Mechanisms of osteocyte mechanotransduction

Clinical Reviews in Bone and Mineral Metabolism

Volumn 8, Issue 4, 2010, Pages 163-169

  Bakker, Astrid D ^a   Klein Nulend, Jenneke ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Adaptation; Fluid flow; Fluid shear stress; Mechanotransduction; Osteocytes; Strain

Indexed keywords

F ACTIN; INOSINE PHOSPHATE; INTEGRIN; MATRIX PROTEIN; PAXILLIN; RNA;

ARTICLE; BONE CELL; BONE DEFORMATION; BONE DEVELOPMENT; BONE MARROW CELL; BONE MATRIX; BONE STRESS; BONE TISSUE; CELL ADHESION; CELL MEMBRANE; CELL STRUCTURE; CYTOPLASM; ELECTRIC POTENTIAL; ELECTRON TOMOGRAPHY; ENDOTHELIUM CELL; EUKARYOTIC FLAGELLUM; EXTRACELLULAR FLUID; FLUID FLOW; HUMAN; INTERSTITIAL FLUID; MECHANICAL STRESS; MECHANOTRANSDUCTION; MEMBRANE PERMEABILITY; MESENCHYMAL STEM CELL; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCYTE; OSTEOLYSIS; RNA SYNTHESIS; SHEAR STRESS; THEORETICAL MODEL; VELOCITY;

EID: 79960134365     PISSN: 15348644     EISSN: 15590119     Source Type: Journal    
DOI: 10.1007/s12018-010-9079-x     Document Type: Article

References (68)

