Toward mechanical systems biology in bone

Annals of Biomedical Engineering

Volumn 40, Issue 11, 2012, Pages 2475-2487

  Trüssel, Andreas ^a   Müller, Ralph ^a   Webster, Duncan ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Bone adaptation; Mechanical systems biology; Mechanobiology; Multiscale modeling; Osteocytes

Indexed keywords

BONE ADAPTATION; MECHANICAL SYSTEMS; MECHANO-BIOLOGY; MULTI-SCALE MODELING; OSTEOCYTES;

COMPUTATIONAL METHODS; LOADING; MECHANICAL ENGINEERING; MECHANICS; PHYSIOLOGY;

BONE;

ANIMAL; BIOLOGICAL MODEL; BONE; HUMAN; MECHANICAL STRESS; PHYSIOLOGY; REVIEW; SYSTEMS BIOLOGY; WEIGHT BEARING;

ANIMALS; BONE AND BONES; HUMANS; MODELS, BIOLOGICAL; STRESS, MECHANICAL; SYSTEMS BIOLOGY; WEIGHT-BEARING;

EID: 84868345940     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-012-0594-4     Document Type: Article

References (87)

1. Adachi, T., Y. Kameo, and M. Hojo. Trabecular bone remodelling simulation considering osteocytic response to fluid-induced shear stress. Philos. Trans. R. Soc. A 368: 2669-2682, 2010.
2. Adachi, T., Y. Tomita, H. Sakaue, and M. Tanaka. Simulation of trabecular surface remodeling based on local stress nonuniformity. Jpn. Soc. Mech. Eng. 40:782-792, 1997.
3. Adachi, T., K. Tsubota, Y. Tomita, and S. J. Hollister. Trabecular surface remodeling simulation for cancellous bone using microstructural voxel finite element models. J. Biomech. Eng. 123:403-409, 2001.
4. Albright, J. The Scientific Basis of Orthopaedics. New York: Appleton-Century Crofts, 1987.
5. Andriacchi, T. P., S. Koo, and S. F. Scanlan. Gait mechanics influence healthy cartilage morphology and osteoarthritis of the knee. J. Bone Joint Surg. Am. 91(Suppl 1):95-101, 2009.
6. Ascenzi, M. G., J. Gill, and A. Lomovtsev. Orientation of collagen at the osteocyte lacunae in human secondary osteons. J. Biomech. 41:3426-3435, 2008.
7. Atkins, G. J., P. S. Rowe, H. P. Lim, K. J. Welldon, R. Ormsby, A. R. Wijenayaka, L. Zelenchuk, A. Evdokiou, and D. M. Findlay. Sclerostin is a locally acting regulator of late-osteoblast/preosteocyte differentiation and regulates mineralization through a MEPE-ASARM-dependent mechanism. J. Bone Miner. Res. 26:1425-1436, 2011.
8. Be'ery-Lipperman, M., and A. Gefen. A method of quantification of stress shielding in the proximal femur using hierarchical computational modeling. Comput. Methods Biomech. 9:35-44, 2006.
9. Bonewald, L. F. Osteocytes: a proposed multifunctional bone cell. J. Musculoskelet. Neuronal Interact. 2:239-241, 2002.
10. Bonewald, L. Osteocytes as multifunctional cells. J. Musculoskelet. Neuronal Interact. 6:331-333, 2006.
11. Bonewald, L. F., and M. L. Johnson. Osteocytes, mechanosensing and Wnt signaling. Bone 42:606-615, 2008.
12. Bonivtch, A. R., L. F. Bonewald, and D. P. Nicolella. Tissue strain amplification at the osteocyte lacuna: a microstructural finite element analysis. J. Biomech. 40: 2199-2206, 2007.
13. Bontoux, N., L. Dauphinot, T. Vitalis, V. Studer, Y. Chen, J. Rossier, and M. C. Potier. Integrating whole transcriptome assays on a lab-on-a-chip for single cell gene profiling. Lab Chip 8:443-450, 2008.
14. Buenzli, P. R., J. Jeon, P. Pivonka, D. W. Smith, and P. T. Cummings. Investigation of bone resorption within a cortical basic multicellular unit using a lattice-based computational model. Bone 50:378-389, 2012.
15. CellML. http://www.cellml.org/. Accessed 15 March 2012.
16. Chambers, T. J., S. Fox, C. J. Jagger, J. M. Lean, and J. W. Chow. The role of prostaglandins and nitric oxide in the response of bone to mechanical forces. Osteoarthritis Cartilage 7:422-423, 1999.
