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

Osteoblasts infill irregular pores under curvature and porosity controls: a hypothesis-testing... 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. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Biomechanics and Modeling in Mechanobiology Springer Journals

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

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Publisher
Springer Berlin Heidelberg
Copyright
Copyright © 2018 by Springer-Verlag GmbH Germany, part of Springer Nature
Subject
Engineering; Theoretical and Applied Mechanics; Biomedical Engineering; Biological and Medical Physics, Biophysics
ISSN
1617-7959
eISSN
1617-7940
D.O.I.
10.1007/s10237-018-1031-x
Publisher site
See Article on Publisher Site

Abstract

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.

Journal

Biomechanics and Modeling in Mechanobiology – Springer Journals

Published: May 30, 2018

References

  • Modeling the effect of curvature on the collective behavior of cells growing new tissue
    Alias, MA; Buenzli, PR
  • Understanding age-induced cortical porosity in women: taccumulation and coalescence of eroded cavities upon existing intracortical canals is the main contributor
    Andreasen, CM; Delaisse, JM; Eerden, BCJ; Leeuwen, JP; Ding, M; Andersen, TL
  • Super-osteons (remodeling clusters) in the cortex of the femoral shaft: influence of age and gender
    Bell, KL; Loveridge, N; Reeve, J; Thomas, CD; Feik, SA; Clement, JG
  • How linear tension converts to curvature: geometric control of bone tissue growth
    Bidan, CM; Kommareddy, KP; Rumpler, M; Kollmannsberger, P; Bréchet, YJM; Fratzl, P; Dunlop, JWC
  • Geometry as a factor for tissue growth: towards shape optimization of tissue engineering scaffolds
    Bidan, CM; Kommareddy, KP; Rumpler, M; Kollmannsberger, P; Fratzl, P; Dunlop, JWC
  • A three-dimensional model for tissue deposition on complex surfaces
    Bidan, CM; Wang, FM; Dunlop, JW
  • Gradual conversion of cellular stress patterns into pre-stressed matrix architecture during in vitro tissue growth
    Bidan, CM; Kollmannsberger, P; Gering, V; Ehrig, S; Joly, P; Petersen, A; Vogel, V; Fratzl, P; Dunlop, JWC
  • The amazing osteocyte
    Bonewald, LF
  • Osteocytes, mechanosensing and Wnt signaling
    Bonewald, LF; Johnson, ML
  • The relation of femoral osteon geometry to age, sex, height and weight
    Britz, HM; Thomas, CDL; Clement, JG; Cooper, DM
  • Age estimation from the auricular surface of the ilium: a revised method
    Buckberry, J; Chamberlain, A
  • Osteocytes as a record of bone formation dynamics: a mathematical model of osteocyte generation in bone matrix
    Buenzli, PR
  • Governing equations of tissue modelling and remodelling: a unified generalised description of surface and bulk balance
    Buenzli, PR
  • Quantifying the osteocyte network in the human skeleton
    Buenzli, PR; Sims, NA
  • Spatio-temporal structure of cell distribution in cortical bone multicellular units: a mathematical model
    Buenzli, PR; Pivonka, P; Smith, D
  • Modelling the anabolic response of bone using a cell population model
    Buenzli, PR; Pivonka, P; Gardiner, BS; Smith, DW
  • Endocortical bone loss in osteoporosis: the role of bone surface availability
    Buenzli, PR; Pivonka, P; Thomas, C; Clement, J
  • Bone refilling in cortical basic multicellular units: insights into tetracycline double labelling from a computational model
    Buenzli, PR; Pivonka, P; Smith, D
  • Mechanotransduction in bone-role of the lacuno-canalicular network
    Burger, EH; Klein-Nulend, J
  • Basic and applied bone biology
    Burr, DB; Akkus, O
  • Geometric control of cell life and death
    Chen, CS; Milan Mrksichl, SH; Whitesides, GM; Ingber, DE
  • Bone poroelasticity
    Cowin, SC
  • Bone mechanics handbook
  • Blood and interstitial flow in the hierarchical pore space architecture of bone tissue
    Cowin, SC; Cardoso, L
  • Strain amplification in the bone mechanosensory system
    Cowin, SC; Weinbaum, S
  • Bone histology: an anthropological perspective
  • The effect of porosity and mineral content on the Young’s modulus of elasticity of compact bone
    Currey, J
  • Dynamics of the transition from osteoblast to osteocyte
    Dallas, SL; Bonewald, LF
  • Exercise and nutritional approaches to prevent frail bones, falls and fractures: an update
    Daly, RM
  • 3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images
    Dong, P; Haupert, S; Hesse, B; Langer, M; Pierre-Jean, GV; Bousson, PF
  • A theoretical model for tissue growth in confined geometries
    Dunlop, J; Fischer, F; Gamsjäger, E; Fratzl, P
