Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation

Journal of Clinical Investigation

Volumn 105, Issue 8, 2000, Pages 1085-1093

  Montero, Aldemar ^a   Okada, Yosuke ^a   Tomita, Masaro ^a   Ito, Masako ^b   Tsurukami, Hiroshi ^c   Nakamura, Toshitaka ^c   Doetschman, Thomas ^d   Coffin, J Douglas ^e   Hurley, Marja M ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b NAGASAKI UNIVERSITY   (Japan)

^c UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF MONTANA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; BONE MASS; BONE MINERALIZATION; CELL CULTURE; GENE EXPRESSION REGULATION; MORPHOMETRICS; MOUSE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL;

EID: 0034007273     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI8641     Document Type: Article

References (83)

1. Gospodarowicz, D. 1990. Basic science and pathology fibroblast growth factor chemical structure and biologic function. Clin. Orthop. Rel. Res. 257:231-248.
2. Hurley, M.M., and Florkiewicz, R. 1996. Fibroblast growth factor and vascular endothelial fibroblast growth factor families. In Principles of bone biology. Bilezikian, J.P., Raisz, L.G., and Rodan, G.A., editors. Academic Press. San Diego, CA. 627-645.
3. Hauschka, P.V., Mavrakos, A.E., Iafrati, M.D., Doleman, S.E., and Klagsbrun, M. 1986. Growth factors in bone matrix. J. Biol. Chem. 261:12665-12674.
4. Shing, Y., et al. 1984. Heparin affinity: duplication of a tumour derived capillary endothelial cell growth facror. Science. 223:1926-1928.
5. Hurley, M.M., Kessler, M., Gronowicz, G., and Raisz, L.G. 1992. The interaction of heparin and basic fibroblast growth factor on collagen synthesis in 21-day fetal rat calvanae. Endocrinology. 130:2675-2681.
6. Saksela, O., and Rifkin, D. 1990. Release of basic fibroblast growth factor-heparan sulfate complexes from endothelial cells by plasminogen activator-mediated proteolytic activity. J. Cell Biol. 110:767-775.
7. Globus, R.K., Plouet, J., and Gospodarowicz, D. 1989. Cultured bovine bone cells synthesize basic fibroblast growth factor and store it in their extracellular matrix. Endocrinology. 124:1539-1547.
8. Hurley, M.M., et al. 1995. Transcriptional regulation of the collagenase gene by basic fibroblast growth factor in osteoblastic MC3T3-E1 cells. Biochem. Biophys. Res. Commun. 214:331-339.
9. Okazaki, R., et al. 1992. Transcriptional activation of the c-fos and c-jun proto-oncogenes by serum growrh factors in osteoblast-like MC3T3-E1 cells. J. Bone. Miner. Res. 7:1149-1155.
10. Hurley, M.M., Marcello, K., Abreu, C., and Kessler, M. 1996. Signal transduction by basic fibroblast growth factor in rat osteoblastic Py1a cells. J. Bone Miner. Res. 11:1256-1263.
11. Coffin, J.D., et al. 1995. Abnormal bone growth and selective translational regulation in basic fibroblast growth facror (FGF-2) transgenic mice. Mol. Biol. Cell. 6:1861-1873.
12. Partanen, J., et al. 1991. FGFR4, a novel acidic fibroblast growth factor receptor with a distinct expression pattern. EMBO J. 10:1347-1354.
13. Orr-Urtreger, A., Givol, D., Yayon, A., Yarden, Y., and Lonai, P. 1991. Developmental expression or two murine fibroblast growth factor receptors, FLG and BEK. Development, 113:1419-1439.
14. Russeau, F., et al. 1994. Mutations in the gene encoding fibroblast growth receptor 3 in achondroplasia. Nature. 371:252-254.
15. Shiang, R., et al. 1994. Mutations in the transmembrane domain of FGFR3 cause the most common generic form of dwarfism, achondroplasia. Cell. 78:335-342.
16. Deng, C., Wynshaw-Boris, A., Zhou, F., Kuo, A., and Leder, P. 1996. Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell. 84:911-921.
17. Colvin, J.S., Bohne, B.A., Harding, G.W., McEwen D.G., and Ornitz, D.M. 1996. Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat. Genet. 12:390-397.
18. Lomri, A., et al. 1998. Increased calvaria cell differentiation and bone matrix formation induced by fibroblast growth receptor 2 mutations in Apert syndrome. J. Clin. Invest. 101:1310-1317.
