Use of rapidly mineralising osteoblasts and short periods of mechanical loading to accelerate matrix maturation in 3D scaffolds

Bone

Volumn 44, Issue 5, 2009, Pages 822-829

  Sittichockechaiwut, Anuphan ^a   Scutt, Andrew M ^b   Ryan, Anthony J ^a   Bonewald, Lynda F ^c   Reilly, Gwendolen C ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

Bioreactors; Mechanobiology; Osteoid; Polyurethane; Tissue engineering

Indexed keywords

CALCIUM; COLLAGEN; COLLAGEN TYPE 1; OSTEOCALCIN; OSTEOPONTIN; POLYURETHAN;

ANIMAL CELL; ARTICLE; BONE MATRIX; BONE MATURATION; BONE MINERALIZATION; CELL DIFFERENTIATION; MECHANICAL STRESS; NONHUMAN; OSTEOBLAST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BIOMECHANICS; CELL LINE; CELL SURVIVAL; EXTRACELLULAR MATRIX; MICE; MICROSCOPY, ELECTRON, SCANNING; OSTEOBLASTS; POLYURETHANES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 63349112865     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2008.12.027     Document Type: Article

References (51)

1. Klein-Nulend J., Bacabac R.G., and Mullender M.G. Mechanobiology of bone tissue. Pathol. Biol. (Paris) 53 (2005) 576-580
2. Bonewald L.F. Mechanosensation and transduction in osteocytes. BoneKEy Osteovision 3 (2006) 7-15
3. Rubin J., Rubin C., and Jacobs C.R. Molecular pathways mediating mechanical signaling in bone. Gene 367 (2006) 1-16
4. Smith-Adaline E.A., Volkman S.K., Ignelzi Jr. M.A., Slade J., Platte S., et al. Mechanical environment alters tissue formation patterns during fracture repair. J. Orthop. Res. 22 (2004) 1079-1085
5. Cullinane D.M., Salisbury K.T., Alkhiary Y., Eisenberg S., Gerstenfeld L., et al. Effects of the local mechanical environment on vertebrate tissue differentiation during repair: does repair recapitulate development?. J. Exp. Biol. 206 (2003) 2459-2471
6. Clark P.A., Rodriguez A., Sumner D.R., Hussain M.A., and Mao J.J. Modulation of bone ingrowth of rabbit femur titanium implants by in vivo axial micromechanical loading. J. Appl. Physiol. 98 (2005) 1922-1929
7. Bacabac R.G., Mizuno D., Schmidt C.F., Mackintosh F.C., Van Loon J.J., et al. Round versus flat: bone cell morphology, elasticity, and mechanosensing. J. Biomech. 41 (2008) 1590-1598
8. Cukierman E., Pankov R., Stevens D.R., and Yamada K.M. Taking cell-matrix adhesions to the third dimension. Science 294 (2001) 1708-1712
9. Jarrahy R., Huang W., Rudkin G.H., Lee J.M., Ishida K., et al. Osteogenic differentiation is inhibited and angiogenic expression is enhanced in MC3T3-e1 cells cultured on three-dimensional scaffolds. Am. J. Physiol., Cell Physiol. 289 (2005) C408-C414
10. Cancedda R., Giannoni P., and Mastrogiacomo M. A tissue engineering approach to bone repair in large animal models and in clinical practice. Biomaterials 28 (2007) 4240-4250
11. Botchwey E.A., Pollack S.R., Levine E.M., and Laurencin C.T. Bone tissue engineering in a rotating bioreactor using a microcarrier matrix system. J. Biomed. Mater. Res. 55 (2001) 242-253
12. Meinel L., Karageorgiou V., Fajardo R., Snyder B., Shinde-Patil V., et al. Bone tissue engineering using human mesenchymal stem cells: effects of scaffold material and medium flow. Ann. Biomed. Eng. 32 (2004) 112-122
13. Porter B.D., Lin A.S., Peister A., Hutmacher D., and Guldberg R.E. Noninvasive image analysis of 3D construct mineralization in a perfusion bioreactor. Biomaterials 28 (2007) 2525-2533
14. Sikavitsas V.I., Bancroft G.N., Lemoine J.J., Liebschner M.A., Dauner M., et al. Flow perfusion enhances the calcified matrix deposition of marrow stromal cells in biodegradable nonwoven fiber mesh scaffolds. Ann. Biomed. Eng. 33 (2005) 63-70
