In vitro models for bone mechanobiology: Applications in bone regeneration and tissue engineering

Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine

Volumn 224, Issue 12, 2010, Pages 1533-1541

  Thompson, M S ^a,b   Epari, D R ^c   Bieler, F ^d   Duda, G N ^d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

bone regeneration; fluid shear stress; in vitro models; mechanobiology; substrate stretch

Indexed keywords

ANALYSIS TECHNIQUES; ANGIOGENESIS; BIOLOGICAL ANALYSIS; BIOLOGICAL RESPONSE; BONE HEALING; BONE REGENERATION; BONE TISSUE ENGINEERING; FLUID SHEAR STRESS; IN-VITRO; LIVING ORGANISMS; MECHANICAL ENVIRONMENT; MECHANICAL QUALITIES; MECHANICAL SENSITIVITY; MECHANICAL STIMULUS; MECHANO-BIOLOGY; REPAIR TISSUES; SUBSTRATE STRAIN; THREE-DIMENSIONAL (3D) MODEL; TIGHT COUPLING; IN-VITRO MODELS; SUBSTRATE STRETCHES;

BONE; CELL CULTURE; MECHANISMS; REPAIR; TISSUE; TISSUE ENGINEERING; BIOLOGY; FLOW OF FLUIDS; SHEAR STRESS;

THREE DIMENSIONAL; TISSUE REGENERATION;

ARTICLE; BIOLOGICAL MODEL; BONE DEVELOPMENT; BONE MATRIX; BONE REGENERATION; CELL PROLIFERATION; CELL SURVIVAL; CYTOLOGY; FLOW KINETICS; MECHANOTRANSDUCTION; METHODOLOGY; OSTEOBLAST; PHYSIOLOGY; STIMULATION; TISSUE ENGINEERING;

BONE MATRIX; BONE REGENERATION; CELL PROLIFERATION; CELL SURVIVAL; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; OSTEOBLASTS; OSTEOGENESIS; PHYSICAL STIMULATION; RHEOLOGY; TISSUE ENGINEERING;

EID: 79952781944     PISSN: 09544119     EISSN: 20413033     Source Type: Journal    
DOI: 10.1243/09544119JEIM807     Document Type: Conference Paper

References (64)

