DLX5 overexpression impairs osteogenic differentiation of human bone marrow stromal cells

European Journal of Cell Biology

Volumn 87, Issue 10, 2008, Pages 751-761

  Muraglia, Anita ^a,b   Perera, Marzia ^a   Verardo, Sara ^a   Liu, Yi ^a,b   Cancedda, Ranieri ^a,b   Quarto, Rodolfo ^c   Corte, Giorgio ^a,b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c CENTRO DI BIOTECNOLOGIE AVANZATE   (Italy)

Author keywords

Bone marrow stromal cells; Differentiation; DLX5

Indexed keywords

TRANSCRIPTION FACTOR DLX5;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; BONE MARROW STROMAL CELL; BONE MATRIX; CELL DIFFERENTIATION; CHONDROGENESIS; CONTROLLED STUDY; EX VIVO STUDY; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; RETROVIRUS INFECTION;

ADOLESCENT; ADULT; ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; GENE EXPRESSION PROFILING; GENETIC VECTORS; HOMEODOMAIN PROTEINS; HUMANS; MESENCHYMAL STEM CELLS; MICE; OSTEOCYTES; OSTEOGENESIS; RETROVIRIDAE; SOXB1 TRANSCRIPTION FACTORS; STROMAL CELLS; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC; YOUNG ADULT;

MUS;

EID: 51249111519     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2008.04.004     Document Type: Article

References (42)

