Structural and Thermodynamic Study on Aldose Reductase: Nitro-substituted Inhibitors with Strong Enthalpic Binding Contribution

Journal of Molecular Biology

Volumn 368, Issue 3, 2007, Pages 618-638

  Steuber, Holger ^a   Heine, Andreas ^a   Klebe, Gerhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

aldose reductase; binding mode; protein ligand interaction; structure based drug design; thermodynamic driving forces

Indexed keywords

ALDEHYDE REDUCTASE; ALDOSE REDUCTASE INHIBITOR; BTB 02809; JFD 00882; UNCLASSIFIED DRUG;

ARTICLE; CALORIMETRY; CHEMICAL STRUCTURE; ENTHALPY; GEOMETRY; HYDROGEN BOND; LIGAND BINDING; PRIORITY JOURNAL; SUBSTITUTION REACTION; THERMODYNAMICS; TITRIMETRY; X RAY CRYSTALLOGRAPHY;

EID: 34047134951     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.12.004     Document Type: Article

References (72)

1. Miyamoto S. Recent advances in aldose reductase inhibitors: potential agents for the treatment of diabetic complications. Expert. Opin. Ther. Patents 12 (2002) 621-631
2. Wild S., Roglic G., Green A., Sicree R., and King H. Global prevalence of diabetes. Diabetes Care 27 (2004) 1047-1053
3. Skyler J.S. Diabetes mellitus: pathogenesis and treatment strategies. J. Med. Chem. 47 (2004) 4113-4117
4. Stumvoll M., Goldstein B.J., and van Haeften T.W. Type 2 diabetes: principles of pathogenesis and therapy. Lancet 365 (2005) 1333-1346
5. Ross S.A., Gulve E.A., and Wang M. Chemistry and biochemistry of type 2 diabetes. Chem. Rev. 104 (2004) 1255-1282
6. Pfeifer M.A., and Schumer M.P. Clinical trials of diabetic neuropathy: past, present and future. Diabetes 44 (1995) 1355-1361
7. Suzen S., and Buyukbingol E. Recent studies of aldose reductase enzyme inhibition for diabetic complications. Curr. Med. Chem. 10 (2003) 1329-1352
8. Yabe-Nishimura C. Aldose reductase in glucose toxicity: a potential target for the prevention of diabetic complications. Pharmacol. Rev. 50 (1998) 21-33
9. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414 (2001) 813-820
10. Evans J.L., Goldfine I.D., Maddux B.A., and Grodsky G.M. Oxidative stress and stress-activated signalling pathways: a unifying hypothesis of type 2 diabetes. Endocrine Rev. 23 (2002) 599-622
11. Price S.A., Agthong S., Middlemas A.B., and Tomlinson D.R. Mitogen-activated protein kinase p38 mediates reduced nerve conduction velocity in experimental diabetic neuropathy. Interactions with aldose reductase. Diabetes 53 (2004) 1851-1856
12. Suzuki L.A., Poot M., Gerrity R.G., and Bornfeldt K.E. Diabetes accelerates smoth muscle accumulation in lesions of atherosclerosis. Lack of direct growth-promoting effects of high glucose levels. Diabetes 50 (2001) 851-860
13. Nakamura J., Kasuya Y., Hamada Y., Nakashima E., Naruse K., Yasuda Y., et al. Glucose-induced hyperproliferation of cultured rat aortic smooth muscle cells through polyol pathway hyperactivity. Diabetologica 44 (2001) 480-487
14. Oyama T., Miyasita Y., Watanabe H., and Shirai K. The role of polyol pathway in high glucose-induced endothelial cell damages. Diabetes Res. Clin. Pract. 73 (2006) 227-234
15. Dan Q., Wong R.L.C., Yin S., Chung S.K., Chung S.S.M., and Lam K.S.L. Interaction between the polyol pathway and non-enzymatic glycation on mesangial cell gene expression. Nephron Exp. Nephrol. 98 (2004) e89-e99
16. Jerums G., Panagiotopoulos S., Forbes J., Osicka T., and Cooper M. Evolving concepts in advanced glycation, diabetic nephropathy, and diabetic vascular disease. Arch. Biochem. Biophys. 419 (2003) 55-62
