The polysialyltransferases interact with sequences in two domains of the neural cell adhesion molecule to allow its polysialylation

Journal of Biological Chemistry

Volumn 288, Issue 10, 2013, Pages 7282-7293

  Thompson, Matthew G ^a   Foley, Deirdre A ^a   Colley, Karen J ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCANS; NEURAL CELL ADHESION MOLECULES; POLYSIALYLATION; PROTEIN SUBSTRATE; RECOGNITION SITE; TWO DOMAINS;

BIOCHEMISTRY; BIOLOGY;

PROTEINS;

ARGININE; ASPARAGINASE; FIBRONECTIN; FIBRONECTIN TYPE III; GLYCOPROTEIN; LYSINE; NERVE CELL ADHESION MOLECULE; OLFACTORY CELL ADHESION MOLECULE; POLYSIALYLTRANSFEASE; TRANSFERASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; DOWN REGULATION; ENZYME BINDING; ENZYME SUBSTRATE COMPLEX; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIALYLATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CERCOPITHECUS AETHIOPS; COS CELLS; FIBRONECTINS; GLYCOSYLATION; IMMUNOBLOTTING; IMMUNOGLOBULINS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NEURAL CELL ADHESION MOLECULES; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SIALIC ACIDS; SIALYLTRANSFERASES; SUBSTRATE SPECIFICITY;

EID: 84874903359     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.438374     Document Type: Article

References (48)

