Assessing the range of kinase autoinhibition mechanisms in the insulin receptor family

Biochemical Journal

Volumn 448, Issue 2, 2012, Pages 213-220

  Artim, Stephen C ^a   Mendrola, Jeannine M ^a   Lemmon, Mark A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Autoinhibition; Insulin receptor kinase; Receptor tyrosine kinase (RTK); Receptor tyrosine kinase like orphan receptor 2 (Ror2); Tropomyosin receptor kinase A (TrkA); X ray crystallography

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANAPLASTIC LYMPHOMA KINASE; ASPARAGINE; FRIZZLED PROTEIN; GLYCINE; INSULIN RECEPTOR; LEUCINE; NERVE GROWTH FACTOR RECEPTOR; PHENYLALANINE; PROTEIN TYROSINE KINASE; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR 2; SCATTER FACTOR RECEPTOR; TROPOMYOSIN RECEPTOR KINASE A; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME SUBSTRATE; HUMAN; HUMAN TISSUE; MUTATION; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTIGENS, CD; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; HUMANS; MODELS, MOLECULAR; MUTATION; NEOPLASMS; PROTEIN STRUCTURE, QUATERNARY; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; RECEPTOR, INSULIN; RECEPTOR, TRKA; RECOMBINANT PROTEINS;

EID: 84869051908     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121365     Document Type: Article

References (41)

