Modeling fluorescence recovery after photobleaching in loaded bone: Potential applications in measuring fluid and solute transport in the osteocytic lacunar-canalicular system

Annals of Biomedical Engineering

Volumn 36, Issue 12, 2008, Pages 1961-1977

  Zhou, Xiaozhou ^a   Novotny, John E ^a   Wang, Liyun ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Bone; Fluid flow; FRAP; Intermittent loading; Osteocyte; Solute transport; Strouhal number

Indexed keywords

BIOCHEMISTRY; BONE; FLUORESCENCE; LIGHT EMISSION; LUMINESCENCE; PHOTOBLEACHING; SOLUTE TRANSPORT; THEOREM PROVING;

BONE ADAPTATIONS; BONE DISEASES; FLOW BEHAVIORS; FLUID FLOW; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FRAP; INTERMITTENT LOADING; MEAN FLOWS; MECHANICAL LOADINGS; OSCILLATION EFFECTS; OSTEOCYTE; PORO ELASTICITIES; POTENTIAL APPLICATIONS; RECOVERY RATES; SOURCE AND SINKS;

TRANSPORT PROPERTIES;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOMECHANICS; BONE; CYTOLOGY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HAVERSIAN CANAL; HUMAN; METABOLISM; OSTEOCYTE; SOLUTION AND SOLUBILITY; THEORETICAL MODEL; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BIOMECHANICS; BONE AND BONES; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HAVERSIAN SYSTEM; HUMANS; MODELS, BIOLOGICAL; MODELS, THEORETICAL; OSTEOCYTES; SOLUTIONS;

EID: 56449127929     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-008-9566-0     Document Type: Article

References (71)