1. Jilka RL. Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone. 2007;40:1434-46. (Pubitemid 46756429)
2. Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR. Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature. 1986;319:516-8. (Pubitemid 16212936)
3. Li YP, Stashenko P. Proinflammatory cytokines tumor necrosis factor-alpha and IL-6, but not IL-1, down-regulate the osteocalcin gene promoter. J Immunol. 1992;148:788-94.
4. Gowen M, Wood DD, Ihrie EJ, McGuire MK, Russell RG. An interleukin 1 like factor stimulates bone resorption in vitro. Nature. 1983;306:378-80. (Pubitemid 14242749)
5. Vezeridis PS, Semeins CM, Chen Q, Klein-Nulend J. Osteocytes subjected to pulsating fluid flow regulate osteoblast proliferation and differentiation. Biochem Biophys Res Commun. 2005; 348:1082-8. (Pubitemid 44233525)
6. Kulkarni RN, Bakker AD, Everts V, Klein-Nulend J. Inhibition of osteoclastogenesis by mechanically loaded osteocytes: Involvement of MEPE. Calcif Tissue Int. 2010;87:461-8.
7. Santos A, Bakker AD, Zandieh-Doulabi B, Semeins CM, Klein- Nulend J. Pulsating fluid flow modulates gene expression of proteins involved in Wnt signaling pathways in osteocytes. J Orthop Res. 2009;27:1280-7.
8. You L, Temiyasathit S, Lee P, Kim CH, Tummala P, Yao W, Kingery W, Malone AM, Kwon RY, Jacobs CR. Osteocytes as mechanosensors in the inhibition of bone resorption due to mechanical loading. Bone. 2008;42:172-9.
9. Tan SD, de Vries TJ, Kuijpers-Jagtman AM, Semeins CM, Everts V, Klein-Nulend J. Osteocytes subjected to fluid flow inhibit osteoclast formation and bone resorption. Bone. 2007;41: 745-51.
10. Robling AG, Bellido T, Turner CH. Mechanical stimulation in vivo reduces osteocyte expression of sclerostin. J Musculoskelet Neuronal Interact. 2006;6:354. (Pubitemid 46099713)
11. Mullender MG, Huiskes R. Proposal for the regulatory mechanism of Wolff's law. J Orthop Res. 1995;13:503-12.
12. Mullender MG, Huiskes R. Osteocytes and bone lining cells: Which are the best candidates for mechano-sensors in cancellous bone? Bone. 1997;20:527-32. (Pubitemid 27270466)
13. Klein-Nulend J, Semeins CM, Ajubi NE, Nijweide PJ, Burger EH. Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts-correlation with prostaglandin upregulation. Biochem Biophys Res Commun. 1995;217: 640-8. (Pubitemid 26011757)
14. El-Haj AJ, Minter SL, Rawlinson SCF, Suswillo R, Lanyon LE. Cellular responses to mechanical loading in vitro. J Bone Miner Res. 1990;5:923-32. (Pubitemid 20307109)
15. Dallas SL, Zaman G, Pead MJ, Lanyon LE. Early strain-related changes in cultured embryonic chick tibiotarsi parallel those associated with adaptive modeling in vivo. J Bone Miner Res. 1993;8:251-9. (Pubitemid 23095890)
16. Lee K, Jessop H, Suswillo R, Zaman G, Lanyon LE. Endocrinology: Bone adaptation requires oestrogen receptor-alpha. Nature. 2003;424:389. (Pubitemid 36917478)
17. Lean JM, Jagger CJ, Chambers TJ, Chow JW. Increased insulinlike growth factor I mRNA expression in rat osteocytes in response to mechanical stimulation. Am J Physiol. 1995;268:E318-27.
18. Forwood MR, Kelly WL, Worth NF. Localization of prostaglandin endoperoxidase H synthase (PGHS)-1 and PGHS-2 in bone following mechanical loading in vivo. Anat Rec. 1998;252:580-6. (Pubitemid 28533405)
19. Terai K, Takano-Yamamoto T, Ohba Y, Hiura K, Sugimoto M, Sato M, Kawahata H, Inaguma N, Kitamura Y, Nomura S. Role of osteopontin in bone remodeling caused by mechanical stress. J Bone Miner Res. 1999;14:839-49. (Pubitemid 29262877)
20. Tatsumi S, Ishii K, Amizuka N, Li M, Kobayashi T, Kohno K, Ito M, Takeshita S, Ikeda K. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab. 2007;5:464-75. (Pubitemid 46825494)
21. Burger EH, Klein-Nulend J. Mechanotransduction in bone: Role of the lacuno-canalicular network. FASEB J. 1999;13:S101-12.
22. Knothe-Tate ML, Niederer P, Knothe U. In vivo tracer transport throught the lacunocanalicular system of rat bone in an environment devoid of mechanical loading. Bone. 1998;22:107-17. (Pubitemid 28058500)
