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Intrinsic and growth-mediated cell and matrix specialization during meniscus tissue assembly

View ORCID ProfileTonia K. Tsinman, Xi Jiang, Lin Han, View ORCID ProfileEiki Koyama, View ORCID ProfileRobert L. Mauck, View ORCID ProfileNathaniel A. Dyment
doi: https://doi.org/10.1101/2021.02.20.432114
Tonia K. Tsinman
1McKay Orthopaedic Research Laboratory, Department of Orthopaedic Surgery Perelman School of Medicine, University of Pennsylvania Philadelphia, PA 19104
2Department of Bioengineering, University of Pennsylvania Philadelphia, PA 19104
3Translational Musculoskeletal Research Center, Corporal Michael Crescenz VA Medical Center Philadelphia, PA 19104
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Xi Jiang
1McKay Orthopaedic Research Laboratory, Department of Orthopaedic Surgery Perelman School of Medicine, University of Pennsylvania Philadelphia, PA 19104
2Department of Bioengineering, University of Pennsylvania Philadelphia, PA 19104
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Lin Han
4School of Biomedical Engineering, Science and Health Systems, Drexel University Philadelphia, PA 19104
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Eiki Koyama
5Translational Research Program in Pediatric Orthopaedics, Children’s Hospital of Philadelphia, Division of Orthopaedic Surgery, Department of Surgery Philadelphia, PA 19104
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Robert L. Mauck
1McKay Orthopaedic Research Laboratory, Department of Orthopaedic Surgery Perelman School of Medicine, University of Pennsylvania Philadelphia, PA 19104
2Department of Bioengineering, University of Pennsylvania Philadelphia, PA 19104
3Translational Musculoskeletal Research Center, Corporal Michael Crescenz VA Medical Center Philadelphia, PA 19104
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  • For correspondence: dyment@pennmedicine.upenn.edu lemauck@pennmedicine.upenn.edu
Nathaniel A. Dyment
1McKay Orthopaedic Research Laboratory, Department of Orthopaedic Surgery Perelman School of Medicine, University of Pennsylvania Philadelphia, PA 19104
2Department of Bioengineering, University of Pennsylvania Philadelphia, PA 19104
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  • For correspondence: dyment@pennmedicine.upenn.edu lemauck@pennmedicine.upenn.edu
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ABSTRACT

The incredible mechanical strength and durability of mature fibrous tissues and their extremely limited turnover and regenerative capacity underscores the importance of proper matrix assembly during early postnatal growth. In tissues with composite extracellular matrix (ECM) structures, such as the adult knee meniscus, fibrous (Collagen-I rich) and cartilaginous (Collagen-II, proteoglycan-rich) matrix components are regionally segregated to the outer and inner portions of the tissue. While this spatial variation in composition is appreciated to be functionally important for resisting complex mechanical loads associated with gait, the establishment of these specialized zones is poorly understood. To address this issue, the following study tracked the growth of the murine meniscus from its embryonic formation through its first month of growth, encompassing the critical time-window during which animals begin to ambulate and weight bear. Using histological analysis, region specific high-throughput qPCR, and Col-1 and Col-2 fluorescent reporter mice, we found that matrix and cellular features defining specific tissue zones were already present at birth, before continuous weight-bearing had occurred. These differences were further refined with postnatal growth and maturation, resulting in specialization of mature tissue regions. Taken together, this work establishes a detailed timeline of the concurrent spatiotemporal changes that occur at both the cellular and matrix level throughout meniscus maturation. The findings of this study provide a framework for investigating the reciprocal feedback between cells and their evolving microenvironments during assembly of a mechanically robust fibrocartilage tissue, thus providing insight into mechanisms of tissue degeneration and effective regenerative strategies.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 21, 2021.
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Intrinsic and growth-mediated cell and matrix specialization during meniscus tissue assembly
Tonia K. Tsinman, Xi Jiang, Lin Han, Eiki Koyama, Robert L. Mauck, Nathaniel A. Dyment
bioRxiv 2021.02.20.432114; doi: https://doi.org/10.1101/2021.02.20.432114
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Intrinsic and growth-mediated cell and matrix specialization during meniscus tissue assembly
Tonia K. Tsinman, Xi Jiang, Lin Han, Eiki Koyama, Robert L. Mauck, Nathaniel A. Dyment
bioRxiv 2021.02.20.432114; doi: https://doi.org/10.1101/2021.02.20.432114

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