Differences in conformational dynamics within the Hsp90 chaperone family reveal mechanistic insights

Frontiers in Molecular Biosciences

Volumn 1, Issue JUN, 2014, Pages

  Graf, Christian ^a,b   Lee, Chung Tien ^a,c   Eva Meier Andrejszki, L ^a   Nguyen, Minh T N ^a   Mayer, Matthias P ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b NOVARTIS PHARMA AG   (Switzerland)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Chaperones; Conformation; Dynamics; Hsp90; Hydrogen exchange mass spectrometry

Indexed keywords

EID: 85041531827     PISSN: None     EISSN: 2296889X     Source Type: Journal    
DOI: 10.3389/fmolb.2014.00004     Document Type: Article

References (56)

1. Ali, J. A., Jackson, A. P., Howells, A. J., and Maxwell, A. (1993). The 43-kilodalton N-terminal fragment of the DNA gyrase B protein hydrolyzes ATP and binds coumarin drugs. Biochemistry 32, 2717-2724. doi: 10.1021/bi00061a033
2. Ali, M. M. U., Roe, S. M., Vaughan, C. K., Meyer, P., Panaretou, B., Piper, P. W., et al. (2006). Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440, 1013-1017. doi: 10.1038/nature04716
3. Andréasson, C., Fiaux, J., Rampelt, H., Mayer, M. P., and Bukau, B. (2008). Hsp110 is a nucleotide-activated exchange factor for Hsp70. J. Biol. Chem. 283, 8877-8884. doi: 10.1074/jbc.M710063200
4. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006). The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201. doi: 10.1093/bioinformatics/bti770
5. Dehner, A., Furrer, J., Richter, K., Schuster, I., Buchner, J., and Kessler, H. (2003). NMR chemical shift perturbation study of the N-terminal domain of Hsp90 upon binding of ADP, AMP-PNP, geldanamycin, and radicicol. Chembiochem 4, 870-877. doi: 10.1002/cbic.200300658
6. DeZwaan, D. C., and Freeman, B. C. (2008). HSP90: the Rosetta stone for cellular protein dynamics? Cell Cycle 7, 1006-1012. doi: 10.4161/cc.7.8.5723
7. Dollins, D. E., Warren, J. J., Immormino, R. M., and Gewirth, D. T. (2007). Structures of GRP94-nucleotide complexes reveal mechanistic differences between the hsp90 chaperones. Mol. Cell 28, 41-56. doi: 10.1016/j.molcel.2007.08.024
8. Fang, Y., Fliss, A. E., Rao, J., and Caplan, A. J. (1998). SBA1 encodes a yeast hsp90 cochaperone that is homologous to vertebrate p23 proteins. Mol. Cell. Biol. 18, 3727-3734
9. Ghaemmaghami, S., Huh, W.-K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., et al. (2003). Global analysis of protein expression in yeast. Nature 425, 737-741. doi: 10.1038/nature02046
10. Graf, C., Stankiewicz, M., Kramer, G., and Mayer, M. P. (2009). Spatially and kinetically resolved changes in the conformational dynamics of the Hsp90 chaperone machine. EMBO J. 28, 602-613. doi: 10.1038/emboj.2008.306
11. Guex, N., Peitsch, M. C., and Schwede, T. (2009). Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 30(Suppl. 1), S162-S173. doi: 10.1002/elps.200900140
12. Harris, S. F., Shiau, A. K., and Agard, D. A. (2004). The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site. Structure 12, 1087-1097. doi: 10.1016/j.str.2004.03.020
13. Hessling, M., Richter, K., and Buchner, J. (2009). Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90. Nat. Struct. Mol. Biol. 16, 287-293. doi: 10.1038/nsmb.1565
14. Hoofnagle, A. N., Resing, K. A., and Ahn, N. G. (2003). Protein analysis by hydrogen exchange mass spectrometry. Annu. Rev. Biophys. Biomol. Struct. 32, 1-25. doi: 10.1146/annurev.biophys.32.110601.142417
15. Johnson, J., Corbisier, R., Stensgard, B., and Toft, D. (1996). The involvement of p23, hsp90, and immunophilins in the assembly of progesterone receptor complexes. J. Steroid Biochem. Mol. Biol. 56, 31-37. doi: 10.1016/0960-0760(95)00221-9
16. Johnson, J. L., and Toft, D. O. (1995). Binding of p23 and hsp90 during assembly with the progesterone receptor. Mol. Endocrinol. 9, 670-678
17. Karagöz, G. E., Duarte, A. M. S., Ippel, H., Uetrecht, C., Sinnige, T., van Rosmalen, M., et al. (2011). N-terminal domain of human Hsp90 triggers binding to the cochaperone p23. Proc. Natl. Acad. Sci. U.S.A. 108, 580-585. doi: 10.1073/pnas.1011867108
