Cracking the molecular origin of intrinsic tyrosine kinase activity through analysis of pathogenic gain-of-function mutations

Cell Reports

Volumn 4, Issue 2, 2013, Pages 376-384

  Chen, Huaibin ^a,b   Huang, Zhifeng ^a,b   Dutta, Kaushik ^c   Blais, Steven ^a   Neubert, Thomas A ^a   Li, Xiaokun ^b   Cowburn, David ^d   Traaseth, Nathaniel J ^e   Mohammadi, Moosa ^a  

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

^b WENZHOU MEDICAL UNIVERSITY   (China)

^c NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; LYSINE; PROTEIN TYROSINE KINASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STRUCTURE; GAIN OF FUNCTION MUTATION; MUTANT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WILD TYPE; X RAY CRYSTALLOGRAPHY;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

EID: 84880806523     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.06.025     Document Type: Article

References (39)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.-W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Banavali N.K., Roux B. Flexibility and charge asymmetry in the activation loop of Src tyrosine kinases. Proteins 2009, 74:378-389.
3. Bellus G.A., McIntosh I., Smith E.A., Aylsworth A.S., Kaitila I., Horton W.A., Greenhaw G.A., Hecht J.T., Francomano C.A. A recurrent mutation in the tyrosine kinase domain of fibroblast growth factor receptor 3 causes hypochondroplasia. Nat. Genet. 1995, 10:357-359.
4. Bellus G.A., Bamshad M.J., Przylepa K.A., Dorst J., Lee R.R., Hurko O., Jabs E.W., Curry C.J., Wilcox W.R., Lachman R.S., et al. 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. 1999, 85:53-65.
5. Bellus G.A., Spector E.B., Speiser P.W., Weaver C.A., Garber A.T., Bryke C.R., Israel J., Rosengren S.S., Webster M.K., Donoghue D.J., Francomano C.A. Distinct missense mutations of the FGFR3 lys650 codon modulate receptor kinase activation and the severity of the skeletal dysplasia phenotype. Am. J. Hum. Genet. 2000, 67:1411-1421.
6. Berk D.R., Spector E.B., Bayliss S.J. Familial acanthosis nigricans due to K650T FGFR3 mutation. Arch. Dermatol. 2007, 143:1153-1156.
7. Berteotti A., Cavalli A., Branduardi D., Gervasio F.L., Recanatini M., Parrinello M. Protein conformational transitions: the closure mechanism of a kinase explored by atomistic simulations. J.Am. Chem. Soc. 2009, 131:244-250.
8. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 1998, 54:905-921.
9. Castro-Feijóo L., Loidi L., Vidal A., Parajes S., Rosón E., Alvarez A., Cabanas P., Barreiro J., Alonso A., Domínguez F., Pombo M. Hypochondroplasia and Acanthosis nigricans: a new syndrome due to the p.Lys650Thr mutation in the fibroblast growth factor receptor 3 gene?. Eur. J. Endocrinol. 2008, 159:243-249.
10. Chen C.P., Chern S.R., Shih J.C., Wang W., Yeh L.F., Chang T.Y., Tzen C.Y. Prenatal diagnosis and genetic analysis of type I and type II thanatophoric dysplasia. Prenat. Diagn. 2001, 21:89-95.
11. Chen H., Ma J., Li W., Eliseenkova A.V., Xu C., Neubert T.A., Miller W.T., Mohammadi M. A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases. Mol. Cell 2007, 27:717-730.
12. Chen H., Xu C.F., Ma J., Eliseenkova A.V., Li W., Pollock P.M., Pitteloud N., Miller W.T., Neubert T.A., Mohammadi M. A crystallographic snapshot of tyrosine trans-phosphorylation in action. Proc. Natl. Acad. Sci. USA 2008, 105:19660-19665.
13. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 1994, 50:760-763. Collaborative Computational Project, Number 4.
14. Corless C.L., Schroeder A., Griffith D., Town A., McGreevey L., Harrell P., Shiraga S., Bainbridge T., Morich J., Heinrich M.C. PDGFRA mutations in gastrointestinal stromal tumors: frequency, spectrum and invitro sensitivity to imatinib. J.Clin. Oncol. 2005, 23:5357-5364.
15. DeLano W.L. The PyMOL Molecular Graphics System 2002, Schrödinger, LLC. Version 1.5.0.4.
16. Dutt A., Salvesen H.B., Chen T.H., Ramos A.H., Onofrio R.C., Hatton C., Nicoletti R., Winckler W., Grewal R., Hanna M., et al. Drug-sensitive FGFR2 mutations in endometrial carcinoma. Proc. Natl. Acad. Sci. USA 2008, 105:8713-8717.
