Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues

Russell A. Morris, Brook Damon, Vladimir Mironov, Vladimir Kasyanov, Anand Ramamurthi, Ricardo Moreno-Rodriguez, Thomas Trusk, Jay D. Potts, Richard L. Goodwin, Jeff Davis, Stanley Hoffman, Xuejun Wen, Yukiko Sugi, Christine B. Kern, Corey H. Mjaatvedt, Debi K. Turner, Toru Oka, Simon J. Conway, Jeffery D. Molkentin, Gabor ForgacsRoger R. Markwald

Research output: Contribution to journalArticle

380 Scopus citations

Abstract

Periostin is predominantly expressed in collagen-rich fibrous connective tissues that are subjected to constant mechanical stresses including: heart valves, tendons, perichondrium, cornea, and the periodontal ligament (PDL). Based on these data we hypothesize that periostin can regulate collagen I fibrillogenesis and thereby affect the biomechanical properties of connective tissues. Immunoprecipitation and immunogold transmission electron microscopy experiments demonstrate that periostin is capable of directly interacting with collagen I. To analyze the potential role of periostin in collagen I fibrillogenesis, gene targeted mice were generated. Transmission electron microscopy and morphometric analyses demonstrated reduced collagen fibril diameters in skin dermis of periostin knockout mice, an indication of aberrant collagen I fibrillogenesis. In addition, differential scanning calorimetry (DSC) demonstrated a lower collagen denaturing temperature in periostin knockout mice, reflecting a reduced level of collagen cross-linking. Functional biomechanical properties of periostin null skin specimens and atrioventricular (AV) valve explant experiments provided direct evidence of the role that periostin plays in regulating the viscoelastic properties of connective tissues. Collectively, these data demonstrate for the first time that periostin can regulate collagen I fibrillogenesis and thereby serves as an important mediator of the biomechanical properties of fibrous connective tissues.

Original languageEnglish (US)
Pages (from-to)695-711
Number of pages17
JournalJournal of Cellular Biochemistry
Volume101
Issue number3
DOIs
StatePublished - Jun 1 2007

Keywords

  • Collagen
  • Connective tissues
  • Fasciclin
  • Fibrillogenesis
  • Periostin

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology

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  • Cite this

    Morris, R. A., Damon, B., Mironov, V., Kasyanov, V., Ramamurthi, A., Moreno-Rodriguez, R., Trusk, T., Potts, J. D., Goodwin, R. L., Davis, J., Hoffman, S., Wen, X., Sugi, Y., Kern, C. B., Mjaatvedt, C. H., Turner, D. K., Oka, T., Conway, S. J., Molkentin, J. D., ... Markwald, R. R. (2007). Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. Journal of Cellular Biochemistry, 101(3), 695-711. https://doi.org/10.1002/jcb.21224