Structure of human ST8SiaIII sialyltransferase provides insight into cell-surface polysialylation

Nature Structural and Molecular Biology

Volumn 22, Issue 8, 2015, Pages 627-635

  Volkers, Gesa ^a   Worrall, Liam J ^a   Kwan, David H ^a,b   Yu, Ching Ching ^a,b   Baumann, Lars ^a,b   Lameignere, Emilie ^a   Wasney, Gregory A ^a   Scott, Nichollas E ^a,b   Wakarchuk, Warren ^b   Foster, Leonard J ^a   Withers, Stephen G ^a   Strynadka, Natalie C J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b RYERSON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; POLYSIALIC ACID; SIALYLTRANSFERASE; ST8SIAIII SIALYLTRANSFERASE; SUGAR; UNCLASSIFIED DRUG; NERVE CELL ADHESION MOLECULE; POLYSACCHARIDE; PROTEIN BINDING; RECOMBINANT PROTEIN; SIA(ALPHA2,3)GAL(BETA1,4)GLCNAC ALPHA-2,8-SIALYLTRANSFERASE; SIALIC ACID DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME GLYCOSYLATION; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ENZYME SYNTHESIS; HONEYBEE; HUMAN; HYDROGEN BOND; HYDROLYSIS; INSECT CELL CULTURE; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; SIALYLATION; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CELL CULTURE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; GLYCOSYLATION; KINETICS; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCEDURES; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; THIN LAYER CHROMATOGRAPHY; X RAY CRYSTALLOGRAPHY;

MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELLS, CULTURED; CHROMATOGRAPHY, THIN LAYER; CRYSTALLOGRAPHY, X-RAY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCOSYLATION; HUMANS; KINETICS; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NEURAL CELL ADHESION MOLECULES; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIALIC ACIDS; SIALYLTRANSFERASES;

EID: 84938750981     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3060     Document Type: Article

References (78)

