L-arginine binding to human inducible nitric oxide synthase: An antisymmetric funnel route toward isoform-specific inhibitors?

Journal of Chemical Information and Modeling

Volumn 51, Issue 6, 2011, Pages 1325-1335

  Floquet, Nicolas ^a   Hernandez, Jean François ^a   Boucher, Jean Luc ^b   Martinez, Jean ^a  

^a UNIVERSITÉ DE MONTPELLIER   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; MOLECULAR DYNAMICS; MONOMERS; NITRIC OXIDE; PORPHYRINS; POSITIVE IONS;

INDUCIBLE NITRIC OXIDE SYNTHASE; MOLECULAR DYNAMICS SIMULATIONS; NITRIC OXIDE SYNTHASES; NORMAL MODE ANALYSIS; PATHOLOGICAL CONDITIONS; REFERENCE TRAJECTORIES; SPECIFIC INHIBITORS; STEERED MOLECULAR DYNAMICS;

DIMERS;

ARGININE; ENZYME INHIBITOR; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOPROTEIN; OXYGENASE; WATER;

ARTICLE; CHEMISTRY; DRUG ANTAGONISM; DRUG DEVELOPMENT; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; HUMAN; METABOLISM; MOLECULAR DYNAMICS; MOVEMENT (PHYSIOLOGY); PROTEIN BINDING; PROTEIN DATABASE; PROTEIN TERTIARY STRUCTURE;

ARGININE; CATALYTIC DOMAIN; DATABASES, PROTEIN; DRUG DISCOVERY; ENZYME INHIBITORS; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOVEMENT; NITRIC OXIDE SYNTHASE TYPE II; OXYGENASES; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; WATER;

EID: 79959743629     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci100422v     Document Type: Article

References (54)