17. Chen, N. X., K. D. Ryder, F. M. Pavalko, C. H. Turner, D. B. Burr, J. Y. Qiu, and R. L. Duncan. Ca2+ regulates fluid shear-induced cytoskeletal reorganization and gene expression in osteoblasts. Am. J. Physiol. Cell Physiol. 278:C989-C997, 2000.
18. Chow, J. W. Role of nitric oxide and prostaglandins in the bone formation response to mechanical loading. Exerc. Sport Sci. Rev. 28:185-188, 2000.
19. Christie, G. R., P. M. Nielsen, S. A. Blackett, C. P. Bradley, and P. J. Hunter. FieldML: concepts and implementation. Philos. Trans. A Math. Phys. Eng. Sci. 367:1869-1884, 2009.
20. Coelho, P. G., P. R. Fernandes, H. C. Rodrigues, J. B. Cardoso, and J. M. Guedes. Numerical modeling of bone tissue adaptation - a hierarchical approach for bone apparent density and trabecular structure. J. Biomech. 42:830-837, 2009.
21. De Souza, R. L., M. Matsuura, F. Eckstein, S. C. F. Rawlinson, L. E. Lanyon, and A. A. Pitsillides. Noninvasive axial loading of mouse tibiae increases cortical bone fori-nation and modifies trabecular organization: a new model to study cortical and cancellous compartments in a single loaded element. Bone 37:810-818, 2005.
22. Emmert-Buck, M. R., R. F. Bonner, P. D. Smith, R. F. Chuaqui, Z. P. Zhuang, S. R. Goldstein, R. A. Weiss, and L. A. Liotta. Laser capture microdissection. Science 274:998-1001, 1996.
23. Fernandez, J. W., M. Akbarshahi, K. M. Crossley, K. B. Shelburne, and M. G. Pandy. Model predictions of increased knee joint loading in regions of thinner articular cartilage after patellar tendon adhesion. J. Orthop. Res. 29:1168-1177, 2011.
24. FieldML. http://www.fieldml.org/. Accessed 15 March 2012.
25. Fritton, J. C., E. R. Myers, T. M. Wright, and M. C. H. van der Meulen. Loading induces site-specific increases in mineral content assessed by microcomputed tomography of the mouse tibia. Bone 36:1030-1038, 2005.
26. Frost, H. M. The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner. 2:73-85, 1987.
27. Fyhrie, D. P., and D. R. Carter. A unifying principle relating stress to trabecular bone morphology. J. Orthop. Res. 4:304-317, 1986.
28. Fyhrie, D. P., and D. R. Carter. Prediction of cancellous bone apparent density with 3-D stress analysis. In: Transactions 32nd Annual Orthopedic Research Society, p. 133, 1986.
29. Galea, G. L., A. Sunters, L. B. Meakin, G. Zaman, T. Sugiyama, L. E. Lanyon, and J. S. Price. Sost down-regulation by mechanical strain in human osteoblastic cells involves PGE2 signaling via EP4. FEBS Lett. 585:2450-2454, 2011.
30. Gerhard, F. A., D. J. Webster, G. H. van Lenthe, and R. Muller. In silico biology of bone modelling and remodelling: adaptation. Philos. Trans. A Math. Phys Eng. Sci. 367:2011-2030, 2009.
31. Gross, T. S., J. L. Edwards, K. J. McLeod, and C. T. Rubin. Strain gradients correlate with sites of periosteal bone formation. J. Bone Miner. Res. 12:982-988, 1997.
32. Gross, T. S., S. Srinivasan, C. C. Liu, T. L. Clemens, and S. D. Bain. Noninvasive loading of the murine tibia: an in vivo model for the study of mechanotransduction. J. Bone Miner. Res. 17:493-501, 2002.
33. Heino, T. J., T. A. Hentunen, and H. K. Vaananen. Conditioned medium from osteocytes stimulates the proliferation of bone marrow mesenchymal stem cells and their differentiation into osteoblasts. Exp. Cell Res. 294:458-468, 2004.
