Ultra-structural defects cause low bone matrix stiffness despite high mineralization in osteogenesis imperfecta mice

Rho, 1998, Mechanical properties and the hierarchical structure of bone, Med Eng Phys, 20, 92, 10.1016/S1350-4533(98)00007-1 Currey, 1984, Effects of differences in mineralization on the mechanical properties of bone, Philos Trans R Soc Lond, B 304, 509, 10.1098/rstb.1984.0042 Ammann, 2003, Bone strength and its determinants, Osteoporos Int, 14, 13, 10.1007/s00198-002-1345-4 Martin, 1991, Determinants of the mechanical properties of bones, J Biomech, 24, 79, 10.1016/0021-9290(91)90379-2 Turner, 2002, Biomechanics of bone: determinants of skeletal fragility and bone quality, Osteoporos Int, 13, 97, 10.1007/s001980200000 Hoc, 2006, Effect of the microstructure on the mechanical properties of Haversian cortical bone, Bone, 38, 466, 10.1016/j.bone.2005.09.017 Zebaze, 2011, Differences in the degree of bone tissue mineralization account for little of the differences in tissue elastic properties, Bone, 48, 1246, 10.1016/j.bone.2011.02.023 Oyen, 2008, Composite bounds on the elastic modulus of bone, J Biomech, 41, 2585, 10.1016/j.jbiomech.2008.05.018 Gupta, 2005, Two different correlations between nanoindentation modulus and mineral content in the bone–cartilage interface, J Struct Biol, 149, 138, 10.1016/j.jsb.2004.10.010 Rauch, 2004, Osteogenesis imperfecta, Lancet, 363, 1377, 10.1016/S0140-6736(04)16051-0 Traub, 1994, Ultrastructural studies of bones from patients with osteogenesis imperfecta, Matrix Biol, 14, 337, 10.1016/0945-053X(94)90200-3 Jones, 1999, The microscopic structure of bone in normal children and patients with osteogenesis imperfecta: a survey using backscattered electron imaging, Calcif Tissue Int, 64, 8, 10.1007/s002239900571 Forlino, 2011, New perspectives on osteogenesis imperfecta, Nat Rev Endocrinol, 7, 540, 10.1038/nrendo.2011.81 Miller, 2007, Abnormal mineral–matrix interactions are a significant contributor to fragility in oim/oim bone, Calcif Tissue Int, 81, 206, 10.1007/s00223-007-9045-x Misof, 2005, Differential effects of alendronate treatment on bone from growing osteogenesis imperfecta and wild-type mouse, Bone, 36, 150, 10.1016/j.bone.2004.10.006 McCarthy, 2002, Alendronate treatment for infants with osteogenesis imperfecta: demonstration of efficacy in a mouse model, Pediatr Res, 52, 660, 10.1203/00006450-200211000-00010 Vanleene, 2011, Transplantation of human fetal blood stem cells in the osteogenesis imperfecta mouse leads to improvement in multiscale tissue properties, Blood, 117, 1053, 10.1182/blood-2010-05-287565 McBride, 1998, Bone geometry and strength measurements in aging mice with the oim mutation, Calcif Tissue Int, 62, 172, 10.1007/s002239900412 Mehta, 1999, Bone material elasticity in a murine model of osteogenesis imperfecta, Connect Tissue Res, 40, 189, 10.3109/03008209909005282 Chipman, 1993, Defective pro alpha 2(I) collagen synthesis in a recessive mutation in mice: a model of human osteogenesis imperfecta, Proc Natl Acad Sci U S A, 90, 1701, 10.1073/pnas.90.5.1701 Camacho, 1996, Mineral changes in a mouse model of osteogenesis imperfecta detected by Fourier transform infrared microscopy, Connect Tissue Res, 35, 259, 10.3109/03008209609029199 Camacho, 1999, The material basis for reduced mechanical properties in oim mice bones, J Bone Miner Res, 14, 264, 10.1359/jbmr.1999.14.2.264 Carriero, 2011, Cortical tissue porosity of brittle osteogenesis imperfecta bone Phillips, 2000, Oim mice exhibit altered femur and incisor mineral composition and decreased bone mineral density, Bone, 27, 219, 10.1016/S8756-3282(00)00311-2 Fratzl, 1996, Bone mineralization in an osteogenesis imperfecta mouse model studied by small-angle X-ray scattering, J Clin Invest, 97, 396, 10.1172/JCI118428 Grabner, 2001, Age-and genotype-dependence of bone material properties in the osteogenesis imperfecta murine model (oim), Bone, 29, 453, 10.1016/S8756-3282(01)00594-4 Schriefer, 2005, A comparison of mechanical