Organization of hydroxyapatite crystals within collagen fibrils

Weiner, Stephen; Traub, Wolfie

Affiliations

¹Isotope Department, The Weizmann Institute of Science, 76100 Rehovot, Israel

²Structural Chemistry Department, The Weizmann Institute of Science, 76100 Rehovot, Israel

Abstract and keywords

Transmission electron micrographs of individual mineralized collagen fibrils show that hydroxyapatite crystals are located mainly within the fibrils at the level of the gap regions. The plate-shaped crystals are observed to be more or less uniformly stacked across the fibril diameter. We therefore suggest that the crystals are primarily located in ‘grooves’ created by contiguous adjacent gaps. Thi proposal is consistent with the observed crystal distribution in the fibril and with their average widths, which are almost lo-times greater than an individual gap diameter.

Keywords: Collagen; Hydroxyapatite crystal; Biomineralization; (Bone, Turkey tendon)

Links

DOI: 10.1016/0014-5793(86)80993-0

PubMed: 3019771

WoS: A1986E461700017

History

Received: 1986-08-04

Cited Works (2)

Year	Entry
1977	Landis WJ, Paine MC, Glimcher MJ. Electron microscopic observations of bone tissue prepared anhydrously in organic solvents. J Ultrastruct Res. April 1977;59(1):1-30.
1952	Robinson RA, Watson ML. Collagen‐crystal relationships in bone as seen in the electron microscope. Anat Rec. November 1952;114(3):383-409.

Cited By (51)

