Human embryonic stem cell-derived mesenchymal stem cell seeding on calcium phosphate cement-chitosan-rgd scaffold for bone repair

Tissue Engineering - Part A

Volumn 19, Issue 7-8, 2013, Pages 915-927

  Chen, Wenchuan ^a,b   Zhou, Hongzhi ^a,c   Weir, Michael D ^a   Tang, Minghui ^a   Bao, Chongyun ^b   Xu, Hockin H K ^a,d,e  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^b SICHUAN UNIVERSITY   (China)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; CELL GROWTH; CHITOSAN; FLOW CYTOMETRY; FLOWCHARTING; PHOSPHATASES; SCAFFOLDS (BIOLOGY); SCANNING ELECTRON MICROSCOPY;

ALKALINE PHOSPHATASE; BONE MINERALS; BONE REGENERATION; BONE REPAIR; BONE TISSUE ENGINEERING; CALCIUM PHOSPHATE CEMENT; CELL DENSITY; COLLAGEN I; COVALENTLY BONDED; CRANIOFACIAL; EMBRYOID BODY; EMBRYONIC STEMS; HUMAN EMBRYONIC STEM CELLS; LIVE CELL; MESENCHYMAL STEM CELL; OSTEOCALCIN; OSTEOCONDUCTIVITY; OSTEOGENIC; OSTEOGENIC DIFFERENTIATION; REGENERATIVE MEDICINE; SCANNING ELECTRON MICROSCOPE; STRENGTH AND TOUGHNESS; SURFACE ANTIGEN;

CELL CULTURE;

ARGINYL-GLYCYL-ASPARTIC ACID; ARGINYLGLYCYLASPARTIC ACID; BIOLOGICAL MARKER; BONE CEMENT; CALCIUM PHOSPHATE; CHITOSAN; IMMOBILIZED PROTEIN; MINERAL; OLIGOPEPTIDE; TISSUE SCAFFOLD;

ARTICLE; BONE; BONE DEVELOPMENT; CELL CULTURE; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECT; EMBRYONIC STEM CELL; FLOW CYTOMETRY; GENETICS; HUMAN; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; ULTRASTRUCTURE; WOUND HEALING;

BIOLOGICAL MARKERS; BONE AND BONES; BONE CEMENTS; CALCIUM PHOSPHATES; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; CHITOSAN; EMBRYONIC STEM CELLS; FLOW CYTOMETRY; HUMANS; IMMOBILIZED PROTEINS; MESENCHYMAL STROMAL CELLS; MINERALS; OLIGOPEPTIDES; OSTEOGENESIS; TISSUE SCAFFOLDS; WOUND HEALING;

EID: 84874677911     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0172     Document Type: Article

References (68)

