2sim › Citations

The structures of Salmonella typhimurium LT2 neuraminidase and its complexes with three inhibitors at high resolution.

Crennell SJ, Garman EF, Philippon C, Vasella A, Laver WG, Vimr ER, Taylor GL
J Mol Biol 259 264-80 (1996)
Related entries: 1dil, 1dim, 2sil

Cited: 61 times
EuropePMC logo PMID: 8656428

Abstract

The structure of Salmonella typhimurium LT2 neuraminidase (STNA) is reported here to a resolution of 1.6 angstroms together with the structures of three complexes of STNA with different inhibitors. The first is 2-deoxy-2,3-dehydro-N-acetyl-neuraminic acid (Neu5Ac2en or DANA), the second and third are phosphonate derivatives of N-acetyl-neuraminic acid (NANA) which have phosphonate groups at the C2 position equatorial (ePANA) and axial (aPANA) to the plane of the sugar ring. The complex structures are at resolutions of 1.6 angstroms, 1.6 angstroms and 1.9 angstroms, respectively. These analyses show the STNA active site to be topologically inflexible and the interactions to be dominated by the arginine triad, with the pyranose rings of the inhibitors undergoing distortion to occupy the space available. Solvent structure differs only around the third phosphonate oxygen, which attracts a potassium ion. The STNA structure is topologically identical to the previously reported influenza virus neuraminidase structures, although very different in detail; the root-mean-square (r.m.s) deviation for 210 C alpha positions considered equivalent is 2.28 angstroms (out of a total of 390 residues in influenza and 381 in STNA). The active site residues are more highly conserved, in that both the viral and bacterial structures contain an arginine triad, a hydrophobic pocket, a tyrosine and glutamic acid residue at the base of the site and a potential proton-donating aspartic acid. However, differences in binding to O4 and to the glycerol side-chain may reflect the different kinetics employed by the two enzymes.

Reviews - 2sim mentioned but not cited (1)

  1. Sialidases from gut bacteria: a mini-review. Juge N, Tailford L, Owen CD. Biochem. Soc. Trans. 44 166-175 (2016)

Articles - 2sim mentioned but not cited (20)

