Structural and functional features of dimeric dihydrodiol dehydrogenase

Cellular and Molecular Life Sciences

Volumn 65, Issue 10, 2008, Pages 1464-1474

  Carbone, V ^a   Hara, A ^b   El Kabbani, O ^a  

^a MONASH UNIVERSITY   (Australia)

^b GIFU PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Crystal structure; Dihydrodiol dehydrogenase; Molecular modeling; Oxido reductases; Site directed mutagenesis

Indexed keywords

DIHYDRODIOL DEHYDROGENASE; DINUCLEOTIDE; OLIGOMER;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ISOLATION; HUMAN; MONKEY; NONHUMAN; OXIDATION; REVIEW; SEQUENCE ANALYSIS; UBIQUITINATION; X RAY;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 44449160397     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-7508-5     Document Type: Review

References (70)

1. Ayengar, P. K., Hayaishi, O., Nakajima, M. and Tomida, I. (1959) Enzymic aromatization of 3,5-cyclohexadiene-1,2-diol. Biochim. Biophys. Acta 33, 111-119.
2. Glatt, H. R., Vorgel, K., Bentley, P. and Oesch, F. (1979) Reduction of benzo[a]pyrene mutagenicity by dihydrodiol dehydrogenase. Nature 277, 319-320.
3. Glatt, H. R., Cooper, C. S., Grover, P. L., Sims, P., Bentley, P., Merdes, M., Waechter F., Vogel K., Guenthner, T. M. and Oesch, F. (1982) Inactivation of a diol epoxide by dihydrodiol dehydrogenase but not by two epoxide hydrolases. Science 215, 1507-1509.
4. Smithgall, T. E., Harvey, R. G. and Penning, T. M. (1986) Regio- and stereospecificity of homogeneous 3α-hydroxysteroid/dihydrodiol dehydrogenase for trans-dihydrodiol metabolites of polycyclic aromatic hydrocarbons. J. Biol. Chem. 261, 6184-6191.
5. Klein, J., Post, K., Thomas, H., Worner, W., Setiabudi, F., Frank, H., Oesch F. and Platt, K. L. (1990) The oxidation of the highly tumorigenic benz[a]anthracene 3,4-dihydrodiol by rat liver dihydrodiol dehydrogenase. Chem. Biol. Interact. 76, 211-226.
6. Harvey, R. G. (1991) Polycyclic Aromatic Hydrocarbons: Chemicals and Carcinogenicity, Cambridge University Press, Cambridge.
7. Simada, T. (2006) Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab. Pharmacokinet. 21, 257-276.
8. Penning, T. M., Burczynski, M. E., Hung, C. F., McCoull, K. D., Palackal, N. T. and Tsuruda, L. S. (1999) Dihydrodiol dehydrogenases and polycyclic aromatic hydrocarbon activation: generation of reactive and redox active o-quinones. Chem. Res. Toxicol. 12, 1-18.
9. Penning, T. M. (2004) Aldo-keto reductases and formation of polycyclic aromatic hydrocarbon o-quinones. Methods Enzymol. 378, 31-67.
10. van Heyningen, R. (1979) Naphthalene cataract in rats and rabbits: a resume. Exp. Eye Res. 28, 435-439.
11. Hara, A., Harada, T., Nakagawa, M., Matsuura, K., Nakayama, T. and Sawada, H. (1989) Isolation from pig lens of two proteins with dihydrodiol dehydrogenase and aldehyde reductase activities. Biochem. J. 264, 403-407.
12. Kalf, G. F., Post, G. B. and Snyder, R. (1987) Solvent toxicology: recent advances in the toxicology of benzene, the glycol ethers, and carbon tetrachloride. Annu. Rev. Pharmacol. Toxicol. 27, 399-427.
13. Glatt, H., Padykula, R., Berchtold, G. A., Ludewig, G., Platt, K. L., Klein, J. and Oesch, F. (1989) Multiple activation pathways of benzene leading to products with varying genotoxic characteristics. Environ. Health. Perspect. 82, 81-89.
14. Vogel, K., Bentley, P., Platt, K. L. and Oesch, F. (1980) Rat liver cytoplasmic dihydrodiol dehydrogenase. Purification to apparent homogeneity and properties. J. Biol. Chem. 255, 9621-9625.
15. Bolcsak, L. E. and Nerland, D. E. (1983) Purification of mouse liver benzene dihydrodiol dehydrogenases. J. Biol. Chem. 258, 7252-7255.
16. Wörner, W. and Oesch, F. (1984) Identity of dihydrodiol dehydrogenase and 3α-hydroxysteroid dehydrogenase in rat but not in rabbit liver cytosol. FEBS Lett. 170, 263-267.
