High-resolution crystal structure of AKR11C1 from Bacillus halodurans: An NADPH-dependent 4-hydroxy-2,3-trans-nonenal reductase

Journal of Molecular Biology

Volumn 354, Issue 2, 2005, Pages 304-316

  Marquardt, Tobias ^a   Kostrewa, Dirk ^a   Balakrishnan, Rajkumar ^b   Gasperina, Antonietta ^a   Kambach, Christian ^a   Podjarny, Alberto ^c   Winkler, Fritz K ^a   Balendiran, Ganesaratnam K ^b   Li, Xiao Dan ^a  

^a PAUL SCHERRER INSTITUTE   (Switzerland)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

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

Author keywords

AKR11C1; Aldo keto reductase; Bacillus halodurans; HNE; Lipid peroxidation detoxification

Indexed keywords

4 HYDROXYNONENAL REDUCTASE; ALDOKETOREDUCTASE 11C1; ARGININE; BENZALDEHYDE; GLYCERALDEHYDE; IOLS PROTEIN; OXIDOREDUCTASE; PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; YQKP PROTEIN;

ARTICLE; BACILLUS; BACILLUS HALODURANS; BACTERIAL SURVIVAL; BINDING SITE; BIOCHEMISTRY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOTOXICITY; DETOXIFICATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HYDROPHOBICITY; LIPID PEROXIDATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PRIORITY JOURNAL; PROTEIN INTERACTION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

BACILLUS (BACTERIUM); BACILLUS HALODURANS; BACTERIA (MICROORGANISMS);

EID: 27644494168     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.09.067     Document Type: Article

References (60)

