Increased proportion of hypermineralized osteocyte lacunae in osteoporotic and osteoarthritic human trabecular bone: Implications for bone remodeling

Bone

Volumn 50, Issue 3, 2012, Pages 688-694

  Carpentier, Vincent T ^a,b   Wong, Jinquan ^a   Yeap, Youwen ^a   Gan, Cheryl ^a   Sutton Smith, Peter ^a,c   Badiei, Arash ^a   Fazzalari, Nicola L ^a,c   Kuliwaba, Julia S ^a,c  

^a HANSON INSTITUTE   (Australia)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Energy dispersive X ray spectrometry; Hypermineralized osteocyte lacunae; Osteoarthritis; Osteoporosis; Quantitative backscattered electron imaging; Trabecular bone

Indexed keywords

ADULT; AGED; ARTICLE; AUTOPSY; BONE DENSITY; BONE HYPERMINERALIZATION; BONE MATRIX; BONE MINERALIZATION; BONE REMODELING; CELL COUNT; CELL DENSITY; FEMALE; FEMUR NECK FRACTURE; HIP OSTEOARTHRITIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; OSTEOARTHRITIS; OSTEOCYTE; OSTEOPOROSIS; TRABECULAR BONE;

AGED; AGED, 80 AND OVER; AGING; BONE AND BONES; BONE REMODELING; CALCIFICATION, PHYSIOLOGIC; FEMALE; HUMANS; MALE; MIDDLE AGED; OSTEOARTHRITIS; OSTEOCYTES; OSTEOPOROSIS;

EID: 84856959164     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.11.021     Document Type: Article

References (49)

