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International Journal of Biomaterials
Volume 2012 (2012), Article ID 915620, 10 pages
Perfusion Flow Enhances Osteogenic Gene Expression and the Infiltration of Osteoblasts and Endothelial Cells into Three-Dimensional Calcium Phosphate Scaffolds
1Department of Biomedical Engineering, Michigan Technological University, 1400 Townsend, Houghton, MI 49931, USA
2School of Forestry and Natural Resources and Department of Genetics, The University of Georgia, 111 Riverbend Road, Athens, GA 30602, USA
3Department of Mechanical Engineering, Colorado State University, 1602 Campus Delivery, Fort Collins, CO 80523, USA
Received 13 March 2012; Accepted 4 July 2012
Academic Editor: Giovanni Vozzi
Copyright © 2012 Matthew J. Barron et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- M. J. Yaszemski, R. G. Payne, W. C. Hayes, R. Langer, and A. G. Mikos, “Evolution of bone transplantation: molecular, cellular and tissue strategies to engineer human bone,” Biomaterials, vol. 17, no. 2, pp. 175–185, 1996.
- T. W. Bauer, “An overview of the histology of skeletal substitute materials,” Archives of Pathology and Laboratory Medicine, vol. 131, no. 2, pp. 217–224, 2007.
- G. J. Meijer, J. D. De Bruijn, R. Koole, and C. A. Van Blitterswijk, “Cell-based bone tissue engineering,” PLoS Medicine, vol. 4, no. 2, article e9, 2007.
- G. F. Muschler, C. Nakamoto, and L. G. Griffith, “Engineering principles of clinical cell-based tissue engineering,” Journal of Bone and Joint Surgery, vol. 86, no. 7, pp. 1541–1558, 2004.
- R. Langer, J. P. Vacanti, C. A. Vacanti, A. Atala, L. E. Freed, and G. Vunjak-Novakovic, “Tissue engineering: biomedical applications,” Tissue Engineering, vol. 1, no. 2, pp. 151–161, 1995.
- P. M. Galletti, K. B. Hellman, and R. M. Nerem, “Tissue engineering: from basic science to products: a preface,” Tissue Engineering, vol. 1, no. 2, pp. 147–149, 1995.
- C. S. N. Choong, D. W. Hutmacher, and J. T. Triffitt, “Co-culture of bone marrow fibroblasts and endothelial cells on modified polycaprolactone substrates for enhanced potentials in bone tissue engineering,” Tissue Engineering, vol. 12, no. 9, pp. 2521–2531, 2006.
- A. Stahl, A. Wenger, H. Weber, G. B. Stark, H. G. Augustin, and G. Finkenzeller, “Bi-directional cell contact-dependent regulation of gene expression between endothelial cells and osteoblasts in a three-dimensional spheroidal coculture model,” Biochemical and Biophysical Research Communications, vol. 322, no. 2, pp. 684–692, 2004.
- A. Wenger, N. Kowalewski, A. Stahl et al., “Development and characterization of a spheroidal coculture model of endothelial cells and fibroblasts for improving angiogenesis in tissue engineering,” Cells Tissues Organs, vol. 181, no. 2, pp. 80–88, 2005.
- R. E. Unger, A. Sartoris, K. Peters et al., “Tissue-like self-assembly in cocultures of endothelial cells and osteoblasts and the formation of microcapillary-like structures on three-dimensional porous biomaterials,” Biomaterials, vol. 28, no. 27, pp. 3965–3976, 2007.
- J. M. Kanczler and R. O. C. Oreffo, “Osteogenesis and angiogenesis: the potential for engineering bone,” European Cells and Materials, vol. 15, pp. 100–114, 2008.
- R. A. D. Carano and E. H. Filvaroff, “Angiogenesis and bone repair,” Drug Discovery Today, vol. 8, no. 21, pp. 980–989, 2003.
- J. Glowacki, “Angiogenesis in fracture repair,” Clinical Orthopaedics and Related Research, supplement 355, pp. S82–S89, 1998.
- J. P. Bilezikian, L. G. Raisz, and G. A. Rodan, “Principles of bone biology,” in Principles of Bone Biology, R. Bilezikian and G. A. Rodan, Eds., vol. 1-2, Academic Press, San Diego, Calif, USA, 2nd edition, 2002.
- R. Burkhardt, G. Kettner, and W. Bohm, “Changes in trabecular bone, hematopoiesis and bone marrow vessels in aplastic anemia, primary osteoporosis, and old age: a comparative histomorphometric study,” Bone, vol. 8, no. 3, pp. 157–164, 1987.
- M. R. Hausman, M. B. Schaffler, and R. J. Majeska, “Prevention of fracture healing in rats by an inhibitor of angiogenesis,” Bone, vol. 29, no. 6, pp. 560–564, 2001.
