Exploring the influence of the protein environment on metal-binding pharmacophores

Journal of Medicinal Chemistry

Volumn 57, Issue 16, 2014, Pages 7126-7135

  Martin, David P ^a   Blachly, Patrick G ^a   McCammon, J Andrew ^a   Cohen, Seth M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE INHIBITOR; METAL; PYRIDINE DERIVATIVE; PYRITHIONE; THIOKETONE;

ANTAGONISTS AND INHIBITORS; CHEMICAL PHENOMENA; CHEMISTRY; DRUG DESIGN; ENZYME ACTIVE SITE; HUMAN; HYDROGEN BOND; METABOLISM; MOLECULAR MODEL; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

CARBONIC ANHYDRASE II; CARBONIC ANHYDRASE INHIBITORS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; HUMANS; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; METALS; MODELS, MOLECULAR; PYRIDINES; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS; THIONES;

EID: 84906874907     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm500984b     Document Type: Article

References (77)

1. Anzellotti, A. I.; Farrell, N. P. Zinc Metalloproteins as Medicinal Targets Chem. Soc. Rev. 2008, 37, 1629-1651
2. Rouffet, M.; Cohen, S. M. Emerging Trends in Metalloprotein Inhibition Dalton Trans. 2011, 40, 3445-3454
3. Supuran, C. T.; Scozzafava, A.; Casini, A. Carbonic Anhydrase Inhibitors Med. Res. Rev. 2003, 23 (2) 146-189
4. Brown, N. J.; Vaughan, D. E. Angiotensin-Converting Enzyme Inhibitors Circulation 1998, 97, 1411-1420
5. Paris, M.; Porcelloni, M.; Binaschi, M.; Fattori, D. Histone Deacetylase Inhibitors: From Bench to Clinic J. Med. Chem. 2008, 51 (6) 1505-1529
6. Young, R. N. Inhibitors of 5-Lipoxygenase: A Therapeutic Potential Yet to be Fully Realized? Eur. J. Med. Chem. 1999, 34, 671-685
7. Fernández-Montero, J. V.; Vispo, E.; Soriano, V. Emerging Antiretroviral Drugs Expert Opin. Pharmacother. 2014, 15 (2) 211-219
8. Martin, D. P.; Puerta, D. T.; Cohen, S. M., Metalloprotein Inhibitors. In Ligand Design in Medicinal Inorganic Chemistry; Storr, T., Ed.; John Wiley and Sons, Inc.: Hoboken, NJ, 2014.
9. Moradei, O.; Vaisburg, A.; Martell, R. E. Histone Deacetylase Inhibitors in Cancer Therapy: New Compounds and Clinical Update of Benzamide-Type Agents Curr. Top. Med. Chem. 2008, 8 (10) 841-858
10. Jacobsen, J. A.; Fullagar, J. L.; Miller, M. T.; Cohen, S. M. Identifying Chelators for Metalloprotein Inhibitors Using a Fragment-Based Approach J. Med. Chem. 2011, 54 (2) 591-602
11. Puerta, D. T.; Lewis, J. A.; Cohen, S. M. New Beginnings for Matrix Metalloproteinase Inhibitors: Identification of High-Affinity Zinc-Binding Groups J. Am. Chem. Soc. 2004, 126 (27) 8388-8389
12. Puerta, D. T.; Mongan, J.; Tran, B. L.; McCammon, J. A.; Cohen, S. M. Potent, Selective Pyrone-Based Inhibitors of Stromelysin-1 J. Am. Chem. Soc. 2005, 127, 14148-14149
13. Agrawal, A.; Romero-Perez, D.; Jacobsen, J. A.; Villarreal, F. J.; Cohen, S. M. Zinc-Binding Groups Modulate Selective Inhibition of MMPs ChemMedChem 2008, 3 (5) 812-820
14. Rouffet, M.; de Oliveira, C. A. F.; Udi, Y.; Agrawal, A.; Sagi, I.; McCammon, J. A.; Cohen, S. M. From Sensors to Silencers: Quinoline- and Benzimidazole-Sulfonamides as Inhibitors for Zinc Proteases J. Am. Chem. Soc. 2010, 132 (24) 8232-8233
