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How Linear Tension Converts to Curvature: Geometric Control of Bone Tissue Growth

By Cécile M. Bidan, Krishna P. Kommareddy, Monika Rumpler, Philip Kollmannsberger, Yves J. M. Bréchet, Peter Fratzl and John W. C. Dunlop

Abstract

This study investigated how substrate geometry influences in-vitro tissue formation at length scales much larger than a single cell. Two-millimetre thick hydroxyapatite plates containing circular pores and semi-circular channels of 0.5 mm radius, mimicking osteons and hemi-osteons respectively, were incubated with MC3T3-E1 cells for 4 weeks. The amount and shape of the tissue formed in the pores, as measured using phase contrast microscopy, depended on the substrate geometry. It was further demonstrated, using a simple geometric model, that the observed curvature-controlled growth can be derived from the assembly of tensile elements on a curved substrate. These tensile elements are cells anchored on distant points of the curved surface, thus creating an actin “chord” by generating tension between the adhesion sites. Such a chord model was used to link the shape of the substrate to cell organisation and tissue patterning. In a pore with a circular cross-section, tissue growth increases the average curvature of the surface, whereas a semi-circular channel tends to be flattened out. Thereby, a single mechanism could describe new tissue growth in both cortical and trabecular bone after resorption due to remodelling. These similarities between in-vitro and in-vivo patterns suggest geometry as an important signal for bone remodelling

Topics: Research Article
Publisher: Public Library of Science
OAI identifier: oai:pubmedcentral.nih.gov:3350529
Provided by: PubMed Central
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    Citations

    1. (1991). A reconstruction of the remodelling cycle in normal human cortical iliac bone.
    2. (2007). Actin stress fibres.
    3. (2002). Actomyosin rings: The riddle of the sphincter.
    4. (2011). Adhesion dynamics and durotaxis in migrating cells.
    5. (2003). Adhesion-dependent cell mechanosensitivity. Annual review of cell and developmental biology 19:
    6. (2006). Biomechanical and molecular regulation of bone remodeling.
    7. (2005). Biomimetic mineral-organic composite scaffolds with controlled internal architecture.
    8. (2009). Biomimetism, biomimetic matrices and the induction of bone formation.
    9. (2006). Cell distribution of stress fibres in response to the geometry of the adhesive environment.
    10. (2010). Cellular mechanisms of bone remodeling.
    11. (2007). Concave Pit-Containing Scaffold Surfaces Improve Stem Cell-Derived Osteoblast Performance and Lead to Significant Bone Tissue Formation.
    12. (1992). Distinct Proliferative and Differentiated Stages of Murine MC3T3-El Cells in Culture: An In Vitro Model of Osteoblast Development.
    13. (2004). Effect of low- and high-intensity pulsed ultrasound on collagen post-translational modifications in MC3T3-E1 osteoblasts.
    14. (2001). Effect of pore size and void fraction on cellular adhesion, proliferation, and matrix deposition.
    15. (2008). Emergence of Patterned Stem Cell Differentiation Within Multicellular Structures.
    16. (2005). Emergent patterns of growth controlled by multicellular form and mechanics.
    17. (2009). Environmental sensing through focal adhesions.
    18. (2009). Estimation of the curvature of an interface from a digital 2D image.
    19. (2005). Exploring and engineering the cell surface interface.
    20. (2010). Extracellular matrix assembly and organization during zebrafish gastrulation.
    21. (2008). Filamentous network mechanics and active contractility determine cell and tissue shape.
    22. (2006). Focal adhesions as mechanosensors: The two-spring model.
    23. (2009). Force propagation across cells: mechanical coherence of dynamic cytoskeletons.
    24. (1997). Geometric control of cell life and death.
    25. (2003). Geometric determinants of directional cell motility revealed using microcontact printing.
    26. (2009). Hydrodynamics of Cellular Cortical Flows and the Formation of Contractile Rings. Physical Review Letters 103.
    27. (2011). In vivo validation of a computational bone adaptation model using open-loop control and time-lapsed micro-computed tomography.
    28. (2006). Local force and geometry sensing regulate cell functions.
    29. (2005). Long-distance propagation of forces in a cell.
    30. (2006). Matrix Elasticity Directs Stem Cell Lineage Specification.
    31. (2008). Mechanical control of tissue morphogenesis.
    32. (1997). Mechanotransduction in bone: osteoblasts are more responsive to fluid forces than mechanical strain.
    33. (2003). Modeling Superconformal Electrodeposition Using The Level Set Method.
    34. (2007). Molecular engineering of cellular environments: Cell adhesion to nano-digital surfaces.
    35. (1993). Molecular Mechanisms Mediating Proliferation Differentiation Interrelationships during Progressive Development of the Osteoblast Phenotype.
    36. (1995). Numerical methods for computing interfacial mean curvature.
    37. (2006). Osteocyte lacunae tissue strain in cortical bone.
    38. (2008). Osteocytes, mechanosensing and Wnt signaling.
    39. (1994). Osteonal and Hemi-Osteonal Remodeling: The Spatial and Temporal Framework for Signal Traffic in Adult Human Bone.
    40. (2004). Parallels between tissue repair and embryo morphogenesis.
    41. (2005). Porous scaffold design for tissue engineering.
    42. (1993). Posttranslational control of collagen fibrillogenesis in mineralizing cultures of chick osteoblasts.
    43. (2008). Quantitative differences in tissue surface tension influence zebrafish germ layer positioning.
    44. (2001). Scaffold design and fabrication technologies for engineering tissues - state of the art and future perspectives.
    45. (2003). Signaling Receptome: A Genomic and Evolutionary Perspective of Plasma Membrane Receptors Involved in Signal Transduction. Science’s STKE
    46. (1995). Simulation of curvature-driven graingrowth by using a modified Monte-Carlo algorithm.
    47. (1993). Smeulders AWM
    48. (2008). Solving partial differential equations on irregular domains with moving interfaces, with applications to superconformal electrodeposition in semiconductor manufacturing.
    49. (2002). Surface curvatures of trabecular bone microarchitecture.
    50. (2005). Tensional homeostasis and the malignant phenotype.
    51. (1984). The cellular basis of bone remodeling: the quantum concept reexamined in light of recent advances in the cell biology of bone.
    52. (2005). The differential adhesion hypothesis: a direct evaluation.
    53. (2008). The effect of geometry on three-dimensional tissue growth.
    54. (2007). The emergence of ECM mechanics and cytoskeletal tension as important regulators of cell function.
    55. (2010). The organization of the osteocyte network mirrors the extracellular matrix orientation in bone.
    56. (2011). The phase-field model in tumor growth.
    57. (2011). The physics of tissue patterning and extracellular matrix organisation: how cells join forces. Soft Matter.
    58. (2005). Three-dimensional growth of differentiating MC3T3-E1 pre-osteoblasts on porous titanium scaffolds.
    59. (2005). Tissue cells feel and respond to the stiffness of their substrate.
    60. (2006). Tissue Geometry Determines Sites of Mammary Branching Morphogenesis in Organotypic Cultures.
    61. (2005). Towards bone replacement materials from calcium phosphates via rapid prototyping and ceramic gelcasting.
    62. (2010). Two stages in three-dimensional in vitro growth of tissue generated by osteoblastlike cells.
    63. (2008). Wetting and roughness.

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