Structural mimicry of a-loop tyrosine phosphorylation by a pathogenic FGF receptor 3 mutation

Structure

Volumn 21, Issue 10, 2013, Pages 1889-1896

  Huang, Zhifeng ^a,b   Chen, Huaibin ^a,b   Blais, Steven ^b   Neubert, Thomas A ^b   Li, Xiaokun ^a   Mohammadi, Moosa ^b  

^a WENZHOU MEDICAL UNIVERSITY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 3; TYROSINE;

ARTICLE; CARCINOGENESIS; CRYSTAL STRUCTURE; HUMAN; HYDROGEN BOND; MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; THANATOPHORIC DWARFISM;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; ENZYME STABILITY; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR MIMICRY; MUTATION, MISSENSE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; SKULL; THANATOPHORIC DYSPLASIA; TYROSINE;

EID: 84885432815     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.07.017     Document Type: Article

References (37)

1. P.D. Adams, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, N.W. Moriarty, R.J. Read, J.C. Sacchettini, N.K. Sauter, and T.C. Terwilliger PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr. D Biol. Crystallogr. 58 2002 1948 1954
2. 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
3. J.H. Bae, E.D. Lew, S. Yuzawa, F. Tomé, I. Lax, and J. Schlessinger The selectivity of receptor tyrosine kinase signaling is controlled by a secondary SH2 domain binding site Cell 138 2009 514 524
4. J.H. Bae, T.J. Boggon, F. Tomé, V. Mandiyan, I. Lax, and J. Schlessinger Asymmetric receptor contact is required for tyrosine autophosphorylation of fibroblast growth factor receptor in living cells Proc. Natl. Acad. Sci. USA 107 2010 2866 2871
5. A. Beenken, and M. Mohammadi The FGF family: biology, pathophysiology and therapy Nat. Rev. Drug Discov. 8 2009 235 253
6. G.A. Bellus, I. McIntosh, E.A. Smith, A.S. Aylsworth, I. Kaitila, W.A. Horton, G.A. Greenhaw, J.T. Hecht, and C.A. Francomano A recurrent mutation in the tyrosine kinase domain of fibroblast growth factor receptor 3 causes hypochondroplasia Nat. Genet. 10 1995 357 359
7. G.A. Bellus, E.B. Spector, P.W. Speiser, C.A. Weaver, A.T. Garber, C.R. Bryke, J. Israel, S.S. Rosengren, M.K. Webster, D.J. Donoghue, and C.A. Francomano Distinct missense mutations of the FGFR3 lys650 codon modulate receptor kinase activation and the severity of the skeletal dysplasia phenotype Am. J. Hum. Genet. 67 2000 1411 1421
8. D. Cappellen, C. De Oliveira, D. Ricol, S. de Medina, J. Bourdin, X. Sastre-Garau, D. Chopin, J.P. Thiery, and F. Radvanyi Frequent activating mutations of FGFR3 in human bladder and cervix carcinomas Nat. Genet. 23 1999 18 20
9. H. Chen, J. Ma, W. Li, A.V. Eliseenkova, C. Xu, T.A. Neubert, W.T. Miller, and M. Mohammadi A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases Mol. Cell 27 2007 717 730
10. H. Chen, C.F. Xu, J. Ma, A.V. Eliseenkova, W. Li, P.M. Pollock, N. Pitteloud, W.T. Miller, T.A. Neubert, and M. Mohammadi A crystallographic snapshot of tyrosine trans-phosphorylation in action Proc. Natl. Acad. Sci. USA 105 2008 19660 19665
11. H. Chen, Z. Huang, K. Dutta, S. Blais, T.A. Neubert, X. Li, D. Cowburn, N.J. Traaseth, and M. Mohammadi Cracking the molecular origin of intrinsic tyrosine kinase activity through analysis of pathogenic gain-of-function mutations Cell Rep. 4 2013 376 384
12. M. Chesi, E. Nardini, L.A. Brents, E. Schröck, T. Ried, W.M. Kuehl, and P.L. Bergsagel Frequent translocation t(4;14)(p16.3;q32.3) in multiple myeloma is associated with increased expression and activating mutations of fibroblast growth factor receptor 3 Nat. Genet. 16 1997 260 264
13. E.Z. Eisenmesser, O. Millet, W. Labeikovsky, D.M. Korzhnev, M. Wolf-Watz, D.A. Bosco, J.J. Skalicky, L.E. Kay, and D. Kern Intrinsic dynamics of an enzyme underlies catalysis Nature 438 2005 117 121
14. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
15. S. Foldynova-Trantirkova, W.R. Wilcox, and P. Krejci Sixteen years and counting: the current understanding of fibroblast growth factor receptor 3 (FGFR3) signaling in skeletal dysplasias Hum. Mutat. 33 2012 29 41
