N-glycan analysis of recombinant l-selectin reveals sulfated GalNAc and GalNAc-GalNAc motifs

Journal of Proteome Research

Volumn 9, Issue 7, 2010, Pages 3403-3411

  Wedepohl, Stefanie ^a,b   Kaup, Matthias ^a   Riese, Sebastian B ^a   Berger, Markus ^a   Dernedde, Jens ^a   Tauber, Rudolf ^a   Blanchard, Véronique ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

GalNAc; L selectin; mass spectrometry; N glycans; sulfate

Indexed keywords

L SELECTIN; N ACETYLGALACTOSAMINE; OROSOMUCOID; RECOMBINANT PROTEIN; POLYSACCHARIDE;

ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEUKOCYTE ADHERENCE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; SULFATION; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; GENETICS; MASS SPECTROMETRY; MOLECULAR GENETICS;

ACETYLGALACTOSAMINE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL LINE; HUMANS; L-SELECTIN; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 77954357663     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100170c     Document Type: Article

References (46)

1. Ley, K.; Laudanna, C.; Cybulsky, M. I.; Nourshargh, S. Getting to the site of inflammation: the leukocyte adhesion cascade updated Nat. Rev. Immunol. 2007, 7 (9) 678-89
2. Schleiffenbaum, B.; Spertini, O.; Tedder, T. F. Soluble L-selectin is present in human plasma at high levels and retains functional activity J. Cell Biol. 1992, 119 (1) 229-38
3. Tedder, T. F.; Isaacs, C. M.; Ernst, T. J.; Demetri, G. D.; Adler, D. A.; Disteche, C. M. Isolation and chromosomal localization of cDNAs encoding a novel human lymphocyte cell surface molecule, LAM-1. Homology with the mouse lymphocyte homing receptor and other human adhesion proteins J. Exp. Med. 1989, 170 (1) 123-33
4. Lasky, L. A.; Singer, M. S.; Yednock, T. A.; Dowbenko, D.; Fennie, C.; Rodriguez, H.; Nguyen, T.; Stachel, S.; Rosen, S. D. Cloning of a lymphocyte homing receptor reveals a lectin domain Cell 1989, 56 (6) 1045-55
5. Siegelman, M. H.; Weissman, I. L. Human homologue of mouse lymph node homing receptor: evolutionary conservation at tandem cell interaction domains Proc. Natl. Acad. Sci. U.S.A. 1989, 86 (14) 5562-6
6. Gagneux, P.; Varki, A. Evolutionary considerations in relating oligosaccharide diversity to biological function Glycobiology 1999, 9 (8) 747-55
7. Sinclair, A. M.; Elliott, S. Glycoengineering: the effect of glycosylation on the properties of therapeutic proteins J. Pharm. Sci. 2005, 94 (8) 1626-35
8. Cumming, D. A. Glycosylation of recombinant protein therapeutics: control and functional implications Glycobiology 1991, 1 (2) 115-30
9. Fieger, C. B.; Emig-Vollmer, S.; Petri, T.; Grafe, M.; Gohlke, M.; Debus, N.; Semmler, W.; Tauber, R.; Volz, B. The adhesive properties of recombinant soluble L-selectin are modulated by its glycosylation Biochim. Biophys. Acta 2001, 1524 (1) 75-85
10. Simmons, D. L. Cellular Interactions in Development: A practical Approach; Oxford University Press: Oxford, 1993.
