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6. The Small World of Osteocytes: Connectomics of the Lacuno-Canalicular Network in Bone

Author

Kollmannsberger, Philip, Kerschnitzki, Michael, Repp, Felix, Wagermaier, Wolfgang, Weinkamer, Richard, and Fratzl, Peter

Subjects
Physics - Biological Physics, Quantitative Biology - Tissues and Organs
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.

Published
2017
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15. The complex structure of Fomes fomentarius represents an architectural design for high-performance ultralightweight materials

Author

Pylkkänen, Robert, primary, Werner, Daniel, additional, Bishoyi, Ajit, additional, Weil, Dominik, additional, Scoppola, Ernesto, additional, Wagermaier, Wolfgang, additional, Safeer, Adil, additional, Bahri, Salima, additional, Baldus, Marc, additional, Paananen, Arja, additional, Penttilä, Merja, additional, Szilvay, Géza R., additional, and Mohammadi, Pezhman, additional

Published
2023
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18. The complex structure of Fomes fomentarius represents an architectural design for high-performance ultralightweight materials

Author

Pylkkänen, Robert, Werner, Daniel, Bishoyi, Ajit, Weil, Dominik, Scoppola, Ernesto, Wagermaier, Wolfgang, Safeer, Adil, Bahri, Salima, Baldus, Marc, Paananen, Arja, Penttilä, Merja, Szilvay, Géza R., Mohammadi, Pezhman, Department of Bioproducts and Biosystems, Max Planck Institute of Colloids and Interfaces, Utrecht University, KLA-Tencor GmbH, VTT Technical Research Centre of Finland, Aalto-yliopisto, and Aalto University

Subjects
Coriolaceae/chemistry
Abstract

We thank C. Li from the Max Planck Institute of Colloids and Interfaces in Potsdam, Germany, for help during synchrotron measurements at the μSpot beamline at BESSY at the Helmholtz-Zentrum Berlin für Materialien und Energie in Berlin, Germany. We acknowledge the provision of facilities and technical support by Aalto University at the OtaNano Nanomicroscopy Center (Aalto-NMC). This work was supported by the Academy of Finland project 348628, the Jenny and Antti Wihuri Foundation (Centre for Young Synbio Scientists), and the Academy of Finland Center of Excellence Program (2022–2029) in Life-Inspired Hybrid Materials (LIBER) project number 346106, and by internal funding from the VTT Technical Research Center of Finland Ltd. We also acknowledge the Dutch Research Council (NWO, domain Applied and Engineering Sciences: MYCOAT project number 18425) and the Horizon 2020 programs of the European Union (FUNGAR; project 58132 and iNEXT-Discovery, project 871037) for NMR studies. Furthermore, the high-field NMR experiments were supported by uNMR-NL, the National Roadmap Large-Scale NMR Facility of the Netherlands (NWO grant 184.032.207), and the uNMR-NL grid (NWO grant 184.035.002). High strength, hardness, and fracture toughness are mechanical properties that are not commonly associated with the fleshy body of a fungus. Here, we show with detailed structural, chemical, and mechanical characterization that Fomes fomentarius is an exception, and its architectural design is a source of inspiration for an emerging class of ultralightweight high-performance materials. Our findings reveal that F. fomentarius is a functionally graded material with three distinct layers that undergo multiscale hierarchical self-assembly. Mycelium is the primary component in all layers. However, in each layer, mycelium exhibits a very distinct microstructure with unique preferential orientation, aspect ratio, density, and branch length. We also show that an extracellular matrix acts as a reinforcing adhesive that differs in each layer in terms of quantity, polymeric content, and interconnectivity. These findings demonstrate how the synergistic interplay of the aforementioned features results in distinct mechanical properties for each layer.

Published
2023

24. Gradients of Orientation, Composition, and Hydration of Proteins for Efficient Light Collection by the Cornea of the Horseshoe Crab

Author

Spaeker, Oliver, primary, Taylor, Gavin J., additional, Wilts, Bodo D., additional, Slabý, Tomáš, additional, Abdel‐Rahman, Mohamed Ashraf Khalil, additional, Scoppola, Ernesto, additional, Schmitt, Clemens N. Z., additional, Sztucki, Michael, additional, Liu, Jiliang, additional, Bertinetti, Luca, additional, Wagermaier, Wolfgang, additional, Scholtz, Gerhard, additional, Fratzl, Peter, additional, and Politi, Yael, additional

Published
2022
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33. Subcanalicular Nanochannel Volume Is Inversely Correlated With Calcium Content in Human Cortical Bone.

Author

Tang, Tengteng, Landis, William, Blouin, Stéphane, Bertinetti, Luca, Hartmann, Markus A., Berzlanovich, Andrea, Weinkamer, Richard, Wagermaier, Wolfgang, and Fratzl, Peter

Abstract

The spatial distribution of mineralization density is an important signature of bone growth and remodeling processes, and its alterations are often related to disease. The extracellular matrix of some vertebrate mineralized tissues is known to be perfused by a lacunocanalicular network (LCN), a fluid‐filled unmineralized structure that harbors osteocytes and their fine processes and transports extracellular fluid and its constituents. The current report provides evidence for structural and compositional heterogeneity at an even smaller, subcanalicular scale. The work reveals an extensive unmineralized three‐dimensional (3D) network of nanochannels (~30 nm in diameter) penetrating the mineralized extracellular matrix of human femoral cortical bone and encompassing a greater volume fraction and surface area than these same parameters of the canaliculi comprising the LCN. The present study combines high‐resolution focused ion beam‐scanning electron microscopy (FIB‐SEM) to investigate bone ultrastructure in 3D with quantitative backscattered electron imaging (qBEI) to estimate local bone mineral content. The presence of nanochannels has been found to impact qBEI measurements fundamentally, such that volume percentage (vol%) of nanochannels correlates inversely with weight percentage (wt%) of calcium. This mathematical relationship between nanochannel vol% and calcium wt% suggests that the nanochannels could potentially provide space for ion and small molecule transport throughout the bone matrix. Collectively, these data propose a reinterpretation of qBEI measurements, accounting for nanochannel presence in human bone tissue in addition to collagen and mineral. Further, the results yield insight into bone mineralization processes at the nanometer scale and present the possibility for a potential role of the nanochannel system in permitting ion and small molecule diffusion throughout the extracellular matrix. Such a possible function could thereby lead to the sequestration or occlusion of the ions and small molecules within the extracellular matrix. © 2022 The Authors. Journal of Bone and Mineral Research published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research (ASBMR). [ABSTRACT FROM AUTHOR]

