Temporal and spatial changes in cartilage-matrix-specific gene expression in mesenchymal stem cells in response to dynamic compression

Tissue Engineering - Part A

Volumn 17, Issue 23-24, 2011, Pages 3085-3093

  Haugh, Matthew G ^a   Meyer, Eric G ^a   Thorpe, Stephen D ^a   Vinardell, Tatiana ^a   Duffy, Garry P ^a,b   Kelly, Daniel J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIALS; CELL CULTURE; DYNAMICS; ENZYME INHIBITION; FLOWCHARTING; GENES; LOADING; POLYMERASE CHAIN REACTION; STEM CELLS; SYNTHESIS (CHEMICAL); TRANSCRIPTION;

AGAROSE; CARTILAGE REPAIR; CELL PHENOTYPE; CHONDROGENESIS; CHONDROGENIC PHENOTYPES; DYNAMIC COMPRESSION; EXPRESSION LEVELS; EXTRACELLULAR MATRICES; LOCAL ENVIRONMENTS; MATRIX GENE EXPRESSIONS; MECHANICAL SIGNALS; MECHANICAL STIMULATION; MECHANICAL STIMULUS; MESENCHYMAL STEM CELL; PERICELLULAR MATRIX; POSITIVE EFFECTS; REVERSE TRANSCRIPTION-POLYMERASE CHAIN REACTION; SPATIAL REGIONS; TEMPORAL AND SPATIAL CHANGES; TEMPORAL APPLICATIONS; TRANSFORMING GROWTH FACTORS;

CARTILAGE;

DNA;

ANIMAL; ARTICLE; CARTILAGE; CHONDROGENESIS; COMPRESSIVE STRENGTH; CYTOLOGY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; MECHANICAL STRESS; MESENCHYMAL STEM CELL; METABOLISM; SWINE; TIME;

ANIMALS; CARTILAGE; CHONDROGENESIS; COMPRESSIVE STRENGTH; DNA; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELLS; STRESS, MECHANICAL; SUS SCROFA; TIME FACTORS;

EID: 82355184372     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2011.0198     Document Type: Article

References (43)