11. Romig, T. S.; Bell, C.; Drolet, D. W. Aptamer affinity chromatography: combinatorial chemistry applied to protein purification J. Chromatogr., B: Biomed. Sci. Appl. 1999, 731 (2) 275-84
12. Packer, N. H.; Lawson, M. A.; Jardine, D. R.; Redmond, J. W. A general approach to desalting oligosaccharides released from glycoproteins Glycoconj. J. 1998, 15 (8) 737-47
13. Bigge, J. C.; Patel, T. P.; Bruce, J. A.; Goulding, P. N.; Charles, S. M.; Parekh, R. B. Nonselective and efficient fluorescent labeling of glycans using 2-amino benzamide and anthranilic acid Anal. Biochem. 1995, 230 (2) 229-38
14. Nuck, R. Enzymatical hydrolysis of N-glycans from glycoproteins and fluorescent labeling by 2-aminobenzamide (2-AB) Methods Mol. Biol. 2008, 446, 231-8
15. Dell, A.; Khoo, K. H.; Panico, M.; McDowell, R. A.; Etienne, A. T.; Reaso, A. J.; Morris, H. R. Glycobiology: a practical approach; Oxford University Press: Oxford, 1993; pp 187 - 222.
16. Wada, Y.; Azadi, P.; Costello, C. E.; Dell, A.; Dwek, R. A.; Geyer, H.; Geyer, R.; Kakehi, K.; Karlsson, N. G.; Kato, K.; Kawasaki, N.; Khoo, K. H.; Kim, S.; Kondo, A.; Lattova, E.; Mechref, Y.; Miyoshi, E.; Nakamura, K.; Narimatsu, H.; Novotny, M. V.; Packer, N. H.; Perreault, H.; Peter-Katalinic, J.; Pohlentz, G.; Reinhold, V. N.; Rudd, P. M.; Suzuki, A.; Taniguchi, N. Comparison of the methods for profiling glycoprotein glycans - HUPO Human Disease Glycomics/Proteome Initiative multi-institutional study Glycobiology 2007, 17 (4) 411-22
17. Ceroni, A.; Maass, K.; Geyer, H.; Geyer, R.; Dell, A.; Haslam, S. M. GlycoWorkbench: a tool for the computer-assisted annotation of mass spectra of glycans J. Proteome Res. 2008, 7 (4) 1650-9
18. Maass, K.; Ranzinger, R.; Geyer, H.; von der Lieth, C. W.; Geyer, R. 'Glyco-peakfinder' - de novo composition analysis of glycoconjugates Proteomics 2007, 7 (24) 4435-44
19. Yan, S. B.; Chao, Y. B.; van Halbeek, H. Novel Asn-linked oligosaccharides terminating in GalNAc beta (1 - >4)[Fuc alpha (1 - >3)]GlcNAc beta (1 - >.) are present in recombinant human protein C expressed in human kidney 293 cells Glycobiology 1993, 3 (6) 597-608
20. Andre, M.; Morelle, W.; Planchon, S.; Milhiet, P. E.; Rubinstein, E.; Mollicone, R.; Chamot-Rooke, J.; Le Naour, F. Glycosylation status of the membrane protein CD9P-1 Proteomics 2007, 7 (21) 3880-95
21. Gohlke, M.; Mach, U.; Nuck, R.; Zimmermann-Kordmann, M.; Grunow, D.; Fieger, C.; Volz, B.; Tauber, R.; Petri, T.; Debus, N.; Reutter, W. Carbohydrate structures of soluble human L-selectin recombinantly expressed in baby-hamster kidney cells Biotechnol. Appl. Biochem. 2000, 32 (Pt 1) 41-51
22. Chan, A. L.; Morris, H. R.; Panico, M.; Etienne, A. T.; Rogers, M. E.; Gaffney, P.; Creighton-Kempsford, L.; Dell, A. A novel sialylated N-acetylgalactosamine-containing oligosaccharide is the major complex-type structure present in Bowes melanoma tissue plasminogen activator Glycobiology 1991, 1 (2) 173-85
