Structural basis for phosphorylation-dependent recruitment of Tel2 to Hsp90 by Pih1

Structure

Volumn 22, Issue 6, 2014, Pages 805-818

  Pal, Mohinder ^a   Morgan, Marc ^a   Phelps, Sarah E L ^a   Roe, S Mark ^a   Parry Morris, Sarah ^a   Downs, Jessica A ^a   Polier, Sigrun ^a,b   Pearl, Laurence H ^a   Prodromou, Chrisostomos ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; HEAT SHOCK PROTEIN 90; PHOSPHOPEPTIDE; PIH 1 PROTEIN; TEL 2 PROTEIN; UNCLASSIFIED DRUG; CHAPERONE; HSP82 PROTEIN, S CEREVISIAE; MULTIPROTEIN COMPLEX; NUCLEAR PROTEIN; PIH1 PROTEIN, S CEREVISIAE; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; TAH1 PROTEIN, S CEREVISIAE; TEL2 PROTEIN, S CEREVISIAE; TELOMERE BINDING PROTEIN;

ARTICLE; BINDING SITE; CHEMICAL ANALYSIS; CRYSTAL STRUCTURE; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TETRATRICOPEPTIDE REPEAT; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE; STATIC ELECTRICITY; X RAY CRYSTALLOGRAPHY;

METAZOA;

CRYSTALLOGRAPHY, X-RAY; HSP90 HEAT-SHOCK PROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STATIC ELECTRICITY; TELOMERE-BINDING PROTEINS;

EID: 84902268012     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.04.001     Document Type: Article

References (38)