  1. LIGSITEcsc: predicting ligand binding sites using the Connolly surface and degree of conservation. Huang B, Schroeder M. BMC Struct Biol 6 19 (2006)
  2. Tools for integrated sequence-structure analysis with UCSF Chimera. Meng EC, Pettersen EF, Couch GS, Huang CC, Ferrin TE. BMC Bioinformatics 7 339 (2006)
  3. PocketPicker: analysis of ligand binding-sites with shape descriptors. Weisel M, Proschak E, Schneider G. Chem Cent J 1 7 (2007)
  4. Sialidase fusion protein as a novel broad-spectrum inhibitor of influenza virus infection. Malakhov MP, Aschenbrenner LM, Smee DF, Wandersee MK, Sidwell RW, Gubareva LV, Mishin VP, Hayden FG, Kim DH, Ing A, Campbell ER, Yu M, Fang F. Antimicrob. Agents Chemother. 50 1470-1479 (2006)
  5. Structural alignment of proteins by a novel TOPOFIT method, as a superimposition of common volumes at a topomax point. Ilyin VA, Abyzov A, Leslin CM. Protein Sci 13 1865-1874 (2004)
  6. BCL::Score--knowledge based energy potentials for ranking protein models represented by idealized secondary structure elements. Woetzel N, Karakaş M, Staritzbichler R, Müller R, Weiner BE, Meiler J. PLoS One 7 e49242 (2012)
  7. Connectivity independent protein-structure alignment: a hierarchical approach. Kolbeck B, May P, Schmidt-Goenner T, Steinke T, Knapp EW. BMC Bioinformatics 7 510 (2006)
  8. Revealing divergent evolution, identifying circular permutations and detecting active-sites by protein structure comparison. Chen L, Wu LY, Wang Y, Zhang S, Zhang XS. BMC Struct Biol 6 18 (2006)
  9. Catalytic preference of Salmonella typhimurium LT2 sialidase for N-acetylneuraminic acid residues over N-glycolylneuraminic acid residues. Minami A, Ishibashi S, Ikeda K, Ishitsubo E, Hori T, Tokiwa H, Taguchi R, Ieno D, Otsubo T, Matsuda Y, Sai S, Inada M, Suzuki T. FEBS Open Bio 3 231-236 (2013)
  10. A novel approach to structural alignment using realistic structural and environmental information. Chen Y, Crippen GM. Protein Sci 14 2935-2946 (2005)
  11. Comparison of protein structures by growing neighborhood alignments. Bhattacharya S, Bhattacharyya C, Chandra NR. BMC Bioinformatics 8 77 (2007)
  12. Improving the performance of the PLB index for ligand-binding site prediction using dihedral angles and the solvent-accessible surface area. Cao C, Xu S. Sci Rep 6 33232 (2016)
  13. Splitting statistical potentials into meaningful scoring functions: testing the prediction of near-native structures from decoy conformations. Aloy P, Oliva B. BMC Struct. Biol. 9 71 (2009)
  14. Comparison of different ranking methods in protein-ligand binding site prediction. Gao J, Liu Q, Kang H, Cao Z, Zhu R. Int J Mol Sci 13 8752-8761 (2012)
  15. PMFF: Development of a Physics-Based Molecular Force Field for Protein Simulation and Ligand Docking. Hwang SB, Lee CJ, Lee S, Ma S, Kang YM, Cho KH, Kim SY, Kwon OY, Yoon CN, Kang YK, Yoon JH, Nam KY, Kim SG, In Y, Chai HH, Acree WE, Grant JA, Gibson KD, Jhon MS, Scheraga HA, No KT. J Phys Chem B 124 974-989 (2020)
  16. A new definition and properties of the similarity value between two protein structures. Saberi Fathi SM. J Biol Phys 42 621-636 (2016)
  17. An Efficient ABC_DE_Based Hybrid Algorithm for Protein-Ligand Docking. Guan B, Zhang C, Zhao Y. Int J Mol Sci 19 E1181 (2018)
  18. Exploring the landscape of protein-ligand interaction energy using probabilistic approach. Pacholczyk M, Kimmel M. J Comput Biol 18 843-850 (2011)
  19. GADP-align: A genetic algorithm and dynamic programming-based method for structural alignment of proteins. Mirzaei S, Razmara J, Lotfi S. Bioimpacts 11 271-279 (2021)
  20. Prediction of the Inhibition of Influenza Virus Neuraminidase Various Strains by Means of a Generalized Model Constructed Using the Data on the Position of Known Ligands. Mikurova AV, Rybina AV, Skvortsov VS. Biochem Mosc Suppl B Biomed Chem 15 166-170 (2021)


Reviews citing this publication (8)

  1. Structural and sequence-based classification of glycoside hydrolases. Henrissat B, Davies G. Curr. Opin. Struct. Biol. 7 637-644 (1997)
  2. Pneumococcal virulence factors: structure and function. Jedrzejas MJ. Microbiol. Mol. Biol. Rev. 65 187-207 ; first page, table of contents (2001)
  3. Sialidases: structures, biological significance and therapeutic potential. Taylor G. Curr. Opin. Struct. Biol. 6 830-837 (1996)
  4. Protein folds in the all-beta and all-alpha classes. Chothia C, Hubbard T, Brenner S, Barns H, Murzin A. Annu Rev Biophys Biomol Struct 26 597-627 (1997)
  5. A hydrophobic platform as a mechanistically relevant transition state stabilising factor appears to be present in the active centre of all glycoside hydrolases. Nerinckx W, Desmet T, Claeyssens M. FEBS Lett. 538 1-7 (2003)
  6. Current limitations to protein threading approaches. Smith TF, Lo Conte L, Bienkowska J, Gaitatzes C, Rogers RG, Lathrop R. J. Comput. Biol. 4 217-225 (1997)
  7. Host Sialic Acids: A Delicacy for the Pathogen with Discerning Taste. Haines-Menges BL, Whitaker WB, Lubin JB, Boyd EF. Microbiol Spectr 3 (2015)
  8. Pathogenicity and Virulence of Trueperella pyogenes: A Review. Rzewuska M, Kwiecień E, Chrobak-Chmiel D, Kizerwetter-Świda M, Stefańska I, Gieryńska M. Int J Mol Sci 20 (2019)

