Nitric oxide synthases activation and inhibition by metallacarborane- cluster-based isoform-specific affectors

Journal of Medicinal Chemistry

Volumn 55, Issue 22, 2012, Pages 9541-9548

  Kaplánek, Robert ^a   Martásek, Pavel ^b,c   Grüner, Bohumír ^d   Panda, Satya ^e   Rak, Jakub ^a   Masters, Bettie Sue Siler ^e   Král, Vladimír ^a,f   Roman, Linda J ^e  

^a INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c CHARLES UNIVERSITY   (Czech Republic)

^d INSTITUTE OF INORGANIC CHEMISTRY   (Czech Republic)

^e University of Texas Health Science Center   (United States)

^f Zentiva Prague   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

BORON DERIVATIVE; CARBORANE DERIVATIVE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ARTICLE; ENZYME ACTIVATION; ENZYME INHIBITION; HYDROGEN BOND; NEUTRON CAPTURE THERAPY; RING OPENING;

BORON COMPOUNDS; COBALT; HUMANS; MODELS, CHEMICAL; MOLECULAR STRUCTURE; NITRIC OXIDE SYNTHASE; ORGANOMETALLIC COMPOUNDS; PROTEIN ISOFORMS;

EID: 84870012199     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm300805x     Document Type: Article

References (77)