34. Henriksen, K., M.Karsdal, J. M.Delaisse, and M.T. Engsig. RANKL and vascular endothelial growth factor (VEGF) induce osteoclast chemotaxis through an ERK1/2-dependent mechanism. J. Biol. Chem. 278:48745-48753, 2003.
35. Huiskes, R., R. Ruimerman, G. H. van Lenthe, and J. D. Janssen. Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405:704-706, 2000.
36. Jacobs, C. R., C. E. Yellowley, B. R. Davis, Z. Zhou, J. M. Cimbala, and H. J. Donahue. Differential effect of steady versus oscillating flow on bone cells. J. Biomech. 31:969-976, 1998.
37. Jacquet, R., J. Hillyer, and W. J. Landis. Analysis of connective tissues by laser capture inicrodissection and reverse transcriptase-polymerase chain reaction. Anal. Biochem. 337:22-34, 2005.
38. Kamioka, H., T. Honjo, and T. A. Takano-Yamamoto. Three-dimensional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. Bone 28:145-149, 2001.
39. Kesavan, C., S. Mohan, S. Oberholtzer, J. E. Wergedal, and D. J. Baylink. Mechanical loading-induced gene expression and BMD changes are different in two inbred mouse strains. J. Appl. Physiol. 99:1951-1957, 2005.
40. Keyak, J. H., J. M. Meagher, H. B. Skinner, and C. D. Mote. Automated three-dimensional finite element modelling of bone: a new method. J. Biomed. Eng. 12:389-397, 1990.
41. Klein-Nulend, J., R. G. Bacabac, and M. G. Mullender. Mechanobiology of bone tissue. Pathol. Biol. 53:576-580, 2005.
42. Klein-Nulend, J., C. M. Semeins, N. E. Ajubi, P. J. Nijweide, and E. H. Burger. 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, 1995.
43. Klein-Nulend, J., A. Vanderplas, C. M. Semeins, N. E. Ajubi, J. A. Frangos, P. J. Nijweide, and E. H. Burger. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J. 9:441-445, 1995.
44. Knothe Tate, M. L. Top down and bottom up engineering of bone. J. Biomech. 44:304-312, 2011.
45. Lambers, F. M., F. A. Schulte, G. Kuhn, D. J. Webster, and R. Mueller. Mouse tail vertebrae adapt to cyclic mechanical loading by increasing bone formation rate and decreasing bone resorption rate as shown by time-lapsed in vivo imaging of dynamic bone morphometry. Bone 49:1340-1350, 2011.
46. Lanyon, L. E. Osteocytes, strain detection, bone modeling and remodeling. Calcif. Tissue Int. 53(Suppl 1):S102-S106; discussion S106-S107, 1993.
47. Lemaire, V., F. L. Tobin, L. D. Greller, C. R. Cho, and L. J. Suva. Modeling the interactions between osteoblast and osteoclast activities in bone remodeling. J. Theor. Biol. 229:293-309, 2004.
48. Maldonado, S., S. Borchers, R. Findeisen, and F. Allgower. Mathematical modeling and analysis of force induced bone growth. Conf. Proc. IEEE Eng. Med. Biol. Soc. 1:3154-3157, 2006.
49. Marcus, J. S., W. F. Anderson, and S. R. Quake. Microfluidic single-cell mRNA isolation and analysis. Anal. Chem. 78:3084-3089, 2006.
50. Moustafa, A., T. Sugiyama, J. Prasad, G. Zaman, T. S. Gross, L. E. Lanyon, and J. S. Price. Mechanical loadingrelated changes in osteocyte sclerostin expression in mice are more closely associated with the subsequent osteogenic response than the peak strains engendered. Osteoporos. Int. 23:1225-1234, 2012.
51. Mullender, M., A. J. El Haj, Y. Yang, M. A. van Duin, E. H. Burger, and J. Klein-Nulend. Mechanotransduction of bone cells in vitro: mechanobiology of bone tissue. Med. Biol. Eng. Comput. 42:14-21, 2004.
52. Nakashima, T., M. Hayashi, T. Fukunaga, K. Kurata, M. Oh-hora, J. Q. Feng, L. F. Bonewald, T. Kodama, A. Wutz, E. F. Wagner, et al. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat. Med. 17:1231-1234, 2011.
53. Nickerson, D., and P. Hunter. Using CellML in computational models of multiscale physiology. Proc. Ann. Int. IEEE EMBS 6:6096-6099, 2005.
