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A novel alpha-helix in the first fibronectin type III repeat of the neural cell adhesion molecule is critical for N-glycan polysialylation.

Mendiratta SS, Sekulic N, Hernandez-Guzman FG, Close BE, Lavie A, Colley KJ
J Biol Chem 281 36052-9 (2006)
Cited: 41 times
EuropePMC logo PMID: 17003032

Abstract

Polysialic acid is a developmentally regulated, anti-adhesive glycan that is added to the neural cell adhesion molecule, NCAM. Polysialylated NCAM is critical for brain development and plays roles in synaptic plasticity, axon guidance, and cell migration. The first fibronectin type III repeat of NCAM, FN1, is necessary for the polysialylation of N-glycans on the adjacent immunoglobulin domain. This repeat cannot be replaced by other fibronectin type III repeats. We solved the crystal structure of human NCAM FN1 and found that, in addition to a unique acidic surface patch, it possesses a novel alpha-helix that links strands 4 and 5 of its beta-sandwich structure. Replacement of the alpha-helix did not eliminate polysialyltransferase recognition, but shifted the addition of polysialic acid from the N-glycans modifying the adjacent immunoglobulin domain to O-glycans modifying FN1. Other experiments demonstrated that replacement of residues in the acidic surface patch alter the polysialylation of both N- and O-glycans in the same way, while the alpha-helix is only required for the polysialylation of N-glycans. Our data are consistent with a model in which the FN1 alpha-helix is involved in an Ig5-FN1 interaction that is critical for the correct positioning of Ig5 N-glycans for polysialylation.

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Reviews citing this publication (10)

  1. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Rutishauser U. Nat Rev Neurosci 9 26-35 (2008)
  2. Sialylation of N-glycans: mechanism, cellular compartmentalization and function. Bhide GP, Colley KJ. Histochem Cell Biol 147 149-174 (2017)
  3. Dissecting polysialic acid and NCAM functions in brain development. Hildebrandt H, Mühlenhoff M, Weinhold B, Gerardy-Schahn R. J Neurochem 103 Suppl 1 56-64 (2007)
  4. Immunoglobulin superfamily cell adhesion molecules: zippers and signals. Aricescu AR, Jones EY. Curr Opin Cell Biol 19 543-550 (2007)
  5. Polysialic acid: biosynthesis, novel functions and applications. Colley KJ, Kitajima K, Sato C. Crit Rev Biochem Mol Biol 49 498-532 (2014)
  6. Paradigms for glycan-binding receptors in cell adhesion. Taylor ME, Drickamer K. Curr Opin Cell Biol 19 572-577 (2007)
  7. Polysialic acid: versatile modification of NCAM, SynCAM 1 and neuropilin-2. Mühlenhoff M, Rollenhagen M, Werneburg S, Gerardy-Schahn R, Hildebrandt H. Neurochem Res 38 1134-1143 (2013)
  8. Brain development needs sugar: the role of polysialic acid in controlling NCAM functions. Mühlenhoff M, Oltmann-Norden I, Weinhold B, Hildebrandt H, Gerardy-Schahn R. Biol Chem 390 567-574 (2009)
  9. Is Polysialylated NCAM Not Only a Regulator during Brain Development But also during the Formation of Other Organs? Galuska CE, Lütteke T, Galuska SP. Biology (Basel) 6 E27 (2017)
  10. NCAM1 Polysialylation: The Prion Protein's Elusive Reason for Being? Mehrabian M, Hildebrandt H, Schmitt-Ulms G. ASN Neuro 8 1759091416679074 (2016)

Articles citing this publication (22)

