FGF-2 inhibits osteogenesis in mouse adipose tissue-derived stromal cells and sustains their proliferative and osteogenic potential state

Tissue Engineering

Volumn 12, Issue 6, 2006, Pages 1405-1418

  Quarto, Natalina ^a   Longaker, Michael T ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMEDICAL ENGINEERING; GROWTH KINETICS; PATIENT TREATMENT;

ADIPOSE TISSUE-DERIVED STROMAL CELLS (ADS); BONE TISSUE ENGINEERING; OSTEOBLAST DIFFERENTIATION; OSTEOGENESIS;

TISSUE CULTURE;

FIBROBLAST GROWTH FACTOR 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MARROW; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SELECTION; CELL SUBPOPULATION; CONTROLLED STUDY; DOSE RESPONSE; GENE OVEREXPRESSION; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STROMA CELL; TISSUE ENGINEERING;

ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; FIBROBLAST GROWTH FACTOR 2; GROWTH INHIBITORS; MALE; MICE; OSTEOGENESIS; STROMAL CELLS; TISSUE ENGINEERING;

EID: 33746846927     PISSN: 10763279     EISSN: None     Source Type: Journal    
DOI: 10.1089/ten.2006.12.1405     Document Type: Article

References (45)

1. Halvorsen, Y.D., Franklin, D., Bond, A.L., Hitt, D.C., Auchter, C., Boskey, A.L., Paschalis, E.P., Wilkinson W.O., and Gimble J.M. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng. 7, 729, 2001.
2. Tholpady, S.S., Katz, A.J., and Ogle, R.C. Mesenchymal stem cells from rat visceral fat exhibit multipotential differentiation in vitro. Anat. Rec. 272A, 398, 2003.
3. Zuk, P.A., Zhu, M., Mizuno, H., Huang, J., Futrell, J.W., Katz A.J., Benhaim, P., Lorenz, H.P., and Hedrick, M.H. Multilineage cells from adipose tissue: implications for cell-based therapies. Tissue Eng. 7, 211, 2001.
4. Zuk, P.A., Zhu, M., Ashjian, P., DeUgarte, D.A., Huang, J.I., Mizuno, H., Alfonso, Z.C., Fraser, J.K., Benhaim, P., and Hedrick, H.M. Human adipose tissue is a source of multipotent cells. Mol. Biol. Cell 13, 4279, 2002.
5. Mizuno, H., Zuk, P.A., Zhu, M., Lorenz, H.P., Benhaim, P., and Hedrick, M.H. Myogenic differentiation by human processed lipoaspirate cells. Plast. Reconstr. Surg. 109, 199, 2002.
6. Ashjian, P.H., Elbarbary, A.S., Edmonds, B., DeUgarte, D., Zhu, M., Zuk, P.A., Lorenz, H.P., Benhaim, P., and Hedrick, M.H. In vitro differentiation of human processed lipoaspirate cells into early neural progenitors. Plast. Reconstr. Surg. 111, 1922, 2003.
7. Erickson, G.R., Gimble, J.M., Franklin, D.M., Rice, H.E., Awad, H., and Guilak, F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem. Biophys. Res. Commun. 290, 763, 2002.
8. Safford, K.M., Hicok, K.C., Safford, S.D., Halvorsen, Y.D., Wilkison, W.O., Gimble, J.M., and Rice, H.E. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem. Biophys. Res. Commun. 294, 371, 2002.
9. Wickham, M.Q., Erickson, G.R., Gimble, J.A., Vail, T.P., and Guilak, F. Multipotent stromal cells derived from the infrapatellar fat pad on the knee. Clin. Orthop. 412, 198, 2003.
10. Dragoo, J.L., Choi, J.Y., Lieberman, J.R., Huang, J., Zuk, P.A., Zhang, J., Hedrick, M.H., and Benhaim, P. Bone induction by BMP-2 transduced stem cells derived from human fat. J. Orthop. Res. 21, 622, 2003.
11. Lee, J.A., Parrett, B.M., Conejero, J. A., Laser, J., Chen, J., Kogon, A.J., Nanda, D., Grant, R.T., and Breitbart, A.S. Biological alchemy: engineering bone and fat from fat-derived stem cells. Ann. Plast. Surg. 50, 610, 2003.
