Skip to main content
SpringerLink
Log in

Periostin in Bone Regeneration

  • Chapter
  • First Online:
Periostin

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1132))

Abstract

Bone regeneration is an efficient regenerative process depending on the recruitment and activation of skeletal stem cells that allow cartilage and bone formation leading to fracture consolidation. Periosteum, the tissue located at the outer surface of bone is now recognized as an essential player in the bone repair process and contains skeletal stem cells with high regenerative potential. The matrix composition of the periosteum defines its roles in bone growth, in cortical bone modeling and remodeling in response to mechanical strain, and in bone repair. Periostin is a key extracellular matrix component of the periosteum involved in periosteum functions. In this chapter, we summarize the current knowledge on the bone regeneration process, the role of the periosteum and skeletal stem cells, and Periostin functions in this context. The matricellular protein Periostin has several roles through all stages of bone repair: in the early days of repair during the initial activation of stem cells within periosteum, in the active phase of cartilage and bone deposition in the facture callus, and in the final phase of bone bridging and reconstitution of the stem cell pool within periosteum.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Claes L, Recknagel S, Ignatius A (2012) Fracture healing under healthy and inflammatory conditions. Nat Rev Rheumatol 8:133–143

    Article  CAS  Google Scholar 

  2. Thompson Z, Miclau T, Hu D, Helms JA (2002) A model for intramembranous ossification during fracture healing. J Orthop Res 20:1091–1098

    Article  CAS  Google Scholar 

  3. Miclau T et al (2007) Effects of delayed stabilization on fracture healing. J Orthop Res 25:1552–1558

    Article  Google Scholar 

  4. Colnot C, Zhang X, Knothe Tate ML (2012) Current insights on the regenerative potential of the periosteum: molecular, cellular, and endogenous engineering approaches. J Orthop Res 30:1869–1878

    Article  CAS  Google Scholar 

  5. Ferretti C, Mattioli-Belmonte M (2014) Periosteum derived stem cells for regenerative medicine proposals: boosting current knowledge. World J Stem Cells 6:266–277

    Article  Google Scholar 

  6. Roberts SJ, van Gastel N, Carmeliet G, Luyten FP (2015) Uncovering the periosteum for skeletal regeneration: the stem cell that lies beneath. Bone 70:10–18

    Article  Google Scholar 

  7. Duhamel HL (1742) Sur le développement et la crue des os des animaux. Acad Roy des Sci Paris Mém 55:354–357

    Google Scholar 

  8. Dupuytren G (1847) On the injuries and diseases of bone. The Sydenham Society, London

    Google Scholar 

  9. Takeshita S, Kikuno R, Tezuka K, Amann E (1993) Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J 294(Pt 1):271–278

    Article  CAS  Google Scholar 

  10. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G (1997) Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89:747–754

    Article  CAS  Google Scholar 

  11. Horiuchi K et al (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14:1239–1249

    Article  CAS  Google Scholar 

  12. Bonnet N, Garnero P, Ferrari S (2016) Periostin action in bone. Mol Cell Endocrinol 432:75–82

    Article  CAS  Google Scholar 

  13. Dimitriou R, Tsiridis E, Giannoudis PV (2005) Current concepts of molecular aspects of bone healing. Injury 36:1392–1404

    Article  Google Scholar 

  14. Einhorn TA, Gerstenfeld LC (2015) Fracture healing: mechanisms and interventions. Nat Rev Rheumatol 11:45–54

    Article  Google Scholar 

  15. Mountziaris PM, Mikos AG (2008) Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng Part B Rev 14:179–186

    Article  CAS  Google Scholar 

  16. Kon T et al (2001) Expression of osteoprotegerin, receptor activator of NF-kappaB ligand (osteoprotegerin ligand) and related proinflammatory cytokines during fracture healing. J Bone Miner Res 16:1004–1014

    Article  CAS  Google Scholar 

  17. Xing Z et al (2010) Multiple roles for CCR2 during fracture healing. Dis Model Mech 3:451–458

    Article  CAS  Google Scholar 

  18. Al-Sebaei MO et al (2014) Role of Fas and Treg cells in fracture healing as characterized in the fas-deficient (lpr) mouse model of lupus. J Bone Miner Res 29:1478–1491

