriko Komatsu & Takako Negishi-Koga & Nam Cong-Nhat Huynh & Ryunosuke Muro & Yutaro Ando & Yuka Seki & Asuka Terashima & Warunee Pluemsakunthai & Takeshi Nitta & Takashi Nakamura, 2022. "Periosteal stem cells control growth plate stem cells during postnatal skeletal growth," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Chujiao Lin & Qiyuan Yang & Dongsheng Guo & Jun Xie & Yeon-Suk Yang & Sachin Chaugule & Ngoc DeSouza & Won-Taek Oh & Rui Li & Zhihao Chen & Aijaz A. John & Qiang Qiu & Lihua Julie Zhu & Matthew B. Gre, 2022. "Impaired mitochondrial oxidative metabolism in skeletal progenitor cells leads to musculoskeletal disintegration," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Lan Zhao & Yumei Lai & Hongli Jiao & Jian Huang, 2024. "Nerve growth factor receptor limits inflammation to promote remodeling and repair of osteoarthritic joints," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Yuki Matsushita & Jialin Liu & Angel Ka Yan Chu & Chiaki Tsutsumi-Arai & Mizuki Nagata & Yuki Arai & Wanida Ono & Kouhei Yamamoto & Thomas L. Saunders & Joshua D. Welch & Noriaki Ono, 2023. "Bone marrow endosteal stem cells dictate active osteogenesis and aggressive tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-23, December.

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