Identification of a novel polyfluorinated compound as a lead to inhibit the human enzymes aldose reductase and AKR1B10: Structure determination of both ternary complexes and implications for drug design

Acta Crystallographica Section D: Biological Crystallography

Volumn 70, Issue 3, 2014, Pages 889-903

  Cousido Siah, Alexandra ^a   Ruiz, Francesc X ^a,b   Mitschler, André ^a   Porté, Sergio ^b   De Lera, Ángel R ^c   Martín, María J ^d   Manzanaro, Sonia ^d   De La Fuente, Jesús A ^d   Terwesten, Felix ^e   Betz, Michael ^e   Klebe, Gerhard ^e   Farrés, Jaume ^b   Parés, Xavier ^b   Podjarny, Alberto ^a  

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

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c UNIVERSITY OF VIGO   (Spain)

^d Instituto Biomar SA   (Spain)

^e PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

AKR1B10; Aldo keto reductases; Aldose reductase; Inhibitors

Indexed keywords

AKR1B10 PROTEIN, HUMAN; ALDEHYDE REDUCTASE; CARBOXYLIC ACID; HALOGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RECOMBINANT PROTEIN;

AKR1B10; ALDO-KETO REDUCTASES; ARTICLE; CHEMISTRY; DRUG ANTAGONISM; DRUG DESIGN; DRUG EFFECT; ENZYME STABILITY; HUMAN; INHIBITORS; MOLECULAR DYNAMICS; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

AKR1B10; ALDO-KETO REDUCTASES; ALDOSE REDUCTASE; INHIBITORS;

ALDEHYDE REDUCTASE; CARBOXYLIC ACIDS; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; ENZYME STABILITY; HALOGENS; HUMANS; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; NADP; RECOMBINANT PROTEINS;

EID: 84896783721     PISSN: 09074449     EISSN: 13990047     Source Type: Journal    
DOI: 10.1107/S1399004713033452     Document Type: Article

References (95)

