Structure of human aldose reductase holoenzyme in complex with statil: An approach to structure-based inhibitor design of the enzyme

Proteins: Structure, Function and Genetics

Volumn 50, Issue 2, 2003, Pages 230-238

  El Kabbani, Ossama ^a   Ramsland, Paul ^a   Darmanin, Connie ^a   Chung, Roland P T ^a   Podjarny, Alberto ^b  

^a MONASH UNIVERSITY   (Australia)

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

Author keywords

Aldose reductase inhibition; Drug design; Molecular modeling; Ternary complex; X ray crystallography

Indexed keywords

ALDEHYDE REDUCTASE; ANION; CARBOXYLIC ACID DERIVATIVE; FLUORINE; HISTIDINE; HOLOENZYME; HYDROGEN; NICOTINAMIDE; PHTHALAZINE DERIVATIVE; PONALRESTAT; TRYPTOPHAN; TYROSINE;

ARTICLE; BINDING SITE; CATALYSIS; CRYSTAL STRUCTURE; HYDROGEN BOND; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ALDEHYDE REDUCTASE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; ENZYME INHIBITORS; HOLOENZYMES; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; PHTHALAZINES; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 0037296422     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.10278     Document Type: Article

References (43)

1. Jez JM, Bennett MJ, Schlegel BP, Lewis M, Penning TM. Comparative anatomy of the aldo-keto reductase superfamily. Biochem J 1997;326:625-636.
2. Warren JC, Murdock GL, Ma Y, Goodman SR, Zimmer WE. Molecular cloning of testicular 20 alpha-hydroxysteriod dehydrogenase: Identity with aldose reductase. Biochemistry 1993;32:1401-1406.
3. Kinoshita JH, Nishimura C. The involvement of aldose reductase in diabetic complications. Diabetes Metab Rev 1988;4:323-337.
4. Dunlop M. Aldose reductase and the role of the polyol pathway in diabetic nephropathy. Kidney Int. 2000;77 (Suppl):S3-S12.
5. Yabe-Nishimura C. Aldose reductase in glucose toxicity: A potential target for the prevention of diabetic complications. Pharmacol Rev 1998;50:21-33.
6. Oates PJ, Mylari BL. Aldose reductase inhibitors: Therapeutic implications for diabetic complications. Exp Opin Invest Drugs 1999;8:1-25.
7. Pfeifer MA, Schumer MP, Gelber DA. Aldose reductase inhibitors: The end of an era or the need for different trial design. Diabetes 1997;46:S82-S89.
8. Sato S, Kador PF. Inhibition of aldehyde reductase by aldose reductase inhibitors. Biochem Pharmacol 1990;40:1033-1042.
9. El-Kabbani O, Wilson DK, Petrash JM, Quiocho FA. Structural features of the aldose reductase and aldehyde reductase inhibitorbinding sites. Mol Vis 1998;4:19-25.
10. Costantino L, Rastelli G, Gamberini MC, Barlocco D. Pharmacological approaches to the treatment of diabetic complications. Exp Opin Ther Patents 2000;10:1245-1262.
11. Wilson DK, Tarle I, Petrash JM, Quiocho FA. Refined 1.8 Å structure of human aldose reductase complexed with the potent inhibitor zopolrestat. Proc Natl Acad Sci USA 1993;90:9847-9851.
12. Urzhumtsev A, Tête-Favier F, Mitschler A, Barbanton J, Barth P, Urzhumtseva L, Biellmann J-F, Podjarny AD, Moras DA. "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.
13. Harrison DHT, Bohren KM, Petsko GA, Ringe D, Gabbay KH. The alrestatin double-decker: Binding of two inhibitor molecules to human aldose reductase reveals a new specificity determinant. Biochemistry 1997;36:16134-16140.
14. Rogniaux H, Van Dorsselaer A, Barth P, Biellmann J-F, Barbanton J, Van Zandt M, Chevrier B, Howard E, Mitschler A, Potier N, Urzhumtseva L, Moras D, Podjarny A. Binding of aldose reductase inhibitors: Correlation of crystallographic and mass spectrometric studies. J Am Soc Mass Spectrom 1999;10:635-647.
15. Oka M, Matsumoto Y, Sugiyama S, Tsuruta N, Matsushima M. A potent aldose reductase inhibitor, (2S,4S)-6-fluoro-2′,5′-dioxyspiro[chroman-4,4′- imidazoline]-2-carboxamide (fidarestat): Its absolute configuration and interaction with aldose reductase by X-ray crystallography. J Med Chem 2000;43:2479-2483.
16. El-Kabbani O, Carper DA, McGowan MH, Devedjiev Y, ReesMilton KJ, Flynn TG. Studies on the inhibitor-binding site of porcine aldehyde reductase: Crystal structure of the holoenzymeinhibitor ternary complex. Proteins 1997;29:186-192.
17. El-Kabbani O, Old SE, Ginell SL, Carper DA. Aldose and aldehyde reductases: Structure-function studies on the coenzyme and inhibitor-binding sites. Mol Vis 1999;5:20-26.
