Establish an automated flow injection ESI-MS method for the screening of fragment based libraries: Application to Hsp90

European Journal of Pharmaceutical Sciences

Volumn 76, Issue , 2015, Pages 83-94

  Riccardi Sirtori, Federico ^a,b   Caronni, Dannica ^a   Colombo, Maristella ^a   Dalvit, Claudio ^a,c   Paolucci, Mauro ^a   Regazzoni, Luca ^b   Visco, Carlo ^a   Fogliatto, Gianpaolo ^a  

^a Oncology Business Unit   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Antitumor agents; Fragment based approach; Hsp90; Mass spectrometry; Medicinal chemistry

Indexed keywords

4 [4 (1,4 BENZODIOXAN 6 YL) 5 METHYL 1H PYRAZOL 3 YL] 6 ETHYLRESORCINOL; ADENOSINE TRIPHOSPHATE; BIOPOLYMER; CHAPERONE; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; LUMINESPIB; NOVOBIOCIN; PYRAZOLE DERIVATIVE; TANESPIMYCIN; LIGAND; MOLECULAR LIBRARY; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ANALYTIC METHOD; ARTICLE; AUTOMATED FLOW INJECTION; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CRYSTALLIZATION; DISSOCIATION CONSTANT; DRUG DEVELOPMENT; DRUG SCREENING; DRUG STRUCTURE; ELECTROSPRAY MASS SPECTROMETRY; FLOW INJECTION ANALYSIS; FLUORESCENCE POLARIZATION IMMUNOASSAY; FLUORINE CHEMICAL SHIFT ANISOTROPY AND EXCHANGE FOR SCREENING; FRAGMENT BASED DRUG DISCOVERY; HIGH THROUGHPUT SCREENING; NEOPLASM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FOLDING; RELIABILITY; X RAY CRYSTALLOGRAPHY; ANTAGONISTS AND INHIBITORS; BINDING COMPETITION; CHEMISTRY; COMPARATIVE STUDY; FLUORESCENCE POLARIZATION; LABORATORY AUTOMATION; METABOLISM; MOLECULAR LIBRARY; PROCEDURES; REPRODUCIBILITY; VALIDATION STUDY;

AUTOMATION, LABORATORY; BINDING SITES; BINDING, COMPETITIVE; CRYSTALLOGRAPHY, X-RAY; DRUG DISCOVERY; FLOW INJECTION ANALYSIS; FLUORESCENCE POLARIZATION; HIGH-THROUGHPUT SCREENING ASSAYS; HSP90 HEAT-SHOCK PROTEINS; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; REPRODUCIBILITY OF RESULTS; SMALL MOLECULE LIBRARIES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 84929173141     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2015.05.001     Document Type: Article

References (68)