1. Marotti G. The structure of bone tissues and the cellular control of their deposition. Ital J Anat Embryol 1996, 101:25-79.
2. Dallas S.L., Bonewald L.F. Dynamics of the transition from osteoblast to osteocyte. Ann N Y Acad Sci 2010, 1192:437-443.
3. Schneider P., Meier M., Wepf R., Muller R. Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network. Bone 2010, 47:848-858.
4. Weinbaum S., Cowin S.C., Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 1994, 27:339-360.
5. Wang L., Wang Y., Han Y., Henderson S.C., Majeska R.J., Weinbaum S., et al. In situ measurement of solute transport in the bone lacunar-canalicular system. Proc Natl Acad Sci U S A 2005, 102:11911-11916.
6. Burger E.H., Klein-Nulend J. Mechanotransduction in bone-role of the lacuno-canalicular network. FASEB J 1999, 13:S101-S112. (Suppl.).
7. Bonewald L.F. The amazing osteocyte. J Bone Miner Res 2011, 26:229-238.
8. Price C., Zhou X., Li W., Wang L. Real-time measurement of solute transport within the lacunar-canalicular system of mechanically loaded bone: direct evidence for load-induced fluid flow. J Bone Miner Res 2011, 26:277-285.
9. Skerry T.M., Bitensky L., Chayen J., Lanyon L.E. Early strain-related changes in enzyme activity in osteocytes following bone loading in vivo. J Bone Miner Res 1989, 4:783-788.
10. Gluhak-Heinrich J., Ye L., Bonewald L.F., Feng J.Q., MacDougall M., Harris S.E., et al. Mechanical loading stimulates dentin matrix protein 1 (DMP1) expression in osteocytes in vivo. J Bone Miner Res 2003, 18:807-817.
11. Robling A.G., Niziolek P.J., Baldridge L.A., Condon K.W., Allen M.R., Alam I., et al. Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 2008, 283:5866-5875.
12. Bonewald L.F., Johnson M.L. Osteocytes, mechanosensing and Wnt signaling. Bone 2008, 42:606-615.
13. Lin C., Jiang X., Dai Z., Guo X., Weng T., Wang J., et al. Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/beta-catenin signaling. J Bone Miner Res 2009, 24:1651-1661.
14. Seeman E. Osteocytes-martyrs for integrity of bone strength. Osteoporos Int 2006, 17:1443-1448.
15. Bonewald L.F. Osteocytes as dynamic multifunctional cells. Ann N Y Acad Sci 2007, 1116:281-290.
16. Feng J.Q., Ward L.M., Liu S., Lu Y., Xie Y., Yuan B., et al. Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat Genet 2006, 38:1310-1315.
17. Frost H.M. Micropetrosis. J Bone Joint Surg Am 1960, 42-A:144-150.
18. Remaggi F., Ferretti M., Cane V., Zaffe D. Histomorphological and chemico-physical analyses of the mineral matrix of micropetrotic human bone. Ann Anat 1996, 178:223-227.
19. Busse B., Djonic D., Milovanovic P., Hahn M., Puschel K., Ritchie R.O., et al. Decrease in the osteocyte lacunar density accompanied by hypermineralized lacunar occlusion reveals failure and delay of remodeling in aged human bone. Aging Cell 2010, 9:1065-1075.
20. Kingsmill V.J., Boyde A. Mineralisation density of human mandibular bone: quantitative backscattered electron image analysis. J Anat 1998, 192(Pt 2):245-256.
21. Boyde A. The real response of bone to exercise. J Anat 2003, 203:173-189.
22. Collins D. The pathology of articular and spinal diseases 1949, Edward Arnold and Co., London.
23. Roschger P., Fratzl P., Eschberger J., Klaushofer K. Validation of quantitative backscattered electron imaging for the measurement of mineral density distribution in human bone biopsies. Bone 1998, 23:319-326.
24. Sutton-Smith P., Beard H., Fazzalari N. Quantitative backscattered electron imaging of bone in proximal femur fragility fracture and medical illness. J Microsc 2008, 229:60-66.
25. Qiu S., Phipps R.J., Ebetino F.H., Palnitkar S., Sudhaker Rao D. Effect of risedronate on osteocyte viability and bone turnover in paired iliac bone biopsies from early postmenopausal women. Calcif Tissue Int 2010, 87:392-397.
26. Roschger P., Plenk H., Klaushofer K., Eschberger J. A new scanning electron microscopy approach to the quantification of bone mineral distribution: backscattered electron image grey-levels correlated to calcium K alpha-line intensities. Scanning Microsc 1995, 9:75-86. discussion 86-8.
27. Bloebaum R.D., Holmes J.L., Skedros J.G. Mineral content changes in bone associated with damage induced by the electron beam. Scanning 2005, 27:240-248.
28. Roschger P., Rinnerthaler S., Yates J., Rodan G.A., Fratzl P., Klaushofer K. Alendronate increases degree and uniformity of mineralization in cancellous bone and decreases the porosity in cortical bone of osteoporotic women. Bone 2001, 29:185-191.
29. Loveridge N., Power J., Reeve J., Boyde A. Bone mineralization density and femoral neck fragility. Bone 2004, 35:929-941.
30. Li B., Aspden R.M. Composition and mechanical properties of cancellous bone from the femoral head of patients with osteoporosis or osteoarthritis. J Bone Miner Res 1997, 12:641-651.
31. Allen M.R., Burr D.B. The pathogenesis of bisphosphonate-related osteonecrosis of the jaw: so many hypotheses, so few data. J Oral Maxillofac Surg 2009, 67:61-70.
32. 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.
33. Jordan G.R., Loveridge N., Power J., Clarke M.T., Parker M., Reeve J. The ratio of osteocytic incorporation to bone matrix formation in femoral neck cancellous bone: an enhanced osteoblast work rate in the vicinity of hip osteoarthritis. Calcif Tissue Int 2003, 72:190-196.
34. Mullender M.G., van der Meer D.D., Huiskes R., Lips P. Osteocyte density changes in aging and osteoporosis. Bone 1996, 18:109-113.
35. Mullender M.G., Tan S.D., Vico L., Alexandre C., Klein-Nulend J. Differences in osteocyte density and bone histomorphometry between men and women and between healthy and osteoporotic subjects. Calcif Tissue Int 2005, 77:291-296.
36. Power J., Noble B.S., Loveridge N., Bell K.L., Rushton N., Reeve J. Osteocyte lacunar occupancy in the femoral neck cortex: an association with cortical remodeling in hip fracture cases and controls. Calcif Tissue Int 2001, 69:13-19.
37. Qiu S., Rao D.S., Palnitkar S., Parfitt A.M. Reduced iliac cancellous osteocyte density in patients with osteoporotic vertebral fracture. J Bone Miner Res 2003, 18:1657-1663.
38. Zoehrer R., Perilli E., Kuliwaba J.S., Shapter J.G., Fazzalari N.L., Voelcker N.H. Human bone material characterization: integrated imaging surface investigation of male fragility fractures. Osteoporos Int 2011, 10.1007/s00198-011-1688-9.
39. Akesson K., Grynpas M.D., Hancock R.G., Odselius R., Obrant K.J. Energy-dispersive X-ray microanalysis of the bone mineral content in human trabecular bone: a comparison with ICPES and neutron activation analysis. Calcif Tissue Int 1994, 55:236-239.
40. Diab T., Allen M.R., Burr D.B. Alendronate treatment results in similar levels of trabecular bone remodeling in the femoral neck and vertebra. Osteoporos Int 2009, 20:647-652.
41. Boivin G., Farlay D., Bala Y., Doublier A., Meunier P.J., Delmas P.D. Influence of remodeling on the mineralization of bone tissue. Osteoporos Int 2009, 20:1023-1026.
42. Ruffoni D., Fratzl P., Roschger P., Klaushofer K., Weinkamer R. The bone mineralization density distribution as a fingerprint of the mineralization process. Bone 2007, 40:1308-1319.
43. Qiu S., Rao D.S., Palnitkar S., Parfitt A.M. Age and distance from the surface but not menopause reduce osteocyte density in human cancellous bone. Bone 2002, 31:313-318.
44. Bell L.S., Kayser M., Jones C. The mineralized osteocyte: a living fossil. Am J Phys Anthropol 2008, 137:449-456.
45. Kogianni G., Mann V., Noble B.S. Apoptotic bodies convey activity capable of initiating osteoclastogenesis and localized bone destruction. J Bone Miner Res 2008, 23:915-927.
46. Noble B.S. The osteocyte lineage. Arch Biochem Biophys 2008, 473:106-111.
47. Harris S.E., Macdougall M., Horn D., Woodruff K., Zimmer S.N., Rebel V.I., et al. Meox2Cre-mediated disruption of CSF-1 leads to osteopetrosis and osteocyte defects. Bone 2012, 50:42-53.
48. Barragan-Adjemian C., Nicolella D., Dusevich V., Dallas M.R., Eick J.D., Bonewald L.F. Mechanism by which MLO-A5 late osteoblasts/early osteocytes mineralize in culture: similarities with mineralization of lamellar bone. Calcif Tissue Int 2006, 79:340-353.
49. Kato Y., Boskey A., Spevak L., Dallas M., Hori M., Bonewald L.F. Establishment of an osteoid preosteocyte-like cell MLO-A5 that spontaneously mineralizes in culture. J Bone Miner Res 2001, 16:1622-1633.