FGFR3 regulates brain size by controlling progenitor cell proliferation and apoptosis during embryonic development

Developmental Biology

Volumn 279, Issue 1, 2005, Pages 73-85

  Inglis Broadgate, Suzanne L ^a   Thomson, Rachel E ^a   Pellicano, Francesca ^a   Tartaglia, Michael A ^a   Pontikis, Charlie C ^b   Cooper, Jonathan D ^b   Iwata, Tomoko ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Apoptosis; Brain size; Cell proliferation; Cortical development; Cortical progenitors; FGF; FGFR3; Mouse

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 3; PHOSPHOTRANSFERASE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN SIZE; CELL COUNT; CELL PROLIFERATION; EMBRYO; EMBRYO DEVELOPMENT; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; STEM CELL; STEREOLOGY; THICKNESS;

EID: 13544257266     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2004.11.035     Document Type: Article

References (67)

1. Y.M. Agazie, N. Movilla, I. Ischenko, and M.J. Hayman The phosphotyrosine phosphatase SHP2 is a critical mediator of transformation induced by the oncogenic fibroblast growth factor receptor 3 Oncogene 22 2003 6909 6918
2. E. Arman, R. Haffner-Krausz, Y. Chen, J.K. Heath, and P. Lonai Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development Proc. Natl. Acad. Sci. U. S. A. 95 1998 5082 5087
3. N. Belluardo, G. Wu, G. Mudo, A.C. Hansson, R. Pettersson, and K. Fuxe Comparative localization of fibroblast growth factor receptor-1, -2, and -3 mRNAs in the rat brain: in situ hybridization analysis J. Comp. Neurol. 379 1997 226 246
4. G.A. Bellus, M.J. Bamshad, K.A. Przylepa, J. Dorst, R.R. Lee, O. Hurko, E.W. Jabs, C.J. Curry, W.R. Wilcox, R.S. Lachman, D.L. Rimoin, and C.A. Francomano Severe achondroplasia with developmental delay and acanthosis nigricans (SADDAN): phenotypic analysis of a new skeletal dysplasia caused by a Lys650Met mutation in fibroblast growth factor receptor 3 Am. J. Med. Genet. 85 1999 53 65
5. E. Bible, P. Gupta, S.L. Hofmann, and J.D. Cooper Regional and cellular neuropathology in the palmitoyl protein thioesterase-1 null mutant mouse model of infantile neuronal ceroid lipofuscinosis Neurobiol. Dis. 16 2004 346 359
6. A. Bulfone, S.M. Smiga, K. Shimamura, A. Peterson, L. Puelles, and J.L. Rubenstein T-brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex Neuron 15 1995 63 78
7. V.S. Caviness Jr., T. Takahashi, and R.S. Nowakowski Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model Trends Neurosci. 18 1995 379 383
8. A. Chenn, and C.A. Walsh Regulation of cerebral cortical size by control of cell cycle exit in neural precursors Science 297 2002 365 369
9. C.L. Chi, S. Martinez, W. Wurst, and G.R. Martin The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum Development 130 2003 2633 2644
10. J.S. Colvin, B.A. Bohne, G.W. Harding, D.G. McEwen, and D.M. Ornitz Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3 Nat. Genet. 12 1996 390 397
11. C.X. Deng, A. Wynshaw-Boris, M.M. Shen, C. Daugherty, D.M. Ornitz, and P. Leder Murine FGFR-1 is required for early postimplantation growth and axial organization Genes Dev. 8 1994 3045 3057
12. C. Deng, A. Wynshaw-Boris, F. Zhou, A. Kuo, and P. Leder Fibroblast growth factor receptor 3 is a negative regulator of bone growth Cell 84 1996 911 921
13. C. Dode, J. Levilliers, J.M. Dupont, A. De Paepe, N. Le Du, N. Soussi-Yanicostas, R.S. Coimbra, S. Delmaghani, S. Compain-Nouaille, F. Baverel, C. Pecheux, D. Le Tessier, C. Cruaud, M. Delpech, F. Speleman, S. Vermeulen, A. Amalfitano, Y. Bachelot, P. Bouchard, S. Cabrol, J.C. Carel, H. Delemarre-van de Waal, B. Goulet-Salmon, M.L. Kottler, O. Richard, F. Sanchez-Franco, R. Saura, J. Young, C. Petit, and J.P. Hardelin Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome Nat. Genet. 33 2003 463 465
14. R. Dono, G. Texido, R. Dussel, H. Ehmke, and R. Zeller Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice EMBO J. 17 1998 4213 4225
15. C.L. Dou, S. Li, and E. Lai Dual role of brain factor-1 in regulating growth and patterning of the cerebral hemispheres Cereb. Cortex 9 1999 543 550
16. T. Edlund, and T.M. Jessell Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system Cell 96 1999 211 224
17. M. Ford-Perriss, H. Abud, and M. Murphy Fibroblast growth factors in the developing central nervous system Clin. Exp. Pharmacol. Physiol. 28 2001 493 503