    Article  CAS  Google Scholar 

  19. Wallace A, Cooney TE, Englund R, Lubahn JD (2011) Effects of interleukin-6 ablation on fracture healing in mice. J Orthop Res 29:1437–1442

    Article  CAS  Google Scholar 

  20. Yang X et al (2007) Callus mineralization and maturation are delayed during fracture healing in interleukin-6 knockout mice. Bone 41:928–936

    Article  CAS  Google Scholar 

  21. Nam D et al (2012) T-lymphocytes enable osteoblast maturation via IL-17F during the early phase of fracture repair. PLoS One 7:e40044

    Article  CAS  Google Scholar 

  22. Gerstenfeld LC et al (2003) Impaired fracture healing in the absence of TNF-alpha signaling: the role of TNF-alpha in endochondral cartilage resorption. J Bone Miner Res 18:1584–1592

    Article  CAS  Google Scholar 

  23. Gerstenfeld LC, Cullinane DM, Barnes GL, Graves DT, Einhorn TA (2003) Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J Cell Biochem 88:873–884

    Article  CAS  Google Scholar 

  24. Motsitsi NS (2008) Management of infected nonunion of long bones: the last decade (1996-2006). Injury 39:155–160

    Article  CAS  Google Scholar 

  25. Barnes GL, Kostenuik PJ, Gerstenfeld LC, Einhorn TA (1999) Growth factor regulation of fracture repair. J Bone Miner Res 14:1805–1815

    Article  CAS  Google Scholar 

  26. Bahney CS et al (2014) Stem cell-derived endochondral cartilage stimulates bone healing by tissue transformation. J Bone Miner Res 29:1269–1282

    Article  CAS  Google Scholar 

  27. Hu DP et al (2017) Cartilage to bone transformation during fracture healing is coordinated by the invading vasculature and induction of the core pluripotency genes. Development 144:221–234

    Article  CAS  Google Scholar 

  28. Park J et al (2015) Dual pathways to endochondral osteoblasts: a novel chondrocyte-derived osteoprogenitor cell identified in hypertrophic cartilage. Biol Open 4:608–621

    Article  CAS  Google Scholar 

  29. Yang L, Tsang KY, Tang HC, Chan D, Cheah KS (2014) Hypertrophic chondrocytes can become osteoblasts and osteocytes in endochondral bone formation. Proc Natl Acad Sci U S A 111:12097–12102

    Article  CAS  Google Scholar 

  30. Zhou X et al (2014) Chondrocytes transdifferentiate into osteoblasts in endochondral bone during development, postnatal growth and fracture healing in mice. PLoS Genet 10:e1004820

    Article  Google Scholar 

  31. Behonick DJ et al (2007) Role of matrix metalloproteinase 13 in both endochondral and intramembranous ossification during skeletal regeneration. PLoS One 2:e1150

    Article  Google Scholar 

  32. Colnot C, Thompson Z, Miclau T, Werb Z, Helms JA (2003) Altered fracture repair in the absence of MMP9. Development 130:4123–4133

    Article  CAS  Google Scholar 

  33. Benjamin M et al (2006) Where tendons and ligaments meet bone: attachment sites (‘entheses’) in relation to exercise and/or mechanical load. J Anat 208:471–490

    Article  CAS  Google Scholar 

  34. Allen MR, Hock JM, Burr DB (2004) Periosteum: biology, regulation, and response to osteoporosis therapies. Bone 35:1003–1012

    Article  CAS  Google Scholar 

  35. Chang H, Knothe Tate ML (2012) Concise review: the periosteum: tapping into a reservoir of clinically useful progenitor cells. Stem Cells Transl Med 1:480–491

    Article  CAS  Google Scholar 

  36. Hohmann EL, Elde RP, Rysavy JA, Einzig S, Gebhard RL (1986) Innervation of periosteum and bone by sympathetic vasoactive intestinal peptide-containing nerve fibers. Science 232:868–871

    Article  CAS  Google Scholar 

  37. Chanavaz M (1995) Anatomy and histophysiology of the periosteum: quantification of the periosteal blood supply to the adjacent bone with 85Sr and gamma spectrometry. J Oral Implantol 21:214–219

    CAS  PubMed  Google Scholar 

  38. Garcia-Castellano JM, Diaz-Herrera P, Morcuende JA (2000) Is bone a target-tissue for the nervous system? New advances on the understanding of their interactions. Iowa Orthop J 20:49–58

