Unusual binding mode of the 2S4R stereoisomer of the potent aldose reductase cyclic imide inhibitor fidarestat (2S4S) in the 15 K crystal structure of the ternary complex refined at 0.78 Å resolution: Implications for the inhibition mechanism

Journal of Medicinal Chemistry

Volumn 51, Issue 5, 2008, Pages 1478-1481

  Zhao, Hai Tao ^a   Hazemann, Isabelle ^b   Mitschler, Andre ^b   Carbone, Vincenzo ^a   Joachimiak, Andrzej ^c   Ginell, Steve ^c   Podjarny, Alberto ^b   El Kabbani, Ossama ^a  

^a MONASH UNIVERSITY   (Australia)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE REDUCTASE; ALDOSE REDUCTASE INHIBITOR; FIDARESTAT;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CRYSTAL STRUCTURE; DRUG BINDING; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG STRUCTURE; ENZYME INHIBITION; INHIBITION KINETICS; NUCLEOTIDE SEQUENCE; STEREOISOMERISM; STRUCTURE ACTIVITY RELATION;

ALDEHYDE REDUCTASE; CRYSTALLOGRAPHY, X-RAY; HUMANS; IMIDAZOLIDINES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN BINDING; STEREOISOMERISM;

EID: 41649116852     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm701514k     Document Type: Article

References (31)

