Activation of bone remodeling after fatigue: Differential response to linear microcracks and diffuse damage

Bone

Volumn 47, Issue 4, 2010, Pages 766-772

  Herman, B C ^a,b   Cardoso, L ^a   Majeska, R J ^a   Jepsen, K J ^b   Schaffler, M B ^a  

^a City University of New York   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Diffuse damage; Fatigue; Linear microcracks; Microdamage; Osteocytes; Remodeling

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE INJURY; BONE MATRIX; BONE REMODELING; CELL ACTIVATION; CELL VIABILITY; CONTROLLED STUDY; FATIGUE; FEMALE; NONHUMAN; OSTEOCYTE; OSTEOLYSIS; RAT; ULNA;

ANIMALS; BONE REMODELING; FATIGUE; OSTEOCYTES; RATS; RATS, SPRAGUE-DAWLEY; STRESS, MECHANICAL; ULNA;

EID: 77956404117     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2010.07.006     Document Type: Article

References (80)

1. Altenburger M.J., Schirrmeister J.F., Lussi A., Klasser M., Hellwig E. In situ fluoride retention and remineralization of incipient carious lesions after the application of different concentrations of fluoride. Eur J Oral Sci 2009, 117(1):58-63.
2. Bederson J.B., Levy A.L., Ding W.H., Kahn R., DiPerna C.A., Jenkins A.L., et al. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 1998, 42(2):352-360.
3. Bentolila V., Boyce T.M., Fyhrie D.P., Drumb R., Skerry T.M., Schaffler M.B. Intracortical remodeling in adult rat long bones after fatigue loading. Bone 1998, 23:275-281.
4. Boskey A.L. Bone mineralization. Bone mechanics handbook 2001, CRC Press, New York. 2 ed. S.C. Cowin (Ed.).
5. Boskey A.L., Wright T.M., Blank R.D. Collagen and bone strength. J Bone Miner Res 1999, 14:330-335.
6. Bonewald L.F. Osteocyte biology: its implications for osteoporosis. J Musculoskelet Neuronal Interact 2004, 4:101-104.
7. Boyce T.M., Fyhrie D., Glotkowski M.C., Radin E.L., Schaffler M.B. Damage type and strain mode associations in human compact bone bending fatigue. J Orthop Res 1998, 16(3):322-329.
8. Boyde A. The real response of bone to exercise. J Anat 2003, 203(2):173-189.
9. Burr D.B., Martin R.B., Schaffler M.B., Radin E.L. Bone remodeling in response to in vivo fatigue microdamage. J Biomech 1985, 18:189-200.
10. Burr D.B., Stafford T. Validity of the bulk-staining technique to separate artifactual from in vivo bone microdamage. Clin Orthop 1990, 260:305-308.
11. Burr D.B., Milgrom C., Fyhrie D., Forwood M., Nyska M., Finestone A., et al. In vivo measurement of human tibial strains during vigorous activity. Bone 1996, 18:405-410.
12. Burr D.B., Forwood M.R., Fyhrie D.P., Martin R.B., Schaffler M.B., Turner C.H. Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res 1997, 12:6-15.
13. Burr D.B. Targeted and nontargeted remodeling. Bone 2002, 30:2-4.
14. Cai F., Shen P., Walker G.D., Reynolds C., Yuan Y., Reynolds E.C. Remineralization of enamel subsurface lesions by chewing gum with added calcium. J Dent 2009, 37(10):763-768.
15. Cardoso L., Herman B.C., Verborgt O., Laudier D.M., Majeska R.J., Schaffler M.B. Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue. J Bone Miner Res 2009, 24(4):597-605.
16. Cheng Y., Deshmukh M., D'Costa A., Demaro J.A., Gidday J.M., Shah A., et al. Caspase inhibitor affords neuroprotection with delayed administration in a rat model of neonatal hypoxic-ischemic brain injury. J Clin Invest 1998, 101(9):1992-1999.