  • Buried alive: how osteoblasts become osteocytes
    Franz-Odendaal, TA; Hall, BK; Witten, PE
  • Modelling the role of surface stress on the kinetics of tissue growth in confined geometries
    Gamsjäger, E; Bidan, C; Fischer, F; Fratzl, P; Dunlop, J
  • The role of osteocytes in targeted bone remodeling: a mathematical model
    Graham, JM; Ayati, BP; Holstein, SA; Martin, JA
  • Contribution of matrix heterogeneity and pores to local strains in human cortical bone
    Granke, M; Lopez, O; Grimal, Q; Allain, JM; Saied, A; Crépin, J; Laugier, P
  • A determination of the minimum sizes of representative volume elements for the prediction of cortical bone elastic properties
    Grimal, Q; Raum, K; Gerisch, A; Laugier, P
  • A computational model for cell/ECM growth on 3D surfaces using the level set method: a bone tissue engineering case study
    Guyot, Y; Papantoniou, I; Chai, Y; Bael, S; Schrooten, J; Geris, L
  • A three-dimensional computational fluid dynamics model of shear stress distribution during neotissue growth in a perfusion bioreactor
    Guyot, Y; Luyten, F; Schrooten, J; Papantoniou, I; Geris, L
  • Coupling curvature-dependent and shear stress-stimulated neotissue growth in dynamic bioreactor cultures: a 3D computational model of a complete scaffold
    Guyot, Y; Papantoniou, I; Luyten, FP; Geris, L
  • Bimodal distribution of osteocyte lacunar size in the human femoral cortex as revealed by micro-CT
    Hannah, K; Thomas, C; Clement, J; Carlo, FD; Peele, A
  • Does 3D orientation account for variation in osteon morphology assessed by 2D histology?
    Hennig, C; Thomas, CDL; Clement, JG; Cooper, DML
  • In vivo, three-dimensional microscopy of trabecular bone
    Kinney, J; Lane, N; Haupt, D
  • Pore geometry regulates early stage human bone marrow cell tissue formation and organisation
    Knychala, J; Bouropoulos, N; Catt, C; Katsamenis, O; Please, C; Sengers, B
  • Microfluidic enhancement of intramedullary pressure increases interstitial fluid flow and inhibits bone loss in hindlimb suspended mice
    Kwon, RY; Meays, DR; Tang, WJ; Frangos, JA
  • Skeletal adaptation to intramedullary pressure-induced interstitial fluid flow is enhanced in mice subjected to targeted osteocyte ablation
    Kwon, RY; Meays, DR; Meilan, AS; Jones, J; Miramontes, R; Kardos, N; Yeh, J; Frangos, JA
  • Coupling of bone resorption and formation in real time: new knowledge gained from human haversian BMUs
    Lassen, NE; Andersen, TL; Pløen, GG; Søe, K; Hauge, EM; Harving, S; Eschen, GET; Delaisse, JM
  • Appositional bone formation in canine bone: a quantitative microscopic study using tetracycline markers
    Lee, WR
  • Towards a cell-based mechanostat theory of bone: the need to account for osteocyte desensitisation and osteocyte replacement
    Lerebours, C; Buenzli, PR
  • A multiscale mechanobiological model of bone remodelling predicts site-specific bone loss in the femur during osteoporosis and mechanical disuse
    Lerebours, C; Buenzli, PR; Scheiner, S; Pivonka, P
  • Nonlinear modelling of cancer: bridging the gap between cells and tumour
    Lowengrub, JS; Frieboes, HB; Jin, F; Chuang, YL; Li, X; Macklin, P; Wise, SM; Cristini, V
  • Bone histology. An anthropological perspective
    Maggiano, CM
  • Cross-sectional analysis of long bones, occupational activities and long-distance trade of the classic maya from xcambarchaeological and osteological evidence
    Maggiano, IS; Schultz, M; Kierdorf, H; Sosa, TS; Maggiano, CM; Tiesler Blos, V
  • Observations on the rate of maturation of the cat osteon
    Manson, JD; Waters, NE
  • Multiple models to capture the variability in biological neurons and networks
    Marder, E; Taylor, AL
  • The osteocyte as a wiring transmission system
    Marotti, G
  • Number, size and arrangement of osteoblasts in osteons at different stages of formation
    Marotti, G; Zallone, AZ; Ledda, M
  • The effects of geometric feedback in the development of osteoporosis
    Martin, R
  • Porosity and specific surface of bone
    Martin, RB
  • Does osteocyte formation cause the nonlinear refilling of osteons?
    Martin, R
  • Skeletal tissue mechanics
    Martin, R; Burr, D; Sharkey, N
  • Differences among species in compact bone tissue microstructure of mammalian skeleton: use of a discriminant function analysis for species identification
    Martiniaková, M; Grosskopf, B; Omelka, R; Vondráková, M; Bauerová, M
  • Histological study of compact bone tissue in some mammals: a method for species determination
    Martiniaková, M; Grosskopf, B; Omelka, R; Dammers, K; Vondráková, M; Bauerová, M
  • Version 9.1.0 (R2016b)
  • The Archaeology of Human Bones