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Kearney CJ, Lee JY, Padera RF, Hsu HP, Spector M (2011) Extracorporeal shock wave-induced proliferation of periosteal cells. J Orthop Res 29:1536–1543

    Article  Google Scholar 

  40. Pead MJ, Skerry TM, Lanyon LE (1988) Direct transformation from quiescence to bone formation in the adult periosteum following a single brief period of bone loading. J Bone Miner Res 3:647–656

    Article  CAS  Google Scholar 

  41. Raab-Cullen DM, Thiede MA, Petersen DN, Kimmel DB, Recker RR (1994) Mechanical loading stimulates rapid changes in periosteal gene expression. Calcif Tissue Int 55:473–478

    Article  CAS  Google Scholar 

  42. Simon TM, Van Sickle DC, Kunishima DH, Jackson DW (2003) Cambium cell stimulation from surgical release of the periosteum. J Orthop Res 21:470–480

    Article  Google Scholar 

  43. Utvag SE, Grundnes O, Reikeraos O (1996) Effects of periosteal stripping on healing of segmental fractures in rats. J Orthop Trauma 10:279–284

    Article  CAS  Google Scholar 

  44. Ozaki A, Tsunoda M, Kinoshita S, Saura R (2000) Role of fracture hematoma and periosteum during fracture healing in rats: interaction of fracture hematoma and the periosteum in the initial step of the healing process. J Orthop Sci 5:64–70

    Article  CAS  Google Scholar 

  45. Zhang X et al (2005) Periosteal stem cells are essential for bone revitalization and repair. J Musculoskelet Neuronal Interact 5:360–362

    CAS  PubMed  Google Scholar 

  46. Zhang X et al (2005) Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. J Bone Miner Res 20:2124–2137

    Article  CAS  Google Scholar 

  47. Colnot C (2009) Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J Bone Miner Res 24:274–282

    Article  Google Scholar 

  48. Lu C et al (2005) Cellular basis for age-related changes in fracture repair. J Orthop Res 23:1300–1307

    Article  CAS  Google Scholar 

  49. Sacchetti B et al (2007) Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131:324–336

    Article  CAS  Google Scholar 

  50. Granero-Molto F et al (2009) Regenerative effects of transplanted mesenchymal stem cells in fracture healing. Stem Cells 27:1887–1898

    Article  CAS  Google Scholar 

  51. Fernandes MB et al (2014) The effect of bone allografts combined with bone marrow stromal cells on the healing of segmental bone defects in a sheep model. BMC Vet Res 10:36

    Article  Google Scholar 

  52. Mizoguchi T et al (2014) Osterix marks distinct waves of primitive and definitive stromal progenitors during bone marrow development. Dev Cell 29:340–349

    Article  CAS  Google Scholar 

  53. Worthley DL et al (2015) Gremlin 1 identifies a skeletal stem cell with bone, cartilage, and reticular stromal potential. Cell 160:269–284

    Article  CAS  Google Scholar 

  54. Zhou BO, Yue R, Murphy MM, Peyer JG, Morrison SJ (2014) Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell 15:154–168

    Article  CAS  Google Scholar 

  55. Duchamp de Lageneste O et al (2018) Periosteum contains skeletal stem cells with high bone regenerative potential controlled by Periostin. Nat Commun 9:773

    Article  Google Scholar 

  56. Nakazawa T et al (2004) Gene expression of periostin in the early stage of fracture healing detected by cDNA microarray analysis. J Orthop Res 22:520–525

    Article  CAS  Google Scholar 

  57. Hirakawa K et al (1994) Localization of the mRNA for bone matrix proteins during fracture healing as determined by in situ hybridization. J Bone Miner Res 9:1551–1557

    Article  CAS  Google Scholar 

  58. Kawaguchi H et al (1994) Stimulation of fracture repair by recombinant human basic fibroblast growth factor in Normal and Streptozotocin-diabetic rats. Endocrinology 135:774–781

