Measurement of nanomolar dissociation constants by titration calorimetry and thermal shift assay - Radicicol binding to Hsp90 and ethoxzolamide binding to CAII

International Journal of Molecular Sciences

Volumn 10, Issue 6, 2009, Pages 2662-2680

  Zubriene, Asta ^a   Matuliene, Jurgita ^a   Baranauskiene, Lina ^a   Jachno, Jelena ^a   Torresan, Jolanta ^a   Michailoviene, Vilma ^a   Cimmperman, Piotras ^a   Matulis, Daumantas ^a  

^a VILNIUS UNIVERSITY   (Lithuania)

Author keywords

Carbonic anhydrase; Ethoxzolamide; Hsp90; Isothermal titration calorimetry; Proteinligand binding; Radicicol; Thermal shift assay

Indexed keywords

CARBONATE DEHYDRATASE II; ETHOXZOLAMIDE; HEAT SHOCK PROTEIN 90;

ARTICLE; CALORIMETRY; DIFFERENTIAL SCANNING CALORIMETRY; ENTHALPY; PROTEIN STABILITY; TITRIMETRY;

CARBONIC ANHYDRASE; ETHOXZOLAMIDE; HSP90; ISOTHERMAL TITRATION CALORIMETRY; PROTEIN-LIGAND BINDING; RADICICOL; THERMAL SHIFT ASSAY;

CALORIMETRY; CARBONIC ANHYDRASE II; ETHOXZOLAMIDE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; KINETICS; LIGANDS; MACROLIDES; MODELS, THEORETICAL; PROTEIN BINDING; THERMODYNAMICS;

EID: 67649644363     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms10062662     Document Type: Article

References (44)