54. Nicolella, D. P., D. E. Moravits, A. M. Gale, L. F. Bonewald, and J. Lankford. Osteocyte lacunae tissue strain in cortical bone. J. Biomech. 39(1735-43):57, 2006.
55. Norman, J., J. G. Shapter, K. Short, L. J. Smith, and N. L. Fazzalari. Micromechanical properties of human trabecular bone: a hierarchical investigation using nanoindentation. J. Biomed. Mater. Res. A 87:196-202, 2008.
56. Parfitt, A. M. Osteonal and hemi-osteonal remodeling - the spatial and temporal framework for signal traffic in adult human bone. J. Cell. Biochem. 55:273-286, 1994.
57. Pitsillides, A. A., S. C. F. Rawlinson, R. F. L. Suswillo, S. Bourrin, G. Zaman, and L. E. Lanyon. Mechanical straininduced NO production by bone cells: a possible role in adaptive bone (re)modeling? FASEB J. 9:1614-1622, 1995.
58. Pivonka, P., J. Zimak, D. W. Smith, B. S. Gardiner, C. R. Dunstan, N. A. Sims, T. J. Martin, and G. R. Mundy. Model structure and control of bone remodeling: a theoretical study. Bone 43:249-263, 2008.
59. Poole, K. E. S., R. L. van Bezooijen, N. Loveridge, H. Hamersma, S. E. Papapoulos, C. W. Lowik, and J. Reeve. Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. FASEB J. 19:1842, 2005.
60. Prendergast, P. J., and D. Taylor. Prediction of bone adaptation using damage accumulation. J. Biomech. 27:1067-1076, 1994.
61. Robling, A. G., P. J. Niziolek, L. A. Baldridge, K. W. Condon, M. R. Allen, I. Alam, S. M. Mantila, J. Gluhak-Heinrich, T. M. Bellido, S. E. Harris, et al. Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J. Biol. Chem. 283:5866-5875, 2008.
62. Robling, A. G., and C. H. Turner. Mechanotransduction in bone: genetic effects on mechanosensitivity in mice. Bone 31:562-569, 2002.
63. Rubin, M. A., and I. Jasiuk. The TEM characterization of the lamellar structure of osteoporotic human trabecular bone. Micron 36:653-664, 2005.
64. Ruimerman, R., P. Hilbers, B. van Rietbergen, and R. Huiskes. A theoretical framework for strain-related trabecular bone maintenance and adaptation. J. Biomech. 38:931-941, 2005.
65. Ryser, M. D., N. Nigam, and S. V. Komarova. Mathematical modeling of spatio-temporal dynamics of a single bone multicellular unit. J. Bone Miner. Res. 24:860-870, 2009.
66. Schulte, F. A., F. M. Lambers, G. Kuhn, and R. Mueller. In vivo micro-computed tomography allows direct threedimensional quantification of both bone formation and bone resorption parameters using time-lapsed imaging. Bone 48:433-442, 2011.
67. Schulte, F. A., F. M. Lambers, D. J. Webster, G. Kuhn, and R. Mueller. Strain energy density predicts sites of local trabecular bone formation and resorption. In: Abstracts 17th Congress of the European Society of Biomechanics (ESB), Edinburgh, UK, 5-7 July 2010, p. 697.
68. Schutze, K., and G. Lahr. Identification of expressed genes by laser-mediated manipulation of single cells. Nat. Biotechnol. 16:737-742, 1998.
69. Shim, V. B., P. J. Hunter, P. Pivonka, and J. W. Fernandez. A multiscale framework based on the physiome markup languages for exploring the initiation of osteoarthritis at the bone-cartilage interface. IEEE Trans. Biomed. Eng. 58:3532-3536, 2011.
70. Tang, F., C. Barbacioru, Y. Wang, E. Nordman, C. Lee, N. Xu, X. Wang, J. Bodeau, B. B. Tuch, A. Siddiqui, et al. mRNA-Seq whole-transcriptome analysis of a single cell. Nat. Methods 6:377-382, 2009.
71. Tang, F. C., P. Hajkova, S. C. Barton, K. Q. Lao, and M. A. Surani. MicroRNA expression profiling of single whole embryonic stem cells. Nucleic Acids Res. 34:e9, 2006.
