Membrane culture of bone marrow stromal cells yields better tissue than pellet culture for engineering cartilage-bone substitute biphasic constructs in a two-step process

Tissue Engineering - Part C: Methods

Volumn 17, Issue 9, 2011, Pages 939-948

  Lee, Whitaik David ^a   Hurtig, Mark B ^b   Kandel, Rita A ^a,c   Stanford, William L ^a,d,e  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BODY FLUIDS; BONE; CARTILAGE; COMPRESSIVE STRENGTH; JOINTS (ANATOMY); MEMBRANES; PELLETIZING; RNA; SCAFFOLDS (BIOLOGY); TISSUE; WOOL;

BIPHASIC; BONE MARROW STROMAL CELLS; BONE SUBSTITUTES; CALCIUM POLYPHOSPHATE; CHONDROCYTES; CLINICAL USE; EXTRACELLULAR MATRICES; HYALINE CARTILAGE TISSUE; IN-VITRO; LONG-TERM GOALS; MATRIX; OSTEOCHONDRAL LESIONS; PRECLINICAL STUDIES; PRIMARY CHONDROCYTES; ROBUST PROTOCOL; STROMAL CELLS; TWO-STEP PROCESS;

CELL CULTURE;

OVIS ARIES;

BIOLOGICAL MARKER; CALCIUM PHOSPHATE; TISSUE SCAFFOLD;

ANIMAL; ARTICLE; ARTIFICIAL MEMBRANE; BONE MARROW CELL; BONE PROSTHESIS; CARTILAGE; CELL DIFFERENTIATION; CHEMISTRY; CHONDROGENESIS; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECT; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; METHODOLOGY; PHYSIOLOGY; SHEEP; STROMA CELL; TISSUE ENGINEERING;

ANIMALS; BIOLOGICAL MARKERS; BONE MARROW CELLS; BONE SUBSTITUTES; CALCIUM PHOSPHATES; CARTILAGE; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CHONDROGENESIS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; MALE; MEMBRANES, ARTIFICIAL; SHEEP; STROMAL CELLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 80052232959     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2011.0147     Document Type: Article

References (108)

