Identification and characterization of an inhibitory fibroblast growth factor receptor 2 (FGFR2) molecule, up-regulated in an Apert Syndrome mouse model

Biochemical Journal

Volumn 436, Issue 1, 2011, Pages 71-81

  Wheldon, Lee M ^a,c   Khodabukus, Naila ^a   Patey, Susannah J ^a   Smith, Terence G ^b   Heath, John K ^a   Hajihosseini, Mohammad K ^b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Apert syndrome; Fibroblast growth factor receptor 2 (FGFR2); mRNA splicing; Nonsense mediated decay (NMD) pathway

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2;

ACROCEPHALOSYNDACTYLY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; EMBRYO; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

ACROCEPHALOSYNDACTYLIA; ANIMALS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; EXONS; HUMANS; MICE; MICE, INBRED STRAINS; MODELS, ANIMAL; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; UP-REGULATION;

EID: 79955539972     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100884     Document Type: Article

References (52)

1. Sekine, K., Ohuchi, H., Fujiwara, M., Yamasaki, M., Yoshizawa, T., Sato, T., Yagishita, N., Matsui, D., Koga, Y., Itoh, N. and Kato, S. (1999) Fgf10 is essential for limb and lung formation. Nat. Genet. 21, 138-141 (Pubitemid 29036301)
2. Saito, T. and Fukumoto, S. (2009) Fibroblast growth factor 23 (FGF23) and disorders of phosphate metabolism. Int. J. Pediatr. Endocrinol. 2009, 496514
3. Meyers, E. N., Lewandoski, M. and Martin, G. R. (1998) An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 18, 136-141 (Pubitemid 28082459)
4. 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 (Pubitemid 26166160)
5. Hajihosseini, M. K. (2008) Fibroblast growth factor signalling in cranial suture development and pathogenesis. Front. Oral Biol. 12, 160-177
6. Wilkie, A. O. (2005) Bad bones, absent smell, selfish testes: the pleiotropic consequences of human FGF receptor mutations. Cytokine Growth Factor Rev. 16, 187-203 (Pubitemid 40616116)
7. McKeehan, W. L., Wang, F. and Kan, M. (1998) The heparan sulfate-fibroblast growth factor family: diversity of structure and function. Prog. Nucleic Acid Res. Mol. Biol. 59, 135-176
8. Beenken, A. and Mohammadi, M. (2009) The FGF family: biology, pathophysiology and therapy. Nat. Rev. Drug Discov. 8, 235-253
9. Hajihosseini, M. K., Lalioti, M. D., Arthaud, S., Burgar, H. R., Brown, J. M., Twigg, S. R., Wilkie, A. O. and Heath, J. K. (2004) Skeletal development is regulated by fibroblast growth factor receptor 1 signalling dynamics. Development 131, 325-335 (Pubitemid 38181372)
10. Tsang, M. and Dawid, I. B. (2004) Promotion and attenuation of FGF signalling through the Ras-MAPK pathway. Sci. STKE 2004, pe17
11. Wheldon, L. M., Haines, B. P., Rajappa, R., Mason, I., Rigby, P. W. and Heath, J. K. (2010) Critical role of FLRT1 phosphorylation in the interdependent regulation of FLRT1 function and FGF receptor signalling. PLoS ONE 5, e10264
12. Kuro-o, M. (2010) Klotho. Pflugers Arch. 459, 333-343
13. Werner, S., Duan, D. S., de Vries, C, Peters, K. G., Johnson, D. E. and Williams, L. T. (1992) Differential splicing in the extracellular region of fibroblast growth factor receptor 1 generates receptor variants with different ligand-binding specificities. Mol. Cell. Biol. 12, 82-88
14. Burgar, H. R., Burns, H. D., Elsden, J. L., Lalioti, M. D. and Heath, J. K. (2002) Association of the signalling adaptor FRS2 with fibroblast growth factor receptor 1 (Fgfrl) is mediated by alternative splicing of the juxtamembrane domain. J. Biol. Chem. 277, 4018-4023 (Pubitemid 34968657)
15. 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
16. Zhang, X., Ibrahimi, O. A., Olsen, S. K., Umemori, H., Mohammadi, M. and Ornitz, D. M. (2006) Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 281, 15694-15700 (Pubitemid 43848456)
17. Duan, D. S., Werner, S. and Williams, L. T. (1992) A naturally occurring secreted form of fibroblast growth factor (FGF) receptor 1 binds basic FGF in preference over acidic FGF. J. Biol. Chem. 267, 16076-16080