19. Xu, X., Weinsrein M., Li, C., and Deng, C.X. 1999. Fibroblast growth factor receptors (FGFRs) and their role in limb development. Cell Tissue Res. 296:33-43.
20. Globus, R.K., Patterson-Buckendahl, F., and Gospodarowicz, D. 1988. Regulation of bovine bone fell proliferation by fibroblast growth factor and transforming growth factor β. Endocrinology. 123:98-105.
21. Rodan, S.B., Wesolowski, G., Yoon, K., and Rodan, G.A. 1989. Opposing effects of fibroblast growth facror and pertussis toxin on alkaline phosphatase, osteopontin, osteocalcin and type 1 collagen mRNA levels in ROS 17/2.8 Cells. J. Biol. Chem. 264:19934-19941.
22. McCarthy, T.L., Centrella, M., and Canalis, E. 1989. Effects of fibroblast growth factors on deoxyribonucleic acid and collagen synthesis in rat parietal hone cells. Endocrinology. 125:2118-2126.
23. Canalis, E., Centrella, M., and McCarthy, T. 1988. Effects of basic fibroblast growth factor on bone formation in vitro. J. Clin. Invest. 81:1572-1577.
24. Hurley, M.M., et al. 1993. Basic fibroblast growth factor inhibits type I collagen gene expression in osteoblastic MC3T3-E1 cells. J. Biol. Chem. 268:5588-5593.
25. Mayahara, H., et al. 1993. In vivo stimulation of endosteal bone formation by basic fibroblast growth factor in rats, Growth Factors. 9:73-80.
26. Nakamura, T., et al. 1995. Stimulation of endosteal bone formation by systemic injections of recombinant basic fihroblast growth factor in rats. Endocrinology. 136:1276-1284.
27. Nagai. H., Tsukuda, R., and Mayahara, H. 1995. Effects of basic fibroblast growth facror (bFGF) on hone formation in growing rats. Bone. 16:367-373.
28. Nakamura, K., et al. 3998. Stimulation of bone formation by intraosseous injection of basic fibroblast growth factor in ovariectomized rats. Int. Orthop. 22:49-54.
29. Dunstan, C.R., et al. 1999. Systemic administration of acidic fibroblast growth factor (FGF-1) prevents bone loss and increases new bone formation in ovariectomized rats. J. Bone Miner. Res. 14:953-959.
30. Liang, H., Pun, S., and Wronski, T.J. 1999. Bone anabolic effects of basic fibroblast growth factor in ovariectomized rats. Endocrinology. 140:5780-5788.
31. Brunner, G., Gabrilove, J., Rifkin, D.B., and Wilson, E.L. 1991. Phospholipase C release of basic fibroblast growth factor from human bone marrow cultures as a biologically active complex with a phosphatidylinosirol anchored heparan sulfate proteoglycan. J. Cell Biol. 114:1275-1283.
32. Oliver, L.J., Rifkin, D.B., Gabrilove, J., Hannocks, M.J., and Wilson, E.L. 1990. Long-term culture of human bone marrow stromal cells in the presence of basic fibroblast growth factor. Growth Factors. 3:231-236.
33. Thomson, B.M., et al. 1993. Preliminary characterization of porcine bone marrow stromal cells: skeletogenic potential, colony-forming activity, and response to dexamethasone, transforming growth factor β, and basic fibroblast factor. J. Bone Miner. Res. 10:1173-1183.
34. Locklin, R.M., Williamson, M.C., Beresford, J.N., Triffitt, J.T., and Owen, M.H. 1995. In vitro effects of growth factors and dexamethasone on rat marrow stromal cells. Clin. Orthpp. Rel. Res. 313:27-35.
35. Long, M.W., Robinson, J.A., Ashcraft, E.A., and Mann, K.G. 1995. Regulation of human bone marrow-derived osteoprogenitor cells by osteogenic growth factors. J. Clin. Invest. 95:881-887.
36. Kawaguchi, H., et al. 1994. Stimulation of fracture repair by recombinant human basic fibroblast growth factor in normal and streptozotocin-diabetic rats. Endocrinology, 135:774-781.
37. Wildburger, R., et al. 1994. Basic fibroblast growth factor (bFGF) immunoreactivity as a possible link between head injury and impaired bone fracture healing. J. Bone Miner. Res. 27:183-193.
38. Scully, S.P., Joyce, M.E., Abidi, N., and Bolander, M.E. 1990. The use of polymerase chain reaction generated nucleotide sequences as probes for hybridization. Mol. Cell Probes, 4:485-495.
