Vertebrate mineralized tissues: A modular structural analysis
Source abstract
Abstract
Vertebrate mineralized tissues, present in bones, teeth and scales, have complex 3D hierarchical structures. As more of these tissues are characterized in 3D using mainly FIB SEM at a resolution that reveals the mineralized collagen fibrils and their organization into collagen fibril bundles, highly complex and diverse structures are being revealed. In this perspective we propose an approach to analyzing these tissues based on the presence of modular structures: material textures, pore shapes and sizes, as well as extents of mineralization. This modular approach is complimentary to the widely used hierarchical approach for describing these mineralized tissues. We present a series of case studies that show how some of the same structural modules can be found in different mineralized tissues, including in bone, dentin and scales. The organizations in 3D of the various structural modules in different tissues may differ. This approach facilitates the framing of basic questions such as: are the spatial relations between modular structures the same or similar in different mineralized tissues? Do tissues with similar sets of modules carry out similar functions or can similar functions be carried out using a different set of modular structures? Do mineralized tissues with similar sets of modules have a common developmental or evolutionary pathway? STATEMENT OF SIGNIFICANCE: 3D organization studies of diverse vertebrate mineralized tissues are revealing detailed, but often confusing details about the material textures, the arrangements of pores and differences in the extent of mineralization within a tissue. The widely used hierarchical scheme for describing such organizations does not adequately provide a basis for comparing these tissues, or addressing issues such as structural components thought to be characteristic of bone, being present in dermal tissues and so on. The classification scheme we present is based on identifying structural components within a tissue that can then be systematically compared to other vertebrate mineralized tissues. We anticipate that this classification approach will provide insights into structure-function relations, as well as the evolution of these tissues.
Source: europepmc · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Bone and Dental Protein Studies · Bone Tissue Engineering Materials · Collagen: Extraction and Characterization
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (83)
Show source-provided references
1. Currey · 2002
2. The material bone: structure- mechanical function relations
3. Mechanical design of biomineralized tissues. Bone and other hierarchical materials
4. Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils
5. Havers · 1691
6. Woven bone overview: structural classification based on its integral role in developmental, repair and pathological bone formation throughout vertebrate groups10.22203/eCM.v038a11 ↗
7. Bone hierarchical structure in three dimensions10.1016/j.actbio.2014.05.024 ↗
8. Dentin on the nanoscale: hierarchical organization, mechanical behavior and bioinspired engineering10.1016/j.dental.2017.03.008 ↗
9. A new approach to studying biological and soft materials using focused ion beam scanning electron microscopy (FIB SEM)10.1088/1742-6596/26/1/012 ↗
10. High resolution 3D structures of mineralized tissues in health and disease10.1038/s41574-021-00479-0 ↗
11. Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network10.1016/j.bone.2010.07.026 ↗
12. Serial FIB/SEM imaging for quantitative 3D assessment of the osteocyte lacuno-canalicular network10.1016/j.bone.2011.04.005 ↗
13. Micro- and nano-CT for the study of bone ultrastructure10.1007/s11914-014-0233-0 ↗
14. Opportunities for biomineralization research using multiscale computed X-ray tomography as exemplified by bone imaging10.1016/j.jsb.2021.107822 ↗