17. +) and aldehyde reductase exhibit benzene dihydrodiol dehydrogenase activity. Biochem. J. 225, 177-181.
18. Nakayama, T., Hara, A., Kariya, K., Hasebe, K., Inoue, Y., Matsuura, K. and Sawada, H. (1987) Hydroxysteroids are physiological substrates of dehydrogenases for alicyclic alcohols and benzene dihydrodiol in rodent and rabbit liver cytosol. Prog. Clin. Biol. Res. 232, 415-430.
19. Matsuura, K., Hara, A., Nakayama, T., Nakagawa, M. and Sawada, H. (1987) Purification and properties of two multiple forms of dihydrodiol dehydrogenase from guinea-pig testis. Biochim. Biophys. Acta 912, 270-277.
20. Sawada, H., Hara, A., Nakagawa, M., Tsukada, F., Ohmura, M. and Matsuura, K. (1989) Separation and properties of multiple forms of dihydrodiol dehydrogenase from hamster liver. Int. J. Biochem. 21, 367-375.
21. Nakagawa, M., Harada, T., Hara, A., Nakayama, T. and Sawada, H. (1989) Purification and properties of multiple forms of dihydrodiol dehydrogenase from monkey liver. Chem. Pharm. Bull. 37, 2852-2854.
22. Hara, A., Taniguchi, H., Nakayama, T. and Sawada, H. (1990) Purification and properties of multiple forms of dihydrodiol dehydrogenase from human liver. J. Biochem. (Tokyo) 108, 250-254.
23. Nakayama, T., Sawada, H., Deyashiki, Y., Kanazu, T., Hara, A., Shinoda M., Matsuura K., Bunai Y. and Ohya I. (1990). Distribution of dimeric dihydrodiol dehydrogenase in pig tissues and its role in carbonyl metabolism. Adv. Exp. Med. Biol. 284, 187-196.
24. Hara, A., Nakayama, T., Harada, T., Kanazu, T., Shinoda, M., Deyashiki, Y. and Sawada, H. (1991) Distribution and characterization of dihydrodiol dehydrogenases in mammalian ocular tissues. Biochem. J. 275, 113-119.
25. Klein, J., Thomas, H., Post, K., Worner, W. and Oesch, F. (1992) Dihydrodiol dehydrogenase activities of rabbit liver are associated with hydroxysteroid dehydrogenases and aldoketo reductases. Eur. J. Biochem. 205, 1155-1162.
26. Mizoguchi, T., Nanjo, H., Umemura, T., Nishinaka, T., Iwata, C., Imanishi, T., Tanaka, T., Terada, T. and Nishihara, T. (1992) A novel dihydrodiol dehydrogenase in bovine liver cytosol: purification and characterization of multiple forms of dihydrodiol dehydrogenase. J. Biochem. (Tokyo) 112, 523-529.
27. Kallberg, Y., Oppermann, U., Jörnvall, H. and Persson, B. (2002) Short-chain dehydrogenases/reductases (SDRs). Eur. J. Biochem. 269, 4409-4417.
28. Testa, B. (1995) In: The Metabolism of Drugs and Other Xenobiotics, pp. 41-69, Testa, B. and Caldwell, J. (eds.), Academic Press, London.
29. Petrash, J. M. (2004) All in the family: aldose reductase and closely related aldo-keto reductases. Cell. Mol. Life Sci. 61, 737-749.
30. Matsunaga, T., Shintani, S. and Hara, A. (2006) Multiplicity of mammalian reductases for xenobiotic carbonyl compounds. Drug Metab. Pharmacokinet. 21, 1-18.
31. El-Kabbani, O. and Podjarny, A. (2007) Selectivity determinants of the aldose and aldehyde reductase inhibitor-binding sites. Cell. Mol. Life Sci. 64, 1970-1978.
32. Jin, Y. and Penning, T. M. (2007) Aldo-keto reductases and bioactivation/detoxication. Annu. Rev. Pharmacol. Toxicol. 47, 263-292.
33. Arimitsu, E., Aoki, S., Ishikura, S., Nakanishi, K., Matsuura, K. and Hara, A. (1999) Cloning and sequencing of the cDNA species for mammalian dimeric dihydrodiol dehydrogenases. Biochem. J. 342, 721-728.
34. +-dependent D-xylose dehydrogenase in pig liver. Chem. Biol. Interact. 130-132, 775-784.
35. Carbone, V., Endo, S., Sumii, R., Chung, R., P.-T., Matsunaga, T., Hara, A. and El-Kabbani, O. (2008) Structures of dimeric dihydrodiol dehydrogenase apoenzyme and inhibitor complex: probing the subunit interface with site-directed mutagenesis. Proteins 70, 176-187.