1. Cutter, C.S., and Mehrara, B.J. Bone grafts and substitutes. J Long Term Eff Med Implants 16, 249, 2006.
2. Johnson, P.C., Mikos, A.G., Fisher, J.P., and Jansen, J.A. Strategic directions in tissue engineering. Tissue Eng 13, 2827, 2007.
3. Laurencin, C.T., Ambrosio, A.M., Borden, M.D., and Cooper, J.A., Jr. Tissue engineering: orthopedic applications. Annu Rev Biomed Eng 1, 19, 1999.
4. Mistry, A.S., and Mikos, A.G. Tissue engineering strategies for bone regeneration. Adv Biochem Eng Biotechnol 94, 1, 2005.
5. Tuan, R.S., Boland, G., and Tuli, R. Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther 5, 32, 2003.
6. Castano-Izquierdo, H., Alvarez-Barreto, J., van den Dolder, J., Jansen, J.A., Mikos, A.G., and Sikavitsas, V.I. Pre-culture period of mesenchymal stem cells in osteogenic media influences their in vivo bone forming potential. J Biomed Mater Res A 82, 129, 2007.
7. Johnson, P.C., and Mikos, A.G. Stem cells: state of the art. In: Johnson, P.C., and Mikos, A.G. eds. Advances in Tissue Engineering, Volume 2: Stem Cells. New Rochelle, NY: Mary Ann Liebert, Inc., 2010, p. 3.
8. Guo, X., Park, H., Young, S., Kretlow, J.D., van den Beucken, J.J., Baggett, L.S., Tabata, Y., Kasper, F.K., Mikos, A.G., and Jansen, J.A. Repair of osteochondral defects with biodegradable hydrogel composites encapsulating marrow mesenchymal stem cells in a rabbit model. Acta Biomater 6, 39, 2010.
9. Mao, J.J., Giannobile, W.V., Helms, J.A., Hollister, S.J., Krebsbach, P.H., Longaker, M.T., and Shi, S. Craniofacial tissue engineering by stem cells. J Dent Res 85, 966, 2006.
10. Varghese, S., Hwang, N.S., Ferran, A., Hillel, A., Theprungsirikul, P., Canver, A.C., Zhang, Z., Gearhart, J., and Elisseeff, J. Engineering musculoskeletal tissues with human embryonic germ cell derivatives. Stem Cells 28, 765, 2010.
11. Benoit, D.S., Nuttelman, C.R., Collins, S.D., and Anseth, K.S. Synthesis and characterization of a fluvastatin-releasing hydrogel delivery system to modulate hMSC differentiation and function for bone regeneration. Biomaterials 27, 6102, 2006.
12. Hsiong, S.X., Boontheekul, T., Huebsch, N., and Mooney, D.J. Cyclic arginine-glycine-aspartate peptides enhance three-dimensional stem cell osteogenic differentiation. Tissue Eng Part A 15, 263, 2009.
13. Kim, S., Kim, S.S., Lee, S.H., Eun, A.S., Gwak, S.J., Song, J.H., Kim, B.S., and Chung, H.M. In vivo bone formation from human embryonic stem cell-derived osteogenic cells in poly(D,L-lactic-co-glycolic acid)/hydroxyapatite composite scaffolds. Biomaterials 29, 1043, 2008.
14. Baksh, D., Yao, R., and Tuan, R.S. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells 25, 1384, 2007.
15. Alhadlaq, A., and Mao, J.J. Mesenchymal stem cells: isolation and therapeutics. Stem Cells Dev 13, 436, 2004.
16. Rahaman, M.N., and Mao, J.J. Stem cell-based composite tissue constructs for regenerative medicine. Biotechnol Bioeng 91, 261, 2005.
17. Mueller, S.M., and Glowacki, J. Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J Cell Biochem 82, 583, 2001.
18. Mendes, S.C., Tibbe, J.M., Veenhof, M., Bakker, K., Both, S., Platenburg, P.P., Oner, F.C., de Bruijn, J.D., and van Blitterswijk, C.A. Bone tissue-engineered implants using human bone marrow stromal cells: effect of culture conditions and donor age. Tissue Eng 8, 911, 2002.
19. Stenderup, K., Justesen, J., Clausen, C., and Kassem, M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33, 919, 2003.
20. Rodriguez, J.P., Montecinos, L., Rios, S., Reyes, P., and Martinez, J. Mesenchymal stem cells from osteoporotic patients produce a type I collagen-deficient extracellular matrix favoring adipogenic differentiation. J Cell Biochem 79, 557, 2000.
21. Suzuki, Y., Kim, K.J., Kotake, S., and Itoh, T. Stromal cell activity in bone marrow from the tibia and iliac crest of patients with rheumatoid arthritis. J Bone Miner Metab 19, 56, 2001.
22. Quarto, R., Thomas, D., and Liang, C.T. Bone progenitor cell deficits and the age-associated decline in bone repair capacity. Calcif Tissue Int 56, 123, 1995.
23. Arpornmaeklong, P., Brown, S.E., Wang, Z., and Krebsbach, P.H. Phenotypic characterization, osteoblastic differentiation, and bone regeneration capacity of human embryonic stem cell-derived mesenchymal stem cells. Stem Cells Dev 18, 955, 2009.