1. D. Hyndman, D.R. Bauman, V.V. Heredia, and T.M. Penning The aldo-keto reductase superfamily homepage Chem. Biol. Interact. 143-144 2003 621 631
2. V. Nahoum, A. Gangloff, P. Legrand, D.W. Zhu, L. Cantin, and B.S. Zhorov Structure of the human 3alpha-hydroxysteroid dehydrogenase type 3 in complex with testosterone and NADP at 1.25-Å resolution J. Biol. Chem. 276 2001 42091 42098
3. K.L. Kavanagh, M. Klimacek, B. Nidetzky, and D.K. Wilson The structure of apo and holo forms of xylose reductase, a dimeric aldo-keto reductase from Candida tenuis Biochemistry 41 2002 8785 8795
4. G. Sanli, and M. Blaber Structural assembly of the active site in an aldo-keto reductase by NADPH cofactor J. Mol. Biol. 309 2001 1209 1218
5. I. Tarle, D.W. Borhani, D.K. Wilson, F.A. Quiocho, and J.M. Petrash Probing the active site of human aldose reductase. Site-directed mutagenesis of Asp-43, Tyr-48, Lys-77, and His-110 J. Biol. Chem. 268 1993 25687 25693
6. R. Cachau, E. Howard, P. Barth, A. Mitschler, B. Chevrier, and V. Lamour Model of the catalytic mechanism of human aldose reductase based on quantum chemical calculations J. Phys. IV France 10 2000 3 13
7. K.M. Bohren, C.E. Grimshaw, and K.H. Gabbay Catalytic effectiveness of human aldose reductase. Critical role of C-terminal domain J. Biol. Chem. 267 1992 20965 20970
8. A. Urzhumtsev, F. Tete-Favier, A. Mitschler, J. Barbanton, P. Barth, and L. Urzhumtseva A 'specificity' pocket inferred from the crystal structures of the complexes of aldose reductase with the pharmaceutically important inhibitors tolrestat and sorbinil Structure 5 1997 601 612
9. S. Khurana, D.B. Powers, S. Anderson, and M. Blaber Crystal structure of 2,5-diketo-D-gluconic acid reductase A complexed with NADPH at 2.1-Å resolution Proc. Natl Acad. Sci. USA 95 1998 6768 6773
10. A.H. Ehrensberger, and D.K. Wilson Structural and catalytic diversity in the two family 11 aldo-keto reductases J. Mol. Biol. 337 2004 661 673
11. G. Obmolova, A. Teplyakov, P.P. Khil, A.J. Howard, R.D. Camerini-Otero, and G.L. Gilliland Crystal structure of the Escherichia coli Tas protein, an NADP(H)-dependent aldo-keto reductase Proteins: Struct. Funct. Genet. 53 2003 323 325
12. K.I. Yoshida, D. Aoyama, I. Ishio, T. Shibayama, and Y. Fujita Organization and transcription of the myo-inositol operon, iol, of Bacillus subtilis J. Bacteriol. 179 1997 4591 4598
13. A. Petersohn, M. Brigulla, S. Haas, J.D. Hoheisel, U. Volker, and M. Hecker Global analysis of the general stress response of Bacillus subtilis J. Bacteriol. 183 2001 5617 5631
14. H. Takami, K. Nakasone, Y. Takaki, G. Maeno, R. Sasaki, and N. Masui Complete genome sequence of the alkaliphilic bacterium Bacillus halodurans and genomic sequence comparison with Bacillus subtilis Nucl. Acids Res. 28 2000 4317 4331
15. T. Kobayashi, Y. Hakamada, S. Adachi, J. Hitomi, T. Yoshimatsu, and K. Koike Purification and properties of an alkaline protease from alkalophilic Bacillus sp. KSM-K16 Appl. Microbiol. Biotechnol. 43 1995 473 481
16. F. Kunst, N. Ogasawara, I. Moszer, A.M. Albertini, G. Alloni, and V. Azevedo The complete genome sequence of the Gram-positive bacterium Bacillus subtilis Nature 390 1997 249 256
17. M.W. Rey, P. Ramaiya, B.A. Nelson, S.D. Brody-Karpin, E.J. Zaretsky, and M. Tang Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species Genome Biol. 5 2004 R77
18. T.D. Read, S.N. Peterson, N. Tourasse, L.W. Baillie, I.T. Paulsen, and K.E. Nelson The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria Nature 423 2003 81 86
19. N. Ivanova, A. Sorokin, I. Anderson, N. Galleron, B. Candelon, and V. Kapatral Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis Nature 423 2003 87 91
20. U. Gerth, E. Kruger, I. Derre, T. Msadek, and M. Hecker Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance Mol. Microbiol. 28 1998 787 802
21. + channels Science 289 2000 123 127
22. J.M. Gulbis, S. Mann, and R. MacKinnon Structure of a voltage-dependent K+ channel beta subunit Cell 97 1999 943 952
23. E. Kozma, E. Brown, E.M. Ellis, and A.J. Lapthorn The high resolution crystal structure of rat liver AKR7A1: understanding the substrate specificites of the AKR7 family Chem. Biol. Interact. 143-144 2003 289 297
24. S.F. Altschul, T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucl. Acids Res. 25 1997 3389 3402
25. F. Corpet Multiple sequence alignment with hierarchical clustering Nucl. Acids Res. 16 1988 10881 10890
26. P. Gouet, E. Courcelle, D.I. Stuart, and F. Metoz ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 15 1999 305 308
27. P. Gouet, X. Robert, and E. Courcelle ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins Nucl. Acids Res. 31 2003 3320 3323
28. E.I. Howard, R. Sanishvili, R.E. Cachau, A. Mitschler, B. Chevrier, and P. Barth 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
29. C.E. Grimshaw, K.M. Bohren, C.J. Lai, and K.H. Gabbay Human aldose reductase: rate constants for a mechanism including interconversion of ternary complexes by recombinant wild-type enzyme Biochemistry 34 1995 14356 14365
30. A.W. Grant, G. Steel, H. Waugh, and E.M. Ellis A novel aldo-keto reductase from Escherichia coli can increase resistance to methylglyoxal toxicity FEMS Microbiol. Letters 218 2003 93 99
31. Y. Trongpanich, K. Abe, Y. Kaneda, T. Morita, and T. Yagi Purification and characterization of pyridoxal 4-dehydrogenase from Aureobacterium luteolum Biosci. Biotechnol. Biochem. 66 2002 54354 54358