1. Jez, J. M.; Bennet, M. J.; Schlegel, B. P.; Lewis, M.; Penning, T. M. Comparative anatomy of the aldo-keto reductase superfamily. Biochem. J. 1997, 326, 625-636.
2. Warren, J. C.; Murdock, G. L.; Ma, Y.; Goodman, S. R.; Zimmer, W. E. Molecular cloning of testicular 20alpha-hydroxysteriod dehydrogenase: identity with aldose reductase. Biochemistry 1993, 32, 1401-1406.
3. Jeffery, J.; Jornvall, H. Sorbitol dehydrogenase. Adv. Enzymol. Relat. Areas Mol. Biol. 1988, 61, 47-106.
4. King, G. L.; Brownlee, M. B. The cellular and molecular mechanisms of diabetic complications. In Endocrinology and Metabolism Clinics of North America; Brownlee, M. B., King, G. L., Eds.; WB Saunders: Philadelphia, PA, 1996; Vol 25, pp 255-270.
5. Cameron, N. E.; Cotter, M. A.; Hohman, T. C. Interacrions between essential fatty acid, prostanoid, polyol pathway and nitric oxide mechanisms in the neurovascular deficit of diabetic rats. Diabetologia 1996, 39, 172-182.
6. Lee, A. Y. W.; Chung, S. S. M. Contributions of polyol pathway to oxdidative stress in diabetic cataract. FASEB J. 1999, 13, 23-30.
7. Chan, N. N.; Vallance, P.; Colhun, H. M. Nitric oxide and vascular responses in Type 1 diabetes. Diabetologia 2000, 43, 137-147.
8. Wrobel, J.; Milien, J.; Sredy, J.; Dietrich, A.; Gorham, B. J.; Malamas, M.; Kelly, J. M.; Bauman, J. G.; Harrison, M. C.; Jones, L. R.; Guinosso, C.; Sestanj. Syntheses of tolrestat analogues containing additional substituents in the ring and their evaluation as aldose reductase inhibitors. Identification of potent, orally active 2-fluoro derivatives. J. Med. Chem. 1991, 34, 2504-2520.
9. Yamagishi, M.; Yamada, Y.; Ozaki, K.; Asao, M.; Shimizu, R.; Suzuki, M.; Matsumoto, M.; Matsuoka, Y.; Mataumoto, K. Biological activities and quantitative structure-activity relationships of spiro[imidazolidine-4, 4′(1′H)-quinazoline]-2,2′,5(3H0-triones as aldose reductase inhibitors. J. Med. Chem. 1992, 35, 2085-2094.
10. Costantino, L.; Rastelli, G.; Vianello, P.; Cignarella, G.; Barlocco, D. Diabetes complications and their potential prevention: aldose reductase inhibition and other approaches. Med. Res. Rev. 1999, 19, 3-23.
11. Mylari, B.; Larson, E.; Beyer, T.; Zembrowski, W.; Aldinger, C.; Dee, M.; Siegel, T.; Singletont, D. Novel, potent aldose reductase Inhibitors: 3,4-Dihydro-4-oxo-3-([5-(trifluoromethyl)-2-benzothiazolyl]methyl} -1-phthalazineacetic acid (Zopolrestat) and congeners. J. Med. Chem. 1991, 34, 108-122.
12. Kaul, C.; Ramarao, P. The role of aldose reductase inhibitors in diabetic complications: Recent trends. Methods Find. Exp. Clin. Pharmacol. 2001, 23, 465-475.
13. Miyamoto, S. Recent advances in aldose reductase inhibitors: Potential agents for the treatment of diabetic complications. Expert Opin. Ther. Pat. 2002, 12, 621-631.
14. El-Kabbani, O.; Darmanin, C.; Schneider, T. R.; Hazemann, I.; Ruiz, F.; Oka, M.; Joachimiak, A.; Schulze-Briese, C.; Tomizaki, T.; Mitschler, A.; Podjarny, A. Ultrahigh resolution drug design. II. Atomic resolution structures of human aldose reductase holoenzyme complexed with fidarestat and minalrestat: Implications for the binding of cyclic imide inhibitors. Proteins 2004, 55, 805-813.
15. Malamas, M. S.; Hohman, T. C.; Milen. Novel spirosuccinimide aldose reductase inhibitors derived from isoquinoline-1,3-diones:2[(4-bromo-2- fluorophenyl)methyl]-6-fluorospiro[isoquinoline-4(1H), 3′-pyrrolidine]-1,2′,3,5′(2H)-tetrone and congeners. J. Med. Chem. 1994, 37, 2043-2058.
16. Malamas, M. S.; Hohman, T. C. N-substituted spirosuccinimide, spiropyridazine, spiroazetidine and acetic acid aldose reductase inhibitors derived from isoquinoline-1, 3-diones. J. Med. Chem. 1994, 37, 2059-2070.
17. Negoro, T.; Murata, M.; Ueda, S.; Fujitani, B.; Ono, Y.; Kuromiya, A.; Komiya, M.; Suzuki, K.; Matsumoto, J. Novel, highly potent aldose reductase inhibitors: R-(-)-2-(4-bromo-2-fluorobenzyl)-1,2,3,4-tetrahydropyrrolo[1, 2-a]pyrazine-4-spiro-3′-pyrolidine-1,2′,3,5-tetrone(AS-3201) and its congeners. J. Med. Chem. 1998, 41, 4118-4129.
18. El-Kabbani, O.; Darmanin, C.; Oka, M.; Schulze-Briese, C.; Tomizaki, T.; Hazemann, I.; Mitschler, A.; Podjarny, A. High-resolution structures of human aldose reductase holoenzyme in complex with stereoisomers of the potent inhibitor Fidarestat: Stereospecific interaction between the enzyme and a cyclic imide type inhibitor. J. Med. Chem. 2004, 47, 4530-4537.
19. Rondeau, J. M.; Tt̂e-Favier, F.; Podjarny, A.; Reymann, J. M.; Barth, P.; Biellmann, J. F.; Moras, D. Novel NADPH-binding domain revealed by the crystal structure of aldose reductase. Nature 1992, 355, 469-472.
20. El-Kabbani, O.; Wilson, D.; Petrash, J. M.; Quiocho, F. A. Structural features of the aldose reductase and aldehyde reductase inhibitor-binding sites. Mol. Vision 1998, 4, 19-25.
21. Urzhumtsev, A.; Tt̂e-Favier, F.; Mitschler, A.; Barbanton, J.; Barth, P.; Urzhumtseva, J. F.; Biellmann, A. D.; Podjarny, A.; Moras, D. A. 'Specificity' pocket inferred from the crystal structures of the complexes of aldose reductase with the pharmaceutically important inhibitors tolrestat and sorbinil. Structure 1997, 5, 601-612.
22. De Winter, H. L.; von Itzstein, M. Aldose reductase as a target for drug design: Molecular modeling calculations on the binding of acyclic sugar substrates to the enzyme. Biochemistry 1995, 34, 8299-8308.
23. Chung, S.; La Mendola, J. Cloning and sequence determination of human placental aldose reductase gene. J. Biol. Chem. 1989, 264, 4775-14777.
24. Matthews, B. W. Solvent content of protein crystals. J. Mol. Biol. 1968, 33, 491-497.
25. Otwinowski, Z.; Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276, 307-326.
26. Brünger, A. T.; Krukowski, A.; Erickson, J. W. Slow-cooling protocols for crystallographic refinement by simulated annealing. Acta Crystallogr., Sect. A: Found. Crystallogr. 1990, 46, 585-593.
27. Sheldrick, G.; Schneider, T. SHELXL: High-resolution refinement. Methods Enzymol. 1997, 277, 319-343.
28. McRee, D. E. XtalView/Xfit - A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 1999, 125, 156-165.
29. Emsley, P.; Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 2126-2132.
30. Petrova, T.; Ginell, S.; Mitschler, A.; Hazemann, I.; Schneider, T.; Cousido, A.; Lunin, V. Y.; Joachimiak, A.; Podjarny, A. Ultrahigh-resolution study of protein atomic displacement parameters at cryotemperatures obtained with a helium cryostat. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2006, 62, 1535-44.
31. Kraulis, P. J. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 1991, 24, 946-950.