Signaling by fibroblast growth factors (FGF) and fibroblast growth factor receptor 2 (FGFR2)-activating mutations blocks mineralization and induces apoptosis in osteoblasts

Journal of Cell Biology

Volumn 149, Issue 6, 2000, Pages 1297-1308

  Mansukhani, Alka ^a   Bellosta, Paola ^a   Sahni, Malika ^a   Basilico, Claudio ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Craniosynostosis; Fibroblast growth factor receptors; Fibroblast growth factors; Osteoblast

Indexed keywords

ALKALINE PHOSPHATASE; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE;

ACROCEPHALOSYNDACTYLY; ANIMAL CELL; APOPTOSIS; ARTICLE; BONE DEVELOPMENT; BONE GROWTH; CALVARIA; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROGENESIS; CONTROLLED STUDY; CRANIOFACIAL SYNOSTOSIS; CROUZON SYNDROME; ENZYME ACTIVATION; GENE MUTATION; MINERALIZATION; MOUSE; NEWBORN; NONHUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKULL SUTURE; TRANSGENIC MOUSE;

ACROCEPHALOSYNDACTYLIA; ALKALINE PHOSPHATASE; ANIMALS; APOPTOSIS; BROMODEOXYURIDINE; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CRANIOFACIAL DYSOSTOSIS; DNA FRAGMENTATION; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; HISTOCYTOCHEMISTRY; MICE; MICE, TRANSGENIC; OSTEOBLASTS; POINT MUTATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSFECTION;

ANIMALIA; MURINAE; MUS MUSCULUS;

EID: 0034640848     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.6.1297     Document Type: Article

References (43)