1. T. Beno Y. J. Yoon S. C. Cowin S. P. Fritton 2006 Estimation of bone permeability using accurate microstructural measurements J. Biomech. 39 2378 2387 10.1016/j.jbiomech.2005.08.005
2. V. Bentolila T. M. Boyce D. P. Fyhrie R. Drumb T. M. Skerry M. B. Schaffler 1998 Intracortical remodeling in adult rat long bones after fatigue loading Bone 23 275 281 10.1016/S8756-3282(98)00104-5
3. S. A. Bloomfield 2001 Cellular and molecular mechanisms for the bone response to mechanical loading Int. J. Sport Nutr. Exerc. Metab. 11(Suppl) S128 S136
4. L. F. Bonewald 2007 Osteocytes as dynamic multifunctional cells Ann. N. Y. Acad. Sci. 1116 281 290 10.1196/annals.1402.018
5. E. H. Burger J. Klein-Nulend 1999 Mechanotransduction in bone-role of the lacuno-canalicular network FASEB J. 13(Suppl) S101 S112
6. E. H. Burger J. Klein-Nulend A. van der Plas P. J. Nijweide 1995 Function of osteocytes in bone-their role in mechanotransduction J. Nutr. 125 2020S 2023S
7. V. Cane G. Marotti G. Volpi D. Zaffe S. Palazzini F. Remaggi M. A. Muglia 1982 Size and density of osteocyte lacunae in different regions of long bones Calcif. Tissue Int. 34 558 563 10.1007/BF02411304
8. R. R. Cooper J. W. Milgram R. A. Robinson 1966 Morphology of the osteon. An electron microscopic study J. Bone Joint Surg. Am. 48 1239 1271
9. S. C. Cowin 1999 Bone poroelasticity J. Biomech. 32 217 238 10.1016/S0021-9290(98)00161-4
10. S. C. Cowin S. Weinbaum Y. Zeng 1995 A case for bone canaliculi as the anatomical site of strain generated potentials J. Biomech. 28 1281 1297 10.1016/0021-9290(95)00058-P
11. R. M. Dillaman R. D. Roer D. M. Gay 1991 Fluid movement in bone: theoretical and empirical J. Biomech. 24 Suppl 1 163 177 10.1016/0021-9290(91) 90386-2
12. J. S. Dodd J. A. Raleigh T. S. Gross 1999 Osteocyte hypoxia: a novel mechanotransduction pathway Am. J. Physiol. 277 C598 C602
13. R. Duriez J. Duriez 1981 Periosteocyte demineralization in disuse osteoporsis. The effect of calcitonin Int. Orthop. 5 299 304 10.1007/BF00271086
14. D. M. Eckmann 1998 Bolus contaminant dispersion in oscillating flow in curved tubes J. Biomech. Eng. 120 238 244 10.1115/1.2798307
15. J. Q. Feng L. M. Ward S. Liu Y. Lu Y. Xie B. Yuan X. Yu F. Rauch S. I. Davis S. Zhang H. Rios M. K. Drezner L. D. Quarles L. F. Bonewald K. E. White 2006 Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism Nat. Genet. 38 1310 1315 10.1038/ng1905
16. M. Ferretti M. A. Muglia F. Remaggi V. Cane C. Palumbo 1999 Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. II. Parallel-fibered and lamellar bones Ital. J. Anat. Embryol. 104 121 131
17. P. Fornells J. M. Garcia-Aznar M. Doblare 2007 A finite element dual porosity approach to model deformation-induced fluid flow in cortical bone Ann. Biomed. Eng. 35 1687 1698 10.1007/s10439-007-9351-5
18. S. P. Fritton K. J. McLeod C. T. Rubin 2000 Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains J. Biomech. 33 317 325 10.1016/S0021-9290(99)00210-9
19. J. C. Fritton E. R. Myers T. M. Wright M. C. van der Meulen 2005 Loading induces site-specific increases in mineral content assessed by microcomputed tomography of the mouse tibia Bone 36 1030 1038 10.1016/j.bone.2005.02.013
20. D. P. Gaver III J. Solway N. Punjabi D. Elad J. B. Grotberg N. Gavriely 1992 Gas dispersion in volume-cycled tube flow. II. Tracer bolus experiments J. Appl. Physiol. 72 321 331
21. D. C. Genetos C. J. Kephart Y. Zhang C. E. Yellowley H. J. Donahue 2007 Oscillating fluid flow activation of gap junction hemichannels induces ATP release from MLO-Y4 osteocytes J. Cell Physiol. 212 207 214 10.1002/jcp.21021
22. I. Glasgow N. Aubry 2003 Enhancement of microfluidic mixing using time pulsing Lab. Chip 3 114 120 10.1039/b302569a
23. I. Glasgow S. Lieber N. Aubry 2004 Parameters influencing pulsed flow mixing in microchannels Anal. Chem. 76 4825 4832 10.1021/ac049813m
24. J. Gluhak-Heinrich L. Ye L. F. Bonewald J. Q. Feng M. MacDougall S. E. Harris D. Pavlin 2003 Mechanical loading stimulates dentin matrix protein 1 (DMP1) expression in osteocytes in vivo J. Bone Miner. Res. 18 807 817 10.1359/jbmr.2003.18.5.807
25. W. L. Goffe G. D. Ferrier J. Rogers 1994 Global optimization of statistical functions with simulated annealing J. Econom. 60 65 99 10.1016/0304-4076(94)90038-8
26. T. S. Gross N. Akeno T. L. Clemens S. Komarova S. Srinivasan D. A. Weimer S. Mayorov 2001 Selected contribution: osteocytes upregulate HIF-1alpha in response to acute disuse and oxygen deprivation J. Appl. Physiol. 90 2514 2519
