Quantitative analysis of Hsp90-client interactions reveals principles of substrate recognition

Cell

Volumn 150, Issue 5, 2012, Pages 987-1001

  Taipale, Mikko ^a   Krykbaeva, Irina ^a   Koeva, Martina ^a   Kayatekin, Can ^a   Westover, Kenneth D ^b   Karras, Georgios I ^a   Lindquist, Susan ^a,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 10; CYCLIN DEPENDENT KINASE 6; DASATINIB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; GANETESPIB; HEAT SHOCK PROTEIN 90; IMATINIB; PROTEIN KINASE LCK; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE 38; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL FATE; CONTROLLED STUDY; DIMERIZATION; ENZYME INHIBITION; ENZYME SPECIFICITY; ENZYME STABILITY; GENE MUTATION; HYDROPHOBICITY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; QUANTITATIVE ANALYSIS; THERMODYNAMICS;

EID: 84865695733     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.06.047     Document Type: Article

References (50)

1. F.J. Adrián, Q. Ding, T. Sim, A. Velentza, C. Sloan, Y. Liu, G. Zhang, W. Hur, S. Ding, and P. Manley Allosteric inhibitors of Bcr-abl-dependent cell proliferation Nat. Chem. Biol. 2 2006 95 102
2. M. Barrios-Rodiles, K.R. Brown, B. Ozdamar, R. Bose, Z. Liu, R.S. Donovan, F. Shinjo, Y. Liu, J. Dembowy, and I.W. Taylor High-throughput mapping of a dynamic signaling network in mammalian cells Science 307 2005 1621 1625
3. S. Boulon, B. Pradet-Balade, C. Verheggen, D. Molle, S. Boireau, M. Georgieva, K. Azzag, M.C. Robert, Y. Ahmad, and H. Neel HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II Mol. Cell 39 2010 912 924
4. J. Buchner Bacterial Hsp90 - desperately seeking clients Mol. Microbiol. 76 2010 540 544
5. A.J. Caplan, A.K. Mandal, and M.A. Theodoraki Molecular chaperones and protein kinase quality control Trends Cell Biol. 17 2007 87 92
6. 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
7. A. Citri, D. Harari, G. Shohat, P. Ramakrishnan, J. Gan, S. Lavi, M. Eisenstein, A. Kimchi, D. Wallach, S. Pietrokovski, and Y. Yarden Hsp90 recognizes a common surface on client kinases J. Biol. Chem. 281 2006 14361 14369
8. M. Costanzo, A. Baryshnikova, J. Bellay, Y. Kim, E.D. Spear, C.S. Sevier, H. Ding, J.L. Koh, K. Toufighi, and S. Mostafavi The genetic landscape of a cell Science 327 2010 425 431
9. S. da Rocha Dias, F. Friedlos, Y. Light, C. Springer, P. Workman, and R. Marais Activated B-RAF is an Hsp90 client protein that is targeted by the anticancer drug 17-allylamino-17-demethoxygeldanamycin Cancer Res. 65 2005 10686 10691
10. E.S. Ehrlich, T. Wang, K. Luo, Z. Xiao, A.M. Niewiadomska, T. Martinez, W. Xu, L. Neckers, and X.F. Yu Regulation of Hsp90 client proteins by a Cullin5-RING E3 ubiquitin ligase Proc. Natl. Acad. Sci. USA 106 2009 20330 20335
11. S.F. Falsone, S. Leptihn, A. Osterauer, M. Haslbeck, and J. Buchner Oncogenic mutations reduce the stability of SRC kinase J. Mol. Biol. 344 2004 281 291
12. S.F. Falsone, B. Gesslbauer, F. Tirk, A.M. Piccinini, and A.J. Kungl A proteomic snapshot of the human heat shock protein 90 interactome FEBS Lett. 579 2005 6350 6354
13. S.F. Falsone, B. Gesslbauer, A. Rek, and A.J. Kungl A proteomic approach towards the Hsp90-dependent ubiquitinylated proteome Proteomics 7 2007 2375 2383
