Architecture of the osteocyte network correlates with bone material quality

Authors

  • Michael Kerschnitzki,

    1. Max Planck Institute of Colloids and Interfaces, Department of Biomaterials, Potsdam, Germany
    2. Berlin-Brandenburg School of Regenerative Therapies (BSRT), Berlin, Germany
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  • Philip Kollmannsberger,

    1. Max Planck Institute of Colloids and Interfaces, Department of Biomaterials, Potsdam, Germany
    2. ETH Zurich, Laboratory of Applied Mechanobiology, Department of Health Sciences and Technology, Zurich, Switzerland
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  • Manfred Burghammer,

    1. European Synchrotron Radiation Facility, Grenoble, France
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  • Georg N Duda,

    1. Berlin-Brandenburg School of Regenerative Therapies (BSRT), Berlin, Germany
    2. Charité, Julius Wolff Institute and Center for Musculoskeletal Surgery, Berlin, Germany
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  • Richard Weinkamer,

    1. Max Planck Institute of Colloids and Interfaces, Department of Biomaterials, Potsdam, Germany
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  • Wolfgang Wagermaier,

    1. Max Planck Institute of Colloids and Interfaces, Department of Biomaterials, Potsdam, Germany
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  • Peter Fratzl

    Corresponding author
    1. Berlin-Brandenburg School of Regenerative Therapies (BSRT), Berlin, Germany
    • Max Planck Institute of Colloids and Interfaces, Department of Biomaterials, Potsdam, Germany
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  • MK and PK contributed equally to this work.

Address correspondence to: Dr. Peter Fratzl, PhD, Max Planck Institute of Colloids & Interfaces, Department of Biomaterials, Am Mühlenberg 1, D-14424 Potsdam, Germany. E-mail: fratzl@mpikg.mpg.de

ABSTRACT

In biological tissues such as bone, cell function and activity crucially depend on the physical properties of the extracellular matrix which the cells synthesize and condition. During bone formation and remodeling, osteoblasts get embedded into the matrix they deposit and differentiate to osteocytes. These cells form a dense network throughout the entire bone material. Osteocytes are known to orchestrate bone remodeling. However, the precise role of osteocytes during mineral homeostasis and their potential influence on bone material quality remains unclear. To understand the mutual influence of osteocytes and extracellular matrix, it is crucial to reveal their network organization in relation to the properties of their surrounding material. Here we visualize and topologically quantify the osteocyte network in mineralized bone sections with confocal laser scanning microscopy. At the same region of the sample, synchrotron small-angle X-ray scattering is used to determine nanoscopic bone mineral particle size and arrangement relative to the cell network. Major findings are that most of the mineral particles reside within less than a micrometer from the nearest cell network channel and that mineral particle characteristics depend on the distance from the cell network. The architecture of the network reveals optimization with respect to transport costs between cells and to blood vessels. In conclusion, these findings quantitatively show that the osteocyte network provides access to a huge mineral reservoir in bone due to its dense organization. The observed correlation between the architecture of osteocyte networks and bone material properties supports the hypothesis that osteocytes interact with their mineralized vicinity and thus, participate in bone mineral homeostasis.

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