Scaffold curvature-mediated novel biomineralization process originates a continuous soft tissue-to-bone interface

París, Michael; Götz, Andreas; Hettrich, Inga; Bidan, Cécile M.; Dunlop, John W. C.; Razi, Hajar; Zizak, Ivo; Hutmacher, Dietmar W.; Fratzl, Peter; Duda, Georg N.; Wagermaier, Wolfgang; Cipitria, Amaia

doi:10.1016/j.actbio.2017.07.029

Cited by 68 publications

(57 citation statements)

References 58 publications

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“…Indeed, the geometry of the environment strongly influences cellbehavior, since it determines the spatial distribution of force patterns that cells sense and transmit. Previous studies on the role of surface curvature on cell and tissue behavior focused on surfaces where one of the principal curvatures is zero [8,20,21] or was not quantitative due to the complexity of the scaffolds [22]. Here we address this problem by growing tissue on scaffolds with rotational symmetry and constant mean curvature.…”

mentioning

confidence: 99%

Surface tension determines tissue shape and growth kinetics

Ehrig

Bidan

West

et al. 2018

Preprint

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mentioning

confidence: 99%

Surface tension determines tissue shape and growth kinetics

Ehrig

Bidan

West

et al. 2018

Preprint

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“…In engineered tissue scaffolds, tissue grown by osteoblastderived cells in pores of different shapes is also observed to be regulated by geometry. The local rate of growth is found to correlate with the curvature of the tissue [11][12][13], and thought to be due to tissue surface tension driving cell proliferation [12][13][14][15]. Phenomenological models that describe these scaffold experiments assume that the evolution of the tissue interface is governed by mean curvature flows, by analogy with surface-tension-induced mean curvature flows that arises in the evolution of bubbles in fluid mechanics.…”

Section: Discussionmentioning

confidence: 99%

“…There are many design questions that need to be addressed in the production of these scaffolds, such as determining their optimal size, shape and material properties [2][3][4]. These properties have been shown to impact cell attachment, viability, proliferation, migration, and differentiation, among other functions [10][11][12][13][14][15][16], and they could be tuned to control the manufacture of complex multicellular tissues or organs. Recent additive manufacturing techniques have leveraged these biophysical relationships in an ad hoc manner: by 3D printing bilayer cylindrical scaffolds as vascular grafts with endothelial and muscle cells [17] or by patterning scaffold pores or fibres * Corresponding author: pascal.buenzli@qut.edu.au to spatially control cell morphology and differentiation [18].…”

Section: Introductionmentioning

confidence: 99%

“…Several mathematical modelling strategies have been developed to explore the interplay between tissue growth and curvature effects [16], such as models based on the idea of mean curvature flow, that borrow ideas from fluid mechanics and the role of surface tension, but that do not consider cells explicitly [11][12][13][14][15]. Other modelling approaches consider the effects of cell-level behaviour and tissue crowding and spreading during surface growth, which lead to hyperbolic curvature flow models [24,22,25].…”

Section: Introductionmentioning

confidence: 99%

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Cell proliferation and migration explain pore bridging dynamics in 3D printed scaffolds of different pore size

Buenzli

Lanaro

Wong

et al. 2020

Preprint

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Tissue growth in bioscaffolds can be influenced significantly by pore geometry, but how this geometric dependence emerges from dynamic cellular processes such as cell proliferation and cell migration remains poorly understood. Here we investigate the influence of pore size on the time required to bridge pores in a 3D printed scaffold by analysing experiments with a mathematical model. Experimentally, the new tissue infills the pore continually from the pore perimeter under strong curvature control, which leads to rounding off of the initial pore shape. Despite the varied shapes assumed by the tissue during this evolution, we find that time to bridge the pore simply increases linearly with the overall pore size. To disentangle the biological influence of cell behaviour and the mechanistic influence of geometry in this experimental observation, we propose a simple reaction-diffusion model of tissue growth based on Porous-Fisher invasion of cells into the pores. First, this model provides a good qualitative representation of the evolution of the tissue; new cellular tissue in the model grows at a rate that depends on the local curvature of the tissue substrate. Second, the model suggests that a linear dependence of bridging time with pore size arises due to geometric reasons alone, not to differences in cell behaviours across pores of different sizes. Our analysis therefore suggests that tissue growth dynamics in these experimental constructs is dominated by mechanistic cell proliferation and cell diffusion processes. The rates of these processes are unaffected by pore geometry, and can be predicted by simple reaction-diffusion models of cells that have robust, consistent behaviours.

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“…The geometric control of biological tissue growth has been evidenced in several tissue engineering constructs [1][2][3], but much of the cellular mechanisms that underlie this control still remain to be elucidated. In-vitro experimental studies track the evolution of the tissue interface and analyse correlations between growth rate and local curvature, but they report little quantitative information about the tissue-forming cells [4][5][6][7][8].…”

Section: Introductionmentioning

confidence: 99%

Osteoblasts infill irregular pores under curvature and porosity controls: a hypothesis-testing analysis of cell behaviours

Alias

Buenzli

2018

Biomech Model Mechanobiol

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The geometric control of bone tissue growth plays a significant role in bone remodelling, age-related bone loss, and tissue engineering. However, how exactly geometry influences the behaviour of bone-forming cells remains elusive. Geometry modulates cell populations collectively through the evolving space available to the cells, but it may also modulate the individual behaviours of cells. To factor out the collective influence of geometry and gain access to the geometric regulation of individual cell behaviours, we develop a mathematical model of the infilling of cortical bone pores and use it with available experimental data on cortical infilling rates. Testing different possible modes of geometric controls of individual cell behaviours consistent with the experimental data, we find that efficient smoothing of irregular pores only occurs when cell secretory rate is controlled by porosity rather than curvature. This porosity control suggests the convergence of a large scale of intercellular signalling to single bone-forming cells, consistent with that provided by the osteocyte network in response to mechanical stimulus. After validating the mathematical model with the histological record of a real cortical pore infilling, we explore the infilling of a population of randomly generated initial pore shapes. We find that amongst all the geometric regulations considered, the collective influence of curvature on cell crowding is a dominant factor for how fast cortical bone pores infill, and we suggest that the irregularity of cement lines thereby explains some of the variability in double labelling data as well as the overall speed of osteon infilling.

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Scaffold curvature-mediated novel biomineralization process originates a continuous soft tissue-to-bone interface

Cited by 68 publications

References 58 publications

Surface tension determines tissue shape and growth kinetics

Surface tension determines tissue shape and growth kinetics

Cell proliferation and migration explain pore bridging dynamics in 3D printed scaffolds of different pore size

Osteoblasts infill irregular pores under curvature and porosity controls: a hypothesis-testing analysis of cell behaviours

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