17. Greene D.A., Arezzo J.C., and Brown M.B. Effect of aldose reductase inhibition on nerve conduction and morphometry in diabetic neuropathy. Zenarestat Study Group. Neurology 53 (1999) 580-591
18. Constantino L., Rastelli G., Vianello P., Cignarella G., and Barlocco D. Diabetes complications and their potential prevention: aldose reductase inhibition and other approaches. Med. Res. Rev. 19 (1999) 3-23
19. Yagihashi S., Yamagishi S.I., Wada Ri R., Baba M., Hohman T.C., Yabe-Nishimura C., and Kokai Y. Neuropathy in diabetic mice overexpressing human aldose reductase and effects of aldose reductase inhibitor. Brain 124 (2001) 2448-2458
20. Mylari B.L., Armento S.J., Beebe D.A., Conn E.L., Coutcher J.B., Dina M.S., et al. A highly selective, non-hydantoin, non-carboxylic acid inhibitor of aldose reductase with potent oral activity in diabetic rat models: 6-(5-chloro-3-methylbenzofuran- 2-sulfonyl)-2-H-pyridazin-3-one. J. Med. Chem. 46 (2003) 2283-2286
21. Baba M., Kimura K., Suda T., and Yagihashi S. Three-year inhibition of aldose reductase on development of symptomatic neuropathy in diabetic patients. J. Peripher. Nerv. Syst. 11 (2006) 176-178
22. Constantino L., Rastelli G., Vianello P., Cignarella G., and Barlocco D. Diabetes complications and their potential prevention: aldose reductase inhibition and other approaches. Med. Res. Rev. 19 (1999) 3-23
23. El-Kabbani O., Darmanin C., Schneider T.R., Hazemann I., Ruiz F., Oka M., et al. 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: Struct. Funct. Genet. 55 (2004) 805-813
24. Van Zandt M.C., Jones M.L., Gunn D.E., Geraci L.S., Jones J.H., Sawicki D.R., et al. Discovery of 3- [(4,5,7-trifluorobenzothiazol-2-yl)methyl]indole-N-acetic acid (Lidorestat) and congeners as highly potent and selective inhibitors of aldose reductase for treatment of chronic diabetic complications. J. Med. Chem. 48 (2005) 3141-3152
25. Howard E.I., Sanishvili R., Cachau R.E., Mitschler A., Chevrier B., Barth P., et al. Ultrahigh resolution drug design I: details of interactions in human aldose reductase-inhibitor complex at 0.66 Å. Proteins: Struct. Funct. Genet. 55 (2004) 792-804
26. El-Kabbani O., Wilson D.K., Petrash J.M., and Quiocho F.A. Structural features of the aldose reductase and aldehyde reductase inhibitor binding sites. Mol. Vis. 4 (1998) 19-25
27. Sato S., and Kador P.F. Inhibition of aldehyde reductase by aldose reductase inhibitors. Biochem. Pharmacol. 40 (1990) 1033-1042
28. Van Zandt M.C., Sibley E.O., McCann E.E., Combs K.J., Flam B., Sawicki D.R., et al. Design and synthesis of highly potent and selective (2-arylcarbamoyl-phenoxy)-acetic acid inhibitors of aldose reductase for treatment of chronic diabetic complications. Bioorg. Med. Chem. 12 (2004) 5661-5675
29. Davydov V.V., Dobaeva N.M., and Bozhkov A.I. Possible role of alteration of aldehyde's scavenger enzymes during aging. Exp. Gerontol. 39 (2004) 11-16
30. Oka M., Matsumoto Y., Sugiyama S., Tsuruta N., and Matsushima M. A potent aldose reductase inhibitor, (2S,4S)-6-fluoro-2′, 5′-dioxospiro [chroman-4,4(-imidazolidine]-2-carboxamide (Fidarestat): its absolute configuration and interactions with the aldose reductase by X-ray crystallography. J. Med. Chem. 43 (2000) 2479-2483
