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Review
. 2011 Oct;68(19):3201-7.
doi: 10.1007/s00018-011-0784-5. Epub 2011 Aug 11.

Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell

Akira Kudo  1
Affiliations
Review

Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell

Akira Kudo. Cell Mol Life Sci. 2011 Oct.

Abstract

More than 10 years have passed since the naming of periostin derived from its expression sites in the periosteum and periodontal ligament. Following this finding, we have accumulated more data on the expression patterns of periostin, and, finally, with the generation of periostin-deficient mice, have revealed functions of periostin in the regeneration of tissues in bone, tooth, heart, and skin, and its action in cancer invasion. Since periostin is a matricellular protein, the first investigation of periostin function showed its enhancement of cell migration by acting outside the cell. On the other hand, recent observations have demonstrated that periostin functions in fibrillogenesis in association with extracellular matrix molecules inside the cell.

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Figures

Fig. 1
Fig. 1
Properties of periostin protein. Periostin is a 90-kDa secreted protein, and its expression is induced by TGFβ. The protein structure of periostin comprises an amino-terminal EMI domain, a tandem repeat of 4 fas1 domains, and a carboxyl-terminal domain. From conservation of the typical fas 1 domains, we characterized periostin as being a member of the fasciclin I family, which includes βigh3 and Drosophila fasciclin I. Periostin domains have the following characteristics: the EMI domain binds to type I collagen, fibronectin, and Notch1; and the Fas I domains bind to tenascin-C and BMP-1. The C-terminal domain gives rise to splice variants and contains proteolytic cleavage sites
Fig. 2
Fig. 2
Assembly between fibronectin and tenascin-C by periostin. Cleavage of the C-terminal end of perostin, including the heparin-binding site (pink), can induce association of the truncated periostin with tenascin-C via the fas I domains of periostin. Fibronectin is associated with periostin at the EMI domain of the latter, and with tenascin-c to form the specific hexabrachion structure, which behaves as a scaffold, in which tenascin-C forms a disulfide-linked hexamer (blue) that binds to the dimer form of fibronectin (red) via periostin
Fig. 3
Fig. 3
Periostin function in collagen cross-link formation. Periostin recruits BMP-1 onto the fibronectin matrix to enhance LOX activity for collagen cross-linkage [13]
Fig. 4
Fig. 4
Mechanistic view of periostin functions. Inflammation or mechanical stress induces the expression of TGFβ and/or IL-4 and IL-13 in macrophages and neutrophils (for inflammation) or in other types of cells (for mechanical stress). These cytokines then induce the expression of periostin as well as that of other ECM molecules such as fibronectin and tenascin-C in fibroblasts, which proteins are mainly splice variants, by acting through transcription factors such as twist and c-fos. The splice variant of periostin is secreted and localized outside the cell in the ECM, where it interacts with integrin αvβ3 on myofibroblasts to induce their cell migration through downstream signals of Akt and FAK phosphorylation. These myofibroblasts produce type I collagen to repair tissues. In this collagen production, periostin together with tenascin-C inside the cell forms a meshwork structure with fibronectin to constitute a scaffold for the cross-linking of type I collagen. This cross-linking is effected by periostin in association with BMP-1 to activate lysyl oxidase (LOX) for enhancement of cross-linking activity inside the cells. During tissue repair, periostin helps in the secretion of MMP-9 and expression of Notch1 on the cell surface
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