18. Barski OA, Gabbay KH, Bohren KM. The C-terminal loop of aldehyde reductase determines the substrate and inhibitor specificity. Biochemistry 1996;35:14276-14280.
19. Lee YS, Chen Z, Kador PF. Molecular modeling studies of the binding modes of aldose reductase inhibitors at the active site of human aldose reductase. Bioorg Med Chem 1998;6:1811-1819.
20. Hohman TC, El-Kabbani O, Malamas MS, Lai K, Putilina T, McGowan MH, Wane Y-Q, Carper DA. Probing the inhibitorbinding site of aldose reductase with site-directed mutagenesis. Eur J Biochem 1998;256:310-316
21. El-Kabbani O, Carper DA, McGowan MH, Ginell SL. Crystal structure of porcine aldehyde reductase at 2.0 Å resolution: Modeling an inhibitor in the active site of the enzyme. Protein Pept Lett 1996;3:427-434.
22. El-Kabbani O, Rogniaux H, Barth P, Chung R, Fletcher E, Dorsselaer A, Podjarny A. Aldose and aldehyde reductases: Correlation of molecular modeling and mass spectrometric studies on the binding of inhibitors to the active site. Proteins 2000;41:407-414.
23. Chung S, La Mendola J. Cloning and sequence determination of human placental aldose reductase gene. J Biol Chem 1989;264:14775-14777.
24. Lamour V, Barth P, Rogniaux H, Poterszman A, Howard E, Mitschler A, Van Dorsselaer A, Podjarny A, Moras D. Production of crystals of human aldose reductase with very high resolution diffraction. Acta Crystallogr 1999;D55:721-723.
25. Matthews BW. Solvent content of protein crystals. J Mol Biol 1968;33:491-497.
26. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Meth Enzymol 1997;276:307-326.
27. Calderone V, Chevrier B, Van Zandt M, Lamour V, Howard E, Poterszman A, Barth P, Mitschler A, Lu J, Dvornik DM, Klebe G, Kraemer O, Moorman AR, Moras D, Podjarny A. The structure of aldose reductase bound to the inhibitor IDD384. Acta Crystallogr 2000;D56:536-540.
28. Adams PD, Pannu NS, Read RJ, Brünger AT. Cross-validated maximum likelihood enhances crystallographic simulated annealing refinement. Proc Natl Acad Sci USA 1997;94:5018-5023.
29. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, GrosseKunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography and NMR system - A new software suite for macromolecular structure determination. Acta Crystallogr 1998;D54:905-921.
30. Roussel A, Cambillau C. TURBO-FRODO molecular graphics program. In: Silicon Graphics Geometry Partner Directory. Mountain View, CA: Silicon Graphics; 1989. p 77-78.
31. Goodford PJ. A computational procedure for determining energetically favourable binding sites on biologically important macromolecules. J Med Chem 1985;28:849-857.
32. Darmanin C, El-Kabbani O. Modelling studies of the active site of human sorbitol dehydrogenase: An approach to structure-based inhibitor design of the enzyme. Bioorg Medchem Lett 2001;11:3133-3136.
33. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
34. Ramachandran GN, Sasisekharan V. Conformation of proteins and polypeptides. Adv Protein Chem 1968;23:283-437.
35. Rondeau J-M, Tête-Favier F, Podjarny A, Reymann J-M, Barth P, Biellmann J-F, Moras D. Novel NADPH-binding domain revealed by the crystal structure ofaldose reductase. Nature 1992;355:469-472.
36. Sorbinil Retinopathy Trial Research Group. A randomized trial of sorbinil, an aldose reductase inhibitor, in diabetic retinopathy. Arch Ophthalmol 1990;108:1234-1244.
37. Foppiano M, Lombardo G. Worldwide pharmacovigilance systems and tolrestat withdrawal. Lancet 1990;349:399-400.
38. El-Kabbani O, Judge K, Ginell SL, Myles DA, DeLucas LJ, Flynn TG. Structure of porcine aldehyde reductase holoenzyme. Nat Struct Biol 1995;2:687-692.
39. El-Kabbani O, Green NC, Lin G, Carson M, Narayana SVL, Moore KM, Flynn TG, DeLucas LJ. Structures of human and porcine aldehyde reductase: An enzyme implicated in diabetic complications. Acta Crystallogr 1994;D50:859-868.
40. Rees-Milton KJ, Jia Z, Green NC, Bhatia M, El-Kabbani O, Flynn TG. Aldehyde reductase: The role of C-terminal residues in defining substrate and cofactor specificities. Arch Biochem Biophys 1998;355:137-144.
41. Luzzati PV. Traitement statistique des erreurs dans la determination des structures cristallines. Acta Crystallogr 1952;5:802-810.
42. Read RJ. Improved fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr 1986;A42:140-149.
43. Kraulis PJ. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 1991;24:946-950.