1. Ingber D. E. Mechanobiology and diseases of mechanotransduction. Ann. Medicine. 2003 ; 35: 564-577
2. Einhorn T. A. The cell and molecular biology of fracture healing. Clin. Orthop. Related Res. 1998 ; (355 suppl.). S7 - S21
3. Merryman W. D., Engler A. J. Innovations in cell mechanobiology. J. Biomechanics. 2010 ; 43: 1
4. Banes A. J., Gilbert J. A., Taylor D., Monbureau O. A new vacuum-operated stress-providing instrument that applies static or variable duration cyclic tension or compression to cells in vitro. J. Cell Sci. 1985 ; 75: 35-42
5. Brown T. D., Bottlang M., Pedersen D. R., Banes A. J. Development and experimental validation of a fluid/structure-interaction finite element model of a vacuum-driven cell culture mechanostimulus system. Comput. Meth. Biomechanics Biomed, Eng. 2000 ; 3: 65-78
6. Thompson M. S., Bleckwehl F. H., Ott C. E., Epari D. R., Duda G. N. Mechanical characterisation of the BioFlex system. Tissue Eng. 2007 ; 13: 1378
7. Matheson L. A., Fairbank N. J., Maksym G. N., Santerre J. P., Labow R. S. Characterization of the Flexcell(TM) Uniflex(TM) cyclic strain culture system with U937 macrophage-like cells. Biomaterials. 2006 ; 27: 226-233
8. Huang C.-H., Chen M.-H., Young T.-H., Jeng J.-H., Chen Y.-J. Interactive effects of mechanical stretching and extracellular matrix proteins on initiating osteogenic differentiation of human mesenchymal stem cells. J. Cell. Biochem. 2009 ; 108: 1263-1273
9. Bieler F. H., Ott C. E., Thompson M. S., Seidel R., Ahrens S., Epari D. R., Wilkening U., Schaser K., Mundlos S., Duda G. N. Biaxial cell stimulation: A mechanical validation. J. Biomechanics. 2009 ; 42: 1692-1696
10. Wall M. E., Weinhold P. S., Siu T., Brown T. D., Banes A. J. Comparison of cellular strain with applied substrate strain in vitro. Journal of Biomechanics. 2007 ; 40: 173-181
11. Neidlinger-Wilke C., Wilke H.-J., Claes L. Cyclic stretching of human osteoblasts affects proliferation and metabolism: A new experimental method and its application. J. Orthop. Res. 1994 ; 12: 70-78
12. Bottlang M., Simnacher M., Schmitt H., Brand R. A., Claes L. A cell strain system for small homogeneous strain applications. Biomed. Technik. 1997 ; 42: 305-309
13. Kaspar D., Seidl W., Neidlinger-Wilke C., Ignatius A., Claes L. Dynamic cell stretching increases human osteoblast proliferation and CICP synthesis but decreases osteocalcin synthesis and alkaline phosphatase activity. J. Biomechanics. 2000 ; 33: 45-51
14. Kaspar D., Seidl W., Neidlinger-Wilke C., Beck A., Claes L., Ignatius A. Proliferation of human-derived osteoblast-like cells depends on the cycle number and frequency of uniaxial strain. J. Biomechanics. 2002 ; 35: 873-880
15. Liedert A., Augat P., Ignatius A., Hausser H. J., Claes L. Mechanical regulation of HB-GAM expression in bone cells. Biochem. Biophys. Res. Comm. 2004 ; 319: 951-958
16. Grabner B., Varga F., Fratzl-Zelman N., Luegmayr E., Glantschnig H., Rumpler M., Tatschl A., Fratzl P., Klaushofer K. A new stretching apparatus for applying anistropic mechanical strain to bone cells in-vitro. Rev. Sci. Instrum. 2000 ; 71: 3522-3529
17. Reich K. M., Frangos J. A. Effect of flow on prostaglandin-E2 and inositol trisphosphate levels in osteoblasts. Am. J. Physiol. Cell Physiol. 1991 ; 261: C428 - C432
18. Klein-Nulend J., van der Plas A., Semeins C. M., Ajubi N. E., Frangos J. A., Nijweide P. J., Burger E. H. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J. 1995 ; 9: 441-445
19. Bakker A. D., Soejima K., Klein-Nulend J., Burger E. H. The production of nitric oxide and prostaglandin E(2) by primary bone cells is shear stress dependent. J. Biomechanics. 2001 ; 34: 671-677
20. Bacabac R. G., Smit T. H., Mullender M. G., van Loon J. J. W. A., Klein-Nulend J. Initial stress-kick is required for fluid shear stress-induced rate-dependent activation of bone cells. Ann. Biomed. Eng. 2005 ; 33: 104-110
21. Anderson E. J., Falls T. D., Sorkin A. M., Knothe Tate M. L. The imperative for controlled mechanical stresses in unraveling cellular mechanisms of mechanotransduction. BioMed. Eng. OnLine. 2006 ; 5: 27