1. Pfeiffer, S.; Mayer, B.; Hemmens, B. Nitric oxide: Chemical puzzles posed by a biological messenger Angew. Chem., Int. Ed. 1999, 38, 1715-1731 (Pubitemid 29290930)
2. Alderton, W. K.; Cooper, C. E.; Knowles, R. G. Nitric oxide synthases: structure, function and inhibition Biochem. J. 2001, 357, 593-615 (Pubitemid 32735142)
3. Geller, D. A.; Billiar, T. R. Molecular biology of nitric oxide synthases Cancer Metastasis Rev. 1998, 17, 7-23 (Pubitemid 28194643)
4. Gosh, D. K.; Salerno, J. C. Nitric oxyde synthases: Domain structure and alignment in enzyme function and control Front. Biosci. 2003, 8, 193-209
5. Masters, B. S.; McMillan, K.; Sheta, E. A.; Nishimura, J. S.; Roman, L. J.; Martasek, P. Neuronal nitric oxide synthase, a modular enzymes formed by convergent evolution: Structure studies of a cysteine thiolate-liganded heme protein that hydroxylates L-arginine to produce NO as a cellular signal FASEB J. 1996, 10, 552-558
6. Stuehr, D. J. Mammalian nitric oxide synthases Biochim. Biophys. Acta 1999, 1411, 217-230 (Pubitemid 29221951)
7. Perreault, M.; Marette, A. Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle Nat. Med. 2001, 7, 1138-1143 (Pubitemid 33010023)
8. Hilliquin, P.; Borderie, D.; Hernvann, A.; Menkes, C. J.; Ekindjian, O. G. Nitric oxide as S-nitrosoproteins in rheumatoid arthritis Arthritis Rheum. 1997, 40, 1512-1517 (Pubitemid 27430964)
9. Brown, G. C.; Bal-Price, A. Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria Mol. Neurobiol. 2003, 27, 325-355 (Pubitemid 38156291)
10. Floyd, R. A. Antioxidants, oxidative stress, and degenerative neurological disorders Proc. Soc. Exp. Biol. Med. 1999, 222, 236-245 (Pubitemid 129708638)
11. Piehl, F.; Lidman, O. Neuroinflammation in the rat-CNS cells and their role in the regulation of immune reactions Immunol. Rev. 2001, 184, 212-225 (Pubitemid 34123777)
12. Carvalho-Filho, M. A.; Ueno, M.; Hirabara, S. M.; Seabra, A. B.; Carvalheira, J. B.; de Oliveira, M. G.; Velloso, L. A.; Curi, R.; Saad, M. J. S-nitrosation of the insulin receptor, insulin receptor substrate 1, and protein kinase B/Akt: a novel mechanism of insulin resistance Diabetes 2005, 54, 959-967 (Pubitemid 40446309)
13. Noronha, B. T.; Li, J. M.; Wheatcroft, S. B.; Shah, A. M.; Kearney, M. T. Inducible nitric oxide synthase has divergent effects on vascular and metabolic function in obesity Diabetes 2005, 54, 1082-1089 (Pubitemid 40446322)
14. Ekmekcioglu, S.; Ellerhorst, J. A.; Prieto, V. G.; Johnson, M. M.; Broemeling, L. D.; Grimm, E. A. Tumor iNOS predicts poor survival for stage III melanoma patients Int. J. Cancer 2006, 119, 861-866 (Pubitemid 44051450)
15. Ekmekcioglu, S.; Tang, C. H.; Grimm, E. A. NO news is not necessarily good news in cancer Curr. Cancer Drug Targets 2005, 5, 103-115 (Pubitemid 40488597)
16. Rimoldi, J. M.; Chimote, S. S. Inhibition of inducible nitric oxide synthase Curr. Opin. Drug Discovery Dev. 1998, 1, 183-191
17. Crane, B. R.; Arvai, A. S.; Ghosh, D. K.; Wu, C.; Getzoff, E. D.; Stuehr, D. J.; Tainer, J. A. Structure of nitric oxide oxygenase deimer with pterin and substrate Science 1998, 279, 2121-2126 (Pubitemid 28196359)
18. Fischmann, T. O.; Hruza, A.; Niu, X. D.; Fossetta, J. D.; Lunn, C. A.; Dolphin, E.; Prongay, A. J.; Reichert, P.; Lundell, D. J.; Narula, S. K.; Weber, P. C. Structural characterization of nitric oxide synthase isoforms reveals striking active-site conservation Nat. Struct. Biol. 1999, 6, 233-242 (Pubitemid 29107226)
19. Li, H.; Raman, C. S.; Glaser, C. B.; Blasko, E.; Young, T. A.; Parkinson, J. F.; Whitlow, M.; Poulos, T. L. Crystal structures of zinc-free and -bound heme domain of human inducible nitric-oxide synthase. Implications for dimer stability and comparison with endothelial nitric-oxide synthase J. Biol. Chem. 1999, 274, 21276-21284
20. Raman, C. S.; Li, H.; Martasek, P.; Kral, V.; Masters, B. S.; Poulos, T. L. Crystal structure of constitutive endothelial nitric oxide synthase: A paradigm for pterin function involving a novel metal center Cell 1998, 95, 939-950 (Pubitemid 29019046)