- J. Rouwkema, J. De Boer, and C. A. Van Blitterswijk, “Endothelial cells assemble into a 3-dimensional prevascular network in a bone tissue engineering construct,” Tissue Engineering, vol. 12, no. 9, pp. 2685–2693, 2006.
- F. Villars, B. Guillotin, T. Amédée et al., “Effect of HUVEC on human osteoprogenitor cell differentiation needs heterotypic gap junction communication,” American Journal of Physiology, vol. 282, no. 4, pp. C775–C785, 2002.
- J. Buschmann, M. Welti, S. Hemmi et al., “Three-dimensional co-cultures of osteoblasts and endothelial cells in degrapol foam: histological and high-field magnetic resonance imaging analyses of pre-engineered capillary networks in bone grafts,” Tissue Engineering, vol. 17, no. 3-4, pp. 291–299, 2011.
- K. Kyriakidou, G. Lucarini, A. Zizzi et al., “Dynamic co-seeding of osteoblast and endothelial cells on 3D polycaprolactone scaffolds for enhanced bone tissue engineering,” Journal of Bioactive and Compatible Polymers, vol. 23, no. 3, pp. 227–243, 2008.
- S. Akita, N. Tamai, A. Myoui et al., “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in tissue-engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering, vol. 10, no. 5-6, pp. 789–795, 2004.
- F. Villars, L. Bordenave, R. Bareille, and J. Amédée, “Effect of human endothelial cells on human bone marrow stromal cell phenotype: role of VEGF?” Journal of Cellular Biochemistry, vol. 79, no. 4, pp. 672–685, 2000.
- C. E. Clarkin, R. J. Emery, A. A. Pitsillides, and C. P. D. Wheeler-Jones, “Evaluation of VEGF-mediated signaling in primary human cells reveals a paracrine action for VEGF in osteoblast-mediated crosstalk to endothelial cells,” Journal of Cellular Physiology, vol. 214, no. 2, pp. 537–544, 2008.
- L. Steffens, A. Wenger, G. B. Stark, and G. Finkenzeller, “In vivo engineering of a human vasculature for bone tissue engineering applications,” Journal of Cellular and Molecular Medicine, vol. 13, no. 9, pp. 3380–3386, 2009.
- H. Yu, P. J. VandeVord, L. Mao, H. W. Matthew, P. H. Wooley, and S. Y. Yang, “Improved tissue-engineered bone regeneration by endothelial cell mediated vascularization,” Biomaterials, vol. 30, no. 4, pp. 508–517, 2009.
- M. I. Santos and R. L. Reis, “Vascularization in bone tissue engineering: physiology, current strategies, major hurdles and future challenges,” Macromolecular Bioscience, vol. 10, no. 1, pp. 12–27, 2010.
- E. Volkmer, I. Drosse, S. Otto et al., “Hypoxia in static and dynamic 3D culture systems for tissue engineering of bone,” Tissue Engineering, vol. 14, no. 8, pp. 1331–1340, 2008.
- J. Malda, T. J. Klein, and Z. Upton, “The roles of hypoxia in the in vitro engineering of tissues,” Tissue Engineering, vol. 13, no. 9, pp. 2153–2162, 2007.
- S. H. Cartmell, B. D. Porter, A. J. García, and R. E. Guldberg, “Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro,” Tissue Engineering, vol. 9, no. 6, pp. 1197–1203, 2003.
- G. N. Bancroft, V. I. Sikavitsas, J. Van Den Dolder et al., “Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 20, pp. 12600–12605, 2002.
- M. J. Jaasma and F. J. O'Brien, “Mechanical stimulation of osteoblasts using steady and dynamic fluid flow,” Tissue Engineering, vol. 14, no. 7, pp. 1213–1223, 2008.
- D. Du, K. S. Furukawa, and T. Ushida, “3D culture of osteoblast-like cells by unidirectional or oscillatory flow for bone tissue engineering,” Biotechnology and Bioengineering, vol. 102, no. 6, pp. 1670–1678, 2009.
- D. Li, T. Tang, J. Lu, and K. Dai, “Effects of flow shear stress and mass transport on the construction of a large-scale tissue-engineered bone in a perfusion bioreactor,” Tissue Engineering, vol. 15, no. 10, pp. 2773–2783, 2009.
- H. L. Holtorf, J. A. Jansen, and A. G. Mikos, “Modulation of cell differentiation in bone tissue engineering constructs cultured in a bioreactor,” Advances in Experimental Medicine and Biology, vol. 585, pp. 225–241, 2006.