31. Steuber H., Zentgraf M., Podjarny A.D., Heine A., and Klebe G. High resolution crystal structure of aldose reductase complexed with the novel sulfonyl-pyridazinone inhibitor exhibiting an alternative active site anchoring group. J. Mol. Biol. 356 (2006) 45-56
32. Varnai P., Richards W., and Lyne P.D. Modelling the catalytic reaction in human aldose reductase. Proteins: Struct. Funct. Genet. 37 (1999) 218-227
33. Cachau R., Howard E., Barth P., Mitschler A., Chevrier B., Lamour V., et al. Model of the catalytic mechanism of human aldose reductase based on quantum chemical calculations. J. Phys. IV France 10 (2000) 3-13
34. Iwata Y., Arisawa M., Hamada R., Kita Y., Mizutani M.Y., Tomioka N., et al. Discovery of novel aldose reductase inhibitors using a protein-structure-based approach: 3D-database search followed by design and synthesis. J. Med. Chem. 44 (2001) 1718-1728
35. Rastelli G., Ferrari A.M., Costantino L., and Gamberoni M.C. Discovery of new inhibitors of aldose reductase from molecular docking and database screening. Bioorg. Med. Chem. 10 (2002) 1437-1450
36. Ferrari A.M., Wei B.Q., Costantino L., and Shoichet B.W. Soft docking and multiple receptor conformations in virtual screening. J. Med. Chem. 47 (2004) 5076-5084
37. Krämer O., Hazemann I., Podjarny A.D., and Klebe G. Virtual screening for inhibitors of human aldose reductase. Proteins: Struct. Funct. Genet. 55 (2004) 814-823
38. Schiffmann R., Heine A., Klebe G., and Klein C.D. Metal ions as cofactors for the binding of inhibitors to methionine aminopeptidase: a critical view of the relevance of in vitro metalloenzyme assays. Angew. Chem. Int. Ed. Engl. 44 (2005) 3620-3623
39. Specker E., Bottcher J., Lilie H., Heine A., Schoop A., Muller G., et al. An old target revisited: two new privileged skeletons and an unexpected binding mode for HIV-protease inhibitors. Angew. Chem. Int. Ed. Engl. 44 (2005) 3140-3144
40. Shoichet B.K. Virtual screening of chemical libraries. Nature 432 (2004) 862-865
41. Lundqvist T. The devil is still in the details-driving early drug discovery forward with biophysical experimental methods. Curr. Opin. Drug Discov. Devel. 8 (2005) 513-519
42. Ruiz F., Hazemann I., Mitschler A., Joachimiak A., Schneider T., Karplus M., and Podjarny A. The crystallographic structure of the aldose reductase-IDD 552 complex shows direct proton donation from tyrosine 48. Acta Crystallog. sect. D 60 (2004) 1347-1354
43. Calderone V., Chevrier B., Van Zandt M., Lamour V., Howard E., Poterszman A., et al. The structure of human aldose reductase bound to the inhibitor IDD 384. Acta Crystallog. sect. D 56 (2000) 536-540
44. Goodford P.J. A computational procedure for determining energetically favourable binding sites on biologically important macromolecules. J. Med. Chem. 28 (1985) 849-857
45. Muzet N., Guillot B., Jelsch C., Howard E., and Lecomte C. Electrostatic complementarity in an aldose reductase complex from ultra-high-resolution crystallography and first-principles calculations. Proc. Natl Acad. Sci. USA 100 (2003) 8742-8747
46. Lecomte C., Guillot B., Muzet N., Pichon-Pesme V., and Jelsch C. Ultra-high-resolution X-ray structure of proteins. Cell. Mol. Life Sci. 61 (2004) 774-782
47. Auffinger P., Hays F.A., Westhof E., and Ho P.S. Halogen bonds in biological molecules. Proc. Natl Acad. Sci.USA 101 (2004) 16789-16794
48. Baker B.M., and Murphy K.P. Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys. J. 71 (1996) 2049-2055