15. Agrawal, A.; DeSoto, J.; Fullagar, J. L.; Maddali, K.; Rostami, S.; Richman, D. D.; Pommier, Y.; Cohen, S. M. Probing Chelation Motifs in HIV Integrase Inhibitors Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (7) 2251-2256
16. Garner, A. L.; Struss, A. K.; Fullagar, J. L.; Agrawal, A.; Moreno, A. Y.; Cohen, S. M.; Janda, K. D. 3-Hydroxy-1-alkyl-2-methylpyridine-4(1 H)-thiones: Inhibition of the Pseudomonas aeruginosa Virulence Factor LasB ACS Med. Chem. Lett. 2012, 3 (8) 668-672
17. Rogolino, D.; Carcelli, M.; Sechi, M.; Neamati, N. Viral enzymes containing magnesium: Metal binding as a successful strategy in drug design Coord. Chem. Rev. 2012, 256 (23-24) 3063-3086
18. Flagg, S. C.; Martin, C. B.; Taabazuing, C. Y.; Holmes, B. E.; Knapp, M. J. Screening Chelating Inhibitors of HIF-Prolyl Hydroxylase Domain 2 (PHD2) and Factor Inhibiting HIF (FIH) J. Inorg. Biochem. 2012, 113, 25-30
19. Johnson, S.; Barile, E.; Farina, B.; Purves, A.; Wei, J.; Chen, L.-H.; Shiryaev, S.; Zhang, Z.; Rodionova, I.; Agrawal, A.; Cohen, S. M.; Osterman, A.; Strongin, A.; Pellecchia, M. Targeting Metalloproteins by Fragment-Based Lead Discovery Chem. Biol. Drug Des. 2011, 78, 211-223
20. Madsen, A. S.; Kristensen, H. M. E.; Lanz, G.; Olsen, C. A. The Effect of Various Zinc Binding Groups on Inhibition of Histone Deacetylases ChemMedChem 2014, 9 (3) 614-626
21. Deng, L.; Sundriyal, S.; Rubio, V.; Shi, Z.-z.; Song, Y. Coordination Chemistry Based Approach to Lipophilic Inhibitors of 1-Deoxy- d -xylulose-5-phosphate Reductoisomerase J. Med. Chem. 2009, 52 (21) 6539-6542
22. Patil, V.; Sodji, Q. H.; Kornacki, J. R.; Mrksich, M.; Oyelere, A. K. 3-Hydroxypridin-2-thione as Novel Zinc Binding Group for Selective Histone Deacetylase Inhibition J. Med. Chem. 2013, 56 (9) 3492-3506
23. Pottel, J.; Therrien, E.; Gleason, J. L.; Moitessier, N. Docking Ligands into Flexible and Solvated Macromolecules. 6. Development and Application to the Docking of HDACs and other Zinc Metalloenzyme Inhibitors J. Chem. Inf. Model. 2014, 54, 254-265
24. Zhang, J.; Yang, W.; Piquemal, J.-P.; Ren, P. Modeling Structural Coordination and Ligand Binding in Zinc Proteins with a Polarizable Potential J. Chem. Theory Comput. 2012, 8, 1314-1324
25. Seebeck, B.; Reulecke, I.; Kämper, A.; Rarey, M. Modeling of Metal Interaction Geometries for Protein-Ligand Docking Proteins 2008, 71, 1237-1254
26. Looney, A.; Han, R.; McNeill, K.; Parkin, G. Tris(pyrazoly1) hydroboratozinc Hydroxide Complexes as Functional Models for Carbonic Anhydrase: On the Nature of the Bicarbonate Intermediate J. Am. Chem. Soc. 1993, 115, 4690-4697
27. Looney, A.; Parkin, G.; Alsfasser, R.; Ruf, M.; Vahrenkamp, H. Zinc Pyrazolylborate Complexes Relevant to the Biological Function of Carbonic Anhydrase Angew. Chem., Int. Ed. 1992, 31 (1) 92-93
28. Parkin, G. Synthetic Analogues Relevant to the Structure and Function of Zinc Enzymes Chem. Rev. 2004, 104 (2) 699-767
29. Puerta, D. T.; Cohen, S. M. Elucidating Drug-Metalloprotein Interactions with Tris(pyrazolyl)borate Model Complexes Inorg. Chem. 2002, 41 (20) 5075-5082
30. Puerta, D. T.; Schames, J. R.; Henchman, R. H.; McCammon, J. A.; Cohen, S. M. From Model Complexes to Metalloprotein Inhibition: A Synergistic Approach to Structure-Based Drug Discovery Angew. Chem., Int. Ed. 2003, 42 (32) 3772-3774
