Temporal exposure to chondrogenic factors modulates human mesenchymal stem cell chondrogenesis in hydrogels

Tissue Engineering - Part A

Volumn 17, Issue 3-4, 2011, Pages 371-380

  Buxton, Amanda N ^a,b   Bahney, Chelsea S ^a   Yoo, Jung U ^a   Johnstone, Brian ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b Case Western Reserve University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL CULTURE; CARTILAGE; COLLAGEN; ETHYLENE; ETHYLENE GLYCOL; GENE EXPRESSION; HYDROGELS; LIGAMENTS; POLYETHYLENE GLYCOLS; POLYETHYLENE OXIDES; STEM CELLS; TISSUE ENGINEERING;

CELL DENSITY; CELL-CELL CONTACT; CHONDROGENESIS; CHONDROGENIC; CHONDROGENIC CELLS; COLLAGEN CONTENT; COLLAGEN DEPOSITION; COLLAGEN I; DEXAMETHASONES; HUMAN MESENCHYMAL STEM CELLS; HUMAN MESENCHYMAL STEM CELLS (HMSCS); HYALINE CARTILAGE; IN-CELL; IN-VITRO; LOWER DENSITY; MATRIX; MATRIX DEPOSITION; OPTIMAL CONDITIONS; PARACRINE; POLY[(ETHYLENE GLYCOL)DIACRYLATE]; PROTEOGLYCANS; TRANSFORMING GROWTH FACTORS;

CELL CULTURE;

SIGNAL PEPTIDE;

ADULT; AGED; ARTICLE; CARTILAGE CELL; CELL CULTURE; CHONDROGENESIS; CULTURE TECHNIQUE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; FEMALE; HUMAN; MALE; MESENCHYMAL STEM CELL; METHODOLOGY; MIDDLE AGED; PHYSIOLOGY; TIME; TISSUE ENGINEERING;

ADULT; AGED; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MESENCHYMAL STEM CELLS; MIDDLE AGED; TIME FACTORS; TISSUE ENGINEERING; YOUNG ADULT;

EID: 79551513942     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0839     Document Type: Article

References (47)