23. Knothe-Tate ML, Steck R, Forwood MR, Niederer P. In vivo demonstration of load-induced fluid flow in the rat tibia and its potential implications for processes associated with functional adaptation. J Exp Biol. 2000;203:2737-45.
24. 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. 2010. doi:10.1002/jbmr.211.
25. Luo G, Cowin SC, Sadegh AM, Arramon YP. Implementation of strain rate as a bone remodeling stimulus. J Biomech Eng. 1995;117:329-38.
26. Mosley JR, Lanyon LE. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone. 1998;23:313-8. (Pubitemid 28454622)
27. Turner CH, Forwood MR, Otter MW. Mechanotransduction in bone: Do bone cells act as sensors of fluid flow? FASEB J. 1994;8:875-8. (Pubitemid 24268880)
28. Turner CH, Owan I, Takano Y. Mechanotransduction in bone: Role of strain rate. Am J Physiol. 1995;269:E438-42.
29. Lanyon LE, Rubin CT. Static vs dynamic loads as an influence on bone remodelling. J Biomech. 1984;17:897-905. (Pubitemid 15166456)
30. Piekarski K, Munro M. Transport mechanism operating between blood supply and osteocytes in long bones. Nature. 1977;269:80-2. (Pubitemid 8160686)
31. Pollack SR, Salzstein R, Pienkowski D. The electric double layer in bone and its influence on stress generated potentials. Calcif Tissue Int. 1984;36:S77-81. (Pubitemid 14043319)
32. Hung CT, Allen FD, Pollack SR, Brighton CT. What is the role of the convective current density in the real time calcium response of cultured bone cells to fluid flow? J Biomech. 1996;29:1403-9. (Pubitemid 26329189)
33. Brakemeier S, Eichler I, Hopp H, Köhler R, Hoyer J. Up-regulation of endothelial stretch-activated cation channels by fluid shear stress. Cardiovasc Res. 2002;53:209-18. (Pubitemid 34020782)
34. Reich KM, Gay CV, Frangos JA. Fluid shear stress as a mediator of osteoblast cyclic adenosine monophosphate production. J Cell Physiol. 1990;143:100-4.
35. Bakker AD, Soejima K, Klein-Nulend J, Burger EH. The production of nitric oxide and prostaglandin E2 by primary bone cells is shear stress dependent. J Biomech. 2001;34:671-7. (Pubitemid 32328255)
36. Bakker AD, Klein-Nulend J, Tanck E, Albers GH, Lips P, Burger EH. Additive effects of estrogen and mechanical stress on nitric oxide and prostaglandin E2 production by bone cells from osteoporotic donors. Osteoporos Int. 2005;16:983-9. (Pubitemid 41127109)
37. Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech. 1994;27:339-60. (Pubitemid 24061729)
38. You L, Cowin SC, Schaffler MB, Weinbaum S. A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech. 2001;34:1375-86. (Pubitemid 32970752)
39. Han Y, Cowin SC, Schaffler MB, Weinbaum S. Mechanotransduction and strain amplification in osteocyte cell processes. Proc Natl Acad Sci USA. 2004;101:16689-94. (Pubitemid 39557774)
40. Wang Y, McNamara LM, Schaffler MB, Weinbaum S. A model for the role of integrins in flow induced mechanotransduction in osteocytes. Proc Natl Acad Sci USA. 2007;104:15941-6. (Pubitemid 350035403)
41. Veno P, Nicolella DP, Sivakumar P, Kalajzic I, Rowe D, Harris SE, Bonewald LF, Dallas SL. Live imaging of osteocytes within their lacunae reveals cell body and dendrite motions. J Bone Min Res. 2006;21(Suppl 1):S38.
42. Fritton SP, Weinbaum S. Fluid and solute transport in bone: Flowinduced mechanotransduction. Annu Rev Fluid Mech. 2009;41: 347-74.
43. Lanyon LE, Hampson WG, Goodship AE, Shah JS. Bone deformation recorded in vivo from strain gauges attached to the human tibial shaft. Acta Orthop Scand. 1975;46:256-68.
44. You J, Yellowley CE, Donahue HJ, Zhang Y, Chen Q, Jacobs CR. Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loadinginduced oscillatory fluid flow. Biomech Eng. 2000;122:387-93.
45. Robinson JA, Chatterjee-Kishore M, Yaworsky PJ, Cullen DM, Zhao W, Li C, Kharode Y, Sauter L, Babij P, Brown EL, Hill AA, Akhter MP, Johnson ML, Recker RR, Komm BS, Bex FJ. Wnt/ beta-catenin signaling is a normal physiological response to mechanical loading in bone. J Biol Chem. 2006;281:31720-8. (Pubitemid 46043263)
46. Bacabac RG, Mizuno D, Schmidt CF, MacKintosh FC, Van Loon JJ, Klein-Nulend J, Smit TH. Round versus flat: Bone cell morphology, elasticity, and mechanosensing. J Biomech. 2008;41: 1590-8.