22. Abercrombie S., Ott C. E., Bleckwehl F. H., Duda G. N., Ventikos Y., Thompson M. S. Fluid shear stresses in Flexcell(TM) device. J. Biomechanics. 2008 ; 41 (suppl. 1). S347
23. Malone A. M. D., Anderson C. T., Tummala P., Kwon R. Y., Johnston T. R., Stearns T., Jacobs C. R. Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc. Natnl Acad. Sci. U.S.A. 2007 ; 104: 13325-13330
24. Myers K. A., Rattner J. B., Shrive N. G., Hart D. A. Osteoblast-like cells and fluid flow: Cytoskeleton-dependent shear sensitivity. Biochem. Biophys. Res. Comm. 2007 ; 364: 214-219
25. Owan I., Burr D. B., Turner C. H., Qui J., Tu Y., Onyia J. E., Duncan R. L. Mechanotransduction in bone: Osteoblasts are more responsive to fluid forces than mechanical strain. Am. J. Physiol. 1997 ; 273: C810 - C815
26. Smalt R., Mitchell F. T., Howard R. L., Chambers T. J. Induction of NO and prostaglandin E2 in osteoblasts by wall-shear stress but not mechanical strain. Am. J. Physiol. 1997 ; 237: E751 - E758
27. You J., Yellowley C. E., Donahue H. J., Zhang Y., Chen Q., Jacobs C. R. Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fluid flow. J. Biomech. Eng. 2000 ; 122: 387-393
28. Kadow-Romacker A., Hoffmann J. E., Duda G., Wildemann B., Schmidmaier G. Effect of mechanical stimulation on osteoblast- and osteoclast-like cells in vitro. Cells Tissues Organs. 2009 ; 190: 61-68
29. Lim C. T., Zhou E. H., Quek S. T. Mechanical models for living cells-a review. J. Biomechanics. 2006 ; 39: 195-216
30. Matziolis G., Tuischer J., Kasper G., Thompson M. S., Bartmeyer B., Krocker D., Perka C., Duda G. Idea and innovation: Simulation of cell differentiation in fracture healing-mechanically loaded composite scaffolds in a novel bioreactor system. Tissue Eng. 2006 ; 12: 201-208
31. Isaksson H., Wilson W., van Donkelaar C. C., Huiskes R., Ito K. Comparison of biophysical stimuli for mechano-regulation of tissue differentiation during fracture healing. J. Biomechanics. 2006 ; 39: 1507-1516
32. Perälä M., Savontaus M., Metsäranta M., Vuorio E. Developmental regulation of mRNA species for types II, IX and XI collagens during mouse embryogenesis. Biochemical J. 1997 ; 324: 209-216
33. Kasper G., Dankert N., Tuischer J., Hoeft M., Gaber T., Glaeser J. D., Zander D., Tschirschmann M., Thompson M., Matziolis G., Duda G. N. Mesenchymal stem cells regulate angiogenesis according to their mechanical environment. Stem Cells. 2007 ; 25: 903-910
34. Wilson C. J., Kasper G., Schütz M. A., Duda G. N. Cyclic strain disrupts endothelial network formation on Matrigel. Microvasc. Res. 2009 ; 78: 358-363
35. Reilly G. C., Engler A. J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomechanics. 2010 ; 43: 55-62
36. Schwarz U. S., Bischofs I. B. Physical determinants of cell organization in soft media. Med. Eng. Physics. 2005 ; 27: 763-772
37. Engler A. J., Sen S., Sweeney H. L., Discher D. E. Matrix elasticity directs stem cell lineage specification. Cell. 2006 ; 126: 677-689
38. Lazopoulos K. A., Stamenovic D. Durotaxis as an elastic stability phenomenon. J. Biomechanics. 2008 ; 41: 1289-1294
39. Martin I., Miot S., Barbero A., Jakob M., Wendt D. Osteochondral tissue engineering. J. Biomechanics. 2007 ; 40: 750-765
40. Sittichockechalwut A., Scutt A. M., Ryan A. J., Bonewald L. F., Reilly G. C. Use of rapidly mineralising osteoblasts and short periods of mechanical loading to accelerate matrix maturation in 3D scaffolds. Bone. 2009 ; 44: 822-829
41. Baas E., Kuiper J. H., Yang Y., Wood M. A., El Haj A. J. In vitro bone growth responds to local mechanical strain in three-dimensional polymer scaffolds. J. Biomechanics. 2010 ; 43: 733-739
42. Datta N., Pham Q. P., Sharma U., Sikavitsas V. I., Jansen J. A., Mikos A. G. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc. Natnl Acad. Sci. U.S.A. 2006 ; 103: 2488-2493
43. Boschetti F., Raimondi M. T., Migliavacca F., Dubini G. Prediction of the micro-fluid dynamic environment imposed to three-dimensional engineered cell systems in bioreactors. J. Biomechanics. 2006 ; 39: 418-425