1. Sigurskjold, B.W. Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal. Biochem. 2000, 277 (2), 260-266.
2. Velazquez-Campoy, A.; Freire, E. Isothermal titration calorimetry to determine association constants for high-affinity ligands. Nat. Protoc. 2006, 1 (1), 186-191.
3. Lo, M.C.; Aulabaugh, A.; Jin, G.; Cowling, R.; Bard, J.; Malamas, M.; Ellestad, G. Evaluation of fluorescence-based thermal shift assays for hit identification in drug discovery. Anal. Biochem. 2004, 332 (1), 153-159.
4. Niesen, F.H.; Berglund, H.; Vedadi, M. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2007, 2 (9), 2212-2221.
5. Pantoliano, M.W.; Petrella, E.C.; Kwasnoski, J.D.; Lobanov, V.S.; Myslik, J.; Graf, E.; Carver, T.; Asel, E.; Springer, B.A.; Lane, P.; Salemme, F.R. High-density miniaturized thermal shift assays as a general strategy for drug discovery. J. Biomol. Screen. 2001, 6 (6), 429-440.
6. Todd, M.J.; Salemme, F.R. Direct binding assays for pharma screening. Genetic Eng. News 2003, 23 (3), 28-29.
7. Cimmperman, P.; Baranauskiene, L.; Jachimoviciute, S.; Jachno, J.; Torresan, J.; Michailoviene, V.; Matuliene, J.; Sereikaite, J.; Bumelis, V.; Matulis, D. A quantitative model of thermal stabilization and destabilization of proteins by ligands. Biophys. J. 2008, 95 (7), 3222-3231.
8. Mezzasalma, T.M.; Kranz, J.K.; Chan, W.; Struble, G.T.; Schalk-Hihi, C.; Deckman, I.C.; Springer, B.A.; Todd, M.J. Enhancing recombinant protein quality and yield by protein stability profiling. J. Biomol. Screen. 2007, 12 (3), 418-428.
9. Ericsson, U.B.; Hallberg, B.M.; Detitta, G.T.; Dekker, N.; Nordlund, P. Thermofluor-based highthroughput stability optimization of proteins for structural studies. Anal. Biochem. 2006, 357 (2), 289-298.
10. Brandts, J.F.; Lin, L.N. Study of strong to ultratight protein interactions using differential scanning calorimetry. Biochemistry 1990, 29 (29), 6927-6940.
11. Shrake, A.; Ross, P.D. Biphasic denaturation of human albumin due to ligand redistribution during unfolding. J. Biol. Chem. 1988, 263 (30), 15392-15399.
12. Anderson, S.R.; Weber, G. Fluorescence polarization of the complexes of 1-anilino-8-naphthalenesulfonate with bovine serum albumin. Evidence for preferential orientation of the ligand. Biochemistry 1969, 8 (1), 371-377.
13. Weber, G.; Laurence, D.J. Fluorescent indicators of adsorption in aqueous solution and on the solid phase. Process Biochem. 1954, 56 (325th Meeting), xxxi.
14. Slavik, J.; Horak, J.; Rihova, L.; Kotyk, A. Anilinonaphthalene sulfonate fluorescence and amino acid transport in yeast. J. Membr. Biol. 1982, 64 (3), 175-179.
15. Matulis, D.; Baumann, C.G.; Bloomfield, V.A.; Lovrien, R.E. 1-Anilino-8-naphthalene sulfonate as a protein conformational tightening agent. Biopolymers 1999, 49 (6), 451-458.
16. Matulis, D.; Lovrien, R. 1-Anilino-8-naphthalene sulfonate anion-protein binding depends primarily on ion pair formation. Biophys. J. 1998, 74 (1), 422-429.
17. Matulis, D.; Kranz, J.K.; Salemme, F.R.; Todd, M.J. Thermodynamic stability of carbonic anhydrase: Measurements of binding affinity and stoichiometry using ThermoFluor. Biochemistry 2005, 44 (13), 5258-5266.
18. Maroney, A.C.; Marugan, J.J.; Mezzasalma, T.M.; Barnakov, A.N.; Garrabrant, T.A.; Weaner, L.E.; Jones, W.J.; Barnakova, L.A.; Koblish, H.K.; Todd, M.J.; Masucci, J.A.; Deckman, I.C.; Galemmo, R.A., Jr.; Johnson, D.L. Dihydroquinone ansamycins: Toward resolving the conflict between low in vitro affinity and high cellular potency of geldanamycin derivatives. Biochemistry 2006, 45 (17), 5678-5685.
19. Shrake, A.; Ross, P.D. Origins and consequences of ligand-induced multiphasic thermal protein denaturation. Biopolymers 1992, 32 (8), 925-940.
20. Shrake, A.; Ross, P.D. Ligand-induced biphasic protein denaturation. J. Biol. Chem. 1990, 265 (9), 5055-5059.
21. Wandinger, S.K.; Richter, K.; Buchner, J. The Hsp90 chaperone machinery. J. Biol. Chem. 2008, 283 (27), 18473-18477.
22. Richter, K.; Meinlschmidt, B.; Buchner, J. Hsp90: From dispensable heat shock protein to global player. In Protein Folding Handbook; Buchner, J., Kiefhaber, T., Eds.; Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, 2005; pp. 768-829.
