QM/MM calculations reveal the different nature of the interaction of two carborane-based sulfamide inhibitors of human carbonic anhydrase II

Journal of Physical Chemistry B

Volumn 117, Issue 50, 2013, Pages 16096-16104

  Pecina, Adam ^a   Lepšik, Martin ^a   Rezac, Jan ^a   Brynda, Jiři ^a,b   Mader, Pavel ^b   Řezáčová, Pavlína ^a,b   Hobza, Pavel ^a,c   Fanfrlík, Jindřich ^a  

^a INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^b INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^c PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTER-AIDED; DIHYDROGEN BONDS; DISPERSION INTERACTION; HUMAN CARBONIC ANHYDRASE II; INORGANIC INHIBITOR; LIGAND BINDING; QM/MM CALCULATIONS; RATIONAL DESIGN;

AMINO ACIDS; BINDING ENERGY; CARBONIC ANHYDRASE; HYDROGEN BONDS; PROTEINS;

CONDENSATION REACTIONS;

AMIDE; BORANE DERIVATIVE; CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE INHIBITOR;

ARTICLE; CHEMICAL STRUCTURE; DRUG ANTAGONISM; ENZYME ACTIVE SITE; HUMAN; QUANTUM THEORY; X RAY CRYSTALLOGRAPHY;

AMIDES; BORANES; CARBONIC ANHYDRASE II; CARBONIC ANHYDRASE INHIBITORS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; QUANTUM THEORY;

EID: 84890905583     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp410216m     Document Type: Article

References (60)