1. Huang, C.Y., Hagar, K.L., Frost, L.E., Sun, Y., and Cheung, H.S. Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells 22, 313, 2004.
2. Caplan, A.I. Mesenchymal stem cells. J Orthop Res 9, 641, 1991.
3. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., and Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
4. Tuan, R.S., Boland, G., and Tuli, R. Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther 5, 32, 2003.
5. Huang, A.H., Farrell, M.J., Kim, M., and Mauck, R.L. Longterm dynamic loading improves the mechanical properties of chondrogenic mesenchymal stem cell-laden hydrogel. Eur Cell Mater 19, 72, 2010.
6. Erickson, I.E., Huang, A.H., Chung, C., Li, R.T., Burdick, J.A., and Mauck, R.L. Differential maturation and structurefunction relationships in mesenchymal stem cell-and chondrocyte-seeded hydrogels. Tissue Eng Part A 15, 1041, 2009.
7. Kopesky, P.W., Lee, H.Y., Vanderploeg, E.J., Kisiday, J.D., Frisbie, D.D., Plaas, A.H., Ortiz, C., and Grodzinsky, A.J. Adult equine bone marrow stromal cells produce a cartilagelike ECM mechanically superior to animal-matched adult chondrocytes. Matrix Biol 29, 427, 2010.
8. Vinardell, T., Thorpe, S.D., Buckley, C.T., and Kelly, D.J. Chondrogenesis and integration of mesenchymal stem cells within an in vitro cartilage defect repair model. Ann Biomed Eng 37, 2556, 2009.
9. Sheehy, E.J., Buckley, C.T., and Kelly, D.J. Chondrocytes and bone marrow derived mesenchymal stem cells undergoing chondrogenesis in agarose hydrogels of solid and channelled architectures respond differentially to dynamic culture conditions. J Tissue Eng Regen Med 2011 [Epub ahead of print]; doi: 10.1002/term.385.
10. Mauck, R.L., Byers, B.A., Yuan, X., and Tuan, R.S. Regulation of cartilaginous ECM gene transcription by chondrocytes and MSCs in 3D culture in response to dynamic loading. Biomech Model Mechanobiol 6, 113, 2007.
11. Babalola, O., and Bonassar, L. Effects of seeding density on proteoglycan assembly of passaged mesenchymal stem cells. Cell Mol Bioeng 3, 197, 2010.
12. Mikic, B., Isenstein, A.L., and Chhabra, A. Mechanical modulation of cartilage structure and function during embryogenesis in the chick. Ann Biomed Eng 32, 18, 2004.
13. Nowlan, N.C., Bourdon, C., Dumas, G., Tajbakhsh, S., Prendergast, P.J., and Murphy, P. Developing bones are differentially affected by compromised skeletal muscle formation. Bone 46, 1275, 2010.
14. Mikic, B., Johnson, T.L., Chhabra, A.B., Schalet, B.J., Wong, M., and Hunziker, E.B. Differential effects of embryonic immobilization on the development of fibrocartilaginous skeletal elements. J Rehabil Res Dev 37, 127, 2000.
15. Chen, X., Macica, C.M., Nasiri, A., and Broadus, A.E. Regulation of articular chondrocyte proliferation and differentiation by indian hedgehog and parathyroid hormonerelated protein in mice. Arthritis Rheum 58, 3788, 2008.
16. Thorpe, S.D., Buckley, C.T., Vinardell, T., O'Brien, F.J., Campbell, V.A., and Kelly, D.J. The response of bone marrow-derived mesenchymal stem cells to dynamic compression following TGF-beta3 induced chondrogenic differentiation. Ann Biomed Eng 38, 2896, 2010.
17. Kelly, D.J., and Jacobs, C.R. The role of mechanical signals in regulating chondrogenesis and osteogenesis of mesenchy-mal stem cells. Birth Defects Res C Embryo Today 90, 75, 2010.
18. Li, Z., Yao, S.-J., Alini, M., and Stoddart, M.J. Chondrogenesis of human bone marrow mesenchymal stem cells in fibrin-polyurethane composites is modulated by frequency and amplitude of dynamic compression and shear stress. Tissue Eng Part A 16, 575, 2010.
19. McMahon, L.A., Reid, A.J., Campbell, V.A., and Prendergast, P.J. Regulatory effects of mechanical strain on the chondrogenic differentiation of MSCs in a collagen-GAG scaffold: experimental and computational analysis. Ann Biomed Eng 36, 185, 2008.
20. Kisiday, J.D., Frisbie, D.D., McIlwraith, C.W., and Grodzinsky, A.J. Dynamic compression stimulates proteoglycan synthesis by mesenchymal stem cells in the absence of chondrogenic cytokines. Tissue Eng Part A 15, 2817, 2009.
21. Buckley, C.T., Vinardell, T., Thorpe, S.D., Haugh, M.G., Jones, E., McGonagle, D., and Kelly, D.J. Functional properties of cartilaginous tissues engineered from infrapatellar fat pad-derived mesenchymal stem cells. J Biomech 43, 920, 2010.