18. Hanneken, A. (2001) Structural characterization of the circulating soluble FGF receptors reveals multiple isoforms generated by secretion and ectodomain shedding. FEBS Lett. 489, 176-181 (Pubitemid 32126404)
19. Maquat, L. E. (2005) Nonsense-mediated mRNA decay in mammals. J. Cell Sci. 118, 1773-1776 (Pubitemid 40723821)
20. Hajihosseini, M. K., Wilson, S., De Moerlooze, L. and Dickson, C. (2001) A splicing switch and gain-of-function mutation in FgfR2-IIIc hemizygotes causes Apert/Pfeiffer-syndrome-like phenotypes. Proc. Natl. Acad. Sci. U.S.A. 98, 3855-3860 (Pubitemid 32249861)
21. Oldridge, M., Zackai, E. H., McDonald-McGinn, D. M., Iseki, S., Morriss-Kay, G. M., Twigg, S. R., Johnson, D., Wall, S. A., Jiang, W., Theda, C. et al. (1999) De novoalu-element insertions in FGFR2 identify a distinct pathological basis for Apert syndrome. Am.J.Hum.Genet. 64, 446-461 (Pubitemid 129500527)
22. Bochukova, E. G., Roscioli, T., Hedges, D. J., Taylor, I. B., Johnson, D., David, D. J., Deininger, P. L. and Wilkie, A. O. (2009) Rare mutations of FGFR2 causing Apert syndrome: identification of the first partial gene deletion, and an Alu element insertion from a new subfamily. Hum. Mutat. 30, 204-211
23. Hajihosseini, M. K., Duarte, R., Pegrum, J., Donjacour, A., Lana-Elola, E., Rice, D. P., Sharpe, J. and Dickson, C. (2009) Evidence that Fgf10 contributes to the skeletal and visceral defects of an Apert syndrome mouse model. Dev. Dyn. 238, 376-385
24. Hajihosseini, M. K. and Dickson, C. (1999) A subset of fibroblast growth factors (Fgfs) promote survival, but Fgf-8b specifically promotes astroglial differentiation of rat cortical precursor cells. Mol. Cell. Neurosci. 14, 468-485 (Pubitemid 30026589)
25. Anderson, J., Burns, H. D., Enriquez-Harris, P., Wilkie, A. O. and Heath, J. K. (1998) Apert syndrome mutations in fibroblast growth factor receptor 2 exhibit increased affinity for FGF ligand. Hum. Mol. Genet. 7, 1475-1483 (Pubitemid 28429929)
26. Smith, T. G., Sweetman, D., Patterson, M., Keyse, S. M. and Munsterberg, A. (2005) Feedback interactions between MKP3 and ERK MAP kinase control scleraxis expression and the specification of rib progenitors in the developing chick somite. Development 132, 1305-1314 (Pubitemid 40528790)
27. Terada, M., Shimizu, A., Sato, N., Miyakaze, S. I., Katayama, H. and Kurokawa-Seo, M. (2001) Fibroblast growth factor receptor 3 lacking the Ig IIIb and transmembrane domains secreted from human squamous cell carcinoma DJM-1 binds to FGFs. Mol. Cell. Biol. Res. Commun. 4, 365-373 (Pubitemid 33098108)
28. Nelson, R. W., Nedelkov, D. and Tubbs, K. A. (2000) Biosensor chip mass spectrometry: a chip-based proteomics approach. Electrophoresis 21, 1155-1163 (Pubitemid 30230780)
29. Miki, T., Bottaro, D. P., Fleming, T. P., Smith, C. L., Burgess, W. H., Chan, A. M. and Aaronson, S. A. (1992) Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc. Natl. Acad. Sci. U.S.A. 89, 246-250
30. Jones, R. B., Wang, F., Luo, Y., Yu, C., Jin, C., Suzuki, T., Kan, M. and McKeehan, W. L. (2001) The nonsense-mediated decay pathway and mutually exclusive expression of alternatively spliced FGFR2IIIb and -Illc mRNAs. J. Biol. Chem. 276, 4158-4167
31. Muhlemann, O., Eberle, A. B., Stalder, L. and Zamudio Orozco, R. (2008) Recognition and elimination of nonsense mRNA. Biochim. Biophys. Acta 1779, 538-549
32. Lewis, B. P., Green, R. E. and Brenner, S. E. (2003) Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. U.S.A. 100, 189-192 (Pubitemid 36078050)
33. Mendell, J. T., Sharifi, N. A., Meyers, J. L., Martinez-Murillo, F. and Dietz, H. C. (2004) Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36, 1073-1078 (Pubitemid 41184468)
34. De Moerlooze, L., Spencer-Dene, B., Revest, J., Hajihosseini, M., Rosewell, I. and Dickson, C. (2000) An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127, 483-492 (Pubitemid 30093396)
35. Tsukuno, M., Suzuki, H. and Eto, Y. (1999) Pfeiffer syndrome caused by haploinsufficient mutation of FGFR2. J. Craniofac. Genet. Dev. Biol. 19, 183-188 (Pubitemid 30095294)
36. Klein, D. E., Nappi, V. M., Reeves, G. T., Shvartsman, S. Y. and Lemmon, M. A. (2004) Argos inhibits epidermal growth factor receptor signalling by ligand sequestration. Nature 430, 1040-1044 (Pubitemid 39128390)