24. Lee, S.J., Lim, G.J., Lee, J.W., Atala, A., and Yoo, J.J. In vitro evaluation of a poly(lactide-co-glycolide)-collagen composite scaffold for bone regeneration. Biomaterials 27, 3466, 2006.
25. Horak, D., Matulka, K., Hlidkova, H., Lapcikova, M., Benes, M.J., Jaros, J., Hampl, A., and Dvorak, P. Pentapeptidemodified poly(N,N-diethylacrylamide) hydrogel scaffolds for tissue engineering. J Biomed Mater Res B Appl Biomater 98, 54, 2011.
26. Chaikof, E.L., Matthew, H., Kohn, J., Mikos, A.G., Prestwich, G.D., and Yip, C.M. Biomaterials and scaffolds in reparative medicine. Ann N Y Acad Sci 961, 96, 2002.
27. Foppiano, S., Marshall, S.J., Marshall, G.W., Saiz, E., and Tomsia, A.P. The influence of novel bioactive glasses on in vitro osteoblast behavior. J Biomed Mater Res A 71, 242, 2004.
28. Deville, S., Saiz, E., Nalla, R.K., and Tomsia, A.P. Freezing as a path to build complex composites. Science 311, 515, 2006.
29. Leach, J.K., Kaigler, D., Wang, Z., Krebsbach, P.H., and Mooney, D.J. Coating of VEGF-releasing scaffolds with bioactive glass for angiogenesis and bone regeneration. Biomaterials 27, 3249, 2006.
30. Ginebra, M.P., Driessens, F.C., and Planell, J.A. Effect of the particle size on the micro and nanostructural features of a calcium phosphate cement: a kinetic analysis. Biomaterials 25, 3453, 2004.
31. Ginebra, M.P., Traykova, T., and Planell, J.A. Calcium phosphate cements as bone drug delivery systems: a review. J Control Release 113, 102, 2006.
32. Jansen, J.A., Vehof, J.W., Ruhe, P.Q., Kroeze-Deutman, H., Kuboki, Y., Takita, H., Hedberg, E.L., and Mikos, A.G. Growth factor-loaded scaffolds for bone engineering. J Control Release 101, 127, 2005.
33. Salinas, C.N., and Anseth, K.S. The influence of the RGD peptide motif and its contextual presentation in PEG gels on human mesenchymal stem cell viability. J Tissue Eng Regen Med 2, 296, 2008.
34. Bohner, M. Design of ceramic-based cements and putties for bone graft substitution. Eur Cell Mater 20, 1, 2010.
35. Brown, W.E., and Chow, L.C. A new calcium phosphate water setting cement. In: Brown, P.W., ed. Cements Research Progress. Westerville, OH: American Ceramic Society, 1986, p. 352.
36. Bohner, M., and Baroud, G. Injectability of calcium phosphate pastes. Biomaterials 26, 1553, 2005.
37. Link, D.P., van den Dolder, J., van den Beucken, J.J., Wolke, J.G., Mikos, A.G., and Jansen, J.A. Bone response and mechanical strength of rabbit femoral defects filled with injectable CaP cements containing TGF-beta 1 loaded gelatin microparticles. Biomaterials 29, 675, 2008.
38. Friedman, C.D., Costantino, P.D., Takagi, S., and Chow, L.C. BoneSource hydroxyapatite cement: a novel biomaterial for craniofacial skeletal tissue engineering and reconstruction. J Biomed Mater Res 43, 428, 1998.
39. Xu, H.H.K., and Simon, C.G., Jr. Fast setting calciumphosphatechitosan scaffold: mechanical properties and biocompatibility. Biomaterials 26, 1337, 2005.
40. Weir, M.D., and Xu, H.H.K. Culture human mesenchymal stem cells with calcium phosphate cement scaffolds for bone repair. J Biomed Mater Res B Appl Biomater 93, 93, 2010.
41. Link, D.P., van den Dolder, J., Wolke, J.G., and Jansen, J.A. The cytocompatibility and early osteogenic characteristics of an injectable calcium phosphate cement. Tissue Eng 13, 493, 2007.
42. Xu, H.H.K., Takagi, S., Quinn, J.B., and Chow, L.C. Fastsetting calcium phosphate scaffolds with tailored macropore formation rates for bone regeneration. J Biomed Mater Res A 68, 725, 2004.
43. Park, K.M., Joung, Y.K., Park, K.D., Lee, S.Y., and Lee, M.C. RGD-conjugated chitosan-pluronic hydrogels as a cell supported scaffold for articular cartilage regeneration. Macromol Res 16, 517, 2008.
44. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S., and Jones, J.M. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145, 1998.
45. Livak, K.J., and Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402, 2001.
46. Wang, Y.H., Liu, Y., Maye, P., and Rowe, D.W. Examination of mineralized nodule formation in living osteoblastic cultures using fluorescent dyes. Biotechnol Prog 22, 1697, 2006.
47. Lodish, H., Berk, A., Zipursky, S.L., Matsudaira, P., Baltimore, D., and Darnell, J. Molecular Cell Biology, 3rd edition. New York: W. H. Freeman & Company, 2000, Chapter 18.
