Glycoconjugate Journal

, Volume 31, Issue 2, pp 145–159 | Cite as

Avian influenza H5 hemagglutinin binds with high avidity to sialic acid on different O-linked core structures on mucin-type fusion proteins

  • Stefan Gaunitz
  • Jining Liu
  • Anki Nilsson
  • Niclas Karlsson
  • Jan Holgersson
Article

Abstract

The interaction between P-selectin glycoprotein ligand-1/mouse IgG2b (PSGL-1/mIgG2b) fusion protein carrying multiple copies of the influenza hemagglutinin receptor Siaα2-3Gal on different O-glycan chains and recombinant human influenza H5N1 A/Vietnam/1203/04 hemagglutinin was investigated with a Biacore biosensor. The fusion protein was produced by stable cell lines in large scale cultures and purified with affinity- and gel filtration chromatography. The C-P55 and 293-P cell lines were established by transfecting the Chinese hamster ovary (CHO)-K1 and Human embryonic kidney (HEK)-293 cell lines with plasmids encoding the PSGL-1/mIgG2b fusion protein, while the C-PSLex cell line was engineered by transfecting CHO-K1 cells with the plasmids encoding the core 2 β1,6GnT-I and FUT-VII glycosyltransferases. Glycosylation was characterized by lectin Western blotting of the proteins and liquid chromatography - mass spectrometry of released non-derivatized O-glycans. Biacore experiments revealed that PSGL-1/mIgG2b is a good binding partner of H5. The binding curves displayed a slow dissociation indicating a multivalent binding. The H5 hemagglutinin binds with similar strength to PSGL-1/mIgG2b carrying mostly sialylated core 1 (clone C-P55), a mix of sialylated core 1 and sialylated lactosamine (clone 293-P) or mainly sialylated lactosamine (clone C-PSLex) O-glycans, indicating that this hemagglutinin is unable to discriminate between these structures. The potential use of the large, flexible PSGL-1/mIgG2b mucin-type fusion protein carrying Siaα2-3Gal as a multivalent inhibitor of influenza virus is discussed.

Keywords

Mucins Avian influenza Hemagglutinin Mass spectrometry Biacore 

Abbreviations

P-selectin glycoprotein ligand-1/mouse IgG2b

PSGL-1/mIgG2b

LC-MS

liquid chromatography mass spectrometry

HexNAc

N-acetylhexosamine

GalNAc

N-acetylgalactosamine

GlcNAc

N-acetylglucosamine

Hex

hexose

Gal

galactose

CHO

chinese hamster ovary cells

Neu5Ac

N-acetylneuraminic acid

Sia

sialic acid

Notes

Acknowledgments

We acknowledge Dr. Jin Chunsheng and Liaqat Ali for their assistance with the liquid chromatography mass spectrometry analysis. We acknowledge Recopharma AB that provided PSGL-1/mIgG2b produced in C-P55, P-PM and C-PSLex and allowed us to use the Wave Bioreactor for the production of the 293-P cells. We thank Åsa Bergström for access to the Biacore 2000 instrument at the Department of Biosciences and Nutrition, Karolinska Institutet. We acknowledge Tom Morton at BioLogic Software for providing the Scrubber 2 software. We thank Catherine Hayes for helping us to publish the mass spectrometry data in the UniCarb-DB.

Conflicts of interest

J.H. is a part time CEO/CSO, board member and shareholder of Recopharma AB.

Funding

This work was supported by the Swedish Research Council [K2011-65X-3031-01-6 to J.H. and 621-2010-5322 to N.G.K.], the County Council of Västra Götaland (ALF) to J.H. and Karolinska Institute Faculty funds (KID-funding) to S.G. The mass spectrometer was obtained by a grant from the Swedish Research Council [342-2004-4434].

