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Active site modulation in the N-acetylneuraminate lyase sub-family as revealed by the structure of the inhibitor-complexed Haemophilus influenzae enzyme.

Barbosa JA, Smith BJ, DeGori R, Ooi HC, Marcuccio SM, Campi EM, Jackson WR, Brossmer R, Sommer M, Lawrence MC
J Mol Biol 303 405-21 (2000)
Related entries: 1f6k, 1f6p, 1f73, 1f74, 1f7b

Cited: 41 times
EuropePMC logo PMID: 11031117

Abstract

The N-acetylneuraminate lyase (NAL) sub-family of (beta/alpha)(8) enzymes share a common catalytic step but catalyse reactions in different biological pathways. Known examples include NAL, dihydrodipicolinate synthetase (DHDPS), d-5-keto-4-deoxyglucarate dehydratase, 2-keto-3-deoxygluconate aldolase, trans-o-hydroxybenzylidenepyruvate hydrolase-aldolase and trans-2'-carboxybenzalpyruvate hydratase-aldolase. Little is known about the way in which the three-dimensional structure of the respective active sites are modulated across the sub-family to achieve cognate substrate recognition. We present here the structure of Haemophilus influenzae NAL determined by X-ray crystallography to a maximum resolution of 1.60 A, in native form and in complex with three substrate analogues (sialic acid alditol, 4-deoxy-sialic acid and 4-oxo-sialic acid). These structures reveal for the first time the mode of binding of the complete substrate in the NAL active site. On the basis of the above structures, that of substrate-complexed DHDPS and sequence comparison across the sub-family we are able to propose a unified model for active site modulation. The model is one of economy, allowing wherever appropriate the retention or relocation of residues associated with binding common substrate substituent groups. Our structures also suggest a role for the strictly conserved tyrosine residue found in all active sites of the sub-family, namely that it mediates proton abstraction by the alpha-keto acid carboxylate in a substrate-assisted catalytic reaction pathway.

Articles - 1f5z mentioned but not cited (9)

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Reviews citing this publication (4)

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Articles citing this publication (28)

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  2. Elucidation of a sialic acid metabolism pathway in mucus-foraging Ruminococcus gnavus unravels mechanisms of bacterial adaptation to the gut. Bell A, Brunt J, Crost E, Vaux L, Nepravishta R, Owen CD, Latousakis D, Xiao A, Li W, Chen X, Walsh MA, Claesen J, Angulo J, Thomas GH, Juge N. Nat Microbiol 4 2393-2404 (2019)
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  6. Reaction mechanism of N-acetylneuraminic acid lyase revealed by a combination of crystallography, QM/MM simulation, and mutagenesis. Daniels AD, Campeotto I, van der Kamp MW, Bolt AH, Trinh CH, Phillips SE, Pearson AR, Nelson A, Mulholland AJ, Berry A. ACS Chem Biol 9 1025-1032 (2014)
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  12. Creation of a tailored aldolase for the parallel synthesis of sialic acid mimetics. Woodhall T, Williams G, Berry A, Nelson A. Angew Chem Int Ed Engl 44 2109-2112 (2005)
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  14. Disaccharides as sialic acid aldolase substrates: synthesis of disaccharides containing a sialic acid at the reducing end. Huang S, Yu H, Chen X. Angew Chem Int Ed Engl 46 2249-2253 (2007)
  15. L-Hydroxyproline and d-Proline Catabolism in Sinorhizobium meliloti. Chen S, White CE, diCenzo GC, Zhang Y, Stogios PJ, Savchenko A, Finan TM. J Bacteriol 198 1171-1181 (2016)
  16. Identification of the bona fide DHDPS from a common plant pathogen. Atkinson SC, Hor L, Dogovski C, Dobson RC, Perugini MA. Proteins 82 1869-1883 (2014)
  17. Identification of biochemical and putative biological role of a xenolog from Escherichia coli using structural analysis. Bhaskar V, Kumar M, Manicka S, Tripathi S, Venkatraman A, Krishnaswamy S. Proteins 79 1132-1142 (2011)
  18. Modulation of substrate specificities of D-sialic acid aldolase through single mutations of Val-251. Chou CY, Ko TP, Wu KJ, Huang KF, Lin CH, Wong CH, Wang AH. J Biol Chem 286 14057-14064 (2011)
  19. Molecular Characterization of a Novel N-Acetylneuraminate Lyase from a Deep-Sea Symbiotic Mycoplasma. Wang SL, Li YL, Han Z, Chen X, Chen QJ, Wang Y, He LS. Mar Drugs 16 E80 (2018)
  20. MosA, a protein implicated in rhizopine biosynthesis in Sinorhizobium meliloti L5-30, is a dihydrodipicolinate synthase. Tam PH, Phenix CP, Palmer DR. J Mol Biol 335 393-397 (2004)
  21. Crystal structure of YagE, a putative DHDPS-like protein from Escherichia coli K12. Manicka S, Peleg Y, Unger T, Albeck S, Dym O, Greenblatt HM, Bourenkov G, Lamzin V, Krishnaswamy S, Sussman JL. Proteins 71 2102-2108 (2008)
  22. Structural Characterization of the Hydratase-Aldolases, NahE and PhdJ: Implications for the Specificity, Catalysis, and N-Acetylneuraminate Lyase Subgroup of the Aldolase Superfamily. LeVieux JA, Medellin B, Johnson WH, Erwin K, Li W, Johnson IA, Zhang YJ, Whitman CP. Biochemistry 57 3524-3536 (2018)
  23. The metalloprotein YhcH is an anomerase providing N-acetylneuraminate aldolase with the open form of its substrate. Kentache T, Thabault L, Deumer G, Haufroid V, Frédérick R, Linster CL, Peracchi A, Veiga-da-Cunha M, Bommer GT, Van Schaftingen E. J Biol Chem 296 100699 (2021)
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  25. A mutagenic analysis of NahE, a hydratase-aldolase in the naphthalene degradative pathway. Lancaster EB, Johnson WH, LeVieux JA, Hardtke HA, Zhang YJ, Whitman CP. Arch Biochem Biophys 733 109471 (2023)
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  27. Identification of aldolase and ferredoxin reductase within the dbt operon of Burkholderia fungorum DBT1. Piccoli S, Andreolli M, Giorgetti A, Zordan F, Lampis S, Vallini G. J Basic Microbiol 54 464-469 (2014)
  28. Preliminary crystallographic analysis of L-2-keto-3-deoxyarabonate dehydratase, an enzyme involved in an alternative bacterial pathway of L-arabinose metabolism. Shimada N, Mikami B, Watanabe S, Makino K. Acta Crystallogr Sect F Struct Biol Cryst Commun 63 393-395 (2007)


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