1. Varki, A. & Schauer, R. in Essentials of Glycobiology (Cold Spring Harbor Laboratory Press, 2009).
2. Sato, C. & Kitajima, K. Disialic, oligosialic and polysialic acids: distribution, functions and related disease. J. Biochem. 154, 115-136 (2013).
3. Crocker, P. R., Paulson, J. C. & Varki, A. Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7, 255-266 (2007).
4. Mühlenhoff, M., Rollenhagen, M., Werneburg, S., Gerardy-Schahn, R. & Hildebrandt, H. Polysialic acid: versatile modification of NCAM, SynCAM 1 and neuropilin-2. Neurochem. Res. 38, 1134-1143 (2013).
5. Acheson, A., Sunshine, J. L. & Rutishauser, U. NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions. J. Cell Biol. 114, 143-153 (1991).
6. Schnaar, R. L., Gerardy-Schahn, R. & Hildebrandt, H. Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol. Rev. 94, 461-518 (2014).
7. Doherty, P., Cohen, J. & Walsh, F. S. Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron 5, 209-219 (1990).
8. Rutishauser, U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9, 26-35 (2008).
9. Isomura, R., Kitajima, K. & Sato, C. Structural and functional impairments of polysialic acid by a mutated polysialyltransferase found in schizophrenia. J. Biol. Chem. 286, 21535-21545 (2011).
10. Falconer, R. A., Errington, R. J., Shnyder, S. D., Smith, P. J. & Patterson, L. H. Polysialyltransferase: a new target in metastatic cancer. Curr. Cancer Drug Targets 12, 925-939 (2012).
11. Cantarel, B. L. et al. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238 (2009).
12. Angata, K. & Fukuda, M. Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie 85, 195-206 (2003).
13. Foley, D. A., Swartzentruber, K. G. & Colley, K. J. 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. J. Biol. Chem. 284, 15505-15516 (2009).
14. Angata, K. et al. Differential biosynthesis of polysialic acid on neural cell adhesion molecule (NCAM) and oligosaccharide acceptors by three distinct alpha 2,8-sialyltransferases, ST8Sia IV (PST), ST8Sia II (STX), and ST8Sia III. J. Biol. Chem. 275, 18594-18601 (2000).
15. Yoshida, Y., Kojima, N., Kurosawa, N., Hamamoto, T. & Tsuji, S. Molecular cloning of Sia alpha 2,3Gal beta 1,4GlcNAc alpha 2,8-sialyltransferase from mouse brain. J. Biol. Chem. 270, 14628-14633 (1995).
16. Lee, Y. C. et al. Cloning and expression of cDNA for a human Sia alpha 2,3Gal beta 1, 4GlcNA:alpha 2,8-sialyltransferase (hST8Sia III). Arch. Biochem. Biophys. 360, 41-46 (1998).
17. Inoko, E. et al. Developmental stage-dependent expression of an alpha2,8-trisialic acid unit on glycoproteins in mouse brain. Glycobiology 20, 916-928 (2010).
18. Jarvis, D. L. Baculovirus-insect cell expression systems. Methods Enzymol. 463, 191-222 (2009).
19. Kojima, N., Tachida, Y., Yoshida, Y. & Tsuji, S. Characterization of mouse ST8Sia II (STX) as a neural cell adhesion molecule-specific polysialic acid synthase: requirement of core alpha1,6-linked fucose and a polypeptide chain for polysialylation. J. Biol. Chem. 271, 19457-19463 (1996).
20. Kitazume-Kawaguchi, S., Kabata, S. & Arita, M. Differential biosynthesis of polysialic or disialic acid structure by ST8Sia II and ST8Sia IV. J. Biol. Chem. 276, 15696-15703 (2001).
21. Blixt, O. et al. Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. USA 101, 17033-17038 (2004).
22. Blixt, O. et al. Glycan microarrays for screening sialyltransferase specificities. Glycoconj. J. 25, 59-68 (2008).
23. Rao, F. V. et al. Structural insight into mammalian sialyltransferases. Nat. Struct. Mol. Biol. 16, 1186-1188 (2009).
24. Kuhn, B. et al. The structure of human alpha-2,6-sialyltransferase reveals the binding mode of complex glycans. Acta Crystallogr. D Biol. Crystallogr. 69, 1826-1838 (2013).
25. Meng, L. et al. Enzymatic basis for N-glycan sialylation: structure of rat alpha2,6-sialyltransferase (ST6GAL1) reveals conserved and unique features for glycan sialylation. J. Biol. Chem. 288, 34680-34698 (2013).
26. Datta, A. K. & Paulson, J. C. The sialyltransferase "sialylmotif" participates in binding the donor substrate CMP-NeuAc. J. Biol. Chem. 270, 1497-1500 (1995).
