Mechanical stimulation of osteoblasts using steady and dynamic fluid flow

Tissue Engineering - Part A.

Volumn 14, Issue 7, 2008, Pages 1213-1223

  Jaasma, Michael J ^a,b   O'Brien, Fergal J ^a,b  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCONVERSION; BIODEGRADABLE POLYMERS; BIOREACTORS; CHEMICAL REACTORS; FLOW RATE; FLUIDS; INDUSTRIAL CHEMICALS; OSTEOBLASTS; PLANTS (BOTANY); TISSUE CULTURE; TISSUE ENGINEERING;

BIOREACTOR CULTURES; BONE TISSUE ENGINEERING; CYCLO-OXYGENASE 2 (COX 2); FLOW PERFUSION; FLUID FLOWING; GLYCOSAMINOGLYCAN (GAG); LOW FLOW RATE; MC3T3 E1; MECHANICAL STIMULATIONS; OSCILLATORY FLUID FLOW (OFF); PEAK FLOWS; PROSTAGLANDIN (PG);

FLOW OF FLUIDS;

CYCLOOXYGENASE 2; OSTEOPONTIN; PROCOLLAGEN; PROCOLLAGEN TYPE 1 ALPHA1; PROSTAGLANDIN E SYNTHASE 1; PROSTAGLANDIN E2;

ANIMAL CELL; ARTICLE; BIOREACTOR; CELL ACTIVITY; CELL COUNT; CELL STRAIN 3T3; CELL VIABILITY; CONTINUOUS FLOW REACTOR; CONTROLLED STUDY; FLOW RATE; FLUID FLOW; MECHANICAL STIMULATION; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; PULSATILE FLOW;

EID: 46449125838     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2007.0321     Document Type: Article

References (41)