References

  1. 1.
    Fouchier, R.A., Munster, V., Wallensten, A., Bestebroer, T.M., Herfst, S., Smith, D., Rimmelzwaan, G.F., Olsen, B., Osterhaus, A.D.: Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79(5), 2814–2822 (2005)PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Baigent, S.J., McCauley, J.W.: Influenza type A in humans, mammals and birds: determinants of virus virulence, host-range and interspecies transmission. Bioessays 25(7), 657–671 (2003)PubMedCrossRefGoogle Scholar
  3. 3.
    Skehel, J.J., Wiley, D.C.: Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Ann Rev Biochem 69, 531–569 (2000)PubMedCrossRefGoogle Scholar
  4. 4.
    Josefsberg, J.O., Buckland, B.: Vaccine process technology. Biotechnol Bioeng 109(6), 1443–1460 (2012)PubMedCrossRefGoogle Scholar
  5. 5.
    Skehel, J.J., Bayley, P.M., Brown, E.B., Martin, S.R., Waterfield, M.D., White, J.M., Wilson, I.A., Wiley, D.C.: Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc Natl Acad Sci U S A 79(4), 968–972 (1982)PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Treanor, J., Nolan, C., O’Brien, D., Burt, D., Lowell, G., Linden, J., Fries, L.: Intranasal administration of a proteosome-influenza vaccine is well-tolerated and induces serum and nasal secretion influenza antibodies in healthy human subjects. Vaccine 24(3), 254–262 (2006)PubMedCrossRefGoogle Scholar
  7. 7.
    Garten, R.J., Davis, C.T., Russell, C.A., Shu, B., Lindstrom, S., Balish, A., Sessions, W.M., Xu, X., Skepner, E., Deyde, V., Okomo-Adhiambo, M., Gubareva, L., Barnes, J., Smith, C.B., Emery, S.L., Hillman, M.J., Rivailler, P., Smagala, J., de Graaf, M., Burke, D.F., Fouchier, R.A., Pappas, C., Alpuche-Aranda, C.M., Lopez-Gatell, H., Olivera, H., Lopez, I., Myers, C.A., Faix, D., Blair, P.J., Yu, C., Keene, K.M., Dotson Jr., P.D., Boxrud, D., Sambol, A.R., Abid, S.H., St George, K., Bannerman, T., Moore, A.L., Stringer, D.J., Blevins, P., Demmler-Harrison, G.J., Ginsberg, M., Kriner, P., Waterman, S., Smole, S., Guevara, H.F., Belongia, E.A., Clark, P.A., Beatrice, S.T., Donis, R., Katz, J., Finelli, L., Bridges, C.B., Shaw, M., Jernigan, D.B., Uyeki, T.M., Smith, D.J., Klimov, A.I., Cox, N.J.: Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325(5937), 197–201 (2009)PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Scholtissek, C., Rohde, W., Von Hoyningen, V., Rott, R.: On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 87(1), 13–20 (1978)PubMedCrossRefGoogle Scholar
  9. 9.
    Kuiken, T., Riteau, B., Fouchier, R.A., Rimmelzwaan, G.F.: Pathogenesis of influenza virus infections: the good, the bad and the ugly. Curr Opin Virol 2(3), 276–286 (2012)PubMedCrossRefGoogle Scholar
  10. 10.
    Johnson, N.P., Mueller, J.: Updating the accounts: global mortality of the 1918–1920 “Spanish” influenza pandemic. Bull Hist Med 76(1), 105–115 (2002)PubMedCrossRefGoogle Scholar
  11. 11.
    Olofsson, S., Kumlin, U., Dimock, K., Arnberg, N.: Avian influenza and sialic acid receptors: more than meets the eye? Lancet Infect Dis 5(3), 184–188 (2005)PubMedGoogle Scholar
  12. 12.
    Kuiken, T., Holmes, E.C., McCauley, J., Rimmelzwaan, G.F., Williams, C.S., Grenfell, B.T.: Host species barriers to influenza virus infections. Science 312(5772), 394–397 (2006)PubMedCrossRefGoogle Scholar
  13. 13.