18. Kiefer, F., Arnold, K., Künzli, M., Bordoli, L., and Schwede, T. (2009). The SWISS-MODEL Repository and associated resources. Nucleic Acids Res. 37, D387-D392. doi: 10.1093/nar/gkn750
19. Kosano, H., Stensgard, B., Charlesworth, M. C., McMahon, N., and Toft, D. (1998). The assembly of progesterone receptor-hsp90 complexes using purified proteins. J. Biol. Chem. 273, 32973-32979. doi: 10.1074/jbc.273.49.32973
20. Krukenberg, K. A., Southworth, D. R., Street, T. O., and Agard, D. A. (2009). pH-dependent conformational changes in bacterial Hsp90 reveal a Grp94-like conformation at pH 6 that is highly active in suppression of citrate synthase aggregation. J. Mol. Biol. 390, 278-291. doi: 10.1016/j.jmb.2009.04.080
21. Lee, C.-T., Graf, C., Mayer, F. J., Richter, S. M., and Mayer, M. P. (2012). Dynamics of the regulation of Hsp90 by the co-chaperone Sti1. EMBO J. 31, 1518-1528. doi: 10.1038/emboj.2012.37
22. Li, J., Richter, K., and Buchner, J. (2010). Mixed Hsp90-cochaperone complexes are important for the progression of the reaction cycle. Nat. Struct. Mol. Biol. 18, 61-66. doi: 10.1038/nsmb.1965
23. Li, J., Richter, K., Reinstein, J., and Buchner, J. (2013). Integration of the accelerator Aha1 in the Hsp90 co-chaperone cycle. Nat. Struct. Mol. Biol. 20, 326-331. doi: 10.1038/nsmb.2502
24. McLaughlin, S. H., Sobott, F., Yao, Z.-P., Zhang, W., Nielsen, P. R., Grossmann, J. G., et al. (2006). The co-chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. J. Mol. Biol. 356, 746-758. doi: 10.1016/j.jmb.2005.11.085
25. Meyer, P., Prodromou, C., Hu, B., Vaughan, C., Roe, S. M., Panaretou, B., et al. (2003). Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions. Mol. Cell 11, 647-658. doi: 10.1016/S1097-2765(03)00065-0
26. Meyer, P., Prodromou, C., Liao, C., Hu, B., Roe, S. M., Vaughan, C. K., et al. (2004). Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. EMBO J. 23, 1402-1410. doi: 10.1038/sj.emboj.7600141
27. Mickler, M., Hessling, M., Ratzke, C., Buchner, J., and Hugel, T. (2009). The large conformational changes of Hsp90 are only weakly coupled to ATP hydrolysis. Nat. Struct. Mol. Biol. 16, 281-286. doi: 10.1038/nsmb.1557
28. Morishima, Y., Kanelakis, K. C., Murphy, P. J. M., Lowe, E. R., Jenkins, G. J., Osawa, Y., et al. (2003). The hsp90 cochaperone p23 is the limiting component of the multiprotein hsp90/hsp70-based chaperone system in vivo where it acts to stabilize the client protein: hsp90 complex. J. Biol. Chem. 278, 48754-48763. doi: 10.1074/jbc.M309814200
29. Panaretou, B., Siligardi, G., Meyer, P., Maloney, A., Sullivan, J. K., Singh, S., et al. (2002). Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol. Cell 10, 1307-1318. doi: 10.1016/S1097-2765(02)00785-2
30. Pearl, L. H., and Prodromou, C. (2000). Structure and in vivo function of Hsp90. Curr. Opin. Struct. Biol. 10, 46-51. doi: 10.1016/S0959-440X(99)00047-0
31. Pearl, L. H., and Prodromou, C. (2006). Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 75, 271-294. doi: 10.1146/annurev.biochem.75.103004.142738
32. Phillips, J. J., Yao, Z.-P., Zhang, W., McLaughlin, S., Laue, E. D., Robinson, C. V., et al. (2007). Conformational dynamics of the molecular chaperone Hsp90 in complexes with a co-chaperone and anticancer drugs. J. Mol. Biol. 372, 1189-1203. doi: 10.1016/j.jmb.2007.04.059
33. Picard, D. (2006). Chaperoning steroid hormone action. Trends Endocrinol. Metab. 17, 229-235. doi: 10.1016/j.tem.2006.06.003
34. Pratt, W. B., and Toft, D. O. (1997). Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 18, 306-360
35. Prodromou, C. (2012). The 'active life' of Hsp90 complexes. Biochim. Biophys. Acta 1823, 614-623. doi: 10.1016/j.bbamcr.2011.07.020
36. Prodromou, C., Panaretou, B., Chohan, S., Siligardi, G., O'Brien, R., Ladbury, J. E., et al. (2000). The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains. EMBO J. 19, 4383-4392. doi: 10.1093/emboj/19.16.4383