49. D'Aquino J.A., Freire E., and Amzel L.M. Binding of small organic molecules to macromolecular targets: evaluation of conformational entropy changes. Proteins: Struct. Funct. Genet. (suppl.) 4 (2000) 93-107
50. Dunitz J.D. The entropic cost of bound water in crystals and biomolecules. Science 264 (1994) 670
51. Yin F., Cao R., Goddard A., Zhang Y., and Oldfield E. Enthalpy versus entropy-driven binding of bisphosphonates to farnesyl diphosphate synthase. J. Am. Chem. Soc. 128 (2006) 3524-3525
52. Teague S.J. Implications of protein flexibility for drug discovery. Nature Rev. Drug Discov. 2 (2003) 527-540
53. Homans S.W. Probing the binding entropy of ligand-protein interactions by NMR. ChemBioChem. 6 (2005) 1585-1591
54. Ford D.M. Enthalpy-entropy compensation is not a general feature of weak association. J. Am. Chem. Soc. 127 (2005) 16167-16170
55. Meyer E.A., Castellano R.K., and Diederich F. Interactions with aromatic rings in chemical and biological recognition. Angew. Chem. Int. Ed. 42 (2003) 1210-1250
56. Cabani S., Gianni P., Mollica V., and Lepori L. Group contributionsto the thermodynamic properties of non-ionic solutes in dilute aqueous solution. J. Sol. Chem. 10 (1981) 563-595
57. Barratt E., Bingham R.J., Warner D.J., Laughton C.A., Phillips S.E.V., and Homans S.W. Van der Waals interactions dominate ligand-protein association in a protein binding site occluded from solvent water. J. Am. Chem. Soc. 127 (2005) 11827-11834
58. Chandler D. Interfaces and the driving force of hydrophobic assembly. Nature 437 (2005) 640-647
59. Hendlich M., Bergner A., Gunther J., and Klebe G. Relibase: design and development of a database for comprehensive analysis of protein-ligand interactions. J. Mol. Biol. 326 (2003) 99-110
60. Thomas K.A., Smith G.M., Thomas T.B., and Feldmann R.J. Electronic distribution within protein phenylalanine aromatic rings are reflected by the three-dimensional oxygen atom environments. Proc. Natl Acad. Sci. USA 79 (1982) 4843-4847
61. α-H··· O hydrogen bonds and van der Waals interactions. J. Mol. Biol. 323 (2002) 69-76
62. Sarkhel S., and Desiraju G.R. N-H...O, O-H...O, and C-H...O hydrogen bonds in protein-ligand complexes: strong and weak interactions in molecular recognition. Proteins: Struct. Funct. Genet. 54 (2004) 247-259
63. Williams M.A., and Ladbury J.E. Hydrogen bonds in Protein-ligand complexes. In: Boehm H.-J., and Schneider G. (Eds). Protein-Ligand interactions: From Molecular Recognition to Drug Design (2003), Wiley-VCH, Weinheim 137-161
64. Llorens O., and Perez J.J. Toward the design of chemical libraries for mass screening biased against mutagenic compounds. J. Med. Chem. 44 (2001) 2793-2804
65. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
66. Brunger A.T., Adams P.D., Clore G.M., De Lano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
67. Sheldrick G.M., and Schneider T. SHELXL: high-resolution refinement. Methods Enzymol. 277 (1997) 319-343
68. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A 47 (1991) 110-119
69. Laskowski R., MacArthur M., Moss D., and Thornton J. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291
70. Fraczkiewicz R., and Braun W. Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comp. Chem. 19 (1998) 319-333
71. Shrake A., and Rupley J.A. Environment and exposure to solvent of protein atoms. Lysozyme and insulin. J. Mol. Biol. 79 (1973) 351-371
72. Holdgate G.A., and Ward W.H.J. Measurements of binding thermodynamics in drug discovery. Drug Discov. Today 10 (2005) 1543-1550