17. Chong Z.Z., Kang J.Q., Maiese K. Essential cellular regulatory elements of oxidative stress in early and late phases of apoptosis in the central nervous system. Antioxid Redox Signal 2004, 6(2):277-287.
18. Colopy S.A., Benz-Dean J., Barrett J.G., Sample S.J., Lu Y., Danova N.A., et al. Response of the osteocyte syncytium adjacent to and distant from linear microcracks during adaptation to cyclic fatigue loading. Bone 2004, 35(4):881-891.
19. Cross K.J., Huq N.L., Palamara J.E., Perich J.W., Reynolds E.C. Physicochemical characterization of casein phosphopeptide-amorphous calcium phosphate nanocomplexes. J Biol Chem 2005, 280(15):15362-15369.
20. Diab T., Sit S., Kim D., Rho J., Vashishth D. Age-dependent fatigue behaviour of human cortical bone. Eur J Morphol 2005, 42(1-2):53-59.
21. Diab T., Condon K.W., Burr D.B., Vashishth D. Age-related change in the damage morphology of human cortical bone and its role in bone fragility. Bone 2006, 38(3):427-431.
22. Diab T., Vashishth D. Morphology, localization and accumulation of in vivo microdamage in human cortical bone. Bone 2007, 40:612-618.
23. Dong X.N., Guda T., Millwater H.R., Wang X. Probabilistic failure analysis of bone using a finite element model of mineral-collagen composites. J Biomech 2009, 42(3):202-209.
24. Ekenman I., Milgrom C., Finestone A., Begin M., Olin C., Arndt T., et al. The role of biomechanical shoe orthoses in tibial stress fracture prevention. Am J Sports Med 2002, 30:866-870.
25. Fazzalari N.L., Kuliwaba J.S., Forwood M.R. Cancellous bone microdamage in the proximal femur: influence of age and osteoarthritis on damage morphology and regional distribution. Bone 2002, 31(6):697-702.
26. Feng J.Q., Huang H., Lu Y., Ye L., Xie Y., Tsutsui T.W., et al. The Dentin matrix protein 1 (Dmp1) is specifically expressed in mineralized, but not soft, tissues during development. J Dent Res 2003, 82(10):776-780.
27. Fisher M. The ischemic penumbra: identification, evolution and treatment concepts. Cerebrovasc Dis 2004, 17(Suppl 1):1-6.
28. Follet H., Li J., Phipps R.J., Hui S., Condon K.W., Burr D.B. Risedronate and alendronate suppress osteocyte apoptosis following cyclic fatigue loading. Bone 2007, 40(4):1172-1177.
29. Frank J.D., Ryan M., Kalscheur V.L., Ruaux-Mason C.P., Hozak R.R., Muir P. Aging and accumulation of microdamage in canine bone. Bone 2002, 30(1):201-206.
30. Frost H.M. The laws of bone structure 1964, Charles C. Thomas, Springfield, Illinois.
31. Frost H.M. Presence of microscopic cracks in vivo in bone. Henry Ford Hosp Med Bull 1960, 8:25-35.
32. 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(5):807-817.
33. Gottlieb R.A., Burleson K.O., Kloner R.A., Babior B.M., Engler R.L. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 1994, 94(4):1621-1628.
34. Gowen L.C., Petersen D.N., Mansolf A.L., Qi H., Stock J.L., Tkalcevic G.T., et al. Targeted disruption of the osteoblast/ osteocyte factor 45 gene (OF45) results in increased bone formation and bone mass. J Biol Chem 2003, 278(3):1998-2007.
35. Hara A.T., Gonzalez-Cabezas C., Creeth J., Zero D.T. The effect of human saliva substitutes in an erosion-abrasion cycling model. Eur J Oral Sci 2008, 116(6):552-556.
36. He G., Dahl T., Veis A., George A. Nucleation of apatite crystals in vitro by self-assembled dentin matrix protein 1. Nat Mater 2003, 2(8):552-558.
37. Herman B.C., Laudier D.M., Cardoso L., Zhu L.-L., Li Y., Majeska R.J., et al. Acute osteocyte response to fatigue microdamage: production of HIF-1α and VEGF-A. Orthop Trans 2007, 32:118.