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3. Pilliar, R.M., Filiaggi, M.J., Wells, J.D., Grynpas, M.D., and Kandel, R.A. Porous calcium polyphosphate scaffolds for bone substitute applications-in vitro characterization. Biomaterials 22, 963, 2001.
4. Waldman, S.D., Grynpas, M.D., Pilliar, R.M., and Kandel, R.A. Characterization of cartilagenous tissue formed on calcium polyphosphate substrates in vitro. J Biomed Mater Res 62, 323, 2002.
5. Kandel, R.A., Grynpas, M., Pilliar, R., Lee, J., Wang, J., Waldman, S., et al. Repair of osteochondral defects with biphasic cartilage-calcium polyphosphate constructs in a sheep model. Biomaterials 27, 4120, 2006.
6. Martini, L., Fini, M., Giavaresi, G., and Giardino, R. Sheep model in orthopedic research: a literature review. Comp Med 51, 292, 2001.
7. Holtzer, H., Abbott, J., Lash, J., and Holtzer, S. The loss of phenotypic traits by differentiated cells in vitro, I. Dedifferentiation of cartilage cells. Proc Natl Acad Sci USA 46, 1533, 1960.
8. Dell'Accio, F., De Bari, C., and Luyten, F.P. Microenvironment and phenotypic stability specify tissue formation by human articular cartilage-derived cells in vivo. Exp Cell Res 287, 16, 2003.
9. Darling, E.M., and Athanasiou, K.A. Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J Orthop Res 23, 425, 2005.
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12. Mandl, E.W., van der Veen, S.W., Verhaar, J.A., and van Osch, G.J. Serum-free medium supplemented with highconcentration FGF2 for cell expansion culture of human ear chondrocytes promotes redifferentiation capacity. Tissue Eng 8, 573, 2002.
13. Jakob, M., Demarteau, O., Schafer, D., Hintermann, B., Dick, W., Heberer, M., et al. Specific growth factors during the expansion and redifferentiation of adult human articular chondrocytes enhance chondrogenesis and cartilaginous tissue formation in vitro. J Cell Biochem 81, 368, 2001.
14. Grigolo, B., Lisignoli, G., Piacentini, A., Fiorini, M., Gobbi, P., Mazzotti, G., et al. Evidence for redifferentiation of human chondrocytes grown on a hyaluronan-based biomaterial (HYAff 11): molecular, immunohistochemical and ultrastructural analysis. Biomaterials 23, 1187, 2002.
15. Yaeger, P.C., Masi, T.L., de Ortiz, J.L., Binette, F., Tubo, R., and McPherson, J.M. Synergistic action of transforming growth factor-beta and insulin-like growth factor-I induces expression of type II collagen and aggrecan genes in adult human articular chondrocytes. Exp Cell Res 237, 318, 1997.
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21. Bigdeli, N., Karlsson, C., Strehl, R., Concaro, S., Hyllner, J., and Lindahl, A. Coculture of human embryonic stem cells and human articular chondrocytes results in significantly altered phenotype and improved chondrogenic differentiation. Stem Cells 27, 1812, 2009.
22. Toh, W.S., Guo, X.M., Choo, A.B., Lu, K., Lee, E.H., and Cao, T. Differentiation and enrichment of expandable chondrogenic cells from human embryonic stem cells in vitro. J Cell Mol Med 13, 3570, 2009.
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28. Berry, L., Grant, M.E., McClure, J., and Rooney, P. Bonemarrow-derived chondrogenesis in vitro. J Cell Sci 101 (Pt 2), 333, 1992.
29. Vinatier, C., Bouffi, C., Merceron, C., Gordeladze, J., Brondello, J.M., Jorgensen, C., et al. Cartilage tissue engineering: towards a biomaterial-assisted mesenchymal stem cell therapy. Curr Stem Cell Res Ther 4, 318, 2009.
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31. Kafienah, W., Mistry, S., Dickinson, S.C., Sims, T.J., Learmonth, I., and Hollander, A.P. Three-dimensional cartilage tissue engineering using adult stem cells from osteoarthritis patients. Arthritis Rheum 56, 177, 2007.