23. Coddeville, B.; Strecker, G.; Wieruszeski, J. M.; Vliegenthart, J. F.; van Halbeek, H.; Peter-Katalinic, J.; Egge, H.; Spik, G. Heterogeneity of bovine lactotransferrin glycans. Characterization of alpha-D-Galp-(1 - >3)-beta-D-Gal- and alpha-NeuAc-(2 - >6)-beta-D-GalpNAc-(1 - >4)- beta-D-GlcNAc-substituted N-linked glycans Carbohydr. Res. 1992, 236, 145-64
24. Bergwerff, A. A.; Thomas-Oates, J. E.; van Oostrum, J.; Kamerling, J. P.; Vliegenthart, J. F. Human urokinase contains GalNAc beta (1-4)[Fuc alpha (1-3)]GlcNAc beta (1-2) as a novel terminal element in N-linked carbohydrate chains FEBS Lett. 1992, 314 (3) 389-94
25. Tomiya, N.; Awaya, J.; Kurono, M.; Hanzawa, H.; Shimada, I.; Arata, Y.; Yoshida, T.; Takahashi, N. Structural elucidation of a variety of GalNAc-containing N-linked oligosaccharides from human urinary kallidinogenase J. Biol. Chem. 1993, 268 (1) 113-26
26. Kubelka, V.; Altmann, F.; Staudacher, E.; Tretter, V.; Marz, L.; Hard, K.; Kamerling, J. P.; Vliegenthart, J. F. Primary structures of the N-linked carbohydrate chains from honeybee venom phospholipase A2 Eur. J. Biochem. 1993, 213 (3) 1193-204
27. Nakata, N.; Furukawa, K.; Greenwalt, D. E.; Sato, T.; Kobata, A. Structural study of the sugar chains of CD36 purified from bovine mammary epithelial cells: occurrence of novel hybrid-type sugar chains containing the Neu5Ac alpha 2 - >6GalNAc beta 1 - >4GlcNAc and the Man alpha 1 - >2Man alpha 1 - >3Man alpha 1 - >6Man groups Biochemistry 1993, 32 (16) 4369-83
28. Baenziger, J. U.; Green, E. D. Pituitary glycoprotein hormone oligosaccharides: structure, synthesis and function of the asparagine-linked oligosaccharides on lutropin, follitropin and thyrotropin Biochim. Biophys. Acta 1988, 947 (2) 287-306
29. Mengeling, B. J.; Manzella, S. M.; Baenziger, J. U. A cluster of basic amino acids within an alpha-helix is essential for alpha-subunit recognition by the glycoprotein hormone N-acetylgalactosaminyltransferase Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (2) 502-6
30. Yang, Y.; Thomas, V. H.; Man, S.; Rice, K. G. Tissue targeting of multivalent GalNAc Le(x) terminated N-glycans in mice Glycobiology 2000, 10 (12) 1341-5
31. Grinnell, B. W.; Hermann, R. B.; Yan, S. B. Human protein C inhibits selectin-mediated cell adhesion: role of unique fucosylated oligosaccharide Glycobiology 1994, 4 (2) 221-5
32. Varki, A. Selectin ligands Proc. Natl. Acad. Sci. U.S.A. 1994, 91 (16) 7390-7
33. Picker, L. J.; Warnock, R. A.; Burns, A. R.; Doerschuk, C. M.; Berg, E. L.; Butcher, E. C. The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140 Cell 1991, 66 (5) 921-33
34. Zollner, O.; Lenter, M. C.; Blanks, J. E.; Borges, E.; Steegmaier, M.; Zerwes, H. G.; Vestweber, D. L-selectin from human, but not from mouse neutrophils binds directly to E-selectin J. Cell Biol. 1997, 136 (3) 707-16
35. Smith, P. L.; Skelton, T. P.; Fiete, D.; Dharmesh, S. M.; Beranek, M. C.; MacPhail, L.; Broze, G. J., Jr.; Baenziger, J. U. The asparagine-linked oligosaccharides on tissue factor pathway inhibitor terminate with SO4-4GalNAc beta 1, 4GlcNAc beta 1,2 Mana alpha J. Biol. Chem. 1992, 267 (27) 19140-6