1. Masters, B. S. In Nitric Oxide, Biology and Pathobiology; Ignarro, L. J., Ed.; Academic Press: New York, 2000.
2. Roman, L. J.; Martásek, P.; Masters, B. S. S. Intrinsic and extrinsic modulation of nitric oxide synthase activity Chem. Rev. 2002, 102 (4) 1179-1189
3. Michel, T.; Feron, O. Nitric oxide synthases: which, where, how, and why? J. Clin. Invest. 1997, 100 (9) 2146-2152
4. Alderton, W. K.; Cooper, C. E.; Knowles, R. G. Nitric oxide synthases: structure, function and inhibition Biochem. J. 2001, 357, 593-615
5. Stuehr, D. J.; Santolini, J.; Wang, Z. Q.; Wei, C. C.; Adak, S. Update on mechanism and catalytic regulation in the NO synthases J. Biol. Chem. 2004, 279 (35) 36167-36170
6. Andrew, P. J.; Mayer, B. Enzymatic function of nitric oxide synthases Cardiovasc. Res. 1999, 43 (3) 521-531
7. Li, H. Y.; Poulos, T. L. Structure-function studies on nitric oxide synthases J. Inorg. Biochem. 2005, 99 (1) 293-305
8. Bruckdorfer, R. The basics about nitric oxide Mol. Aspects Med. 2005, 26 (1-2) 3-31
9. Gomez-Vidal, J. A.; Martásek, P.; Roman, L. J.; Silverman, R. B. Potent and selective conformationally restricted neuronal nitric oxide synthase inhibitors J. Med. Chem. 2004, 47 (3) 703-710
10. Hah, J. M.; Martásek, P.; Roman, L. J.; Silverman, R. B. Aromatic reduced amide bond peptidomimetics as selective inhibitors of neuronal nitric oxide synthase J. Med. Chem. 2003, 46 (9) 1661-1669
11. Hah, J. M.; Roman, L. J.; Martásek, P.; Silverman, R. B. Reduced amide bond peptidomimetics. (4 S)- N -(4-Amino-5-[aminoalkyl]aminopentyl)- N ′-nitroguanidines, potent and highly selective inhibitors of neuronal nitric oxide synthase J. Med. Chem. 2001, 44 (16) 2667-2670
12. Huang, H.; Martásek, P.; Roman, L. J.; Masters, B. S. S.; Silverman, R. B. N -omega-Nitroarginine-containing dipeptide amides. Potent and highly selective inhibitors of neuronal nitric oxide synthase J. Med. Chem. 1999, 42 (16) 3147-3153
13. Huang, H.; Martásek, P.; Roman, L. J.; Silverman, R. B. Synthesis and evaluation of peptidomimetics as selective inhibitors and active site probes of nitric oxide synthases J. Med. Chem. 2000, 43 (15) 2938-2945
14. Huang, H.; Martásek, P.; Roman, L. J.; Silverman, R. B. Synthesis and evaluation of dipeptide amides containing N -omega-nitroarginine and d -2,4-diaminobutyric acids as inhibitors of neuronal nitric oxide synthase J. Enzyme Inhib. 2001, 16 (3) 233-239
15. Lee, Y.; Marletta, M. A.; Martásek, P.; Roman, L. J.; Masters, B. S. S.; Silverman, R. B. Conformationally-restricted arginine analogues as alternative substrates and inhibitors of nitric oxide syntheses Bioorg. Med. Chem. 1999, 7 (6) 1097-1104
16. Lee, Y.; Martásek, P.; Roman, L. J.; Masters, B. S. S.; Silverman, R. B. Imidazole-containing amino acids as selective inhibitors of nitric oxide synthases Bioorg. Med. Chem. 1999, 7 (9) 1941-1951
17. Silverman, R. B.; Huang, H.; Marletta, M. A.; Martásek, P. Selective inhibition of neuronal nitric oxide synthase by N -omega- nitroarginine- and phenylalanine-containing dipeptides and dipeptide esters J. Med. Chem. 1997, 40 (18) 2813-2817
18. Zhang, H. Q.; Fast, W.; Marletta, M. A.; Martásek, P.; Silverman, R. B. Potent and selective inhibition of neuronal nitric oxide synthase by N -omega-propyl- l -arginine J. Med. Chem. 1997, 40 (24) 3869-3870
19. Silverman, R. B. Design of selective neuronal nitric oxide synthase inhibitors for the prevention and treatment of neurodegenerative diseases Acc. Chem. Res. 2009, 42 (3) 439-451
20. Ji, H.; Tan, S.; Igarashi, J.; Li, H.; Derricke, M.; Martásek, P.; Roman, L. J.; Vásquez-Vivar, J.; Poulos, T. L.; Silverman, R. B. Selective neuronal nitric oxide synthase inhibitors and the prevention of cerebral palsy Ann. Neurol. 2009, 65 (2) 209-217
21. Erdal, E. P.; Litzinger, E. A.; Seo, J. W.; Zhu, Y. Q.; Ji, H. T.; Silverman, R. B. Selective neuronal nitric oxide synthase inhibitors Curr. Top. Med. Chem. 2005, 5 (7) 603-624