1. Dancey, J. E., Bedard, P. L., Onetto, N. and Hudson, T. J. (2012) The genetic basis for cancer treatment decisions. Cell 148, 409-420
2. Yauch, R. L. and Settleman, J. (2012) Recent advances in pathway-targeted cancer drug therapies emerging from cancer genome analysis. Curr. Opin. Genet. Dev. 22, 45-49
3. Lemmon, M. A. and Schlessinger, J. (2010) Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134
4. Zhang, X., Gureasko, J., Shen, K., Cole, P. A. and Kuriyan, J. (2006) An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125, 1137-1149
5. Sharma, S. V., Bell, D. W., Settleman, J. and Haber, D. A. (2007) Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 7, 169-181
6. Jura, N., Zhang, X., Endres, N. F., Seeliger, M. A., Schindler, T. and Kuriyan, J. (2011) Catalytic control in the EGF receptor and its connection to general kinase regulatory mechanisms. Mol. Cell 42, 9-22
7. Bossi, R. T., Saccardo, M. B., Ardini, E., Menichincheri, M., Rusconi, L., Magnaghi, P., Orsini, P., Avanzi, N., Borgia, A. L., Nesi, M. et al. (2010) Crystal structures of anaplastic lymphoma kinase in complex with ATP competitive inhibitors. Biochemistry 49, 6813-6825
8. Lee, C. C., Jia, Y., Li, N., Sun, X., Ng, K., Ambing, E., Gao, M. Y., Hua, S., Chen, C., Kim, S. et al. (2010) Crystal structure of the ALK (anaplastic lymphoma kinase) catalytic domain. Biochem. J. 430, 425-437
9. Bresler, S. C., Wood, A. C., Haglund, E. A., Courtright, J., Belcastro, L. T., Plegaria, J. S., Cole, K., Toporovskaya, Y., Zhao, H., Carpenter, E. L. et al. (2011) Differential inhibitor sensitivity of anaplastic lymphoma kinase variants found in neuroblastoma. Sci. Transl. Med. 3, 108ra114
10. Manning, G., Whyte, D. B., Martinez, R., Hunter, T. and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298, 1912-1934
11. Morris, S. W., Kirstein, M. N., Valentine, M. B., Dittmer, K. G., Shapiro, D. N., Saltman, D. L. and Look, A. T. (1994) Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science 263, 1281-1284
12. Carpenter, E. L. and Mossé, Y. P. (2012) Targeting ALK in neuroblastoma-preclinical and clinical advancements. Nat. Rev. Clin. Oncol. 9, 391-399
13. Hubbard, S. R., Wei, L., Ellis, L. and Hendrickson, W. A. (1994) Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 372, 746-754
14. Munshi, S., Kornienko, M., Hall, D. L., Reid, J. C., Waxman, L., Stirdivant, S. M., Darke, P. L. and Kuo, L. C. (2002) Crystal structure of the apo, unactivated insulin-like growth factor-1 receptor kinase: implication for inhibitor specificity. J. Biol. Chem. 277, 38797-38802
15. Till, J. H., Becerra, M., Watty, A., Lu, Y., Ma, Y., Neubert, T. A., Burden, S. J. and Hubbard, S. R. (2002) Crystal structure of the MuSK tyrosine kinase: insights into receptor autoregulation. Structure 10, 1187-1196
16. Wang, W., Marimuthu, A., Tsai, J., Kumar, A., Krupka, H. I., Zhang, C., Powell, B., Suzuki, Y., Nguyen, H., Tabrizizad, M. et al. (2006) Structural characterization of autoinhibited c-Met kinase produced by coexpression in bacteria with phosphatase. Proc. Natl. Acad. Sci. U.S.A. 103, 3563-3568
17. Wang, J., Steinbacher, S., Augustin, M., Schreiner, P., Epstein, D., Mulvihill, M. J. and Crew, A. P. (2010) The crystal structure of a constitutively active mutant RON kinase suggests an intramolecular autophosphorylation hypothesis. Biochemistry 49, 7972-7974
18. Brodeur, G. M., Minturn, J. E., Ho, R., Simpson, A. M., Iyer, R., Varela, C. R., Light, J. E., Kolla, V. and Evans, A. E. (2009) Trk receptor expression and inhibition in neuroblastomas. Clin. Cancer Res. 15, 3244-3250
19. Rebagay, G., Yan, S., Liu, C. and Cheung, N. K. (2012) ROR1 and ROR2 in human malignancies: potentials for targeted therapy. Front. Oncol. 2, 34
20. Hammerman, P. S., Sos, M. L., Ramos, A. H., Xu, C., Dutt, A., Zhou, W., Brace, L. E., Woods, B. A., Lin, W., Zhang, J. et al. (2011) Mutations in the DDR2 kinase gene identify a novel therapeutic target in squamous cell lung cancer. Cancer Discovery 1, 78-89
21. Huang, E. J. and Reichardt, L. F. (2003) Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72, 609-642
22. Green, J. L., Kuntz, S. G. and Sternberg, P. W. (2008) Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol. 18, 536-544
23. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
24. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760-763
25. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 2126-2132
26. Brunger, 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. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 54, 905-921
27. 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. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 213-221
28. Winn, M. D., Isupov, M. N. and Murshudov, G. N. (2001) Use of TLS anisotropic displacements in macromolecular refinement. Acta Crystallogr. Sect. D Biol. Crystallogr. 57, 122-133
29. Laskowski, R. A., MacArthur, M. W., Moss, D. S. and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
30. Huse, M. and Kuriyan, J. (2002) The conformational plasticity of protein kinases. Cell 109, 275-282
31. Tartari, C. J., Gunby, R. H., Coluccia, A. M., Sottocornola, R., Cimbro, B., Scapozza, L., Donella-Deana, A., Pinna, L. A. and Gambacorti-Passerini, C. (2008) Characterization of some molecular mechanisms governing autoactivation of the catalytic domain of the anaplastic lymphoma kinase. J. Biol. Chem. 283, 3743-3750
32. Jura, N., Endres, N. F., Engel, K., Deindl, S., Das, R., Lamers, M. H., Wemmer, D. E., Zhang, X. and Kuriyan, J. (2009) Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 137, 1293-1307
33. Albaugh, P., Fan, Y., Mi, Y., Sun, F., Adrian, F., Li, N., Jia, Y., Sarkisova, Y., Kreusch, A., Hood, T. et al. (2012) Discovery of GNF-5837, a selective TRK inhibitor with efficacy in rodent cancer tumor models. ACS Med. Chem. Lett. 3, 140-145
34. Bertrand, T., Kothe, M., Liu, J., Dupuy, A., Rak, A., Berne, P. F., Davis, S., Gladysheva, T., Valtre, C., Crenne, J. Y. and Mathieu, M. (2012) The crystal structures of TrkA and TrkB suggest key regions for achieving selective inhibition. J. Mol. Biol. 423, 439-453
35. Wang, T., Lamb, M. L., Block, M. H., Davies, A. M., Han, Y., Hoffmann, E., Ioannidis, S., Josey, J. A., Liu, Z.-Y., Lyne, P. D. et al. (2012) Discovery of disubstituted imidazo[4,5-b ]pyridines and purines as potent TrkA inhibitors. ACS Med. Chem. Lett. 3, 705-709
36. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797
37. Mohammadi, M., Schlessinger, J. and Hubbard, S. R. (1996) Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell 86, 577-587
38. Shen, J. and Maruyama, I. N. (2011) Nerve growth factor receptor TrkA exists as a preformed, yet inactive, dimer in living cells. FEBS Lett. 585, 295-299
39. Shen, J. and Maruyama, I. N. (2012) Brain-derived neurotrophic factor receptor TrkB exists as a preformed dimer in living cells. J. Mol. Signaling 7, 2
40. Forbes, S. A., Tang, G., Bindal, N., Bamford, S., Dawson, E., Cole, C., Kok, C. Y., Jia, M., Ewing, R., Menzies, A. et al. (2010) COSMIC (the Catalogue of Somatic Mutations in Cancer): a resource to investigate acquired mutations in human cancer. Nucleic Acids Res. 38, D652-D657
41. Hubbard, S. R. (1997) Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 16, 5572-5581