37. Kawano, Y. and Kypta, R. (2003) Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 116, 2627-2634 (Pubitemid 36857216)
38. Celli, G., LaRochelle, W. J., Mackem, S., Sharp, R. and Merlino, G. (1998) Soluble dominant-negative receptor uncovers essential roles for fibroblast growth factors in multi-organ induction and patterning. EMBO J. 17, 1642-1655 (Pubitemid 28119118)
39. Duchesne, L., Tissot, B., Rudd, T. R., Dell, A. and Fernig, D. G. (2006) N-glycosylation of ibroblast growth factor receptor 1 regulates ligand and heparan sulfate co-receptor binding. J. Biol. Chem. 281, 27178-27189 (Pubitemid 44401747)
40. Polanska, U. M., Duchesne, L., Harries, J. C., Fernig, D. G. and Kinnunen, T. K. (2009) N-Glycosylation regulates fibroblast growth factor receptor/EGL-15 activity in Caenorhabditis elegans in vivo. J. Biol. Chem. 284, 33030-33039
41. Cohen, Jr, M. M. and Kreiborg, S. (1993) An updated pediatric perspective on the Apert syndrome. Am. J. Dis. Child. 147, 989-993 (Pubitemid 23262002)
42. Slaney, S. F., Oldridge, M., Hurst, J. A., Moriss-Kay, G. M., Hall, C. M., Poole, M. D. and Wilkie, A. O. (1996) Differential effects of FGFR2 mutations on syndactyly and cleft palate in Apert syndrome. Am. J. Hum. Genet. 58, 923-932 (Pubitemid 26115163)
43. Fairbanks, T. J., De Langhe, S., Sala, F. G., Warburton, D., Anderson, K. D., Bellusci, S. and Burns, R. C. (2004) Fibroblast growth factor 10 (Fgf10) invalidation results in anorectal malformation in mice. J. Pediatr. Surg. 39, 360-365 (Pubitemid 38338349)
44. Ibrahimi, O. A., Zhang, F., Eliseenkova, A. V., Itoh, N., Linhardt, R. J. and Mohammadi, M. (2004) Biochemical analysis of pathogenic ligand-dependent FGFR2 mutations suggests distinct pathophysiological mechanisms for craniofacial and limb abnormalities. Hum. Mol. Genet. 13, 2313-2324 (Pubitemid 39359928)
45. Tanimoto, Y, Yokozeki, M., Hiura, K., Matsumoto, K., Nakanishi, H., Matsumoto, T., Marie, P. J. and Moriyama, K. (2004) A soluble form of fibroblast growth factor receptor 2 (FGFR2) with S252W mutation acts as an efficient inhibitor for the enhanced osteoblastic differentiation caused by FGFR2 activation in Apert syndrome. J. Biol. Chem. 279, 45926-45934 (Pubitemid 39491585)
46. Jang, J. H., Shin, K. H., Park, Y. J., Lee, R. J., McKeehan, W. L. and Park, J. G. (2000) Novel transcripts of fibroblast growth factor receptor 3 reveal aberrant splicing and activation of cryptic splice sequences in colorectal cancer. Cancer Res. 60, 4049-4052 (Pubitemid 30636582)
47. Takaishi, S., Sawada, M., Morita, Y., Seno, H., Fukuzawa, H. and Chiba, T. (2000) Identification of a novel alternative splicing of human FGF receptor 4: soluble-form splice variant expressed in human gastrointestinal epithelial cells. Biochem. Biophys. Res. Commun. 267, 658-662 (Pubitemid 30076854)
48. Ezzat, S., Zheng, L., Yu, S. and Asa, S. L. (2001) A soluble dominant negative fibroblast growth factor receptor 4 isoform in human MCF-7 breast cancer cells. Biochem. Biophys. Res. Commun. 287, 60-65 (Pubitemid 32912463)
49. Jang, J. H. (2002) Identification and characterization of soluble isoform of fibroblast growth factor receptor 3 in human SaOS-2 osteosarcoma cells. Biochem. Biophys. Res. Commun. 292, 378-382
50. Jang, J. H., Shin, K. H. and Park, J. G. (2001) Mutations in fibroblast growth factor receptor 2 and fibroblast growth factor receptor 3 genes associated with human gastric and colorectal cancers. Cancer Res. 61, 3541-3543
51. Ricol, D., Cappellen, D., El Marjou, A., Gil-Diez-de-Medina, S., Girault, J. M., Yoshida, T., Ferry, G., Tucker, G., Poupon, M. F., Chopin, D. et al. (1999) Tumour suppressive properties of fibroblast growth factor receptor 2-IIIb in human bladder cancer. Oncogene 18, 7234-7243 (Pubitemid 30032102)
52. Yamaguchi, F., Saya, H., Bruner, J. M. and Morrison, R. S. (1994) Differential expression of two fibroblast growth factor-receptor genes is associated with malignant progression in human astrocytomas. Proc. Natl. Acad. Sci. U.S.A. 91, 484-488 (Pubitemid 24041426)