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Structural basis for the recognition and cleavage of polysialic acid by the bacteriophage K1F tailspike protein EndoNF.

Schulz EC, Schwarzer D, Frank M, Stummeyer K, Mühlenhoff M, Dickmanns A, Gerardy-Schahn R, Ficner R
J Mol Biol 397 341-51 (2010)
Related entries: 3gvj, 3gvk

Cited: 21 times
EuropePMC logo PMID: 20096705

Abstract

An alpha-2,8-linked polysialic acid (polySia) capsule confers immune tolerance to neuroinvasive, pathogenic prokaryotes such as Escherichia coli K1 and Neisseria meningitidis and supports host infection by means of molecular mimicry. Bacteriophages of the K1 family, infecting E. coli K1, specifically recognize and degrade this polySia capsule utilizing tailspike endosialidases. While the crystal structure for the catalytic domain of the endosialidase of bacteriophage K1F (endoNF) has been solved, there is yet no structural information on the mode of polySia binding and cleavage available. The crystal structure of activity deficient active-site mutants of the homotrimeric endoNF cocrystallized with oligomeric sialic acid identified three independent polySia binding sites in each endoNF monomer. The bound oligomeric sialic acid displays distinct conformations at each site. In the active site, a Sia(3) molecule is bound in an extended conformation representing the enzyme-product complex. Structural and biochemical data supported by molecular modeling enable to propose a reaction mechanism for polySia cleavage by endoNF.

Articles - 3gvl mentioned but not cited (1)

  1. The β-reducing end in α(2-8)-polysialic acid constitutes a unique structural motif. Azurmendi HF, Battistel MD, Zarb J, Lichaa F, Negrete Virgen A, Shiloach J, Freedberg DI. Glycobiology 27 900-911 (2017)


Reviews citing this publication (8)

  1. Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Schnaar RL, Gerardy-Schahn R, Hildebrandt H. Physiol. Rev. 94 461-518 (2014)
  2. Molecular architecture of tailed double-stranded DNA phages. Fokine A, Rossmann MG. Bacteriophage 4 e28281 (2014)
  3. Insights from bacterial subtilases into the mechanisms of intramolecular chaperone-mediated activation of furin. Shinde U, Thomas G. Methods Mol. Biol. 768 59-106 (2011)
  4. Evolution of the CNS myelin gene regulatory program. Li H, Richardson WD. Brain Res. 1641 111-121 (2016)
  5. Exploring the interactions between bacteriophage-encoded glycan binding proteins and carbohydrates. Simpson DJ, Sacher JC, Szymanski CM. Curr. Opin. Struct. Biol. 34 69-77 (2015)
  6. Micro-community cytometry: sensing changes in cell health and glycoconjugate expression by imaging and flow cytometry. Smith PJ, Falconer RA, Errington RJ. J Microsc 251 113-122 (2013)
  7. Neuroimmunomodulatory properties of polysialic acid. Gretenkort L, Thiesler H, Hildebrandt H. Glycoconj J 40 277-294 (2023)
  8. Yersinia Phages and Food Safety. Leon-Velarde CG, Jun JW, Skurnik M. Viruses 11 (2019)

Articles citing this publication (12)

  1. A multivalent adsorption apparatus explains the broad host range of phage phi92: a comprehensive genomic and structural analysis. Schwarzer D, Buettner FF, Browning C, Nazarov S, Rabsch W, Bethe A, Oberbeck A, Bowman VD, Stummeyer K, Mühlenhoff M, Leiman PG, Gerardy-Schahn R. J. Virol. 86 10384-10398 (2012)
  2. Structure of the receptor-binding carboxy-terminal domain of bacteriophage T7 tail fibers. Garcia-Doval C, van Raaij MJ. Proc. Natl. Acad. Sci. U.S.A. 109 9390-9395 (2012)
  3. Metabolism of vertebrate amino sugars with N-glycolyl groups: resistance of α2-8-linked N-glycolylneuraminic acid to enzymatic cleavage. Davies LR, Pearce OM, Tessier MB, Assar S, Smutova V, Pajunen M, Sumida M, Sato C, Kitajima K, Finne J, Gagneux P, Pshezhetsky A, Woods R, Varki A. J. Biol. Chem. 287 28917-28931 (2012)
  4. The sialate O-acetylesterase EstA from gut Bacteroidetes species enables sialidase-mediated cross-species foraging of 9-O-acetylated sialoglycans. Robinson LS, Lewis WG, Lewis AL. J. Biol. Chem. 292 11861-11872 (2017)
  5. Sialylation Is Dispensable for Early Murine Embryonic Development in Vitro. Abeln M, Borst KM, Cajic S, Thiesler H, Kats E, Albers I, Kuhn M, Kaever V, Rapp E, Münster-Kühnel A, Weinhold B. Chembiochem 18 1305-1316 (2017)
  6. Structure and biochemical characterization of bacteriophage phi92 endosialidase. Schwarzer D, Browning C, Stummeyer K, Oberbeck A, Mühlenhoff M, Gerardy-Schahn R, Leiman PG. Virology 477 133-143 (2015)
  7. The Aspergillus fumigatus sialidase is a 3-deoxy-D-glycero-D-galacto-2-nonulosonic acid hydrolase (KDNase): structural and mechanistic insights. Telford JC, Yeung JH, Xu G, Kiefel MJ, Watts AG, Hader S, Chan J, Bennet AJ, Moore MM, Taylor GL. J. Biol. Chem. 286 10783-10792 (2011)
  8. Molecular characterization, structural analysis and determination of host range of a novel bacteriophage LSB-1. Chai Y, Xiong H, Ma X, Cheng L, Huang G, Zhang ZR. Virol. J. 7 255 (2010)
  9. Synthesis of new polysialic acid derivatives. Su Y, Kasper C, Kirschning A, Dräger G, Berski S. Macromol Biosci 10 1028-1033 (2010)
  10. Characterization of a New Temperate Escherichia coli Phage vB_EcoP_ZX5 and Its Regulatory Protein. Li P, Yong S, Zhou X, Shen J. Pathogens 11 1445 (2022)
  11. Inverting family GH156 sialidases define an unusual catalytic motif for glycosidase action. Bule P, Chuzel L, Blagova E, Wu L, Gray MA, Henrissat B, Rapp E, Bertozzi CR, Taron CH, Davies GJ. Nat Commun 10 4816 (2019)
  12. Rational identification and characterisation of peptide ligands for targeting polysialic acid. Shastry DG, Irudayanathan FJ, Williams A, Koffas M, Linhardt RJ, Nangia S, Karande P. Sci Rep 10 7697 (2020)


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