22. Thorpe, S.D., Buckley, C.T., Vinardell, T., O'Brien, F.J., Campbell, V.A., and Kelly, D.J. Dynamic compression can inhibit chondrogenesis of mesenchymal stem cells. Biochem Biophys Res Commun 377, 458, 2008.
23. Meyer, E.G., Buckley, C.T., Thorpe, S.D., and Kelly, D.J. Low oxygen tension is a more potent promoter of chondrogenic differentiation than dynamic compression. J Biomech 43, 2516, 2010.
24. Guaccio, A., Borselli, C., Oliviero, O., and Netti, P.A. Oxygen consumption of chondrocytes in agarose and collagen gels: a comparative analysis. Biomaterials 29, 1484, 2008.
25. Buckley, C.T., Vinardell, T., and Kelly, D.J. Oxygen tension differentially regulates the functional properties of cartilaginous tissues engineered from infrapatellar fat pad derived MSCs and articular chondrocytes. Osteoarthritis Cartilage 18, 1345, 2010.
26. Mouw, J.K., Connelly, J.T., Wilson, C.G., Michael, K.E., and Levenston, M.E. Dynamic compression regulates the expression and synthesis of chondrocyte-specific matrix molecules in bone marrow stromal cells. Stem Cells 25, 655, 2007.
27. Lennon, D.P., and Caplan, A.I. Isolation of human marrowderived mesenchymal stem cells. Exp Hematol 34, 1604, 2006.
28. Kim, Y.J., Sah, R.L., Doong, J.Y., and Grodzinsky, A.J. Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174, 168, 1988.
29. Kafienah, W., and Sims, T.J. Biochemical methods for the analysis of tissue-engineered cartilage. Methods Mol Biol 238, 217, 2004.
30. Ignat'eva, N., Danilov, N., Averkiev, S., Obrezkova, M., Lunin, V., and Sobol', E. Determination of hydroxyproline in tissues and the evaluation of the collagen content of the tissues. J Anal Chem 62, 51, 2007.
31. Kumar, B.M., Yoo, J.G., Ock, S.A., Kim, J.G., Song, H.J., Kang, E.J., Cho, S.K., Lee, S.L., Cho, J.H., Balasubramanian, S., and Rho, G.J. In vitro differentiation of mesenchymal progenitor cells derived from porcine umbilical cord blood. Mol Cells 24, 343, 2007.
32. Zou, L., Zou, X., Chen, L., Li, H., Mygind, T., Kassem, M., and Bunger, C. Multilineage differentiation of porcine bone marrow stromal cells associated with specific gene expression pattern. J Orthop Res 26, 56, 2008.
33. 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.
34. Campbell, J.J., Lee, D.A., and Bader, D.L. Dynamic compressive strain influences chondrogenic gene expression in human mesenchymal stem cells. Biorheology 43, 455, 2006.
35. Lewis, M.C., MacArthur, B.D., Malda, J., Pettet, G., and Please, C.P. Heterogeneous proliferation within engineered cartilaginous tissue: the role of oxygen tension. Biotechnol Bioeng 91, 607, 2005.
36. Zhou, S., Cui, Z., and Urban, J.P.G. Nutrient gradients in engineered cartilage: Metabolic kinetics measurement and mass transfer modeling. Biotechnol Bioeng 101, 408, 2008.
37. Huang, A.H., Farrell, M.J., and Mauck, R.L. Mechanics and mechanobiology of mesenchymal stem cell-based engineered cartilage. J Biomech 43, 128, 2010.
38. Vigfúsdó ttir, Á ., Pasrija, C., Thakore, P., Schmidt, R., and Hsieh, A. Role of pericellular matrix in mesenchymal stem cell deformation during chondrogenic differentiation. Cell Mol Bioeng 3, 387, 2010.
39. van der Windt, A.E., Haak, E., Das, R.H., Kops, N., Welting, T.J., Caron, M.M., van Til, N.P., Verhaar, J.A., Weinans, H., and Jahr, H. Physiological tonicity improves human chondrogenic marker expression through nuclear factor of activated T-cells 5 in vitro. Arthritis Res Ther 12, R100, 2010.
40. Urban, J.P., Hall, A.C., and Gehl, K.A. Regulation of matrix synthesis rates by the ionic and osmotic environment of articular chondrocytes. J Cell Physiol 154, 262, 1993.
41. Palmer, G.D., Chao Ph, P.H., Raia, F., Mauck, R.L., Valhmu, W.B., and Hung, C.T. Time-dependent aggrecan gene expression of articular chondrocytes in response to hyperosmotic loading. Osteoarthritis Cartilage 9, 761, 2001.
42. Hung, C.T., LeRoux, M.A., Palmer, G.D., Chao, P.H., Lo, S., and Valhmu, W.B. Disparate aggrecan gene expression in chondrocytes subjected to hypotonic and hypertonic loading in 2D and 3D culture. Biorheology 40, 61, 2003.
43. Negoro, K., Kobayashi, S., Takeno, K., Uchida, K., and Baba, H. Effect of osmolarity on glycosaminoglycan production and cell metabolism of articular chondrocyte under three-dimensional culture system. Clin Exp Rheumatol 26, 534, 2008.