31. Cho, J. H.; Kim, D. H.; Chung, S. J.; Ha, N.-C.; Oh, B.-H.; Choi, K. Y. Insight into the Stereochemistry in the Inhibition of Carboxypeptidase A with N -(hydroxyaminocarbonyl)phenylalanine: Binding Modes of an Enantiomeric Pair of the Inhibitor to Carboxypeptidase A Bioorg. Med. Chem. 2002, 10, 2015-2022
32. Gaucher, J. F.; Selkti, M.; Tiraboschi, G.; Prangé, T.; Roques, B. P.; Tomas, A.; Fournié-Zaluski, M. C. Crystal Structures of α-Mercaptoacyldipeptides in the Thermolysin Active Site: Structural Parameters for a Zn Monodentation or Bidentation in Metalloendopeptidases Biochemistry 1999, 38 (39) 12569-12576
33. Bauman, J. D.; Patel, D.; Baker, S. F.; Vijayan, R. S. K.; Xiang, A.; Parhi, A. K.; Martínez-Sobrido, L.; LaVoie, E. J.; Das, K.; Arnold, E. Crystallographic Fragment Screening and Structure-Based Optimization Yields a New Class of Influenza Endonuclease Inhibitors ACS Chem. Biol. 2013, 8, 2501-2508
34. Krishnamurthy, V. M.; Kaufman, G. K.; Urbach, A. R.; Gitlin, I.; Gudiksen, K. L.; Weibel, D. B.; Whitesides, G. M. Carbonic Anhydrase as a Model for Biophysical and Physical-Organic Studies of Proteins and Protein-Ligand Binding Chem. Rev. 2008, 108 (3) 946-1051
35. Martin, D. P.; Blachly, P. G.; Marts, A. R.; Woodruff, T. M.; Oliveira, C. A. F. d.; McCammon, J. A.; Tierney, D. L.; Cohen, S. M. 'Unconventional' Coordination Chemistry by Metal Chelating Fragments in a Metalloprotein Active Site J. Am. Chem. Soc. 2014, 136 (14) 5400-5406
36. Wischeler, J. S.; Innocenti, A.; Vullo, D.; Agrawal, A.; Cohen, S. M.; Heine, A.; Supuran, C. T.; Klebe, G. Bidentate Zinc Chelators for α-Carbonic Anhydrases that Produce a Trigonal Bipyramidal Coordination Geometry ChemMedChem 2010, 5 (9) 1609-1615
37. Kawai, K.; Nagata, N. Metal-Ligand Interactions: An Analysis of Zinc Binding Groups Using the Protein Data Bank Eur. J. Med. Chem. 2012, 51, 271-276
38. Barrese, A. A.; Genis, C.; Fisher, S. Z.; Orwenyo, J. N.; Kumara, M. T.; Dutta, S. K.; Phillips, E.; Kiddle, J. J.; Tu, C.; Silverman, D. N.; Govindasamy, L.; Agbandje-McKenna, M.; McKenna, R.; Tripp, B. C. Inhibition of Carbonic Anhydrase II by Thioxolone: A Mechanistic and Structural Study Biochemistry 2008, 47 (10) 3174-3184
39. Martin, D. P.; Hann, Z. S.; Cohen, S. M. Metalloprotein-Inhibitor Binding: Human Carbonic Anhydrase II as a Model for Probing Metal-Ligand Interactions in a Metalloprotein Active Site Inorg. Chem. 2013, 52 (21) 12207-12215
40. Brayton, D.; Jacobsen, F. E.; Cohen, S. M.; Farmer, P. J. A Novel Heterocyclic Atom Exchange Reaction with Lawesson's Reagent: A One-Pot Synthesis of Dithiomaltol Chem. Commun. 2006, 206-208
41. Tekeste, T.; Vahrenkamp, H. Modeling Zinc Enzyme Inhibition with Functional Thiolate Ligands Inorg. Chem. 2006, 45 (26) 10799-10806
42. Puerta, D. T.; Cohen, S. M. Examination of Novel Zinc-Binding Groups for Use in Matrix Metalloproteinase Inhibitors Inorg. Chem. 2003, 42 (11) 3423-3430
43. Platts, J. A.; Howard, S. T.; Bracke, B. R. F. Directionality of Hydrogen Bonds to Sulfur and Oxygen J. Am. Chem. Soc. 1996, 118 (11) 2726-2733
