Threonine 22 Phosphorylation Attenuates Hsp90 Interaction with Cochaperones and Affects Its Chaperone Activity

Molecular Cell

Volumn 41, Issue 6, 2011, Pages 672-681

  Mollapour, Mehdi ^a   Tsutsumi, Shinji ^a   Truman, Andrew W ^b,f   Xu, Wanping ^a   Vaughan, Cara K ^c   Beebe, Kristin ^a   Konstantinova, Anna ^a   Vourganti, Srinivas ^a   Panaretou, Barry ^d   Piper, Peter W ^b   Trepel, Jane B ^a   Prodromou, Chrisostomos ^e   Pearl, Laurence H ^e   Neckers, Len ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF LONDON   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF SUSSEX   (United Kingdom)

^f UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CASEIN KINASE II; CELL CYCLE PROTEIN 37; CHAPERONE; HEAT SHOCK PROTEIN 90; MUTANT PROTEIN; PROTEIN AHA1; THREONINE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROPHOBICITY; MUTATION; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; WILD TYPE;

CASEIN KINASE II; CELL CYCLE PROTEINS; CHAPERONINS; FUNGAL PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MOLECULAR CHAPERONES; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; THREONINE;

EID: 79952665421     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.02.011     Document Type: Article

References (37)

1. Ali M.M., Roe S.M., Vaughan C.K., Meyer P., Panaretou B., Piper P.W., Prodromou C., Pearl L.H. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 2006, 440:1013-1017.
2. Bandhakavi S., McCann R.O., Hanna D.E., Glover C.V. A positive feedback loop between protein kinase CKII and Cdc37 promotes the activity of multiple protein kinases. J. Biol. Chem. 2003, 278:2829-2836.
3. Bron P., Giudice E., Rolland J.P., Buey R.M., Barbier P., Díaz J.F., Peyrot V., Thomas D., Garnier C. Apo-Hsp90 coexists in two open conformational states in solution. Biol. Cell 2008, 100:413-425.
4. Cunningham C.N., Krukenberg K.A., Agard D.A. Intra- and intermonomer interactions are required to synergistically facilitate ATP hydrolysis in Hsp90. J. Biol. Chem. 2008, 283:21170-21178.
5. Flom G.A., Lemieszek M., Fortunato E.A., Johnson J.L. Farnesylation of Ydj1 is required for in vivo interaction with Hsp90 client proteins. Mol. Biol. Cell 2008, 19:5249-5258.
6. Garabedian M.J., Yamamoto K.R. Genetic dissection of the signaling domain of a mammalian steroid receptor in yeast. Mol. Biol. Cell 1992, 3:1245-1257.
7. Hawle P., Siepmann M., Harst A., Siderius M., Reusch H.P., Obermann W.M. The middle domain of Hsp90 acts as a discriminator between different types of client proteins. Mol. Cell. Biol. 2006, 26:8385-8395.
8. Hessling M., Richter K., Buchner J. Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90. Nat. Struct. Mol. Biol. 2009, 16:287-293.
9. Kim Y.S., Alarcon S.V., Lee S., Lee M.J., Giaccone G., Neckers L., Trepel J.B. Update on Hsp90 inhibitors in clinical trial. Curr. Top. Med. Chem. 2009, 9:1479-1492.
10. Koulov A.V., Lapointe P., Lu B., Razvi A., Coppinger J., Dong M.Q., Matteson J., Laister R., Arrowsmith C., Yates J.R., Balch W.E. Biological and structural basis for Aha1 regulation of Hsp90 ATPase activity in maintaining proteostasis in the human disease cystic fibrosis. Mol. Biol. Cell 2010, 21:871-884.
11. Lees-Miller S.P., Anderson C.W. Two human 90-kDa heat shock proteins are phosphorylated in vivo at conserved serines that are phosphorylated in vitro by casein kinase II. J. Biol. Chem. 1989, 264:2431-2437.
12. Loo M.A., Jensen T.J., Cui L., Hou Y., Chang X.B., Riordan J.R. Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome. EMBO J. 1998, 17:6879-6887.
13. Louvion J.F., Abbas-Terki T., Picard D. Hsp90 is required for pheromone signaling in yeast. Mol. Biol. Cell 1998, 9:3071-3083.
14. Mayer M.P., Prodromou C., Frydman J. The Hsp90 mosaic: a picture emerges. Nat. Struct. Mol. Biol. 2009, 16:2-6.
15. Mickler M., Hessling M., Ratzke C., Buchner J., Hugel T. The large conformational changes of Hsp90 are only weakly coupled to ATP hydrolysis. Nat. Struct. Mol. Biol. 2009, 16:281-286.