1. S. Bauer, L.K. Yu, G.D. Demetri, and J.A. Fletcher Heat shock protein 90 inhibition in imatinib-resistant gastrointestinal stromal tumor Cancer Res. 66 2006 9153 9161
2. K. Benkestock, C.K. Van Pelt, T. Akerud, A. Sterling, P.O. Edlund, and J. Roeraade Automated nano-electrospray mass spectrometry for protein-ligand screening by noncovalent interaction applied to human H-FABP and A-FABP J. Biomol. Screen. 8 2003 247 256
3. K. Benkestock, P.O. Edlund, and J. Roeraade Electrospray ionization mass spectrometry as a tool for determination of drug binding sites to human serum albumin by noncovalent interaction Rapid Commun. Mass Spectrom. 19 2005 1637 1643
4. M.A. Biamonte, J. Shi, K. Hong, D.C. Hurst, L. Zhang, J. Fan, D.J. Busch, P.L. Karjian, A.A. Maldonado, J.L. Sensintaffar, Y.-C. Yang, A. Kamal, R.E. Lough, K. Lundgren, F.J. Burrows, G.A. Timony, M.F. Boehm, and S.R. Kasibhatla Orally active purine-based inhibitors of the heat shock protein 90 J. Med. Chem. 49 2005 817 828
5. M.A. Biamonte, R. Van de Water, J.W. Arndt, R.H. Scannevin, D. Perret, and W.C. Lee Heat shock protein 90: inhibitors in clinical trials J. Med. Chem. 53 2010 3 17
6. Brasca, M.G., Casale, E., Ferguson, R., Polucci, P., Zuccotto, F., 2010. Resorcinol Derivatives as Hsp90 Inhibitors.
7. K. Breuker, and F.W. McLafferty Stepwise evolution of protein native structure with electrospray into the gas phase, 10(-12) to 10(2) s Proc. Natl. Acad. Sci. U.S.A. 105 2008 18145 18152
8. P.A. Brough, W. Aherne, X. Barril, J. Borgognoni, K. Boxall, J.E. Cansfield, K.M. Cheung, I. Collins, N.G. Davies, M.J. Drysdale, B. Dymock, S.A. Eccles, H. Finch, A. Fink, A. Hayes, R. Howes, R.E. Hubbard, K. James, A.M. Jordan, A. Lockie, V. Martins, A. Massey, T.P. Matthews, E. McDonald, C.J. Northfield, L.H. Pearl, C. Prodromou, S. Ray, F.I. Raynaud, S.D. Roughley, S.Y. Sharp, A. Surgenor, D.L. Walmsley, P. Webb, M. Wood, P. Workman, and L. Wright 4,5-diarylisoxazole Hsp90 chaperone inhibitors: potential therapeutic agents for the treatment of cancer J. Med. Chem. 51 2008 196 218
9. H.Y. Carr, and E.M. Purcell Effects of diffusion on free precession in nuclear magnetic resonance experiments Phys. Rev. 94 1954 630
10. R.A. Carr, M. Congreve, C.W. Murray, and D.C. Rees Fragment-based lead discovery: leads by design Drug Discov. Today 10 2005 987 992
11. E. Casale, N. Amboldi, M.G. Brasca, D. Caronni, N. Colombo, C. Dalvit, E.R. Felder, G. Fogliatto, A. Galvani, A. Isacchi, P. Polucci, L. Riceputi, F. Sola, C. Visco, F. Zuccotto, and F. Casuscelli Fragment-based hit discovery and structure-based optimization of aminotriazoloquinazolines as novel Hsp90 inhibitors Bioorg. Med. Chem. 22 2014 4135 4150
12. S. Chandarlapaty, A. Sawai, Q. Ye, A. Scott, M. Silinski, K. Huang, P. Fadden, J. Partdrige, S. Hall, P. Steed, L. Norton, N. Rosen, and D.B. Solit SNX2112, a synthetic heat shock protein 90 inhibitor, has potent antitumor activity against HER kinase-dependent cancers Clin. Cancer Res. 14 2008 240 248
13. K.M. Cheung, T.P. Matthews, K. James, M.G. Rowlands, K.J. Boxall, S.Y. Sharp, A. Maloney, S.M. Roe, C. Prodromou, L.H. Pearl, G.W. Aherne, E. McDonald, and P. Workman The identification, synthesis, protein crystal structure and in vitro biochemical evaluation of a new 3,4-diarylpyrazole class of Hsp90 inhibitors Bioorg. Med. Chem. Lett. 15 2005 3338 3343
14. G. Chiosis, M.N. Timaul, B. Lucas, P.N. Munster, F.F. Zheng, L. Sepp-Lorenzino, and N. Rosen A small molecule designed to bind to the adenine nucleotide pocket of Hsp90 causes Her2 degradation and the growth arrest and differentiation of breast cancer cells Chem. Biol. 8 2001 289 299
15. G. Chiosis, B. Lucas, A. Shtil, H. Huezo, and N. Rosen Development of a purine-scaffold novel class of Hsp90 binders that inhibit the proliferation of cancer cells and induce the degradation of Her2 tyrosine kinase Bioorg. Med. Chem. 10 2002 3555 3564