27. T. S. Gross K. A. King N. A. Rabaia P. Pathare S. Srinivasan 2005 Upregulation of osteopontin by osteocytes deprived of mechanical loading or oxygen J. Bone Miner. Res. 20 250 256 10.1359/JBMR.041004
28. S. Gururaja H. J. Kim C. C. Swan R. A. Brand R. S. Lakes 2005 Modeling deformation-induced fluid flow in cortical bone's canalicular-lacunar system Ann. Biomed. Eng. 33 7 25 10.1007/s10439-005-8959-6
29. R. G. Keanini R. D. Roer R. M. Dillaman 1995 A theoretical model of circulatory interstitial fluid flow and species transport within porous cortical bone J. Biomech. 28 901 914 10.1016/0021-9290(94)00157-Y
30. J. Klein-Nulend C. M. Semeins N. E. Ajubi P. J. Nijweide E. H. Burger 1995 Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts-correlation with prostaglandin upregulation Biochem. Biophys. Res. Commun. 217 640 648 10.1006/bbrc.1995.2822
31. M. L. Knothe Tate U. Knothe 2000 An ex vivo model to study transport processes and fluid flow in loaded bone J. Biomech. 33 247 254 10.1016/S0021-9290(99)00143-8
32. M. L. Knothe Tate P. Niederer U. Knothe 1998 In vivo tracer transport through the lacunocanalicular system of rat bone in an environment devoid of mechanical loading Bone 22 107 117 10.1016/S8756-3282(97)00234-2
33. R. H. Kufahl S. Saha 1990 A theoretical model for stress-generated fluid flow in the canaliculi-lacunae network in bone tissue J. Biomech. 23 171 180 10.1016/0021-9290(90)90350-C
34. H. A. Leddy F. Guilak 2003 Site-specific molecular diffusion in articular cartilage measured using fluorescence recovery after photobleaching Ann. Biomed. Eng. 31 753 760 10.1114/1.1581879
35. T. Lemaire S. Naili A. Remond 2006 Multiscale analysis of the coupled effects governing the movement of interstitial fluid in cortical bone Biomech. Model. Mechanobiol. 5 39 52 10.1007/s10237-005-0009-7
36. C. Y. Li M. B. Schaffler H. T. Wolde-Semait C. J. Hernandez K. J. Jepsen 2005 Genetic background influences cortical bone response to ovariectomy J. Bone Miner. Res. 20 2150 2158 10.1359/JBMR.050819
37. W. Li X. Zhou J. E. Novotny L. Wang 2007 Solute transport among osteocytes in live animals J. Musculoskelet. Neuronal Interact. 7 366 367
38. A. F. Mak J. D. Zhang 2001 Numerical simulation of streaming potentials due to deformation-induced hierarchical flows in cortical bone J. Biomech. Eng. 123 66 70 10.1115/1.1336796
39. G. Marotti M. Ferretti F. Remaggi C. Palumbo 1995 Quantitative evaluation on osteocyte canalicular density in human secondary osteons Bone 16 125 128 10.1016/S8756-3282(94)00019-0
40. G. Marotti F. Remaggi D. Zaffe 1985 Quantitative investigation on osteocyte canaliculi in human compact and spongy bone Bone 6 335 337 10.1016/8756-3282(85)90325-4
41. L. Y. Mi S. P. Fritton M. Basu S. C. Cowin 2005 Analysis of avian bone response to mechanical loading-part one: distribution of bone fluid shear stress induced by bending and axial loading Biomech. Model. Mechanobiol. 4 118 131 10.1007/s10237-004-0065-4
42. B. Noble 2005 Microdamage and apoptosis Eur. J. Morphol. 42 91 98 10.1080/09243860500096248
43. N. Petrov S. R. Pollack 2003 Comparative analysis of diffusive and stress induced nutrient transport efficiency in the lacunar-canalicular system of osteons Biorheology 40 347 353
44. K. Piekarski M. Munro 1977 Transport mechanism operating between blood supply and osteocytes in long bones Nature 269 80 82 10.1038/269080a0
45. K. E. Poole R. L. van Bezooijen N. Loveridge H. Hamersma S. E. Papapoulos C. W. Lowik J. Reeve 2005 Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation FASEB J. 19 1842 1844
46. Y. X. Qin W. Lin C. Rubin 2002 The pathway of bone fluid flow as defined by in vivo intramedullary pressure and streaming potential measurements Ann. Biomed. Eng. 30 693 702 10.1114/1.1483863
47. E. A. Reits J. J. Neefjes 2001 From fixed to FRAP: measuring protein mobility and activity in living cells Nat. Cell Biol. 3 E145 E147 10.1038/35078615
48. F. Remaggi V. Cane C. Palumbo M. Ferretti 1998 Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. I. Woven-fibered and parallel-fibered bones Ital. J. Anat. Embryol. 103 145 155
49. H. F. Rios L. Ye V. Dusevich D. Eick L. F. Bonewald J. Q. Feng 2005 DMP1 is essential for osteocyte formation and function J. Musculoskelet. Neuronal Interact. 5 325 327
