Designed Hsp90 Heterodimers Reveal an Asymmetric ATPase-Driven Mechanism In Vivo

Molecular Cell

Volumn 53, Issue 2, 2014, Pages 344-350

  Mishra, Parul ^a   Bolon, Daniel N A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DIMER; HEAT SHOCK PROTEIN 90; HETERODIMER;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME MECHANISM; GENE MUTATION; HYDROLYSIS; IN VIVO STUDY; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN SUBUNIT; YEAST;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; DIMERIZATION; FUNGAL PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HYDROLYSIS; MODELS, BIOLOGICAL; PROTEIN ENGINEERING; YEASTS;

EID: 84892840819     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.12.024     Document Type: Article

References (46)

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. Arlander S.J., Felts S.J., Wagner J.M., Stensgard B., Toft D.O., Karnitz L.M. Chaperoning checkpoint kinase 1 (Chk1), an Hsp90 client, with purified chaperones. J. Biol. Chem. 2006, 281:2989-2998.
3. Borkovich K.A., Farrelly F.W., Finkelstein D.B., Taulien J., Lindquist S. hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell. Biol. 1989, 9:3919-3930.
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. Cunningham C.N., Southworth D.R., Krukenberg K.A., Agard D.A. The conserved arginine 380 of Hsp90 is not a catalytic residue, but stabilizes the closed conformation required for ATP hydrolysis. Protein Sci. 2012, 21:1162-1171.
6. Dutta R., Inouye M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 2000, 25:24-28.
7. Gietz R.D., Schiestl R.H., Willems A.R., Woods R.A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 1995, 11:355-360.
8. Grenert J.P., Johnson B.D., Toft D.O. The importance of ATP binding and hydrolysis by hsp90 in formation and function of protein heterocomplexes. J. Biol. Chem. 1999, 274:17525-17533.
9. Hagn F., Lagleder S., Retzlaff M., Rohrberg J., Demmer O., Richter K., Buchner J., Kessler H. Structural analysis of the interaction between Hsp90 and the tumor suppressor protein p53. Nat. Struct. Mol. Biol. 2011, 18:1086-1093.
10. Harris S.F., Shiau A.K., Agard D.A. The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site. Structure 2004, 12:1087-1097.
11. Hartson S.D., Barrett D.J., Burn P., Matts R.L. Hsp90-mediated folding of the lymphoid cell kinase p56lck. Biochemistry 1996, 35:13451-13459.
12. Havranek J.J., Harbury P.B. Automated design of specificity in molecular recognition. Nat. Struct. Biol. 2003, 10:45-52.
13. 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.
14. Hietpas R.T., Jensen J.D., Bolon D.N. Experimental illumination of a fitness landscape. Proc. Natl. Acad. Sci. USA 2011, 108:7896-7901.
15. Hietpas R.T., Bank C., Jensen J.D., Bolon D.N. Shifting fitness landscapes in response to altered environments. Evolution 2013, 67:3512-3522.
16. Jhaveri K., Taldone T., Modi S., Chiosis G. Advances in the clinical development of heat shock protein 90 (Hsp90) inhibitors in cancers. Biochim. Biophys. Acta 2012, 1823:742-755.
17. Jiang L., Mishra P., Hietpas R.T., Zeldovich K.B., Bolon D.N. Latent effects of Hsp90 mutants revealed at reduced expression levels. PLoS Genet. 2013, 9:e1003600.
18. McLaughlin S.H., Ventouras L.A., Lobbezoo B., Jackson S.E. Independent ATPase activity of Hsp90 subunits creates a flexible assembly platform. J. Mol. Biol. 2004, 344:813-826.
19. Meyer P., Prodromou C., Hu B., Vaughan C., Roe S.M., Panaretou B., Piper P.W., Pearl L.H. Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions. Mol. Cell 2003, 11:647-658.
20. 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.
21. Mimnaugh E.G., Chavany C., Neckers L. Polyubiquitination and proteasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J. Biol. Chem. 1996, 271:22796-22801.
22. Nathan D.F., Vos M.H., Lindquist S. In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc. Natl. Acad. Sci. USA 1997, 94:12949-12956.