    Suzuki, Y., Ito, T., Suzuki, T., Holland Jr., R.E., Chambers, T.M., Kiso, M., Ishida, H., Kawaoka, Y.: Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 74(24), 11825–11831 (2000)PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Matrosovich, M., Klenk, H.D.: Natural and synthetic sialic acid-containing inhibitors of influenza virus receptor binding. Rev Med Virol 13(2), 85–97 (2003)PubMedCrossRefGoogle Scholar
  15. 15.
    van Riel, D., Munster, V.J., de Wit, E., Rimmelzwaan, G.F., Fouchier, R.A., Osterhaus, A.D., Kuiken, T.: H5N1 virus attachment to lower respiratory tract. Science 312(5772), 399 (2006)PubMedCrossRefGoogle Scholar
  16. 16.
    Sorrell, E.M., Schrauwen, E.J., Linster, M., De Graaf, M., Herfst, S., Fouchier, R.A.: Predicting ‘airborne’ influenza viruses: (trans-) mission impossible? Curr Opin Virol 1(6), 635–642 (2011)PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Totani, K., Kubota, T., Kuroda, T., Murata, T., Hidari, K.I., Suzuki, T., Suzuki, Y., Kobayashi, K., Ashida, H., Yamamoto, K., Usui, T.: Chemoenzymatic synthesis and application of glycopolymers containing multivalent sialyloligosaccharides with a poly(L-glutamic acid) backbone for inhibition of infection by influenza viruses. Glycobiology 13(5), 315–326 (2003)PubMedCrossRefGoogle Scholar
  18. 18.
    Horimoto, T., Kawaoka, Y.: Strategies for developing vaccines against H5N1 influenza A viruses. Trends Mol Med 12(11), 506–514 (2006)PubMedCrossRefGoogle Scholar
  19. 19.
    Osterholm, M.T., Kelley, N.S.: Mammalian-transmissible H5N1 influenza: facts and perspective. mBio 3(2), e00045–00012 (2012)PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Fouchier, R.A., Schneeberger, P.M., Rozendaal, F.W., Broekman, J.M., Kemink, S.A., Munster, V., Kuiken, T., Rimmelzwaan, G.F., Schutten, M., Van Doornum, G.J., Koch, G., Bosman, A., Koopmans, M., Osterhaus, A.D.: Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 101(5), 1356–1361 (2004)PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Michaelis, M., Geiler, J., Klassert, D., Doerr, H.W., Cinatl Jr., J.: Infection of human retinal pigment epithelial cells with influenza A viruses. Invest Ophthalmol Vis Sci 50(11), 5419–5425 (2009)PubMedCrossRefGoogle Scholar
  22. 22.
    Belser, J.A., Gustin, K.M., Maines, T.R., Pantin-Jackwood, M.J., Katz, J.M., Tumpey, T.M.: Influenza virus respiratory infection and transmission following ocular inoculation in ferrets. PLoS Pathog 8(3), e1002569 (2012)PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Stevens, J., Blixt, O., Tumpey, T.M., Taubenberger, J.K., Paulson, J.C., Wilson, I.A.: Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312(5772), 404–410 (2006)PubMedCrossRefGoogle Scholar
  24. 24.
    Suenaga, E., Mizuno, H., Penmetcha, K.K.: Monitoring influenza hemagglutinin and glycan interactions using surface plasmon resonance. Biosensors Bioelectronics 32(1), 195–201 (2012)PubMedCrossRefGoogle Scholar
  25. 25.
    Osterholm, M.T., Kelley, N.S., Sommer, A., Belongia, E.A.: Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 12(1), 36–44 (2012)PubMedCrossRefGoogle Scholar
  26. 26.
    Moscona, A.: Neuraminidase inhibitors for influenza. New Engl J Med 353(13), 1363–1373 (2005)PubMedCrossRefGoogle Scholar
  27. 27.
    Ison, M.G., Hayden, F.G.: Therapeutic options for the management of influenza. Curr Opin Pharmacol 1(5), 482–490 (2001)PubMedCrossRefGoogle Scholar
  28. 28.