23. Pearl, L.H.; Prodromou, C.; Workman, P. The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem. J. 2008, 410 (3), 439-453.
24. Blagg, B.S.; Kerr, T.D. Hsp90 inhibitors: small molecules that transform the Hsp90 protein folding machinery into a catalyst for protein degradation. Med. Res. Rev. 2006, 26 (3), 310-338.
25. Drysdale, M.J.; Brough, P.A.; Massey, A.; Jensen, M.R.; Schoepfer, J. Targeting Hsp90 for the treatment of cancer. Curr. Opin. Drug Discov. Devel. 2006, 9 (4), 483-495.
26. Whitesell, L.; Lindquist, S.L. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 2005, 5 (10), 761-772.
27. Solit, D.B.; Chiosis, G. Development and application of Hsp90 inhibitors. Drug Discov. Today 2008, 13 (1-2), 38-43.
28. 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 (7087), 1013-1017.
29. Delmotte, P.; Delmotte-Plaque, J. A new antifungal substance of fungal origin. Nature 1953, 171 (4347), 344.
30. Schulte, T.W.; Akinaga, S.; Soga, S.; Sullivan, W.; Stensgard, B.; Toft, D.; Neckers, L.M. Antibiotic radicicol binds to the N-terminal domain of Hsp90 and shares important biologic activities with geldanamycin. Cell Stress Chaperones 1998, 3 (2), 100-108.
31. Roe, S.M.; Prodromou, C.; O'Brien, R.; Ladbury, J.E.; Piper, P.W.; Pearl, L.H. Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. J. Med. Chem. 1999, 42 (2), 260-266.
32. Sharp, S.Y.; Boxall, K.; Rowlands, M.; Prodromou, C.; Roe, S.M.; Maloney, A.; Powers, M.; Clarke, P.A.; Box, G.; Sanderson, S.; Patterson, L.; Matthews, T.P.; Cheung, K.M.; Ball, K.; Hayes, A.; Raynaud, F.; Marais, R.; Pearl, L.; Eccles, S.; Aherne, W.; McDonald, E.; Workman, P. In vitro biological characterization of a novel, synthetic diaryl pyrazole resorcinol class of heat shock protein 90 inhibitors. Cancer Res. 2007, 67 (5), 2206-2216.
33. Supuran, C.T. Carbonic anhydrases - an overview. Curr. Pharm. Des. 2008, 14 (7), 603-614.
34. Supuran, C.T. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat. Rev. Drug Discov. 2008, 7 (2), 168-181.
35. Thoms, S. Hydrogen bonds and the catalytic mechanism of human carbonic anhydrase II. J. Theor. Biol. 2002, 215 (4), 399-404.
36. Di Fiore, A.; Pedone, C.; Antel, J.; Waldeck, H.; Witte, A.; Wurl, M.; Scozzafava, A.; Supuran, C.T.; De Simone, G. Carbonic anhydrase inhibitors: the X-ray crystal structure of ethoxzolamide complexed to human isoform II reveals the importance of thr200 and gln92 for obtaining tightbinding inhibitors. Bioorg. Med. Chem. Lett. 2008, 18 (8), 2669-2674.
37. Garnier, C.; Protasevich, I.; Gilli, R.; Tsvetkov, P.; Lobachov, V.; Peyrot, V.; Briand, C.; Makarov, A. The two-state process of the heat shock protein 90 thermal denaturation: Effect of calcium and magnesium. Biochem. Biophys. Res. Commun. 1998, 249 (1), 197-201.
38. Agatsuma, T.; Ogawa, H.; Akasaka, K.; Asai, A.; Yamashita, Y.; Mizukami, T.; Akinaga, S.; Saitoh, Y. Halohydrin and oxime derivatives of radicicol: synthesis and antitumor activities. Bioorg. Med. Chem. 2002, 10 (11), 3445-3454.
39. Robertson, A.D.; Murphy, K.P. Protein structure and the energetics of protein stability. Chem. Rev. 1997, 97 (5), 1251-1268.
40. Rosgen, J.; Hinz, H.J. Phase diagrams: a graphical representation of linkage relations. J. Mol. Biol. 2003, 328 (1), 255-271.
41. Casini, A.; Antel, J.; Abbate, F.; Scozzafava, A.; David, S.; Waldeck, H.; Schafer, S.; Supuran, C.T. Carbonic anhydrase inhibitors: SAR and X-ray crystallographic study for the interaction of sugar sulfamates/sulfamides with isozymes I, II and IV. Bioorg. Med. Chem. Lett. 2003, 13 (5), 841-845.
42. Baranauskiene, L.; Matuliene, J.; Matulis, D. Determination of the thermodynamics of carbonic anhydrase acid-unfolding by titration calorimetry. J. Biochem. Biophys. Methods 2008, 70 (6), 1043-1047.
43. Sigg, H.P.; Loeffler, W. Production of radicicol. US Pat. 3428526, 1969.
44. Richter, K.; Muschler, P.; Hainzl, O.; Buchner, J. Coordinated ATP hydrolysis by the Hsp90 dimer. J. Biol. Chem. 2001, 276 (36), 33689-33696.