1. P.V. Afonine, R.W. Grosse-Kunstleve, N. Echols, J.J. Headd, N.W. Moriarty, M. Mustyakimov, T.C. Terwilliger, A. Urzhumtsev, P.H. Zwart, and P.D. Adams Towards automated crystallographic structure refinement with phenix.refine Acta Crystallogr. D Biol. Crystallogr. 68 2012 352 367
2. M.M. Ali, S.M. Roe, C.K. Vaughan, P. Meyer, B. Panaretou, P.W. Piper, C. Prodromou, and L.H. Pearl Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex Nature 440 2006 1013 1017
3. A.A. Ali, R.M. Jukes, L.H. Pearl, and A.W. Oliver Specific recognition of a multiply phosphorylated motif in the DNA repair scaffold XRCC1 by the FHA domain of human PNK Nucleic Acids Res. 37 2009 1701 1712
4. R. Back, C. Dominguez, B. Rothé, C. Bobo, C. Beaufils, S. Moréra, P. Meyer, B. Charpentier, C. Branlant, F.H. Allain, and X. Manival High-resolution structural analysis shows how Tah1 tethers Hsp90 to the R2TP complex Structure 21 2013 1834 1847
5. S. Boulon, B. Pradet-Balade, C. Verheggen, D. Molle, S. Boireau, M. Georgieva, K. Azzag, M.C. Robert, Y. Ahmad, and H. Neel et al. HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II Mol. Cell 39 2010 912 924
6. H. Dote, W.E. Burgan, K. Camphausen, and P.J. Tofilon Inhibition of hsp90 compromises the DNA damage response to radiation Cancer Res. 66 2006 9211 9220
7. K. Eckert, J.M. Saliou, L. Monlezun, A. Vigouroux, N. Atmane, C. Caillat, S. Quevillon-Chéruel, K. Madiona, M. Nicaise, and S. Lazereg et al. The Pih1-Tah1 cochaperone complex inhibits Hsp90 molecular chaperone ATPase activity J. Biol. Chem. 285 2010 31304 31312
8. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
9. Z. Horejsí, H. Takai, C.A. Adelman, S.J. Collis, H. Flynn, S. Maslen, J.M. Skehel, T. de Lange, and S.J. Boulton CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability Mol. Cell 39 2010 839 850
10. P.V. Hornbeck, I. Chabra, J.M. Kornhauser, E. Skrzypek, and B. Zhang PhosphoSite: A bioinformatics resource dedicated to physiological protein phosphorylation Proteomics 4 2004 1551 1561
11. K.E. Hurov, C. Cotta-Ramusino, and S.J. Elledge A genetic screen identifies the Triple T complex required for DNA damage signaling and ATM and ATR stability Genes Dev. 24 2010 1939 1950
12. N. Izumi, A. Yamashita, H. Hirano, and S. Ohno Heat shock protein 90 regulates phosphatidylinositol 3-kinase-related protein kinase family proteins together with the RUVBL1/2 and Tel2-containing co-factor complex Cancer Sci. 103 2012 50 57
13. B. Jiménez, F. Ugwu, R. Zhao, L. Ortí, T. Makhnevych, A. Pineda-Lucena, and W.A. Houry Structure of minimal tetratricopeptide repeat domain protein Tah1 reveals mechanism of its interaction with Pih1 and Hsp90 J. Biol. Chem. 287 2012 5698 5709
14. W. Kabsch Xds Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
15. Y. Kakihara, and W.A. Houry The R2TP complex: discovery and functions Biochim. Biophys. Acta 1823 2012 101 107
16. M.L. Kilkenny, A.S. Doré, S.M. Roe, K. Nestoras, J.C. Ho, F.Z. Watts, and L.H. Pearl Structural and functional analysis of the Crb2-BRCT2 domain reveals distinct roles in checkpoint signaling and DNA damage repair Genes Dev. 22 2008 2034 2047
17. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
18. E.B. Krissinel, M.D. Winn, C.C. Ballard, A.W. Ashton, P. Patel, E.A. Potterton, S.J. McNicholas, K.D. Cowtan, and P. Emsley The new CCP4 Coordinate Library as a toolkit for the design of coordinate-related applications in protein crystallography Acta Crystallogr. D Biol. Crystallogr. 60 2004 2250 2255
19. S.H. Millson, C.K. Vaughan, C. Zhai, M.M. Ali, B. Panaretou, P.W. Piper, L.H. Pearl, and C. Prodromou Chaperone ligand-discrimination by the TPR-domain protein Tah1 Biochem. J. 413 2008 261 268
20. R.M. Morgan, L.C. Hernández-Ramírez, G. Trivellin, L. Zhou, S.M. Roe, M. Korbonits, and C. Prodromou Structure of the TPR domain of AIP: lack of client protein interaction with the C-terminal α-7 helix of the TPR domain of AIP is sufficient for pituitary adenoma predisposition PLoS ONE 7 2012 e53339
21. H. Omran, D. Kobayashi, H. Olbrich, T. Tsukahara, N.T. Loges, H. Hagiwara, Q. Zhang, G. Leblond, E. O'Toole, and C. Hara et al. Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins Nature 456 2008 611 616
22. A. Paci, X.H. Liu, H. Huang, A. Lim, W.A. Houry, and R. Zhao The stability of the small nucleolar ribonucleoprotein (snoRNP) assembly protein Pih1 in Saccharomyces cerevisiae is modulated by its C terminus J. Biol. Chem. 287 2012 43205 43214
23. L.H. Pearl Hsp90 and Cdc37 - a chaperone cancer conspiracy Curr. Opin. Genet. Dev. 15 2005 55 61
24. L.H. Pearl, C. Prodromou, and P. Workman The Hsp90 molecular chaperone: an open and shut case for treatment Biochem. J. 410 2008 439 453
25. S. Polier, R.S. Samant, P.A. Clarke, P. Workman, C. Prodromou, and L.H. Pearl ATP-competitive inhibitors block protein kinase recruitment to the Hsp90-Cdc37 system Nat. Chem. Biol. 9 2013 307 312
26. C. Prodromou, G. Siligardi, R. O'Brien, D.N. Woolfson, L. Regan, B. Panaretou, J.E. Ladbury, P.W. Piper, and L.H. Pearl Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones EMBO J. 18 1999 754 762
27. C. Prodromou, B. Panaretou, S. Chohan, G. Siligardi, R. O'Brien, J.E. Ladbury, S.M. Roe, P.W. Piper, and L.H. Pearl The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains EMBO J. 19 2000 4383 4392
28. 1) Mol. Cell 51 2013 723 736
29. C. Scheufler, A. Brinker, G. Bourenkov, S. Pegoraro, L. Moroder, H. Bartunik, F.U. Hartl, and I. Moarefi Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine Cell 101 2000 199 210
30. cdc37 J. Biol. Chem. 277 2002 20151 20159
31. H. Takai, Y. Xie, T. de Lange, and N.P. Pavletich Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes Genes Dev. 24 2010 2019 2030
32. A. Tarkar, N.T. Loges, C.E. Slagle, R. Francis, G.W. Dougherty, J.V. Tamayo, B. Shook, M. Cantino, D. Schwartz, C. Jahnke UK10K DYX1C1 is required for axonemal dynein assembly and ciliary motility Nat. Genet. 45 2013 995 1003
33. J. Te, L. Jia, J. Rogers, A. Miller, and S.D. Hartson Novel subunits of the mammalian Hsp90 signal transduction chaperone J. Proteome Res. 6 2007 1963 1973
34. 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
35. R. Yamamoto, M. Hirono, and R. Kamiya Discrete PIH proteins function in the cytoplasmic preassembly of different subsets of axonemal dyneins J. Cell Biol. 190 2010 65 71
36. M. Zhang, M. Windheim, S.M. Roe, M. Peggie, P. Cohen, C. Prodromou, and L.H. Pearl Chaperoned ubiquitylation - crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex Mol. Cell 20 2005 525 538
37. M. Zhang, M. Botër, K. Li, Y. Kadota, B. Panaretou, C. Prodromou, K. Shirasu, and L.H. Pearl Structural and functional coupling of Hsp90- and Sgt1-centred multi-protein complexes EMBO J. 27 2008 2789 2798
38. R. Zhao, M. Davey, Y.C. Hsu, P. Kaplanek, A. Tong, A.B. Parsons, N. Krogan, G. Cagney, D. Mai, and J. Greenblatt et al. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone Cell 120 2005 715 727