Sequential application of steady and pulsatile medium perfusion enhanced the formation of engineered bone

Tissue Engineering - Part A

Volumn 19, Issue 9-10, 2013, Pages 1244-1254

  Correia, Cristina ^a,b   Bhumiratana, Sarindr ^a   Sousa, Rui A ^b   Reis, Rui L ^b   Vunjak Novakovic, Gordana ^a  

^a Department of Earth and Environmental Sciences   (United States)

^b UNIVERSITY OF MINHO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; BONE; FLOW OF FLUIDS; GENE EXPRESSION; LOADING; SHEAR FLOW; STEM CELLS; TISSUE;

BIOMECHANICAL PROPERTIES; BONE-LIKE TISSUE; HUMAN ADIPOSE STEM CELLS; HYDRODYNAMIC SHEAR FORCES; INTERSTITIAL FLOW; MECHANOTRANSDUCTION; OSTEOGENIC CELLS; SEQUENTIAL APPLICATIONS;

SCAFFOLDS (BIOLOGY);

SILK; TISSUE SCAFFOLD;

ADIPOSE TISSUE; ANIMAL; ARTICLE; BIOMECHANICS; BONE DEVELOPMENT; CHEMISTRY; CYTOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; METHODOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL; TISSUE ENGINEERING;

ADIPOSE TISSUE; ANIMALS; BIOMECHANICS; HUMANS; IMMUNOHISTOCHEMISTRY; OSTEOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; SILK; STEM CELLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84875595913     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2011.0701     Document Type: Article

References (48)

