BMP2 initiates chondrogenic lineage development of adult human mesenchymal stem cells in high-density culture

Differentiation

Volumn 71, Issue 9-10, 2003, Pages 567-577

  Schmitt, Bernhard ^a   Ringe, Jochen ^a,b   Häupl, Thomas ^a   Notter, Michael ^c   Manz, Rudi ^d   Burmester, Gerd Rüdiger ^a   Sittinger, Michael ^a   Kaps, Christian ^a,b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b TRANSTISSUE TECHNOLOGIES GMBH   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d German Rheumatism Research Center   (Germany)

Author keywords

Bone marrow; Bone morphogenetic protein; Chondrogenesis; Gene expression analysis; High density culture; Mesenchymal stem cells

Indexed keywords

AGGRECAN; BONE MORPHOGENETIC PROTEIN 2; CARTILAGE LINK PROTEIN; CARTILAGE OLIGOMETRIC MATRIX PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; COLLAGEN TYPE 9; FATTY ACID BINDING PROTEIN; OSTEOCALCIN; PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; BONE DEVELOPMENT; CARTILAGE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL STIMULATION; CHONDROGENESIS; EXTRACELLULAR MATRIX; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MESENCHYME; PRIORITY JOURNAL; STEM CELL; TISSUE ENGINEERING;

EID: 0346496061     PISSN: 03014681     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2003.07109003.x     Document Type: Article

References (48)