37. Prodromou, C., Roe, S. M., O'Brien, R., Ladbury, J. E., Piper, P. W., and Pearl, L. H. (1997a). Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90, 65-75
38. Prodromou, C., Roe, S. M., Piper, P. W., and Pearl, L. H. (1997b). A molecular clamp in the crystal structure of the N-terminal domain of the yeast Hsp90 chaperone. Nat. Struct Biol. 4, 477-482. doi: 10.1038/nsb0697-477
39. Ratzke, C., Mickler, M., Hellenkamp, B., Buchner, J., and Hugel, T. (2010). Dynamics of heat shock protein 90 C-terminal dimerization is an important part of its conformational cycle. Proc. Natl. Acad. Sci. U.S.A. 107, 16101-16106. doi: 10.1073/pnas.1000916107
40. Ratzke, C., Nguyen, M. N. T., Mayer, M. P., and Hugel, T. (2012). From a ratchet mechanism to random fluctuations evolution of Hsp90's mechanochemical cycle. J. Mol. Biol. 423, 462-471. doi: 10.1016/j.jmb.2012.07.026
41. Richter, K., Muschler, P., Hainzl, O., and Buchner, J. (2001). Coordinated ATP hydrolysis by the Hsp90 dimer. J. Biol. Chem. 276, 33689-33696. doi: 10.1074/jbc.M103832200
42. Richter, K., Walter, S., and Buchner, J. (2004). The Co-chaperone Sba1 connects the ATPase reaction of Hsp90 to the progression of the chaperone cycle. J. Mol. Biol. 342, 1403-1413. doi: 10.1016/j.jmb.2004.07.064
43. Rist, W., Graf, C., Bukau, B., and Mayer, M. P. (2006). Amide hydrogen exchange reveals conformational changes in hsp70 chaperones important for allosteric regulation. J. Biol. Chem. 281, 16493-16501. doi: 10.1074/jbc.M600847200
44. Rist, W., Jørgensen, T. J. D., Roepstorff, P., Bukau, B., and Mayer, M. P. (2003). Mapping temperature-induced conformational changes in the Escherichia coli heat shock transcription factor sigma 32 by amide hydrogen exchange. J. Biol. Chem. 278, 51415-51421. doi: 10.1074/jbc.M307160200
45. Sato, S., Fujita, N., and Tsuruo, T. (2000). Modulation of Akt kinase activity by binding to Hsp90. Proc. Natl. Acad. Sci. U.S.A. 97, 10832-10837. doi: 10.1073/pnas.170276797
46. Shiau, A. K., Harris, S. F., Southworth, D. R., and Agard, D. A. (2006). Structural Analysis of E. coli hsp90 reveals dramatic nucleotide-dependent conformational rearrangements. Cell 127, 329-340. doi: 10.1016/j.cell.2006.09.027
47. Siligardi, G., Hu, B., Panaretou, B., Piper, P. W., Pearl, L. H., and Prodromou, C. (2004). Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle. J. Biol. Chem. 279, 51989-51998. doi: 10.1074/jbc.M410562200
48. Southworth, D. R., and Agard, D. A. (2008). Species-dependent ensembles of conserved conformational states define the Hsp90 chaperone ATPase cycle. Mol. Cell 32, 631-640. doi: 10.1016/j.molcel.2008.10.024
49. Sreedhar, A. S., Kalmár, E., Csermely, P., and Shen, Y.-F. (2004). Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett. 562, 11-15. doi: 10.1016/S0014-5793(04)00229-7
50. Stebbins, C. E., Russo, A. A., Schneider, C., Rosen, N., Hartl, F. U., and Pavletich, N. P. (1997). Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89, 239-250. doi: 10.1016/S0092-8674(00)80203-2
51. Sullivan, W., Stensgard, B., Caucutt, G., Bartha, B., McMahon, N., Alnemri, E. S., et al. (1997). Nucleotides and two functional states of hsp90. J. Biol. Chem. 272, 8007-8012. doi: 10.1074/jbc.272.12.8007
52. Wales, T. E., and Engen, J. R. (2006). Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom. Rev. 25, 158-170. doi: 10.1002/mas.20064
53. Wegele, H., Müller, L., and Buchner, J. (2004). Hsp70 and Hsp90-a relay team for protein folding. Rev. Physiol. Biochem. Pharmacol. 151, 1-44. doi: 10.1007/s10254-003-0021-1
54. Weikl, T., Abelmann, K., and Buchner, J. (1999). An unstructured C-terminal region of the Hsp90 co-chaperone p23 is important for its chaperone function. J. Mol. Biol. 293, 685-691. doi: 10.1006/jmbi.1999.3172
55. Young, J. C., and Hartl, F. U. (2000). Polypeptide release by Hsp90 involves ATP hydrolysis and is enhanced by the co-chaperone p23. EMBO J. 19, 5930-5940. doi: 10.1093/emboj/19.21.5930
56. Young, J. C., Moarefi, I., and Hartl, F. U. (2001). Hsp90: a specialized but essential protein-folding tool. J. Cell Biol. 154, 267-273. doi: 10.1083/jcb.200104079