1. Martin, A.D., & McCulloch, R.G. Bone dynamics: stress, strain and fracture. J Sport Sci 5, 155, 1987.
2. Jones, H.H., Priest, J.D., Hayes, W.C., Tichenor, C.C., and Nagel, D.A. Humeral hypertrophy in response to exercise. J Bone Joint Surg Am 59, 204, 1977.
3. Jacobs, C.R., et al. Differential effect of steady versus oscillating flow on bone cells. J Biomech 31, 969, 1998.
4. Burger, E.H., & Klein-Nulend, J. Mechanotransduction in bone-role of the lacuno-canalicular network. FASEB J 13 Suppl, S101, 1999.
5. Hung, C.T., Pollack, S.R., Reilly, T.M., & Brighton, C.T. Real-time calcium response of cultured bone-cells to fluidflow. Clin Orthop Relat Res 256, 1995.
6. Reich, K.M., & Frangos, J.A. Effect of flow on prostaglandin-E2 and inositol trisphosphate levels in osteoblasts. Am J Physiol 261, C428, 1991.
7. Donahue, T.L.H., 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.
8. Santos, A., Bakker, A.D., Zandieh-Doulabi, B., Semeins, C.M., & Klein-Nulend, J. Pulsating fluid flow modulates gene expression of proteins involved in Wnt signaling pathways in osteocytes. J Orthop Res 27, 1280, 2009.
9. Knippenberg, M., et al. Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fluid shear stress on osteogenic stimulation. Tissue Eng 11, 1780, 2005.
10. Grayson, W.L., et al. Optimizing the medium perfusion rate in bone tissue engineering bioreactors. Biotechnol Bioeng 108, 1159, 2011.
11. Grayson, W.L., et al. Effects of initial seeding density and fluid perfusion rate on formation of tissue-engineered bone. Tissue Eng Part A 14, 1809, 2008.
12. Bhumiratana, S., et al. Nucleation and growth of mineralized bone matrix on silk-hydroxyapatite composite scaffolds. Biomaterials 32, 2812, 2011.
13. Gomes, M.E., Holtorf, H.L., Reis, R.L., & Mikos, A.G. Influence of the porosity of starch-based fiber mesh scaffolds on the proliferation and osteogenic differentiation of bone marrow stromal cells cultured in a flow perfusion bioreactor. Tissue Eng 12, 801, 2006.
14. Martins, A.M., et al. Combination of enzymes and flow perfusion conditions improves osteogenic differentiation of bone marrow stromal cells cultured upon starch/poly(epsilon-caprolactone) fiber meshes. J Biomed Mater Res A 94, 1061, 2010.
15. Frohlich, M., et al. Bone grafts engineered from human adipose-derived stem cells in perfusion bioreactor culture. Tissue Eng Part A 16, 179, 2010.
16. Scherberich, A., Galli, R., Jaquiery, C., Farhadi, J., and Martin, I. Three-dimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem cells 25, 1823, 2007.
17. Gimble, J.M., & Bunnel, B.A. Adipose-Derived Stem Cells: Methods and Protocols, Vol. 702, New York: Springer Science + Business Media, LLC, 2011.
18. Gimble, J.M., Katz, A.J., & Bunnell, B.A. Adipose-derived stem cells for regenerative medicine. Circ Res 100, 1249, 2007.
19. Bacabac, R.G., et al. Nitric oxide production by bone cells is fluid shear stress rate dependent. Biochem Biophys Res Commun 315, 823, 2004.
20. Jaasma, M.J., & O'Brien, F.J. Mechanical stimulation of osteoblasts using steady and dynamic fluid flow. Tissue Eng Part A 14, 1213, 2008.
21. Sikavitsas, V.I., Bancroft, G.N., Holtorf, H.L., Jansen, J.A., and Mikos, A.G. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc Natl Acad Sci U S A 100, 14683, 2003.
22. Bancroft, G.N., et al. 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.
23. Weinbaum, S., Cowin, S.C., & Zeng, Y. A Model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 27, 339, 1994.
24. Anderson, E.J., Kaliyamoorthy, S., Alexander, J.I.D., and Tate, M.L.K. Nano-microscale models of periosteocytic flow show differences in stresses imparted to cell body and processes. Ann Biomed Eng 33, 52, 2005.
25. Meinel, L., et al. Engineering bone-like tissue in vitro using human bone marrow stem cells and silk scaffolds. J Biomed Mater Res Part A 71A, 25, 2004.
26. Wang, Y., et al. In vivo degradation of three-dimensional silk fibroin scaffolds. Biomaterials 29, 3415, 2008.
27. Correia, C., et al. Development of silk-based scaffolds for tissue engineering of bone from human adipose-derived stem cells. Acta Biomater 8, 2483, 2012.
28. Correia, C., et al. Human adipose derived cells can serve as a single cell source for the in vitro cultivation of vascularized bone grafts. J Tissue Eng Regen Med 2012. DOI: 10.1002/term.1564.
29. Kim, U.J., Park, J., Kim, H.J., Wada, M., & Kaplan, D.L. Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin. Biomaterials 26, 2775, 2005.
30. McIntosh, K., et al. The immunogenicity of human adiposederived cells: temporal changes in vitro. Stem cells 24, 1246, 2006.
31. Mitchell, J.B., et al. Immunophenotype of human adiposederived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem cells 24, 376, 2006.
32. Zuk, P.A., et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7, 211, 2001.
33. Liu, X.W.S., Sajda, P., Saha, P.K., Wehrli, F.W., & Guo, X.E. Quantification of the roles of trabecular microarchitecture and trabecular type in determining the elastic modulus of human trabecular bone. J Bone Miner Res 21, 1608, 2006.
34. Mauck, R.L., et al. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng 122, 252, 2000.
35. Coletti, F., Macchietto, S., & Elvassore, N. Mathematical modeling of three-dimensional cell cultures in perfusion bioreactors. Ind Eng Chem Res 45, 8158, 2006.
36. Martin, I., Wendt, D., & Heberer, M. The role of bioreactors in tissue engineering. Trends Biotechnol 22, 80, 2004.
37. Klein-Nulend, J., et al. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J 9, 441, 1995.
38. Piekarski, K., & Munro, M. Transport mechanism operating between blood supply and osteocytes in long bones. Nature 269, 80, 1977.
39. Knothe Tate, M.L., & Knothe, U. An ex vivo model to study transport processes and fluid flow in loaded bone. J Biomech 33, 247, 2000.
40. Klein-Nulend, J., Roelofsen, J., Semeins, C.M., Bronckers, A.L., & Burger, E.H. Mechanical stimulation of osteopontin mRNA expression and synthesis in bone cell cultures. J Cell Physiol 170, 174, 1997.
41. Mullender, M., et al. Mechanotransduction of bone cells in vitro: mechanobiology of bone tissue. Med Biol Eng Comput 42, 14, 2004.
42. Toma, C.D., Ashkar, S., Gray, M.L., Schaffer, J.L., & Gerstenfeld, L.C. Signal transduction of mechanical stimuli is dependent on microfilament integrity: identification of osteopontin as a mechanically induced gene in osteoblasts. J Bone Miner Res 12, 1626, 1997.
43. Tong, L., Buchman, S.R., Ignelzi, M.A., Jr., Rhee, S., and Goldstein, S.A. Focal adhesion kinase expression during mandibular distraction osteogenesis: evidence for mechanotransduction. Plast Reconstr Surg 111, 211; discussion 223, 2003.
44. Nauman, E.A., Satcher, R.L., Keaveny, T.M., Halloran, B.P., and Bikle, D.D. Osteoblasts respond to pulsatile fluid flow with shortterm increases in PGE(2) but no change in mineralization. J Appl Physiol 90, 1849, 2001.
45. Claveau, D., et al. Microsomal prostaglandin E synthase-1 is a major terminal synthase that is selectively up-regulated during cyclooxygenase-2- dependent prostaglandin E2 production in the rat adjuvant-induced arthritis model. J Immunol 170, 4738, 2003.
46. Waclawik, A., Blitek, A., & Ziecik, A.J. Oxytocin and tumor necrosis factor alpha stimulate expression of prostaglandin E2 synthase and secretion of prostaglandin E2 by luminal epithelial cells of the porcine endometrium during early pregnancy. Reproduction 140, 613, 2010.
47. Salvado, M.D., Alfranca, A., Escolano, A., Haeggstrom, J.Z., and Redondo, J.M. COX-2 limits prostanoid production in activated HUVECs and is a source of PGH2 for transcellular metabolism to PGE2 by tumor cells. Arterioscler Thromb Vasc Biol 29, 1131, 2009.
48. Murakami, M., et al. Regulation of prostaglandin E-2 biosynthesis by inducible membrane-associated prostaglandin E-2 synthase that acts in concert with cyclooxygenase-2. J Biol Chem 275, 32783, 2000.