32. Krinner, A., Zscharnack, M., Bader, A., Drasdo, D., and Galle, J. Impact of oxygen environment on mesenchymal stem cell expansion and chondrogenic differentiation. Cell Prolif 42, 471, 2009.
33. Ahmed, N., Stanford, W.L., and Kandel, R.A. Mesenchymal stem and progenitor cells for cartilage repair. Skeletal Radiol 36, 909, 2007.
34. Matsuda, C., Takagi, M., Hattori, T., Wakitani, S., and Yoshida, T. Differentiation of human bone marrow mesenchymal stem cells to chondrocytes for construction of threedimensional cartilage tissue. Cytotechnology 47, 11, 2005.
35. Markway, B.D., Tan, G.K., Brooke, G., Hudson, J.E., Cooper-White, J.J., and Doran, M.R. Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell Transplant 19, 29, 2010.
36. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315, 2006.
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39. Rentsch, C., Hess, R., Rentsch, B., Hofmann, A., Manthey, S., Scharnweber, D., et al. Ovine bone marrow mesenchymal stem cells: isolation and characterization of the cells and their osteogenic differentiation potential on embroidered and surface-modified polycaprolactone-co-lactide scaffolds. In Vitro Cell Dev Biol Anim 46, 624, 2010.
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45. Barbero, A., Grogan, S.P., Mainil-Varlet, P., and Martin, I. Expansion on specific substrates regulates the phenotype and differentiation capacity of human articular chondrocytes. J Cell Biochem 98, 1140, 2006.
46. Dickhut, A., Pelttari, K., Janicki, P., Wagner, W., Eckstein, V., Egermann, M., et al. Calcification or dedifferentiation: requirement to lock mesenchymal stem cells in a desired differentiation stage. J Cell Physiol 219, 219, 2009.
47. Allan, K.S., Pilliar, R.M., Wang, J., Grynpas, M.D., and Kandel, R.A. Formation of biphasic constructs containing cartilage with a calcified zone interface. Tissue Eng 13, 167, 2007.
48. Mueller, M.B., and Tuan, R.S. Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 58, 1377, 2008.
49. Zscharnack, M., Hepp, P., Richter, R., Aigner, T., Schulz, R., Somerson, J., et al. Repair of chronic osteochondral defects using predifferentiated mesenchymal stem cells in an ovine model. Am J Sports Med 38, 1857, 2010.
50. Swieszkowski, W., Tuan, B.H., Kurzydlowski, K.J., and Hutmacher, D.W. Repair and regeneration of osteochondral defects in the articular joints. Biomol Eng 24, 489, 2007.
51. Im, G.-I., Ahn, J.-H., Kim, S.-Y., Choi, B.-S., and Lee, S.-W. A Hyaluronate-atelocollagen/b-tricalcium phosphate-hydroxyapatite biphasic scaffold for the repair of osteochondral defects: a porcine study. Tissue Eng Part A 16, 1189, 2009.
52. Kasten, A., Muller, P., Bulnheim, U., Groll, J., Bruellhoff, K., Beck, U., et al. Mechanical integrin stress and magnetic forces induce biological responses in mesenchymal stem cells which depend on environmental factors. J Cell Biochem 111, 1586, 2010.
53. Woodfield, T.B., Miot, S., Martin, I., van Blitterswijk, C.A., and Riesle, J. The regulation of expanded human nasal chondrocyte re-differentiation capacity by substrate composition and gas plasma surface modification. Biomaterials 27, 1043, 2006.
54. Kawazoe, Y., Katoh, S., Onodera, Y., Kohgo, T., Shindoh, M., and Shiba, T. Activation of the FGF signaling pathway and subsequent induction of mesenchymal stem cell differentiation by inorganic polyphosphate. Int J Biol Sci 4, 37, 2008.
55. Mankin, H.J. The response of articular cartilage to mechanical injury. J Bone Joint Surg Am 64, 460, 1982.
56. Grynpas, M.D., Pilliar, R.M., Kandel, R.A., Renlund, R., Filiaggi, M., and Dumitriu, M. Porous calcium polyphosphate scaffolds for bone substitute applications in vivo studies. Biomaterials 23, 2063, 2002.