1. ABI Prism 77 (1997) User Bulletin #2, ABI Prism 7700 Sequence Detection System. Applied Biosystems 1-36.
2. Ahrens, M., Ankenbauer, T., Schroder, D., Hollnagel, A., Mayer, H. and Gross, G. (1993) Expression of human bone morphogenetic proteins-2 or -4 in murine mesenchymal progenitor C3H10T1/2 cells induces differentiation into distinct mesenchymal cell lineages. DNA Cell Biol 12:871-880.
3. Barry, F.P., Boynton, R.E., Haynesworth, S., Murphy, J.M. and Zaia, J. (1999) The monoclonal antibody SH-2, raised against human mesenchymal stem cells, recognizes an epitope on endoglin (CD105). Biochem Biophys Res Commun 265:134-139.
4. Barry, F., Boynton, R.E., Liu, B. and Murphy, J.M. (2001) Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation- dependent gene expression of matrix components. Exp Cell Res 268:189-200.
5. Bruder, S.P., Ricalton, N.S., Boynton, R.E., Connolly, T.J., Jaiswal, N., Zaia, J. and Barry, F.P. (1998) Mesenchymal stem cell surface antigen SB-10 corresponds to activated leukocyte cell adhesion molecule and is involved in osteogenic differentiation. J Bone Miner Res 13:655-663.
6. Buckwalter, J.A. (2002) Articular cartilage injuries. Clin Orthop 402:21-37.
7. Caplan, A.I. (1994) The mesengenic process. Clin Plast Surg 21:429-435.
8. Caplan, A.I. and Bruder, S.P. (2001) Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med 7:259-264.
9. Carlberg, A.L., Pucci, B., Rallapalli, R., Tuan, R.S. and Hall, D.J. (2001) Efficient chondrogenic differentiation of mesenchymal cells in micromass culture by retroviral gene transfer of BMP-2. Differentiation 67:128-138.
10. Chomczynski, P. (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 15:532-534, 536-537.
11. Colter, D.C., Sekiya, I. and Prockop, D.J. (2001) Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci USA 98:7841-7845.
12. Conget, P.A. and Minguell, J.J. (1999) Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J Cell Physiol 181:67-73.
13. Cunningham, N.S., Paralkar, V. and Reddi, A.H. (1992) Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor β1 mRNA expression. Proc Natl Acad Sci USA 89:11740-11744.
14. Denker, A.E., Haas, A.R., Nicoll, S.B. and Tuan, R.S. (1999) Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: I. Stimulation by bone morphogenetic protein-2 in high-density micromass cultures. Differentiation 64:67-76.
15. Duprez, D.M., Coltey, M., Amthor, H., Brickell, P.M. and Tickle, C. (1996) Bone morphogenetic protein-2 (BMP-2) inhibits muscle development and promotes cartilage formation in chick limb bud cultures. Dev Biol 174:448-452.
16. Galotto, M., Berisso, G., Delfino, L., Podesta, M., Ottaggio, L., Dallorso, S., Dufour, C., Ferrara, G.B., Abbondandolo, A., Dini, G., Bacigalupo, A., Cancedda, R. and Quarto, R. (1999) Stromal damage as consequence of high-dose chemo/radio-therapy in bone marrow transplant recipients. Exp Hematol 27:1460-1466.
17. Gubler, U. and Hoffman, B.J. (1983) A simple and very efficient method for generating cDNA libraries. Gene 25: 263-269.
18. Hanada, K., Solchaga, L.A., Caplan, A.I., Hering, T.M., Goldberg, V.M., Yoo, J.U. and Johnstone, B. (2001) BMP-2 induction and TGF-β1 modulation of rat periosteal cell chondrogenesis. J Cell Biochem 81:284-294.
19. Haynesworth, S.E., Goshima, J., Goldberg, V.M. and Caplan, A.I. (1992) Characterization of cells with osteogenic potential from human marrow. Bone 13:81-88.
20. Iwasaki, M., Nakata, K., Nakahara, H., Nakase, T., Kimura, T., Kimata, K., Caplan, A.I. and Ono, K. (1993) Transforming growth factor-β1 stimulates chondrogenesis and inhibits osteogenesis in high density culture of periosteum-derived cells. Endocrinology 132:1603-1608.
21. Johnstone, B., Hering, T.M., Caplan, A.I., Goldberg, V.M. and Yoo, J.U. (1998) In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238:265-272.
22. Katagiri, T. and Takahashi, N. (2002) Regulatory mechanism of osteoblast and osteoclast differentiation. Oral Dis 8:147-159.
23. Kim, W.J., Mohan, R.R., Mohan, R.R. and Wilson, S.E. (1999) Effect of PDGF, IL-1α, and BMP2/4 on corneal fibroblast chemotaxis: expression of the platelet-derived factor system in the cornea. Invest Ophthalmol Vis Sci 40:1364-1372.
24. Lennon, D.P., Haynesworth, S.E., Bruder, S.P., Jaiswal, N. and Caplan, A.I. (1996) Human and animal mesenchymal progenitor cells from bone marrow: identification of serum for optimal selection and proliferation. In Vitro Cell Dev Biol 32:602-611.
25. Luyten, F.P., Yu, Y.M., Yanagishita, M., Vukicevic, S., Hammonds, R.G. and Reddi, A.H. (1992) Natural bovine osteogenin and recombinant human bone morphogenetic protein-2B are equipotent in the maintenance of proteoglycans in bovine articular cartilage explant cultures. J Biol Chem 267:3691-3695.
26. Lyons, K.M., Pelton, R.W. and Hogan, B.L. (1990) Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for bone morphogenetic protein-2A (BMP-2A). Development 109:833-844.
27. Mackay, A.M., Beck, S.C., Murphy, J.M., Barry, F.P., Chichester, C.O. and Pittenger, M.F. (1998) Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4:415-428.
28. Majumdar, M.K., Wang, E. and Morris, E.A. (2001) BMP-2 and BMP-9 promotes chondrogenic differentiation of human multi-potential mesenchymal cells and overcomes the inhibitory effect of IL-1. J Cell Physiol 189:275-284.
29. Mankin, H.J. (1982) The response of articular cartilage to mechanical injury. J Bone Joint Surg Am 64:460-466.
30. Nakase, T., Nomura, S., Yoshikawa, H., Hashimoto, J., Hirota, S., Kitamura, Y., Oikawa, S., Ono, K. and Takaoka, K. (1994) Transient and localized expression of bone morphogenetic protein 4 messenger RNA during fracture healing. J Bone Miner Res 9:651-659.
31. Noble, B.S., Dean, V., Loveridge, N. and Thomson, B.M. (1995) Dextran sulfate promotes the rapid aggregation of porcine bone-marrow stromal cells. Bone 17:375-382.
32. Perides, G., Hu, G., Rueger, D.C. and Charness, M.E. (1993) Osteogenic protein-1 regulates L1 and neural cell adhesion molecule gene expression in neural cells. J Biol Chem 268:25197-25205.
33. 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. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
34. Reddi, A.H. (1992) Regulation of cartilage and bone differentiation by bone morphogenetic proteins. Curr Opin Cell Biol 4:850-855.
35. Ringe, J., Kaps, C., Schmitt, B., Büscher, K., Bartel, J., Smolian, H., Schultz, O., Burmester, G.R., Häupl, T. and Sittinger, M. (2002) Porcine mesenchymal stem cells: induction of distinct mesenchymal cell lineages. Cell Tissue Res 307:321-327.
36. Sailor, L.Z., Hewick, R.M. and Morris, E.A. (1996) Recombinant human bone morphogenetic protein-2 maintains the articular chondrocyte phenotype in long-term culture. J Orthop Res 14:937-945.
37. Sekiya, I., Colter, D.C. and Prockop, D.J. (2001) BMP-6 enhances chondrogenesis in a subpopulation of human marrow stromal cells. Biochem Biophys Res Commun 284:411-418.
38. Shapiro, F., Koide, S. and Glimcher, M.J. (1993) Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg Am 75:532-553.
39. Silbermann, M., von der Mark, K., Maor, G. and van Menxel, M. (1987) Dexamethasone impairs growth and collagen synthesis in condylar cartilage in vitro. Bone Miner 2:87-106.
40. Solursh, M. (1991) Formation of cartilage tissue in vitro. J Cell Biochem 45:258-260.
41. Steadman, J.R., Rodkey, W.G. and Rodrigo, J.J. (2001) Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin Orthop 391S:362-369.
42. Vukicevic, S., Luyten, F.P. and Reddi, A.M. (1989) Stimulation of the expression of osteogenic and chondrogenic phenotypes in vitro by osteogenin. Proc Natl Acad Sci USA 86:8793-8797.
43. Wakitani, S., Imoto, K., Yamamoto, T., Saito, M., Murata, N. and Yoneda, M. (2002) Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 10:199-206.
44. Wall, N.A. and Hogan, B.L. (1994) TGF-β related genes in development. Curr Opin Genet Dev 4:517-522.
45. Wozney, J.M. and Rosen, V. (1998) Bone morphogenetic protein and bone morphogenetic protein gene family in bone formation and repair. Clin Orthop 346:26-37.
46. Yoo, J.U., Barthel, T.S., Nishimura, K., Solchaga, L., Caplan, A.I., Goldberg, V.M. and Johnstone, B. (1998) The chondrogenic potential of human bone-marrow-derived mesenchymal progenitor cells. J Bone Joint Surg Am 80:1745-1757.
47. Zhang, W., Green, C. and Stott, N.S. (2002) Bone morphogenetic protein-2 modulation of chondrogenic differentiation in vitro involves gap junction-mediated intercellular communication. J Cell Physiol 193:233-243.
48. Zimmermann, B. and Cristea, R. (1993) Dexamethasone induces chondrogenesis in organoid culture of cell mixtures from mouse embryos. Anat Embryol (Berl) 187:67-73.