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Cell Growth and Development

The Transmembrane Mutation G380R in Fibroblast Growth Factor Receptor 3 Uncouples Ligand-Mediated Receptor Activation from Down-Regulation

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Pages 516-522 | Received 14 Jul 1999, Accepted 11 Oct 1999, Published online: 28 Mar 2023

REFERENCES

  • Basilico, C., and Moscatelli, D.. 1992. The FGF family of growth factors and oncogenes. Adv. Cancer Res. 59:115–165
  • Bellus, G. A., McIntosh, I., Szabo, J., Aylsworth, A., Kaitila, I., and Francomano, C. A.. 1996. Hypochondroplasia: molecular analysis of the fibroblast growth factor receptor 3 gene. Ann. N. Y. Acad. Sci. 785:182–187
  • Cancedda, R., Descalzi Cancedda, F., and Castagnola, P.. 1995. Chondrocyte differentiation. Int. Rev. Cytol. 159:265–358
  • Coffin, J. D., Florkiewicz, R. Z., Neumann, J., Mort-Hopkins, T., Dorn, G. W.II, Lightfoot, P., German, R., Howles, P. N., Kier, A., O'Toole, B. A. 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
  • 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
  • Delezoide, A. L., Lasselin-Benoist, C., Legeai-Mallet, L., Brice, P., Senee, V., Yayon, A., Munnich, A., Vekemans, M., and Bonaventure, J.. 1997. Abnormal FGFR 3 expression in cartilage of thanatophoric dysplasia fetuses. Hum. Mol. Genet. 6:1899–1906
  • Deng, C., Wynshaw, B. 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
  • Givol, D., and Yayon, A.. 1992. Complexity of FGF receptors: genetic basis for structural diversity and functional specificity. FASEB J. 6:3362–3369
  • Grigoriadis, A. E., Heersche, J. N., and Aubin, J. E.. 1988. Differentiation of muscle, fat, cartilage, and bone from progenitor cells present in a bone-derived clonal cell population: effect of dexamethasone. J. Cell Biol. 106:2139–2151
  • Horton, W. A., Machado, M. A., Ellard, J., Campbell, D., Putnam, E. A., Aulthouse, A. L., Sun, X., and Sandell, L. J.. 1993. An experimental model of human chondrocyte differentiation. Prog. Clin. Biol. Res. 3838:533–540
  • Jingushi, S., Scully, S. P., Joyce, M. E., Sugioka, Y., and Bolander, M. E.. 1995. Transforming growth factor-beta 1 and fibroblast growth factors in rat growth plate. J. Orthop. Res. 13:761–768
  • Johnson, D. E., and Williams, L. T.. 1993. Structural and functional diversity in the FGF receptor multigene family. Adv. Cancer Res. 60:1–41
  • Keegan, K., Meyer, S., and Hayman, M. J.. 1991. Structural and biosynthetic characterization of the fibroblast growth factor receptor 3 (FGFR-3) protein. Oncogene 6:2229–2236
  • Leach, R. J., Sokol, C., and McMurtry, J. P.. 1997. Immunolocalization of basic fibroblast growth factor in porcine epiphyseal growth plate. Domest. Anim. Endocrinol. 14:129–132
  • Li, Y., Mangasarian, K., Mansukhani, A., and Basilico, C.. 1997. Activation of FGF receptors by mutations in the transmembrane domain. Oncogene 14:1397–1406
  • McConahey, P. J., and Dixon, F. J.. 1980. Radioiodination of proteins by the use of the chloramine-T method. Methods Enzymol. 70:210–213
  • McDougall, S., Fu, Y. H., Lowe, G. N., Williams, A., Polendo, R., Benya, P. D., Iida-Klein, A., Fang, M. A., and Hahn, T. J.. 1996. Surface adhesion-mediated regulation of chondrocyte-specific gene expression in the nontransformed RCJ 3.1C5.18 rat chondrocyte cell line. J. Bone Miner. Res. 11:1130–1138
  • Naski, M. C., Wang, Q., Xu, J., and Ornitz, D. M.. 1996. Graded activation of fibroblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia. Nat. Genet. 13:233–237
  • Nilsson, A., Ohlsson, C., Isaksson, O. G., Lindahl, A., and Isgaard, J.. 1994. Hormonal regulation of longitudinal bone growth. Eur. J. Clin. Nutr. 48 (Suppl. 1):S150–158
  • Peters, K., Ornitz, D., Werner, S., and Williams, L.. 1993. Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis. Dev. Biol. 155:423–430
  • Peters, K. G., Werner, S., Chen, G., and Williams, L. T.. 1992. Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse. Development 114:233–243
  • Ponseti, I. V.. 1970. Skeletal growth in achondroplasia. J. Bone Jt. Surg. Am. Vol. 52:701–716
  • Ponseti, I. V.. 1988. Bone formation in achondroplasia. Basic Life Sci. 48:109–122
