Insights into subtle conformational differences in the substrate-binding loop of fungal 17β-hydroxysteroid dehydrogenase: A combined structural and kinetic approach

Biochemical Journal

Volumn 441, Issue 1, 2012, Pages 151-160

  Cassetta, Alberto ^a   Krastanova, Ivet ^b   Kristan, Katja ^c   Švegelj, Mojca Brunskole ^c   Lamba, Doriano ^a   Lanišnik Rižner, Tea ^c   Stojan, Jure ^c  

^a CNR   (Italy)

^b SINCROTRONE TRIESTE   (Italy)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

17 hydroxysteroid dehydrogenase (17 HSD); Carbonyl reductase; Cochliobolus lunatus; Phyto oestrogen; Short chain dehydrogenase reductase (SDR)

Indexed keywords

COUMESTROL; ESTR 4 ENE 3,17 DIONE; TESTOSTERONE 17BETA DEHYDROGENASE; TESTOSTERONE 17BETA DEHYDROGENASE APO; TESTOSTERONE 17BETA DEHYDROGENASE COUMESTROL; TESTOSTERONE 17BETA DEHYDROGENASE HOLO; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CATALYSIS; COCHLIOBOLUS; COCHLIOBOLUS LUNATUS; COENZYME; CRYSTAL STRUCTURE; DISSOCIATION; ENZYME ACTIVITY; FLOW KINETICS; GENE MUTATION; IC 50; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SOLUBILITY;

ASCOMYCOTA; BINDING SITES; COUMESTROL; CRYSTALLIZATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; HYDROXYSTEROID DEHYDROGENASES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84055178177     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110567     Document Type: Article

References (47)