32. N. Yokochi, Y. Yoshikane, Y. Trongpanich, K. Ohnishi, and T. Yagi Molecular cloning, expression, and properties of an unusual aldo-keto reductase family enzyme, pyridoxal 4-dehydrogenase, that catalyzes irreversible oxidation of pyridoxal J. Biol. Chem. 279 2004 37377 37384
33. P.R. Gerber, and K. Muller MAB, a generally applicable molecular force field for structure modelling in medicinal chemistry J. Comput. Aided Mol. Des. 9 1995 251 268
34. D.K. Wilson, K.M. Bohren, K.H. Gabbay, and F.A. Quiocho An unlikely sugar substrate site in the 1.65 Å structure of the human aldose reductase holoenzyme implicated in diabetic complications Science 257 1992 81 84
35. K.M. Bohren, J.M. Brownlee, A.C. Milne, K.H. Gabbay, and D.H. Harrison The structure of Apo R268A human aldose reductase: hinges and latches that control the kinetic mechanism Biochim. Biophys. Acta 1748 2005 201 212
36. S.S. Singhal, P. Zimniak, R. Sharma, S.K. Srivastava, S. Awasthi, and Y.C. Awasthi A novel glutathione S-transferase isozyme similar to GST 8-8 of rat and mGSTA4-4 (GST 5.7) of mouse is selectively expressed in human tissues Biochim. Biophys. Acta 1204 1994 279 286
37. N.L. Parinandi, E.W. Thompson, and H.H. Schmid Diabetic heart and kidney exhibit increased resistance to lipid peroxidation Biochim. Biophys. Acta 1047 1990 63 69
38. G. Stenberg, M. Ridderstrom, A. Engstrom, S.E. Pemble, and B. Mannervik Cloning and heterologous expression of cDNA encoding class alpha rat glutathione transferase 8-8, an enzyme with high catalytic activity towards genotoxic alpha,beta-unsaturated carbonyl compounds Biochem. J. 284 1992 313 319
39. K.V. Ramana, B.L. Dixit, S. Srivastava, G.K. Balendiran, S.K. Srivastava, and A. Bhatnagar Selective recognition of glutathiolated aldehydes by aldose reductase Biochemistry 39 2000 12172 12180
40. M.E. Burczynski, G.R. Sridhar, N.T. Palackal, and T.M. Penning The reactive oxygen species-and Michael acceptor-inducible human aldo-keto reductase AKR1C1 reduces the alpha,beta-unsaturated aldehyde 4-hydroxy-2-nonenal to 1,4-dihydroxy-2-nonene J. Biol. Chem. 276 2001 2890 2897
41. S. Srivastava, A. Chandra, N.H. Ansari, S.K. Srivastava, and A. Bhatnagar Identification of cardiac oxidoreductase(s) involved in the metabolism of the lipid peroxidation-derived aldehyde-4-hydroxynonenal Biochem. J. 329 1998 469 475
42. H. Esterbauer, R.J. Schaur, and H. Zollner Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes Free Radic. Biol. Med. 11 1991 81 128
43. A. Bhatnagar, and S.K. Srivastava Aldose reductase: congenial and injurious profiles of an enigmatic enzyme Biochem. Med. Metab. Biol. 48 1992 91 121
44. J.M. Petrash, T.M. Harter, C.S. Devine, P.O. Olins, A. Bhatnagar, S. Liu, and S.K. Srivastava Involvement of cysteine residues in catalysis and inhibition of human aldose reductase. Site-directed mutagenesis of Cys-80, -298, and -303 J. Biol. Chem. 267 1992 24833 24840
45. M.J. Bennett, R.H. Albert, J.M. Jez, H. Ma, T.M. Penning, and M. Lewis Steroid recognition and regulation of hormone action: crystal structure of testosterone and NADP+ bound to 3 alpha-hydroxysteroid/dihydrodiol dehydrogenase Structure 5 1997 799 812
46. D.H. Harrison, K.M. Bohren, D. Ringe, G.A. Petsko, and K.H. Gabbay An anion binding site in human aldose reductase: mechanistic implications for the binding of citrate, cacodylate, and glucose 6-phosphate Biochemistry 33 1994 2011 2020
47. K. Horikoshi Alkaliphiles: some applications of their products for biotechnology Microbiol. Mol. Biol. Rev. 63 1999 735 750
48. M.S. Muntyan, I.V. Popova, D.A. Bloch, E.V. Skripnikova, and V.S. Ustiyan Energetics of alkalophilic representatives of the genus bacillus Biochemistry (Mosc) 70 2005 137 142
49. T.A. Krulwich, M. Ito, and A.A. Guffanti The Na(+)-dependence of alkaliphily in Bacillus Biochim. Biophys. Acta 1505 2001 158 168
50. W. Kabsch Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Crystallog. 26 1993 795 800
51. T.R. Schneider, and G.M. Sheldrick Substructure solution with SHELXD Acta Crystallog. sect. D 58 2002 1772 1779
52. de La Fortelle, E. & Bricogne, G. (1997). Methods maximum-liklihood heavy-atom parameter refinement for the multiple isomorphous replacement and multiwavelength anomalous diffraction methods. In Methods in Enzymology volume 276, pp. 472-494, Academic Press, New York.
53. J.P. Abrahams, S.K. Buchanan, M.J. Van Raaij, I.M. Fearnley, A.G. Leslie, and J.E. Walker The structure of bovine F1-ATPase complexed with the peptide antibiotic efrapeptin Proc. Natl Acad. Sci. USA 93 1996 9420 9424
54. R.J. Morris, A. Perrakis, and V.S. Lamzin ARP/wARP's model-building algorithms. I. The main chain Acta Crystallog. sect. D 58 2002 968 975
55. A. Perrakis, R. Morris, and V.S. Lamzin Automated protein model building combined with iterative structure refinement Nature Struct. Biol. 6 1999 458 463
56. R.A. Laskowski, D.S. Moss, and J.M. Thornton Main-chain bond lengths and bond angles in protein structures J. Mol. Biol. 231 1993 1049 1067
57. R.W. Hooft, G. Vriend, C. Sander, and E.E. Abola Errors in protein structures Nature 381 1996 272
58. S.C. Lovell, J.M. Word, J.S. Richardson, and D.C. Richardson The penultimate rotamer library Proteins: Struct. Funct. Genet. 40 2000 389 408
59. D.W. Marquardt An algorithm for least-squares estimation of nonlinear parameters J. Soc. Ind. Appl. Math. 11 1963 431 441
60. R.A. Engh, and R. Hubert Accurate bond and angle parameters for X-ray protein structure refinement Acta Crystallog. sect. A 47 1991 392 400