Incorporation of Tenascin-C into the Extracellular Matrix by Periostin Underlies an Extracellular Meshwork Architecture

Abstract

Extracellular matrix (ECM) underlies a complicated multicellular architecture that is subjected to significant forces from mechanical environment. Although various components of the ECM have been enumerated, mechanisms that evolve the sophisticated ECM architecture remain to be addressed. Here we show that periostin, a matricellular protein, promotes incorporation of tenascin-C into the ECM and organizes a meshwork architecture of the ECM. We found that both periostin null mice and tenascin-C null mice exhibited a similar phenotype, confined tibial periostitis, which possibly corresponds to medial tibial stress syndrome in human sports injuries. Periostin possessed adjacent domains that bind to tenascin-C and the other ECM protein: fibronectin and type I collagen, respectively. These adjacent domains functioned as a bridge between tenascin-C and the ECM, which increased deposition of tenascin-C on the ECM. The deposition of hexabrachions of tenascin-C may stabilize bifurcations of the ECM fibrils, which is integrated into the extracellular meshwork architecture. This study suggests a role for periostin in adaptation of the ECM architecture in the mechanical environment.

Periostin is required for matricellular localization of CCN3 in periodontal ligament of mice

“…As found presently for CCN3, tenascin-C also interacts with the 4 repeats of the Fas 1 domain (Kii et al 2010). Thus, periostin may promote the appropriate localization of the matricellular proteins by mediating the interaction between these proteins and the extracellular matrix.…”

“…Periostin directly binds to the extracellular matrix proteins (collagen I and fibronectin) via its EMI domain (Kii et al 2010; Fig. 3).…”

“…The HA tag in the pCAGIPuro-periostin-HA (Kii et al 2010) was replaced with the FLAG tag by the standard PCR method. The ΔEMIΔCT-FLAG, CCN3-FLAG, and CCN3-d5-HA expression vectors were newly constructed with the following primers: for ΔEMIΔCT-FLAG, 5′-ACCGAATTCAAGCT…”

NFκB-Induced Periostin Activates Integrin-β3 Signaling to Promote Renal Injury in GN

“…29,30 The ability of periostin to interact and stabilize fibrillar collagens and other extracellular matrix molecules is probably a key event by which periostin controls extracellular matrix deposition and development of fibrosis. [3][4][5] We found de novo expressed periostin to colocalize and interact with integrin-b3 in glomeruli and vascular SMCs of NTS mice. Overexpression of periostin in aortic SMCs induced migration together with increased integrin-b3 expression and FAK phosphorylation.…”

“…1,2 Periostin interacts with extracellular matrix components, including collagen I, tenascin-C, and fibronectin, promoting collagen fibrillogenesis and increased strength performance of the extracellular matrix. [3][4][5] Interaction of periostin with cell-surface integrins avb3 and avb5 has been associated with increased adhesion and migration of cancer cells and vascular smooth muscle cells (SMCs). 6,7 Periostin is highly induced in vitro by TGF-b1, 1,5,8 and it was also found to be upregulated by angiotensin II in cardiac fibroblasts.…”