1. Penning, T. M. (1997) Molecular endocrinology of hydroxysteroid dehydrogenases. Endocr. Rev. 18, 281-305
2. Penning, T. M. (2003) Hydroxysteroid dehydrogenases and pre-receptor regulation of steroid hormone action. Hum. Reprod. Update 9, 193-205
3. Luu-The, V. and Labrie, F. (2010) The intracrine sex steroid biosynthesis pathways. Prog. Brain Res. 181, 177-192
4. Donova, M. V., Egorova, O. V. and Nikolayeva, V. M. (2005) Steroid 17β-reduction by microorganisms: a review. Process Biochem. 40, 2253-2262
5. Moeller, G. and Adamski, J. (2009) Integrated view on 17β-hydroxysteroid dehydrogenases. Mol. Cell. Endocrinol. 301, 7-19
6. Marchais-Oberwinkler, S., Henn, C., Moller, G., Klein, T., Negri, M., Oster, A., Spadaro, A., Werth, R., Wetzel, M., Xu, K. et al. (2011) 17β-Hydroxysteroid dehydrogenases (17β-HSDs) as therapeutic targets: protein structures, functions, and recent progress in inhibitor development. J. Steroid Biochem. Mol. Biol. 125, 66-82
7. Mindnich, R., Möller, G. and Adamski, J. (2004) The role of 17β-hydroxysteroid dehydrogenases. Mol. Cell. Endocrinol. 218, 7-20
8. Cresnar, B. and Zakelj-Mavric, M. (2009) Aspects of the steroid response in fungi. Chem. Biol. Interact. 178, 303-309
9. Kavanagh, K. L., Jornvall, H., Persson, B. and Oppermann, U. (2008) The SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell. Mol. Life Sci. 65, 3895-906
10. Jornvall, H., Persson, B., Krook, M., Atrian, S., Gonzalez-Duarte, R., Jeffery, J. and Ghosh, D. (1995) Short-chain dehydrogenases/ reductases (SDRs). Biochemistry 34, 6003-6013
11. Tanaka, N., Nonaka, T., Nakamura, K. T. and Hara, A. (2001) SDR: structure, mechanism of action, and substrate recognition. Curr. Org. Chem. 5, 89-111 (Pubitemid 32421676)
12. Sherbet, D. P., Papari-Zareei, M., Khan, N., Sharma, K. K., Brandmaier, A., Rambally, S., Chattopadhyay, A., Andersson, S., Agarwal, A. K. and Auchus, R. J. (2007) Coenzymes, redox state, and directional preferences of hydroxysteroid dehydrogenases. Mol. Cell. Endocrinol. 265-266, 83-88 (Pubitemid 46273967)
13. Lanišnik Rižner, T., Zakelj-Mavric, M., Plemenitas, A. and Zorko, M. (1996) Purification and characterization of 17β-hydroxysteroid dehydrogenase from the filamentous fungus Cochliobolus lunatus. J. Steroid Biochem. Mol. Biol. 59, 205-214 (Pubitemid 27036273)
14. Kristan, K., Brunskole, M., Stojan, J. and Lanisnik Rizner, T. (2009) Two homologous fungal carbonyl reductases with different substrate specificities. Chem. Biol. Interact. 178, 295-302
15. Lanisnik Rizner, T., Moeller, G., Thole, H. H., Zakelj-Mavric, M. and Adamski, J. (1999) A novel 17β-hydroxysteroid dehydrogenase in the fungus Cochliobolus lunatus: new insights into the evolution of steroid-hormone signalling. Biochem. J. 337, 425-431
16. Lanisnik Rizner, T. and Zakelj-Mavric, M. (2000) Characterization of fungal 17β-hydroxysteroid dehydrogenases. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 127, 53-63
17. Lanisnik Rizner, T., Adamski, J. and Stojan, J. (2000) 17β-hydroxysteroid dehydrogenase from Cochliobolus lunatus: model structure and substrate specificity. Arch. Biochem. Biophys. 384, 255-262 (Pubitemid 32012799)
18. Kristan, K., Lanisnik Rizner, T., Stojan, J., Gerber, J. K., Kremmer, E. and Adamski, J. (2003) Significance of individual amino-acid residues for coenzyme and substrate specificity of 17β-hydroxysteroid dehydrogenase from the fungus Cochliobolus lunatus. Chem. Biol. Interact. 143-144, 493-501 (Pubitemid 36253598)
19. Kristan, K., Stojan, J., Moller, G., Adamski, J. and Lanisnik Rizner, T. (2005) Coenzyme specificity in fungal 17β-hydroxysteroid dehydrogenase. Mol. Cell. Endocrinol. 241, 80-87 (Pubitemid 41263390)
20. Lanisnik Rizner, T., Stojan, J. and Adamski, J. (2001) 17β-Hydroxysteroid dehydrogenase from the fungus Cochliobolus lunatus: structural and functional aspects. Chem. Biol. Interact. 130-132, 793-803 (Pubitemid 32295864)
21. 227 in the substrate specificities of fungal 17β-hydroxysteroid dehydrogenase and trihydroxynaphthalene reductase: steroids versus smaller substrates. J. Steroid. Biochem. Mol. Biol., doi:10.1016/j.jsbmb.2011.03.019
22. Kallberg, Y., Oppermann, U., Jornvall, H. and Persson, B. (2002) Short-chain dehydrogenases/reductases (SDRs). Eur. J. Biochem. 269, 4409-4417
23. Persson, B., Kallberg, Y., Oppermann, U. and Jornvall, H. (2003) Coenzyme-based functional assignments of short-chain dehydrogenases/ reductases (SDRs). Chem. Biol. Interact. 143-144, 271-278 (Pubitemid 36253590)