16. C.M. Furdui, E.D. Lew, J. Schlessinger, and K.S. Anderson Autophosphorylation of FGFR1 kinase is mediated by a sequential and precisely ordered reaction Mol. Cell 21 2006 711 717
17. R. Goetz, and M. Mohammadi Exploring mechanisms of FGF signalling through the lens of structural biology Nat. Rev. Mol. Cell Biol. 14 2013 166 180
18. A. Goriely, R.M. Hansen, I.B. Taylor, I.A. Olesen, G.K. Jacobsen, S.J. McGowan, S.P. Pfeifer, G.A. McVean, E. Rajpert-De Meyts, and A.O. Wilkie Activating mutations in FGFR3 and HRAS reveal a shared genetic origin for congenital disorders and testicular tumors Nat. Genet. 41 2009 1247 1252
19. C. Guo, C.R. Degnin, M.B. Laederich, G.P. Lunstrum, P. Holden, J. Bihlmaier, D. Krakow, Y.J. Cho, and W.A. Horton Sprouty 2 disturbs FGFR3 degradation in thanatophoric dysplasia type II: a severe form of human achondroplasia Cell. Signal. 20 2008 1471 1477
20. S.R. Hubbard, and J.H. Till Protein tyrosine kinase structure and function Annu. Rev. Biochem. 69 2000 373 398
21. T.A. Jones, J.Y. Zou, S.W. Cowan, and M. Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr. A 47 1991 110 119
22. S.H. Kan, N. Elanko, D. Johnson, L. Cornejo-Roldan, J. Cook, E.W. Reich, S. Tomkins, A. Verloes, S.R. Twigg, and S. Rannan-Eliya Genomic screening of fibroblast growth-factor receptor 2 reveals a wide spectrum of mutations in patients with syndromic craniosynostosis Am. J. Hum. Genet. 70 2002 472 486
23. 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
24. A. Logié, C. Dunois-Lardé, C. Rosty, O. Levrel, M. Blanche, A. Ribeiro, J.M. Gasc, J. Jorcano, S. Werner, and X. Sastre-Garau Activating mutations of the tyrosine kinase receptor FGFR3 are associated with benign skin tumors in mice and humans Hum. Mol. Genet. 14 2005 1153 1160
25. M. Mohammadi, J. Schlessinger, and S.R. Hubbard Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism Cell 86 1996 577 587
26. M. Mohammadi, I. Dikic, A. Sorokin, W.H. Burgess, M. Jaye, and J. Schlessinger Identification of six novel autophosphorylation sites on fibroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction Mol. Cell. Biol. 16 1996 977 989
27. 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
28. J. Navaza Amore - an automated package for molecular replacement Acta Crystallogr. A 50 1994 157 163
29. N. Nowroozi, S. Raffioni, T. Wang, B.L. Apostol, R.A. Bradshaw, and L.M. Thompson Sustained ERK1/2 but not STAT1 or 3 activation is required for thanatophoric dysplasia phenotypes in PC12 cells Hum. Mol. Genet. 14 2005 1529 1538
30. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode C.W. Carter, R.M. Sweets, Methods in Enzymology 1997 University of Virginia Charlottesville 307 326
31. P.L. Tavormina, R. Shiang, L.M. Thompson, Y.Z. Zhu, D.J. Wilkin, R.S. Lachman, W.R. Wilcox, D.L. Rimoin, D.H. Cohn, and J.J. Wasmuth Thanatophoric dysplasia (types I and II) caused by distinct mutations in fibroblast growth factor receptor 3 Nat. Genet. 9 1995 321 328
32. J. Villali, and D. Kern Choreographing an enzyme's dance Curr. Opin. Chem. Biol. 14 2010 636 643
33. M.K. Webster, and D.J. Donoghue Enhanced signaling and morphological transformation by a membrane-localized derivative of the fibroblast growth factor receptor 3 kinase domain Mol. Cell. Biol. 17 1997 5739 5747
34. M.K. Webster, and D.J. Donoghue FGFR activation in skeletal disorders: too much of a good thing Trends Genet. 13 1997 178 182
35. 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
36. W.R. Wilcox, P.L. Tavormina, D. Krakow, H. Kitoh, R.S. Lachman, J.J. Wasmuth, L.M. Thompson, and D.L. Rimoin Molecular, radiologic, and histopathologic correlations in thanatophoric dysplasia Am. J. Med. Genet. 78 1998 274 281
37. A.O. Wilkie Bad bones, absent smell, selfish testes: the pleiotropic consequences of human FGF receptor mutations Cytokine Growth Factor Rev. 16 2005 187 203