14. Y.X. Fan, L. Wong, J. Ding, N.A. Spiridonov, R.C. Johnson, and G.R. Johnson Mutational activation of ErbB2 reveals a new protein kinase autoinhibition mechanism J. Biol. Chem. 283 2008 1588 1596
15. O. Fedorov, B. Marsden, V. Pogacic, P. Rellos, S. Müller, A.N. Bullock, J. Schwaller, M. Sundström, and S. Knapp A systematic interaction map of validated kinase inhibitors with Ser/Thr kinases Proc. Natl. Acad. Sci. USA 104 2007 20523 20528
16. A.A. Fodor, and R.W. Aldrich Influence of conservation on calculations of amino acid covariance in multiple sequence alignments Proteins 56 2004 211 221
17. A. Ghosh, M. Chawla-Sarkar, and D.J. Stuehr Hsp90 interacts with inducible NO synthase client protein in its heme-free state and then drives heme insertion by an ATP-dependent process FASEB J. 25 2011 2049 2060
18. N. Grammatikakis, J.H. Lin, A. Grammatikakis, P.N. Tsichlis, and B.H. Cochran p50(cdc37) acting in concert with Hsp90 is required for Raf-1 function Mol. Cell. Biol. 19 1999 1661 1672
19. P.J. Gray Jr., T. Prince, J. Cheng, M.A. Stevenson, and S.K. Calderwood Targeting the oncogene and kinome chaperone CDC37 Nat. Rev. Cancer 8 2008 491 495
20. R.E. Iacob, J. Zhang, N.S. Gray, and J.R. Engen Allosteric interactions between the myristate- and ATP-site of the Abl kinase PLoS ONE 6 2011 e15929
21. S. Iwasaki, M. Kobayashi, M. Yoda, Y. Sakaguchi, S. Katsuma, T. Suzuki, and Y. Tomari Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes Mol. Cell 39 2010 292 299
22. D.F. Jarosz, and S. Lindquist Hsp90 and environmental stress transform the adaptive value of natural genetic variation Science 330 2010 1820 1824
23. Y. Kadota, K. Shirasu, and R. Guerois NLR sensors meet at the SGT1-HSP90 crossroad Trends Biochem. Sci. 35 2010 199 207
24. K.A. Krukenberg, T.O. Street, L.A. Lavery, and D.A. Agard Conformational dynamics of the molecular chaperone Hsp90 Q. Rev. Biophys. 44 2011 229 255
25. A.K. Mandal, P. Lee, J.A. Chen, N. Nillegoda, A. Heller, S. DiStasio, H. Oen, J. Victor, D.M. Nair, J.L. Brodsky, and A.J. Caplan Cdc37 has distinct roles in protein kinase quality control that protect nascent chains from degradation and promote posttranslational maturation J. Cell Biol. 176 2007 319 328
26. G. Manning, D.B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam The protein kinase complement of the human genome Science 298 2002 1912 1934
27. G. Manning, D.S. Reiner, T. Lauwaet, M. Dacre, A. Smith, Y. Zhai, S. Svard, and F.D. Gillin The minimal kinome of Giardia lamblia illuminates early kinase evolution and unique parasite biology Genome Biol. 12 2011 R66
28. C.N. Pace, and J.M. Scholtz A helix propensity scale based on experimental studies of peptides and proteins Biophys. J. 75 1998 422 427
29. D. Picard Chaperoning steroid hormone action Trends Endocrinol. Metab. 17 2006 229 235
30. W.B. Pratt, Y. Morishima, and Y. Osawa The Hsp90 chaperone machinery regulates signaling by modulating ligand binding clefts J. Biol. Chem. 283 2008 22885 22889
31. C. Queitsch, T.A. Sangster, and S.L. Lindquist Hsp90 as a capacitor of phenotypic variation Nature 417 2002 618 624
32. K. Richter, J. Soroka, L. Skalniak, A. Leskovar, M. Hessling, J. Reinstein, and J. Buchner Conserved conformational changes in the ATPase cycle of human Hsp90 J. Biol. Chem. 283 2008 17757 17765
33. D. Ricketson, U. Hostick, L. Fang, K.R. Yamamoto, and B.D. Darimont A conformational switch in the ligand-binding domain regulates the dependence of the glucocorticoid receptor on Hsp90 J. Mol. Biol. 368 2007 729 741