    Article  CAS  Google Scholar 

  59. Bornstein P (2009) Matricellular proteins: an overview. J Cell Commun Signal 3:163–165

    Article  Google Scholar 

  60. Litvin J et al (2004) Expression and function of periostin-isoforms in bone. J Cell Biochem 92:1044–1061

    Article  CAS  Google Scholar 

  61. Kruzynska-Frejtag A et al (2004) Periostin is expressed within the developing teeth at the sites of epithelial-mesenchymal interaction. Dev Dyn 229:857–868

    Article  CAS  Google Scholar 

  62. Zhu S et al (2008) Immunolocalization of Periostin-like factor and Periostin during embryogenesis. J Histochem Cytochem 56:329–345

    Article  CAS  Google Scholar 

  63. Murphy-Ullrich JE, Sage EH (2014) Revisiting the matricellular concept. Matrix Biol 37:1–14

    Article  CAS  Google Scholar 

  64. Alford AI, Hankenson KD (2006) Matricellular proteins: extracellular modulators of bone development, remodeling, and regeneration. Bone 38:749–757

    Article  CAS  Google Scholar 

  65. Rios H et al (2005) Periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol 25:11131–11144

    Article  CAS  Google Scholar 

  66. Cobo T et al (2016) Role of Periostin in adhesion and migration of bone remodeling cells. PLoS One 11:e0147837

    Article  Google Scholar 

  67. Sonnenberg-Riethmacher E, Miehe M, Riethmacher D (2015) Promotion of periostin expression contributes to the migration of Schwann cells. J Cell Sci 128:3345–3355

    Article  CAS  Google Scholar 

  68. Heo SC et al (2011) Periostin mediates human adipose tissue-derived mesenchymal stem cell-stimulated tumor growth in a xenograft lung adenocarcinoma model. Biochim Biophys Acta 1813:2061–2070

    Article  CAS  Google Scholar 

  69. Matsuzawa M et al (2015) Periostin of human periodontal ligament fibroblasts promotes migration of human mesenchymal stem cell through the alphavbeta3 integrin/FAK/PI3K/Akt pathway. J Periodontal Res 50:855–863

    Article  CAS  Google Scholar 

  70. Naik PK et al (2012) Periostin promotes fibrosis and predicts progression in patients with idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 303:L1046–L1056

    Article  CAS  Google Scholar 

  71. Takayama G et al (2006) Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J Allergy Clin Immunol 118:98–104

    Article  CAS  Google Scholar 

  72. O’Driscoll SW, Saris DB, Ito Y, Fitzimmons JS (2001) The chondrogenic potential of periosteum decreases with age. J Orthop Res 19:95–103

    Article  Google Scholar 

  73. Ferretti C et al (2015) Human periosteal derived stem cell potential: the impact of age. Stem Cell Rev 11(3):487–500

    Article  CAS  Google Scholar 

  74. Zhang F et al (2017) Periostin upregulates Wnt/beta-catenin signaling to promote the osteogenesis of CTLA4-modified human bone marrow-mesenchymal stem cells. Sci Rep 7:41634

    Article  CAS  Google Scholar 

  75. Bonnet N, Conway SJ, Ferrari SL (2012) Regulation of beta catenin signaling and parathyroid hormone anabolic effects in bone by the matricellular protein periostin. Proc Natl Acad Sci U S A 109:15048–15053

    Article  CAS  Google Scholar 

  76. Robinson JA et al (2006) Wnt/beta-catenin signaling is a normal physiological response to mechanical loading in bone. J Biol Chem 281:31720–31728

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work is supported by Osteosynthesis and Trauma Care Foundation, ANR-13-BSV1-001, ANR-18-CE14-0033 and NIH R01AR072707.

Author information

Authors and Affiliations

  1. INSERM UMR1163, Imagine Institute, Paris Descartes University, Paris, France

    Oriane Duchamp de Lageneste & Céline Colnot

Authors
  1. Oriane Duchamp de Lageneste
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Céline Colnot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Céline Colnot .

Editor information

Editors and Affiliations

  1. International Frontier, Tokyo Institute of Technology, Tokyo, Japan

    Akira Kudo

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Duchamp de Lageneste, O., Colnot, C. (2019). Periostin in Bone Regeneration. In: Kudo, A. (eds) Periostin. Advances in Experimental Medicine and Biology, vol 1132. Springer, Singapore. https://doi.org/10.1007/978-981-13-6657-4_6

Download citation

Publish with us

Policies and ethics

Search

Navigation