24. Lanisnik Rizner, T. and Wheeler, M. H. (2003) Melanin biosynthesis in the fungus Curvularia lunata (teleomorph: Cochliobolus lunatus). Can. J. Microbiol. 49, 110-119 (Pubitemid 36628188)
25. Stojan, J., Brunskole, M. and Lanisnik Rizner, T. (2009) Simultaneous binding of coenzyme and two ligand molecules into the active site of fungal trihydroxynaphthalene reductase. Chem. Biol. Interact. 178, 268-273
26. Lanisnik Rizner, T., Stojan, J. and Adamski, J. (2001) Searching for the physiological function of 17β-hydroxysteroid dehydrogenase from the fungus Cochliobolus lunatus: studies of substrate specificity and expression analysis. Mol. Cell. Endocrinol. 171, 193-198 (Pubitemid 32098214)
27. Kristan, K., Krajnc, K., Konc, J., Gobec, S., Stojan, J. and Lanisnik Rizner, T. (2005) Phytoestrogens as inhibitors of fungal 17β-hydroxysteroid dehydrogenase. Steroids 70, 626-635 (Pubitemid 40916218)
28. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
29. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
30. Cassetta, A., Budefeld, T., Lanisnik Rizner, T., Kristan, K., Stojan, J. and Lamba, D. (2005) Crystallization, X-ray diffraction analysis and phasing of 17β-hydroxysteroid dehydrogenase from the fungus Cochliobolus lunatus. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 1032-1034 (Pubitemid 44210707)
31. Powell, H., Leslie, A. and Battye, G. (2007) Mosflm 7.0.1 and its new interface: iMosflm 0.5.3., CCP4 Newsletter on Protein Crystallography, No. 46, Daresbury Laboratory, Warrington
32. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760-763
33. Brunger, A. T. (2007) Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2, 2728-2733
34. Emsley, P., Lohkamp, B., Scott, W. G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 486-501
35. 164 regulates accessibility to the active site in fungal 17β-hydroxysteroid dehydrogenase. Biochimie 89, 63-71
36. Benach, J., Atrian, S., Gonzalez-Duarte, R. and Ladenstein, R. (1998) The refined crystal structure of Drosophila lebanonensis alcohol dehydrogenase at 1.9 Å resolution. J. Mol. Biol. 282, 383-399 (Pubitemid 28418791)
37. Stojan, J. (1997) Analysis of progress curves in an acetylcholinesterase reaction: a numerical integration treatment. J. Chem. Inform. Comp. Sci. 37, 1025-1027
38. Bevc, S., Konc, J., Stojan, J., Hodošček, M., Penca, M., Praprotnik, M. and Janežič, D. (2011) ENZO: a web tool for derivation and evaluation of kinetic models of enzyme catalyzed reactions. PLoS ONE 6, e22265
39. Kristan, K., Deluca, D., Adamski, J., Stojan, J. and Lanisnik Rizner, T. (2005) Dimerization and enzymatic activity of fungal 17β-hydroxysteroid dehydrogenase from the short-chain dehydrogenase/reductase superfamily. BMC Biochem. 6, 28
40. Brunskole, M., Kristan, K., Stojan, J. and Lanisnik Rizner, T. (2009) Mutations that affect coenzyme binding and dimer formation of fungal 17β-hydroxysteroid dehydrogenase. Mol. Cell. Endocrinol. 301, 47-50
41. Janin, J. and Chothia, C. (1990) The structure of protein-protein recognition sites. J. Biol. Chem. 265, 16027-16030
42. Andersson, A., Jordan, D., Schneider, G. and Lindqvist, Y. (1996) Crystal structure of the ternary complex of 1,3,8-trihydroxynaphthalene reductase from Magnaporthe grisea with NADPH and an active-site inhibitor. Structure 4, 1161-1170 (Pubitemid 27005384)
43. Benach, J., Atrian, S., Gonzalez-Duarte, R. and Ladenstein, R. (1999) The catalytic reaction and inhibition mechanism of Drosophila alcohol dehydrogenase: observation of an enzyme-bound NAD-ketone adduct at 1.4 Å resolution by X-ray crystallography. J. Mol. Biol. 289, 335-355 (Pubitemid 29278386)
44. Filling, C., Berndt, K. D., Benach, J., Knapp, S., Prozorovski, T., Nordling, E., Ladenstein, R., Jornvall, H. and Oppermann, U. (2002) Critical residues for structure and catalysis in short-chain dehydrogenases/reductases. J. Biol. Chem. 277, 25677-25684 (Pubitemid 34959957)
45. Liao, D., Basarab, G. S., Gatenby, A. A., Valent, B. and Jordan, D. B. (2001) Structures of trihydroxynaphthalene reductase-fungicide complexes: implications for structure-based design and catalysis. Structure 9, 19-27 (Pubitemid 32064346)
46. Poornam, G. P., Matsumoto, A., Ishida, H. and Hayward, S. (2009) A method for the analysis of domain movements in large biomolecular complexes. Proteins Struct. Funct. Bioinformat. 76, 201-212
47. Schneider, T. R. (2002) A genetic algorithm for the identification of conformationally invariant regions in protein molecules. Acta Crystallogr. Sect. D Biol. Crystallogr. 58, 195-208