Abstract
Osteocytes and their cell processes reside in a large, interconnected network of voids pervading the mineralized bone matrix of most vertebrates. This osteocyte lacuno-canalicular network (OLCN) is believed to play important roles in mechanosensing, mineral homeostasis, and for the mechanical properties of bone. While the extracellular matrix structure of bone is extensively studied on ultrastructural and macroscopic scales, there is a lack of quantitative knowledge on how the cellular network is organized. Using a recently introduced imaging and quantification approach, we analyze the OLCN in different bone types from mouse and sheep that exhibit different degrees of structural organization not only of the cell network but also of the fibrous matrix deposited by the cells. We define a number of robust, quantitative measures that are derived from the theory of complex networks. These measures enable us to gain insights into how efficient the network is organized with regard to intercellular transport and communication. Our analysis shows that the cell network in regularly organized, slow-growing bone tissue from sheep is less connected, but more efficiently organized compared to irregular and fast-growing bone tissue from mice. On the level of statistical topological properties (edges per node, edge length and degree distribution), both network types are indistinguishable, highlighting that despite pronounced differences at the tissue level, the topological architecture of the osteocyte canalicular network at the subcellular level may be independent of species and bone type. Our results suggest a universal mechanism underlying the self-organization of individual cells into a large, interconnected network during bone formation and mineralization.
Highlights
Network structures are ubiquitous in Nature and often fulfill important functions in transport and signal processing
The osteocyte lacuno-canalicular network (OLCN) reconstructed from confocal laser scanning microscopy (CLSM) image stacks is described as a network graph, i.e. by the locations of nodes and edges, and the adjacency matrix, which contains information on how nodes are connected through edges. This makes it possible to calculate generic statistical and topological properties such as edge length and degree distributions, and relationships between these properties. With this proof-of-principle approach, we aim to address the question whether the known differences in tissue organization and appearance of the OLCN in different types of bone from different species are reflected in the organization of the network of cell processes, or if the network at the cellular and subcellular level is independent of bone type and level of organization
We developed a strategy for the quantification of the architecture of the osteocyte network using different bone types from mouse and sheep for the proof of principle
Summary
Network structures are ubiquitous in Nature and often fulfill important functions in transport and signal processing. The organization into networks can already occur on the level of the individual cells, with neurons using their extended dendrites and synapses to connect with other cells as the prototypical example (Cajal and May 1928, Helmstaedter et al 2013, Takemura et al 2013) It has been known for a long time that the mineralized bone tissue of most vertebrates is densely populated by cells called osteocytes. These cells are embedded in the extracellular bone matrix during bone deposition, and are linked with each other and with blood vessels through a highly interconnected network of cell processes (Bonewald 2011) in appearance and size similar to the neuronal system (Buenzli and Sims 2015). The functional relevance of this network and the details of its architecture are still under debate, despite a large number of recent studies in this field (Asada et al 2013, Thi et al 2013, Hesse et al 2015, Milovanovic et al 2015, Sano et al 2015, Nango et al 2016)
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