17. Hubbard S.R. Autoinhibitory mechanisms in receptor tyrosine kinases. Front. Biosci. 2002, 7:d330-d340.
18. Hubbard S.R., Till J.H. Protein tyrosine kinase structure and function. Annu. Rev. Biochem. 2000, 69:373-398.
19. Hunter T. Signaling-2000 and beyond. Cell 2000, 100:113-127.
20. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 1991, 47:110-119.
21. Kabsch W. A solution for the best rotation to relate two sets of vectors. Acta Crystallogr. A 1976, 32:922-923.
22. Kan S.H., Elanko N., Johnson D., Cornejo-Roldan L., Cook J., Reich E.W., Tomkins S., Verloes A., Twigg S.R., Rannan-Eliya S., et al. Genomic screening of fibroblast growth-factor receptor 2 reveals a wide spectrum of mutations in patients with syndromic craniosynostosis. Am. J. Hum. Genet. 2002, 70:472-486.
23. Lemmon M.A., Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010, 141:1117-1134.
24. Li P., Martins I.R., Amarasinghe G.K., Rosen M.K. Internal dynamics control activation and activity of the autoinhibited Vav DH domain. Nat. Struct. Mol. Biol. 2008, 15:613-618.
25. Masterson L.R., Shi L., Metcalfe E., Gao J., Taylor S.S., Veglia G. Dynamically committed, uncommitted, and quenched states encoded in protein kinase A revealed by NMR spectroscopy. Proc. Natl. Acad. Sci. USA 2011, 108:6969-6974.
26. Medeiros F., Corless C.L., Duensing A., Hornick J.L., Oliveira A.M., Heinrich M.C., Fletcher J.A., Fletcher C.D. KIT-negative gastrointestinal stromal tumors: proof of concept and therapeutic implications. Am. J. Surg. Pathol. 2004, 28:889-894.
27. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallogr. A 1994, 50:157-163.
28. Otwinowski Z., Minor W. Processing of X-Ray Diffraction Data Collected in Oscillation Mode 1997, Volume 276. Academic Press, New York.
29. Pellicena P., Kuriyan J. Protein-protein interactions in the allosteric regulation of protein kinases. Curr. Opin. Struct. Biol. 2006, 16:702-709.
30. Pollock P.M., Gartside M.G., Dejeza L.C., Powell M.A., Mallon M.A., Davies H., Mohammadi M., Futreal P.A., Stratton M.R., Trent J.M., Goodfellow P.J. Frequent activating FGFR2 mutations in endometrial carcinomas parallel germline mutations associated with craniosynostosis and skeletal dysplasia syndromes. Oncogene 2007, 26:7158-7162.
31. Rajakulendran T., Sicheri F. Allosteric protein kinase regulation by pseudokinases: insights from STRAD. Sci. Signal. 2010, 3:pe8.
32. Renhowe P.A., Pecchi S., Shafer C.M., Machajewski T.D., Jazan E.M., Taylor C., Antonios-McCrea W., McBride C.M., Frazier K., Wiesmann M., et al. Design, structure-activity relationships and invivo characterization of 4-amino-3-benzimidazol-2-ylhydroquinolin-2-ones: a novel class of receptor tyrosine kinase inhibitors. J.Med. Chem. 2009, 52:278-292.
33. Shan Y., Eastwood M.P., Zhang X., Kim E.T., Arkhipov A., Dror R.O., Jumper J., Kuriyan J., Shaw D.E. Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 2012, 149:860-870.
34. 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., Wasmuth J.J. Thanatophoric dysplasia (types I and II) caused by distinct mutations in fibroblast growth factor receptor 3. Nat. Genet. 1995, 9:321-328.
35. Tavormina P.L., Bellus G.A., Webster M.K., Bamshad M.J., Fraley A.E., McIntosh I., Szabo J., Jiang W., Jabs E.W., Wilcox W.R., et al. 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. 1999, 64:722-731.
36. Vajo Z., Francomano C.A., Wilkin D.J. The molecular and genetic basis of fibroblast growth factor receptor 3 disorders: the achondroplasia family of skeletal dysplasias, Muenke craniosynostosis, and Crouzon syndrome with acanthosis nigricans. Endocr. Rev. 2000, 21:23-39.
37. Volkman B.F., Lipson D., Wemmer D.E., Kern D. Two-state allosteric behavior in a single-domain signaling protein. Science 2001, 291:2429-2433.
38. Webster M.K., D'Avis P.Y., Robertson S.C., Donoghue D.J. 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. 1996, 16:4081-4087.
39. Wilcox W.R., Tavormina P.L., Krakow D., Kitoh H., Lachman R.S., Wasmuth J.J., Thompson L.M., Rimoin D.L. Molecular, radiologic, and histopathologic correlations in thanatophoric dysplasia. Am. J. Med. Genet. 1998, 78:274-281.