44. Maes F., Ransbeeck P., van Oosterwyck H., Verdonck P. Modeling fluid flow through irregular scaffolds for perfusion bioreactors. Biotechnol. Bioeng. 2009 ; 103: 621-630
45. Sandino C., Planell J., Lacroix D. A finite element study of mechanical stimuli in scaffolds for bone tissue engineering. J. Biomechanics. 2008 ; 41: 1005-1041
46. Stops A. J. F., Heraty K. B., Browne M., O'Brien F. J., McHugh P. E. A prediction of cell differentiation and proliferation within a collagen-glycosaminoglycan scaffold subjected to mechanical strain and perfusive fluid flow. J. Biomechanics. 2010 ; 43: 618-626
47. Schwartz Z., Denison T. A., Bannister S. R., Cochran D. L., Liu Y. H., Lohmann C. H., Wieland M., Boyan B. D. Osteoblast response to fluid induced shear depends on substrate microarchitecture and varies with time. J. Biomed. Mater. Res. 2007 ; 83: 20-32
48. El Haj A. J., Minter S. L., Rawlinson S. C., Suswillo R., Lanyon L. E. Cellular responses to mechanical loading in vitro. J. Bone Mineral Res. 1990 ; 5: 923-932
49. Hoffler C. E., Hankenson K. D., Miller J. D., Bilkhu S. K., Goldstein S. A. Novel explant model to study mechanotransduction and cell-cell communication. J. Orthop. Res. 2006 ; 24: 1687-1698
50. Chan M. E., Lu X. L., Huo B., Baik A. D., Chiang V., Guldberg R. E., Lu H. H., Guo X. E. A trabecular bone explant model of osteocyte-osteoblast co-culture for bone mechanobiology. Cell. Molec. Bioeng. 2009 ; 2: 405-415
51. Thompson M. S., Schell H., Lienau J., Duda G. N. Digital image correlation: A technique for determining local mechanical conditions within early bone callus. Med. Eng. Physics. 2007 ; 29: 820-823
52. Nolte P. A., Klein-Nulend J., Albers G. H. R., Marti R. K., Semeins C. M., Goei S. W., Burger E. H. Low-intensity ultrasound stimulates endochondral ossifcation in vitro. J. Orthop. Res. 2001 ; 19: 301-307
53. Lienau J., Duda G. N., Schell H. Does in vitro low-intensity pulsed ultrasound stimulate endochondral ossification?. Biomed. Technik. 2008 ; 53: 300-305
54. Trepczik B., Lienau J., Schell H., Epari D. R., Thompson M. S., Hoffman J. E., Kadow-Romacker A., Mundlos S., Duda G. N. Endochondral ossification in vitro is influenced by mechanical bending. Bone. 2007 ; 40: 597-603
55. Nowlan N. C., Murphy P., Prendergast P. J. A dynamic pattern of mechanical stimulation promotes ossification in avian embryonic long bones. J. Biomechanics. 2008 ; 41: 249-258
56. Pitsillides A. A. Early effects of embryonic movement: 'a shot out of the dark'. J. Anat. 2006 ; 208: 417-431
57. Ozcivici E., Luu Y. K., Adler B., Qin Y. X., Rubin J., Judex S., Rubin C. T. Mechanical signals as anabolic agents in bone. Nat. Rev. Rheumatol. 2010 ; 6: 50-59
58. van Oers R. F. M., Ruimerman R., Tanck E., Hilbers P. A. J., Huiskes R. A unified theory for osteonal and hemi-osteonal remodeling. Bone. 2008 ; 42: 250-259
59. Ott C. E., Bauer S., Manke T., Ahrens S., Rödelsperger C., Grünhagen J., Kornak U., Mundlos S., Robinson P. N. Promiscuous and depolarization-induced Immediate-Early Response genes mediate mechanotransduction in osteoblasts. J. Bone Mineral Res. 2009 ; 24: 1247-1262
60. Harvey A. K., Thompson M. S., Cochlin L., Raju P. A., Cui Z., Cornell H., Hulley P. A., Brady J. M. Functional imaging of tendon. Ann. Brit. Machine Vision Assoc. 2009 2009 ;: 1-11
61. Ugryumova N., Jacobs J., Bonesi M., Matcher S. J. Novel optical imaging technique to determine the 3-D orientation of collagen fibers in cartilage: Variable-incidence angle polarization-sensitive optical coherence tomography. Osteoarthritis Cartilage. 2009 ; 17: 33-42
62. Lendlein A., Langer R. Biodegradable, elastic shape-memory polymers for potential biomedical applications. Science. 2002 ; 296: 1673-1676
63. Alsousou J., Thompson M. S., Hulley P. A., Noble A., Willett K. The biology of platelet-rich plasma and its application in trauma and orthopaedic surgery. J. Bone Jt Surg. 2009 ; 91-B: 987-996
64. Chung S., Sudo R., Mack P. J., Wan C. R., Vickerman V., Kamm R. D. Cell migration into scaffolds under co-culture conditions in a microfluidic platform. Lab on a Chip. 2009 ; 9: 269-275