16. M. Congreve, R. Carr, C. Murray, and H. Jhoti A 'rule of three' for fragment-based lead discovery? Drug Discov. Today 8 2003 876 877
17. R.A. Copeland Evaluation of enzyme inhibitors in drug discovery. A guide for medicinal chemists and pharmacologists Methods Biochem. Anal. 46 2005 1 265
18. P. Csermely, T. Schnaider, C. Soti, Z. Prohaszka, and G. Nardai The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review Pharmacol. Ther. 79 1998 129 168
19. J.B. Cunniff, and P. Vouros False positives and the detection of cyclodextrin inclusion complexes by electrospray mass spectrometry J. Am. Soc. Mass Spectrom. 6 1995 437 447
20. C. Dalvit, M. Flocco, B.J. Stockman, and M. Veronesi Competition binding experiments for rapidly ranking lead molecules for their binding affinity to human serum albumin Comb. Chem. High Throughput Screen. 5 2002 645 650
21. C. Dalvit, P.E. Fagerness, D.T. Hadden, R.W. Sarver, and B.J. Stockman Fluorine-NMR experiments for high-throughput screening: theoretical aspects, practical considerations, and range of applicability J. Am. Chem. Soc. 125 2003 7696 7703
22. C. Dalvit, D. Caronni, N. Mongelli, M. Veronesi, and A. Vulpetti NMR-based quality control approach for the identification of false positives and false negatives in high throughput screening Curr. Drug Discov. Technol. 3 2006 115 124
23. B.W. Dymock, X. Barril, P.A. Brough, J.E. Cansfield, A. Massey, E. McDonald, R.E. Hubbard, A. Surgenor, S.D. Roughley, P. Webb, P. Workman, L. Wright, and M.J. Drysdale Novel, potent small-molecule inhibitors of the molecular chaperone Hsp90 discovered through structure-based design J. Med. Chem. 48 2005 4212 4215
24. A. El-Hawiet, E.N. Kitova, L. Liu, and J.S. Klassen Quantifying labile protein-ligand interactions using electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 21 2010 1893 1899
25. D.A. Erlanson, R.S. McDowell, and T. O'Brien Fragment-based drug discovery J. Med. Chem. 47 2004 3463 3482
26. J. Gao, X. Cheng, R. Chen, G.B. Sigal, J.E. Bruce, B.L. Schwartz, S.A. Hofstadler, G.A. Anderson, R.D. Smith, and G.M. Whitesides Screening derivatized peptide libraries for tight binding inhibitors to carbonic anhydrase II by electrospray ionization-mass spectrometry J. Med. Chem. 39 1996 1949 1955
27. M.P. Goetz, D.O. Toft, M.M. Ames, and C. Erlichman The Hsp90 chaperone complex as a novel target for cancer therapy Ann. Oncol. 14 2003 1169 1176
28. M.J. Greig, and J.M. Robinson Detection of oligonucleotide-ligand complexes by ESI-MS (DOLCE-MS) as a component of high throughput screening J. Biomol. Screen. 5 2000 441 454
29. M.J. Hartshorn, C.W. Murray, A. Cleasby, M. Frederickson, I.J. Tickle, and H. Jhoti Fragment-based lead discovery using X-ray crystallography J. Med. Chem. 48 2005 403 413
30. A.J. Heck, and R.H. Van Den Heuvel Investigation of intact protein complexes by mass spectrometry Mass Spectrom. Rev. 23 2004 368 389
31. S.A. Hofstadler, and K.A. Sannes-Lowery Applications of ESI-MS in drug discovery: interrogation of noncovalent complexes Nat. Rev. Drug Discov. 5 2006 585 595
32. M.C. Jecklin, S. Schauer, C.E. Dumelin, and R. Zenobi Label-free determination of protein-ligand binding constants using mass spectrometry and validation using surface plasmon resonance and isothermal titration calorimetry J. Mol. Recognit. 22 2009 319 329
33. M.C. Jecklin, D. Touboul, R. Jain, E.N. Toole, J. Tallarico, P. Drueckes, P. Ramage, and R. Zenobi Affinity classification of kinase inhibitors by mass spectrometric methods and validation using standard IC(50) measurements Anal. Chem. 81 2009 408 419
34. M.C. Jecklin, D. Touboul, R. Jain, E.N. Toole, J. Tallarico, P. Drueckes, P. Ramage, and R. Zenobi Affinity classification of kinase inhibitors by mass spectrometric methods and validation using standard IC(50) measurements Anal. Chem. 81 2009 408 419
