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 Conway, Jeffery D. Molkentin, Gabor ForgacsRoger R. Markwald

Research output: Contribution to journalArticle

357 Citations (Scopus)

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

Fingerprint

Connective Tissue
Collagen
Tissue
Transmission Electron Microscopy
Knockout Mice
Skin
Transmission electron microscopy
Periodontal Ligament
Mechanical Stress
Ligaments
Heart Valves
Tendons
Differential Scanning Calorimetry
Dermis
Immunoprecipitation
Cornea
Differential scanning calorimetry
Genes
Experiments
Temperature

Keywords

  • Collagen
  • Connective tissues
  • Fasciclin
  • Fibrillogenesis
  • Periostin

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology

Cite this

Morris, R. A., Damon, B., Mironov, V., Kasyanov, V., Ramamurthi, A., Moreno-Rodriguez, R., ... 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

Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. / Morris, Russell A.; Damon, Brook; Mironov, Vladimir; Kasyanov, Vladimir; Ramamurthi, Anand; Moreno-Rodriguez, Ricardo; Trusk, Thomas; Potts, Jay D.; Goodwin, Richard L.; Davis, Jeff; Hoffman, Stanley; Wen, Xuejun; Sugi, Yukiko; Kern, Christine B.; Mjaatvedt, Corey H.; Turner, Debi K.; Oka, Toru; Conway, Simon; Molkentin, Jeffery D.; Forgacs, Gabor; Markwald, Roger R.

In: Journal of Cellular Biochemistry, Vol. 101, No. 3, 01.06.2007, p. 695-711.

Research output: Contribution to journalArticle

Morris, RA, Damon, B, Mironov, V, Kasyanov, V, Ramamurthi, A, Moreno-Rodriguez, R, Trusk, T, Potts, JD, Goodwin, RL, Davis, J, Hoffman, S, Wen, X, Sugi, Y, Kern, CB, Mjaatvedt, CH, Turner, DK, Oka, T, Conway, S, Molkentin, JD, Forgacs, G & Markwald, RR 2007, 'Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues', Journal of Cellular Biochemistry, vol. 101, no. 3, pp. 695-711. https://doi.org/10.1002/jcb.21224
Morris RA, Damon B, Mironov V, Kasyanov V, Ramamurthi A, Moreno-Rodriguez R et al. Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. Journal of Cellular Biochemistry. 2007 Jun 1;101(3):695-711. https://doi.org/10.1002/jcb.21224
Morris, Russell A. ; Damon, Brook ; Mironov, Vladimir ; Kasyanov, Vladimir ; Ramamurthi, Anand ; Moreno-Rodriguez, Ricardo ; Trusk, Thomas ; Potts, Jay D. ; Goodwin, Richard L. ; Davis, Jeff ; Hoffman, Stanley ; Wen, Xuejun ; Sugi, Yukiko ; Kern, Christine B. ; Mjaatvedt, Corey H. ; Turner, Debi K. ; Oka, Toru ; Conway, Simon ; Molkentin, Jeffery D. ; Forgacs, Gabor ; Markwald, Roger R. / Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. In: Journal of Cellular Biochemistry. 2007 ; Vol. 101, No. 3. pp. 695-711.
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