15. Three-dimensional imaging of collagen fibril organization in rat circumferential lamellar bone using a dual beam electron microscope reveals ordered and disordered sub-lamellar structures10.1016/j.bone.2012.10.034 ↗
16. Unique three-dimensional structure of a fish mandible bone subjected to unusually high mechanical loads10.1016/j.jsb.2020.107530 ↗
17. Characterization of the growth plate-bone interphase region using cryo-FIB SEM 3D volume imaging10.1016/j.jsb.2021.107781 ↗
18. Logistics of bone mineralization in the chick embryo studied by 3D cryo FIB-SEM imaging10.1002/advs.202301231 ↗
19. A structural census of the current population of protein sequences10.1073/pnas.94.22.11911 ↗
20. The 3D organization of the mineralized scales of the sturgeon has structures reminiscent of dentin and bone: a FIB-SEM study10.1016/j.jsb.2023.108045 ↗
21. Focused ion beam-SEM 3D analysis of mineralized osteonal bone: lamellae and cement sheath structures10.1016/j.actbio.2020.11.002 ↗
22. Three-dimensional structure of minipig fibrolamellar bone: adaptation to axial loading10.1016/j.jsb.2014.03.007 ↗
23. Mineral and organic matrix interaction in normally calcifying tissue visualized in three dimentions by high voltage electron microscopic tomography and graphic image reconstruction10.1006/jsbi.1993.1003 ↗
24. Osteodentin in the Atlantic wolffish (Anarhichas lupus): dentin or bone?10.1002/jmor.21438 ↗
25. Twisted plywood architecture of collagen fibrils in human compact bone osteons10.1007/BF02556330 ↗
26. The three-dimensional structure of anosteocytic lamellated bone of fish10.1016/j.actbio.2014.10.025 ↗
27. The fibrous structure of coelacanth scales: a twisted ‘plywood10.1016/0040-8166(78)90054-X ↗
28. The distribution of collagen fibrils in the dentine matrix
29. Human root dentin: structural anisotropy and Vickers microhardness isotropy10.3109/03008209809021502 ↗
30. Focused ion beam-SEM 3D study of osteodentin in the teeth of the atlantic wolfish Anarhichas lupus10.1016/j.jsb.2024.108062 ↗
31. Discontinuities in the human bone-PDL-cementum complex10.1016/j.biomaterials.2011.06.021 ↗
32. Organization of apatite crystals in human woven bone10.1016/S8756-3282(02)00945-6 ↗
33. Scanning electron microscope studies of bone
34. A 3D network of nanochannels for possible ion and molecule transit in mineralizing bone and cartilage10.1002/anbr.202100162 ↗
35. Three-dimensional structural interrelations between cells, extracellular matrix, and mineral in normally mineralizing avian leg tendon10.1073/pnas.1917932117 ↗
36. AFM analysis of the lacunar-canalicular network in demineralized compact bone10.1111/j.1365-2818.2010.03431.x ↗
37. Nanci · 2008
38. Effects of differences in mineralization on the mechanical properties of bone
39. Morphology of bone and histochemical staining characteristics of bone cells
40. On the mineral in collagen of human crown dentine10.1016/j.biomaterials.2010.03.030 ↗
41. Remodeling in bone without osteocytes: billfish challenge bone structure-function paradigms10.1073/pnas.1412372111 ↗
42. The microradiographic appearance of dentine
43. Three dimensional structures of the inner and outer pig petrous bone using FIB-SEM: implications for development and ancient DNA preservation10.1016/j.jsb.2023.107998 ↗
44. The canine baculum: the structure and mechanical properties of an unusual bone10.1016/j.jsb.2011.06.006 ↗
45. The structure and function of normally mineralizing avian tendons10.1016/S1095-6433(02)00248-9 ↗
46. Bone mineral organization at the mesoscale: a review of mineral ellipsoids in bone and at bone interfaces10.1016/j.actbio.2022.02.024 ↗
47. Crossfibrillar mineral tessellation in normal and Hyp mouse bone as revealed by 3D FIB-SEM microscopy10.1016/j.jsb.2020.107603 ↗
48. Origin and the evolution of bone and dentin, and of their phosphorylated, acid-rich proteins
49. Presence of the earliest vertebrate hard tissues in conodonts10.1126/science.1598573 ↗