1. Johnstone, B., and Yoo, J. Mesenchymal cell transfer for articular cartilage repair. Expert Opin Biol Ther 1, 915, 2001.
2. Johnstone, B., Yoo, J., and Stewart, M. Cell Sources for Cartilage Tissue Engineering. Hoboken, NJ: Wiley, 2006.
3. Richardson, S.M., Hoyland, J.A., Mobasheri, R., Csaki, C., Shakibaei, M., and Mobasheri, A. Mesenchymal stem cells in regenerative medicine: opportunities and challenges for articular cartilage and intervertebral disc tissue engineering. J Cell Physiol 222, 23, 2010.
4. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
5. Yoo, J.U., Barthel, T.S., Nishimura, K., Solchaga, L., Caplan, A.I., Goldberg, V.M., et al. The chondrogenic potential of human bone-marrow-derived mesenchymal progenitor cells. J Bone Joint Surg Am 80, 1745, 1998.
6. Johnstone, B., Hering, T.M., Caplan, A.I., Goldberg, V.M., and Yoo, J.U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238, 265, 1998.
7. Derfoul, A., Perkins, G.L., Hall, D.J., and Tuan, R.S. Glucocorticoids promote chondrogenic differentiation of adult human mesenchymal stem cells by enhancing expression of cartilage extracellular matrix genes. Stem Cells 24, 1487, 2006.
8. Awad, H.A., Halvorsen, Y.D., Gimble, J.M., and Guilak, F. Effects of transforming growth factor beta1 and dexameth-asone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng 9, 1301, 2003.
9. Miura, Y., Fitzsimmons, J.S., Commisso, C.N., Gallay, S.H., and O'Driscoll, S.W. Enhancement of periosteal chondrogenesis in vitro. Dose-response for transforming growth factor-beta 1 (TGF-beta 1). Clin Orthop Relat Res 301, 271, 1994.
10. Mizuta, H., Sanyal, A., Fukumoto, T., Fitzsimmons, J.S., Matsui, N., Bolander, M.E., et al. The spatiotemporal expression of TGF-beta1 and its receptors during periosteal chondrogenesis in vitro. J Orthop Res 20, 562, 2002.
11. Miura, Y., Parvizi, J., Fitzsimmons, J.S., and O'Driscoll, S.W. Brief exposure to high-dose transforming growth factor-beta1 enhances periosteal chondrogenesis in vitro: a preliminary report. J Bone Joint Surg Am 84-A, 793, 2002.
12. Diekman, B.O., Rowland, C.R., Caplan, A.I., Lennon, D., and Guilak, F. Chondrogenesis of adult stem cells from adipose tissue and bone marrow: induction by growth factors and cartilage derived matrix. Tissue Eng Part A 16, 523, 2010.
13. Williams, C.G., Kim, T.K., Taboas, A., Malik, A., Manson, P., and Elisseeff, J. In vitro chondrogenesis of bone marrow-derived mesenchymal stem cells in a photopolymerizing hydrogel. Tissue Eng 9, 679, 2003.
14. Nicodemus, G.D., and Bryant, S. Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng Part B Rev 14, 149, 2008.
15. Lutolf, M.P., and Hubbell, J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23, 47, 2005.
16. Ifkovits, J.L., and Burdick, J.A. Review: photopolymerizable and degradable biomaterials for tissue engineering applications. Tissue Eng 13, 2369, 2007.
17. Buxton, A.N., Zhu, J., Marchant, R., West, J.L., Yoo, J.U., and Johnstone, B. Design and characterization of poly(ethylene glycol) photopolymerizable semi-interpenetrating networks for chondrogenesis of human mesenchymal stem cells. Tissue Eng 13, 2549, 2007.
18. Mann, B.K., Schmedlen, R.H., and West, J.L. Tethered-TGF-beta increases extracellular matrix production of vascular smooth muscle cells. Biomaterials 22, 439, 2001.
19. Farndale, R.W., Buttle, D.J., and Barrett, A.J. Improved quantitation and discrimination of sulphated glycosamino-glycans by use of dimethylmethylene blue. Biochim Biophys Acta 883, 173, 1986.
20. Sanford, L.P., Ormsby, I., Gittenberger-de Groot, A.C., Sariola, H., Friedman, R., Boivin, G.P., et al. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124, 2659, 1997.
21. Targeting arthritis. Department of Health and Human Services, Atlanta, GA, 2003.
22. Murphy, L., Schwartz, T.A., Helmick, C.G., Renner, J.B., Tudor, G., Koch, G., et al. Lifetime risk of symptomatic knee osteoarthritis. Arthritis Rheum 59, 1207, 2008.
23. Stockwell, R.A. The interrelationship of cell density and cartilage thickness in mammalian articular cartilage. J Anat 109, 411, 1971.
24. Mobasheri, A., Bondy, C.A., Moley, K., Mendes, A.F., Rosa, S.C., Richardson, S.M., et al. Facilitative Glucose Transporters in Articular Chondrocytes. New York, NY: Springer, 2008.