15. Freed L.E., Guilak F., Guo X.E., Gray M.L., Tranquillo R., et al. Advanced tools for tissue engineering: scaffolds, bioreactors, and signaling. Tissue Eng. 12 (2006) 3285-3305
16. Jaasma M.J., and O'Brien F.J. Mechanical stimulation of osteoblasts using steady and dynamic fluid flow. Tissue Eng. Part A 23 (2008) 23
17. Tanaka S.M., Sun H.B., Roeder R.K., Burr D.B., Turner C.H., et al. Osteoblast responses one hour after load-induced fluid flow in a three-dimensional porous matrix. Calcif. Tissue Int. 76 (2005) 261-271
18. Vance J., Galley S., Liu D.F., and Donahue S.W. Mechanical stimulation of MC3T3 osteoblastic cells in a bone tissue-engineering bioreactor enhances prostaglandin e2 release. Tissue Eng. 11 (2005) 1832-1839
19. Sumanasinghe R.D., Bernacki S.H., and Loboa E.G. Osteogenic differentiation of human mesenchymal stem cells in collagen matrices: effect of uniaxial cyclic tensile strain on bone morphogenetic protein (BMP-2) mRNA expression. Tissue Eng. 12 (2006) 3459-3465
20. Jagodzinski M., Breitbart A., Wehmeier M., Hesse E., Haasper C., et al. Influence of perfusion and cyclic compression on proliferation and differentiation of bone marrow stromal cells in 3-dimensional culture. J. Biomech. 41 (2008) 1885-1891
21. Mauney J.R., Sjostorm S., Blumberg J., Horan R., O'Leary J.P., et al. Mechanical stimulation promotes osteogenic differentiation of human bone marrow stromal cells on 3-D partially demineralized bone scaffolds in vitro. Calcif. Tissue Int. 74 (2004) 458-468
22. Kato Y., Boskey A., Spevak L., Dallas M., Hori M., et al. Establishment of an osteoid preosteocyte-like cell MLO-A5 that spontaneously mineralizes in culture. J. Bone. Miner. Res. 16 (2001) 1622-1633
23. Barragan-Adjemian C., Nicolella D., Dusevich V., Dallas M.R., Eick J.D., et al. Mechanism by which MLO-A5 late osteoblasts/early osteocytes mineralize in culture: similarities with mineralization of lamellar bone. Calcif. Tissue Int. 79 (2006) 340-353
24. Chen X., Macica C.M., Ng K.W., and Broadus A.E. Stretch-induced PTH-related protein gene expression in osteoblasts. J. Bone Miner. Res. 20 (2005) 1454-1461
25. Bonzani I.C., Adhikari R., Houshyar S., Mayadunne R., Gunatillake P., et al. Synthesis of two-component injectable polyurethanes for bone tissue engineering. Biomaterials 28 (2007) 423-433
26. Fassina L., Visai L., Asti L., Benazzo F., Speziale P., et al. Calcified matrix production by SAOS-2 cells inside a polyurethane porous scaffold, using a perfusion bioreactor. Tissue Eng. 11 (2005) 685-700
27. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983) 55-63
28. Ng K.W., Leong D.T., and Hutmacher D.W. The challenge to measure cell proliferation in two and three dimensions. Tissue Eng. 11 (2005) 182-191
29. Gregory C.A., Gunn W.G., Peister A., and Prockop D.J. An alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal. Biochem. 329 (2004) 77-84
30. Tullberg-Reinert H., and Jundt G. In situ measurement of collagen synthesis by human bone cells with a sirius red-based colorimetric microassay: effects of transforming growth factor beta2 and ascorbic acid 2-phosphate. Histochem. Cell Biol. 112 (1999) 271-276
31. Duty A.O., Oest M.E., and Guldberg R.E. Cyclic mechanical compression increases mineralization of cell-seeded polymer scaffolds in vivo. J. Biomech. Eng. 129 (2007) 531-539