1. Adams, P. D. et al. (2010). Acta Cryst. D66, 213-221.
2. Ballatore, C., Huryn, D. M.& Smith,A. B. III (2013). ChemMedChem, 8, 385-395.
3. Barski, O. A., Gabbay, K. H., Grimshaw, C. E. & Bohren, K. M. (1995). Biochemistry, 34, 11264-11275.
4. Barski, O. A., Tipparaju, S. M. & Bhatnagar, A. (2008). Drug Metab. Rev. 40, 553-624.
5. Biadene, M., Hazemann, I., Cousido, A., Ginell, S., Joachimiak, A., Sheldrick, G. M., Podjarny, A. & Schneider, T. R. (2007). Acta Cryst. D63, 665-672.
6. Bohren, K. M. & Grimshaw, C. E. (2000). Biochemistry, 39, 9967-9974.
7. Calderone, V., Chevrier, B., Van Zandt, M., Lamour, V., Howard, E., Poterszman, A., Barth, P., Mitschler, A., Lu, J., Dvornik, D. M., Klebe, G., Kraemer, O., Moorman, A. R., Moras, D. & Podjarny, A. (2000). Acta Cryst. D56, 536-540.
8. Cao, D., Fan, S. T. & Chung, S. S. M. (1998). J. Biol. Chem. 273, 11429-11435.
9. Case, D. A. et al. (2012). Amber12. University of California, San Francisco, USA. http://ambermd.org.
10. Changjin, Z. (2013). Diabetes Mellitus - Insights and Perspectives, edited by O. O. Oguntibeju, pp. 17-46. Rijeka: InTech.
11. Chung, Y. T., Matkowskyj, K. A., Li, H., Bai, H., Zhang, W., Tsao, M.-S., Liao, J. & Yang, G.-Y. (2012). Mod. Pathol. 25, 758-766.
12. Costantino, L., Rastelli, G., Gamberini, M. C., Vinson, J. A., Bose, P., Iannone, A., Staffieri, M., Antolini, L., Del Corso, A., Mura, U. & Albasini, A. (1999). J. Med. Chem. 42, 1881-1893.
13. Darden, T., York, D. & Pedersen, L. (1993). J. Chem. Phys. 98, 10089.
14. Díez-Dacal, B., Gayarre, J., Gharbi, S., Timms, J. F., Coderch, C., Gago, F. & Pé rez-Sala, D. (2011). Cancer Res. 71, 4161-4171.
15. Dunitz, J. D. (2004). Chembiochem, 5, 614-621.
16. 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. (2004). Proteins, 55, 805-813.
17. El-Kabbani, O. & Podjarny, A. (2007). Cell. Mol. Life Sci. 64, 1970-1978.
18. El-Kabbani, O., Ruiz, F., Darmanin, C. & Chung, R. P.-T. (2004). Cell. Mol. Life Sci. 61, 750-762.
19. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. (2010). Acta Cryst. D66, 486-501.
20. Endo, S., Matsunaga, T., Kuwata, K., Zhao, H.-T., El-Kabbani, O., Kitade, Y. & Hara, A. (2010). Bioorg. Med. Chem. 18, 2485-2490.
21. Endo, S., Matsunaga, T., Mamiya, H., Ohta, C., Soda, M., Kitade, Y., Tajima, K., Zhao, H.-T., El-Kabbani, O. & Hara, A. (2009). Arch. Biochem. Biophys. 487, 1-9.
22. Endo, S., Matsunaga, T., Soda, M., Tajima, K., Zhao, H.-T., El- Kabbani, O. & Hara, A. (2010). Biol. Pharm. Bull. 33, 886-890.
23. Fenical,W., Jensen, P. R., Palladino, M. A., Lam, K. S., Lloyd, G. K. & Potts, B. C. (2009). Bioorg. Med. Chem. 17, 2175-2180.
24. Fuente, J. A. de la & Manzanaro, S. (2003). Nat. Prod. Rep. 20, 243-251.
25. Fuente, J. A. de la, Manzanaro, S., Martín, M. J., de Quesada, T. G., Reymundo, I., Luengo, S. M. & Gago, F. (2003). J. Med. Chem. 46, 5208-5221.
26. Fuhrmann, C. N., Daugherty, M. D. & Agard, D. A. (2006). J. Am. Chem. Soc. 128, 9086-9102.
27. Fukumoto, S. et al. (2005). Clin. Cancer Res. 11, 1776-1785.
28. Gallego, O., Belyaeva, O. V., Porté, S., Ruiz, F. X., Stetsenko, A. V., Shabrova, E. V., Kostereva, N. V., Farré s, J., Paré s, X. & Kedishvili, N. Y. (2006). Biochem. J. 399, 101-109.
29. Gallego, O., Ruiz, F. X., Ardè vol, A., Domínguez, M., Alvarez, R., de Lera, A. R., Rovira, C., Farré s, J., Fita, I. & Paré s, X. (2007). Proc. Natl Acad. Sci. USA, 104, 20764-20769.
30. Götz, A. W., Williamson, M. J., Xu, D., Poole, D., Le Grand, S. & Walker, R. C. (2012). J. Chem. Theory Comput. 8, 1542-1555.
31. Gregson, R. M., Glidewell, C., Ferguson, G. & Lough, A. J. (2000). Acta Cryst. B56, 39-57.
32. Harrison, D. H., Bohren, K. M., Ringe, D., Petsko, G. A. & Gabbay, K. H. (1994). Biochemistry, 33, 2011-2020.