Published
2023
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40. Novel murine model of atypical type VI osteogenesis imperfecta has altered osteocyte canalicular network, disordered collagen orientation along with hypermineralization of bone matrix

Author

Hedjazi, Ghazal, primary, Guterman-Ram, Gali, additional, Blouin, Stéphane, additional, Hartmann, Markus A., additional, Schemenz, Victoria, additional, Wagermaier, Wolfgang, additional, Fratzl, Peter, additional, Zwerina, Jochen, additional, Fratzl-Zelman, Nadja, additional, and Marini, Joan C., additional

Published
2021
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42. Mineralization generates megapascal contractile stresses in collagen fibrils.

Author

Hang Ping, Wagermaier, Wolfgang, Horbelt, Nils, Scoppola, Ernesto, Chenghao Li, Werner, Peter, Zhengyi Fu, and Fratzl, Peter

Subjects
*MINERALIZATION, *COLLAGEN, *STRONTIUM, *X-ray scattering, *REINFORCED concrete
Abstract

During bone formation, collagen fibrils mineralize with carbonated hydroxyapatite, leading to a hybrid material with excellent properties. Other minerals are also known to nucleate within collagen in vitro. For a series of strontium- and calcium-based minerals, we observed that their precipitation leads to a contraction of collagen fibrils, reaching stresses as large as several megapascals. The magnitude of the stress depends on the type and amount of mineral. Using in-operando synchrotron x-ray scattering, we analyzed the kinetics of mineral deposition. Whereas no contraction occurs when the mineral deposits outside fibrils only, intrafibrillar mineralization generates fibril contraction. This chemomechanical effect occurs with collagen fully immersed in water and generates a mineral-collagen composite with tensile fibers, reminiscent of the principle of reinforced concrete. [ABSTRACT FROM AUTHOR]

Published
2022
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46. Rapid collagen-directed mineralization of calcium fluoride nanocrystals with periodically patterned nanostructures

Author

Fang, Weijian, primary, Ping, Hang, additional, Wagermaier, Wolfgang, additional, Jin, Shenbao, additional, Amini, Shahrouz, additional, Fratzl, Peter, additional, Sha, Gang, additional, Xia, Fanjie, additional, Wu, Jinsong, additional, Xie, Hao, additional, Zhai, Pengcheng, additional, Wang, Weimin, additional, and Fu, Zhengyi, additional

Published
2021
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47. Alterations of Bone Material Properties in Growing  Ifitm5/Bril p.S42 Knock-In Mice, a New Model for Atypical  Type VI Osteogenesis Imperfecta

Author

Hedjazi, Ghazal, primary, Guterman-Ram, Gali, additional, Blouin, Stéphane, additional, Schemenz, Victoria, additional, Wagermaier, Wolfgang, additional, Fratzl, Peter, additional, Hartmann, Markus A., additional, Zwerina, Jochen, additional, Fratzl-Zelman, Nadja, additional, and Marini, Joan C., additional

Published
2021
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48. Proceedings of the National Academy of Sciences of the United States of America / The mechanoresponse of bone is closely related to the osteocyte lacunocanalicular network architecture

Author

van Tol, Alexander Franciscus, Schemenz, Victoria, Wagermaier, Wolfgang, Roschger, Andreas, Razi, Hajar, Vitienes, Isabela, Fratzl, Peter, Willie, Bettina M., and Weinkamer, Richard

Subjects
Mechanobiology, Fluid flow, Bone adaptation, Lacunocanalicular network, In vivo μCT
Abstract

Organisms rely on mechanosensing mechanisms to adapt to changes in their mechanical environment. Fluid-filled network structures not only ensure efficient transport but can also be employed formechanosensation. The lacunocanalicular network (LCN) is a fluid-filled network structure, which pervades our bones and accommodates a cell network of osteocytes. For the mechanism of mechanosensation, it was hypothesized that load-induced fluid flow results in forces that can be sensed by the cells. We use a controlled in vivo loading experiment on murine tibiae to test this hypothesis, whereby the mechanoresponse was quantified experimentally by in vivo microcomputed tomography (μCT) in terms of formed and resorbed bone volume. By imaging the LCN using confocal microscopy in bone volumes covering the entire cross-section of mouse tibiae and by calculating the fluid flow in the three-dimensional (3D) network, we could perform a direct comparison between predictions based on fluid flow velocity and the experimentally measured mechanoresponse. While local strain distributions estimated by finite-element analysis incorrectly predicts preferred bone formation on the periosteal surface, we demonstrate that additional consideration of the LCN architecture not only corrects this erroneous bias in the prediction but also explains observed differences in the mechanosensitivity between the three investigated mice. We also identified the presence of vascular channels as an important mechanism to locally reduce fluid flow. Flow velocities increased for a convergent network structure where all of the flow is channeled into fewer canaliculi. We conclude that, besides mechanical loading, LCN architecture should be considered as a key determinant of bone adaptation.

Published
2020

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