1. Grimes, R. N. Carboranes, 2 nd ed.; Academic Press: London, 2011.
2. -. Chem. Rev. 2006, 106, 5208.
3. 12 and their derivatives Chem. Rev. 1992, 92, 209
4. 12 Chem. Rev. 1992, 92, 225
5. Serrano-Andrés, L.; Oliva, J. M. Photochemical window mechanism for controlled atom release in carborane endohedral boxes: Theoretical evidence Chem. Phys. Lett. 2006, 432, 235
6. Crespo, O.; Gimeno, M. C.; Laguna, A.; Ospino, I.; Aullon, G.; Oliva, J. M. Organometallic gold complexes of carborane. Theoretical comparative analysis of ortho, meta, and para derivatives and luminescence studies Dalton Trans. 2009, 3807
7. Oliva, J. M.; Serrano-Andrés, L.; Klein, D. J.; Schleyer, P. V.; Michl, J. Design of Carborane Molecular Architectures via Electronic Structure Computations. Int. J. Photoenergy 2009.
8. Grimes, R. N. Metallacarboranes in the new millennium Coord. Chem. Rev. 2000, 200, 773
9. Teixidor, F.; Nuñez, R.; Flores, M. A.; Demonceau, A.; Viñas, C. Forced exo-nido rhoda and ruthenacarboranes as catalyst precursors: a review J. Organomet. Chem. 2000, 614, 48
10. Bednarska, K.; Olejniczak, A. B.; Wojtczak, B. A.; Sulowska, Z.; Lesnikowski, Z. J. Adenosine and 2′-deoxyadenosine modified with boron cluster pharmacophores as new classes of human blood platelet function modulators ChemMedChem 2010, 5, 749
11. Lesnikowski, Z. J. Boron clusters-A new entity for DNA-oligonucleotide modification Eur. J Org. Chem. 2003, 4489
12. Issa, F.; Kassiou, M.; Rendina, L. M. Boron in drug discovery: carboranes as unique pharmacophores in biologically active compounds Chem. Rev. 2011, 111, 5701
13. Scholz, M.; Hey-Hawkins, E. Carbaboranes as pharmacophores: properties, synthesis, and application strategies Chem. Rev. 2011, 111, 7035
14. Satapathy, R.; Dash, B. P.; Maguire, J. A.; Hosmane, N. S. New Developments in the Medicinal Chemistry of Carboranes Collect. Czech. Chem. Commun. 2010, 75, 995
15. Lesnikowski, Z. J. Boron units as pharmacophores-New applications and opportunities of boron cluster chemistry Collect. Czech. Chem. Commun. 2007, 72, 1646
16. Sivaev, I. B.; Bregadze, V. V. Polyhedral Boranes for Medical Applications: Current Status and Perspectives Eur. J. Inorg. Chem. 2009, 1433
17. Hawthorne, M. F.; Maderna, A. Applications of radiolabeled boron clusters to the diagnosis and treatment of cancer Chem. Rev. 1999, 99, 3421
18. Bialek-Pietras, M.; Olejniczak, A. B.; Tachikawa, S.; Nakamura, H.; Lesnikowski, Z. J. Towards new boron carriers for boron neutron capture therapy: Metallacarboranes bearing cobalt, iron and chromium and their cholesterol conjugates Bioorg. Med. Chem. 2013, 21, 1136
19. Schaffran, T.; Lissel, F.; Samatanga, B.; Karlsson, G.; Burghardt, A.; Edwards, K.; Winterhalter, M.; Peschka-Suss, R.; Schubert, R.; Gabel, D. Dodecaborate cluster lipids with variable headgroups for boron neutron capture therapy: Synthesis, physical-chemical properties and toxicity J. Organomet. Chem. 2009, 694, 1708
20. Justus, E.; Awad, D.; Hohnholt, M.; Schaffran, T.; Edwards, K.; Karlsson, G.; Damian, L.; Gabel, D. Synthesis, liposomal preparation, and in vitro toxicity of two novel dodecaborate cluster lipids for boron neutron capture therapy Bioconjugate Chem. 2007, 18, 1287
21. Nakamura, H.; Ueno, M.; Lee, J. D.; Ban, H. S.; Justus, E.; Fan, P.; Gabel, D. Synthesis of dodecaborate-conjugated cholesterols for efficient boron delivery in neutron capture therapy Tetrahedron Lett. 2007, 48, 3151
22. Řezáčová, P.; Cígler, P.; Matìjíček, P.; Lepšík, M.; Pokorná, J.; Grunner, B.; Konvalinka, J. Boron Science-New Technologies and Applications; CRC Press: New York, 2011.
23. Farras, P.; Juarez-Perez, E. J.; Lepšík, M.; Luque, R.; Nuñez, R.; Teixidor, F. Metallacarboranes and their interactions: theoretical insights and their applicability Chem. Soc. Rev. 2012, 41, 3445
24. Cígler, P.; Kožíšek, M.; Řezá čová, P.; Brynda, J.; Otwinowski, Z.; Pokorná, J.; Plešek, J.; Gruner, B.; Doleckova-Marešova, L.; Máša, M. From nonpeptide toward noncarbon protease inhibitors: metallacarboranes as specific and potent inhibitors of HIV protease Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 15394
25. Fanfrlík, J.; Lepšík, M.; Horinek, D.; Havlas, Z.; Hobza, P. Interaction of carboranes with biomolecules: formation of dihydrogen bonds ChemPhysChem 2006, 7, 1100
26. Fanfrlík, J.; Hnyk, D.; Lepšík, M.; Hobza, P. Interaction of heteroboranes with biomolecules. Part 2. The effect of various metal vertices and exo-substitutions Phys. Chem. Chem. Phys. 2007, 9, 2085
27. Fanfrlík, J.; Brynda, J.; Řezáč, J.; Hobza, P.; Lepšík, M. Interpretation of Protein/Ligand Crystal Structure using QM/MM Calculations: Case of HIV-1 Protease/Metallacarborane Complex J. Phys. Chem. B 2008, 112, 15094
28. Matějíček, P.; Zedník, J.; Uselova, K.; Pleštil, J.; Fanfrlík, J.; Nykanen, A.; Ruokolainen, J.; Hobza, P.; Procházka, K. Stimuli-Responsive Nanoparticles Based on Interaction of Metallacarborane with Poly(ethylene oxide) Macromolecules 2009, 42, 4829
29. Sedlák, R.; Fanfrlík, J.; Hnyk, D.; Hobza, P.; Lepšík, M. Interactions of Boranes and Carboranes with Aromatic Systems: CCSD(T) Complete Basis Set Calculations and DFT-SAPT Analysis of Energy Components J. Phys. Chem. A 2010, 114, 11304
30. Reynolds, R. C.; Campbell, S. R.; Fairchild, R. G.; Kisliuk, R. L.; Micca, P. L.; Queener, S. F.; Riordan, J. M.; Sedwick, W. D.; Waud, W. R.; Leung, A. K. W. Novel boron-containing, nonclassical antifolates: Synthesis and preliminary biological and structural evaluation J. Med. Chem. 2007, 50, 3283