33. Hernandes, M. Z., Cavalcanti, S. M. T., Moreira, D. R. M., de Azevedo, W. F. Jr & Leite, A. C. L. (2010). Curr. Drug Targets, 11, 303-314.
34. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A. & Simmerling, C. (2006). Proteins, 65, 712-725.
35. Howard, E. I., Sanishvili, R., Cachau, R. E., Mitschler, A., Chevrier, B., Barth, P., Lamour, V., Van Zandt, M., Sibley, E., Bon, C., Moras, D., Schneider, T. R., Joachimiak, A. & Podjarny, A. (2004). Proteins, 55, 792-804.
36. Huggins, D. J., Sherman, W. & Tidor, B. (2012). J. Med. Chem. 55, 1424-1444.
37. Humphrey, W., Dalke, A. & Schulten, K. (1996). J. Mol. Graph. 14, 33-38.
38. Jakalian, A., Bush, B. L., Jack, D. B. & Bayly, C. I. (2000). J. Comput. Chem. 21, 132-146.
39. Jakalian, A., Jack, D. B. & Bayly, C. I. (2002). J. Comput. Chem. 23, 1623-1641.
40. Jarman, M., Barrie, S. E., Deadman, J. J., Houghton, J., McCague, R. & Rowlands, M. G. (1990). J. Med. Chem. 33, 2452-2455.
41. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. (1983). J. Chem. Phys. 79, 926.
42. Kim, Y. et al. (2008). Nature Methods, 5, 853-854.
43. Kipper, K., Herodes, K. & Leito, I. (2011). J. Chromatogr. A, 1218, 8175-8180.
44. Lamour, V., Barth, P., Rogniaux, H., Poterszman, A., Howard, E., Mitschler, A., Van Dorsselaer, A., Podjarny, A. & Moras, D. (1999). Acta Cryst. D55, 721-723.
45. Lecomte, C., Jelsch, C., Guillot, B., Fournier, B. & Lagoutte, A. (2008). J. Synchrotron Rad. 15, 202-203.
46. Le Grand, S., Götz, A. W. & Walker, R. C. (2013). Comput. Phys. Commun. 184, 374-380.
47. Liu, Z., Zhong, L., Krishack, P. A., Robbins, S., Cao, J. X., Zhao, Y., Chung, S. & Cao, D. (2009). Gene, 437, 39-44.
48. Loncharich, R. J., Brooks, B. R. & Pastor, R. W. (1992). Biopolymers, 32, 523-535.
49. Lovering, A. L., Ride, J. P., Bunce, C. M., Desmond, J. C., Cummings, S. M. & White, S. A. (2004). Cancer Res. 64, 1802-1810.
50. Ma, J., Yan, R., Zu, X., Cheng, J.-M., Rao, K., Liao, D.-F. & Cao, D. (2008). J. Biol. Chem. 283, 3418-3423.
51. Manzanaro, S., Salva, J. & de la Fuente, J. A. (2006). J. Nat. Prod. 69, 1485-1487.
52. Martin, R. (2000). Handbook of Hydroxybenzophenones, p. 423. Dordrecht: Kluwer Academic Publishers.
53. Matsunaga, T., Endo, S., Soda, M., Zhao, H.-T., El-Kabbani, O., Tajima, K. & Hara, A. (2009). Biochem. Biophys. Res. Commun. 389, 128-132.
54. Murshudov, G. N., Skubá k, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F. & Vagin, A. A. (2011). Acta Cryst. D67, 355-367.
55. Navaza, J. (2001). Acta Cryst. D57, 1367-1372.
56. Oates, P. J. (2008). Curr. Drug Targets, 9, 14-36.
57. O'Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T. & Hutchison, G. R. (2011). J. Cheminform. 3, 33.
58. Otwinowski, Z. & Minor,W. (1997). Methods Enzymol. 276, 307-326.
59. Parisini, E., Metrangolo, P., Pilati, T., Resnati, G. & Terraneo, G. (2011). Chem. Soc. Rev. 40, 2267-2278.
60. Penning, T. M. (2005). Clin. Cancer Res. 11, 1687-1690.
61. Podjarny, A., Cachau, R. E., Schneider, T., Van Zandt, M. & Joachimiak, A. (2004). Cell. Mol. Life Sci. 61, 763-773.
62. Prince, E., Finger, L. W. & Konnert, J. H. (2006). International Tables for Crystallography, Vol. C, edited by E. Prince, pp. 694-701. Dordrecht: Kluwer Academic Publishers.
63. Quinn, A. M., Harvey, R. G. & Penning, T. M. (2008). Chem. Res. Toxicol. 21, 2207-2215.
64. Ramana, K. V. & Srivastava, S. K. (2010). Int. J. Biochem. Cell Biol. 42, 17-20.
65. Ramunno, A., Cosconati, S., Sartini, S., Maglio, V., Angiuoli, S., La Pietra, V., Di Maro, S., Giustiniano, M., La Motta, C., Da Settimo, F., Marinelli, L. & Novellino, E. (2012). Eur. J. Med. Chem. 51, 216-226.
66. Rastelli, G., Antolini, L., Benvenuti, S. & Costantino, L. (2000). Bioorg. Med. Chem. 8, 1151-1158.
67. Rastelli, G., Costantino, L., Gamberini, M. C., Del Corso, A., Mura, U., Petrash, J. M., Ferrari, A. M. & Pacchioni, S. (2002). Bioorg. Med. Chem. 10, 1427-1436.