35. K. Jhaveri, T. Taldone, S. Modi, and G. Chiosis Advances in the clinical development of heat shock protein 90 (Hsp90) inhibitors in cancers Biochim. Biophys. Acta 1823 2011 742 755
36. R. Karlsson, P.S. Katsamba, H. Nordin, E. Pol, and D.G. Myszka Analyzing a kinetic titration series using affinity biosensors Anal. Biochem. 349 2006 136 147
37. S. Kromidas HPLC made to Measure: A Practical Handbook for Optimization 2006 Wiley-VCH; [Chichester: John Wiley, distributor] Weinheim
38. P. Kuzmic Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase Anal. Biochem. 237 1996 260 273
39. C.A. Lepre, J.M. Moore, and J.W. Peng Theory and applications of NMR-based screening in pharmaceutical research Chem. Rev. 104 2004 3641 3676
40. D. Lesuisse, G. Lange, P. Deprez, D. Benard, B. Schoot, G. Delettre, J.P. Marquette, P. Broto, V. Jean-Baptiste, P. Bichet, E. Sarubbi, and E. Mandine SAR and X-ray. A new approach combining fragment-based screening and rational drug design: application to the discovery of nanomolar inhibitors of Src SH2 J. Med. Chem. 45 2002 2379 2387
41. L. Liu, D. Bagal, E.N. Kitova, P.D. Schnier, and J.S. Klassen Hydrophobic protein-ligand interactions preserved in the gas phase J. Am. Chem. Soc. 131 2009 15980 15981
42. K. Lundgren, H. Zhang, J. Brekken, N. Huser, R.E. Powell, N. Timple, D.J. Busch, L. Neely, J.L. Sensintaffar, Y.C. Yang, A. McKenzie, J. Friedman, R. Scannevin, A. Kamal, K. Hong, S.R. Kasibhatla, M.F. Boehm, and F.J. Burrows BIIB021, an orally available, fully synthetic small-molecule inhibitor of the heat shock protein Hsp90 Mol. Cancer Ther. 8 2009 921 929
43. H.J. Maple, R.A. Garlish, L. Rigau-Roca, J. Porter, I. Whitcombe, C.E. Prosser, J. Kennedy, A.J. Henry, R.J. Taylor, M.P. Crump, and J. Crosby Automated protein-ligand interaction screening by mass spectrometry J. Med. Chem. 55 2012 837 851
44. S. Mathur, M. Badertscher, M. Scott, and R. Zenobi Critical evaluation of mass spectrometric measurement of dissociation constants: accuracy and cross-validation against surface plasmon resonance and circular dichroism for the calmodulin-melittin system Phys. Chem. Chem. Phys. 9 2007 6187 6198
45. S. Meiboom, and D. Gill Modified spin-echo method for measuring nuclear relaxation times Rev. Sci. Instrum. 29 1958 688 692
46. T. Neumann, H.D. Junker, K. Schmidt, and R. Sekul SPR-based fragment screening: advantages and applications Curr. Top. Med. Chem. 7 2007 1630 1642
47. M. Peschke, U.H. Verkerk, and P. Kebarle Features of the ESI mechanism that affect the observation of multiply charged noncovalent protein complexes and the determination of the association constant by the titration method J. Am. Soc. Mass Spectrom. 15 2004 1424 1434
48. V. Pinciroli, R. Biancardi, N. Colombo, M. Colombo, and V. Rizzo Characterization of small combinatorial chemistry libraries by (1)H NMR. Quantitation with a convenient and novel internal standard J. Comb. Chem. 3 2001 434 440
49. C.V. Robinson, E.W. Chung, B.B. Kragelund, J. Knudsen, R.T. Aplin, F.M. Poulsen, and C.M. Dobson Probing the nature of noncovalent interactions by mass spectrometry. A study of protein-CoA ligand binding and assembly J. Am. Chem. Soc. 118 1996 8646 8653
50. F. Rosu, V. Gabelica, C. Houssier, and E. De Pauw Determination of affinity, stoichiometry and sequence selectivity of minor groove binder complexes with double-stranded oligodeoxynucleotides by electrospray ionization mass spectrometry Nucl. Acids Res. 30 2002 e82
51. K.A. Sannes-Lowery, J.J. Drader, R.H. Griffey, and S.A. Hofstadler Fourier transform ion cyclotron resonance mass spectrometry as a high throughput affinity screen to identify RNA binding ligands. TrAC Trends Anal. Chem. 19 2000 481 491
52. C.A. Schalley Molecular recognition and supramolecular chemistry in the gas phase Mass Spectrom. Rev. 20 2001 253 309