18. T. Fukuchi-Shimogori, and E.A. Grove Neocortex patterning by the secreted signaling molecule FGF8 Science 294 2001 1071 1074
19. Y. Furuta, D.W. Piston, and B.L. Hogan Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development Development 124 1997 2203 2212
20. S. Garel, K.J. Huffman, and J.L. Rubenstein Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants Development 130 2003 1903 1914
21. K.C. Hart, S.C. Robertson, and D.J. Donoghue Identification of tyrosine residues in constitutively activated fibroblast growth factor receptor 3 involved in mitogenesis, Stat activation, and phosphatidylinositol 3-kinase activation Mol. Biol. Cell. 12 2001 931 942
22. J.M. Hebert, M. Lin, J. Partanen, J. Rossant, and S.K. McConnell FGF signaling through FGFR1 is required for olfactory bulb morphogenesis Development 130 2003 1101 1111
23. R.F. Hevner, L. Shi, N. Justice, Y. Hsueh, M. Sheng, S. Smiga, A. Bulfone, A.M. Goffinet, A.T. Campagnoni, and J.L. Rubenstein Tbr1 regulates differentiation of the preplate and layer 6 Neuron 29 2001 353 366
24. K.L. Ho, C.H. Chang, S.S. Yang, and J.L. Chason Neuropathologic findings in thanatophoric dysplasia Acta Neuropathol. (Berl). 63 1984 218 228
25. T. Iwata, L. Chen, C. Li, D.A. Ovchinnikov, R.R. Behringer, C.A. Francomano, and C.X. Deng A neonatal lethal mutation in FGFR3 uncouples proliferation and differentiation of growth plate chondrocytes in embryos Hum. Mol. Genet. 9 2000 1603 1613
26. T. Iwata, C.L. Li, C.X. Deng, and C.A. Francomano Highly activated Fgfr3 with the K644M mutation causes prolonged survival in severe dwarf mice Hum. Mol. Genet. 10 2001 1255 1264
27. D.M Jacobowitz, and L.C. Abbott Chemoarchitedtonic atlas of the developing mouse brain 1997 CRC Press Florida, USA
28. M.H. Kaufman, and J.B.L. Bard The Anatomical Basis of the Mouse Development 1999 Academic Press London
29. C.Y. Kuan, K.A. Roth, R.A. Flavell, and P. Rakic Mechanisms of programmed cell death in the developing brain Trends Neurosci. 23 2000 291 297
30. C. Li, L. Chen, T. Iwata, M. Kitagawa, X.Y. Fu, and C.X. Deng A Lys644Glu substitution in fibroblast growth factor receptor 3 (FGFR3) causes dwarfism in mice by activation of STATs and ink4 cell cycle inhibitors Hum. Mol. Genet. 8 1999 35 44
31. P.M. Lievens, and E. Liboi The thanatophoric dysplasia type II mutation hampers complete maturation of fibroblast growth factor receptor 3 (FGFR3), which activates signal transducer and activator of transcription 1 (STAT1) from the endoplasmic reticulum J. Biol. Chem. 278 2003 17344 17349
32. T. Lin, S.B. Sandusky, H. Xue, K.W. Fishbein, R.G. Spencer, M.S. Rao, and C.A. Francomano A central nervous system specific mouse model for thanatophoric dysplasia type II Hum. Mol. Genet. 12 2003 2863 2871
33. S. Martinez, P.H. Crossley, I. Cobos, J.L. Rubenstein, and G.R. Martin FGF8 induces formation of an ectopic isthmic organizer and isthmocerebellar development via a repressive effect on Otx2 expression Development 126 1999 1189 1200
34. M.J. McLeod Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S Teratology 22 1980 299 301
35. E.N. Meyers, M. Lewandoski, and G.R. Martin An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination Nat. Genet. 18 1998 136 141
36. E. Monsonego-Ornan, R. Adar, T. Feferman, O. Segev, and A. Yayon The transmembrane mutation G380R in fibroblast growth factor receptor 3 uncouples ligand-mediated receptor activation from down-regulation Mol. Cell. Biol. 20 2000 516 522
37. M.C. Naski, Q. Wang, J. Xu, and D.M. Ornitz Graded activation of fibroblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia Nat. Genet. 13 1996 233 237
38. S.C. Noctor, V. Martinez-Cerdeno, L. Ivic, and A.R. Kriegstein Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases Nat. Neurosci. 7 2004 136 144
39. L.Y. Oh, A. Denninger, J.S. Colvin, A. Vyas, S. Tole, D.M. Ornitz, and R. Bansal Fibroblast growth factor receptor 3 signaling regulates the onset of oligodendrocyte terminal differentiation J. Neurosci. 23 2003 883 894
40. D.M. Ornitz, J. Xu, J.S. Colvin, D.G. McEwen, C.A. MacArthur, F. Coulier, G. Gao, and M. Goldfarb Receptor specificity of the fibroblast growth factor family J. Biol. Chem. 271 1996 15292 15297
41. A. Orr-Urtreger, D. Givol, A. Yayon, Y. Yarden, and P. Lonai Developmental expression of two murine fibroblast growth factor receptors, flg and bek Development 113 1991 1419 1434