1. Acampora D., Merlo G.R., Paleari L., Zerega B., Postiglione M.P., Mantero S., Bober E., Barbieri O., Simeone A., and Levi G. Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene DLX5. Development 126 (1999) 3795-3809
2. Banfi A., Muraglia A., Dozin B., Mastrogiacomo M., Cancedda R., and Quarto R. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy. Exp. Hematol. 28 (2000) 707-715
3. Bendall A.J., Hu G., Levi G., and Abate-Shen C. DLX5 regulates chondrocyte differentiation at multiple stages. Int. J. Dev. Biol. 47 (2003) 335-344
4. Berry L., Grant M.E., McClure J., and Rooney P. Bone-marrow-derived chondrogenesis in vitro. J. Cell Sci. 101 (1992) 333-342
5. Bianco P., Riminucci M., Gronthos S., and Robey P.G. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19 (2001) 180-192
6. Chen X., Li X., Wang W., and Lufkin T. Dlx5 and Dlx6: an evolutionary conserved pair of murine homeobox genes expressed in the embryonic skeleton. Ann. NY Acad. Sci. 785 (1996) 38-47
7. Denizot F., and Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 89 (1986) 271-277
8. Ellis P., Fagan B.M., Magness S.T., Hutton S., Taranova O., Hayashi S., McMahon A., Rao M., and Pevny L. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev. Neurosci. 26 (2004) 148-165
9. Erceg I., Tadic T., Kronenberg M.S., Marijanovic I., and Lichtler A.C. DLX5 regulation of mouse osteoblast differentiation mediated by avian retrovirus vector. Croat. Med. J. 44 (2003) 407-411
10. Ferrari D., and Kosher R.A. DLX5 is a positive regulator of chondrocyte differentiation during endochondral ossification. Dev. Biol. 252 (2002) 257-270
11. Frolik C.A., Ellis L.F., and Williams D.C. Isolation and characterization of insulin-like growth factor-II from human bone. Biochem. Biophys. Res. Commun. 151 (1988) 1011-1018
12. Geoffroy V., Kneissel M., Fournier B., Boyde A., and Matthias P. High bone resorption in adult aging transgenic mice overexpressing cbfa1/runx2 in cells of the osteoblastic lineage. Mol. Cell. Biol. 22 (2002) 6222-6233
13. Goshima J., Goldberg V.M., and Caplan A.I. The osteogenic potential of culture-expanded rat marrow mesenchymal cells assayed in vivo in calcium phosphate ceramic blocks. Clin. Orthop. Relat. Res. 262 (1991) 298-311
14. Graham V., Khudyakov J., Ellis P., and Pevny L. SOX2 functions to maintain neural progenitor identity. Neuron 39 (2003) 749-765
15. Gundle R., Joyner C.J., and Triffitt J.T. Human bone tissue formation in diffusion chamber culture in vivo by bone-derived cells and marrow stromal fibroblastic cells. Bone 16 (1995) 597-601
16. Haynesworth S.E., Goshima J., Goldberg V.M., and Caplan A.I. Characterization of cells with osteogenic potential from human marrow. Bone 13 (1992) 81-88
17. Hock J.M., Centrella M., and Canalis E. Insulin-like growth factor I has independent effects on bone matrix formation and cell replication. Endocrinology 122 (1988) 254-260
18. 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 (1998) 265-272
19. Kim Y.J., Lee M.H., Wozney J.M., Cho J.Y., and Ryoo H.M. Bone morphogenetic protein-2-induced alkaline phosphatase expression is stimulated by DLX5 and repressed by Msx2. J. Biol. Chem. 279 (2004) 50773-50780
20. Krebsbach P.H., Kuznetsov S.A., Satomura K., Emmons R.V., Rowe D.W., and Robey P.G. Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 63 (1997) 1059-1069
21. Kuznetsov S.A., Krebsbach P.H., Satomura K., Kerr J., Riminucci M., Benayahu D., and Robey P.G. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J. Bone Miner. Res. 12 (1997) 1335-1347
22. Lee M.H., Kwon T.G., Park H.S., Wozney J.M., and Ryoo H.M. BMP-2-induced Osterix expression is mediated by DLX5 but is independent of Runx2. Biochem. Biophys. Res. Commun. 309 (2003) 689-694
23. Levi G., Puche A.C., Mantero S., Barbieri O., Trombino S., Paleari L., Egeo A., and Merlo G.R. The DLX5 homeodomain gene is essential for olfactory development and connectivity in the mouse. Mol. Cell. Neurosci. 22 (2003) 530-543
24. Li H., Marijanovic I., Kronenberg M.S., Erceg I., Stover M.L., Velonis D., Mina M., Heinrich J.G., Harris S.E., Upholt W.B., Kalajzic I., and Lichtler A.C. Expression and function of Dlx genes in the osteoblast lineage. Dev. Biol. 316 (2008) 458-470
25. Liu W., Toyosawa S., Furuichi T., Kanatani N., Yoshida C., Liu Y., Himeno M., Narai S., Yamaguchi A., and Komori T. Overexpression of Cbfa1 in osteoblasts inhibits osteoblast maturation and causes osteopenia with multiple fractures. J. Cell Biol. 155 (2001) 157-166
26. Long J.E., Garel S., Depew M.J., Tobet S., and Rubenstein J.L. DLX5 regulates development of peripheral and central components of the olfactory system. J. Neurosci. 23 (2003) 568-578
27. Mansukhani A., Ambrosetti D., Holmes G., Cornivelli L., and Basilico C. Sox2 induction by FGF and FGFR2 activating mutations inhibits Wnt signaling and osteoblast differentiation. J. Cell Biol. 168 (2005) 1065-1076
28. Mark M.P., Butler W.T., Prince C.W., Finkelman R.D., and Ruch J.V. Developmental expression of 44-kDa bone phosphoprotein (osteopontin) and bone gamma-carboxyglutamic acid (Gla)-containing protein (osteocalcin) in calcifying tissues of rat. Differentiation 37 (1988) 123-136
29. Martin I., Muraglia A., Campanile G., Cancedda R., and Quarto R. Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. Endocrinology 138 (1997) 4456-4462
30. Martin I., Mastrogiacomo M., De Leo G., Muraglia A., Beltrame F., Cancedda R., and Quarto R. Fluorescence microscopy imaging of bone for automated histomorphometry. Tissue Eng. 8 (2002) 847-852
31. Mastrogiacomo M., Derubeis A.R., and Cancedda R. Bone and cartilage formation by skeletal muscle derived cells. J. Cell. Physiol. 204 (2005) 594-603
32. Merlo G.R., Paleari L., Mantero S., Zerega B., Adamska M., Rinkwitz S., Bober E., and Levi G. The DLX5 homeobox gene is essential for vestibular morphogenesis in the mouse embryo through a BMP4-mediated pathway. Dev. Biol. 248 (2002) 157-169
33. Miyama K., Yamada G., Yamamoto T.S., Takagi C., Miyado K., Sakai M., Ueno N., and Shibuya H. A BMP-inducible gene, DLX5, regulates osteoblast differentiation and mesoderm induction. Dev. Biol. 208 (1999) 123-133
34. Muraglia A., Corsi A., Riminucci M., Mastrogiacomo M., Cancedda R., Bianco P., and Quarto R. Formation of a chondro-osseous rudiment in micromass cultures of human bone-marrow stromal cells. J. Cell Sci. 116 (2003) 2949-2955
35. Perera M., Merlo G.R., Verardo S., Paleari L., Corte G., and Levi G. Defective neuronogenesis in the absence of DLX5. Mol. Cell. Neurosci. 25 (2004) 153-161
36. 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 (1999) 143-147
37. Robledo R.F., Rajan L., Li X., and Lufkin T. The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev. 16 (2002) 1089-1101
38. Ryoo H.M., Hoffmann H.M., Beumer T., Frenkel B., Towler D.A., Stein G.S., Stein J.L., van Wijnen A.J., and Lian J.B. Stage-specific expression of Dlx-5 during osteoblast differentiation: involvement in regulation of osteocalcin gene expression. Mol. Endocrinol. 11 (1997) 1681-1694
39. Simeone A., Acampora D., Pannese M., D'Esposito M., Stornaiuolo A., Gulisano M., Mallamaci A., Kastury K., Druck T., Huebner K., and Boncinelli E. Cloning and characterization of two members of the vertebrate Dlx gene family. Proc. Natl. Acad. Sci. USA 91 (1994) 2250-2254
40. Stein G.S., Lian J.B., and Owen T.A. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J. 4 (1990) 3111-3123
41. Tadic T., Dodig M., Erceg I., Marijanovic I., Mina M., Kalajzic Z., Velonis D., Kronenberg M.S., Kosher R.A., Ferrari D., and Lichtler A.C. Overexpression of DLX5 in chicken calvarial cells accelerates osteoblastic differentiation. J. Bone Miner. Res. 17 (2002) 1008-1014
42. Zhao G.Q., Zhao S., Zhou X., Eberspaecher H., Solursh M., and de Crombrugghe B. rDlx, a novel Distal-less-like homeoprotein is expressed in developing cartilages and discrete neuronal tissues. Dev. Biol. 164 (1994) 37-51