25. Mobasheri, A., Vannucci, S.J., Bondy, C.A., Carter, S.D., Innes, J.F., Arteaga, M.F., et al. Glucose transport and metabolism in chondrocytes: a key to understanding chon-drogenesis, skeletal development and cartilage degradation in osteoarthritis. Histol Histopathol 17, 1239, 2002.
26. Otte, P. Basic cell metabolism of articular cartilage. Manometric studies. Z Rheumatol 50, 304, 1991.
27. Kavalkovich, K.W., Boynton, R.E., Murphy, J.M., and Barry, F. Chondrogenic differentiation of human mesenchymal stem cells within an alginate layer culture system. In Vitro Cell Dev Biol Anim 38, 457, 2002.
28. Chimal-Monroy, J., and Diaz de Leon, L. Expression of N-cadherin, N-CAM, fibronectin and tenascin is stimulated by TGF-beta1, beta2, beta3 and beta5 during the formation of precartilage condensations. Int J Dev Biol 43, 59, 1999.
29. Tuli, R., Tuli, S., Nandi, S., Huang, X., Manner, P.A., Hozack, W.J., et al. Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves N-cadherin and mitogen-activated protein kinase and Wnt signaling crosstalk. J Biol Chem 278, 41227, 2003.
30. Serra, R., Johnson, M., Filvaroff, E.H., LaBorde, J., Sheehan, D.M., Derynck, R., et al. Expression of a truncated, kinase-defective TGF-beta type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J Cell Biol 139, 541, 1997.
31. Watanabe, H. Transcriptional crosstalk between Smad, ERK1/2, and p38 mitogen-activated protein kinase pathways regulates transforming growth factor-b-induced ag-grecan gene expression in chondrogenic ATDC5 cells. J Biol Chem 227, 14466, 2001.
32. Cheng, S.L., Yang, J.W., Rifas, L., Zhang, S.F., and Avioli, L.V. Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone. Endocrinology 134, 277, 1994.
33. Mauck, R.L., Yuan, X., and Tuan, R.S. Chondrogenic differentiation and functional maturation of bovine mesen-chymal stem cells in long-term agarose culture. Osteoarthritis Cartilage 14, 179, 2006.
34. Salinas, C.N., Cole, B.B., Kasko, A.M., and Anseth, K.S. Chondrogenic differentiation potential of human mesen-chymal stem cells photoencapsulated within poly(ethylene glycol)-arginine-glycine-aspartic acid-serine thiol-methacry-late mixed-mode networks. Tissue Eng 13, 1025, 2007.
35. Solursh, M., Linsenmayer, T.F., and Jensen, K.L. Chon-drogenesis from single limb mesenchyme cells. Dev Biol 94, 259, 1982.
36. Solursh, M., and Reiter, R.S. Determination of limb bud chondrocytes during a transient block of the cell cycle. Cell Differ 4, 131, 1975.
37. Archer, C.W., Rooney, P., and Wolpert, L. Cell shape and cartilage differentiation of early chick limb bud cells in culture. Cell Differ 11, 245, 1982.
38. Zanetti, N.C., and Solursh, M. Induction of chondrogenesis in limb mesenchymal cultures by disruption of the actin cytoskeleton. J Cell Biol 99, 115, 1984.
39. Pelttari, K., Steck, E., and Richter, W. The use of mesen-chymal stem cells for chondrogenesis. Injury 39 Suppl 1, S58, 2008.
40. Bedi, A., Feeley, B.T., and Williams, R.J., 3rd. Management of articular cartilage defects of the knee. J Bone Joint Surg Am 92, 994, 2010.
41. 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.
42. 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.
43. Carter, D.R., Beaupre, G.S., Wong, M., Smith, R.L., An-driacchi, T.P., and Schurman, D.J. The mechanobiology of articular cartilage development and degeneration. Clin Orthop Relat Res S69, 2004.
44. Wong, M., and Carter, D.R. Articular cartilage functional histomorphology and mechanobiology: a research perspective. Bone 33, 1, 2003.
45. Khan, I.M., Redman, S.N., Williams, R., Dowthwaite, G.P., Oldfield, S.F., and Archer, C.W. The development of syno-vial joints. Curr Top Dev Biol 79, 1, 2007.
46. Ito, M.M., and Kida, M.Y. Morphological and biochemical re-evaluation of the process of cavitation in the rat knee joint: cellular and cell strata alterations in the interzone. J Anat 197 (Pt 4), 659, 2000.
47. Koyama, E., Shibukawa, Y., Nagayama, M., Sugito, H., Young, B., Yuasa, T., et al. A distinct cohort of progenitor cells participates in synovial joint and articular cartilage formation during mouse limb skeletogenesis. Dev Biol 316, 62, 2008.