- J. Vance, S. Galley, D. F. Liu, and S. W. Donahue, “Mechanical stimulation of MC3T3 osteoblastic cells in a bone tissue-engineering bioreactor enhances prostaglandin E2 release,” Tissue Engineering, vol. 11, no. 11-12, pp. 1832–1839, 2005.
- V. I. Sikavitsas, G. N. Bancroft, H. L. Holtorf, J. A. Jansen, and A. G. Mikos, “Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 25, pp. 14683–14688, 2003.
- Y. Wang, T. Uemura, J. Dong, H. Kojima, J. Tanaka, and T. Tateishi, “Application of perfusion culture system improves in vitro and in vivo osteogenesis of bone marrow-derived osteoblastic cells in porous ceramic materials,” Tissue Engineering, vol. 9, no. 6, pp. 1205–1214, 2003.
- N. A. Plunkett, S. Partap, and F. J. O'Brien, “Osteoblast response to rest periods during bioreactor culture of collagen-glycosaminoglycan scaffolds,” Tissue Engineering, vol. 16, no. 3, pp. 943–951, 2010.
- F. Zhao, R. Chella, and T. Ma, “Effects of shear stress on 3-D human mesenchymal stem cell construct development in a perfusion bioreactor system: experiments and hydrodynamic modeling,” Biotechnology and Bioengineering, vol. 96, no. 3, pp. 584–595, 2007.
- N. Datta, Q. P. Pham, U. Sharma, V. I. Sikavitsas, J. A. Jansen, and A. G. Mikos, “In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 8, pp. 2488–2493, 2006.
- H. L. Holtorf, N. Datta, J. A. Jansen, and A. G. Mikos, “Scaffold mesh size affects the osteoblastic differentiation of seeded marrow stromal cells cultured in a flow perfusion bioreactor,” Journal of Biomedical Materials Research, vol. 74, no. 2, pp. 171–180, 2005.
- J. Street, M. Bao, L. DeGuzman et al., “Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 15, pp. 9656–9661, 2002.
- N. Ozawa, M. Shichiri, M. Iwashina, N. Fukai, T. Yoshimoto, and Y. Hirata, “Laminar shear stress up-regulates inducible nitric oxide synthase in the endothelium,” Hypertension Research, vol. 27, no. 2, pp. 93–99, 2004.
- K. Yamamoto, T. Takahashi, T. Asahara et al., “Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress,” Journal of Applied Physiology, vol. 95, no. 5, pp. 2081–2088, 2003.
- C. Fidkowski, M. R. Kaazempur-Mofrad, J. Borenstein, J. P. Vacanti, R. Langer, and Y. Wang, “Endothelialized microvasculature based on a biodegradable elastomer,” Tissue Engineering, vol. 11, no. 1-2, pp. 302–309, 2005.
- S. C. Cowin, Bone Mechanics Handbook, vol. 1, CRC Press, Boca Raton, Fla, USA, 2nd edition, 2001.
- C. N. Cornell, “Osteoconductive materials and their role as substitutes for autogenous bone grafts,” Orthopedic Clinics of North America, vol. 30, no. 4, pp. 591–598, 1999.
- S. Weinbaum, S. C. Cowin, and Y. Zeng, “A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses,” Journal of Biomechanics, vol. 27, no. 3, pp. 339–360, 1994.
- M. W. Pfaffl, “A new mathematical model for relative quantification in real-time RT-PCR,” Nucleic Acids Research, vol. 29, no. 9, article e45, 2001.
- M. E. Gomes, V. I. Sikavitsas, E. Behravesh, R. L. Reis, and A. G. Mikos, “Effect of flow perfusion on the osteogenic differentiation of bone marrow stromal cells cultured on starch-based three-dimensional scaffolds,” Journal of Biomedical Materials Research, vol. 67, no. 1, pp. 87–95, 2003.
- C. K. Griffith, C. Miller, R. C. A. Sainson et al., “Diffusion limits of an in vitro thick prevascularized tissue,” Tissue Engineering, vol. 11, no. 1-2, pp. 257–266, 2005.
- E. Potier, E. Ferreira, R. Andriamanalijaona et al., “Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression,” Bone, vol. 40, no. 4, pp. 1078–1087, 2007.
- D. S. Steinbrech, B. J. Mehrara, P. B. Saadeh et al., “Hypoxia regulates VEGF expression and cellular proliferation by osteoblasts in vitro,” Plastic and Reconstructive Surgery, vol. 104, no. 3, pp. 738–747, 1999.
- T. A. Owen, M. Aronow, V. Shalhoub et al., “Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix,” Journal of Cellular Physiology, vol. 143, no. 3, pp. 420–430, 1990.
- G. S. Stein and J. B. Lian, “Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype,” Endocrine Reviews, vol. 14, no. 4, pp. 424–442, 1993.