Collagen fibril morphology and organization: Implications for force transmission in ligament and tendon

Paolo P. Provenzano, Ray Vanderby

Research output: Contribution to journalArticlepeer-review

227 Scopus citations

Abstract

Connective tissue mechanical behavior is primarily determined by the composition and organization of collagen. In ligaments and tendons, type I collagen is the principal structural element of the extracellular matrix, which acts to transmit force between bones or bone and muscle, respectively. Therefore, characterization of collagen fibril morphology and organization in fetal and skeletally mature animals is essential to understanding how tissues develop and obtain their mechanical attributes. In this study, tendons and ligaments from fetal rat, bovine, and feline, and mature rat were examined with scanning electron microscopy. At early fetal developmental stages, collagen fibrils show fibril overlap and interweaving, apparent fibril ends, and numerous bifurcating/fusing fibrils. Late in fetal development, collagen fibril ends are still present and fibril bundles (fibers) are clearly visible. Examination of collagen fibrils from skeletally mature tissues, reveals highly organized regions but still include fibril interweaving, and regions that are more randomly organized. Fibril bifurcations/fusions are still present in mature tissues but are less numerous than in fetal tissue. To address the continuity of fibrils in mature tissues, fibrils were examined in individual micrographs and consecutive overlaid micrographs. Extensive microscopic analysis of mature tendons and ligaments detected no fibril ends. These data strongly suggest that fibrils in mature ligament and tendon are either continuous or functionally continuous. Based upon this information and published data, we conclude that force within these tissues is directly transferred through collagen fibrils and not through an interfibrillar coupling, such as a proteoglycan bridge.

Original languageEnglish (US)
Pages (from-to)71-84
Number of pages14
JournalMatrix Biology
Volume25
Issue number2
DOIs
StatePublished - Mar 2006

Bibliographical note

Funding Information:
This work was funded in part through grants from N.A.S.A. (NAG9-1152), the N.S.F. (CMS9907977), and the NIH (AR49466). The authors thank the Materials Science Center for access to the scanning electron microscope, Rick Noll for technical assistance with the microscope, Phil Oshel for technical assistance with specimen preparation, and Dr. Kei Hayashi for helping obtain fetal animals.

Keywords

  • Cell-matrix interaction
  • Extracellular matrix
  • Scanning electron microscopy
  • Structure-function
  • Three-dimensional matrix organization

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