12. Cowan, M.C., Shi, Y.Y., Aalami, O.O., Chou,Y.F., Mari, C., Thomas, R., Quarto, N., Contag, C.H., Wu, B., and Longaker, M.T. Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nature Biotech. 22, 560, 2004.
13. Karsenty, G., and Wagner, E. Reaching a genetic and molecular understanding of skeletal development. Dev. Cell 2, 389, 2002.
14. Marie, P.J. Fibroblast growth factor signaling controlling osteoblast differentiation. Gene 316, 23, 2003.
15. Quarto, N., Talarico, D., Sommer, A., Florkiewicz, R.Z., Basilico, C., and Rifkin, D.B. Transformation by basic fibroblast growth factor requires high levels of expression: comparison with transformation by hst/K-fgf. Oncogene Res., 5, 101, 1989.
16. Bhargava, U., Bar-Lev, M., Bellows, G.G., and Aubin, J.E. Ultrastructural analysis of bone nodules formed in vitro by isolated fetal rat calvarial cells. Bone 9, 155, 1988.
17. Powell, P.P., and Klagsbrun, M. Three forms of rat basic fibroblast growth factor are made from a single mRNA and localize to the nucleus. J. Cell. Physiol. 148, 202, 1991.
18. Florkiewicz, R.Z., and Sommer, A. Human basic fibroblast growth factor gene encodes four polypeptides: three initiate translation from non-AUG codons. Proc. Natl. Acad. Sci. USA 86, 3978, 1989.
19. Prats, H., Kaghad, M., Prats, A. C., Klagsbrun, M., Lelias, J. M., Liauzun, P., Chalon, P., Tauber, J. P., Amalric, F., Smith, J. A., et al. CUG initiation codon used for the synthesis of a cell surface antigen coded by the murine leukemia virus. Proc. Natl. Acad. Sci. USA 86, 1836, 1988b.
20. Renko, M., Quarto, N., Morimoto, T., and Rifkin, D.B., 1990. Nuclear and cytoplasmic localization of different basic fibroblast growth factor species. J. Cell Physiol. 144, 108, 1990.
21. Quarto, N., Finger, P.P., and Rifkin, D.B. The NH2-terminal extension of high molecular weight bFGF is a nuclear targeting signal. J. Cell Physiol. 147, 311, 1991a.
22. Bugler, B., Amalric, P., and Prats, H. Alternative initiation of translation determines cytoplasmic or nuclear localization of basic fibroblast growth factor. Mol. Cell. Biol. 11, 573, 1991.
23. Mignatti, P., Morimoto, T., and Rifkin, D.B. 1992. Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J. Cell Physiol. 151, 81, 1992.
24. Stein, G.S., Lian, J.B., Stein, A.J., Van Wijnen, A.J., and Montecino, M. Transcriptional control of osteoblast growth and differentiation. Physiol Rev 76, 593, 1996.
25. Ducy, P., Zhang, R., Geoffroy, V., Ridall, A.L., and Karsenty, G. Osf2/Cbfa1: a transcriptional activator of osteoblasts differentiation. Cell 89, 747, 1997.
26. Kim, H-J., Kim, J-H., Bae, S-C., Choi, J-Y., Kim, H-J., and Ryoo, H-M. The protein kinase C pathway plays a central role in the fibroblast growth factor-stimulated expression and transactivation activity of Runx2. J. Biol. Chem. 278, 319, 2003.
27. Rodan, S.B., Wesolowski, G., Yoon, K., and Rodan, G.A. Opposing effects of fibroblast growth factor and pertussis on alkaline phosphatase, osteopontin, osteocalcin, and type I collagen mRNA levels in ROS 17/2.8 cells. J. Biol. Chem. 264, 19934, 1989.
28. Canalis, E., Centrella, M., and McCarthy, T. Effects of basic fibroblast growth factor on bone formation in vitro. J. Clin. Invest. 81, 1572, 1988.
29. Mansukhani, A., Bellosta, P., Sahni M., and Basilico, C. Signaling by fibroblast growth factors (FGF) and fibroblast growth factor receptor 2 (FGFR2)-activating mutations blocks mineralization and induces apoptosis in osteoblasts. J. Cell Biol. 149, 1297, 2000.