38. Hsieh Y.F., Silva M.J. In vivo fatigue loading of the rat ulna induces both bone formation and resorption and leads to time-related changes in bone mechanical properties and density. J Orthop Res 2002, 20(4):764-771.
39. Igarashi M., Kamiya N., Ito K., Takagi M. In situ localization and in vitro expression of osteoblast/ osteocyte factor 45 mRNA during bone cell differentiation. Histochem J 2002, 34(5):255-263.
40. Ito H., Koefoed M., Tiyapatanaputi P., Gromov K., Goater J.J., Carmouche J., et al. Remodeling of cortical bone allografts mediated by adherent rAAV-RANKL and VEGF gene therapy. Nat Med 2005, 11(3):291-297.
41. Jee W.S.S., Li X.J., Schaffler M.B. Adaptation of diaphyseal structure with aging and increased mechanical usage in the adult rat: a histomorphometrical and biomechanical study. Anat Rec 1991, 230(3):332-338.
42. Komaba H., Fukagawa M. FGF23: a key player in mineral and bone disorder in CKD. Nefrologia 2009, 29(5):392-396.
43. Kotha S.P., Hsieh Y.F., Strigel R.M., Muller R., Silva M.J. Experimental and finite element analysis of the rat ulnar loading model-correlations between strain and bone formation following fatigue loading. J Biomech 2004, 37:541-548.
44. Lee T.C., Myers E.R., Hayes W.C. Fluorescence-aided detection of microdamage in compact bone. J Anat 1998, 193(Pt 2):179-184.
45. Li C.Y., Schaffler M.B., Wolde-Semait H.T., Hernandez C.J., Jepsen K.J. Genetic background influences cortical bone response to ovariectomy. J Bone Miner Res 2005, 20:2150-2158.
46. Martin R.B. Is all cortical bone remodeling initiated by microdamage?. Bone 2002, 30(1):8-13.
47. Martin R.B. Fatigue microdamage as an essential element of bone mechanics and biology. Calcif Tissue Int 2003, 73(2):101-107.
48. Mashiba T., Hirano T., Turner C.H., Forwood M.R., Johnston C.C., Burr D.B. Suppressed bone turnover by bisphosphonates increases microdamage accumulation and reduces some biomechanical properties in dog rib. J Bone Miner Res 2000, 15(4):613-620.
49. Milgrom C., Finestone A., Shlamkovitch N., Giladi M., Radin E. Anterior knee pain caused by overactivity: a long term prospective followup. Clin Orthop Relat Res 1996, 331:256-260.
50. Mori S., Burr D.B. Increased intracortical remodeling following fatigue damage. Bone 1993, 14:103-109.
51. Muir P., Johnson K.A., Ruaux-Mason C.P. In vivo matrix microdamage in a naturally occurring canine fatigue fracture. Bone 1999, 25(5):571-576.
52. Nalla R.K., Kruzic J.J., Kinney J.H., Ritchie R.O. Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials 2005, 26:217-231.
53. Nampei A., Hashimoto J., Hayashida K., Tsuboi H., Shi K., Tsuji I., et al. Matrix extracellular phosphoglycoprotein (MEPE) is highly expressed in osteocytes in human bone. J Bone Miner Metab 2004, 22(3):176-184.
54. Noble B.S., Peet N., Stevens H.Y., Brabbs A., Mosley J.R., Reilly G.C., et al. Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol Cell Physiol 2003, 284(4):C934-C943.
55. Noble B. Microdamage and apoptosis. Eur J Morphol 2005, 42(1-2):91-98.
56. Norman T.L., Wang Z. Microdamage of human cortical bone: incidence and morphology in long bones. Bone 1997, 20:375-379.
57. Nunamaker D.M., Butterweck D.M., Provost M.T. Fatigue fractures in thoroughbred racehorses: relationships with age, peak bone strain, and training. J Orthop Res 1990, 8:604-611.
