Disruption of the Fgf2 gene activates the adipogenic and suppresses the osteogenic program in mesenchymal marrow stromal stem cells

Bone

Volumn 47, Issue 2, 2010, Pages 360-370

  Xiao, Liping ^a   Sobue, Takanori ^a   Esliger, Alycia ^a   Kronenberg, Mark S ^a   Coffin, J Douglas ^b   Doetschman, Thomas ^c   Hurley, Marja M ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF MONTANA   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Adipogenesis; Aging; Fgf2 null mice; Osteoporosis

Indexed keywords

ADIPONECTIN; ALKALINE PHOSPHATASE; BETA ACTIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; FIBROBLAST GROWTH FACTOR 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2;

ADIPOCYTE; ADIPOGENESIS; AGE DISTRIBUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE DEVELOPMENT; BONE MARROW CELL; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; FEMALE; GENE DISRUPTION; GENOTYPE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOLYSIS; SIGNAL TRANSDUCTION; STROMA CELL; AGING; ANIMAL; CELL COUNT; CELL CULTURE; CELL PROLIFERATION; CFU COUNTING; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; MESENCHYMAL STROMA CELL; METABOLISM; PHOTON ABSORPTIOMETRY;

ABSORPTIOMETRY, PHOTON; ADIPOCYTES; ADIPOGENESIS; AGING; ANIMALS; BONE DENSITY; BONE MARROW CELLS; CELL COUNT; CELL PROLIFERATION; CELLS, CULTURED; COLONY-FORMING UNITS ASSAY; FEMALE; FIBROBLAST GROWTH FACTOR 2; GENE DELETION; GENE EXPRESSION REGULATION; MESENCHYMAL STEM CELLS; MICE; MICE, KNOCKOUT; OSTEOGENESIS; STROMAL CELLS; MESENCHYMAL STROMAL CELLS;

EID: 77955981309     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2010.05.021     Document Type: Article

References (42)