30. Sakano, S., Hasegawa, Y., Murata, Y., Ito, T., Genda, E., Iwata, H., Ishiguro, N., and Seo, H. Inhibitory effect of bFGF on endochondral hereotopic ossification. Biochem. Biophys. Res. Commun. 293, 680, 2002.
31. Chaudhary, L.R., Hofmeister A.M., and Hruska, K.A. Differential growth factor control of bone formation through osteoprogenitor differentiation. Bone 34, 402, 2004.
32. 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, 4456, 1997.
33. Bianchi, G., Banfi, A., Mastrogiacoma, M., Notaro, R., Luzzatto, L., Cancedda, R., and Quarto, R. Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. Exp. Cell Res. 287, 98, 2003.
34. Tsutsumi, S., Shimazu, A., Miyazaki, K., Pan, H., Koike, C., Yoshida, E., Takagishi, K., and Kato, Y. Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem. Biophys. Res. Commun. 288, 414, 2001.
35. Xu, R.H., Peck, R.M., Li, D.S., Feng, X., Ludwig, T., and Thomson, J.A. Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nature Methods 2, 185, 2005.
36. Kawaguchi, H., Kurokawa, T., Kanada, K., Hiyama, Y., Tamura, M., Ogata, E., and Matsumoto, T. Stimulation of fracture repair by recombinant human basic fibroblast growth factor in normal and streptozotocin-diabetic rats. Endocrinology 135, 774, 1994.
37. Nakamura, T., Hara, Y., Tagawa, M., Tamura, M., Yuge, T., Fukuda, H., and Nigi, H. Recombinant human basic fibroblast growth factor accelerates fracture healing by enhancing callus remodeling in experimental dog tibial fracture. J. Bone Miner. Res. 13, 942, 1998.
38. Radomsky, M.L., Thompson, A.Y., Spiro, R.C., and Poser, J.W. Potential role of fibroblast growth factor in enhancement of fracture healing. Clin. Orthop. 355, 283, 1998.
39. Kato, T., Kawaguchi, H., Hanada, K., Aoyama, I., Hiyama, Y., Nakamura, T., Kuzutani, K., Tamura, M., Kurokawa, T., and Nakamura, K. Single local injection of recombinant fibroblast growth factor-2 stimulates healing of segmental bone defects in rabbits. J. Orthop. Res. 16, 654, 1998.
40. Inui, K., Maeda, M., Sano, A., Fujioka, K., Yutani, Y., Sakawa, A., Yamano, Y., Kato, Y., and Koike, T. Local application of basic fibroblast growth factor minipellet induces the healing of segmental bony defects in rabbits. Calcif. Tissue Int. 63, 490, 1998.
41. Tabata, Y., Yamada, K., Hong, L., Miyamoto, S., Hashimoto, N., and Ikada, Y. Skull bone regeneration in primates in response to basic fibroblast growth factor. J. Neurosurg. 91, 851, 1995.
42. Coffin, J.D., Florkiewicz, R.Z., Neumann, J., Mort-Hopkins, T., Dorn, G.W. 2nd, Lightfoot, P., German, R., Howles, P.N., Kier, A., O'Toole, B.A., et al. Abnormal bone growth and selective translational regulation in basic fibroblast growth factor (FGF-2) transgenic mice. Mol. Biol. Cell. 6, 1861, 1995.
43. Ohbayashi, N., Shibayama, M., Kurotaki, Y., Imanishi, M., Fujimori, T., Itoh, N., and Takada, S. FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev., 16, 870, 2002.
44. Liu, Z., Xu, J., Colvin, J.S., and Ornitz, D.M. Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev., 16, 859, 2002.
45. Raucci, A., Laplantine, E., Mansukani, A., Basilico, C. Activation of the ERK1/2 and p18 mitogen-activated protein kinase pathways mediates fibroblast growth factor-induced growth arrest of chondrocytes. J. Biol. Chem. 279, 1747, 2004.