22. Issa, F.; Kassiou, M.; Rendina, L. M. Boron in drug discovery: carboranes as unique pharmacophores in biologically active compounds Chem. Rev. 2011, 111 (9) 5701-5722
23. Scholz, M.; Hey-Hawkins, E. Carbaboranes as pharmacophores: properties, synthesis, and application strategies Chem. Rev. 2011, 111 (11) 7035-7062
24. Hawthorne, M. F. The role of chemistry in the development of boron neutron-capture therapy of cancer Angew. Chem., Int. Ed. Engl. 1993, 32 (7) 950-984
25. Tjarks, W. The use of boron clusters in the rational design of boronated nucleosides for neutron capture therapy of cancer J. Organomet. Chem. 2000, 614, 37-47
26. Bregadze, V. I.; Sivaev, I. B.; Glazun, S. A. Polyhedral boron compounds as potential diagnostic and therapeutic antitumor agents Anti-Cancer Agents Med. Chem. 2006, 6 (2) 75-109
27. Crossley, E. L.; Ziolkowski, E. J.; Coderre, J. A.; Rendina, L. M. Boronated DNA-binding compounds as potential agents for boron neutron capture therapy Mini-Rev. Med. Chem. 2007, 7 (3) 303-313
28. Valliant, J. F.; Guenther, K. J.; King, A. S.; Morel, P.; Schaffer, P.; Sogbein, O. O.; Stephenson, K. A. The medicinal chemistry of carboranes Coord. Chem. Rev. 2002, 232 (1-2) 173-230
29. Armstrong, A. F.; Valliant, J. F. The bioinorganic and medicinal chemistry of carboranes: from new drug discovery to molecular imaging and therapy Dalton Trans. 2007, 38, 4240-4251
30. Hawthorne, M. F.; Maderna, A. Applications of radiolabeled boron clusters to the diagnosis and treatment of cancer Chem. Rev. 1999, 99 (12) 3421-3434
31. Soloway, A. H.; Tjarks, W.; Barnum, B. A.; Rong, F. G.; Barth, R. F.; Codogni, I. M.; Wilson, J. G. The chemistry of neutron capture therapy Chem. Rev. 1998, 98 (4) 1515-1562
32. Lesnikowski, Z. J. Boron units as pharmacophores. New applications and opportunities of boron cluster chemistry Collect. Czech. Chem. Commun. 2007, 72 (12) 1646-1658
33. Cígler, P.; Kožíšek, M.; Řezá čová, P.; Brynda, J.; Otwinowski, Z.; Pokorná, J.; Plešek, J.; Grüner, B.; Dolečková- Marešová, L.; Máša, M.; Sedláček, J.; Bodem, J.; Kräusslich, H. G.; Král, V.; Konvalinka, J. From nonpeptide toward noncarbon protease inhibitors: metallacarboranes as specific and potent inhibitors of HIV protease Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (43) 15394-15399
34. Kožíšek, M.; Cígler, P.; Lepší k, M.; Fanfrlík, J.; Řezáčová, P.; Brynda, J.; Pokorná, J.; Plešek, J.; Grüner, B.; Šaš ková, K. G.; Václavíková, J.; Král, V.; Konvalinka, J. Inorganic polyhedral metallacarborane inhibitors of HIV protease: a new approach to overcoming antiviral resistance J. Med. Chem. 2008, 51 (15) 4839-4843
35. Řezáčová, P.; Pokorná, J.; Brynda, J.; Kožíšek, M.; Cígler, P.; Lepšík, M.; Fanfrlík, J.; Rezáč, J.; Šašková, K. G.; Sieglová, I.; Plešek, J.; Šícha, V.; Grüner, B.; Oberwinkler, H.; Sedláček, J.; Kräusslich, H. G.; Hobza, P.; Král, V.; Konvalinka, J. Design of HIV protease inhibitors based on inorganic polyhedral metallacarboranes J. Med. Chem. 2009, 52 (22) 7132-7141
36. Scholz, M.; Bensdorf, K.; Gust, R.; Hey-Hawkins, E. Asborin: the carbaborane analogue of aspirin ChemMedChem 2009, 4 (5) 746-748
37. Scholz, M.; Kaluderović, G. N.; Kommera, H.; Paschke, R.; Will, J.; Sheldrick, W. S.; Hey-Hawkins, E. Carbaboranes as pharmacophores: similarities and differences between aspirin and asborin Eur. J. Med. Chem. 2011, 46 (4) 1131-1139
38. Page, M. F. Z.; Jalisatgi, S. S.; Maderna, A.; Hawthorne, M. F. Design and synthesis of a candidate alpha-human thrombin irreversible inhibitor containing a hydrophobic carborane pharmacophore Synthesis 2008, 4, 555-563
39. Endo, Y.; Yoshimi, T.; Kimura, K.; Itai, A. Protein kinase C modulators bearing dicarba-closo-dodecaborane as a hydrophobic pharmacophore Bioorg. Med. Chem. Lett. 1999, 9 (17) 2561-2564
40. Tsuji, M.; Koiso, Y.; Takahashi, H.; Hashimoto, Y.; Endo, Y. Modulators of tumor necrosis factor alpha production bearing dicarba-closo-dodecaborane as a hydrophobic pharmacophore Biol. Pharm. Bull. 2000, 23 (4) 513-516
