Structural-Thermodynamic Relationships of Interactions in the N-Terminal ATP-Binding Domain of Hsp90

Journal of Molecular Biology

Volumn 392, Issue 4, 2009, Pages 923-936

  Nilapwar, Sanjay ^a   Williams, Eleanor ^a   Fu, Christopher ^a   Prodromou, Christosmos ^b   Pearl, Laurence H ^b   Williams, Mark A ^c   Ladbury, John E ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

cancer therapeutics; change in heat capacity; inhibitor; isothermal titration calorimetry; nucleotide binding

Indexed keywords

17 DEMETHOXY 17 (2 DIMETHYLAMINOETHYLAMINO)GELDANAMYCIN; ADENOSINE TRIPHOSPHATE; ANSAMYCIN DERIVATIVE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; TANESPIMYCIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENTHALPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TEMPERATURE DEPENDENCE; THERMODYNAMICS;

EID: 69749124536     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.07.041     Document Type: Article

References (57)

1. Pearl L.H., and Prodromou C. Structure and in vivo function of Hsp90. Curr. Opin. Struct. Biol. 10 (2000) 46-51
2. Pratt W.B. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 3 (1997) 306-360
3. Pratt W.B. The role of the hsp90-based chaperone system; involvement in signal transduction by nuclear receptors and receptors signaling via MAP kinase. Annu. Rev. Pharmacol. Toxicol. 37 (1997) 297-326
4. Pratt W.B. The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc. Soc. Exp. Biol. Med. 217 (1998) 420-434
5. Pearl L.H. Hsp90 and Cdc37-a chaperone cancer conspiracy. Curr. Opin. Genet. Dev. 15 (2005) 55-61
6. Piper P.W. The Hsp90 chaperone as a promising drug target. Curr. Opin. Invest. Drugs 2 (2001) 1606-1610
7. Drysdale M.J., Brough P.A., Massey A., Rugaard Jensen M., and Schoepfer J. Targeting Hsp90 for the treatment of cancer. Curr. Opin. Drug Discovery Dev. 9 (2006) 483-495
8. Smith J.R., and Workman P. Targeting the cancer chaperone Hsp90. Drug Discovery Today 4 (2008) 219-227
9. Whitesall L., and Lindquist S.L. Hsp90 and the chaperoning of cancer. Nat. Rev. Cancer 5 (2005) 761-772
10. Panaretou B., Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., and Pearl L.H. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J. 17 (1998) 4829-4836
11. Obermann W.M.J., Sonderman H., Russo A.A., Pavletich N.P., and Hartl F.U. In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J. Cell Biol. 143 (1998) 901-910
12. c-erbB-2 receptor protein by geldanamycin. J. Biol. Chem. 271 (1996) 4974-4977
13. Schneider C., SeppLorenzino L., Nimmesgem E., Ouerfelli O., Danishefsky S., Rosen N., and Hartl F.U. Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc. Natl Acad. Sci. USA 93 (1996) 14536-14541
14. Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., and Pearl L.H. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90 (1997) 65-75
15. Maloney A., and Workman P. HSP90 as a new therapeutic target for cancer therapy: the story unfolds. Exp. Opin. Biol. Ther. 2 (2002) 3-14
16. Stebbins C.E., Russo A.A., Schneider C., Rosen N., Hartl F.U., and Pavletich N.P. Crystal structure of an Hsp90-geldanamycin complex: targeting of the protein chaperone by an antitumor agent. Cell 89 (1997) 239-240
17. Roe S.M., Prodromou C., O'Brien R., Ladbury J.E., Piper P.W., and Pearl L.H. Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. J. Med. Chem. 42 (1999) 260-266
18. Ali M.M.U., Roe S.M., Vaughan C.K., Meyer P., Panaretou B., Piper P.W., et al. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440 (2006) 1013-1017
19. Cooper A., Johnson C.M., Lakey J.H., and Nöllmann M. Heat does not come in different colours: entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions. Biophys. Chem. 93 (2001) 215-230
20. Cooper A. Heat capacity effects in protein folding and ligand binding: a re-evaluation of the role of water in biomolecular thermodynamics. Biophys. Chem. 115 (2005) 89-97
21. Ladbury J.E., and Williams M.A. The extended interface: measuring non-local effects in biomolecular interactions. Curr. Opin. Struct. Biol. 14 (2004) 562-569
22. Ladbury J.E., Wright J.G., Sturtevant J.M., and Sigler P.B. A thermodynamic study of the trp repressor-operator interaction. J. Mol. Biol. 238 (1994) 669-681
23. Morton C.J., and Ladbury J.E. Water-mediated protein-DNA interactions: the relationship of thermodynamics to structural detail. Protein Sci. 5 (1996) 2115-2118
24. Holdgate G.A., Tunnicliffe A., Ward W.H.J., Weston S.A., Rosenbrock G., Barth P.T., et al. The entropic penalty of ordered water accounts fora thermodynamic and crystallographic study. Biochemistry 36 (1997) 9663-9673
25. Bergqvist S., Williams M.A., O'Brien R., and Ladbury J.E. Heat capacity effects of water molecules and ions at a protein-DNA interface. J. Mol. Biol. 336 (2004) 829-842
26. Stegmann C.M., Seeliger D., Sheldrick G.M., de Groot B.L., and Wahl M.C. The thermodynamic influence of trapped water molecules on a protein-ligand interaction. Angew. Chem. Int. Ed. 48 (2009) 5207-5210
27. Sturtevant J.M. Heat capacity and entropy in processes involving proteins. Proc. Natl Acad. Sci. USA 74 (1977) 2236-2240