21. Li, H.; Igarashi, J.; Jamal, J.; Yang, W.; Poulos, T. L. Structural studies of constitutive nitric oxide synthases with diatomic ligands bound J. Biol. Inorg. Chem. 2006, 11, 753-768 (Pubitemid 44100470)
22. Li, H.; Poulos, T. L. Structure-function studies on nitric oxide synthases J. Inorg. Biochem. 2005, 99, 293-305 (Pubitemid 39642983)
23. Ji, H.; Li, H.; Flinspach, M.; Poulos, T. L.; Silverman, R. B. Computer modeling of selective regions in the active site of nitric oxide synthases: implication for the design of isoform-selective inhibitors J. Med. Chem. 2003, 46, 5700-5711 (Pubitemid 37543320)
24. Silverman, R. B. Design of selective neuronal nitric oxide synthase inhibitors for the prevention and treatment of neurodegenerative diseases Acc. Chem. Res. 2009, 42, 439-451
25. Garcin, E. D.; Arvai, A. S.; Rosenfeld, R. J.; Kroeger, M. D.; Crane, B. R.; Andersson, G.; Andrews, G.; Hamley, P. J.; Mallinder, P. R.; Nicholls, D. J.; St-Gallay, S. A.; Tinker, A. C.; Gensmantel, N. P.; Mete, A.; Cheshire, D. R.; Connolly, S.; Stuehr, D. J.; Aberg, A.; Wallace, A. V.; Tainer, J. A.; Getzoff, E. D. Anchored plasticity opens doors for selective inhibitor design in nitric oxide synthase Nat. Chem. Biol. 2008, 4, 700-707
26. Isralewitz, B.; Baudry, J.; Gullingsrud, J.; Kosztin, D.; Schulten, K. Steered molecular dynamics investigations of protein function J. Mol. Graphics Modell. 2001, 19, 13-25 (Pubitemid 32411500)
27. Mehboob, S.; Guo, L.; Fu, W.; Mittal, A.; Yau, T.; Truong, K.; Johlfs, M.; Long, F.; Fung, L. W.; Johnson, M. E. Glutamate racemase dimerization inhibits dynamic conformational flexibility and reduces catalytic rates Biochemistry 2009, 48, 7045-7055
28. Vashisth, H.; Abrams, C. F. Ligand escape pathways and (un)binding free energy calculations for the hexameric insulin-phenol complex Biophys. J. 2008, 95, 4193-4204
29. Shen, J.; Li, W.; Liu, G.; Tang, Y.; Jiang, H. Computational insights into the mechanism of ligand unbinding and selectivity of estrogen receptors J. Phys. Chem. B 2009, 113, 10436-10444
30. Wang, J.; Wang, W.; Kollman, P. A.; Case, D. A. Automatic atom type and bond type perception in molecular mechanical calculations J. Mol. Graphics Modell. 2006, 25, 247-260 (Pubitemid 44363172)
31. Wang, J.; 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, 1157-1174
32. Brooks, B. R.; Brooks, C. L.; Mackerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; Caflisch, A.; Caves, L.; Cui, Q.; Dinner, A. R.; Feig, M.; Fischer, S.; Gao, J.; Hodoscek, M.; Im, W.; Kuczera, K.; Lazaridis, T.; Ma, J.; Ovchinnikov, V.; Paci, E.; Pastor, R. W.; Post, C. B.; Pu, J. Z.; Schaefer, M.; Tidor, B.; Venable, R. M.; Woodcock, H. L.; Wu, X.; Yang, W.; York, D. M.; Karplus, M. CHARMM: the biomolecular simulation program J. Comput. Chem. 2009, 30, 1545-1614
33. Foloppe, N.; Nilsson, L. The glutaredoxin -C-P-Y-C- motif: influence of peripheral residues Structure 2004, 12, 289-300 (Pubitemid 38224551)
34. Foloppe, N.; Sagemark, J.; Nordstrand, K.; Berndt, K. D.; Nilsson, L. Structure, dynamics and electrostatics of the active site of glutaredoxin 3 from Escherichia coli: comparison with functionally related proteins J. Mol. Biol. 2001, 310, 449-470 (Pubitemid 32664879)
35. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable molecular dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802 (Pubitemid 43078511)
36. Trott, O.; Olson, A. J. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 2010, 31, 455-461
37. Morris, G. M.; Huey, R.; Lindstrom, W.; Sanner, M. F.; Belew, R. K.; Goodsell, D. S.; Olson, A. J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 2009, 30, 2785-2791
38. Morris, G. M.; Huey, R.; Lindstrom, W.; Sanner, M. F.; Belew, R. K.; Goodsell, D. S.; Olson, A. J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 2009, 30, 2785-2791
39. Floquet, N.; Hery-Huynh, S.; Dauchez, M.; Derreumaux, P.; Tamburro, A. M.; Alix, A. J. Structural characterization of VGVAPG, an elastin-derived peptide Biopolymers 2004, 76, 266-280 (Pubitemid 38724854)