41. Hawthorne, M. F.; Young, D. C.; Wegner, P. A. Carbametallic boron hydride derivatives. I. Apparent analogs of ferrocene and ferricinium ion J. Am. Chem. Soc. 1965, 87 (8) 1818-1819
42. Plešek, J. Potential applications of the boron cluster compounds Chem. Rev. 1992, 92 (2) 269-278
43. Plešek, J.; Heřmánek, S.; Franken, A.; Císařová, I.; Nachtigal, C. Dimethyl sulfate induced nucleophilic substitution of the [bis(1,2-dicarbollido)-3-cobalt(1-)]ate ion. Syntheses, properties and structures of its 8,8′-mu-sulfato, 8-phenyl and 8-dioxane derivatives Collect. Czech. Chem. Commun. 1997, 62 (1) 47-56
44. Sivaev, I. B.; Bregadze, V. I. Chemistry of cobalt bis(dicarbollides). A review Collect. Czech. Chem. Commun. 1999, 64 (5) 783-805
45. Plešek, J.; Grüner, B.; Báča, J.; Fusek, J.; Císařová, I. Syntheses of the B-(8)-hydroxy- and B((8),(8)′)-dihydroxy-derivatives of the bis(1,2-dicarbollido)-3- colbalt(1-)ate ion by its reductive acetoxylation and hydroxylation: molecular structure of [8,8′-mu-CH3C(O)(2)(1,2-C2B9H10)(2)-3-Co](0) zwitterion determined by X-ray diffraction analysis J. Organomet. Chem. 2002, 649 (2) 181-190
46. Plešek, J.; Grüner, B.; Císařová, I.; Báča, J.; Selucký, P.; Rais, J. Functionalized cobalt bis(dicarbollide) ions as selective extraction reagents for removal of M2+ and M3+ cations from nuclear waste, crystal and molecular structures of the [8,8′-mu-CIP(O)(O)(2)(1,2-C2B9H10)(2)-3,3′-Co]HN(C2H5)(3) and [8,8′-mu-Et2NP(O)(O)(2) (1,2-C2B9H10)(2)-3,3′-Co](HN(CH3)(3)) J. Organomet. Chem. 2002, 657 (1-2) 59-70
47. Matějíček, P.; Cígler, P.; Procházka, K.; Král, V. Molecular assembly of metallacarboranes in water: light scattering and microscopy study Langmuir 2006, 22 (2) 575-581
48. Matějíček, P.; Cígler, P.; Olejniczak, A. B.; Andrysiak, A.; Wojtczak, B.; Procházka, K.; Lesnikowski, Z. J. Aggregation behavior of nucleoside-boron cluster conjugates in aqueous solutions Langmuir 2008, 24 (6) 2625-2630
49. Semioshkin, A. A.; Sivaev, I. B.; Bregadze, V. I. Cyclic oxonium derivatives of polyhedral boron hydrides and their synthetic applications Dalton Trans. 2008, 8, 977-992
50. Sivaev, I. B.; Bregadze, V. V. Polyhedral boranes for medical applications: current status and perspectives Eur. J. Inorg. Chem. 2009, 11, 1433-1450
51. Rak, J.; Kaplánek, R.; Král, V. Solubilization and deaggregation of cobalt bis(dicarbollide) derivatives in water by biocompatible excipients Bioorg. Med. Chem. Lett. 2010, 20 (3) 1045-1048
52. Rak, J.; Jakubek, M.; Kaplánek, R.; Matějíč ek, P.; Král, V. Cobalt bis(dicarbollide) derivatives: solubilization and self-assembly suppression Eur. J. Med. Chem. 2011, 46 (4) 1140-1146
53. Fanfrlík, J.; Lepšik, M.; Horinek, D.; Havlas, Z.; Hobza, P. Interaction of carboranes with biomolecules: formation of dihydrogen bonds ChemPhysChem 2006, 7 (5) 1100-1105
54. Li, H. Y.; Shimizu, H.; Flinspach, M.; Jamal, J.; Yang, W. P.; Xian, M.; Cai, T. W.; Wen, E. Z.; Jia, Q. A.; Wang, P. G.; Poulos, T. L. The novel binding mode of N -alkyl- N ′-hydroxyguanidine to neuronal nitric oxide synthase provides mechanistic insights into NO biosynthesis Biochemistry 2002, 41 (47) 13868-13875
55. Flinspach, M.; Li, H. Y.; Jamal, J.; Yang, W. P.; Huang, H.; Silverman, R. B.; Poulos, T. L. Structures of the neuronal and endothelial nitric oxide synthase heme domain with d -nitroarginine-containing dipeptide inhibitors bound Biochemistry 2004, 43 (18) 5181-5187
56. Raman, C. S.; Li, H.; Martásek, P.; Král, 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 (7) 939-50
57. 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 (3) 233-242
58. Crane, B. R.; Arvai, A. S.; Ghosh, D. K.; Wu, C. Q.; Getzoff, E. D.; Stuehr, D. J.; Tainer, J. A. Structure of nitric oxide synthase oxygenase dimer with pterin and substrate Science 1998, 279 (5359) 2121-2126