1. Anderson, J., H.D. Burns, P. Enriquez-Harris, A.O.M. Wilke, and J.K Heath. 1998. Apert syndrome mutations in fibroblasl growth factor receptor 2 exhibit increased affinity for FGF ligand. Human Mol. Genet. 7:1475-1483.
2. Arman, E., R. Haffner-Krausz, Y. Chen, J.K. Heath, and P. Lonai. 1998. Targeted disruption of fibroblast growth factor (FGK) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc. Natl. Acad. Sci. USA. 95:5082-5087.
3. Bellosta, P., Q. Zhang, S.P. Goff, and C. Basilico. 1997. Signaling through the ARK tyrosine kinase receptor protects from apoptosis in the absence of growth stimulation. Oncogene. 15:2387-2397.
4. Burke, D., D. Wilkes, T.L. Blundell, and S. Malcolm. 1998. Fibroblast growth factor receptors: lessons from the genes. Trends Biochem. Sci. 23:259-262.
5. Coffin, J.D., R.Z. Florkiewicz, J. Neumann, T. Mort-Hopkins, G.W. Dorn H, P. Lightfoot, R. German, P.N. Howles, A. Kier, B.A. O'Toole, et al. 1995. Abnormal bone growth and selective translational regulation in basic fibroblast growth factor (FGF-2) transgenic mice. Mol. Biol. Cell. 6:1861-1873.
6. Debiais, F., M. Hott, A.M. Graulet, and P.J. Marie. 1998. The effects of fibroblast growth factor-2 on human neonatal calvaria osteoblastic cells are differentiation stage specific. J. Bone Miner. Res. 13:645-654.
7. Deng, C.-X., A. Wynshaw-Boris, M.M. Shen, C. Daugherty, D.M. Ornitz, and P. Leder. 1994. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 8:3045-3057.
8. Deng, C., A. Wynshaw-Boris, F. Zhou, A. Kuo, and P. Leder. 1996. Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell. 84:911-921.
9. Evan, G.I., A.H. Wyllie, C.S. Gilbert, T.D. Littlewood, H. Land, M. Brooks, C.M. Waters, L.Z. Penn, and D.C. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell. 69:119-128.
10. Fragale, A., M. Tartaglia, S. Bernardini, A.M.M. Di Stasi, C. Di Rocco, F. Velardi, A. Teti, P.A. Battaglia, and S. Migliaccio. 1999. Decreased proliferation and altered differentiation in osteoblasts from genetically and clinically distinct craniosynostotic disorders. Am. J. Pathol. 154:1465-1477.
11. Galvin, B.D., K.C. Hart, A.N. Meyer, M.K. Webster, and D.J. Donoghue. 1996. Constitutive receptor activation by Crouzon syndrome mutations in fibroblast growth factor receptor (FGFR)2 and KGFR2/Neu chimeras. Proc. Natl. Anal. Sci. USA. 93:7894-7899.
12. Goldfarb, M. 1996. Functions of fibroblast growth factors in vertebrate development. Cytokine Growth Factor Rev. 7:311-325.
13. Hill, P.A., A. Tumber, and M.C. Meikle. 1997. Multiple extracellular signals promote osteoblast survival and apoptosis. Endocrinology. 138:3849-3858.
14. Hurley, M.M., and R.Z. Florkiewicz. 1996. Fibroblast growth factor and vascular endothelial cell growth factor families. In Principles of Bone Biology. J.P. Bilezikian, L.G. Raisz, and G.A. Rodan. editors. Academic Press. New York, 69-86.
15. Iseki, S., A.O.M. Wilkie, J.K. Heath, T. Ishimaru, K. Eto, and G.M. Morriss-Kay. 1997. Fgfr2 and osteopontin domains in the developing skull vault are mutually exclusive and can be altered by locally applied FGF2. Development. 124:3375-3384.
16. Iseki, S., A.O.M. Wilkie, and G.M. Morriss-Kay. 1999. Fgfr1 and Fgfr2 have distinct differentiation- and proliferation-related roles in the developing mouse skull vault. Development. 126:5611-5620.
17. Jilka, R.L., R.S. Weinstein, T. Bellido, A.M. Parfitt, and S.C. Manolagas. 1998. Osteoblast programmed cell death (apoptosis): modulation by growth factors and cytokines. J. Bone Miner. Res. 13:793-802.
18. Jilka, R.L., R.S. Weinsein, T. Bellido, P. Roberson, A.M. Parfitt, and S.C. Manolagas. 1999. Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J. Clin. Invest. 104:439-446.
19. Kennedy, S.G., A.J. Wagner, S.D. Conzen, J. Jordan, A. Bellacosa, P.N. Tsichlis, and N. Hay. 1997. The Pl 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 11:701-713.
20. Kim, H.-J., D.P.C. Rice, P.J. Kettunen, and I. Thesleff. 1998. FGF-, BMP- and Shh-mediated signalling pathways in the regulation of cranial suture morphogenesis and calvarial bone development. Development. 125:1241-1251.
21. Kouhara, H., Y.R. Hadari, T. Spivak-Kroizman, J. Schilling, D. Bar-Sagi, I. Lax, and J. Schlessinger. 1997. A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell. 89: 693-702.