Articles citing this publication (32)

  1. Structure validation by Calpha geometry: phi,psi and Cbeta deviation. Lovell SC, Davis IW, Arendall WB, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC. Proteins 50 437-450 (2003)
  2. Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog. Chiu CP, Watts AG, Lairson LL, Gilbert M, Lim D, Wakarchuk WW, Withers SG, Strynadka NC. Nat. Struct. Mol. Biol. 11 163-170 (2004)
  3. Bacterial neuraminidase facilitates mucosal infection by participating in biofilm production. Soong G, Muir A, Gomez MI, Waks J, Reddy B, Planet P, Singh PK, Kaneko Y, Wolfgang MC, Hsiao YS, Tong L, Prince A. J. Clin. Invest. 116 2297-2305 (2006)
  4. The NanA neuraminidase of Streptococcus pneumoniae is involved in biofilm formation. Parker D, Soong G, Planet P, Brower J, Ratner AJ, Prince A. Infect. Immun. 77 3722-3730 (2009)
  5. Structural evidence for a second sialic acid binding site in avian influenza virus neuraminidases. Varghese JN, Colman PM, van Donkelaar A, Blick TJ, Sahasrabudhe A, McKimm-Breschkin JL. Proc. Natl. Acad. Sci. U.S.A. 94 11808-11812 (1997)
  6. Sensor domain of the Mycobacterium tuberculosis receptor Ser/Thr protein kinase, PknD, forms a highly symmetric beta propeller. Good MC, Greenstein AE, Young TA, Ng HL, Alber T. J. Mol. Biol. 339 459-469 (2004)
  7. The high resolution structures of free and inhibitor-bound Trypanosoma rangeli sialidase and its comparison with T. cruzi trans-sialidase. Amaya MF, Buschiazzo A, Nguyen T, Alzari PM. J. Mol. Biol. 325 773-784 (2003)
  8. Lysosomal neuraminidase. Catalytic activation in insect cells is controlled by the protective protein/cathepsin A. Bonten EJ, d'Azzo A. J. Biol. Chem. 275 37657-37663 (2000)
  9. M cell targeting with Aleuria aurantia lectin as a novel approach for oral allergen immunotherapy. Roth-Walter F, Schöll I, Untersmayr E, Fuchs R, Boltz-Nitulescu G, Weissenböck A, Scheiner O, Gabor F, Jensen-Jarolim E. J. Allergy Clin. Immunol. 114 1362-1368 (2004)
  10. Probing molecular function of trypanosomal sialidases: single point mutations can change substrate specificity and increase hydrolytic activity. Paris G, Cremona ML, Amaya MF, Buschiazzo A, Giambiagi S, Frasch AC, Alzari PM. Glycobiology 11 305-311 (2001)
  11. The crystal structure of an intramolecular trans-sialidase with a NeuAc alpha2-->3Gal specificity. Luo Y, Li SC, Chou MY, Li YT, Luo M. Structure 6 521-530 (1998)
  12. Cloning and characterization of sialidases with 2-6' and 2-3' sialyl lactose specificity from Pasteurella multocida. Mizan S, Henk A, Stallings A, Maier M, Lee MD. J. Bacteriol. 182 6874-6883 (2000)
  13. Bacterial catabolism of nonulosonic (sialic) acid and fitness in the gut. Almagro-Moreno S, Boyd EF. Gut Microbes 1 45-50 (2010)
  14. Cloning, expression, and characterization of a neuraminidase gene from Arcanobacterium pyogenes. Jost BH, Songer JG, Billington SJ. Infect. Immun. 69 4430-4437 (2001)
  15. Crystal structures of respiratory pathogen neuraminidases. Hsiao YS, Parker D, Ratner AJ, Prince A, Tong L. Biochem. Biophys. Res. Commun. 380 467-471 (2009)
  16. Enzymatic synthesis and properties of glycoconjugates with legionaminic acid as a replacement for neuraminic acid. Watson DC, Leclerc S, Wakarchuk WW, Young NM. Glycobiology 21 99-108 (2011)