27. Geremia, R. A., Harduin-Lepers, A. & Delannoy, P. Identification of two novel conserved amino acid residues in eukaryotic sialyltransferases: implications for their mechanism of action. Glycobiology 7, v-vii (1997).
28. Jeanneau, C. et al. Structure-function analysis of the human sialyltransferase ST3Gal I: role of N-glycosylation and a novel conserved sialylmotif. J. Biol. Chem. 279, 13461-13468 (2004).
29. Wen, D. X. et al. Primary structure of Gal beta 1,3(4)GlcNAc alpha 2,3-sialyltransferase determined by mass spectrometry sequence analysis and molecular cloning: evidence for a protein motif in the sialyltransferase gene family. J. Biol. Chem. 267, 21011-21019 (1992).
30. Datta, A. K. Comparative sequence analysis in the sialyltransferase protein family: analysis of motifs. Curr. Drug Targets 10, 483-498 (2009).
31. Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (2007).
32. Varki, A., Esko, J. D. & Colley, K. J. in Essentials of Glycobiology (Cold Spring Harbor Laboratory Press, 2009).
33. Angata, K., Yen, T. Y., El-Battari, A., Macher, B. A. & Fukuda, M. Unique disulfide bond structures found in ST8Sia IV polysialyltransferase are required for its activity. J. Biol. Chem. 276, 15369-15377 (2001).
34. Kulahin, N. et al. Direct demonstration of NCAM cis-dimerization and inhibitory effect of palmitoylation using the BRET2 technique. FEBS Lett. 585, 58-64 (2011).
35. Chiu, C. P. et al. Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog. Nat. Struct. Mol. Biol. 11, 163-170 (2004).
36. Qasba, P. K., Ramakrishnan, B. & Boeggeman, E. Substrate-induced conformational changes in glycosyltransferases. Trends Biochem. Sci. 30, 53-62 (2005).
37. Nakata, D., Zhang, L. & Troy, F. A. II. Molecular basis for polysialylation: a novel polybasic polysialyltransferase domain (PSTD) of 32 amino acids unique to the alpha 2,8-polysialyltransferases is essential for polysialylation. Glycoconj. J. 23, 423-436 (2006).
38. Audry, M. et al. Current trends in the structure-activity relationships of sialyltransferases. Glycobiology 21, 716-726 (2011).
39. Datta, A. K., Sinha, A. & Paulson, J. C. Mutation of the sialyltransferase S-sialylmotif alters the kinetics of the donor and acceptor substrates. J. Biol. Chem. 273, 9608-9614 (1998).
40. Klohs, W. D., Bernacki, R. J. & Korytnyk, W. Effects of nucleotides and nucleotide:analogs on human serum sialyltransferase. Cancer Res. 39, 1231-1238 (1979).
41. Lin, L. Y. et al. Structure and mechanism of the lipooligosaccharide sialyltransferase from Neisseria meningitidis. J. Biol. Chem. 286, 37237-37248 (2011).
42. Zielinska, D. F., Gnad, F., Wisniewski, J. R. & Mann, M. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897-907 (2010).
43. Funderburgh, J. L. Keratan sulfate: structure, biosynthesis, and function. Glycobiology 10, 951-958 (2000).
44. Tai, G. H., Huckerby, T. N. & Nieduszynski, I. A. Multiple non-reducing chain termini isolated from bovine corneal keratan sulfates. J. Biol. Chem. 271, 23535-23546 (1996).
45. Lauder, R. M., Huckerby, T. N. & Nieduszynski, I. A. Lectin affinity chromatography of articular cartilage fibromodulin: Some molecules have keratan sulphate chains exclusively capped by alpha(2-3)-linked sialic acid. Glycoconj. J. 28, 453-461 (2011).
46. Juneja, S. C. & Veillette, C. Defects in tendon, ligament, and enthesis in response to genetic alterations in key proteoglycans and glycoproteins: a review. Arthritis 2013, 154812 (2013).
47. Bentrop, J., Marx, M., Schattschneider, S., Rivera-Milla, E. & Bastmeyer, M. Molecular evolution and expression of zebrafish St8SiaIII, an alpha-2,8-sialyltransferase involved in myotome development. Dev. Dyn. 237, 808-818 (2008).
48. Angata, K., Chan, D., Thibault, J. & Fukuda, M. Molecular dissection of the ST8Sia IV polysialyltransferase: distinct domains are required for neural cell adhesion molecule recognition and polysialylation. J. Biol. Chem. 279, 25883-25890 (2004).
49. Zapater, J. L. & Colley, K. J. Sequences prior to conserved catalytic motifs of polysialyltransferase ST8Sia IV are required for substrate recognition. J. Biol. Chem. 287, 6441-6453 (2012).
50. Song, Y. et al. High-resolution comparative modeling with RosettaCM. Structure 21, 1735-1742 (2013).