    Mays, Simon
  • Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure
    McCalden, RW; McGeough, JA; Barker, MB; Court-Brown, CM
  • Cell migration and organization in the intestinal crypt using a latticefree model
    Meineke, FA; Potten, CS; Loeffler, M
  • Histomorphometric analysis of the effects of osteocyte density on osteonal morphology and remodeling
    Metz, LN; Martin, RB; Turner, AS
  • From a discrete to a continuum model of cell dynamics in one dimension
    Murray, PJ; Edwards, CM; Tindall, MJ; Maini, PK
  • Emergent patterns of growth controlled by multicellular form and mechanics
    Nelson, CM; Jean, RP; Tan, JL; Liu, WF; Sniadecki, NJ; Spector, AA; Chen, CS; Langer, R
  • Biomaterials and scaffolds for tissue engineering
    O’Brien, FJ
  • Bone histomorphometry: techniques and interpretation, chap 9
    Parfitt, A
  • Osteonal and hemi-osteonal remodeling: the spatial and temporal framework for signal traffic in adult human bone
    Parfitt, AM
  • Scaffold curvature-mediated novel biomineralization process originates a continuous soft tissue-to-bone interface
    Paris, M; Gtz, A; Hettrich, I; Bidan, CM; Dunlop, JW; Razi, H; Zizak, I; Hutmacher, DW; Fratzl, P; Duda, GN; Wagermaier, W; Cipitria, A
  • Morphometry and patterns of lamellar bone in human Haversian systems
    Pazzaglia, UE; Congiu, T; Marchese, M; Spagnuolo, R; Quacci, D
  • A discrete model for streaming potentials in a single osteon
    Petrov, N; Pollack, S; Blagoeva, R
  • The influence of bone surface availability in bone remodelling: a mathematical model including coupled geometrical and biomechanical regulations of bone cells
    Pivonka, P; Buenzli, PR; Scheiner, S; Hellmich, R; Dunstan, C
  • A model of osteon closure in cortical bone
    Polig, E; Jee, W
  • Collective migration of an epithelial monolayer in response to a model wound
    Poujade, M; Grasland-Mongrain, E; Hertzog, A; Jouanneau, J; Chavrier, P; Ladoux, B; Buguin, A; Silberzan, P
  • Sclerostin and the regulation of bone formation: effects in hip osteoarthritis and femoral neck fracture
    Power, J; Poole, KE; Bezooijen, R; Doube, M; Caballero-Alias, AM; Lowik, C; Papapoulos, S; Reeve, J; Loveridge, N
  • Deer antlers: a zoological curiosity or the key to understanding organ regeneration in mammals?
    Price, JS; Allen, S; Faucheux, C; Althnaian, T; Mount, JG
  • Understanding and controlling the bone-implant interface
    Puleo, D; Nanci, A
  • Fluid pressure gradients, arising from oscillations in intramedullary pressure, is correlated with the formation of bone and inhibition of intracortical porosity
    Qin, YX; Kaplan, T; Saldanha, A; Rubin, C
  • Biomimetism, biomimetic matrices and the induction of bone formation
    Ripamonti, U
  • Morphology of the drifting osteon
    Robling, AG; Stout, SD
  • Spatial distribution of tissue level properties in a human femoral cortical bone
    Rohrbach, D; Lakshmanan, S; Peyrin, F; Langer, M; Gerisch, A; Grimal, Q; Laugier, P; Raum, K
  • Switchable adhesive substrates: revealing geometry dependence in collective cell behavior
    Rolli, CG; Nakayama, H; Yamaguchi, K; Spatz, JP; Kemkemer, R; Nakanishi, J
  • The effect of geometry on three-dimensional tissue growth
    Rumpler, M; Woesz, A; Dunlop, J; Dongen, J; Fratzl, P
  • Stiffness of compact bone: effects of porosity and density
    Schaffler, MB; Burr, DB
  • Differentiation potential of mesenchymal progenitor cells following transplantation into calvarial defects
    Schantz, JT; Woodruff, MA; Lam, CX; Lim, TC; Machens, HG; Teoh, SH; Hutmacher, DW
  • Principles of bone biology
    Seeman, E
  • Biomaterials and bone mechanotransduction
    Sikavitsas, VI; Temenoff, JS; Mikos, AG
  • Coupling the activities of bone formation and resorption: a multitude of signals within the basic multicellular unit
    Sims, NA; Martin, TJ
  • Relationships of loading history and structural and material characteristics of bone: development of the mule deer calcaneus
    Skedros, JG; Hunt, KJ; Bloebaum, RD
  • Cement lines of secondary osteons in human bone are not mineral-deficient: new data in a historical perspective
    Skedros, JG; Holmes, JL; Vajda, EG; Bloebaum, RD
  • Increase in pore area, and not pore density, is the main determinant in the development of porosity in human cortical bone
    Thomas, CDL; Feik, SA; Clement, JG
  • Mechanotransduction in bone: do bone cells act as sensors of fluid flow?
    Turner, CH; Forwood, MR; Otter, MW
  • Relationships between shape and size of the osteoblasts and the accretion rate of trabecular bone surfaces
    Zallone, AZ

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