36. Gohlke, M.; Mach, U.; Nuck, R.; Volz, B.; Fieger, C.; Tauber, R.; Reutter, W. H (0) blood group determinant is present on soluble human L-selectin expressed in BHK-cells FEBS Lett. 1999, 450 (1-2) 111-6
37. Grossmann, M.; Szkudlinski, M. W.; Tropea, J. E.; Bishop, L. A.; Thotakura, N. R.; Schofield, P. R.; Weintraub, B. D. Expression of human thyrotropin in cell lines with different glycosylation patterns combined with mutagenesis of specific glycosylation sites. Characterization of a novel role for the oligosaccharides in the in vitro and in vivo bioactivity J. Biol. Chem. 1995, 270 (49) 29378-85
38. Van den Nieuwenhof, I. M.; Koistinen, H.; Easton, R. L.; Koistinen, R.; Kamarainen, M.; Morris, H. R.; Van Die, I.; Seppala, M.; Dell, A.; Van den Eijnden, D. H. Recombinant glycodelin carrying the same type of glycan structures as contraceptive glycodelin-A can be produced in human kidney 293 cells but not in chinese hamster ovary cells Eur. J. Biochem. 2000, 267 (15) 4753-62
39. Siciliano, R. A.; Morris, H. R.; McDowell, R. A.; Azadi, P.; Rogers, M. E.; Bennett, H. P.; Dell, A. The Lewis x epitope is a major non-reducing structure in the sulphated N-glycans attached to Asn-65 of bovine pro-opiomelanocortin Glycobiology 1993, 3 (3) 225-39
40. Skelton, T. P.; Kumar, S.; Smith, P. L.; Beranek, M. C.; Baenziger, J. U. Pro-opiomelanocortin synthesized by corticotrophs bears asparagine-linked oligosaccharides terminating with SO4-4GalNAc beta 1,4GlcNAc beta 1,2Man alpha J. Biol. Chem. 1992, 267 (18) 12998-3006
41. Hard, K.; Van Zadelhoff, G.; Moonen, P.; Kamerling, J. P.; Vliegenthart, F. G. The Asn-linked carbohydrate chains of human Tamm-Horsfall glycoprotein of one male. Novel sulfated and novel N-acetylgalactosamine-containing N-linked carbohydrate chains Eur. J. Biochem. 1992, 209 (3) 895-915
42. Hooper, L. V.; Beranek, M. C.; Manzella, S. M.; Baenziger, J. U. Differential expression of GalNAc-4-sulfotransferase and GalNAc-transferase results in distinct glycoforms of carbonic anhydrase VI in parotid and submaxillary glands J. Biol. Chem. 1995, 270 (11) 5985-93
43. Fiete, D.; Baenziger, J. U. Isolation of the SO4-4-GalNAcbeta1, 4GlcNAcbeta1,2Manalpha-specific receptor from rat liver J. Biol. Chem. 1997, 272 (23) 14629-37
44. Fiete, D.; Beranek, M. C.; Baenziger, J. U. The macrophage/endothelial cell mannose receptor cDNA encodes a protein that binds oligosaccharides terminating with SO4-4-GalNAcbeta1,4GlcNAcbeta or Man at independent sites Proc. Natl. Acad. Sci. U.S.A. 1997, 94 (21) 11256-61
45. Marttila-Ichihara, F.; Turja, R.; Miiluniemi, M.; Karikoski, M.; Maksimow, M.; Niemela, J.; Martinez-Pomares, L.; Salmi, M.; Jalkanen, S. Macrophage mannose receptor on lymphatics controls cell trafficking Blood 2008, 112 (1) 64-72
46. Irjala, H.; Johansson, E. L.; Grenman, R.; Alanen, K.; Salmi, M.; Jalkanen, S. Mannose receptor is a novel ligand for L-selectin and mediates lymphocyte binding to lymphatic endothelium J. Exp. Med. 2001, 194 (8) 1033-42