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      Mineral tessellation in bone and the stenciling principle for extracellular matrix mineralization.

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          Abstract

          We review here the Stenciling Principle for extracellular matrix mineralization that describes a double-negative process (inhibition of inhibitors) that promotes mineralization in bone and other mineralized tissues, whereas the default condition of inhibition alone prevents mineralization elsewhere in soft connective tissues. The stenciling principle acts across multiple levels from the macroscale (skeleton/dentition vs soft connective tissues), to the microscale (for example, entheses, and the tooth attachment complex where the soft periodontal ligament is situated between mineralized tooth cementum and mineralized alveolar bone), and to the mesoscale (mineral tessellation). It relates to both small-molecule (e.g. pyrophosphate) and protein (e.g. osteopontin) inhibitors of mineralization, and promoters (enzymes, e.g. TNAP, PHEX) that degrade the inhibitors to permit and regulate mineralization. In this process, an organizational motif for bone mineral arises that we call crossfibrillar mineral tessellation where mineral formations - called tesselles - geometrically approximate prolate ellipsoids and traverse multiple collagen fibrils (laterally). Tesselle growth is directed by the structural anisotropy of collagen, being spatially restrained in the shorter transverse tesselle dimensions (averaging 1.6 × 0.8 × 0.8 μm, aspect ratio 2, length range 1.5-2.5 μm). Temporo-spatially, the tesselles abut in 3D (close ellipsoid packing) to fill the volume of lamellar bone extracellular matrix. Poorly mineralized interfacial gaps between adjacent tesselles remain discernable even in mature lamellar bone. Tessellation of a same, small basic unit to form larger structural assemblies results in numerous 3D interfaces, allows dissipation of critical stresses, and enables fail-safe cyclic deformations. Incomplete tessellation in osteomalacia/odontomalacia may explain why soft osteomalacic bones buckle and deform under loading.

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          Author and article information

          Journal
          J Struct Biol
          Journal of structural biology
          Elsevier BV
          1095-8657
          1047-8477
          March 2022
          : 214
          : 1
          Affiliations
          [1 ] Faculty of Dentistry, McGill University, 3640 University Street, Montréal, Québec H3A 0C7, Canada; Department of Anatomy and Cell Biology, School of Biomedical Sciences, Faculty of Medicine and Health Sciences, McGill University, 3640 University Street, Montréal, Québec H3A 0C7, Canada. Electronic address: marc.mckee@mcgill.ca.
          [2 ] Department of Anatomy and Cell Biology, School of Biomedical Sciences, Faculty of Medicine and Health Sciences, McGill University, 3640 University Street, Montréal, Québec H3A 0C7, Canada.
          [3 ] Department of Bioengineering, Faculty of Engineering, McGill University, 3480 University Street, Montréal, Québec H3A 0E9, Canada. Electronic address: natalie.reznikov@mcgill.ca.
          Article
          S1047-8477(21)00128-3
          10.1016/j.jsb.2021.107823
          34915130
          9f6feb49-8802-4c1b-821a-d9f75e764319
          History

          X-linked hypophosphatemia,Tissue-nonspecific alkaline phosphatase,Teeth,Pyrophosphate,Phosphate-regulating endopeptidase homolog X-linked,Osteopontin,Osteomalacia,Mineralized tissues,Mineralization,Hypophosphatasia,FIB-SEM tomography,Extracellular matrix,Electron microscopy,Crossfibrillar mineral tessellation,Bone,Biomineralization

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