Altered lacunar and vascular porosity in osteogenesis imperfecta mouse bone as revealed by synchrotron tomography contributes to bone fragility

Bone

Volumn 61, Issue , 2014, Pages 116-124

  Carriero, A ^a,b   Doube, M ^a,d   Vogt, M ^a   Busse, B ^c   Zustin, J ^c   Levchuk, A ^b   Schneider, P ^b   Muller R ^b   Shefelbine, S J ^a,e  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d ROYAL VETERINARY COLLEGE   (United Kingdom)

^e Northeastern University   (United States)

Author keywords

Bone; Canal; Oim; Osteocyte lacunae; Osteogenesis imperfecta; Porosity

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; BIOMECHANICS; BLOOD VESSEL; BONE CHARACTERISTICS AND FUNCTIONS; BONE DENSITY; BONE FAILURE; BONE FRAGILITY; BONE MINERALIZATION; BONE QUALITY; BRIGHT FIELD MICROSCOPY; CONTROLLED STUDY; CORTICAL BONE; DIAPHYSIS; FINITE ELEMENT ANALYSIS; HUMERUS; LACUNAR POROSITY; MALE; MECHANICAL PERFORMANCE; MOUSE; NONHUMAN; OSTEOGENESIS IMPERFECTA; POROSITY; STAINING; SYNCHROTRON RADIATION; SYNCHROTRON TOMOGRAPHY; THREE DIMENSIONAL IMAGING; TIBIA; TOMOGRAPHY; VASCULAR POROSITY; WILD TYPE;

BONE; CANAL; OIM; OSTEOCYTE LACUNAE; OSTEOGENESIS IMPERFECTA; POROSITY;

ANIMALS; BONE AND BONES; DISEASE MODELS, ANIMAL; IMAGING, THREE-DIMENSIONAL; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; OSTEOGENESIS IMPERFECTA; POROSITY; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84893415183     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.12.020     Document Type: Article

References (46)