1. Farrell, E., O'Brien, F.J., Doyle, P., Fischer, J., Yannas, I., Harley, B.A., O'Connell, B., Prendergast, P.J., and Campbell, V.A. A collagen-glycosaminoglycan scaffold supports adult rat mesenchymal stem cell differentiation along osteogenic and chondrogenic routes. Tissue Eng 12, 459, 2006.
2. Cartmell, S.H., Porter, B.D., Garcia, A.J., and Guldberg, R.E. Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro. Tissue Eng 9, 1197, 2003.
3. Ishaug-Riley, S.L., Crane-Kruger, G.M., Yaszemski, M.J., and Mikos, A.G. Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers. Biomaterials 19, 1405, 1998.
4. Goldstein, A.S., Juarez, T.M., Helmke, C.D., Gustin, M.C., and Mikos, A.G. Effect of convection on osteoblastic cell growth and function in biodegradable polymer foam scaffolds. Biomaterials 22, 1279, 2001.
5. Botchwey, E.A., Dupree, M.A., Pollack, S.R., Levine, E.M., and Laurencin, C.T. Tissue engineered bone: measurement of nutrient transport in three-dimensional matrices. J Biomed Mater Res A 67, 357, 2003.
6. Martin, I., Wendt, D., and Heberer, M. The role of bioreactors in tissue engineering. Trends Biotechnol 22, 80, 2004.
7. Bancroft, G.N., Sikavitsas, V.I., van den Dolder, J., Sheffield, T.L., Ambrose, C.G., Jansen, J.A., and Mikos, A.G. Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner. Proc Natl Acad Sci U S A 99, 12600, 2002.
8. Sikavitsas, V.I., Bancroft, G.N., Lemoine, J.J., Liebschner, M.A., Dauner, M., and Mikos, A.G. Flow perfusion enhances the calcified matrix deposition of marrow stromal cells in biodegradable nonwoven fiber mesh scaffolds. Ann Biomed Eng 33, 63, 2005.
9. 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, 2525, 2007.
10. 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, 1832, 2005.
11. Jacobs, C.R., Yellowley, C.E., Davis, B.R., Zhou, Z., Cimbala, J.M., and Donahue, H.J. Differential effect of steady versus oscillatory flow on bone cells. J Biomech 31, 969, 1998.
12. Turner, C.H. Three rules for bone adaptation to mechanical stimuli. Bone 23, 399, 1998.
13. Freed, L.E., and Vunjak-Novakovic, G. Tissue engineering bioreactors. In: Lanza, R.P., Langer, R., and Vacanti, J., eds. Principles of Tissue Engineering. San Diego, CA: Academic Press, 2000, pp. 143-156.
14. Griffith, L.G., and Naughton, G. Tissue engineering - current challenges and expanding opportunities. Science 295, 1009, 2002.
15. Gomes, M.E., Bossano, C.M., Johnston, C.M., Reis, R.L., and Mikos, A.G. In vitro localization of bone growth factors in constructs of biodegradable scaffolds seeded with marrow stromal cells and cultured in a flow perfusion bioreactor. Tissue Eng 12, 177, 2006.
16. Smalt, R., Mitchell, F.T., Howard, R.L., and Chambers, T.J. Induction of NO and prostaglandin E2 in osteoblasts by wall-shear stress but not mechanical strain. Am J Physiol 273, E751, 1997.
17. Nauman, E.A., Satcher, R.L., Keaveny, T.M., Halloran, B.P., and Bikle, D.D. Osteoblasts respond to pulsatile fluid flow with short-term increases in PGE2 but no change in mineralization. J Appl Physiol 90, 1849, 2001.
18. Murakami, M., Naraba, H., Tanioka, T., Semmyo, N., Nakatani, Y., Kojima, F., Ikeda, T., Fueki, M., Ueno, A., Oh, S., and Kudo, I. Regulation of prostaglandin E2 biosynthesis by inducible membrane-associated prostaglandin E2 synthase that acts in concert with cyclooxygenase-2. J Biol Chem 275, 32783, 2000.
19. Forwood, M.R. Inducible cyclo-oxygenase (COX-2) mediates the induction of bone formation by mechanical loading in vivo. J Bone Miner Res 11, 1688, 1996.
20. Chen, N.X., Ryder, K.D., Pavalko, F.M., Turner, C.H., Burr, D.B., Qiu, J., and Duncan, R.L. Ca(2+) regulates fluid shear-induced cytoskeletal reorganization and gene expression in osteoblasts. Am. J. Physiol. Cell Physiol., 278, C989, 2000.
21. Gosset, M., Berenbaum, F., Levy, A., Pigenet, A., Thirion, S., Saffar, J.L., and Jacques, C. Prostaglandin E2 synthesis in cartilage explants under compression: mPGES-1 is a mechanosensitive gene. Arthritis Res. Ther., 8, R135, 2006.
22. Datta, N., Pham, Q.P., Sharma, U., Sikavitsas, V.I., Jansen, J.A., and Mikos, A.G. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc. Natl. Acad. Sci. U. S. A., 103, 2488, 2006.
23. Jaasma, M.J., Jackson, W.M., Tang, R.Y., and Keaveny, T.M. Adaptation of cellular mechanical behavior to mechanical loading for osteoblastic cells. J. Biomech., 40, 1938, 2007.
24. Robling, A.G., Hinant, F.M., Burr, D.B., and Turner, C.H. Shorter, more frequent mechanical loading sessions enhance bone mass. Med. Sci. Sports Exerc., 34, 196, 2002.
25. Robling, A.G., Hinant, F.M., Burr, D.B., and Turner, C.H. Improved bone structure and strength after long-term mechanical loading is greatest if loading is separated into short bouts. J. Bone Miner Res 17, 1545, 2002.
26. Robling, A.G., Burr, D.B., and Turner, C.H. Recovery periods restore mechanosensitivity to dynamically loaded bone. J Exp Biol 204, 3389, 2001.
27. O'Brien, F.J., Harley, B.A., Yannas, I.V., and Gibson, L. Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds. Biomaterials 25, 1077, 2004.
28. Lee, C.R., Grodzinsky, A.J., and Spector, M. The effects of cross-linking of collagen-glycosaminoglycan scaffolds on compressive stiffness, chondrocyte-mediated contraction, proliferation and biosynthesis. Biomaterials 22, 3145, 2001.
29. Jaasma, M.J., Plunkett, N.A., and O'Brien, F.J. Design and validation of a dynamic flow perfusion bioreactor for use with compliant tissue engineering scaffolds. J Biotech 133, 490, 2008.
30. Freyria, A.M., Yang, Y., Chajra, H., Rousseau, C.F., Ronziere, M.C., Herbage, D., and El Haj, A.J. Optimization of dynamic culture conditions: effects on biosynthetic activities of chondrocytes grown in collagen sponges. Tissue Eng 11, 674, 2005.
31. Holtorf, H.L., Jansen, J.A., and Mikos, A.G. Flow perfusion culture induces the osteoblastic differentiation of marrow stroma cell-scaffold constructs in the absence of dexamethasone. J Biomed Mater Res A 72, 326, 2005.
32. Bakker, A.D., Soejima, K., Klein-Nulend, J., and Burger, E.H. The production of nitric oxide and prostaglandin E2 by primary bone cells is shear stress dependent. J Biomech 34, 671, 2001.
33. 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, 1363, 2003.
34. Holtorf, H.L., Datta, N., Jansen, J.A., and Mikos, A.G. Scaffold mesh size affects the osteoblastic differentiation of seeded marrow stromal cells cultured in a flow perfusion bioreactor. J Biomed Mater Res A 74, 171, 2005.
35. You, J., Reilly, G.C., Zhen, X., Yellowley, C.E., Chen, Q., Donahue, H.J., and Jacobs, C.R. Osteopontin gene regulation by oscillatory fluid flow via intracellular calcium mobilization and activation of mitogen-activated protein kinase in MC3T3-E1 osteoblasts. J Biol Chem 276, 13365, 2001.
36. Sharp, L.A., Dulaney, K.O., and Goldstein, A.S. Effect of pulsatile fluid flow on the differentiation of bone marrow stromal cells. Abstract presented at the 53rd Annual Meeting of the Orthopaedic Research Society, San Diego, CA, 2007. Abstract no. 900.
37. Stein, G.S., and Lian, J.B. Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype. Endocr Rev 14, 424, 1993.
38. Siddhivarn, C., Banes, A., Champagne, C., Riche, E.L., Weerapradist, W., and Offenbacher, S. Prostaglandin D2 pathway and peroxisome proliferator- activated receptor gamma-1 expression are induced by mechanical loading in an osteoblastic cell line. J Periodontal Res 41, 92, 2006.
39. Koshihara, Y., and Kawamura, M. Prostaglandin D2 stimulates calcification of human osteoblastic cells. Biochem Biophys Res Commun 159, 1206, 1989.
40. Takagi, T., Yamamoto, T., Asano, S., and Tamaki, H. Effect of prostaglandin D2 on the femoral bone mineral density in ovariectomized rats. Calcif Tissue Int 52, 442, 1993.
41. Burr, D.B., Robling, A.G., and Turner, C.H. Effects of biomechanical stress on bones in animals. Bone 30, 781, 2002.