36. Hara, A., Mouri, K. and Sawada, H. (1987) Purification and partial characterization of dimeric dihydrodiol dehydrogenase from monkey kidney. Biochem. Biophys. Res. Commun. 145, 1260-1266.
37. Sato, K., Nakanishi, M., Deyashiki, Y., Hara, A., Matsuura, K. and Ohya, I. (1994) Purification and characterization of dimeric dihydrodiol dehydrogenase from dog liver. J. Biochem. (Tokyo) 116, 711-717.
38. Nakagawa, M., Matsuura, K., Hara, A., Sawada, H., Bunai, Y. and Ohya, I. (1989) Dimeric dihydrodiol dehydrogenase in monkey kidney. Substrate specificity, stereospecificity of hydrogen transfer, and distribution. J. Biochem. (Tokyo) 106, 1104-1109.
39. Nakagawa, M., Tsukada, F., Nakayama, T., Matsuura, K., Hara, A. and Sawada, H. (1989) Identification of two dihydrodiol dehydrogenases associated with 3(17)α-hydroxysteroid dehydrogenase activity in mouse kidney. J. Biochem. (Tokyo) 106, 633-638.
40. Yamaguchi, S., Inazu, A., Deyashiki, Y., Nakayama, T., Sato, K., Miyabe, Y. and Hara, A. (1994) Stereospecificity of trans-dihydrodiol oxidation by dimeric and monomeric dihydrodiol dehydrogenases from mammalian tissues. J. Biochem. (Tokyo) 115, 493-496.
41. +- dependent D-xylose dehydrogenase from pig liver. Purification and properties. Biochem. J. 266, 637-644.
42. Sato, K., Inazu, A., Yamaguchi, S., Nakayama, T., Deyashiki, Y., Sawada, H. and Hara, A. (1993) Monkey 3-deoxyglucosone reductase: tissue distribution and purification of three multiple forms of the kidney enzyme that are identical with dihydrodiol dehydrogenase, aldehyde reductase, and aldose reductase. Arch. Biochem. Biophys. 307, 286-294.
43. Thornalley, P. J., Langborg, A. and Minhas, H. S. (1999) Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem. J. 344, 109-116.
44. Hara, A., Shinoda, M., Kanazu, T., Nakayama, T., Deyashiki, Y. and Sawada, H. (1991) Inhibition of dimeric dihydrodiol dehydrogenases of rabbit and pig lens by ascorbic acid. Biochem. J. 275, 121-126.
45. Shinoda, M., Hara, A., Nakayama, T., Deyashiki, Y. and Yamaguchi, S. (1992) Inhibition of dimeric dihydrodiol dehydrogenase by 4-hydroxyphenylketone derivatives: aspects of inhibitor structure and binding specificity. J. Biochem. (Tokyo) 112, 840-844.
46. Asada, Y., Aoki, S., Ishikura, S., Usami, N. and Hara, A. (2000). Roles of His-79 and Tyr-180 of D-xylose/dihydrodiol dehydrogenase in catalytic function. Biochem. Biophys. Res. Commun. 278, 333-337.
47. El-Kabbani, O., Chung, R. P., Ramsland, P. A., Asada, Y., Ishikura, S., Usami, N. and Hara, A. (2002) Crystallization and preliminary X-ray diffraction analysis of monkey dimeric dihydrodiol dehydrogenase. Acta Crystallogr. D Biol. Crystallogr. 58, 163-164.
48. Westover, J. B., Goodman, S. I. and Frerman, F. E. (2003) Pathogenic mutations in the carboxyl-terminal domain of glutaryl-CoA dehydrogenase: effects on catalytic activity and the stability of the tetramer. Mol. Genet. Metab. 79, 245-256.
49. Bjork, A., Mantzilas, D., Sirevag, R. and Eijsink, V. G. (2003) Electrostatic interactions across the dimer-dimer interface contribute to the pH-dependent stability of a tetrameric malate dehydrogenase. FEBS Lett. 553, 423-426.
50. Dambe, T. R., Kuhn, A. M., Brossette, T., Giffhorn, F. and Scheidig, A. J. (2006) Crystal structure of NADP(H)-dependent 1,5-anhydro-D-fructose reductase from Sinorhizobium morelense at 2.2 A resolution: construction of a NADH-accepting mutant and its application in rare sugar synthesis. Biochemistry 45, 10030-10042.
51. Whitby, F. G., Phillips, J. D., Hill, C. P., McCoubrey, W. and Maines, M. D. (2002) Crystal structure of a biliverdin IXα reductase enzyme-cofactor complex. J. Mol. Biol. 319, 1199-1210.
52. Franklin, E., Browne, S., Hayes, J., Boland, C., Dunne, A., Elliot, G. and Mantle, T. J. (2007) Activation of biliverdin-IXalpha reductase by inorganic phosphate and related anions. Biochem. J. 405, 61-67.