    Jefferson, T., Jones, M.A., Doshi, P., Del Mar, C.B., Heneghan, C.J., Hama, R., Thompson, M.J.: Neuraminidase inhibitors for preventing and treating influenza in healthy adults and children. Cochrane Database Syst Rev (Online) 1, CD008965 (2012)Google Scholar
  29. 29.
    Moscona, A.: Oseltamivir resistance–disabling our influenza defenses. New England J Med 353(25), 2633–2636 (2005)CrossRefGoogle Scholar
  30. 30.
    Bovin, N.V., Tuzikov, A.B.., Chinarev, A.A., Gambaryan, A.S.: Multimeric glycotherapeutics: new paradigm. Glycoconj J 21(8–9), 471–478 (2004)PubMedCrossRefGoogle Scholar
  31. 31.
    Liu, J., Gustafsson, A., Breimer, M.E., Kussak, A., Holgersson, J.: Anti-pig antibody adsorption efficacy of {alpha}-Gal carrying recombinant P-selectin glycoprotein ligand-1/immunoglobulin chimeras increases with core 2 {beta}1, 6-N-acetylglucosaminyltransferase expression. Glycobiology 15(6), 571–583 (2005)PubMedCrossRefGoogle Scholar
  32. 32.
    Ogata, M., Hidari, K.I., Murata, T., Shimada, S., Kozaki, W., Park, E.Y., Suzuki, T., Usui, T.: Chemoenzymatic synthesis of sialoglycopolypeptides as glycomimetics to block infection by avian and human influenza viruses. Bioconjug Chem 20(3), 538–549 (2009)PubMedCrossRefGoogle Scholar
  33. 33.
    Sauter, N.K., Bednarski, M.D., Wurzburg, B.A., Hanson, J.E., Whitesides, G.M., Skehel, J.J., Wiley, D.C.: Hemagglutinins from two influenza virus variants bind to sialic acid derivatives with millimolar dissociation constants: a 500-MHz proton nuclear magnetic resonance study. Biochemistry 28(21), 8388–8396 (1989)PubMedCrossRefGoogle Scholar
  34. 34.
    Toogood, P.L., Galliker, P.K., Glick, G.D., Knowles, J.R.: Monovalent sialosides that bind tightly to influenza A virus. J Med Chem 34(10), 3138–3140 (1991)PubMedCrossRefGoogle Scholar
  35. 35.
    Lowe, J.B.: Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr Opin Cell Biol 15(5), 531–538 (2003)PubMedCrossRefGoogle Scholar
  36. 36.
    Carlow, D.A., Gossens, K., Naus, S., Veerman, K.M., Seo, W., Ziltener, H.J.: PSGL-1 function in immunity and steady state homeostasis. Immunol Rev 230(1), 75–96 (2009)PubMedCrossRefGoogle Scholar
  37. 37.
    Ahlen, G., Strindelius, L., Johansson, T., Nilsson, A., Chatzissavidou, N., Sjoblom, M., Rova, U., Holgersson, J.: Mannosylated mucin-type immunoglobulin fusion proteins enhance antigen-specific antibody and T lymphocyte responses. PloS one 7(10), e46959 (2012)PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Lindberg, L., Liu, J., Gaunitz, S., Nilsson, A., Johansson, T., Karlsson, N.G., Holgersson, J.: Mucin-type fusion proteins with blood group A or B determinants on defined O-glycan core chains produced in glycoengineered CHO cells and their use as immunoaffinity matrices. Glycobiology (2013).Google Scholar
  39. 39.
    Gustafsson, A., Sjoblom, M., Strindelius, L., Johansson, T., Fleckenstein, T., Chatzissavidou, N., Lindberg, L., Angstrom, J., Rova, U., Holgersson, J.: Pichia pastoris-produced mucin-type fusion proteins with multivalent O-glycan substitution as targeting molecules for mannose-specific receptors of the immune system. Glycobiology 21(8), 1071–1086 (2011)PubMedCrossRefGoogle Scholar
  40. 40.
    Lofling, J., Holgersson, J.: Core saccharide dependence of sialyl Lewis X biosynthesis. Glycoconj J 26(1), 33–40 (2009)PubMedCrossRefGoogle Scholar
  41. 41.