48. Tang, M., Chen, W., Weir, M.D., Thein-Han, W., and Xu, H.H.K. Human embryonic stem cell-encapsulation in alginate microbeads in macroporous calcium phosphate cement for bone tissue engineering. Acta Biomater 8, 3436, 2012.
49. Heng, B.C., Cao, T., Stanton, L.W., Robson, P., and Olsen, B. Strategies for directing the differentiation of stem cells into the osteogenic lineage in vitro. J Bone Miner Res 19, 1379, 2004.
50. Fenno, L.E., Ptaszek, L.M., and Cowan, C.A. Human embryonic stem cells: emerging technologies and practical applications. Curr Opin Genet Dev 18, 324, 2008.
51. Trivedi, P., and Hematti, P. Simultaneous generation of CD34 + primitive hematopoietic cells and CD73 + mesenchymal stem cells from human embryonic stem cells cocultured with murine OP9 stromal cells. Exp Hematol 35, 146, 2007.
52. Trivedi, P., and Hematti, P. Derivation and immunological characterization of mesenchymal stromal cells from human embryonic stem cells. Exp Hematol 36, 350, 2008.
53. Gruenloh, W., Kambal, A., Sondergaard, C., McGee, J., Nacey, C., Kalomoiris, S., Pepper, K., Olson, S., Fierro, F., and Nolta, J.A. Characterization and in vivo testing of mesenchymal stem cells derived from human embryonic stem cells. Tissue Eng Part A 17, 1517, 2011.
54. Niwa, H., Miyazaki, J., and Smith, A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24, 372, 2000.
55. Le, B.K., Tammik, C., Rosendahl, K., Zetterberg, E., and Ringden, O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 31, 890, 2003.
56. Karp, J.M., Ferreira, L.S., Khademhosseini, A., Kwon, A.H., Yeh, J., and Langer, R.S. Cultivation of human embryonic stem cells without the embryoid body step enhances osteogenesis in vitro. Stem Cells 24, 835, 2006.
57. Olivier, E.N., Rybicki, A.C., and Bouhassira, E.E. Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells 24, 1914, 2006.
58. Ahn, S.E., Kim, S., Park, K.H., Moon, S.H., Lee, H.J., Kim, G.J., Lee, Y.J., Park, K.H., Cha, K.Y., and Chung, H.M. Primary bone-derived cells induce osteogenic differentiation without exogenous factors in human embryonic stem cells. Biochem Biophys Res Commun 340, 403, 2006.
59. Inanc, B., Elcin, A.E., and Elcin, Y.M. Effect of osteogenic induction on the in vitro differentiation of human embryonic stem cells cocultured with periodontal ligament fibroblasts. Artif Organs 31, 792, 2007.
60. Kuznetsov, S.A., Cherman, N., and Robey, P.G. In vivo bone formation by progeny of human embryonic stem cells. Stem Cells Dev 20, 269, 2011.
61. Bohner, M., Gbureck, U., and Barralet, J.E. Technological issues for the development of more efficient calcium phosphate bone cements: a critical assessment. Biomaterials 26, 6423, 2005.
62. Kouvroukoglou, S., Dee, K.C., Bizios, R., McIntire, L.V., and Zygourakis, K. Endothelial cell migration on surfaces modified with immobilized adhesive peptides. Biomaterials 21, 1725, 2000.
63. Wissink, M.J., Beernink, R., Poot, A.A., Engbers, G.H., Beugeling, T., van Aken, W.G., and Feijen, J. Relation between cell density and the secretion of von Willebrand factor and prostacyclin by human umbilical vein endothelial cells. Biomaterials 22, 2283, 2001.
64. Goncalves, F., Kawano, Y., Pfeifer, C., Stansbury, J.W., and Braga, R.R. Influence of BisGMA, TEGDMA, and BisEMA contents on viscosity, conversion, and flexural strength of experimental resins and composites. Eur J Oral Sci 117, 442, 2009.
65. Miller, M.A., Race, A., Gupta, S., Higham, P., Clarke, M.T., and Mann, K.A. The role of cement viscosity on cement-bone apposition and strength: an in vitro model with medullary bleeding. J Arthroplasty 22, 109, 2007.
66. Kim, K., Dean, D., Mikos, A.G., and Fisher, J.P. Effect of initial cell seeding density on early osteogenic signal expression of rat bone marrow stromal cells cultured on crosslinked poly(propylene fumarate) disks. Biomacromolecules 10, 1810, 2009.
67. Yang, F., Williams, C.G., Wang, D.A., Lee, H., Manson, P.N., and Elisseeff, J. The effect of incorporating RGD adhesive peptide in polyethylene glycol diacrylate hydrogel on osteogenesis of bone marrow stromal cells. Biomaterials 26, 5991, 2005.
68. Morgan, A.W., Roskov, K.E., Lin-Gibson, S., Kaplan, D.L., Becker, M.L., and Simon, C.G., Jr. Characterization and optimization of RGD-containing silk blends to support osteoblastic differentiation. Biomaterials 29, 2556, 2008.