53. Rossmann, M. G., Moras, D. and Olsen, K. W. (1974) Chemical and biological evolution of a nucleotide-binding protein. Nature 250, 194-199.
54. Tanaka, N., Nonaka, T., Nakamura, T. K. and Hara, A. (2001) SDR: Structure, mechanism of action and substrate recognition. Curr. Org. Chem. 5, 89-111.
55. Oppermann, U., Filling, C., Hult, M., Shafqat, N., Wu, X., Lindh, M., Shafqat, J., Nordling, E., Kallberg, Y., Persson, B. and Jornvall, H. (2003) Short-chain dehydrogenases/reductases (SDR): the 2002 update. Chem. Biol. Interact. 143-144, 247-253.
56. Kingston, R. L., Scopes, R. K. and Baker, E. N. (1996) The structure of glucose-fructose oxido-reductase from Zymomonas mobilis: an osmoprotective periplasmic enzyme containing non-dissociable NADP. Structure 4, 1413-1428.
57. Nurizzo, D., Halbig, D., Sprenger, G. A. and Baker, E. N. (2001) Crystal structures of the precursor form of glucosefructose oxido-reductase from Zymomonas mobilis and its complexes with bound ligands. Biochemistry 40, 13857-13867.
58. Zachariou, M. and Scopes, R. K. (1986) Glucose-fructose oxido-reductase, a new enzyme isolated from Zymomonas mobilis that is responsible for sorbitol production. J. Bacteriol. 167, 863-869.
59. Loos, H., Kramer, R., Sahm, H. and Sprenger, G. A. (1994) Sorbitol promotes growth of Zymomonas mobilis in environments with high concentrations of sugar: evidence for a physiological function of glucose-fructose oxido-reductase in osmoprotection. J. Bacteriol. 176, 7688-7693.
60. Chhabra, S. R., Shockley, K. R., Conners, S. B., Scott, K. L., Wolfinger, R. D. and Kelly, R. M. (2003). Carbohydrate-induced differential gene expression patterns in the hyperthermophilic bacterium Thermotoga maritima. J. Biol. Chem. 278, 7540-7552.
61. Kuhn, A., Yu, S. and Giffhorn, F. (2006) Catabolism of 1,5-anhydro-D-fructose in Sinorhizobium morelense S-30.7.5, discovery, characterization, and overexpression of a new 1,5-anhydro-D-fructose reductase and its application in sugar analysis and rare sugar synthesis. Appl. Environ. Microbiol. 72, 1248-1257.
62. Hardman, M. J. and Scopes, R. K. (1988) The kinetics of glucose-fructose oxido-reductase from Zymomonas mobilis. Eur. J. Biochem. 173, 203-209.
63. Filling, C., Berndt, K. D., Benach, J., Knapp, S., Prozorovski, T., Nordling, E., Ladenstein R., Jörnvall, H. and Oppermann, U. (2002) Critical residues for structure and catalysis in short-chain dehydrogenases/reductases. J. Biol. Chem. 277, 25677-25684.
64. Barski, O. A., Gabbay, K. H. and Bohren, K. M. (1996) The C-terminal loop of aldehyde reductase determines the substrate and inhibitor specificity. Biochemistry 35, 14276-14280.
65. Hoog, S. S., Pawlowski, J. E., Alzari, P. M., Penning, T. M. and Lewis, M. (1994) Three-dimensional structure of rat liver 3 alpha-hydroxysteroid/ dihydrodiol dehydrogenase: a member of the aldo-keto reductase superfamily. Proc. Natl. Acad. Sci. USA 91, 2517-2521.
66. Hwang, C. C., Chang, Y. H., Hsu, C. N., Hsu, H. H., Li, C. W. and Pon, H. I. (2005) Mechanistic roles of Ser-114, Tyr-155, and Lys-159 in 3alpha-hydroxysteroid dehydrogenase/carbonyl reductase from Comamonas testosteroni. J. Biol. Chem. 280, 3522-3528.
67. El-Kabbani, O., Ishikura, S., Darmanin, C., Carbone, V., Chung, R. P., Usami, N. and Hara, A. (2004) Crystal structure of human L-xylulose reductase holoenzyme: probing the role of Asn107 with site-directed mutagenesis. Proteins 55, 724-732.
68. DeLano WL. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
69. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
70. Brodskii, L. I., Ivanov, V. V., Kalaidzidis, I. L., Leontovich, A. M., Nikolaev, V. K., Feranchuk, S. I. and Drachev, V. A. (1995) GeneBee-NET: an Internet based server for biopolymer structure analysis. Biokhimiia 60, 1221-1230.