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Nonuniformity in ligaments is a structural strategy for optimizing functionality

Gili R. S. Naveh, Jonathan E. Foster, Tomas M. Silva Santisteban, Xianrui Yang, and Bjorn R. Olsen
PNAS September 4, 2018 115 (36) 9008-9013; published ahead of print August 20, 2018 https://doi.org/10.1073/pnas.1807324115
Gili R. S. Naveh
aDepartment of Developmental Biology, Harvard School of Dental Medicine, Harvard University, Boston, MA 02115;bDepartment of Orthodontics and Craniofacial Orthopedics, School of Dental Medicine, Boston University, Boston, MA 02118;
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  • For correspondence: gili_naveh@hsdm.harvard.edu
Jonathan E. Foster
aDepartment of Developmental Biology, Harvard School of Dental Medicine, Harvard University, Boston, MA 02115;
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Tomas M. Silva Santisteban
cMaterials and Structural Analysis Division, Thermo Fisher Scientific, Houston, TX 77084
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Xianrui Yang
aDepartment of Developmental Biology, Harvard School of Dental Medicine, Harvard University, Boston, MA 02115;
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Bjorn R. Olsen
aDepartment of Developmental Biology, Harvard School of Dental Medicine, Harvard University, Boston, MA 02115;
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  1. Edited by Lia Addadi, Weizmann Institute of Science, Rehovot, Israel, and approved July 26, 2018 (received for review May 8, 2018)

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Significance

Structure and function are intermingled and inseparable. Therefore, the structure–function dependency sequence is mostly unclear. Using the periodontal ligament as a model, employing a technique utilizing a loading system inside a microCT, we were able to visualize in 3D the fresh collagen networks and correlate their distribution and direction with loads exerted on the ligament. We show that the ligament structure is not uniform and is determined before it becomes functional, and therefore we propose that structural nonuniformity is specifically designed to optimize ligament function to the variable forces it sustains.

Abstract

Ligaments serve as compliant connectors between hard tissues. In that role, they function under various load regimes and directions. The 3D structure of ligaments is considered to form as a uniform entity that changes due to function. The periodontal ligament (PDL) connects the tooth to the bone and sustains different types of loads in various directions. Using the PDL as a model, employing a fabricated motorized setup in a microCT, we demonstrate that the fibrous network structure within the PDL is not uniform, even before the tooth becomes functional. Utilizing morphological automated segmentation methods, directionality analysis, as well as second harmonic generation imaging, we find high correlation between blood vessel distribution and fiber density. We also show a structural feature in a form of a dense collar around the neck of the tooth as well as a preferred direction of the fibrous network. Finally, we show that the PDL develops as a nonuniform structure, with an architecture designed to sustain specific types of load in designated areas. Based on these findings, we propose that ligaments in general should be regarded as nonuniform entities, structured already at developmental stages for optimal functioning under variable load regimes.

  • periodontal ligament
  • nonuniformity
  • fiber directionality
  • microCT
  • fiber segmentation

Footnotes

  • ↵1To whom correspondence should be addressed. Email: gili_naveh{at}hsdm.harvard.edu.
  • Author contributions: G.R.S.N. and B.R.O. designed research; G.R.S.N. and X.Y. performed research; G.R.S.N. and T.M.S.S. contributed new reagents/analytic tools; G.R.S.N. and J.E.F. analyzed data; and G.R.S.N., J.E.F., and B.R.O. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1807324115/-/DCSupplemental.

  • Copyright © 2018 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Nonuniformity in ligaments is a structural strategy for optimizing functionality
Gili R. S. Naveh, Jonathan E. Foster, Tomas M. Silva Santisteban, Xianrui Yang, Bjorn R. Olsen
Proceedings of the National Academy of Sciences Sep 2018, 115 (36) 9008-9013; DOI: 10.1073/pnas.1807324115

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Nonuniformity in ligaments is a structural strategy for optimizing functionality
Gili R. S. Naveh, Jonathan E. Foster, Tomas M. Silva Santisteban, Xianrui Yang, Bjorn R. Olsen
Proceedings of the National Academy of Sciences Sep 2018, 115 (36) 9008-9013; DOI: 10.1073/pnas.1807324115
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