Year	Entry
2011	Wang R, Gupta HS. Deformation and fracture mechanisms of bone and nacre. Ann Rev Mater Res. August 2011;41:41-73.
1991	van der Rest M. The collagens of bone. In: Hall BK, ed. Bone. Volume 3: Bone Matrix and Bone Specific Products. Boca Raton, FL: Inc., CRC Press; 1991:187-237.
2001	Lucchinetti E. Dense bone tissue as a molecular composite. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:13-1–13-15.
2002	Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.
2014	Reznikov N, Shahar R, Weiner S. Bone hierarchical structure in three dimensions. Acta Biomater. September 2014;10(8):3815-3826.
2022	Micheletti C, Hurley A, Gourrier A, Palmquist A, Tang T, Shah FA, Grandfield K. Bone mineral organization at the mesoscale: a review of mineral ellipsoids in bone and at bone interfaces. Acta Biomater. April 1, 2022;142:1-13.
1996	Ziv V, Wagner HD, Weiner S. Microstructure-microhardness relations in parallel-fibered and lamellar bone. Bone. May 1996;18(5):417-428.
1997	Weiner S, Arad T, Sabanay I, Traub. W. Rotated plywood structure of primary lamellar bone in the rat: orientations of the collagen fibril arrays. Bone. June 1997;20(6):509-514.
1999	Wenk H-R, Heidelbach F. Crystal alignment of carbonated apatite in bone and calcified tendon: results from quantitative texture analysis. Bone. April 1999;24(4):361-369.
2003	Su X, Sun K, Cui FZ, Landis WJ. Organization of apatite crystals in human woven bone. Bone. February 2003;32(2):150-162.
2014	Reznikov N, Shahar R, Weiner S. Three-dimensional structure of human lamellar bone: the presence of two different materials and new insights into the hierarchical organization. Bone. February 2014;59:93-104.
2020	Schwarcz HP, Binkley DM, Luo L, Grandfield K. A search for apatite crystals in the gap zone of collagen fibrils in bone using dark-field illumination. Bone. June 2020;135:115304.
2020	Reznikov N, Hoac B, Buss DJ, Addison WN, Barros NMT, McKee MD. Biological stenciling of mineralization in the skeleton: local enzymatic removal of inhibitors in the extracellular matrix. Bone. September 2020;138:115447.
1991	Arsenault AL. Image analysis of collagen-associated mineral distribution in cryogenically prepared turkey leg tendons. Calcif Tiss Int. January 1991;48(1):56-62.
2020	Maghsoudi-Ganjeh M, Wang X, Zeng X. Nanomechanics and ultrastructure of bone: a review. Comput Model Eng Sci. 2020;125(1):1-32.
1989	Weiner S, Traub W. Crystal size and organization in bone. Connect Tissue Res. 1989;21(1-4):259-265.
1994	Ziv V, Weiner S. Bone crystal sizes: a comparison of transmission electron microscopic and x-ray diffraction line width broadening techniques. Connect Tissue Res. 1994;30(3):165-175.
1992	Weiner S, Traub W. Bone structure: from ȧngstroms to microns. FASEB J. February 1992;6(3):879-885.
1991	Weiner S, Arad T, Traub W. Crystal organization in rat bone lamellae. FEBS Lett. July 1991;285(1):49-54.
1992	Wagner HD, Weiner S. On the relationship between the microstructure of bone and its mechanical stiffness. J Biomech. November 1992;25(11):1311-1320.
2007	Rath Bonivtch A, Bonewald LF, Nicolella DP. Tissue strain amplification at the osteocyte lacuna: a microstructural finite element analysis. J Biomech. 2007;40(10):2199-2206.
1993	Skedros JG, Bloebaum RD, Bachus KN, Boyce TM. The meaning of graylevels in backscattered electron images of bone. J Biomed Mater Res. January 1993;7(1):47-56.
1998	Akiva U, Wagner HD, Weiner S. Modelling the three-dimensional elastic constants of parallel-fibred and lamellar bone. J Mater Sci. March 15, 1998;33(6):1497-1509.
2000	Liu D, Wagner HD, Weiner S. Bending and fracture of compact circumferential and osteonal lamellar bone of the baboon tibia. J Mater Sci Mater Med. January 2000;11(1):49-60.
2012	Faingold A, Cohen SR, Wagner HD. Nanoindentation of osteonal bone lamellae. J Mech Behav Biomed Mater. May 2012;9:198-206.
2016	Georgiadis M, Müller R, Schneider P. Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils. J R Soc Interface. June 1, 2016;13(119):20160088.
1996	Landis WJ, Hodgens KJ, Song MJ, Arena J, Kiyonaga S, Marko M, Owen C, McEwen BF. Mineralization of collagen may occur on fibril surfaces: evidence from conventional and high-voltage electron microscopy and three-dimensional imaging. J Struct Biol. July 1996;117(1):24-35.
1999	Weiner S, Traub W, Wagner HD. Lamellar bone: structure–function relations. J Struct Biol. June 1999;126(3):241-255.
2020	Buss DJ, Reznikov N, McKee MD. Crossfibrillar mineral tessellation in normal and Hyp mouse bone as revealed by 3D FIB-SEM microscopy. J Struct Biol. November 1, 2020;212(2):107603.
2012	Russell NA, Pelletier MH, Bruce WJ, Walsh WR. The effect of gamma irradiation on the anisotropy of bovine cortical bone. Med Eng Phys. October 2012;34(8):1117-1122.
2005	Nyman JS, Reyes M, Wang X. Effect of ultrastructural changes on the toughness of bone. Micron. October–December 2005;36(7-8):566-582.
1996	Landis WJ, Hodgens KJ, Arena J, Song MJ, McEwen BF. Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microsc Res Tech. 1996;33(2):192-202.
1989	Traub W, Arad T, Weiner S. Three-dimensional ordered distribution of crystals in turkey tendon collagen fibers. Proc Natl Acad Sci USA. December 1989;86(24):9822-9826.
2013	Kim G. The Effects of Mineralization and Crystallinity on the Mechanical Behavior of Bone [PhD thesis]. Ithaca, NY: Cornell University; May 2013.
2017	Shah FA. Osteocytes as Indicators of Bone Quality: Multiscale Structure-Composition Characterisation of the Bone-Implant Interface [PhD thesis]. University of Gothenburg; 2017.
2023	Micheletti C. Multimodal and Multiscale Characterization of Bone and Bone Interfaces in Health and Disease [PhD thesis]. University of Gothenburg; 2023.
2014	Klosowski MM. Electron Microscopy Characterisation of in Vivo Collagen and Mineral Ultra-Structures, Their Development and Pathologies [PhD thesis]. Imperial College London; August 2014.
2023	Buss DJ. Mineralization of Biological Fiber Systems [PhD thesis]. McGill University; July 2023.
2010	Grandfield K. Characterization of Biomaterial-Bone Interfaces With Transmission Electron Microscopy [Master's thesis]. Hamilton, ON: McMaster University; June 2010.
2019	Neves E. The Effect of Strain on the Minerlization of Individual Collagen Fibrils [Master's thesis]. Northeastern University; December 2019.
2006	Gleeson JP. Composition and Mechanical Properties of Osteoarthritic Subchondral Trabecular Tibial Bone [PhD thesis]. Trinity College Dublin; November 2006.
2011	Ebacher V. Experimental Study of Deformation and Microcracking in Human Cortical Bone [PhD thesis]. Vancouver, BC: University of British Columbia; May 2011.
2018	Tang T. Fracture Mechanisms and Structural Fragility of Human Femoral Cortical Bone [PhD thesis]. Vancouver, BC: University of British Columbia; April 2018.
2011	Zimmermann EA. Deformation and Fracture of Human Cortical Bone Across Multiple Length-Scales [PhD thesis]. Berkeley, CA: Berkeley, University of California; F 2011.
2005	Kozloff KM. Influence of a Collagen Mutation of the Mechanical Nature of Bone: Governing Factors in a Disease Model for Osteogenesis Imperfecta Type IV [PhD thesis]. University of Michigan; 2005.
2011	Raghavan M. Investigation of Mineral and Collagen Organization in Bone Using Raman Spectroscopy [PhD thesis]. University of Michigan; 2011.
2008	Atsawasuwan P. Lysyl Oxidase Regulates Transforming Growth Factor-Β1 Function in Bone [PhD thesis]. University of North Carolina at Chapel Hill; 2008.
2010	Reyes MJ. Age-Related Influence of Bone Remodeling on Local Tissue Properties of Human Cortical Bone [PhD thesis]. San Antionio, TX: University of Texas at San Antonio; December 2010.
2015	Xu H. The Coupling Effect of Water and GAGs on the in Situ Toughness of Bone Are Age-Dependent [Master's thesis]. San Antionio, TX: University of Texas at San Antonio; December 2015.
2014	Reznikov N. The Adaptation of Mechanical Properties of Lamellar Bone Tissue [PhD thesis]. Weizmann Institute of Science; July 2014.
2009	Rath AL. The Effects of Strain and Perilacunar Environment on the Mechanotransduction of Osteocytes [PhD thesis]. Winston-Salem, NC: Wake Forest University; May 2009.