59. Martásek, P.; Liu, Q.; Liu, J. W.; Roman, L. J.; Gross, S. S.; Sessa, W. C.; Masters, B. S. S. Characterization of bovine endothelial nitric oxide synthase expressed in E-coli Biochem. Biophys. Res. Commun. 1996, 219 (2) 359-365
60. Roman, L. J.; Martásek, P.; Miller, R. T.; Harris, D. E.; de La Garza, M. A.; Shea, T. M.; Kim, J. J.; Masters, B. S. The C termini of constitutive nitric-oxide synthases control electron flow through the flavin and heme domains and affect modulation by calmodulin J. Biol. Chem. 2000, 275 (38) 29225-29232
61. Roman, L. J.; Miller, R. T.; de la Garza, M. A.; Kim, J. J. P.; Masters, B. S. S. The C terminus of mouse macrophage inducible nitric-oxide synthase attenuates electron flow through the flavin domain J. Biol. Chem. 2000, 275 (29) 21914-21919
62. Roman, L. J.; Sheta, E. A.; Martásek, P.; Gross, S. S.; Liu, Q.; Masters, B. S. S. High-level expression of functional-rat neuronal nitric-oxide synthase in Escherichia-coli Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (18) 8428-8432
63. Zhang, M. J.; Vogel, H. J. Characterization of the calmodulin-binding domain of rat cerebellar nitric-oxide synthase J. Biol. Chem. 1994, 269 (2) 981-985
64. Hevel, J. M.; Marletta, M. A. Nitric-oxide synthase assays Methods Enzymol. 1994, 233, 250-258
65. Connors, K. A. In Binding Constants; John Wiley & Sons: New York, 1981.
66. Plešek, J.; Rajabi, F. H.; Vangani, V.; Fusek, J. Constitution and Properties of the 8,8(′)-Mu-H2no (1,2-C2b9h10)2-3-Co Bridged Cobaltaborane Collect. Czech. Chem. Commun. 1994, 59 (6) 1326-1336
67. Plešek, J.; Grüner, B.; Heřmánek, S.; Fusek, J.; Votavová, H. Constitution and HPLC resolution of enantiomers of the [8,4′-Mu-R2n-Commo-(1,2-C2b9h10)2-3-Co] complex: the 3rd isomer of nitrogen-bridged bisicosahedral cobaltacarborane Collect. Czech. Chem. Commun. 1994, 59 (2) 374-380
68. Plešek, J.; Heřmánek, S.; Baše, K.; Todd, L. J.; Wright, W. F. Zwitterionic compounds of 8,8′-X(C2B9H10)2Co series with monoatomic O, S, Se, Te, N bridges between carborane ligands Collect. Czech. Chem. Commun. 1976, 41 (12) 3509-3515
69. Janoušek, Z.; Plešek, J.; Heřmánek, S.; Baše, K.; Todd, L. J.; Wright, W. F. Synthesis and characteristics of sulfur interligand bridge-derivatives and of some S-substituted compounds in the (C2B9H11)2Co-series: conformations of (C2B9H11)2Mx-metallocarboranes Collect. Czech. Chem. Commun. 1981, 46 (11) 2818-2833
70. Grüner, B.; Císařová, I.; Čá slavský, J.; Bonnetot, B.; Cornu, D. Synthesis of 12-hydroxy and 12-dioxane derivatives of the closo-1-carbadodecaborate(1-) ion. Variations on the Plesek's cobalt bis(dicarbollide) pattern Collect. Czech. Chem. Commun. 2002, 67 (7) 953-964
71. Holub, J.; Grüner, B.; Císařová, I.; Fusek, J.; Plzák, Z.; Teixidor, F.; Viñas, C.; Štíbr, B. A series of the twelve-vertex ferratricarbollides [2-(eta(5)-C5H5)-9-X-closo-2,1, 7,9-FeC3B8H10] (where x = H2N, MeHN, Me2N, (BuHN)-H-t, Bu-t(Me)N). A highly stable metallatricarbaborane system with amine functions in the para position to the metal center Inorg. Chem. 1999, 38 (12) 2775-2780
72. Hertler, W. R.; Raasch, M. S. Chemistry of Bboranes. 14. Amination of B10h10-2 + B12h12-2 with Hydroxylamine- O -sulfonic acid J. Am. Chem. Soc. 1964, 86 (18) 3661-3668
73. Grüner, B.; Bonnetot, B.; Mongeot, H. Synthesis of N- and B-substituted derivatives of closo-amino-undecahydro-dodecaborate(1-) anion Collect. Czech. Chem. Commun. 1997, 62 (8) 1185-1204
74. Sivaev, I. B.; Starikova, Z. A.; Sjöberg, S.; Bregadze, V. I. Synthesis of functional derivatives of the [3,3′-Co(1,2-C2B2H11)(2)](-) anion J. Organomet. Chem. 2002, 649 (1-2) 1-8
75. Katritzky, A. R.; Rogovoy, B. V. Recent developments in guanylating agents ARKIVOC 2005, 49-87
76. Lee, Y. B.; Folk, J. E. Branched-chain and unsaturated 1,7-diaminoheptane derivatives as deoxyhypusine synthase inhibitors Bioorg. Med. Chem. 1998, 6 (3) 253-270
77. Kraus, T.; Budešínský, M.; Závada, J. Synthesis of per-6-guanidinylated cyclodextrins Tetrahedron Lett. 2006, 47 (5) 679-681