57. Pilliar, R.M., Filiaggi, M.J., Wells, J.D., Grynpas, M.D., and Kandel, R.A. Porous calcium polyphosphate scaffolds for bone substitute applications-in vitro characterization. Biomaterials 22, 963, 2001.
58. Waldman, S.D., Grynpas, M.D., Pilliar, R.M., and Kandel, R.A. Characterization of cartilagenous tissue formed on calcium polyphosphate substrates in vitro. J Biomed Mater Res 62, 323, 2002.
59. Kandel, R.A., Grynpas, M., Pilliar, R., Lee, J., Wang, J., Waldman, S., et al. Repair of osteochondral defects with biphasic cartilage-calcium polyphosphate constructs in a sheep model. Biomaterials 27, 4120, 2006.
60. Martini, L., Fini, M., Giavaresi, G., and Giardino, R. Sheep model in orthopedic research: a literature review. Comp Med 51, 292, 2001.
61. Holtzer, H., Abbott, J., Lash, J., and Holtzer, S. The loss of phenotypic traits by differentiated cells in vitro, I. Dedifferentiation of cartilage cells. Proc Natl Acad Sci USA 46, 1533, 1960.
62. Dell'Accio, F., De Bari, C., and Luyten, F.P. Microenvironment and phenotypic stability specify tissue formation by human articular cartilage-derived cells in vivo. Exp Cell Res 287, 16, 2003.
63. Darling, E.M., and Athanasiou, K.A. Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J Orthop Res 23, 425, 2005.
64. Mandl, E.W., van der Veen, S.W., Verhaar, J.A., and van Osch, G.J. Multiplication of human chondrocytes with low seeding densities accelerates cell yield without losing redifferentiation capacity. Tissue Eng 10, 109, 2004.
65. Goldberg, A.J., Lee, D.A., Bader, D.L., and Bentley, G. Autologous chondrocyte implantation. Culture in a TGF-betacontaining medium enhances the re-expression of a chondrocytic phenotype in passaged human chondrocytes in pellet culture. J Bone Joint Surg Br 87, 128, 2005.
66. Mandl, E.W., van der Veen, S.W., Verhaar, J.A., and van Osch, G.J. Serum-free medium supplemented with highconcentration FGF2 for cell expansion culture of human ear chondrocytes promotes redifferentiation capacity. Tissue Eng 8, 573, 2002.
67. Jakob, M., Demarteau, O., Schafer, D., Hintermann, B., Dick, W., Heberer, M., et al. Specific growth factors during the expansion and redifferentiation of adult human articular chondrocytes enhance chondrogenesis and cartilaginous tissue formation in vitro. J Cell Biochem 81, 368, 2001.
68. Grigolo, B., Lisignoli, G., Piacentini, A., Fiorini, M., Gobbi, P., Mazzotti, G., et al. Evidence for redifferentiation of human chondrocytes grown on a hyaluronan-based biomaterial (HYAff 11): molecular, immunohistochemical and ultrastructural analysis. Biomaterials 23, 1187, 2002.
69. Yaeger, P.C., Masi, T.L., de Ortiz, J.L., Binette, F., Tubo, R., and McPherson, J.M. Synergistic action of transforming growth factor-beta and insulin-like growth factor-I induces expression of type II collagen and aggrecan genes in adult human articular chondrocytes. Exp Cell Res 237, 318, 1997.
70. Chaipinyo, K., Oakes, B.W., and van Damme, M.P. Effects of growth factors on cell proliferation and matrix synthesis of low-density, primary bovine chondrocytes cultured in collagen I gels. J Orthop Res 20, 1070, 2002.
71. Martin, I., Vunjak-Novakovic, G., Yang, J., Langer, R., and Freed, L.E. Mammalian chondrocytes expanded in the presence of fibroblast growth factor 2 maintain the ability to differentiate and regenerate three-dimensional cartilaginous tissue. Exp Cell Res 253, 681, 1999.
72. Bonaventure, J., Kadhom, N., Cohen-Solal, L., Ng, K.H., Bourguignon, J., Lasselin, C., et al. Reexpression of cartilagespecific genes by dedifferentiated human articular chon-drocytes cultured in alginate beads. Exp Cell Res 212, 97, 1994.