44. Innocenti, A.; Hilvo, M.; Scozzafava, A.; Lindfors, M.; Nordlund, H. R.; Kulomaa, M. S.; Parkkila, S.; Supuran, C. T. Carbonic Anhydrase Inhibitors: The Very Weak Inhibitors Dithiothreitol, B-Mercaptoethanol, Tris(carboxyethyl) phosphine and Threitol Interfere with the Binding of Sulfonamides to Isozymes II and IX Bioorg. Med. Chem. Lett. 2008, 18 (6) 1898-1903
45. Sun, P.-J.; Fernando, Q.; Freiser, H. Formation Constants of Transition Metal Complexes of 2-Hydroxypyridine-1-oxide and 2-Mercaptopyridine-1-oxide Anal. Chem. 1964, 36 (13) 2485-2488
46. Lewis, J. A.; Mongan, J.; McCammon, J. A.; Cohen, S. M. Evaluation and Binding Mode Prediction of Thiopyrone-Based Inhibitors of Anthrax Lethal Factor ChemMedChem 2006, 1 (7) 694-697
47. Aisen, P.; Leibman, A.; Zweier, J. Stoichiometric and Site Characteristics of the Binding of Iron to Human Transferrin J. Biol. Chem. 1978, 253 (6) 1930-1937
48. Smith, R. M.; Martell, A. E. Critical Stability Constants, Enthalpies and Entropies for the Formation of Metal Complexes of Aminopolycarboxylic Acids and Carboxylic Acids Sci. Total Environ. 1987, 64, 125-147
49. Palmiter, R. D. Protection Against Zinc Toxicity by Metallothionein and Zinc Transporter 1 Proc. Natl. Acad. Sci. U. S. A. 2004, 101 (14) 4918-4923
50. Reddi, A. R.; Guzman, T. R.; Breece, R. M.; Tierney, D. L.; Gibney, B. R. Deducing the Energetic Cost of Protein Folding in Zinc Finger Proteins Using Designed Metallopeptides J. Am. Chem. Soc. 2007, 129 (42) 12815-12827
51. Yu, Y.; Gutierrez, E.; Kovacevic, Z.; Saletta, F.; Obeidy, P.; Rahmanto, Y. S.; Richardson, D. R. Iron Chelators for the Treatment of Cancer Curr. Med. Chem. 2012, 19 (17) 2689-2702
52. Agrawal, A.; de Oliveira, C. A. F.; Cheng, Y.; Jacobsen, J. A.; McCammon, J. A.; Cohen, S. M. Thioamide Hydroxypyrothiones Supersede Amide Hydroxypyrothiones in Potency against Anthrax Lethal Factor J. Med. Chem. 2009, 52 (4) 1063-1074
53. Abramovitch, R. A.; Knaus, E. E. The Direct Thionation and Aminoalkylation of Pyridine 1-oxides and Related Reactions J. Heterocycl. Chem. 1975, 12 (4) 683-690
54. Martin, D. P.; Cohen, S. M. Nucleophile Recognition as an Alternative Inhibition Mode for Benzoic Acid Based Carbonic Anhydrase Inhibitors Chem. Commun. 2012, 48, 5259-5261
55. Avvaru, B. S.; Kim, C. U.; Sippel, K. H.; Gruner, S. M.; Agbandje-McKenna, M.; Silverman, D. N.; McKenna, R. A Short, Strong Hydrogen Bond in the Active Site of Human Carbonic Anhydrase II Biochemistry 2010, 49 (2) 249-251
56. Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Refinement of Macromolecular Structures by the Maximum-Likelihood Method Acta Crystallogr., Sect. D.: Biol. Crystallogr. 1997, D53, 240-255
57. Emsley, P.; Cowtan, K. Coot: Model-Building Tools for Molecular Graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, D60, 2126-2132
58. Schüttelkopf, A. W.; Aalten, D. M. F. v. PRODRG: A Tool for High-Throughput Crystallography of Protein-Ligand Complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, D60, 1355-1363
59. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, Jr., J. A.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, J. M.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, Ö.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09, revision A.1; Gaussian, Inc.: Wallingford, CT, 2009.