68. Rayment, I. (1997). Methods Enzymol. 276, 171-179.
69. Rayment, I., Rypniewski, W. R., Schmidt-Bäse, K., Smith, R., Tomchick, D. R., Benning, M. M., Winkelmann, D. A., Wesenberg, G. & Holden, H. M. (1993). Science, 261, 50-58.
70. Roe, D. R. & Cheatham, T. E. (2013). J. Chem. Theory Comput. 9, 3084-3095.
71. Ruiz, F. X., Cousido-Siah, A., Mitschler, A., Farré s, J., Paré s, X. & Podjarny, A. (2013). Chem. Biol. Interact. 202, 178-185.
72. Ruiz, F. X., Gallego, O., Ardè vol, A., Moro, A., Domínguez, M., Alvarez, S., Alvarez, R., de Lera, A. R., Rovira, C., Fita, I., Paré s, X. & Farré s, J. (2009). Chem. Biol. Interact. 178, 171-177.
73. Ruiz, F. X., Porté, S., Paré s, X. & Farré s, J. (2012). Front. Pharmacol. 3, 58.
74. Ryckaert, J.-P., Ciccotti, G. & Berendsen, H. J. C. (1977). J. Comput. Phys. 23, 327-341.
75. Salomon-Ferrer, R., Götz, A. W., Poole, D., Le Grand, S. & Walker, R. C. (2013). J. Chem. Theory Comput. 9, 3878-3888.
76. Sheldrick, G. M. (2008). Acta Cryst. A64, 112-122.
77. Shinde, P. B., Lee, Y.M., Dang, H. T., Hong, J., Lee, C.-O. & Jung, J. H. (2008). Bioorg. Med. Chem. Lett. 18, 6414-6418.
78. Sledz, P., Zheng, H., Murzyn, K., Chruszcz, M., Zimmerman, M. D., Chordia, M. D., Joachimiak, A. & Minor,W. (2010). Protein Sci. 19, 1395-1404.
79. Soda, M., Endo, S., Matsunaga, T., Zhao, H.-T., El-Kabbani, O., Iinuma, M., Yamamura, K. & Hara, A. (2012). Biol. Pharm. Bull. 35, 2075-2080.
80. Soda, M., Hu, D., Endo, S., Takemura, M., Li, J., Wada, R., Ifuku, S., Zhao, H.-T., El-Kabbani, O., Ohta, S., Yamamura, K., Toyooka, N., Hara, A. & Matsunaga, T. (2012). Eur. J. Med. Chem. 48, 321-329.
81. Steuber, H., Heine, A., Podjarny, A. & Klebe, G. (2008). J. Mol. Biol. 379, 991-1016.
82. Takemura, M., Endo, S., Matsunaga, T., Soda, M., Zhao, H.-T., El- Kabbani, O., Tajima, K., Iinuma, M. & Hara, A. (2011). J. Nat. Prod. 74, 1201-1206.
83. Tammali, R., Reddy, A. B., Saxena, A., Rychahou, P. G., Evers, B. M., Qiu, S., Awasthi, S., Ramana, K. V. & Srivastava, S. K. (2011). Carcinogenesis, 32, 1259-1267.
84. Tang, W. H., Martin, K. A. & Hwa, J. (2012). Front. Pharmacol. 3, 87.
85. Urzhumtsev, A., Tête-Favier, F., Mitschler, A., Barbanton, J., Barth, P., Urzhumtseva, L., Biellmann, J. F., Podjarny, A. & Moras, D. (1997). Structure, 5, 601-612.
86. Vallejos, M. J., Auffinger, P. & Ho, P. S. (2012). International Tables for Crystallography, Vol. F, edited by E. Arnold, D. M. Himmel & M. G. Rossmann, pp. 821-826. Chichester: John Wiley & Sons.
87. Verma, M., Martin, H. J., Haq, W., O'Connor, T. R., Maser, E. & Balendiran, G. K. (2008). Eur. J. Pharmacol. 584, 213-221.
88. Walter, T. S., Meier, C., Assenberg, R., Au, K. F., Ren, J., Verma, A., Nettleship, J. E., Owens, R. J., Stuart, D. I. & Grimes, J. M. (2006). Structure, 14, 1617-1622.
89. Wang, C., Yan, R., Luo, D., Watabe, K., Liao, D.-F. & Cao, D. (2009). J. Biol. Chem. 284, 26742-26748.
90. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A. & Case, D. A. (2004). J. Comput. Chem. 25, 1157-1174.
91. Wang, R.,Wang, G., Ricard, M. J., Ferris, B., Strulovici-Barel, Y., Salit, J., Hackett, N. R., Gudas, L. J. & Crystal, R. G. (2010). Chest, 138, 1402-1410.
92. Yadav, U. C., Mishra, R., Aguilera-Aguirre, L., Sur, S., Bolodgh, I., Ramana, K. V. & Srivatsava, S. K. (2013). Inflamm. Allergy Drug Targets, 12, 178-186.
93. Zeindl-Eberhart, E., Haraida, S., Liebmann, S., Jungblut, P. R., Lamer, S., Mayer, D., Jäger, G., Chung, S. & Rabes, H. M. (2004). Hepatology, 39, 540-549.
94. Zhang, L., Zhang, H., Zhao, Y., Li, Z., Chen, S., Zhai, J., Chen, Y., Xie, W., Wang, Z., Li, Q., Zheng, X. & Hu, X. (2013). FEBS Lett. 587, 3681-3686
95. Zhao, H.-T., Soda, M., Endo, S., Hara, A. & El-Kabbani, O. (2010). Eur. J. Med. Chem. 45, 4354-4357.