58. O'Brien F.J., Hardima D.A., Hazenberg J.G., Mercy M.V., Mohsin S., Taylor D., et al. The behaviour of microcracks in compact bone. Eur J Morphol 2005, 42:71-79.
59. Razzaque M.S. The FGF23-Klotho axis: endocrine regulation of phosphate homeostasis. Nat Rev Endocrinol 2009, 5(11):611-619.
60. Reynolds E.C. Calcium phosphate-based remineralization systems: scientific evidence?. Aust Dent J 2008, 53(3):268-273.
61. Rodriguez M., Lucchesi B.R., Schaper J. Apoptosis in myocardial infarction. Ann Med 2002, 34(6):470-479.
62. Saito T., Nishii Y., Yasuda T., Ito N., Suzuki H., Igarashi T., et al. Familial hypophosphatemic rickets caused by a large deletion in PHEX gene. Eur J Endocrinol 2009, 161(4):647-651.
63. Schaffler M.B., Li X.J., Jee W.S., Ho S.W., Stern P.J. Skeletal tissue responses to thermal injury: an experimental study. Bone 1988, 9:397-406.
64. Schaffler M.B., Pitchford W.C., Choi K., Riddle J.M. Examination of compact bone microdamage using back-scattered electron microscopy. Bone 1994, 15:483-488.
65. Schaffler M.B., Choi K., Milgrom C. Aging and matrix microdamage accumulation in human compact bone. Bone 1995, 17:521-525.
66. Schaffler M.B. Bone fatigue and remodeling in the development of stress fractures. Musculoskeletal fatigue and stress fractures 2001, 161-182. CRC Press, Boca Raton.
67. Schaffler M.B. Role of bone turnover in microdamage. Osteoporos Int 2003, 14:73-80.
68. Silva M.J., Uthgenannt B.A., Rutlin J.R., Wohl G.R., Lewis J.S., Welch M.J. In vivo skeletal imaging of 18F-fluoride with positron emission tomography reveals damage- and time-dependent responses to fatigue loading in the rat ulna. Bone 2006, 39(2):229-236.
69. Silva M.J., Touhey D.C. Bone formation after damaging in vivo fatigue loading results in recovery of whole-bone monotonic strength and increased fatigue life. J Orthop Res 2007, 25(2):52-61.
70. Tami A.E., Nasser P., Verborgt O., Schaffler M.B., Knothe Tate M.L. The role of interstitial fluid flow in the remodeling response to fatigue loading. J Bone Miner Res 2002, 17:2030-2037.
71. ten Cate J.M. Remineralization of deep enamel dentine caries lesions. Aust Dent J 2008, 53(3):281-285.
72. Tommasini S.M., Nasser P., Schaffler M.B., Jepsen K.J. Relationship between bone morphology and bone quality in male tibias: implications for stress fracture risk. J Bone Miner Res 2005, 20(8):1372-1380.
73. Turner C.H. Biomechanics of bone: determinants of skeletal fragility and bone quality. Osteoporos Int 2002, 13:97-104.
74. Vashishth D., Koontz J., Qiu S.J., Lundin-Cannon D., Yeni Y.N., Schaffler M.B., et al. In vivo diffuse damage in human vertebral trabecular bone. Bone 2000, 26:147-152.
75. Verborgt O., Gibson G.J., Schaffler M.B. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res 2000, 15:60-67.
76. Verborgt O., Tatton N.A., Majeska R.J., Schaffler M.B. Spatial distribution of Bax and Bcl-2 in osteocytes after bone fatigue: complementary roles in bone remodeling regulation?. J Bone Miner Res 2002, 17:907-914.
77. Wang L., Wan 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 2005, 102(33):11911-11916.
78. Winkler D.G., Sutherland M.K., Geoghegan J.C., Yu C., Hayes T., Skonier J.E., et al. Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J 2003, 22:6267-6276.
79. Young M.F. Bone matrix proteins: their function, regulation, and relationship to osteoporosis. Osteoporos Int 2003, 14(Suppl 3):S35-S42.
80. Zar J.H. Biostatistical analysis 1999, Prentice Hall, Upper Saddle River. 4th ed.