32. Sikavitsas V.I., Bancroft G.N., and Mikos A.G. Formation of three-dimensional cell/polymer constructs for bone tissue engineering in a spinner flask and a rotating wall vessel bioreactor. J. Biomed. Mater. Res. 62 (2002) 136-148
33. Archer R., and Williams D.J. Why tissue engineering needs process engineering. Nat. Biotechnol. 23 (2005) 1353-1355
34. Zahm A.M., Bucaro M.A., Srinivas V., Shapiro I.M., and Adams C.S. Oxygen tension regulates preosteocyte maturation and mineralization. Bone 43 (2008) 25-31
35. Donahue T.L., Haut T.R., Yellowley C.E., Donahue H.J., and Jacobs C.R. Mechanosensitivity of bone cells to oscillating fluid flow induced shear stress may be modulated by chemotransport. J. Biomech. 36 (2003) 1363-1371
36. Riddle R.C., Hippe K.R., and Donahue H.J. Chemotransport contributes to the effect of oscillatory fluid flow on human bone marrow stromal cell proliferation. J. Orthop. Res. 26 (2008) 918-924
37. Chung C.H., Golub E.E., Forbes E., Tokuoka T., and Shapiro I.M. Mechanism of action of beta-glycerophosphate on bone cell mineralization. Calcif. Tissue Int. 51 (1992) 305-311
38. Datta N., Pham Q.P., Sharma U., Sikavitsas V.I., Jansen J.A., et al. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 2488-2493
39. Mauney J.R., Volloch V., and Kaplan D.L. Role of adult mesenchymal stem cells in bone tissue engineering applications: current status and future prospects. Tissue Eng. 11 (2005) 787-802
40. Karageorgiou V., and Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 26 (2005) 5474-5491
41. Guelcher S.A., Patel V., Gallagher K.M., Connolly S., Didier J.E., et al. Synthesis and in vitro biocompatibility of injectable polyurethane foam scaffolds. Tissue Eng. 12 (2006) 1247-1259
42. Clarke D.A., Coll C., Drury P., Crawford A., Ryan A.J., et al. Polyurethane scaffolds for long term mechanical loading in musculoskeletal tissue engineering. Tissue Eng. 13 (2007) 1743
43. Diederichs S., Freiberger F., and van Griensven M. Effects of repetitive and short time strain in human bone marrow stromal cells. J. Biomed. Mater. Res. A. 2 (2008) 2
44. Simmons C.A., Matlis S., Thornton A.J., Chen S., Wang C.Y., et al. Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signal-regulated kinase (ERK1/2) signaling pathway. J. Biomech. 36 (2003) 1087-1096
45. Kraynik A.M. Foam structure: from soap froth to solid foams. MRS Bull. 28 (2003) 275-278
46. Isaksson H., Comas O., van Donkelaar C.C., Mediavilla J., Wilson W., et al. Bone regeneration during distraction osteogenesis: mechano-regulation by shear strain and fluid velocity. J. Biomech. 40 (2007) 2002-2011
47. Claes L.E., and Heigele C.A. Magnitudes of local stress and strain along bony surfaces predict the course and type of fracture healing. J. Biomech. 32 (1999) 255-266
48. Lacroix D., and Prendergast P.J. A mechano-regulation model for tissue differentiation during fracture healing: analysis of gap size and loading. J. Biomech. 35 (2002) 1163-1171
49. Wood M.A., Yang Y., Baas E., Meredith D.O., Richards R.G., et al. Correlating cell morphology and osteoid mineralization relative to strain profile for bone tissue engineering applications. J. R. Soc. Interface 11 (2007) 11
50. Judex S., Lei X., Han D., and Rubin C. Low-magnitude mechanical signals that stimulate bone formation in the ovariectomized rat are dependent on the applied frequency but not on the strain magnitude. J. Biomech. 40 (2007) 1333-1339
51. Cowie R., Walker R.D., and Scutt A. The use of high-frequency, low-intensity vibration to stimulate the proliferation and differentiation of primary rat bone marrow cells. Cytotherapy 8 (2006) 63