28. Prodromou C., Roe S.M., Piper P.W., and Pearl L.H. A molecular clamp in the crystal structure of the N-terminal domain of the yeast Hsp90 chaperone. Nat. Struct. Biol. 4 (1997) 477-482
29. Baker B.M., and Murphy K.P. Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys. J. 71 (1996) 2049-2055
30. Cohn M., and Hughes Jr. T.R. Phosphorous magnetic resonance spectra of adenosine di- and triphosphate: I. Effect of pH. J. Biol. Chem. 235 (1960) 3250-3253
31. Boukhalfa H., Lewis J.G., and Crumbliss A.L. Beryllium(II) binding to ATP and ADP: potentiometric determination of the thermodynamic constants and implications for in vivo toxicity. BioMetals 17 (2004) 105-109
32. Oda M., Furukawa K., Ogata K., Sarai A., and Nakamura H. Thermodynamics of specific and non-specific DNA binding by the c-Myb DNA-binding domain. J. Mol. Biol. 276 (1998) 571-590
33. Spolar R.S., Livingstone J.R., and Record Jr. M.T. Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water. Biochemistry 31 (1992) 3947-3955
34. Spolar R.S., and Record J.M.T. Coupling of local folding to site-specific binding of proteins to DNA. Science 263 (1994) 777-784
35. Jez J.M., Chen J.C.-H., Rastelli G., Stroud R.M., and Santi D.V. Crystal structure and molecular modelling of 17-DMAG in complex with human Hsp90. Chem. Biol. 10 (2003) 361-368
36. Salek R.M., Williams M.A., Prodromou C., Pearl L.H., and Ladbury J.E. Backbone resonance assignments of the 25 kD N-terminal ATPase domain from the Hsp90 chaperone. J. Biomol. NMR 23 (2002) 327-328
37. Dehner A., Furrer J., Richter K., Schuster I., Buchner J., and Kessler H. NMR chemical shift perturbation study of the N-terminal domain of Hsp90 upon binding of ADP, AMPPNP, geldanamycin and radicicol. ChemBioChem 4 (2003) 870-877
38. Luque I., Mayorga O.L., and Freire E. Structure-based thermodynamic scale of alpha-helix propensities in amino acids. Biochemistry 35 (1996) 13681-13688
39. Prodromou C., Panaretou B., Chohan S., Siligardi G., O'Brien R., Ladbury J.E., et al. The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains. EMBO J. 19 (2000) 4383-4392
40. Tribolet R., and Sigel H. Influence of the protonation degree on the self-association properties of adenosine 5′-triphosphate (ATP). Eur. J. Biochem. 170 (1988) 617-626
41. Sheller K.H., and Sigel H. A proton nuclear magnetic resonance study of purine and pyrimidine nucleoside 5′-diphosphates. Extent of macrochelate formation in monomeric metal ion complexes and promotion of self-stacking by metal ions. J. Am. Chem. Soc. 105 (1983) 5891-5900
42. 15N NMR. J. Org. Chem. 67 (2002) 790-802
43. Hovey J.K., and Tremaine P.R. Thermodynamics of the complexes of aqueous iron(III), aluminum, and several divalent cations with EDTA: heat capacities, volumes, and variations in stability with temperature. J. Phys. Chem. 89 (1985) 5541-5549
44. Colombo G., Morra G., Meli M., and Verkhivker G. Understanding ligand-based modulation of the Hsp90 molecular chaperone dynamics at atomic resolution. Proc. Natl Acad. USA 105 (2008) 7976-7981
45. Graf C., Stankiewicz M., Kramer G., and Mayer M. Spatially and kinetically resolved changes in the conformational dynamics of the Hsp90 chaperone machine. EMBO J. 28 (2009) 602-613
46. Jung H.-I., Bowden S.J., Cooper A., and Perham R.N. Thermodynamic analysis of the binding of component enzymes in the assembly of the pyruvate dehydrogenase multienzyme complex of Bacillus stearothermophilus. Protein Sci. 11 (2002) 1091-1100
47. Ladbury J.E. Counting the calories to stay in the groove. Structure 3 (1995) 635-639
48. Ladbury J.E., and Chowdhry B.Z. Sensing the heat: the application of isothermal titration calorimetry to thermodynamic studies of biomolecular interactions. Chem. Biol. 3 (1996) 791-801
49. Wiseman T., Williston S., Brandts J.F., and Lin L.N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179 (1989) 131-137
50. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPIPE-a multidimensional spectral processing system based on UNIX PIPES. J. Biomol. NMR 6 (1995) 277-293
51. Kraulis P.J. ANSIG: a program for the assignment of protein H 2D NMR spectra by interactive computer graphics. J. Magn. Reson. 84 (1989) 627-633
52. Provencher S.W., and Glockner J. Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20 (1981) 33-37
53. Hubbard, S. J. & Thornton, J. M. (1993). 'NACCESS' Computer Program. Department of Biochemistry and Molecular Biology, University College London. http://wolf.bms.umist.ac.uk/naccess/.
54. Lee B., and Richards F.M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55 (1971) 379-400
55. Habermann S.M., and Murphy K.P. Energetics of hydrogen bonding in proteins: a model compound study. Protein Sci. 5 (1996) 1229-1239
56. Garcia-Hernandez E., Zubillaga R.A., Chavelas-Adame E.A., Vazquez-Contreras E., Rojo-Dominguez A., and Costas M. Structural energetics of protein-carbohydrate interactions: insights derived from the study of lysozyme binding to its natural saccharide inhibitors. Protein Sci. 12 (2003) 135-142
57. Abraham M.H., and Marcus Y. The thermodynamics of solvation ions: 1. The heat capacity of hydration at 298.15 K. J. Chem. Soc., Faraday Trans. 82 (1986) 3255-3274