39. Hurley, M.M., Lee, S.K., Raisz, L.G., Bernicker, P., and Lorenzo, J.A. 1998. Basic fibroblast growth factor induces osteoclast formation in murine hone marrow cultures. Bone. 22:309-316.
40. Kawaguchi, H., et al. 1995. Transcription induction of prostaglandin G/H synthase-2 by basic fibroblast growth factor. J. Clin. Invest. 96:923-930.
41. Hurley, M.M., Abreu, C., Gronowicz, G., Kawaguchi, H., and Lorenzo, J. 1994. Expression and regulation of basic fibroblast growth factor mRNA levels in mouse osteoblastic MC3T3-E1 cells. J. Biol. Chem. 269:9392-9396.
42. Sabbieti, M.G., et al. 1999. Prostaglandins regulate the expression of fibroblast growth factor-2 in bone. Endocrinology. 140:434-444.
43. Hurley, M.M., et al. 1999. Parathyroid hormone regulates the expression of fibroblast growth factor-2 mRNA and fibroblasr growth factor receptor mRNA in osteoblastic cells. J. Bone Miner. Res. 14:776-783.
44. Cohen, M.M. 1997. Transforming growth factor Bs and fibroblast growth factors and their receptors: role in sutural biology and craniosynostosis. J. Bone Miner. Ref. 12:322-331.
45. Ornirz, D.M., et al. 1996. Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271:15292-15297.
46. Buckland, R.A., Collinson, J.M., Graham, E., Davison, D.R., and Hill, R.E. 1998. Antagonistic effects of FGF-4 on BMP induction of apoptosis and chondrogenesis in the chick limb bud. Mech. Dev. 71:143-150.
47. Kim, H.J., Rice, D.P., Kettunen, P.J., and Thesleff, I. 1998. FGF-, BMP- and Shh-mediated signaling pathways in the regulation of cranial suture morphogenesis and calvanal hone development. Development, 125:1241-1251.
48. Xu, J., Lawshe, A., MacArthur, C.A., and Ornitz, D.M 1999. Genomic structure, mapping, activity and expression of fibroblast growth factor 17. Mech. Dev. 83:165-178.
49. Sckine, K., et al. 1999. FGF-10 is essential for limb and lung formation. Nat. Genet. 21:138-141.
50. Hartung, H., et al. 1997. Murine FGF-12 and FGF-13: expression in embryonic nervous system, connective tissue and heart. Mech. Dev. 64:31-39.
51. Zhou, M., et al. 1998. Fibroblast growth factor 2 control of vascular tone. Nat. Med. 4:201-207.
52. Hattersley, G. and Chambers, T.J. 1990. Effects of interleukin 3 and of granulocyte-macrophage and macrophage colony stimulating factors on osteoclast differentiation from mouse hematopoietic tissue. J. Cell Physiol. 142:201-209
53. Onega, S., Ittmann, M., Tsang, S.H., Erlich, M., and Bailico, C. 1998. Neuronal detects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc. Natl. Acad. Sci. USA. 97:5672-5677.
54. Dono, R., Texido, G., Dussel, R., Ehmke, H., and Zeller, R. 1998. Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice. EMBO J. 17:4213-4225.
55. 2 on bone: Induction of a transition from nonadherent to adherent osteoblast precursors. J. Bone. Miner. Res. 10:474-487.
56. Chomczynski, P., and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidimum rhiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
57. Towbin, H., Staehelin, T., and Gordon, J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci., USA. 76:4350-4554.
58. Hebert, J.M., Basilico, C., Goldfarb, M., Haub, O., ami Martin, G.R. 1990. Isolation of cDNAs encoding four mouse FGF family members and characterization of their expression patterns during embryogenesis. Dev. Biol. 138:454-463.
59. Narusawa, K., et al. 1995. The effect of recombinant human insulin-like growth factor (rhIGF)-1 and rhIGF-1/IGF binding prorein-3 administration on rat osteopenia induced by ovariectomy with concomitant bilateral sciatic neurectomy. J. Bone. Miner. Res. 10:1853-1864.
60. Murakami, H., Nakamura, T., Tsurukami, H., Abe, M., Barbier, A., and Suzuki, K. 1994. Effects of tiludronate on bone mass, structure, and turnover ar the epiphyseal, primary, and secondary spongiosa in the proximal tibia of growing rats after sciatic neurectomy. J. Bone Miner. Res. 9:1355-1364.
61. Parfitt, A.M., et al. 1983. Relationships between surface, volume, and thickness of iliac trabecular bone m aging and osteoporosis. Implications for rhe microanatomic and cellular mechanisms of bone loss. J. Clin. Invest. 72:1396-1409.