    Lofling, J.C., Hauzenberger, E., Holgersson, J.: Absorption of anti-blood group A antibodies on P-selectin glycoprotein ligand-1/immunoglobulin chimeras carrying blood group A determinants: core saccharide chain specificity of the Se and H gene encoded alpha1,2 fucosyltransferases in different host cells. Glycobiology 12(3), 173–182 (2002)PubMedCrossRefGoogle Scholar
  42. 42.
    Gustafsson, A.: Carbohydrate-Dependent Inhibition of Protein-Carbohydrate Interactions, Doctoral thesis. Sahlgrenska Academy at Göteborg University (2005)Google Scholar
  43. 43.
    Cherian, R.M., Gaunitz, S., Nilsson, A., Liu, J., Karlsson, N.G., Holgersson, J.: Shiga-like toxin binds with high avidity to multivalent O-linked blood group P1 determinants on mucin type fusion proteins. Glycobiology (2013). doi: 10.1093/glycob/cwt086
  44. 44.
    Lindberg, L., Theinert, K., Liu, J., Holgersson, J.: Adsorption of chain type-specific ABO antibodies on Sepharose-linked A and B tetrasaccharides. Transfusion 52(11), 2356–2367 (2012)PubMedCrossRefGoogle Scholar
  45. 45.
    Karlsson, N.G., Packer, N.H.: Analysis of O-linked reducing oligosaccharides released by an in-line flow system. Anal Biochem 305(2), 173–185 (2002)PubMedCrossRefGoogle Scholar
  46. 46.
    van Dijk, W., Havenaar, E.C., Brinkman-van der Linden, E.C.: Alpha 1-acid glycoprotein (orosomucoid): pathophysiological changes in glycosylation in relation to its function. Glycoconj J 12(3), 227–233 (1995)PubMedCrossRefGoogle Scholar
  47. 47.
    Gornik, O., Lauc, G.: Glycosylation of serum proteins in inflammatory diseases. Dis Markers 25(4–5), 267–278 (2008)PubMedCrossRefGoogle Scholar
  48. 48.
    Xu, X., Nagarajan, H., Lewis, N.E., Pan, S., Cai, Z., Liu, X., Chen, W., Xie, M., Wang, W., Hammond, S., Andersen, M.R., Neff, N., Passarelli, B., Koh, W., Fan, H.C., Wang, J., Gui, Y., Lee, K.H., Betenbaugh, M.J., Quake, S.R., Famili, I., Palsson, B.O., Wang, J.: The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line. Nature Biotechnol 29(8), 735–741 (2011)CrossRefGoogle Scholar
  49. 49.
    Beck, A., Wagner-Rousset, E., Bussat, M.C., Lokteff, M., Klinguer-Hamour, C., Haeuw, J.F., Goetsch, L., Wurch, T., Van Dorsselaer, A., Corvaia, N.: Trends in glycosylation, glycoanalysis and glycoengineering of therapeutic antibodies and Fc-fusion proteins. Curr Pharm Biotechnol 9(6), 482–501 (2008)PubMedCrossRefGoogle Scholar
  50. 50.
    Gustafsson, A., Holgersson, J.: A new generation of carbohydrate-based therapeutics: recombinant mucin-type fusion proteins as versatile inhibitors of protein–carbohydrate interactions. Expert Opin Drug Disc 1(2), 161–178 (2006)CrossRefGoogle Scholar
  51. 51.
    Hidari, K.I., Shimada, S., Suzuki, Y., Suzuki, T.: Binding kinetics of influenza viruses to sialic acid-containing carbohydrates. Glycoconj J 24(9), 583–590 (2007)PubMedCrossRefGoogle Scholar
  52. 52.
    Meng, B., Marriott, A.C., Dimmock, N.J.: The receptor preference of influenza viruses. Influenza Other Respir Viruses 4(3), 147–153 (2010)PubMedCrossRefGoogle Scholar
  53. 53.
    Fasting, C., Schalley, C.A., Weber, M., Seitz, O., Hecht, S., Koksch, B., Dernedde, J., Graf, C., Knapp, E.W., Haag, R.: Multivalency as a chemical organization and action principle. Angewandte Chemie Int ed 51(42), 10472–10498 (2012)CrossRefGoogle Scholar
  54. 54.
    Chabre, Y.M., Roy, R.: The chemists way to prepare multivalency. In: Gabius, H.-J. (ed.) The sugar code - fundamentals of glycosciences, pp. 53–70. WILEY-VCH, Weinheim (2009)Google Scholar
  55. 55.