  17. The 1.8 A structures of leech intramolecular trans-sialidase complexes: evidence of its enzymatic mechanism. Luo Y, Li SC, Li YT, Luo M. J. Mol. Biol. 285 323-332 (1999)
  18. A Gibbs free energy correlation for automated docking of carbohydrates. Hill AD, Reilly PJ. J Comput Chem 29 1131-1141 (2008)
  19. Comparison of protein surfaces using a genetic algorithm. Poirrette AR, Artymiuk PJ, Rice DW, Willett P. J. Comput. Aided Mol. Des. 11 557-569 (1997)
  20. Structural basis for inhibition of erythrocyte invasion by antibodies to Plasmodium falciparum protein CyRPA. Chen L, Xu Y, Wong W, Thompson JK, Healer J, Goddard-Borger ED, Lawrence MC, Cowman AF. Elife 6 (2017)
  21. Structural and biochemical characterization of the broad substrate specificity of Bacteroides thetaiotaomicron commensal sialidase. Park KH, Kim MG, Ahn HJ, Lee DH, Kim JH, Kim YW, Woo EJ. Biochim. Biophys. Acta 1834 1510-1519 (2013)
  22. CrystalDock: a novel approach to fragment-based drug design. Durrant JD, Friedman AJ, McCammon JA. J Chem Inf Model 51 2573-2580 (2011)
  23. Molecular cloning and expression of mouse brain sialidase. Fronda CL, Zeng G, Gao L, Yu RK. Biochem. Biophys. Res. Commun. 258 727-731 (1999)
  24. Elucidation of the role of functional amino acid residues of the small sialidase from Clostridium perfringens by site-directed mutagenesis. Kleineidam RG, Kruse S, Roggentin P, Schauer R. Biol. Chem. 382 313-319 (2001)
  25. One-bead-one-inhibitor-one-substrate screening of neuraminidase activity. Ying L, Gervay-Hague J. Chembiochem 6 1857-1865 (2005)
  26. Effect of cysteine modifications on the activity of the 'small' Clostridium perfringens sialidase. Kruse S, Pommerencke J, Kleineidam RG, Roggentin P, Schauer R. Glycoconj. J. 15 769-775 (1998)
  27. Synthesis of selective inhibitors against V. cholerae sialidase and human cytosolic sialidase NEU2. Khedri Z, Li Y, Cao H, Qu J, Yu H, Muthana MM, Chen X. Org. Biomol. Chem. 10 6112-6120 (2012)
  28. Computational 3-D modeling and site-directed mutation of an antibody that binds Neu2en5Ac, a transition state analogue of a sialic acid. Kamei H, Shimazaki K, Nishi Y. Proteins 45 285-296 (2001)
  29. A sialosyl sulfonate as a potent inhibitor of influenza virus replication. Hadházi Á, Pascolutti M, Bailly B, Dyason JC, Borbás A, Thomson RJ, von Itzstein M. Org. Biomol. Chem. 15 5249-5253 (2017)
  30. Macrocyclic mechanism-based inhibitor for neuraminidases. Kai H, Hinou H, Naruchi K, Matsushita T, Nishimura S. Chemistry 19 1364-1372 (2013)
  31. Crystal structure of the Propionibacterium acnes surface sialidase, a drug target for P. acnes-associated diseases. Yu ACY, Volkers G, Jongkees SAK, Worrall LJ, Withers SG, Strynadka NCJ. Glycobiology 32 162-170 (2022)
  32. Use of conformationally restricted pyridinium alpha-D-N-acetylneuraminides to probe specificity in bacterial and viral sialidases. Watson JN, Knoll TL, Chen JH, Chou DT, Borgford TJ, Bennet AJ. Biochem. Cell Biol. 83 115-122 (2005)


Related citations provided by authors (2)

  1. Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase.. Crennell SJ, Garman EF, Laver WG, Vimr ER, Taylor GL Proc Natl Acad Sci U S A 90 9852-6 (1993)
  2. Purification, Crystallisation and Preliminary Crystallographic Study of Neuraminidase from Vibrio Cholerae and Salmonella Typhimurium. Taylor GL, Vimr ER, Garman EF, Laver WG J. Mol. Biol. 226 1287- (1992)

Quick links