62. Goulet, R.W., et al. 1994. The relationship between the structural and orthogonal compressive properties of trabecular bone. J. Biomech. 27:375-389.
63. Ruegsegger, P. and Muller, R. 1996. A microtomographic system for rhe nondestructive evaluation of hone architecture. Calcif. Tissue Int. 58:61-75.
64. Gonzalez, A.-M., Buscaglia, M. Ong, M., and Baird A. 1990. Distribution of basic fibroblast growth factor in the 18-day rat fetus: localization in the basement membranes of diverse tissues. J. Cell Biol. 110:753-765.
65. Gonzalez, A.M., Hill, D.J., Logan, A., Maher, P.A., and Baird, A. 1996. Distribution of fibroblast growth factor (FGF)-2 and FGF receptor-1 messenger RNA expression and protein presence in the mid-trimester human fetus. Pediatr. Res. 39:375-385.
66. Bikfalvi, A., Klein, S., Pintucci, G., and Rifkin, D.B. 1997. Biological roles of fibroblast growth facror-2. Endocrine Rev. 18:26-45.
67. Pavis, M.G., et al. 1997. Intracrine and autocrine effects of basic fibroblast growth factor in vascular smooth muscle cells. J. Mol. Cell Cardiol. 29:1061-1072.
68. Owen, M. 1985. Lineage of osteogenic cells and their relationship to the stromal system. W.A. Peck, editor. Bone and mineral research. 3:1-25.
69. Friedenstein, A.J. 1990. Osteogenic stem cells in the hone marrow. J. Bone Miner. Res. 7:243-272.
70. Stein, G.S., and Lian, J.B. 1993. Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype. Endocr. Rev. 14:424-442.
71. Avibin, J.K., Liu, E., Malaval, L., and Gupta, A.K, 1995. Osteoblast and chondroblast differentiation. Bone. 17:77S-83S.
72. Lennon, D.P., Haynesworth, S.E., Young, R.G., Dennis, J.E., and Caplan, A I. 1995. A chemically defined medium supports in vitro proliferation and maintains the osteochondral potential of rat marrow-derived mesenchymal stem cells. J. Exp. Cell Res. 219:211-222.
73. Noff, D., Pitaru, S., and Savion, N. 1989. Basic fibroblast growth factor enhances the capacity of bone marrow cells to form bone-like nodules In Vitro. FEBS Lett. 250:619-621.
74. Picaru, S., Kotev-Emeth, S., Noff, D., Kaffuler, S., and Savion, N. 1993. 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. 8:919-926.
75. Wergedal, J.E., Mohan, S., Lundy, M., and Haylink, D.J. 1990. 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. 5:179-185.
76. Pri-Chen, S., Pitaru, S., Lokiec, F., and Savion, N. 1998. 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 23:111-117.
77. Berrada, S., Lefebvre, F., and Harmand, M-F. 1995. The effect of recombinant human basic fibroblast growth factor RHFGF-2 on human osteoblasts in growth and phenotype expression. In Vitro Cell Dev. Biol-Annu. 31:698-702.
78. Martin, I., Muraglia, A., Campanile, G., Cancedda, R., and Quarto, R. 1997. Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogemc precursors from human bone marrow. Endocrinology 138:4456-4462.
79. Scutt, A., and Bertram, P. 1999. Basic fibroblast growth factor in the presence of dexamethasone stimulates colony formation, expansion, and osteoblastic differentiation by rat bone marrow stromal cells. Calcif. Tissue Int. 64:69-77.
80. Hanada, K., Dennis, J.E., and Caplan, A.I. 1997. Stimulatory effects of basic fibroblast growth factor and bone morphogenetic protein-2 on osteogenic differentiation of rat bone marrow-derived mesenchymal stem cells J. Bone Miner. Res. 12:1606-1614.
81. Triffitt, J.T. 1996. Fibroblast growth factor and vascular endothelial fibroblast growth factor families. In Principles of bone biology. Bilezikian, J.P., Raisz, L.G., and Rodan, G.A., editors Academic Press. San Diego, CA. 627-645.
82. Kajkenova, O., et al. 1997. Increased adipogenesis and myelopoiesis in the bone marrow of SAMP6, a murine model of defective osteoblastogenesis and low turnover osteopema. J. Bone Miner Res. 12:1772-1779.
83. Allouche, M. 1995. Basic fibroblast growth factor and hematopoeisis. Leukemia, 9:937-942.