22. Li, Y., C. Basilico, and A. Mansukhani. 1994. Cell transformation by fibroblast growth factors can be suppressed by truncated fibroblast growth factor receptors. Mol. Cell. Biol. 14:7660-7669.
23. Lomri, A., J. Lemonnier, M. Hott, N. de Parseval, E. Lajeunie, A. Munnich, D. Renier, and P.J. Marie. 1998. Increased calvaria cell differentiation and bone matrix formation induced by fibroblast growth factor receptor 2 mutations in Apert syndrome. J. Clin. Invest. 101:1310-1317.
24. Mangasarian, K., Y. Li, A. Mansukhani, and C. Basilico. 1997. Mutation associated with Crouzon syndrome causes ligand-independent dimerization and activation of FGF receptor-2. J. Cell. Physiol. 172:117-125.
25. Mansukhani, A., P. Dell'Era, D. Moscatelli, S. Kornbluth, H. Hanafusa, and C. Basilico. 1992. Charactezation of the murine BEK fibroblast growth factor (FGF) receptor: activation by three members of the FGF family and requirement for heparin. Proc. Natl. Acad. Sci. USA. 89:3305-3309.
26. Miho, Y., Y. Kouroku, E. Fujita, T. Mukasa, K. Urase, T. Kasahara, A. Isoai, M. Y. Momoi, and T. Momoi. 1999. bFGF inhibits the activation of caspase-3 and apoptosis of P19 embryonal carcinoma cells during neuronal differentiation. Cell Death Differ. 6:463-470.
27. Muenke, M., and U. Schell. 1995. Fibroblast-growth-factor receptor mutations in human skeletal disorders. Trends Genet. 11:308-313.
28. Muller, A.J., J.C. Young, A.M. Pendergast, M. Pondel, N.R. Landau, D.R. Littman, and O.N. Witte, 1991. BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol. Cell. Biol. 11:1785-1792.
29. Mundy, G., R. Garrett, S. Harris, J. Chan, D. Chen, G. Rossini, B. Boyce, M. Zhao, and G. Gutierrez. 1999. Stimulation of bone formation in vitro and in rodents by statins. Science. 286:1946-1949.
30. Naski, M.C., and D.M. Ornitz. 1998. FGF signaling in skeletal development. Front. Biosci. 3:781-794.
31. Ornitz, D.M., J. Xu, J.S. Colvin, D.G. McEwen, C.A. MacArthur, F. Coulier, G. Gao, and M. Goldfarb. 1996. Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271:15292-15297.
32. Pitaru, S., S. Kotev-Emeth, D. Noff, S. Kaffuler, and N. Savion. 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. 8:919-929.
33. Rice, D., H. Kim, and I. Thesleff. 1999. Apoptosis in murine calvarial bone and suture development. Eur. J. Oral Sci. 107:265-275.
34. Rice, D.P.C., T. Aberg, Y.S. Chan, Z. Tang, P.J. Kettunen, L. Pakarinen, R.E. Maxson, and I. Thesleff. 2000. Integration of FGF and TWIST in calvarial bone and suture development. Development. 127:1845-1855.
35. Robertson, S.C., A.N. Meyer, K.C . Hurt, B.D. Galvin, M.K. Webster, and D.J. Donoghue. 1998. Activating mutations in he extracellular domain of the fibroblast growth factor receptor 2 function by disruption of the disulfide bond in the third immunoglobulin-like domain. Proc. Natl. Acad. Sci. USA. 45:4567-4572.
36. Sahni, M., D.-C. Ambrosetti, A. Mansukhani, R. Gertner, D. Levy, and C. Basilico. 1999. FGF signaling inhibits chondrocyte proliferation and regulates bone development through the STAT-1 pathway. Genes Dev. 13:1261-1366.
37. Saxton, T.M., M. Henkemeyer, S. Gasca, R. Shen, D.J. Rossi, F. Shalaby, G.S. Feng, and T. Pawson. 1997. Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2. EMBO (Eur. Mol. Biol. Organ.) J. 16:2352-2364.
38. Slaney, S.F., M. Oldridge, J.A. Hurst, G.M. Morris-Kay, C.M. Hall, M.D. Poole, and A.O.M. Wilkie. 1996. Differential effects of FGFR2 mutations on syndactyly and cleft palate in Apert syndrome. Am. J. Hum. (Genet. 58:923-932.
39. Stein, G.S., J.B. Lian, J.L. Stein, A.J. van Wijnen, B. Frenkel, and M. Montecino. 1996. Mechanisms regulating osteoblast proliferation and differentiation. In Principles of Bone Biology. J.P. Bilezikian, L.G. Raisz, and G.A. Rodan, editors. Academic Press, New York, 69-86.
40. Su. W.-C.S., M. Kitagawa, N. Xue, B. Xie, S. Garofalo, J. Cho, C. Deng, W.A. Horton, and X.-Y. Fu. 1997. Activation of Stat1 by mutant fibroblast growth-factor receptor in thanatophoric dysplasia type II dwarfism. Nature. 386:288-292.
41. Su, J., M. Muranjan, and J. Sap. 1999. Receptor protein tyrosine phosphatase alpha activates Src-family kinases and controls integrin-mediated responses in fibroblasts. Curr. Biol. 9:505-511.
42. Wilkie, A.O.M. 1997. Craniosynostosis: genes and mechanisms. Human Mol. Genet. 6:1647-1656.
43. Yamaguchi, T.P., K. Harpal, M. Henkemeyer, and J. Rossant. 1994. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 15:3032-3044.