1. Varki, A. (1993) Biological roles of oligosaccharides. All of the theories are correct. Glycobiology 3, 97-130 (Pubitemid 23132602)
2. Haltiwanger, R. S., and Lowe, J. B. (2004) Role of glycosylation in development. Annu. Rev. Biochem. 73, 491-537 (Pubitemid 39050378)
3. Johnson, C. P., Fujimoto, I., Rutishauser, U., and Leckband, D. E. (2005) Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J. Biol. Chem. 280, 137-145 (Pubitemid 40164974)
4. Hildebrandt, H., Mühlenhoff, M., Weinhold, B., and Gerardy-Schahn, R. (2007) Dissecting polysialic acid and NCAM functions in brain development. J. Neurochem. 103, 56-64
5. Rutishauser, U. (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9, 26-35 (Pubitemid 350295686)
6. Rutishauser, U. (1996) Polysialic acid and the regulation of cell interactions. Curr. Opin. Cell Biol. 8, 679-684 (Pubitemid 26381725)
7. Nakayama, J., Angata, K., Ong, E., Katsuyama, T., and Fukuda, M. (1998) Polysialic acid, a unique glycan that is developmentally regulated by two polysialyltransferases, PST and STX, in the central nervous system. From biosynthesis to function. Pathol. Int. 48, 665-677 (Pubitemid 28445187)
8. Weinhold, B., Seidenfaden, R., Rockle, I.,Mühlenhoff, M., Schertzinger, F., Conzelmann, S., Marth, J. D., Gerardy-Schahn, R., and Hildebrandt, H. (2005) Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J. Biol. Chem. 280, 42971-42977 (Pubitemid 43049260)
9. Hildebrandt, H., Becker, C., Gluer, S., Rosner, H., Gerardy-Schahn, R., and Rahmann, H. (1998) Polysialic acid on the neural cell adhesion molecule correlates with expression of polysialyltransferases and promotes neuroblastoma cell growth. Cancer Res. 58, 779-784 (Pubitemid 28099491)
10. Komminoth, P., Roth, J., Lackie, P. M., Bitter-Suermann, D., and Heitz, P. U. (1991) Polysialic acid of the neural cell adhesion molecule distinguishes small cell lung carcinoma from carcinoids. Am. J. Pathol. 139, 297-304
11. Roth, J., Brada, D., Blaha, I., Ghielmini, C., Bitter-Suermann, D., Komminoth, P., and Heitz, P. U. (1988) Evaluation of polysialic acid in the diagnosis of Wilms' tumor. A comparative study on urinary tract tumors and non-neuroendocrine tumors. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 56, 95-102
12. Roth, J., Zuber, C., Wagner, P., Blaha, I., Bitter-Suermann, D., and Heitz, P. U. (1988) Presence of the long chain form of polysialic acid of the neural cell adhesion molecule in Wilms' tumor. Identification of a cell adhesion molecule as an oncodevelopmental antigen and implications for tumor histogenesis. Am. J. Pathol. 133, 227-240 (Pubitemid 19017485)
13. Scheidegger, E. P., Lackie, P. M., Papay, J., and Roth, J. (1994) In vitro and in vivo growth of clonal sublines of human small cell lung carcinoma is modulated by polysialic acid of the neural cell adhesion molecule. Lab. Invest. 70, 95-106 (Pubitemid 24080109)
14. Barbeau, D., Liang, J. J., Robitalille, Y., Quirion, R., and Srivastava, L. K. (1995) Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc. Natl. Acad. Sci. U.S.A. 92, 2785-2789
15. Isomura, R., Kitajima, K., and Sato, C. (2011) Structural and functional impairments of polysialic acid by a mutated polysialyltransferase found in schizophrenia. J. Biol. Chem. 286, 21535-21545
16. Kanato, Y., Kitajima, K., and Sato, C. (2008) Direct binding of polysialic acid to a brain-derived neurotrophic factor depends on the degree of polymerization. Glycobiology 18, 1044-1053 (Pubitemid 352762839)
17. Ono, S., Hane, M., Kitajima, K., and Sato, C. (2012) Novel regulation of fibroblast growth factor 2 (FGF2)-mediated cell growth by polysialic acid. J. Biol. Chem. 287, 3710-3722
18. Eckhardt, M., Mühlenhoff, M., Bethe, A., Koopman, J., Frosch, M., and Gerardy-Schahn, R. (1995) Molecular characterization of eukaryotic polysialyltransferase-1. Nature 373, 715-718
19. Kojima, N., Yoshida, Y., and Tsuji, S. (1995) A developmentally regulated member of the sialyltransferase family (ST8Sia II, STX) is a polysialic acid synthase. FEBS Lett. 373, 119-122
20. Scheidegger, E. P., Sternberg, L. R., Roth, J., and Lowe, J. B. (1995)Ahuman STX cDNA confers polysialic acid expression in mammalian cells. J. Biol. Chem. 270, 22685-22688
21. Yabe, U., Sato, C., Matsuda, T., and Kitajima, K. (2003) Polysialic acid in human milk. CD36 is a new member of mammalian polysialic acid-containing glycoprotein. J. Biol. Chem. 278, 13875-13880 (Pubitemid 36799927)
22. Zuber, C., Lackie, P. M., Catterall, W. A., and Roth, J. (1992) Polysialic acid is associated with sodium channels and the neural cell adhesion molecule N-CAM in adult rat brain. J. Biol. Chem. 267, 9965-9971
23. Curreli, S., Arany, Z., Gerardy-Schahn, R., Mann, D., and Stamatos, N. M. (2007) Polysialylated neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte interactions. J. Biol. Chem. 282, 30346-30356 (Pubitemid 350035196)
24. Galuska, S. P., Rollenhagen, M., Kaup, M., Eggers, K., Oltmann-Norden, I., Schiff, M., Hartmann, M., Weinhold, B., Hildebrandt, H., Geyer, R., Mühlenhoff, M., and Geyer, H. (2010) Synaptic cell adhesion molecule Syn-CAM 1 is a target for polysialylation in postnatal mouse brain. Proc. Natl. Acad. Sci. U.S.A. 107, 10250-10255