50. A. G. Robling P. J. Niziolek L. A. Baldridge K. W. Condon M. J. Allen I. Alam S. M. Mantila J. Gluhak-Heinrich T. M. Bellido S. E. Harris C. H. Turner 2007 Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin J. Biol. Chem. 283 5866 5875
51. S. M. Schmidt M. J. McCready A. E. Ostafin 2005 Effect of oscillating fluid shear on solute transport in cortical bone J. Biomech. 38 2337 2343
52. G. Silvestrini P. Ballanti M. Sebastiani M. Leopizzi M. Di Vito E. Bonucci 2007 OPG and RANKL mRNA and protein expressions in the primary and secondary metaphyseal trabecular bone of PTH-treated rats are independent of that of SOST J. Mol. Histol. 39 237 242
53. T. H. Smit J. M. Huyghe S. C. Cowin 2002 Estimation of the poroelastic parameters of cortical bone J. Biomech. 35 829 835 10.1016/S0021-9290(02)00021-0
54. R. Steck P. Niederer M. L. Knothe Tate 2003 A finite element analysis for the prediction of load-induced fluid flow and mechanochemical transduction in bone J. Theor. Biol. 220w 249 259 10.1006/jtbi.2003.3163
55. M. Su H. Jiang P. Zhang Y. Liu E. Wang A. Hsu H. Yokota 2006 Knee-loading modality drives molecular transport in mouse femur Ann. Biomed. Eng. 34 1600 1606 10.1007/s10439-006-9171-z
56. E. Takai R. L. Mauck C. T. Hung X. E. Guo 2004 Osteocyte viability and regulation of osteoblast function in a 3D trabecular bone explant under dynamic hydrostatic pressure J. Bone Miner. Res. 19 1403 1410 10.1359/JBMR.040516
57. S. Tatsumi K. Ishii N. Amizuka M. Li T. Kobayashi K. Kohno M. Ito S. Takeshita K. Ikeda 2007 Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction Cell Metab. 5 464 475 10.1016/j.cmet.2007.05. 001
58. O. Verborgt G. J. Gibson M. B. Schaffler 2000 Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo J. Bone Miner. Res. 15 60 67 10.1359/jbmr.2000.15.1.60
59. L. Wang C. Ciani S. B. Doty S. P. Fritton 2004 Delineating bone's interstitial fluid pathway in vivo Bone 34 499 509 10.1016/j.bone.2003.11.022
60. L. Wang S. C. Cowin S. Weinbaum S. P. Fritton 2000 Modeling tracer transport in an osteon under cyclic loading Ann. Biomed. Eng. 28 1200 1209 10.1114/1.1317531
61. L. Wang S. P. Fritton S. C. Cowin S. Weinbaum 1999 Fluid pressure relaxation depends upon osteonal microstructure: modeling an oscillatory bending experiment J. Biomech. 32 663 672 10.1016/S0021-9290(99)00059-7
62. L. Wang S. P. Fritton S. Weinbaum S. C. Cowin 2003 On bone adaptation due to venous stasis J. Biomech. 36 1439 1451 10.1016/S0021-9290(03)00241-0
63. Y. Wang K. Hutter 2001 Comparisons of numerical methods with respect to convectively dominated problems Int. J. Numer. Meth. Fluids 37 721 745 10.1002/fld.197
64. L. Wang Y. Wang Y. Han S. C. Henderson R. J. Majeska S. Weinbaum M. B. Schaffler 2005 In situ measurement of solute transport in the bone lacunar-canalicular system Proc. Natl. Acad. Sci. USA 102 11911 11916 10.1073/pnas.0505193102
65. S. Weinbaum S. C. Cowin Y. Zeng 1994 A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses J. Biomech. 27 339 360 10.1016/0021-9290(94)90010-8
66. I. Westbroek N. E. Ajubi M. J. Alblas C. M. Semeins J. Klein-Nulend E. H. Burger P. J. Nijweide 2000 Differential stimulation of prostaglandin G/H synthase-2 in osteocytes and other osteogenic cells by pulsating fluid flow Biochem. Biophys. Res. Commun. 268 414 419 10.1006/bbrc.2000.2154
67. L. You S. C. Cowin M. B. Schaffler S. Weinbaum 2001 A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix J. Biomech. 34 1375 1386 10.1016/S0021-9290(01)00107-5
68. L. You S. Temiyasathit P. Lee C. H. Kim P. Tummala W. Yao W. Kingery A. M. Malone R. Y. Kwon C. R. Jacobs 2008 Osteocytes as mechanosensors in the inhibition of bone resorption due to mechanical loading Bone 42 172 179 10.1016/j.bone.2007.09.047
69. L. D. You S. Weinbaum S. C. Cowin M. B. Schaffler 2004 Ultrastructure of the osteocyte process and its pericellular matrix Anat. Rec. A Discov. Mol. Cell Evol. Biol. 278 505 513 10.1002/ar.a.20050
70. Y. Zeng S. C. Cowin S. Weinbaum 1994 A fiber matrix model for fluid flow and streaming potentials in the canaliculi of an osteon Ann. Biomed. Eng. 22 280 292 10.1007/BF02368235
71. X. Zhang R. H. Adamson F. R. Curry S. Weinbaum 2006 A 1-D model to explore the effects of tissue loading and tissue concentration gradients in the revised Starling principle Am. J. Physiol. Heart Circ. Physiol. 291 H2950 H2964 10.1152/ajpheart.01160.2005