42. S. Ortega, M. Ittmann, S.H. Tsang, M. Ehrlich, and C. Basilico Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2 Proc. Natl. Acad. Sci. U. S. A. 95 1998 5672 5677
43. K. Peters, D. Ornitz, S. Werner, and L. Williams Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis Dev. Biol. 155 1993 423 430
44. U. Pirvola, J. Ylikoski, R. Trokovic, J. Hebert, S. McConnell, and J. Partanen FGFR1 is required for the development of the auditory sensory epithelium Neuron 35 2002 671 680
45. N.P. Pringle, W.P. Yu, M. Howell, J.S. Colvin, D.M. Ornitz, and W.D. Richardson Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains Development 130 2003 93 102
46. R. Raballo, J. Rhee, R. Lyn-Cook, J.F. Leckman, M.L. Schwartz, and F.M. Vaccarino Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex J. Neurosci. 20 2000 5012 5023
47. P. Rakic A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution Trends Neurosci. 18 1995 383 388
48. M.E. Ross, and C.A. Walsh Human brain malformations and their lessons for neuronal migration Annu. Rev. Neurosci. 24 2001 1041 1070
49. Y. Sasai, R. Kageyama, Y. Tagawa, R. Shigemoto, and S. Nakanishi Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split Genes Dev. 6 1992 2620 2634
50. J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 103 2000 211 225
51. K. Shimamura, and J.L. Rubenstein Inductive interactions direct early regionalization of the mouse forebrain Development 124 1997 2709 2718
52. D.M. Shin, S. Korada, R. Raballo, C.S. Shashikant, A. Simeone, J.R. Taylor, and F. Vaccarino Loss of glutamatergic pyramidal neurons in frontal and temporal cortex resulting from attenuation of FGFR1 signaling is associated with spontaneous hyperactivity in mice J. Neurosci. 24 2004 2247 2258
53. R.L. Sidman, and P. Rakic Neuronal migration, with special reference to developing human brain: a review Brain Res. 62 1973 1 35
54. E.E. Storm, J.L. Rubenstein, and G.R. Martin Dosage of Fgf8 determines whether cell survival is positively or negatively regulated in the developing forebrain Proc. Natl. Acad. Sci. U. S. A. 100 2003 1757 1762
55. G. Szebenyi, and J.F. Fallon Fibroblast growth factors as multifunctional signaling factors Int. Rev. Cytol. 185 1999 45 106
56. T. Takahashi, R.S. Nowakowski, and V.S. Caviness Jr. Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse J. Neurosci. 13 1993 820 833
57. T. Takahashi, R.S. Nowakowski, and V.S. Caviness Jr. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall J. Neurosci. 15 1995 6046 6057
58. P.L. Tavormina, G.A. Bellus, M.K. Webster, M.J. Bamshad, A.E. Fraley, I. McIntosh, J. Szabo, W. Jiang, E.W. Jabs, W.R. Wilcox, J.J. Wasmuth, D.J. Donoghue, L.M. Thompson, and C.A. Francomano A novel skeletal dysplasia with developmental delay and acanthosis nigricans is caused by a Lys650Met mutation in the fibroblast growth factor receptor 3 gene Am. J. Hum. Genet. 64 1999 722 731
59. S. Temple The development of neural stem cells Nature 414 2001 112 117
60. S. Temple, and X. Qian bFGF, neurotrophins, and the control or cortical neurogenesis Neuron 15 1995 249 252
61. R. Trokovic, N. Trokovic, S. Hernesniemi, U. Pirvola, D.M. Vogt Weisenhorn, J. Rossant, A.P. McMahon, W. Wurst, and J. Partanen FGFR1 is independently required in both developing mid-and hindbrain for sustained response to isthmic signals EMBO J. 22 2003 1811 1823
62. F.M. Vaccarino, M.L. Schwartz, R. Raballo, J. Nilsen, J. Rhee, M. Zhou, T. Doetschman, J.D. Coffin, J.J. Wyland, and Y.T. Hung Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis Nat. Neurosci. 2 1999 246 253
63. M.K. Webster, P.Y. D'Avis, S.C. Robertson, and D.J. Donoghue 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 1996 4081 4087
64. T. Wongmongkolrit, M. Bush, and U. Roessmann Neuropathological findings in thanatophoric dysplasia Arch. Pathol. Lab. Med. 107 1983 132 135
65. T.P. Yamaguchi, K. Harpal, M. Henkemeyer, and J. Rossant fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation Genes Dev. 8 1994 3032 3044
66. N. Yazaki, Y. Hosoi, K. Kawabata, A. Miyake, M. Minami, M. Satoh, M. Ohta, T. Kawasaki, and N. Itoh Differential expression patterns of mRNAs for members of the fibroblast growth factor receptor family, FGFR-1-FGFR-4, in rat brain J. Neurosci. Res. 37 1994 445 452
67. W. Ye, K. Shimamura, J.L. Rubenstein, M.A. Hynes, and A. Rosenthal FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate Cell 93 1998 755 766