  • Raffioni, S., Zhu, Y. Z., Bradshaw, R. A., and Thompson, L. M.. 1998. Effect of transmembrane and kinase domain mutations on fibroblast growth factor receptor 3 chimera signaling in PC12 cells. A model for the control of receptor tyrosine kinase activation. J. Biol. Chem. 273:35250–35259
  • Robertson, S. C., Meyer, A. N., Hart, K. C., Galvin, B. D., Webster, M. K., and Donoghue, D. J.. 1998. Activating mutations in the 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 95:4567–4572
  • Rossant, J., Ciruna, B., and Partanen, J.. 1997. FGF signaling in mouse gastrulation and anteroposterior patterning. Cold Spring Harbor Symp. Quant. Biol. 62:127–133
  • Rousseau, F., Bonaventure, J., Legeai, M. L., Pelet, A., Rozet, J. M., Maroteaux, P., Le, M. M., and Munnich, A.. 1994. Mutations in the gene encoding fibroblast growth factor receptor-3 in achondroplasia. Nature 371:252–254
  • Rousseau, F., el Ghouzzi, V., Delezoide, A. L., Legeai-Mallet, L., Le Merrer, M., Munnich, A., and Bonaventure, J.. 1996. Missense FGFR3 mutations create cysteine residues in thanatophoric dwarfism type I (TD1). Hum. Mol. Genet. 5:509–512
  • Segev, O., Chumakov I., Nevo Z., Givol D., Madar-Shapiro L., Sheinin Y., Weinreb M., and Yayon A.. Restrained chondrocyte proliferation and maturation with abnormal growth plate vascularization and ossification in human FGFR-3G380R transgenic mice. Hum. Mol. Genet., in press.
  • Shiang, R., Thompson, L. M., Zhu, Y. Z., Church, D. M., Fielder, T. J., Bocian, M., Winokur, S. T., and Wasmuth, J. J.. 1994. Mutations in the transmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia. Cell 78:335–342
  • Sorkin, A., Helin, K., Waters, C. M., Carpenter, G., and Beguinot, L.. 1992. Multiple autophosphorylation sites of the epidermal growth factor receptor are essential for receptor kinase activity and internalization. Contrasting significance of tyrosine 992 in the native and truncated receptors. J. Biol. Chem. 267:8672–8678
  • Sorkin, A., Waters, C., Overholser, K. A., and Carpenter, G.. 1991. Multiple autophosphorylation site mutations of the epidermal growth factor receptor. Analysis of kinase activity and endocytosis. J. Biol. Chem. 266:8355–8362
  • Sorokin, A., Mohammadi, M., Huang, J., and Schlessinger, J.. 1994. Internalization of fibroblast growth factor receptor is inhibited by a point mutation at tyrosine 766. J. Biol. Chem. 269:17056–17061
  • Tavormina, P. L., Shiang, R., Thompson, L. M., Zhu, Y. Z., Wilkin, D. J., Lachman, R. S., Wilcox, W. R., Rimoin, D. L., Cohn, D. H., and Wasmuth, J. J.. 1995. Thanatophoric dysplasia (types I and II) caused by distinct mutations in fibroblast growth factor receptor 3. Nat. Genet. 9:321–328
  • Thompson, L. M., Raffioni, S., Wasmuth, J. J., and Bradshaw, R. A.. 1997. Chimeras of the native form or achondroplasia mutant (G375C) of human fibroblast growth factor receptor 3 induce ligand-dependent differentiation of PC12 cells. Mol. Cell. Biol. 17:4169–4177
  • Ullrich, A., and Schlessinger, J.. 1990. Signal transduction by receptors with tyrosine kinase activity. Cell 61:203–212
  • Webster, M. K., D'Avis, P. Y., Robertson, S. C., and Donoghue, D. J.. 1996. Profound ligand-independent kinase activation of fibroblast growth factor receptor 3 by the activation loop mutation responsible for a lethal skeletal dysplasia, thanatophoric dysplasia type II. Mol. Cell. Biol. 16:4081–4087
  • Webster, M. K., and Donoghue, D. J.. 1996. Constitutive activation of fibroblast growth factor receptor 3 by the transmembrane domain point mutation found in achondroplasia. EMBO J. 15:520–527
  • Webster, M. K., and Donoghue, D. J.. 1997. FGFR activation in skeletal disorders: too much of a good thing. Trends Genet. 13:178–182
  • Weiner, D. B., Liu, J., Cohen, J. A., Williams, W. V., and Greene, M. I.. 1989. A point mutation in the neu oncogene mimics ligand induction of receptor aggregation. Nature 339:230–231
  • Wilkie, A. O., Morriss, K. G., Jones, E. Y., and Heath, J. K.. 1995. Functions of fibroblast growth factors and their receptors. Curr. Biol. 5:500–507
  • Wuechner, C., Nordqvist, A. C., Winterpacht, A., Zabel, B., and Schalling, M.. 1996. Developmental expression of splicing variants of fibroblast growth factor receptor 3 (FGFR3) in mouse. Int. J. Dev. Biol. 40:1185–1188

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