34. S.L. Rutherford, and S.L. Lindquist Hsp90 as a capacitor for morphological evolution Nature 396 1998 336 342
35. V. Specchia, L. Piacentini, P. Tritto, L. Fanti, R. D'Alessandro, G. Palumbo, S. Pimpinelli, and M.P. Bozzetti Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons Nature 463 2010 662 665
36. M. Taipale, D.F. Jarosz, and S. Lindquist HSP90 at the hub of protein homeostasis: emerging mechanistic insights Nat. Rev. Mol. Cell Biol. 11 2010 515 528
37. S.S. Taylor, and A.P. Kornev Protein kinases: evolution of dynamic regulatory proteins Trends Biochem. Sci. 36 2010 65 77
38. C.K. Vaughan, U. Gohlke, F. Sobott, V.M. Good, M.M. Ali, C. Prodromou, C.V. Robinson, H.R. Saibil, and L.H. Pearl Structure of an Hsp90-Cdc37-Cdk4 complex Mol. Cell 23 2006 697 707
39. W. Xu, X. Yuan, Z. Xiang, E. Mimnaugh, M. Marcu, and L. Neckers Surface charge and hydrophobicity determine ErbB2 binding to the Hsp90 chaperone complex Nat. Struct. Mol. Biol. 12 2005 120 126
40. Y. Xu, M.A. Singer, and S.L. Lindquist Maturation of the tyrosine kinase c-src as a kinase and as a substrate depends on the molecular chaperone Hsp90 Proc. Natl. Acad. Sci. USA 96 1999 109 114
41. J. Yang, N. Campobasso, M.P. Biju, K. Fisher, X.Q. Pan, J. Cottom, S. Galbraith, T. Ho, H. Zhang, and X. Hong Discovery and characterization of a cell-permeable, small-molecule c-Abl kinase activator that binds to the myristoyl binding site Chem. Biol. 18 2011 177 186
42. W. Ying, Z. Du, L. Sun, K.P. Foley, D.A. Proia, R.K. Blackman, D. Zhou, T. Inoue, N. Tatsuta, and J. Sang Ganetespib, a unique triazolone-containing Hsp90 inhibitor, exhibits potent antitumor activity and a superior safety profile for cancer therapy Mol. Cancer Ther. 11 2011 475 484
43. Fedorov, O., Marsden, B., Pogacic, V., Rellos, P., Müller, S., Bullock, A.N., Schwaller, J., Sundström, M., and Knapp, S. (2007). A systematic interaction map of validated kinase inhibitors with Ser/Thr kinases. Proc. Natl. Acad. Sci. USA 104, 20523-20528.
44. Fodor, A.A., and Aldrich, R.W. (2004). Influence of conservation on calculations of amino acid covariance in multiple sequence alignments. Proteins 56, 211-221.
45. Johannessen, C.M., Boehm, J.S., Kim, S.Y., Thomas, S.R., Wardwell, L., Johnson, L.A., Emery, C.M., Stransky, N., Cogdill, A.P., Barretina, J., et al. (2010). COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 468, 968-972.
46. Lamesch, P., Li, N., Milstein, S., Fan, C., Hao, T., Szabo, G., Hu, Z., Venkatesan, K., Bethel, G., Martin, P., et al. (2007). hORFeome v3.1: a resource of human open reading frames representing over 10,000 human genes. Genomics 89, 307-315.
47. Li, W., Bengtson, M.H., Ulbrich, A., Matsuda, A., Reddy, V.A., Orth, A., Chanda, S.K., Batalov, S., and Joazeiro, C.A. (2008). Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. PLoS ONE 3, e1487.
48. 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.
49. Seeliger, M.A., Young, M., Henderson, M.N., Pellicena, P., King, D.S., Falick, A.M., and Kuriyan, J. (2005). High yield bacterial expression of active c-Abl and c-Src tyrosine kinases. Protein Sci. 14, 3135-3139.
50. Vaquerizas, J.M., Kummerfeld, S.K., Teichmann, S.A., and Luscombe, N.M. (2009). A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 10, 252-263.