53. T. Scheibel, H.I. Siegmund, R. Jaenicke, P. Ganz, H. Lilie, and J. Buchner The charged region of Hsp90 modulates the function of the N-terminal domain Proc. Natl. Acad. Sci. U.S.A. 96 1999 1297 1302
54. T.W. Schulte, and L.M. Neckers The benzoquinone ansamycin 17-allylamino-17-demethoxygeldanamycin binds to HSP90 and shares important biologic activities with geldanamycin Cancer Chemother. Pharmacol. 42 1998 273 279
55. T. Shimamura, D. Li, H. Ji, H.J. Haringsma, E. Liniker, C.L. Borgman, A.M. Lowell, Y. Minami, K. McNamara, S.A. Perera, S. Zaghlul, R.K. Thomas, H. Greulich, S. Kobayashi, L.R. Chirieac, R.F. Padera, S. Kubo, M. Takahashi, D.G. Tenen, M. Meyerson, K.K. Wong, and G.I. Shapiro Hsp90 inhibition suppresses mutant EGFR-T790M signaling and overcomes kinase inhibitor resistance Cancer Res. 68 2008 5827 5838
56. R.D. Smith, K.J. Light-Wahl, B.E. Winger, and J.A. Loo Preservation of non-covalent associations in electrospray ionization mass spectrometry: multiply charged polypeptide and protein dimers Org. Mass Spectrom. 27 1992 811 821
57. N.F. Smith, A. Hayes, K. James, B.P. Nutley, E. McDonald, A. Henley, B. Dymock, M.J. Drysdale, F.I. Raynaud, and P. Workman Preclinical pharmacokinetics and metabolism of a novel diaryl pyrazole resorcinol series of heat shock protein 90 inhibitors Mol. Cancer Ther. 5 2006 1628 1637
58. J. Sun, E.N. Kitova, W. Wang, and J.S. Klassen Method for distinguishing specific from nonspecific protein-ligand complexes in nanoelectrospray ionization mass spectrometry Anal. Chem. 78 2006 3010 3018
59. J. Sun, E.N. Kitova, N. Sun, and J.S. Klassen Method for identifying nonspecific protein-protein interactions in nanoelectrospray ionization mass spectrometry Anal. Chem. 79 2007 8301 8311
60. F. Vallee, C. Carrez, F. Pilorge, A. Dupuy, A. Parent, L. Bertin, F. Thompson, P. Ferrari, F. Fassy, A. Lamberton, A. Thomas, R. Arrebola, S. Guerif, A. Rohaut, V. Certal, J.M. Ruxer, T. Gouyon, C. Delorme, A. Jouanen, J. Dumas, C. Grepin, C. Combeau, H. Goulaouic, N. Dereu, V. Mikol, P. Mailliet, and H. Minoux Tricyclic series of heat shock protein 90 (Hsp90) inhibitors part I: discovery of tricyclic imidazo[4,5-c]pyridines as potent inhibitors of the Hsp90 molecular chaperone J. Med. Chem. 54 2011 7206 7219
61. R.H. Van den Heuvel, and A.J. Heck Native protein mass spectrometry: from intact oligomers to functional machineries Curr. Opin. Chem. Biol. 8 2004 519 526
62. V. Vivat Hannah, C. Atmanene, D. Zeyer, A. Van Dorsselaer, and S. Sanglier-Cianfàrani Native MS: an "ESI" way to support structure- and fragment-based drug discovery Future Med. Chem. 2 2009 35 50
63. Z.X. Wang An exact mathematical expression for describing competitive binding of two different ligands to a protein molecule FEBS Lett. 360 1995 111 114
64. Z. Wang, M. Cui, F. Song, L. Lu, Z. Liu, and S. Liu Evaluation of flavonoids binding to DNA duplexes by electrospray ionization mass spectrometry J. Am. Soc. Mass Spectrom. 19 2008 914 922
65. M. Wigger, J.R. Eyler, S.A. Benner, W. Li, and A.G. Marshall Fourier transform-ion cyclotron resonance mass spectrometric resolution, identification, and screening of non-covalent complexes of Hck Src homology 2 domain receptor and ligands from a 324-member peptide combinatorial library J. Am. Soc. Mass Spectrom. 13 2002 1162 1169
66. A. Wortmann, M.C. Jecklin, D. Touboul, M. Badertscher, and R. Zenobi Binding constant determination of high-affinity protein-ligand complexes by electrospray ionization mass spectrometry and ligand competition J. Mass Spectrom. 43 2008 600 608
67. Y. Xu, C. Afonso, R. Wen, and J.C. Tabet Investigation of double-stranded DNA/drug interaction by ESI/FT ICR: orientation of dissociations relates to stabilizing salt bridges J. Mass Spectrom. 43 2008 1531 1544
68. J.H. Zhang, T.D. Chung, and K.R. Oldenburg A simple statistical parameter for use in evaluation and validation of high throughput screening assays J. Biomol. Screen. 4 1999 67 73