73. Malda, J., Kreijveld, E., Temenoff, J.S., van Blitterswijk, C.A., and Riesle, J. Expansion of human nasal chondrocytes on macroporous microcarriers enhances redifferentiation. Biomaterials 24, 5153, 2003.
74. Seda Tigli, R., Ghosh, S., Laha, M.M., Shevde, N.K., Daheron, L., Gimble, J., et al. Comparative chondrogenesis of human cell sources in 3D scaffolds. J Tissue Eng Regen Med 3, 348, 2009.
75. Bigdeli, N., Karlsson, C., Strehl, R., Concaro, S., Hyllner, J., and Lindahl, A. Coculture of human embryonic stem cells and human articular chondrocytes results in significantly altered phenotype and improved chondrogenic differentiation. Stem Cells 27, 1812, 2009.
76. Toh, W.S., Guo, X.M., Choo, A.B., Lu, K., Lee, E.H., and Cao, T. Differentiation and enrichment of expandable chondrogenic cells from human embryonic stem cells in vitro. J Cell Mol Med 13, 3570, 2009.
77. Jukes, J.M., Moroni, L., van Blitterswijk, C.A., and de Boer, J. Critical steps toward a tissue-engineered cartilage implant using embryonic stem cells. Tissue Eng Part A 14, 135, 2008.
78. Hwang, N.S., and Elisseeff, J. Application of stem cells for articular cartilage regeneration. J Knee Surg 22, 60, 2009.
79. Schreml, S., Babilas, P., Fruth, S., Orso, E., Schmitz, G., Mueller, M.B., et al. Harvesting human adipose tissue-derived adult stem cells: resection versus liposuction. Cytotherapy 11, 947, 2009.
80. Steinert, A.F., Proffen, B., Kunz, M., Hendrich, C., Ghivizzani, S.C., Noth, U., et al. Hypertrophy is induced during the in vitro chondrogenic differentiation of human mesenchymal stem cells by bone morphogenetic protein-2 and bone morphogenetic protein-4 gene transfer. Arthritis Res Ther 11, R148, 2009.
81. Weber, C., Gokorsch, S., and Czermak, P. Expansion and chondrogenic differentiation of human mesenchymal stem cells. Int J Artif Organs 30, 611, 2007.
82. Berry, L., Grant, M.E., McClure, J., and Rooney, P. Bonemarrow-derived chondrogenesis in vitro. J Cell Sci 101 (Pt 2), 333, 1992.
83. Vinatier, C., Bouffi, C., Merceron, C., Gordeladze, J., Brondello, J.M., Jorgensen, C., et al. Cartilage tissue engineering: towards a biomaterial-assisted mesenchymal stem cell therapy. Curr Stem Cell Res Ther 4, 318, 2009.
84. Satija, N.K., Singh, V.K., Verma, Y.K., Gupta, P., Sharma, S., Afrin, F., et al. Mesenchymal stem cell-based therapy: a new paradigm in regenerative medicine. J Cell Mol Med 13, 4385, 2009.
85. Kafienah, W., Mistry, S., Dickinson, S.C., Sims, T.J., Learmonth, I., and Hollander, A.P. Three-dimensional cartilage tissue engineering using adult stem cells from osteoarthritis patients. Arthritis Rheum 56, 177, 2007.
86. Krinner, A., Zscharnack, M., Bader, A., Drasdo, D., and Galle, J. Impact of oxygen environment on mesenchymal stem cell expansion and chondrogenic differentiation. Cell Prolif 42, 471, 2009.
87. Ahmed, N., Stanford, W.L., and Kandel, R.A. Mesenchymal stem and progenitor cells for cartilage repair. Skeletal Radiol 36, 909, 2007.
88. Matsuda, C., Takagi, M., Hattori, T., Wakitani, S., and Yoshida, T. Differentiation of human bone marrow mesenchymal stem cells to chondrocytes for construction of threedimensional cartilage tissue. Cytotechnology 47, 11, 2005.
89. Markway, B.D., Tan, G.K., Brooke, G., Hudson, J.E., Cooper-White, J.J., and Doran, M.R. Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell Transplant 19, 29, 2010.
90. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315, 2006.
91. McCarty, R.C., Gronthos, S., Zannettino, A.C., Foster, B.K., and Xian, C.J. Characterisation and developmental potential of ovine bone marrow derived mesenchymal stem cells. J Cell Physiol 219, 324, 2009.