50. Endochondral bone in the early Devonian 'placoderm' from Mongolia10.1038/s41559-020-01290-2 ↗
51. Comparative histology of caniniform teeth in some predatory ichthyophagous teleosts
52. A comparative histological study of fossil and recent bone tissues. Part I
53. Ueber funktionell wichtige Anordnungsweisen der eineren und groberen Bauelemente des Wirbeltierknochens.II. Spezieller Teil Der Bau der Haversschen Lamellensysteme und seine funktionelle Bedeutung10.1007/BF02162810 ↗
54. Three-dimensional structure of human lamellar bone: the presence of two different materials and new insights into the hierarchical organization10.1016/j.bone.2013.10.023 ↗
55. Ellipsoidal mesoscale mineralization pattern in human cortical bone revealed in 3D by plasma focused ion beam serial sectioning10.1016/j.jsb.2020.107615 ↗
56. Towards a connectomic description of the osteocyte lacunocanalicular network in bone10.1007/s11914-019-00515-z ↗
57. Martin · 1989
58. Bending and fracture of compact circumferential and osteonal lamellar bone of the baboon tibia10.1023/A:1008989719560 ↗
59. Difference in the blood-supply of bone of different histological types10.1242/jcs.s3-101.55.351 ↗
60. Currey · 1984
61. Poorly ordered bone as an endogenous scaffold for the deposition of highly oriented lamellar tissuein rapidly growing ovine bone10.1159/000324467 ↗
62. The extracellular matrix of cartilage in the growth plate before and during calcification: changes in composition and degradation of Type II collagen10.1007/BF00301630 ↗
63. Morphological convergence of pharyngeal jaw structure in durophagous perciform fish10.1046/j.1095-8312.2003.00231.x ↗
64. Bony fishes
65. Palaeohistological Notes. 4. The interpretation of osteodentine, with remarks on the dentition in the Devonian dipnoan Griphognathus10.1111/j.1463-6409.1976.tb00684.x ↗
66. Muscle force regulates bone shaping for optimal loadbearing capacity during embryogenesis10.1242/dev.063768 ↗
67. The mechanics of tessellations - bioinspired strategies for fracture resistance10.1039/C5CS00598A ↗
68. Insights into the structure and composition of the peritubular dentin organic matrix and the lamina limitans10.1016/j.micron.2011.08.003 ↗
69. The mechanical properties of human dentin: a critical review and re-evaluation of the dental literature10.1177/154411130301400103 ↗
70. On the functional morphology of the human petrous bone10.1002/aja.1001690407 ↗
71. Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing10.1098/rspb.2018.1820 ↗
72. The viability and spatial distribution of osteocytes in the human labyrynthine capsule: a quantitative study using vector-based stereology10.1016/j.heares.2010.09.007 ↗
73. The petrous bone contains high concentrations of osteocytes: one possible reason why ancient DNA is better preserved in this bone10.1371/journal.pone.0269348 ↗
74. Temporal bone dynamics, the hard way: formation, growth, modeling, repair and quantum type bone remodeling in the otic capsule10.3109/00016489409127318 ↗
75. Lowenstam · 1989
76. Strain-mode-specific mechanical testing and the interpretation of bone adaptation in the deer calcaneus
77. Are tensile and compressive Young's moduli of compact bone different?10.1016/j.jmbbm.2008.03.004 ↗
78. The cast of clasts: catabolism and vascular invasion during bone growth, repair, and disease by osteoclasts, chondroclasts, and septoclasts10.3109/03008207.2016.1140752 ↗
79. Inhibition of the terminal differentiation of odontoblasts and their transdifferentiation into osteoblasts in Runx2 transgenic mice10.1679/aohc.71.131 ↗
80. Regulation of osteoblast and odontoblast differentiation by RUNX210.1016/S1349-0079(10)80004-0 ↗
81. Odontoblasts: specialized hard-tissue-forming cells in the dentin-pulp complex10.1111/cga.12169 ↗
82. The role of biomineralization in disorders of skeletal development and tooth formation10.1038/s41574-021-00488-z ↗
83. Cells at the edge: the dentin-bone interface in Zebrafish teeth10.3389/fphys.2021.723210 ↗