Catalytic mechanism of perosamine N-acetyltransferase revealed by high-resolution X-ray crystallographic studies and kinetic analyses

Biochemistry

Volumn 51, Issue 16, 2012, Pages 3433-3444

  Thoden, James B ^a   Reinhardt, Laurie A ^a   Cook, Paul D ^b   Menden, Patrick ^c   Cleland, W W ^a   Holden, Hazel M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF MOUNT UNION   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ALTERNATIVE SUBSTRATES; AMIDE GROUPS; C-TERMINAL DOMAINS; CATALYTIC MECHANISMS; CRYSTALLOGRAPHIC STUDIES; GENERAL BASE; GRAM-NEGATIVE BACTERIA; HIGH RESOLUTION; HIGH-RESOLUTION STRUCTURES; KINETIC ANALYSIS; KINETIC DATA; MUTANT PROTEINS; N-ACETYLTRANSFERASES; N-TERMINAL DOMAINS; OXYANION HOLE; PATHOGENIC ESCHERICHIA COLI; TRANSITION STATE; TRIMERIC ENZYMES;

AMIDES; BIOCHEMISTRY; ENZYMES; ESCHERICHIA COLI; X RAY CRYSTALLOGRAPHY;

PROTEINS;

BACTERIAL PROTEIN; COENZYME A; DEOXYSUGAR; GUANOSINE DIPHOSPHATE; PERB PROTEIN; PEROSAMINE N ACETYLTRANSFERASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CAULOBACTER CRESCENTUS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

ACETYLTRANSFERASES; BACTERIAL PROTEINS; BINDING SITES; CATALYSIS; CATALYTIC DOMAIN; CAULOBACTER CRESCENTUS; CRYSTALLOGRAPHY, X-RAY; HYDROGEN-ION CONCENTRATION; KINETICS; MANNOSE; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

EID: 84860151942     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300197h     Document Type: Article

References (38)