92. Mrugala, D., Bony, C., Neves, N., Caillot, L., Fabre, S., Moukoko, D., et al. Phenotypic and functional characterisation of ovine mesenchymal stem cells: application to a cartilage defect model. Ann Rheum Dis 67, 288, 2008.
93. Rentsch, C., Hess, R., Rentsch, B., Hofmann, A., Manthey, S., Scharnweber, D., et al. Ovine bone marrow mesenchymal stem cells: isolation and characterization of the cells and their osteogenic differentiation potential on embroidered and surface-modified polycaprolactone-co-lactide scaffolds. In Vitro Cell Dev Biol Anim 46, 624, 2010.
94. Murdoch, A.D., Grady, L.M., Ablett, M.P., Katopodi, T., Meadows, R.S., and Hardingham, T.E. Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: generation of scaffold-free cartilage. Stem Cells 25, 2786, 2007.
95. Chevrier, A., Nelea, M., Hurtig, M.B., Hoemann, C.D., and Buschmann, M.D. Meniscus structure in human, sheep, and rabbit for animal models of meniscus repair. J Orthop Res 27, 1197, 2009.
96. Taylor, D.W., Ahmed, N., Gan, L., Gross, A.E., and Kandel, R.A. Proteoglycan and collagen accumulation by passaged chondrocytes can be enhanced through side-by-side culture with primary chondrocytes. Tissue Eng Part A 16, 643, 2010.
97. Walker, E., Ohishi, M., Davey, R.E., Zhang, W., Cassar, P.A., Tanaka, T.S., et al. Prediction and testing of novel transcriptional networks regulating embryonic stem cell self-renewal and commitment. Cell Stem Cell 1, 71, 2007.
98. Pelttari, K., Winter, A., Steck, E., Goetzke, K., Hennig, T., Ochs, B.G., et al. Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum 54, 3254, 2006.
99. Barbero, A., Grogan, S.P., Mainil-Varlet, P., and Martin, I. Expansion on specific substrates regulates the phenotype and differentiation capacity of human articular chondrocytes. J Cell Biochem 98, 1140, 2006.
100. Dickhut, A., Pelttari, K., Janicki, P., Wagner, W., Eckstein, V., Egermann, M., et al. Calcification or dedifferentiation: requirement to lock mesenchymal stem cells in a desired differentiation stage. J Cell Physiol 219, 219, 2009.
101. Allan, K.S., Pilliar, R.M., Wang, J., Grynpas, M.D., and Kandel, R.A. Formation of biphasic constructs containing cartilage with a calcified zone interface. Tissue Eng 13, 167, 2007.
102. Mueller, M.B., and Tuan, R.S. Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 58, 1377, 2008.
103. Zscharnack, M., Hepp, P., Richter, R., Aigner, T., Schulz, R., Somerson, J., et al. Repair of chronic osteochondral defects using predifferentiated mesenchymal stem cells in an ovine model. Am J Sports Med 38, 1857, 2010.
104. Swieszkowski, W., Tuan, B.H., Kurzydlowski, K.J., and Hutmacher, D.W. Repair and regeneration of osteochondral defects in the articular joints. Biomol Eng 24, 489, 2007.
105. Im, G.-I., Ahn, J.-H., Kim, S.-Y., Choi, B.-S., and Lee, S.-W. A Hyaluronate-atelocollagen/b-tricalcium phosphate-hydroxyapatite biphasic scaffold for the repair of osteochondral defects: a porcine study. Tissue Eng Part A 16, 1189, 2009.
106. Kasten, A., Muller, P., Bulnheim, U., Groll, J., Bruellhoff, K., Beck, U., et al. Mechanical integrin stress and magnetic forces induce biological responses in mesenchymal stem cells which depend on environmental factors. J Cell Biochem 111, 1586, 2010.
107. Woodfield, T.B., Miot, S., Martin, I., van Blitterswijk, C.A., and Riesle, J. The regulation of expanded human nasal chondrocyte re-differentiation capacity by substrate composition and gas plasma surface modification. Biomaterials 27, 1043, 2006.
108. Kawazoe, Y., Katoh, S., Onodera, Y., Kohgo, T., Shindoh, M., and Shiba, T. Activation of the FGF signaling pathway and subsequent induction of mesenchymal stem cell differentiation by inorganic polyphosphate. Int J Biol Sci 4, 37, 2008.