47. Bonivtch AR, Bonewald LF, Nicolella DP. Tissue strain amplification at the osteocyte lacuna: A microstructural finite element analysis. J Biomech. 2007;40:2199-206. (Pubitemid 46977404)
48. Vatsa A, Semeins CM, Smit TH, Klein-Nulend J. Paxillin localisation in osteocytes-is it determined by the direction of loading? Biochem Biophys Res Commun. 2008;377:1019-24.
49. Vatsa A, Breuls RG, Semeins CM, Salmon PL, Smit TH, Klein- Nulend J. Osteocyte morphology in fibula and calvaria-is there a role for mechanosensing? Bone. 2008;43:452-8.
50. Krempien B, Friedrich E, Ritz E. Effect of PTH on osteocyte ultrastructure. Adv Exp Med Biol. 1978;103:437-50.
51. Qing H, Bonewald LF. Osteocyte remodeling of the perilacunar and pericanalicular matrix. Int J Oral Sci. 2009;1:59-65.
52. Gardinier JD, Townend CW, Jen KP, Wu Q, Duncan RL, Wang L. In situ permeability measurement of the mammalian lacunarcanalicular system. Bone. 2010;46:1075-81.
53. Wang L, Fritton SP, Cowin SC, Weinbaum S. Fluid pressure relaxation depends upon osteonal microstructure: Modeling an oscillatory bending experiment. J Biomech. 1999;32:663-72. (Pubitemid 29322085)
54. Liu C, Zhao Y, Cheung WY, Gandhi R, Wang L, You L. Effects of cyclic hydraulic pressure on osteocytes. Bone. 2010;46:1449-56.
55. Klein-Nulend J, van der Plas A, Semeins CM, Ajubi NE, Frangos JA, Nijweide PJ, Burger EH. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J. 1995;9:441-5.
56. Malone AM, Anderson CT, Tummala P, Kwon RY, Johnston TR, Stearns T, Jacobs CR. Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc Natl Acad Sci USA. 2007;104:13325-30. (Pubitemid 47293944)
57. Bell A. The pipe and the pinwheel: Is pressure an effective stimulus for the 9?0 primary cilium? Cell Biol Int. 2008;32:462-8. (Pubitemid 351608566)
58. Lories RJ, Peeters J, Bakker A, Tylzanowski P, Derese I, Schrooten J, Thomas JT, Luyten FP. Articular cartilage and biomechanical properties of the long bones in Frzb-knockout mice. Arthritis Rheum. 2007;56:4095-103. (Pubitemid 350262337)
59. de Jong WC, Korfage JA, Langenbach GE. Variations in habitual bone strains in vivo: Long bone versus mandible. J Struct Biol. 2010;172:311-8.
60. Fritton SP, McLeod KJ, Rubin CT. Quantifying the strain history of bone: Spatial uniformity and self-similarity of low-magnitude strains. J Biomech. 2000;33:317-25.
61. Qin YX, Kaplan T, Saldanha A, Rubin C. Fluid pressure gradients, arising from oscillations in intramedullary pressure, is correlated with the formation of bone and inhibition of intracortical porosity. J Biomech. 2003;36:1427-37. (Pubitemid 37117350)
62. Kwon RY, Meays DR, Tang WJ, Frangos JA. Microfluidic enhancement of intramedullary pressure increases interstitial fluid flow and inhibits bone loss in hindlimb suspended mice. J Bone Miner Res. 2010;25:1798-807.
63. Kwon RY, Frangos JA. Quantification of lacunar-canalicular interstitial fluid flow through computational modeling of fluorescence recovery after photobleaching. Cell Mol Bioeng. 2010; 3:296-306.
64. Rubin CT, Capilla E, Luu YK, Busa B, Crawford H, Nolan DJ, Mittal V, Rosen CJ, Pessin JE, Judex S. Adipogenesis is inhibited by brief, daily exposure to high-frequency, extremely low-magnitude mechanical signals. Proc Natl Acad Sci USA. 2007; 104:17879-84. (Pubitemid 350210928)
65. Ozcivici E, Luu YK, Rubin CT, Judex S. Low-level vibrations retain bone marrow's osteogenic potential and augment recovery of trabecular bone during reambulation. PLoS One. 2010;5:e11178.
66. Sugawara Y, Kamioka H, Honjo T, Tezuka K, Takano-Yamamoto T. Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. Bone. 2005; 36:877-83. (Pubitemid 40616022)
67. Smit TH, Burger EH. Is BMU-coupling a strain-regulated phenomenon? A finite element analysis. J Bone Miner Res. 2000; 15:301-7. (Pubitemid 30095717)
68. Smit TH, Burger EH, Huyghe JM. A case for strain-induced fluid flow as a regulator of BMU-coupling and osteonal alignment. J Bone Miner Res. 2002;17:2021-9. (Pubitemid 35239204)