1. Wells, J. G., Davis, B. R., Wachsmuth, I. K., Riley, L. W., Remis, R. S., Sokolow, R., and Morris, G. K. (1983) Laboratory investigation of hemorrhagic colitis outbreaks associated with a rare Escherichia coli serotype J. Clin. Microbiol. 18, 512-520
2. Mead, P. S. and Griffin, P. M. (1998) Escherichia coli O157:H7 Lancet 352, 1207-1212
3. Perry, M. B., MacLean, L., and Griffith, D. W. (1986) Structure of the O-chain polysaccharide of the phenol-phase soluble lipopolysaccharide of Escherichia coli 0:157:H7 Biochem. Cell Biol. 64, 21-28
4. Haishima, Y., Kondo, S., and Hisatsune, K. (1990) The occurrence of α(1 - - 2) linked N -acetylperosamine-homopolymer in lipopolysaccharides of non-O1 Vibrio cholerae possessing an antigenic factor in common with O1 V. cholerae Microbiol. Immunol. 34, 1049-1054
5. Ovchinnikova, O. G., Kocharova, N. A., Katzenellenbogen, E., Zatonsky, G. V., Shashkov, A. S., Knirel, Y. A., Lipinski, T., and Gamian, A. (2004) Structures of two O -polysaccharides of the lipopolysaccharide of Citrobacter youngae PCM 1538 (serogroup O9) Carbohydr. Res. 339, 881-884
6. Awram, P. and Smit, J. (2001) Identification of lipopolysaccharide O antigen synthesis genes required for attachment of the S -layer of Caulobacter crescentus Microbiology 147, 1451-1460
7. Albermann, C. and Beuttler, H. (2008) Identification of the GDP- N -acetyl- d -perosamine producing enzymes from Escherichia coli O157:H7 FEBS Lett. 582, 479-484
8. Somoza, J. R., Menon, S., Schmidt, H., Joseph-McCarthy, D., Dessen, A., Stahl, M. L., Somers, W. S., and Sullivan, F. X. (2000) Structural and kinetic analysis of Escherichia coli GDP-mannose 4,6 dehydratase provides insights into the enzyme's catalytic mechanism and regulation by GDP-fucose Struct. Folding Des. 8, 123-135
9. Mulichak, A. M., Bonin, C. P., Reiter, W. D., and Garavito, R. M. (2002) Structure of the MUR1 GDP-mannose 4,6-dehydratase from Arabidopsis thaliana: Implications for ligand binding and specificity Biochemistry 41, 15578-15589
10. Webb, N. A., Mulichak, A. M., Lam, J. S., Rocchetta, H. L., and Garavito, R. M. (2004) Crystal structure of a tetrameric GDP- d -mannose 4,6-dehydratase from a bacterial GDP- d -rhamnose biosynthetic pathway Protein Sci. 13, 529-539
11. Albermann, C. and Piepersberg, W. (2001) Expression and identification of the RfbE protein from Vibrio cholerae O1 and its use for the enzymatic synthesis of GDP-D-perosamine Glycobiology 11, 655-661
12. Zhao, G., Liu, J., Liu, X., Chen, M., Zhang, H., and Wang, P. G. (2007) Cloning and characterization of GDP-perosamine synthetase (Per) from Escherichia coli O157:H7 and synthesis of GDP-perosamine in vitro Biochem. Biophys. Res. Commun. 363, 525-530
13. Cook, P. D. and Holden, H. M. (2008) GDP-perosamine synthase: Structural analysis and production of a novel trideoxysugar Biochemistry 47, 2833-2840
14. Raetz, C. R. and Roderick, S. L. (1995) A left-handed parallel β helix in the structure of UDP- N -acetylglucosamine acyltransferase Science 270, 997-1000
15. Brown, K., Pompeo, F., Dixon, S., Mengin-Lecreulx, D., Cambillau, C., and Bourne, Y. (1999) Crystal structure of the bifunctional N -acetylglucosamine 1-phosphate uridyltransferase from Escherichia coli: A paradigm for the related pyrophosphorylase superfamily EMBO J. 18, 4096-4107
16. Olsen, L. R. and Roderick, S. L. (2001) Structure of the Escherichia coli GlmU pyrophosphorylase and acetyltransferase active sites Biochemistry 40, 1913-1921
17. 2+ at 1.96 Å resolution J. Mol. Biol. 305, 279-289
18. Sulzenbacher, G., Gal, L., Peneff, C., Fassy, F., and Bourne, Y. (2001) Crystal structure of Streptococcus pneumoniae N -acetylglucosamine-1-phosphate uridyltransferase bound to acetyl-coenzyme A reveals a novel active site architecture J. Biol. Chem. 276, 11844-11851
19. Rangarajan, E. S., Ruane, K. M., Sulea, T., Watson, D. C., Proteau, A., Leclerc, S., Cygler, M., Matte, A., and Young, N. M. (2008) Structure and active site residues of PglD, an N -acetyltransferase from the bacillosamine synthetic pathway required for N -glycan synthesis in Campylobacter jejuni Biochemistry 47, 1827-1836
20. Olivier, N. B. and Imperiali, B. (2008) Crystal structure and catalytic mechanism of PglD from Campylobacter jejuni J. Biol. Chem. 283, 27937-27946
21. Thoden, J. B., Cook, P. D., Schaffer, C., Messner, P., and Holden, H. M. (2009) Structural and functional studies of QdtC: An N -acetyltransferase required for the biosynthesis of dTDP-3-acetamido-3,6-dideoxy-α- d -glucose Biochemistry 48, 2699-2709
22. Thoden, J. B. and Holden, H. M. (2010) Molecular structure of WlbB, a bacterial N -acetyltransferase involved in the biosynthesis of 2,3-diacetamido-2,3-dideoxy- d -mannuronic acid Biochemistry 49, 4644-4653
23. Kubiak, R. L. and Holden, H. M. (2012) Structural Studies on AntD: An N -Acyltransferase Involved in the Biosynthesis of d -Anthrose Biochemistry 51, 867-878
24. Holden, H. M., Cook, P. D., and Thoden, J. B. (2010) Biosynthetic enzymes of unusual microbial sugars Curr. Opin. Struct. Biol. 20, 543-550
25. Terwilliger, T. C. and Berendzen, J. (1999) Automated MAD and MIR structure solution Acta Crystallogr. D55 (Part 4) 849-861
26. Terwilliger, T. C. (2000) Maximum-likelihood density modification Acta Crystallogr. D56 (Part 8) 965-972
27. Terwilliger, T. C. (2003) Automated main-chain model building by template matching and iterative fragment extension Acta Crystallogr. D59, 38-44
28. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
29. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255
30. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
31. Minor, W., Cymborowski, M., Otwinowski, Z., and Chruszcz, M. (2006) HKL-3000: The integration of data reduction and structure solution-from diffraction images to an initial model in minutes Acta Crystallogr. D62, 859-866
32. Sheldrick, G. M. and Schneider, T. R. (1997) SHELXL: High-resolution refinement Methods Enzymol. 277, 319-343
33. Cleland, W. W. (1979) Statistical analysis of enzyme kinetic data Methods Enzymol. 63, 103-138
34. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
35. Vuorio, R., Harkonen, T., Tolvanen, M., and Vaara, M. (1994) The novel hexapeptide motif found in the acyltransferases LpxA and LpxD of lipid A biosynthesis is conserved in various bacteria FEBS Lett. 337, 289-292
36. Ray, W. J., Jr. and Puvathingal, J. M. (1985) A simple procedure for removing contaminating aldehydes and peroxides from aqueous solutions of polyethylene glycols and of nonionic detergents that are based on the polyoxyethylene linkage Anal. Biochem. 146, 307-312
37. McCarthy, T. J., Plog, M. A., Floy, S. A., Jansen, J. A., Soukup, J. K., and Soukup, G. A. (2005) Ligand requirements for glmS ribozyme self-cleavage Chem. Biol. 12, 1221-1226
38. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.