23. Nørby J.G. Coupled assay of Na+,K+-ATPase activity. Methods Enzymol. 1988, 156:116-119.
24. Obermann W.M., Sondermann H., Russo A.A., Pavletich N.P., Hartl F.U. In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J. Cell Biol. 1998, 143:901-910.
25. 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.
26. Pratt W.B., Toft D.O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 1997, 18:306-360.
27. Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., Pearl L.H. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 1997, 90:65-75.
28. Ratzke C., Berkemeier F., Hugel T. Heat shock protein 90's mechanochemical cycle is dominated by thermal fluctuations. Proc. Natl. Acad. Sci. USA 2012, 109:161-166.
29. Retzlaff M., Hagn F., Mitschke L., Hessling M., Gugel F., Kessler H., Richter K., Buchner J. Asymmetric activation of the hsp90 dimer by its cochaperone aha1. Mol. Cell 2010, 37:344-354.
30. Richter K., Muschler P., Hainzl O., Buchner J. Coordinated ATP hydrolysis by the Hsp90 dimer. J. Biol. Chem. 2001, 276:33689-33696.
31. Röhl A., Rohrberg J., Buchner J. The chaperone Hsp90: changing partners for demanding clients. Trends Biochem. Sci. 2013, 38:253-262.
32. Rudiger S., Freund S.M., Veprintsev D.B., Fersht A.R. CRINEPT-TROSY NMR reveals p53 core domain bound in an unfolded form to the chaperone Hsp90. Proc. Natl. Acad. Sci. USA 2002, 99:11085-11090.
33. Schneider C., Sepp-Lorenzino L., Nimmesgern E., Ouerfelli O., Danishefsky S., Rosen N., Hartl F.U. Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc. Natl. Acad. Sci. USA 1996, 93:14536-14541.
34. Schulte T.W., Blagosklonny M.V., Romanova L., Mushinski J.F., Monia B.P., Johnston J.F., Nguyen P., Trepel J., Neckers L.M. Destabilization of Raf-1 by geldanamycin leads to disruption of the Raf-1-MEK-mitogen-activated protein kinase signalling pathway. Mol. Cell. Biol. 1996, 16:5839-5845.
35. Shiau A.K., Harris S.F., Southworth D.R., Agard D.A. Structural Analysis of E. coli hsp90 reveals dramatic nucleotide-dependent conformational rearrangements. Cell 2006, 127:329-340.
36. 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.
37. Southworth D.R., Agard D.A. Client-loading conformation of the Hsp90 molecular chaperone revealed in the cryo-EM structure of the human Hsp90:Hop complex. Mol. Cell 2011, 42:771-781.
38. Stepanova L., Leng X., Parker S.B., Harper J.W. Mammalian p50Cdc37 is a protein kinase-targeting subunit of Hsp90 that binds and stabilizes Cdk4. Genes Dev. 1996, 10:1491-1502.
39. Street T.O., Lavery L.A., Agard D.A. Substrate binding drives large-scale conformational changes in the Hsp90 molecular chaperone. Mol. Cell 2011, 42:96-105.
40. Street T.O., Lavery L.A., Verba K.A., Lee C.T., Mayer M.P., Agard D.A. Cross-monomer substrate contacts reposition the Hsp90 N-terminal domain and prime the chaperone activity. J. Mol. Biol. 2012, 415:3-15.
41. Taipale M., Krykbaeva I., Koeva M., Kayatekin C., Westover K.D., Karras G.I., Lindquist S. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 2012, 150:987-1001.
42. Vaughan C.K., Gohlke U., Sobott F., Good V.M., Ali M.M., Prodromou C., Robinson C.V., Saibil H.R., Pearl L.H. Structure of an Hsp90-Cdc37-Cdk4 complex. Mol. Cell 2006, 23:697-707.
43. Wayne N., Bolon D.N. Dimerization of Hsp90 is required for in vivo function. Design and analysis of monomers and dimers. J. Biol. Chem. 2007, 282:35386-35395.
44. Wayne N., Lai Y., Pullen L., Bolon D.N. Modular control of cross-oligomerization: analysis of superstabilized Hsp90 homodimers in vivo. J. Biol. Chem. 2010, 285:234-241.
45. Whitesell L., Mimnaugh E.G., De Costa B., Myers C.E., Neckers L.M. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA 1994, 91:8324-8328.
46. Zhao R., Davey M., Hsu Y.C., Kaplanek P., Tong A., Parsons A.B., Krogan N., Cagney G., Mai D., Greenblatt J., et al. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 2005, 120:715-727.