51. Gray, J. J. et al. Protein-protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations. J. Mol. Biol. 331, 281-299 (2003).
52. Foley, D. A., Swartzentruber, K. G., Lavie, A. & Colley, K. J. Structure and mutagenesis of neural cell adhesion molecule domains: evidence for flexibility in the placement of polysialic acid attachment sites. J. Biol. Chem. 285, 27360-27371 (2010).
53. Foley, D. A., Swartzentruber, K. G., Thompson, M. G., Mendiratta, S. S. & Colley, K. J. Sequences from the first fibronectin type III repeat of the neural cell adhesion molecule allow O-glycan polysialylation of an adhesion molecule chimera. J. Biol. Chem. 285, 35056-35067 (2010).
54. Mendiratta, S. S., Sekulic, N., Lavie, A. & Colley, K. J. Specific amino acids in the first fibronectin type III repeat of the neural cell adhesion molecule play a role in its recognition and polysialylation by the polysialyltransferase ST8Sia IV/PST. J. Biol. Chem. 280, 32340-32348 (2005).
55. Thompson, M. G., Foley, D. A. & Colley, K. J. The polysialyltransferases interact with sequences in two domains of the neural cell adhesion molecule to allow its polysialylation. J. Biol. Chem. 288, 7282-7293 (2013).
56. Close, B. E., Tao, K. & Colley, K. J. Polysialyltransferase-1 autopolysialylation is not requisite for polysialylation of neural cell adhesion molecule. J. Biol. Chem. 275, 4484-4491 (2000).
57. Mühlenhoff, M., Manegold, A., Windfuhr, M., Gotza, B. & Gerardy-Schahn, R. The impact of N-glycosylation on the functions of polysialyltransferases. J. Biol. Chem. 276, 34066-34073 (2001).
58. Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98, 10037-10041 (2001).
59. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
60. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
61. Bunkóczi, G. & Read, R. J. Improvement of molecular-replacement models with Sculptor. Acta Crystallogr. D Biol. Crystallogr. 67, 303-312 (2011).
62. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
63. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
64. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367 (2011).
65. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
66. Winn, M. D., Isupov, M. N. & Murshudov, G. N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57, 122-133 (2001).
67. Laskowski, R. A. PDBsum new things. Nucleic Acids Res. 37, D355-D359 (2009).
68. Pettersen, E. F. et al. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
69. Gilbert, M. et al. The genetic bases for the variation in the lipo-oligosaccharide of the mucosal pathogen, Campylobacter jejuni: biosynthesis of sialylated ganglioside mimics in the core oligosaccharide. J. Biol. Chem. 277, 327-337 (2002).
70. Gosselin, S., Alhussaini, M., Streiff, M. B., Takabayashi, K. & Palcic, M. M. A continuous spectrophotometric assay for glycosyltransferases. Anal. Biochem. 220, 92-97 (1994).
71. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V. & Mann, M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860 (2006).
72. Ishihama, Y., Rappsilber, J. & Mann, M. Modular stop and go extraction tips with stacked disks for parallel and multidimensional peptide fractionation in proteomics. J. Proteome Res. 5, 988-994 (2006).
73. Rappsilber, J., Mann, M. & Ishihama, Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906 (2007).
74. Cristobal, A. et al. In-house construction of a UHPLC system enabling the identification of over 4000 protein groups in a single analysis. Analyst 137, 3541-3548 (2012).
75. Scott, N. E. et al. Simultaneous glycan-peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, higher energy collisional dissociation, and electron transfer dissociation MS applied to the N-linked glycoproteome of Campylobacter jejuni. Mol. Cell. Proteomics 10, M000031-MCP201 (2011).
76. Neuhauser, N., Michalski, A., Cox, J. & Mann, M. Expert system for computer assisted annotation of MS/MS spectra. Mol. Cell. Proteomics 11, 1500-1509 (2012).
77. Schulz, B. L. & Aebi, M. Analysis of glycosylation site occupancy reveals a role for Ost3p and Ost6p in site-specific N-glycosylation efficiency. Mol. Cell. Proteomics 8, 357-364 (2009).
78. Eswar, N. et al. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics 15, 5. 6 (2006).