1. Moerman E.J., Teng K., Lipschitz D.A., Lecka-Czernik B. Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: the role of PPAR-2 transcription factor and TGF--/BMP signaling pathways. Aging Cell 2004, 3:379-389.
2. Gimble J.M., Zvonic S., Floyd Z.E., Kassem L., Nuttall M.E. Playing with bone and fat. J. Cell. Biochem. 2006, 98:251-266.
3. Kirkland J.L., Tchkonia T., Pirtskhalava T., Han J., Karagiannides I. Adipogenesis and aging: does aging make fat go MAD?. Exp. Gerontol. 2002, 37:757-767.
4. Moore S.G., Dawson K.L. Red and yellow marrow in the femur: age-related changes in appearance at MR imaging. Radiology 1990, 175:219-223.
5. Feve B. Adipogenesis: cellular and molecular aspects. Best Pract. Res. Clin. Endocrinol. Metab. 2005, 19(4):483-499.
6. Rosen E.D., MacDougald O.A. Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 2006, 7:885-896.
7. Rickard D.J., Wang F.-L., Rodriguez-Rojas A.-M., et al. Intermittent treatment with parathyroid hormone (PTH) as well as a non-peptide small molecule agonist of the TPH1 receptor inhibits adipocyte differentiation in human bone marrow stromal cells. Bone 2006, 39(6):1361-1372.
8. Abe E., Yamamoto M., Taguchi Y., et al. Essential requirement of BMPSs-2/4 for both osteoblast and osteoclast formation in murine bone marrow cultures from adult mice: antagonism by noggin. J. Bone Miner. Res. 2000, 15:663-673.
9. Sottile V., Seuwen K. Bone morphongenetic protein-2 stimulates adipogenic differentiation of mesenchymal precursor cells in synergy with BRL 49653 (rosiglitazone). FEBS Lett. 2000, 475:201-204.
10. Hurley M.M., Marie P., Florkiewicz R.Z. Fibroblast growth factor and fibroblast growth factor Receptor families. Principles of Bone Biology 2003, 627-645. Academic Press, San Diego. J.P. Bilezikian, L.G. Raisz, G. Rodan (Eds.).
11. Rodan S.B., Wesolowski G., Yoon K., Rodan G.A. Opposing effects of fibroblast growth factor and pertussis toxin on alkaline phosphatase, osteopontin, osteocalcin and type I collagen mRNA levels in ROS 17/2.8 Cells. J. Biol. Chem. 1989, 264:19934-19941.
12. McCarthy T.L., Centrella M., Canalis E. Effects of fibroblast growth factors on deoxyribonucleic acid and collagen synthesis in rat parietal bone cells. Endocrinology 1989, 125:2118-2126.
13. Canalis E., Centrella M., McCarthy T. Effects of basic fibroblast growth factor on bone formation in vitro. J. Clin. Invest. 1988, 81:1572-1577.
14. Hurley M.M., Abreu C., Harrison J.R., Lichtler A., Raisz L.G., Kream B.E. Basic fibroblast growth factor inhibits type I collagen gene expression in osteoblastic MC3T3-E1 cells. J. Biol. Chem. 1993, 268:5588-5593.
15. Mayahara H., Ito T., Nagai H., et al. In vivo stimulation of endosteal bone formation by basic fibroblast growth factor in rats. Growth Factors 1993, 9:73-80.
16. Noff D., Pitaru S., Savion N. Basic fibroblast growth factor enhances the capacity of bone marrow cells to form bone-like nodules In Vitro. FEBS Lett. 1989, 250(2):619-621.
17. Pitaru S., Kotev-Emeth S., Noff D., Kaffuler S., Savion N. Effect of basic fibroblast growth factor on the growth and differentiation of adult stromal bone marrow cells: enhanced development of mineralized bone-like tissue in culture. J. Bone Miner. Res. 1993, 8:919-926.
18. Rifas L., McDermott MJ Zhang S.F., Olivier C., Avioli LV Cheng S.L. Basic fibroblast growth factor inhibits growth and differentiation of human bone marrow osteoprogenitor cells. J. Bone Miner. Res. 1995, 10(1):S411.
19. Wergedal J.E., Mohan S., Lundy M., Baylink D.J. Skeletal growth factor and other growth factors known to be present in bone matrix stimulate proliferation and protein synthesis in human bone cells. J. Bone Miner. Res. 1990, 5:179-185.
20. Pri-Chen S., Pitaru S., Lokiec F., Savion N. Basic fibroblast growth factor enhances the growth and expression of the osteogenic phenotype of dexamethasone-treated human bone marrow-derived bone-like cells in culture. Bone 1998, 23(2):111-117.
21. Berrada S., Lefebvre F., Harmand M.F. The effect of recombinant human basic fibroblast growth factor RHFGF-2 on human osteoblasts in growth and phenotype expression. In Vitro Cell. Dev. Biol. Anim. 1995, 31:698-702.
22. Martin I., Muraglia A., Campanile G., Cancedda R., Quarto R. Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. Endocrinology 1997, 138(10):4456-4462.
23. Zhou M., Sutliff R.L., Paul R.J., et al. Fibroblast growth factor 2 control of vascular tone. Nat. Med. 1998, 4:201-207.
24. Montero A., Okada Y., Tomita M., et al. Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J. Clin. Invest. 2000, 105:1085-1093.
25. Hurley M.M., Lee S.K., Raisz L.G., Bernicker P., Lorenzo J.A. Basic fibroblast growth factor induces osteoclast formation in murine bone marrow cultures. Bone 1998, 22:309-316.
26. Kawaguchi H., Pilbeam C.C., Gronowicz G., et al. Transcription induction of prostaglandin G/H synthase-2 by basic fibroblast growth factor. J. Clin. Invest. 1995, 96:923-930.
27. Okada Y., Montero A., Zhang X., et al. Impaired osteoclast formation in bone marrow cultures in Fgf2 null mice in response to parathyroid hormone. J. Biol. Chem. 2006, 278(23):21258-21266.
28. Jilka R.L., Weinstein R.S., Takahashi K., Parfitt A.M., Manolagas S.C. Linkage of decreased bone mass with impaired osteoblastogenesis in a murine model of accelerated senescence. J. Clin. Invest. 1996, 97:1732-1740.
29. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29(9):e45.
30. Newell F.S., Su H., Tornqvist H., Whitehead J.P., Prins J.B.B., Hutley L.J. Characterization of the transcriptional and functional effects of fibroblast growth factor-1 on human preadipocyte differentiation. FASEB J. 2006, 20:E2133-E2145.
31. Neubauer M., Fischbach C., Bauer-Kreisel P., et al. Basic fibroblast growth factor enhances PPARγ ligand-induced adipogenesis of mesenchymal stem cells. FEBS Lett. 2004, 577:277-283.
32. Locklin R.M., Oreffo R.O.C., Triffitt J.T. Effects of TGFβ on bFGF on the differentiation of human bone marrow stromal fibroblasts. Cell Biol. Int. 1999, 23(3):185-194.
33. Kawaguchi N., Toriyama K., Nicodemou-Lena E., Inou K., Torii S., Kitagawa Y. De novo adipogenesis in mice at the site of injection of basement membrane and basic fibroblast growth factor. Cell Biol 1998, 95:1062-1066.
34. Chapman A.B., Knight D.M., Dieckmann B.S., Ringold G.M. Analysis of gene expression during differentiation of adipogenic cells in culture and hormonal control of the developmental program. J. Biol. Chem. 1984, 259(24):15548-15555.
35. Navre M., Ringold G.M. Differential effects of fibroblast growth factor and tumor promoters on the initiation and maintenance of adipocyte differentiation. J. Cell Biol. 1989, 109:1857-1863.
36. Prusty D., Park B.-H., Davis K.E., Farmer S.R. Activation of MEK/ERK signaling promotes adipogenesis by enhancing peroxisome proliferator-activated receptor γ (PPARγ) and C/EBPα gene expression during the differentiation of 3T3-L1 preadipocytes. J. Biol. Chem. 2002, 277(48):46226-46232.
37. Xiao Z., Awad H.A., Liu S., et al. Selective Runx2 deficiency leads to low turnover osteopenia in adult mice. Dev. Biol. 2005, 283:345-356.
38. Naganawa T., Xiao L., Abogunde E., et al. In vivo and in vitro comparison of the effects of FGF-2 null and haplo-insufficiency on bone formation in mice. Biochem. Biophys. Res. Commun. 2006, 339(2):490-498.
39. Rosen E.D., Walkey C.J., Puigserver P., Spiegelman B.M. Transcriptional regulation of adipogenesis. Genes Dev. 2000, 14:1293-1307.
40. Lecka-Czernik B., Gubrij I., Moerman E.J., et al. Inhibition of Osf2/Cbfa1 expression and terminal osteoblast differentiation by PPARγ2. J. Cell. Biochem. 1999, 74:357-371.
41. Akune T., Ohba S., Kamekura S., et al. PPARγ insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J. Clin. Invest. 2004, 113(6):846-855.
42. Ogawa S., Urano T., Hosoi T., et al. Association of BMD with a polymorphism of the peroxisome proliferator-activated receptor gamma gene: PPARgamma expression in osteoblasts. Biochem. Biophys. Res. Commun. 1999, 260:122-126.