properties derived from multiple skeletal sites in mice, J Biomech, 38, 467, 10.1016/j.jbiomech.2004.04.020 Boyde, 1999, The mineralization density of iliac crest bone from children with osteogenesis imperfecta, Calcif Tissue Int, 64, 185, 10.1007/s002239900600 Kingsmill, 1998, Variation in the apparent density of human mandibular bone with age and dental status, J Anat, 192, 233, 10.1046/j.1469-7580.1998.19220233.x Oyen, 2003, Load-displacement behaviour during sharp indentation of viscous–elastic–plastic materials, J Mater Res, 18, 139, 10.1557/JMR.2003.0020 Oyen, 2007, Examination of local variations in viscous, elastic, and plastic indentation responses in healing bone, J Mater Sci Mater Med, 18, 623, 10.1007/s10856-007-2311-7 Rho, 1997, Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation, Biomaterials, 18, 1325, 10.1016/S0142-9612(97)00073-2 Oyen, 2006, Nanoindentation hardness of mineralized tissues, J Biomech, 39, 2699, 10.1016/j.jbiomech.2005.09.011 Porter, 2005, A transmission electron microscopy study of mineralization in age-induced transparent dentin, Biomaterials, 26, 7650, 10.1016/j.biomaterials.2005.05.059 Hengsberger, 2002, Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological condition, Bone, 30, 178, 10.1016/S8756-3282(01)00624-X Silva, 2004, Nanoindentation and whole-bone bending estimates of material properties in bones from the senescence accelerated mouse SAMP6, J Biomech, 37, 1639, 10.1016/j.jbiomech.2004.02.018 Rho, 1999, Effects of drying on the mechanical properties of bovine femur measured by nanoindentation, J Mater Sci Mater Med, 10, 485, 10.1023/A:1008901109705 Fan, 2003, Effects of viscoelasticity and time-dependent plasticity on nanoindentation measurements of human cortical bone, J Biomed Mater Res A, 67, 208, 10.1002/jbm.a.10027 Akhter, 2004, Bone intrinsic material properties in three inbred mouse strains, Calcif Tissue Int, 75, 416, 10.1007/s00223-004-0241-7 McBride, 1997, Altered collagen structure in mouse tail tendon lacking the alpha(2)I chain, J Mol Biol, 270, 275, 10.1006/jmbi.1997.1106 Miles, 2002, The role of the [alpha]2 chain in the stabilization of the collagen type I heterotrimer: a study of the type I homotrimer in oim mouse tissues, J Mol Biol, 321, 797, 10.1016/S0022-2836(02)00703-9 Sims, 2011, Properties of collagen in oim mouse tissues, Connect Tissue Res, 44, 202, 10.1080/03008200390181663 Kuznetsova, 2001, Osteogenesis imperfecta murine: interaction between type I collagen homotrimers, J Mol Biol, 309, 807, 10.1006/jmbi.2001.4682 Kuznetsova, 2003, Changes in thermal stability and microunfolding pattern of collagen helix resulting from the loss of [alpha]2(I) chain in osteogenesis imperfecta murine, J Mol Biol, 331, 191, 10.1016/S0022-2836(03)00715-0 Ferguson, 2003, Nanomechanical properties and mineral concentration in articular calcified cartilage and subchondral bone, J Anat, 203, 191, 10.1046/j.1469-7580.2003.00193.x Doube, 2010, Combined nanoindentation testing and scanning electron microscopy of bone and articular calcified cartilage in an equine fracture predilection site, Eur Cell Mater, 19, 242, 10.22203/eCM.v019a23 Currey, 1964, Three analogies to explain the mechanical properties of bone, Biorheology, 2, 1, 10.3233/BIR-1964-2101 Hellmich, 2002, Are mineralized tissues open crystal foams reinforced by crosslinked collagen?—Some energy arguments, J Biomech, 35, 1199, 10.1016/S0021-9290(02)00080-5 Hellmich C, Barthélémy J-F, Dormieux L. Mineral–collagen interactions in elasticity of bone ultrastructure — a continuum micromechanics approach. European Journal of Mechanics - A/Solids September;23:783–810. Oyen, 2005 Oyen, 2005, Finite element modeling of bone ultrastructure as a two-phase composite, Vol. 844, 263 Park-Wyllie, 2011, Bisphosphonate use and the risk of subtrochanteric or femoral shaft fractures in older women, JAMA, 305, 783, 10.1001/jama.2011.190 Marini, 2003, Do bisphosphonates make children's bones better or brittle?, N Engl J Med, 349, 423, 10.1056/NEJMp038103