  1. Polysialylated neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte interactions. Curreli S, Arany Z, Gerardy-Schahn R, Mann D, Stamatos NM. J Biol Chem 282 30346-30356 (2007)
  2. Identification of sequences in the polysialyltransferases ST8Sia II and ST8Sia IV that are required for the protein-specific polysialylation of the neural cell adhesion molecule, NCAM. Foley DA, Swartzentruber KG, Colley KJ. J Biol Chem 284 15505-15516 (2009)
  3. Kinetic analysis of L1 homophilic interaction: role of the first four immunoglobulin domains and implications on binding mechanism. Gouveia RM, Gomes CM, Sousa M, Alves PM, Costa J. J Biol Chem 283 28038-28047 (2008)
  4. Pharmacological inhibition of polysialyltransferase ST8SiaII modulates tumour cell migration. Al-Saraireh YM, Sutherland M, Springett BR, Freiberger F, Ribeiro Morais G, Loadman PM, Errington RJ, Smith PJ, Fukuda M, Gerardy-Schahn R, Patterson LH, Shnyder SD, Falconer RA. PLoS One 8 e73366 (2013)
  5. Structure of the tandem fibronectin type 3 domains of neural cell adhesion molecule. Carafoli F, Saffell JL, Hohenester E. J Mol Biol 377 524-534 (2008)
  6. Polysialylation of the synaptic cell adhesion molecule 1 (SynCAM 1) depends exclusively on the polysialyltransferase ST8SiaII in vivo. Rollenhagen M, Kuckuck S, Ulm C, Hartmann M, Galuska SP, Geyer R, Geyer H, Mühlenhoff M. J Biol Chem 287 35170-35180 (2012)
  7. Fibroblast growth factor-derived peptides: functional agonists of the fibroblast growth factor receptor. Li S, Christensen C, Kiselyov VV, Køhler LB, Bock E, Berezin V. J Neurochem 104 667-682 (2008)
  8. A necessary and sufficient determinant for protein-selective glycosylation in vivo. Miller E, Fiete D, Blake NM, Beranek M, Oates EL, Mi Y, Roseman DS, Baenziger JU. J Biol Chem 283 1985-1991 (2008)
  9. A peptide motif from the second fibronectin module of the neural cell adhesion molecule, NCAM, NLIKQDDGGSPIRHY, is a binding site for the FGF receptor. Jacobsen J, Kiselyov V, Bock E, Berezin V. Neurochem Res 33 2532-2539 (2008)
  10. Sequences prior to conserved catalytic motifs of polysialyltransferase ST8Sia IV are required for substrate recognition. Zapater JL, Colley KJ. J Biol Chem 287 6441-6453 (2012)
  11. Sequences at the interface of the fifth immunoglobulin domain and first fibronectin type III repeat of the neural cell adhesion molecule are critical for its polysialylation. Thompson MG, Foley DA, Swartzentruber KG, Colley KJ. J Biol Chem 286 4525-4534 (2011)
  12. The polysialyltransferases interact with sequences in two domains of the neural cell adhesion molecule to allow its polysialylation. Thompson MG, Foley DA, Colley KJ. J Biol Chem 288 7282-7293 (2013)
  13. Characterization of a new rhamnogalacturonan acetyl esterase from Bacillus halodurans C-125 with a new putative carbohydrate binding domain. Navarro-Fernández J, Martínez-Martínez I, Montoro-García S, García-Carmona F, Takami H, Sánchez-Ferrer A. J Bacteriol 190 1375-1382 (2008)
  14. NCAM-derived peptides function as agonists for the fibroblast growth factor receptor. Hansen SM, Køhler LB, Li S, Kiselyov V, Christensen C, Owczarek S, Bock E, Berezin V. J Neurochem 106 2030-2041 (2008)
  15. Effects of amino acid substitutions in the sialylmotifs on molecular expression and enzymatic activities of α2,8-sialyltransferases ST8Sia-I and ST8Sia-VI. Takashima S, Matsumoto T, Tsujimoto M, Tsuji S. Glycobiology 23 603-612 (2013)
  16. Sequences from the first fibronectin type III repeat of the neural cell adhesion molecule allow O-glycan polysialylation of an adhesion molecule chimera. Foley DA, Swartzentruber KG, Thompson MG, Mendiratta SS, Colley KJ. J Biol Chem 285 35056-35067 (2010)
  17. WITHDRAWN: Polysialylation of NCAM. Hildebrandt H, Mühlenhoff M, Gerardy-Schahn R. Neurochem Res (2008)
  18. Intrabodies against the Polysialyltransferases ST8SiaII and ST8SiaIV inhibit Polysialylation of NCAM in rhabdomyosarcoma tumor cells. Somplatzki S, Mühlenhoff M, Kröger A, Gerardy-Schahn R, Böldicke T. BMC Biotechnol 17 42 (2017)
  19. WITHDRAWN: NCAM and the FGF-Receptor. Kiselyov VV. Neurochem Res (2008)
  20. WITHDRAWN: Structural Biology of NCAM. Soroka V, Kasper C, Poulsen FM. Neurochem Res (2008)
  21. WITHDRAWN: Biosynthesis of NCAM. Kolkova K. Neurochem Res (2008)
  22. WITHDRAWN: Synthetic NCAM-derived Ligands of the Fibroblast Growth Factor Receptor. Hansen SM, Li S, Bock E, Berezin V. Neurochem Res (2008)


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