31. Fujii, S.; Masuno, H.; Taoda, Y.; Kano, A.; Wongmayura, A.; Nakabayashi, M.; Ito, N.; Shimizu, M.; Kawachi, E.; Hirano, T.; Endo, Y. Boron cluster-based development of potent nonsecosteroidal vitamin D receptor ligands: direct observation of hydrophobic interaction between protein surface and carborane J. Am. Chem. Soc. 2011, 133, 20933
32. 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, 946
33. Supuran, C. T. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators Nat. Rev. Drug Discovery 2008, 7, 168
34. Gitto, R.; Damiano, F. M.; Máder, P.; De Luca, L.; Ferro, S.; Supuran, C. T.; Vullo, D.; Brynda, J.; Řezáčová, P.; Chimirri, A. Synthesis, Structure-Activity Relationship Studies, and X-ray Crystallographic Analysis of Arylsulfonamides as Potent Carbonic Anhydrase Inhibitors J. Med. Chem. 2012, 55, 3891
35. Brynda, J.; Máder, P.; Šícha, V.; Fábry, M.; Poncová, K.; Bakardiev, M.; Grüner, B.; Cígler, P.; Řezáčová, P. Carborane-Based Carbonic Anhydrase Inhibitors. Angew. Chem., Int. Ed., DOI: 10.1002/anie.201307583.
36. Plešek, J. Potential Applications of the Boron Cluster Compounds Chem. Rev. 1992, 92, 269
37. Word, J. M.; Lovell, S. C.; Richardson, J. S.; Richardson, D. C. Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation J. Mol. Biol. 1999, 285, 1735
38. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Crowley, M.; Walker, R. C.; Zhang, W.; et al. AMBER 10; University of California: San Francisco, CA, 2008.
39. Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.; Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. UCSF chimera-A visualization system for exploratory research and analysis J. Comput. Chem. 2004, 25, 1605
40. Jurečka, P.; Černý, J.; Hobza, P.; Salahub, D. Density functional theory augmented with an empirical dispersion term. Interaction energies and geometries of 80 noncovalent complexes compared with ab initio quantum mechanics calculations J. Comput. Chem. 2007, 28, 555
41. Bayly, C. I.; Cieplak, P.; Cornell, W. D.; Kollman, P. A. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges-the RESP model J. Phys. Chem. 1993, 97, 10269
42. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M. C.; Xiong, G. M.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 2003, 24, 1999
43. Wang, J. M.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field J. Comput. Chem. 2004, 25, 1157
44. Bitzek, E.; Koskinen, P.; Gahler, F.; Moseler, M.; Gumbsch, P. Structural relaxation made simple Phys. Rev. Lett. 2006, 97, 170201
45. Berendsen, H. J. C.; Postma, J. P. M.; Vangunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684
46. Ahlrichs, R.; Bar, M.; Haser, M.; Horn, H.; Kolmel, C. Electronic structure calculations on workstation computers-the program system Turbomole Chem. Phys. Lett. 1989, 162, 165
47. Svensson, M.; Humbel, S.; Froese, R. D. J.; Matsubara, T.; Sieber, S.; Morokuma, K. A multilayered integrated MO+MM method for geometry optimizations and single point energy predictions. A test for Diels-Alder reactions and Pt(P(t-Bu)(3))(2)+H-2 oxidative addition J. Phys. Chem. 1996, 100, 19357
48. Tsui, V.; Case, D. A. Theory and applications of the generalized Born solvation model in macromolecular Simulations Biopolymers 2001, 56, 275
49. Feyereisen, M.; Fitzgerald, G.; Komornicki, A. Use of approximate integrals in ab initio theory. An application in MP2 energy calculations Chem. Phys. Lett. 1993, 208, 359
50. Kolář, M.; Fanfrlík, J.; Lepšík, M.; Forti, F.; Luque, F. J.; Hobza, P. Assessing the Accuracy and Performance of Implicit Solvent Models for Drug Molecules: Conformational Ensemble Approaches J. Phys. Chem. B 2013, 117, 5950
51. 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, 799
52. Gutten, O.; Besseová, I.; Rulíšek, L. Interaction of metal ions with biomolecular lignds: How accurate are calculated free energies associated with metal ion complexation? J. Phys. Chem. A 2011, 115, 11394
53. Massova, I.; Kollman, P. A. Computational alanine scanning to probe protein-protein interactions: A novel approach to evaluate binding free energies J. Am. Chem. Soc. 1999, 121, 8133
54. Klamt, A.; Ecklert, F.; Hornig, M. COSMO-RS: A novel view to physiological solvation and partition questions J. Comput.-Aided Mol. Des. 2001, 15, 355
55. Klamt, A. Conductor-like Screening Model for Real Solvents: A New Approach to the Quantitative Calculation of Solvation Phenomena J. Phys. Chem. 1995, 99, 2224
56. DeLano, W. L. The PyMOL Molecular Graphics System; Scientific: Palo Alto, CA, 2002.
57. Buhl, M.; Hnyk, D.; Machacek, J. Computational study of structures and prperties of metalloboranes: cobalt bis(dicarbollide) Chem.-Eur. J. 2005, 11, 4109
58. Juarez-Perez, E. J.; Viñas, C.; Teixidor, F.; Nuñez, R. First example of the formation of a Si-C bond from an intramolecular Si-H···H-C diyhydrogen interaction in a metallacarborane: A theoretical study J. Organomet. Chem. 2009, 694, 1764
59. Lepšík, M.; Řezáč, J.; Kolář, M.; Pecina, A.; Hobza, P.; Fanfrlík, J. The semiempirical quantum mechanical scoring function for in silico drug design ChemPlusChem 2013, 78, 921
60. Fanfrlík, J.; Brahmkshtriya, P. S.; Řezáč, J.; Jílková, A.; Horn, M.; Mareš, M.; Hobza, P.; Lepšík, M. Quantum mechanics-based scoring rationalizes the irreversible inactivation of parasitic Schistosoma mansoni cysteine peptidase by vinyl sulfone inhibitors. J. Phys. Chem. B 2013, 117, 14973.