72. Turner, C. H., M. R. Forwood, and M. W. Otter. Mechanotransduction in bone - do bone-cells act as sensors of fluid flow. FASEB J. 8:875-878, 1994.
73. van Bezooijen, R. L., B. A. J. Roelen, A. Visser, L. van der Wee-Pals, E. de Wilt, M. Karperien, H. Hamersma, S. E. Papapoulos, P. ten Dijke, and C. Lowik. Sclerostin is an osteocyte-expressed negative regulator of bone formation, but not a classical BMP antagonist. J. Exp. Med. 199:805-814, 2004.
74. van der Meulen, M. C. H., T. G. Morgan, X. Yang, T. H. Baldini, E. R. Myers, T. M. Wright, and M. P. G. Bostrom. Cancellous bone adaptation to in vivo loading in a rabbit model. Bone 38:871-877, 2006.
75. Warden, S. J., and C. H. Turner. Mechanotransduction in cortical bone is most efficient at loading frequencies of 5-10 Hz. Bone 34:261-270, 2004.
76. Wasserman, E., D. Webster, M. Attar-Namdar, R. Mueller, and I. Bab. Method for differential isolation of RNA from mouse caudal trabecular osteoblasts and osteocytes. J. Biomech. 41:S131-S131, 2008.
77. Webster, D. J., P. L. Morley, G. H. van Lenthe, and R. Mueller. A novel in vivo mouse model for mechanically stimulated bone adaptation - a combined experimental and computational validation study. Comput. Methods Biomech. Biomed. Eng. 11:435-441, 2008.
78. Webster, D., and R. Muller. In silico models of bone remodeling from macro to nano-from organ to cell. Wires Syst. Biol. Med. 3:241-251, 2011.
79. White, A. K., M. VanInsberghe, O. I. Petriv, M. Hamidi, D. Sikorski, M. A. Marra, J. Piret, S. Aparicio, and C. L. Hansen. High-throughput microfluidic single-cell RTqPCR. Proc. Natl Acad. Sci. USA 108:13999-14004, 2011.
80. Winkler, D. G., M. K. Sutherland, J. C. Geoghegan, C. P. Yu, T. Hayes, J. E. Skonier, D. Shpektor, M. Jonas, B. R. Kovacevich, K. Staehling-Hampton, et al. Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J. 22:6267-6276, 2003.
81. Wolff, J. Das Gesetz der Transformation der Knochen. Berlin: Hirschwald, 1892.
82. Xing, W. R., D. Baylink, C. Kesavan, Y. Hu, S. Kapoor, R. B. Chadwick, and S. Mohan. Global gene expression analysis in the bones reveals involvement of several novel genes and pathways in mediating an anabolic response of mechanical loading in mice. J. Cell. Biochem. 96:1049-1060, 2005.
83. Xiong, J., M. Onal, R. L. Jilka, R. S. Weinstein, S. C. Manolagas, and C. A. O'Brien. Matrix-embedded cells control osteoclast formation. Nat. Med. 17:U1235-U1262, 2011.
84. Yang, X. B., R. S. Tare, K. A. Partridge, H. I. Roach, N. M. Clarke, S. M. Howdle, K. M. Shakesheff, and R. O. Oreffo. Induction of human osteoprogenitor chemotaxis, proliferation, differentiation, and bone formation by osteoblast stimulating factor-1/pleiotrophin: osteoconductive biomimetic scaffolds for tissue engineering. J. Bone Miner. Res. 18:47-57, 2003.
85. Zaman, G., H. L. Jessop, M. Muzylak, R. L. De Souza, A. A. Pitsillides, J. S. Price, and L. L. Lanyon. Osteocytes use estrogen receptor alpha to respond to strain but their ER alpha content is regulated by estrogen. J. Bone Miner. Res. 21:1297-1306, 2006.
86. Zhao, S., Y. Kato, Y. Zhang, S. Harris, S. S. Ahuja, and L. F. Bonewald. MLO-Y4 osteocyte-like cells support osteoclast formation and activation. J. Bone Miner. Res. 17:2068-2079, 2002.
87. Zhong, J. F., Y. Chen, J. S. Marcus, A. Scherer, S. R. Quake, C. R. Taylor, and L. P. Weiner. A microfluidic processor for gene expression profiling of single human embryonic stem cells. Lab Chip 8:68-74, 2008.