60. Becke, A. D. Density-Functional Thermochemistry 0.3. The Role of Exact Exchange J. Chem. Phys. 1993, 98 (7) 5648-5652
61. Lee, C. T.; Yang, W. T.; Parr, R. G. Development of the Colle-Salvetti Correlation-Energy Formula into a Functional of the Electron Density Phys. Rev. B 1988, 37 (2) 785-789
62. Stephens, P. J.; Devlin, F. J.; Chabalowski, C. F.; Frisch, M. J. Ab Initio Calculation of Vibrational Absorption and Circular-Dichroism Spectra Using Density-Functional Force Fields J. Phys. Chem. 1994, 98 (45) 11623-11627
63. Vosko, S. H.; Wilk, L.; Nusair, M. Accurate Spin-Dependent Electron Liquid Correlation Energies for Local Spin-Density Calculations-A Critical Analysis Can. J. Phys. 1980, 58 (8) 1200-1211
64. Ryde, U. Carboxylate Binding Modes in Zinc Proteins: A Theoretical Study Biophys. J. 1999, 77 (5) 2777-2787
65. Dudev, T.; Lim, C. Tetrahedral vs Octahedral ZincComplexes with Ligands of Biological Interest: A DFT/CDM Study J. Am. Chem. Soc. 2000, 122 (45) 11146-11153
66. Barone, V.; Cossi, M. Quantum Calculation of Molecular Energies and Energy Gradients in Solution by a Conductor Solvent Model J. Phys. Chem. A 1998, 102 (11) 1995-2001
67. Cossi, M.; Rega, N.; Scalmani, G.; Barone, V. Energies, Structures, and Electronic Properties of Molecules in Solution with the C-PCM Solvation Model J. Comput. Chem. 2003, 24 (6) 669-681
68. Klamt, A.; Schuurmann, G. Cosmo-A New Approach to Dielectric Screening in Solvents with Explicit Expressions for the Screening Energy and Its Gradient J. Chem. Soc., Perkin Trans. 2 1993, 5) 799-805
69. Bickelhaupt, F. M.; Baerends, E. J. Kohn-Sham density functional theory: predicting and understanding chemistry Reviews in Computational Chemistry, Wiley: New York, 2000; Vol. 15, pp 1-86.
70. Kitaura, K.; Morokuma, K. A New Energy Decomposition Scheme for Molecular Interactions Within the Hartree-Fock Approximation Int. J. Quantum Chem. 1976, 10 (2) 325-340
71. te Velde, G.; Bickelhaupt, F. M.; Baerends, E. J.; Guerra, C. F.; Van Gisbergen, S. J. A.; Snijders, J. G.; Ziegler, T. Chemistry with ADF J. Comput. Chem. 2001, 22 (9) 931-967
72. ADF 2009; Scientific Computing and Modelling NV, Vrije Universiteit, Theoretical Chemistry: Amsterdam, 2009.
73. Kollman, P. Free Energy Calculations: Applications to Chemical and Biochemical Phenomena Chem. Rev. 1993, 93 (7) 2395-2417
74. Straatsma, T. P.; McCammon, J. A. Multiconfiguration Thermodynamic Integration J. Chem. Phys. 1991, 95 (2) 1175
75. Straatsma, T. P.; McCammon, J. A. Computational Alchemy Annu. Rev. Phys. Chem. 1992, 43 (1) 407-435
76. Kaus, J. W.; Pierce, L. T.; Walker, R. C.; McCammon, J. A. Improving the Efficiency of Free Energy Calculations in the Amber Molecular Dynamics Package J. Chem. Theory Comput. 2013, 9 (9) 4131-4139
77. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J; Duke, R. E.; Luo, R.; Walker, R. C.; Zhang, W.; Merz, K. M.; Roberts, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Swails, J.; Götz, A. W.; Kolossváry, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Wolf, R. M.; Liu, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Cai, Q.; Ye, X.; Wang, J.; Hsieh, M.-J.; Cui, G.; Roe, D. R.; Mathews, D. H.; Seetin, M. G.; Salomon-Ferrer, R.; Sagui, C.; Babin, V.; Luchko, T.; Gusarov, S.; Kovalenko, A.; Kollman, P. A. AMBER 14; University of California: San Francisco, 2012.