40. McMillan, K.; Adler, M.; Auld, D. S.; Baldwin, J. J.; Blasko, E.; Browne, L. J.; Chelsky, D.; Davey, D.; Dolle, R. E.; Eagen, K. A.; Erickson, S.; Feldman, R. I.; Glaser, C. B.; Mallari, C.; Morrissey, M. M.; Ohlmeyer, M. H.; Pan, G.; Parkinson, J. F.; Phillips, G. B.; Polokoff, M. A.; Sigal, N. H.; Vergona, R.; Whitlow, M.; Young, T. A.; Devlin, J. J. Allosteric inhibitors of inducible nitric oxide synthase dimerization discovered via combinatorial chemistry Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 1506-1511 (Pubitemid 30118471)
41. GN-hydroxy-L-arginine oxidation Arch. Biochem. Biophys. 2003, 411, 83-92 (Pubitemid 36268782)
42. Sato, Y.; Sagami, I.; Matsui, T.; Shimizu, T. Unusual role of Tyr588 of neuronal nitric oxide synthase in controlling substrate specificity and electron transfer Biochem. Biophys. Res. Commun. 2001, 281, 621-626 (Pubitemid 32917845)
43. Wang, Z. Q.; Wei, C. C.; Sharma, M.; Pant, K.; Crane, B. R.; Stuehr, D. J. A conserved Val to Ile switch near the heme pocket of animal and bacterial nitric-oxide synthases helps determine their distinct catalytic profiles J. Biol. Chem. 2004, 279, 19018-19025 (Pubitemid 38623332)
44. Raman, C. S.; Li, H.; Martasek, P.; Southan, G.; Masters, B. S.; Poulos, T. L. Crystal structure of nitric oxide synthase bound to nitro indazole reveals a novel inactivation mechanism Biochemistry 2001, 40, 13448-13455 (Pubitemid 33130772)
45. Rosenfeld, R. J.; Garcin, E. D.; Panda, K.; Andersson, G.; Aberg, A.; Wallace, A. V.; Morris, G. M.; Olson, A. J.; Stuehr, D. J.; Tainer, J. A.; Getzoff, E. D. Conformational changes in nitric oxide synthases induced by chlorzoxazone and nitroindazoles: crystallographic and computational analyses of inhibitor potency Biochemistry 2002, 41, 13915-13925 (Pubitemid 35364865)
46. Davey, D. D.; Adler, M.; Arnaiz, D.; Eagen, K.; Erickson, S.; Guilford, W.; Kenrick, M.; Morrissey, M. M.; Ohlmeyer, M.; Pan, G.; Paradkar, V. M.; Parkinson, J.; Polokoff, M.; Saionz, K.; Santos, C.; Subramanyam, B.; Vergona, R.; Wei, R. G.; Whitlow, M.; Ye, B.; Zhao, Z. S.; Devlin, J. J.; Phillips, G. Design, synthesis, and activity of 2-imidazol-1-ylpyrimidine derived inducible nitric oxide synthase dimerization inhibitors J. Med. Chem. 2007, 50, 1146-1157 (Pubitemid 46496315)
47. Crane, B. R.; Arvai, A. S.; Gachhui, R.; Wu, C.; Ghosh, D. K.; Getzoff, E. D.; Stuehr, D. J.; Tainer, J. A. The structure of nitric oxide synthase oxygenase domain and inhibitor complexes Science 1997, 278, 425-431 (Pubitemid 27454419)
48. Matter, H.; Kumar, H. S.; Fedorov, R.; Frey, A.; Kotsonis, P.; Hartmann, E.; Frohlich, L. G.; Reif, A.; Pfleiderer, W.; Scheurer, P.; Ghosh, D. K.; Schlichting, I.; Schmidt, H. H. Structural analysis of isoform-specific inhibitors targeting the tetrahydrobiopterin binding site of human nitric oxide synthases J. Med. Chem. 2005, 48, 4783-4792 (Pubitemid 41033121)
49. Bahar, I.; Lezon, T. R.; Bakan, A.; Shrivastava, I. H. Normal Mode Analysis of Biomolecular Structures: Functional Mechanisms of Membrane Proteins Chem. Rev. 2010, 110, 1463-1497
50. Bakan, A.; Bahar, I. The intrinsic dynamics of enzymes plays a dominant role in determining the structural changes induced upon inhibitor binding Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 14349-14354
51. Floquet, N.; Marechal, J. D.; Badet-Denisot, M. A.; Robert, C. H.; Dauchez, M.; Perahia, D. Normal mode analysis as a prerequisite for drug design: application to matrix metalloproteinases inhibitors FEBS Lett. 2006, 580, 5130-5136 (Pubitemid 44415782)
52. Gorren, A. C.; List, B. M.; Schrammel, A.; Pitters, E.; Hemmens, B.; Werner, E. R.; Schmidt, K.; Mayer, B. Tetrahydrobiopterin-free neuronal nitric oxide synthase: evidence for two identical highly anticooperative pteridine binding sites Biochemistry 1996, 35, 16735-16745 (Pubitemid 27020518)
53. Gorren, A. C.; Schrammel, A.; Schmidt, K.; Mayer, B. Thiols and neuronal nitric oxide synthase: complex formation, competitive inhibition, and enzyme stabilization Biochemistry 1997, 36, 4360-4366 (Pubitemid 27171611)
54. Humphrey, W.; Dalke, A.; Schulten, K. VMD: visual molecular dynamics J. Mol. Graphics 1996, 14 (27-28) 33-38 (Pubitemid 26152973)