C-terminal phosphorylation of Hsp70 and Hsp90 regulates alternate binding to co-chaperones CHIP and HOP to determine cellular protein folding/degradation balances

Oncogene

Volumn 32, Issue 25, 2013, Pages 3101-3110

  Muller, P ^a   Ruckova, E ^a   Halada, P ^b   Coates, P J ^c   Hrstka, R ^a   Lane, D P ^d   Vojtesek, B ^a  

^a MASARYK MEMORIAL CANCER INSTITUTE   (Czech Republic)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d AGENCY FOR SCIENCE   (Singapore)

Author keywords

chaperone; CHIP; folding; HOP; Hsp70; Hsp90

Indexed keywords

CELL PROTEIN; CHAPERONE; CHAPERONE CHIP; CHAPERONE HOP; CYTOKERATIN 1; CYTOKERATIN 2; GLYCOGEN SYNTHASE KINASE 3BETA; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CANCER CELL; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MEDIATOR; NUCLEOTIDE SEQUENCE; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HEAT-SHOCK PROTEINS; HEK293 CELLS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN FOLDING; RNA, MESSENGER; UBIQUITIN-PROTEIN LIGASES;

EID: 84879412911     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.314     Document Type: Article

References (31)

1. Buchner J. Hsp90 & Co-a holding for folding. Trends Biochem Sci 1999; 24: 136-141.
2. Mayer MP, Bukau B. Molecular chaperones: the busy life of Hsp90. Curr Biol 1999; 9: R322-R325.
3. Taipale M, Jarosz DF, Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 2010; 11: 515-528.
4. Young JC, Agashe VR, Siegers K, Hartl FU. Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 2004; 5: 781-791.
5. Hohfeld J, Cyr DM, Patterson C. From the cradle to the grave: molecular cha-perones that may choose between folding and degradation. EMBO Rep 2001; 2: 885-890.
6. Krukenberg KA, Street TO, Lavery LA, Agard DA. Conformational dynamics of the molecular chaperone Hsp90. Q Rev Biophys 2011; 44: 229-255.
7. Liu FH, Wu SJ, Hu SM, Hsiao CD, Wang C. Specific interaction of the 70-kDa heat shock cognate protein with the tetratricopeptide repeats. J Biol Chem 1999; 274: 34425-34432.
8. Russell LC, Whitt SR, Chen MS, Chinkers M. Identification of conserved residues required for the binding of a tetratricopeptide repeat domain to heat shock protein 90. J Biol Chem 1999; 274: 20060-20063.
9. Ramsey AJ, Russell LC, Whitt SR, Chinkers M. Overlapping sites of tetratricopeptide repeat protein binding and chaperone activity in heat shock protein 90. J Biol Chem 2000; 275: 17857-17862.
10. Peterson LB, Blagg BS. To fold or not to fold: modulation and consequences of Hsp90 inhibition. Future Med Chem 2009; 1: 267-283.
11. Hutt D, Balch WE. Cell biology. The proteome in balance. Science 2010; 329: 766-767.
12. Meggio F, Pinna LA. One-thousand-and-one substrates of protein kinase CK2? FASEB J 2003; 17: 349-368.
13. Blom N, Gammeltoft S, Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 1999; 294: 1351-1362.
14. Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H et al. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 2000; 101: 199-210.
15. Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, Prodromou C et al. Chaperoned ubiquitylation-crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol Cell 2005; 20: 525-538.
16. Brinker A, Scheufler C, Von Der Mulbe F, Fleckenstein B, Herrmann C, Jung G et al. Ligand discrimination by TPR domains. Relevance and selectivity of EEVD-recognition in Hsp70 x Hop x Hsp90 complexes. J Biol Chem 2002; 277: 19265-19275.
17. Grummt I. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 2003; 17: 1691-1702.
18. Muller P, Hrstka R, Coomber D, Lane DP, Vojtesek B. Chaperone-dependent stabilization and degradation of p53 mutants. Oncogene 2008; 27: 3371-3383.
19. Kajiro M, Hirota R, Nakajima Y, Kawanowa K, So-ma K, Ito I et al. The ubiquitin ligase CHIP acts as an upstream regulator of oncogenic pathways. Nat Cell Biol 2009; 11: 312-319.
20. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004; 6: 1-6.
21. Miyata Y. Protein kinase CK2 in health and disease: CK2: the kinase controlling the Hsp90 chaperone machinery. Cell Mol Life Sci 2009; 66: 1840-1849.
22. Lees-Miller SP, Anderson CW. The human double-stranded DNA-activated protein kinase phosphorylates the 90-kDa heat-shock protein, hsp90 alpha at two NH2-terminal threonine residues. J Biol Chem 1989; 264: 17275-17280.
23. Mollapour M, Tsutsumi S, Donnelly AC, Beebe K, Tokita MJ, Lee MJ et al. Swe1-Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function. Mol Cell 2010; 37: 333-343.
24. Kundrat L, Regan L. Balance between folding and degradation for Hsp90-dependent client proteins: a key role for CHIP. Biochemistry 2010; 49: 7428-7438.
25. Li J, Soroka J, Buchner J. The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochim Biophys Acta 2011; 1823: 624-635.
26. Mayer MP. Gymnastics of molecular chaperones. Mol Cell 2010; 39: 321-331.
27. Workman P. Altered states: selectively drugging the Hsp90 cancer chaperone. Trends Mol Med 2004; 10: 47-51.
28. Powers MV, Jones K, Barillari C, Westwood I, van Montfort RL, Workman P. Targeting HSP70: the second potentially druggable heat shock protein and molecular chaperone? Cell Cycle 2010; 9: 1542-1550.
29. Pacey S, Wilson RH, Walton M, Eatock MM, Hardcastle A, Zetterlund A et al. A phase I study of the heat shock protein 90 inhibitor alvespimycin (17-DMAG) given intravenously to patients with advanced solid tumors. Clin Cancer Res 2011; 17: 1561-1570.
30. Keefe AD, Wilson DS, Seelig B, Szostak JW. One-step purification of recombinant proteins using a nanomolar-affinity streptavidin-binding peptide, the SBP-Tag. Protein Expr Purif 2001; 23: 440-446.
31. Zhang R, Mayhood T, Lipari P, Wang Y, Durkin J, Syto R et al. Fluorescence polarization assay and inhibitor design for MDM2/p53 interaction. Anal Biochem 2004; 331: 138-146.