1. Rauch F., Glorieux F.H. Osteogenesis imperfecta. Lancet 2004, 363:1377-1385.
2. Huber M.A. Osteogenesis imperfecta. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007, 103:314-320.
3. Cole W.G. The Nicholas Andry Award-1996. The molecular pathology of osteogenesis imperfecta. Clin Orthop Relat Res 1997, 343:235-248.
4. Cole W.G. Advances in osteogenesis imperfecta. Clin Orthop Relat Res 2002, 401:6-16.
5. Chipman S.D., Sweet H.O., McBride D.J., Davisson M.T., Marks S.C., Shuldiner A.R., et al. 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 1993, 90:1701-1705.
6. Zhang H., Doty S.B., Hughes C., Dempster D., Camacho N.P. Increased resorptive activity and accompanying morphological alterations in osteoclasts derived from the oim/oim mouse model of osteogenesis imperfecta. J Cell Biochem 2007, 102:1011-1020.
7. Kalajzic I., Terzic J., Rumboldt Z., Mack K., Naprta A., Ledgard F., et al. Osteoblastic response to the defective matrix in the osteogenesis imperfecta murine (oim) mouse. Endocrinology 2002, 143:1594-1601.
8. Camacho N.P., Hou L., Toledano T.R., Ilg W.A., Brayton C.F., Raggio C.L., et al. The material basis for reduced mechanical properties in oim mice bones. J Bone Miner Res 1999, 14:264-272.
9. Phillips C.L., Bradley D.A., Schlotzhauer C.L., Bergfeld M., Libreros-Minotta C., Gawenis L.R., et al. Oim mice exhibit altered femur and incisor mineral composition and decreased bone mineral density. Bone 2000, 27:219-226.
10. Camacho N.P., Landis W.J., Boskey A.L. Mineral changes in a mouse model of osteogenesis imperfecta detected by Fourier transform infrared microscopy. Connect Tissue Res 1996, 35:259-265.
11. Grabner B., Landis W.J., Roschger P., Rinnerthaler S., Peterlik H., Klaushofer K., et al. Age- and genotype-dependence of bone material properties in the osteogenesis imperfecta murine model (oim). Bone 2001, 29:453-457.
12. Boyde A., Travers R., Glorieux F.H., Jones S.J. The mineralization density of iliac crest bone from children with osteogenesis imperfecta. Calcif Tissue Int 1999, 64:185-190.
13. Zionts L.E., Nash J.P., Rude R., Ross T., Stott N.S. Bone mineral density in children with mild osteogenesis imperfecta. J Bone Joint Surg Br 1995, 77:143-147.
14. Nyman J.S., Reyes M., Wang X. Effect of ultrastructural changes on the toughness of bone. Micron 2005, 36:566-582.
15. Saban J., Zussman M.A., Havey R., Patwardhan A.G., Schneider G.B., King D. Heterozygous oim mice exhibit a mild form of osteogenesis imperfecta. Bone 1996, 19:575-579.
16. McBride D.J., Shapiro J.R., Dunn M.G. Bone geometry and strength measurements in aging mice with the oim mutation. Calcif Tissue Int 1998, 62:172-176.
17. Vanleene M., Saldanha Z., Cloyd K.L., Jell G., Bou-Gharios G., Bassett J.H., et al. Transplantation of human fetal blood stem cells in the osteogenesis imperfecta mouse leads to improvement in multiscale tissue properties. Blood 2011, 117:1053-1060.
18. Vanleene M., Porter A., Guillot P.V., Boyde A., Oyen M., Shefelbine S. Ultra-structural defects cause low bone matrix stiffness despite high mineralization in osteogenesis imperfecta mice. Bone 2012, 50:1317-1323.
19. Nadiarnykh O., Plotnikov S., Mohler W.A., Kalajzic I., Redford-Badwal D., Campagnola P.J. Second harmonic generation imaging microscopy studies of osteogenesis imperfecta. J Biomed Opt 2007, 12:051805.
20. Boyde A., Maconnachie E., Reid S.A., Delling G., Mundy G.R. Scanning electron microscopy in bone pathology: review of methods, potential and applications. Scan Electron Microsc 1986, 4:1537-1554.
21. Cassella J.P., Stamp T.C., Ali S.Y. A morphological and ultrastructural study of bone in osteogenesis imperfecta. Calcif Tissue Int 1996, 58:155-165.
22. Jones S.J., Glorieux F.H., Travers R., Boyde A. The microscopic structure of bone in normal children and patients with osteogenesis imperfecta: a survey using backscattered electron imaging. Calcif Tissue Int 1999, 64:8-17.
23. Rauch F., Travers R., Parfitt A.M., Glorieux F.H. Static and dynamic bone histomorphometry in children with osteogenesis imperfecta. Bone 2000, 26:581-589.
24. Stampanoni M., Groso A., Isenegger A., Mikuljan G., Chen Q., Meister D., et al. TOMCAT: a beamline for TOmographic Microscopy and Coherent rAdiology experimenTs. AIP Conf Proc 2007, 879:848-851.
25. Rasband W.S. ImageJ, U.S. National Institutes of Health, Bethesda, MD, USA http://rsb.info.nih.gov/ij/2011.
26. Ridler T.W., Calvard S. Picture thresholding using an iterative selection method. IEEE Trans Syst Man Cybern 1978, 8:603-632.
27. Doube M., Klosowski M.M., Arganda-Carreras I., Cordelieres F.P., Dougherty R.P., Jackson J.S., et al. BoneJ: free and extensible bone image analysis in ImageJ. Bone 2010, 47:1076-1079.
28. Stauber M., Müller R. Volumetric spatial decomposition of trabecular bone into rods and plates-a new method for local bone morphometry. Bone 2006, 38:475-484.
29. Schneider P., Stauber M., Voide R., Stampanoni M., Donahue L.R., Müller R. Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT. J Bone Miner Res 2007, 22:1557-1570.
30. Schmid B., Schindelin J., Cardona A., Longair M., Heisenberg M. A high-level 3D visualization API for Java and ImageJ. BMC Bioinformatics 2010, 11:274.
31. Carter Y., Thomas C.D., Clement J.G., Peele A.G., Hannah K., Cooper D.M. Variation in osteocyte lacunar morphology and density in the human femur-a synchrotron radiation micro-CT study. Bone 2013, 52:126-132.
32. Mueller T.L., Christen D., Sandercott S., Boyd S.K., van Rietbergen B., Eckstein F., et al. Computational finite element bone mechanics accurately predicts mechanical competence in the human radius of an elderly population. Bone 2011, 48:1232-1238.
33. Pistoia W., van Rietbergen B., Ruegsegger P. Mechanical consequences of different scenarios for simulated bone atrophy and recovery in the distal radius. Bone 2003, 33:937-945.
34. Hahn M., Vogel M., Delling G. Undecalcified preparation of bone tissue: report of technical experience and development of new methods. Virchows Arch A Pathol Anat Histopathol 1991, 418:1-7.
35. Voide R., Schneider P., Stauber M., Wyss P., Stampanoni M., Sennhauser U., et al. Time-lapsed assessment of microcrack initiation and propagation in murine cortical bone at submicrometer resolution. Bone 2009, 45:164-173.
36. Dong X.N., Zoghi M., Ran Q., Wang X. Collagen mutation causes changes of the microdamage morphology in bone of an OI mouse model. Bone 2010, 47:1071-1075.
37. Vatsa A., Breuls R.G., Semeins C.M., Salmon P.L., Smit T.H., Klein-Nulend J. Osteocyte morphology in fibula and calvaria-is there a role for mechanosensing?. Bone 2008, 43:452-458.
38. Hirose S., Li M., Kojima T., de Freitas P.H., Ubaidus S., Oda K., et al. A histological assessment on the distribution of the osteocytic lacunar canalicular system using silver staining. J Bone Miner Metab 2007, 25:374-382.
39. Remaggi F., Cane V., Palumbo C., Ferretti M. Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. I. Woven-fibered and parallel-fibered bones. Ital J Anat Embryol 1998, 103:145-155.
40. Hernandez C.J., Majeska R.J., Schaffler M.B. Osteocyte density in woven bone. Bone 2004, 35:1095-1099.
41. Kerschnitzki M., Wagermaier W., Roschger P., Seto J., Shahar R., Duda G.N., et al. The organization of the osteocyte network mirrors the extracellular matrix orientation in bone. J Struct Biol 2011, 173:303-311.
42. Boskey A., Pleshko Camacho N. FT-IR imaging of native and tissue-engineered bone and cartilage. Biomaterials 2007, 28:2465-2478.
43. Schneider P., Voide R., Stampanoni M., Donahue L.R., Muller R. The importance of the intracortical canal network for murine bone mechanics. Bone 2013, 53:120-128.
44. Voide R., Schneider P., Stauber M., van Lenthe G.H., Stampanoni M., Müller R. The importance of murine cortical bone microstructure for microcrack initiation and propagation. Bone 2011, 49:1186-1193.
45. Jepsen K.J., Hu B., Tommasini S.M., Courtland H.W., Price C., Cordova M., et al. Phenotypic integration of skeletal traits during growth buffers genetic variants affecting the slenderness of femora in inbred mouse strains. Mamm Genome 2009, 20:21-33.
46. Brodt M.D., Ellis C.B., Silva M.J. Growing C57Bl/6 mice increase whole bone mechanical properties by increasing geometric and material properties. J Bone Miner Res 1999, 14:2159-2166.