25. Close, B. E., and Colley, K. J. (1998) In vivo autopolysialylation and localization of the polysialyltransferases PST and STX. J. Biol. Chem. 273, 34586-34593 (Pubitemid 29008942)
26. Mühlenhoff, M., Eckhardt, M., Bethe, A., Frosch, M., and Gerardy-Schahn, R. (1996) Autocatalytic polysialylation of polysialyltransferase-1. EMBO J. 15, 6943-6950 (Pubitemid 27023265)
27. Close, B. E., Mendiratta, S. S., Geiger, K. M., Broom, L. J., Ho, L. L., and Colley, K. J. (2003) The minimal structural domains required for neural cell adhesion molecule polysialylation by PST/ST8Sia IV and STX/ST8Sia II. J. Biol. Chem. 278, 30796-30805 (Pubitemid 36994587)
28. Mendiratta, S. S., Sekulic, N., Hernandez-Guzman, F. G., Close, B. E., Lavie, A., and Colley, K. J. (2006) A novel α-helix in the first fibronectin type III repeat of the neural cell adhesion molecule is critical for N-glycan polysialylation. J. Biol. Chem. 281, 36052-36059 (Pubitemid 46041338)
29. Mendiratta, S. S., Sekulic, N., Lavie, A., and Colley, K. J. (2005) 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 (Pubitemid 41361844)
30. Thompson, M. G., Foley, D. A., Swartzentruber, K. G., and Colley, K. J. (2011) 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. J. Biol. Chem. 286, 4525-4534
31. Angata, K., Suzuki, M., McAuliffe, J., Ding, Y., Hindsgaul, O., and Fukuda, M. (2000) Differential biosynthesis of polysialic acid on neural cell adhesion molecule (NCAM) and oligosaccharide acceptors by three distinct-2,8-sialyltransferases, ST8Sia IV (PST), ST8Sia II (STX), and ST8Sia III. J. Biol. Chem. 275, 18594-18601 (Pubitemid 30414823)
32. Kojima, N., Tachida, Y., Yoshida, Y., and Tsuji, S. (1996) Characterization of mouse ST8Sia II (STX) as a neural cell adhesion molecule-specific polysialic acid synthase. Requirement of core-1,6-linked fucose and a polypeptide chain for polysialylation. J. Biol. Chem. 271, 19457-19463 (Pubitemid 26271619)
33. Cunningham, B. A., Hemperly, J. J., Murray, B. A., Prediger, E. A., Brackenbury, R., and Edelman, G. M. (1987) Neural cell adhesion molecule. Structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236, 799-806 (Pubitemid 17071152)
34. Nelson, R. W., Bates, P. A., and Rutishauser, U. (1995) Protein determinants for specific polysialylation of the neural cell adhesion molecule. J. Biol. Chem. 270, 17171-17179
35. Foley, D. A., Swartzentruber, K. G., Thompson, M. G., Mendiratta, S. S., and Colley, K. J. (2010) 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
36. Paoloni-Giacobino, A., Chen, H., and Antonarakis, S. E. (1997) Cloning of a novel human neural cell adhesion molecule gene (NCAM2) that maps to chromosome region 21q21 and is potentially involved in Down syndrome. Genomics 43, 43-51 (Pubitemid 27310521)
37. Yoshihara, Y., Kawasaki, M., Tamada, A., Fujita, H., Hayashi, H., Kagamiyama, H., and Mori, K. (1997) OCAM. A new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J. Neurosci. 17, 5830-5842 (Pubitemid 27310498)
38. Walz, A., Mombaerts, P., Greer, C. A., and Treloar, H. B. (2006) Disrupted compartmental organization of axons and dendrites within olfactory glomeruli of mice deficient in the olfactory cell adhesion molecule, OCAM. Mol. Cell. Neurosci. 32, 1-14 (Pubitemid 43868092)
39. Takahashi, S., Kato, K., Nakamura, K., Nakano, R., Kubota, K., and Hamada, H. (2011) Neural cell adhesion molecule 2 as a target molecule for prostate and breast cancer gene therapy. Cancer Sci. 102, 808-814
40. Alenius, M., and Bohm, S. (1997) Identification of a novel neural cell adhesion molecule-related gene with a potential role in selective axonal projection. J. Biol. Chem. 272, 26083-26086 (Pubitemid 27458812)
41. Deutscher, S. L., Nuwayhid, N., Stanley, P., Briles, E. I., and Hirschberg, C. B. (1984) Translocation across Golgi vesicle membranes. A CHO glycosylation mutant deficient in CMP-sialic acid transport. Cell 39, 295-299 (Pubitemid 15191212)
42. Kulahin, N., Kristensen, O., Rasmussen, K. K., Olsen, L., Rydberg, P., Vestergaard, B., Kastrup, J. S., Berezin, V., Bock, E., Walmod, P. S., and Gajhede, M. (2011) Structural model and trans-interaction of the entire ectodomain of the olfactory cell adhesion molecule. Structure 19, 203-211
43. Foley, D. A., Swartzentruber, K. G., Lavie, A., and Colley, K. J. (2010) 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
44. Bohne-Lang, A., and von der Lieth, C. W. (2005) GlyProt. In silico glycosylation of proteins. Nucleic Acids Res. 33, W214-W219
45. Angata, K., Suzuki, M., and Fukuda, M. (2002) ST8Sia II and ST8Sia IV polysialyltransferases exhibit marked differences in utilizing various acceptors containing oligosialic acid and short polysialic acid. The basis for cooperative polysialylation by two enzymes. J. Biol. Chem. 277, 36808-36817
46. Galuska, S. P., Geyer, R., Gerardy-Schahn, R., Mühlenhoff, M., and Geyer, H. (2008) Enzyme-dependent variations in the polysialylation of the neural cell adhesion molecule (NCAM) in vivo. J. Biol. Chem. 283, 17-28
47. Foley, D. A., Swartzentruber, K. G., and Colley, K. J. (2009) 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
48. Zapater, J. L., and Colley, K. J. (2012) Sequences prior to conserved catalytic motifs of polysialyltransferase ST8Sia IV are required for substrate recognition. J. Biol. Chem. 287, 6441-6453