    Jefferis, R.: Recombinant antibody therapeutics: the impact of glycosylation on mechanisms of action. Trends Pharmacol Sci 30(7), 356–362 (2009)PubMedCrossRefGoogle Scholar
  56. 56.
    Crocker, P.R., Paulson, J.C., Varki, A.: Siglecs and their roles in the immune system. Nat Rev Immunol 7(4), 255–266 (2007)PubMedCrossRefGoogle Scholar
  57. 57.
    Li, H., d’Anjou, M.: Pharmacological significance of glycosylation in therapeutic proteins. Curr Opin Biotechnol 20(6), 678–684 (2009)PubMedCrossRefGoogle Scholar
  58. 58.
    Durocher, Y., Butler, M.: Expression systems for therapeutic glycoprotein production. Curr Opin Biotechnol 20(6), 700–707 (2009)PubMedCrossRefGoogle Scholar
  59. 59.
    Sorensen, A.L., Clausen, H., Wandall, H.H.: Carbohydrate clearance receptors in transfusion medicine. Biochim Biophys Acta 1820(11), 1797–1808 (2012)PubMedCrossRefGoogle Scholar
  60. 60.
    Robinson, M.J., Sancho, D., Slack, E.C., LeibundGut-Landmann, S., Reis e Sousa, C.: Myeloid C-type lectins in innate immunity. Nature Immunol 7(12), 1258–1265 (2006)CrossRefGoogle Scholar
  61. 61.
    Mahla, R.S., Reddy, M.C., Prasad, D.V., Kumar, H.: Sweeten PAMPs: role of sugar complexed pamps in innate immunity and vaccine biology. Frontiers Immunol 4, 248 (2013)CrossRefGoogle Scholar
  62. 62.
    Nayak, D.P., Hui, E.K., Barman, S.: Assembly and budding of influenza virus. Virus Res 106(2), 147–165 (2004)PubMedCrossRefGoogle Scholar
  63. 63.
    Olofsson, S., Bergstrom, T.: Glycoconjugate glycans as viral receptors. Annals Med 37(3), 154–172 (2005)CrossRefGoogle Scholar
  64. 64.
    Karlsson, N.G., Schulz, B.L., Packer, N.H.: Structural determination of neutral O-linked oligosaccharide alditols by negative ion LC-electrospray-MSn. J Am Soc Mass Spectrom 15(5), 659–672 (2004)PubMedCrossRefGoogle Scholar
  65. 65.
    Ceroni, A., Dell, A., Haslam, S.M.: The GlycanBuilder: a fast, intuitive and flexible software tool for building and displaying glycan structures. Source Code Biol Med 2, 3 (2007)PubMedCentralPubMedCrossRefGoogle Scholar
  66. 66.
    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 7(4), 1650–1659 (2008)PubMedCrossRefGoogle Scholar
  67. 67.
    Hayes, C.A., Karlsson, N.G., Struwe, W.B., Lisacek, F., Rudd, P.M., Packer, N.H., Campbell, M.P.: UniCarb-DB: a database resource for glycomic discovery. Bioinformatics 27(9), 1343–1344 (2011)PubMedCrossRefGoogle Scholar
  68. 68.
    Varki, A., Cummings, R.D., Esko, J.D., Freeze, H.H., Stanley, P., Marth, J.D., Bertozzi, C.R., Hart, G.W., Etzler, M.E.: Symbol nomenclature for glycan representation. Proteomics 9(24), 5398–5399 (2009)PubMedCentralPubMedCrossRefGoogle Scholar
  69. 69.
    Domon, B., Costello, C.E.: A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconj J 5(4), 397–409 (1988)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Stefan Gaunitz
    • 1
  • Jining Liu
    • 2
  • Anki Nilsson
    • 3
  • Niclas Karlsson
    • 4
  • Jan Holgersson
    • 2
  1. 1.Division of Clinical Immunology and Transfusion Medicine, Department of Laboratory Medicine, Karolinska University HospitalKarolinska InstituteHuddingeSweden
  2. 2.Department of Clinical Chemistry and Transfusion Medicine, Institute of Biomedicine, the Sahlgrenska AcademyUniversity of GothenburgGothenburgSweden
  3. 3.Recopharma ABGothenburgSweden
  4. 4.Department of Medical Biochemistry, Institute of Biomedicine, Sahlgrenska AcademyUniversity of GothenburgGothenburgSweden

Personalised recommendations