16. Millson S.H., Truman A.W., King V., Prodromou C., Pearl L.H., Piper P.W. A two-hybrid screen of the yeast proteome for Hsp90 interactors uncovers a novel Hsp90 chaperone requirement in the activity of a stress-activated mitogen-activated protein kinase, Slt2p (Mpk1p). Eukaryot. Cell 2005, 4:849-860.
17. Miyata Y., Nishida E. Analysis of the CK2-dependent phosphorylation of serine 13 in Cdc37 using a phospho-specific antibody and phospho-affinity gel electrophoresis. FEBS J. 2007, 274:5690-5703.
18. Miyata Y., Yahara I. The 90-kDa heat shock protein, HSP90, binds and protects casein kinase II from self-aggregation and enhances its kinase activity. J. Biol. Chem. 1992, 267:7042-7047.
19. Mollapour M., Tsutsumi S., Donnelly A.C., Beebe K., Tokita M.J., Lee M.J., Lee S., Morra G., Bourboulia D., Scroggins B.T., et al. Swe1Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function. Mol. Cell 2010, 37:333-343.
20. Murphy S.M., Bergman M., Morgan D.O. Suppression of c-Src activity by C-terminal Src kinase involves the c-Src SH2 and SH3 domains: analysis with Saccharomyces cerevisiae. Mol. Cell. Biol. 1993, 13:5290-5300.
21. Nathan D.F., Lindquist S. Mutational analysis of Hsp90 function: interactions with a steroid receptor and a protein kinase. Mol. Cell. Biol. 1995, 15:3917-3925.
22. Panaretou B., Piper P. Isolation of yeast plasma membranes. Methods Mol. Biol. 1996, 53:117-121.
23. Panaretou B., Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., Pearl L.H. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J. 1998, 17:4829-4836.
24. Panaretou B., Siligardi G., Meyer P., Maloney A., Sullivan J.K., Singh S., Millson S.H., Clarke P.A., Naaby-Hansen S., Stein R., et al. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol. Cell 2002, 10:1307-1318.
25. Pearl L.H., Prodromou C. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 2006, 75:271-294.
26. Pratt W.B., Galigniana M.D., Morishima Y., Murphy P.J. Role of molecular chaperones in steroid receptor action. Essays Biochem. 2004, 40:41-58.
27. Prodromou C., Panaretou B., Chohan S., Siligardi G., O'Brien R., Ladbury J.E., Roe S.M., Piper P.W., Pearl L.H. The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains. EMBO J. 2000, 19:4383-4392.
28. Ratzke C., Mickler M., Hellenkamp B., Buchner J., Hugel T. Dynamics of heat shock protein 90 C-terminal dimerization is an important part of its conformational cycle. Proc. Natl. Acad. Sci. USA 2010, 107:16101-16106.
29. Rose D.W., Wettenhall R.E., Kudlicki W., Kramer G., Hardesty B. The 90-kilodalton peptide of the heme-regulated eIF-2 alpha kinase has sequence similarity with the 90-kilodalton heat shock protein. Biochemistry 1987, 26:6583-6587.
30. Southworth D.R., Agard D.A. Species-dependent ensembles of conserved conformational states define the Hsp90 chaperone ATPase cycle. Mol. Cell 2008, 32:631-640.
31. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11:515-528.
32. Trepel J., Mollapour M., Giaccone G., Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat. Rev. Cancer 2010, 10:537-549.
33. Vaughan C.K., Mollapour M., Smith J.R., Truman A., Hu B., Good V.M., Panaretou B., Neckers L., Clarke P.A., Workman P., et al. Hsp90-dependent activation of protein kinases is regulated by chaperone-targeted dephosphorylation of Cdc37. Mol. Cell 2008, 31:886-895.
34. Wandinger S.K., Suhre M.H., Wegele H., Buchner J. The phosphatase Ppt1 is a dedicated regulator of the molecular chaperone Hsp90. EMBO J. 2006, 25:367-376.
35. Wandinger S.K., Richter K., Buchner J. The Hsp90 chaperone machinery. J. Biol. Chem. 2008, 283:18473-18477.
36. Xu Y., Lindquist S. Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc. Natl. Acad. Sci. USA 1993, 90:7074-7078.
37. Youker R.T., Walsh P., Beilharz T., Lithgow T., Brodsky J.L. Distinct roles for the Hsp40 and Hsp90 molecular chaperones during cystic fibrosis transmembrane conductance regulator degradation in yeast. Mol. Biol. Cell 2004, 15:4787-4797.