Abstract
Sialic acids are one of the most important molecules of life, since they occupy the terminal position on macromolecules and cell membranes and are involved in many biological and pathological phenomena. The structures of sialic acids, comprising a family of over 40 neuraminic acid derivatives, have been elucidated. However, many aspects of the regulation of their metabolism at the enzyme and gene levels, as well as of their functions remain mysterious. Sialic acids play a dual role, not only are they indispensable for the protection to and adaptation of life, but are also utilised by life-threatening infectious microorganisms. In this article the present state of knowledge in sialobiology, with an emphasis on my personal experience in this research area, is outlined including a discussion of necessary future work in this fascinating field of cell biology.
Article PDF
Similar content being viewed by others
References
Gottschalk A, (ed) The chemistry and biology of sialic acids and related substances, (University Press, Cambridge, 1960).
Blix G, Gottschalk A, Klenk E, Proposed nomenclature in the field of neuraminic and sialic acids, Nature 179, 1088 (1957).
Faillard H, Schauer R, Glycoproteins as lubricants, protective agents, carriers, structural proteins and as participants in other functions. In Glycoproteins, Their Composition, Structure and Function, edited by Gottschalk A, BBA Library 5, (Elsevier, Amsterdam, 1972), pp. 1246–67.
Klenk E, Neuraminsäure, das Spaltprodukt eines neuen Gehirn-lipoids, Hoppe-Seyler's Z Physiol Chem 268, 50–8 (1941).
Blix G, Ñber die Kohlenhydratgruppen des Submaxillarismucins, Hoppe-Seyler's Z Physiol Chem 240, 43–54 (1936).
Schauer R, Chemistry, metabolism and biological functions of sialic acids, Adv Carbohydr Chem Biochem 40, 131–234 (1982).
Schauer R (ed) Sialic Acids – Chemistry, Metabolism and Function, Cell Biology Monogr, Vol. 10 (Springer, Wien/New York, 1982).
Schauer R, Kamerling JP, Chemistry, biochemistry and biology of sialic acids. In Glycoproteins II, edited by Montreuil J, Vliegenthart JFG, Schachter H, (Elsevier, Amsterdam, 1997), pp. 243–402.
Varki A, Diversity in the sialic acids, Glycobiology 2, 25–40 (1992).
Schauer R, Faillard H, Zur Wirkungsspezifität der Neuraminidase, Hoppe-Seyler's Z Physiol Chem 349, 961–8 (1968).
Reuter G, Schauer R, Enzymic methods of sialic acid analysis. In Methods in Carbohydrate Chemistry edited by BeMiller JN, Manners DJ, Sturgeon RJ, Vol. 10 (Wiley, New York, 1994), pp. 29–39.
Kamerling JP, Vliegenthart JFG, Versluis C, Schauer R, Identification of O-acetylated N-acylneuraminic acids by mass spectrometry, Carbohydr Res 41, 7–17 (1975).
Kamerling JP, Vliegenthart JFG, Schauer R, Strecker G, Montreuil J, Isolation and identification of 2-deoxy-2,3-dehydro-N-acetylneuraminic acid from the urine of a patient with sialuria, Eur J Biochem 56, 253–8 (1975).
Zanetta J-P, Timmermann P, Leroy Y, Gas-liquid chromatography of the heptafluorobutyrate derivatives of the O-methylglycosides on capillary columns: a method for the quantitative determination of the monosaccharide composition of glycoproteins and glycolipids, Glycobiology 9, 255–66 (1999).
Hara, S, Yamaguchi M, Takemori Y, Furuhata K, Ogura H, Nakamura M, Determination of mono-O-acetylated N-acetyl-neuraminic acids in rat sera by fluorometric high-performance liquid chromatography, Anal Biochem 179, 162–6 (1989).
Shukla AK, Schauer R, Separation of sialic acids by HPLC, Fresenius Z Anal Chem 311, 376 (1982).
Smith H, Questions about the behaviour of bacterial pathogens in vivo, Phil Trans R Soc Lond B 355, 551–64 (2000).
Krauß JH, Reuter G, Schauer R, Weckesser J, Mayer H, Sialic acid-containing lipopolysaccharides of purple nonsulfur bacteria, Arch Microbiol 150, 584–9 (1988).
Schauer R, Reuter G, Mühlpfordt H, Andrade AFB, Pereira MEA, The occurrence of N-acetyl-and N-glycolylneuraminic acid in Trypanosoma cruzi, Hoppe-Seyler's Z Physiol Chem 364, 1053–7 (1983).
Roth J, Kemp A, Reuter G, Schauer R, Gehring WJ, Occurrence of sialic acids in Drasophila melanogaster, Science 256, 673–5 (1992).
Malykh YN, Krisch B, Gerardy-Schahn R, Lapina EB, Shaw L, Schauer R, The presence of N-acetylneuraminic acid in Malpighian tubules of larvae of the cicada Philaenus spumarius, Glycoconjugate J 16, 731–9 (1999).
Karaçali S, Kirmizigül S, Deveci R, Deveci Ö, Onat T, Gürcü B, Presence of sialic acid in prothoracic glands of Galleria mellonella (Lepidoptera), Tissue & Cell 29, 315–21 (1997).
Marchal I, Jarvis DL, Cacan R, Verbert A, Glycoproteins from insect cells: sialylated or not? Biol Chem 382, 151–9 (2001).
Gowda DC, Reuter G, Schauer R, Structural features of an acidic polysaccharide from the mucin of Drosera binata, Phytochemistry 21, 2297–300 (1982).
Muralikrishna G, Reuter G, Peter-Katalinie J, Egge H, Hanisch F-G, Siebert H-C, Schauer R, Identification of a new ganglioside from the starfish Asterias rubens, Carhohydr Res 236, 321–6 (1992).
Bergwerff AA, Hulleman SD, Kamerling JP, Vliegenthart JFG, Shaw L, Reuter G, Schauer R, Nature and biosynthesis of sialic acids in the starfish Asterias rubens, Biochimie 74, 25–38 (1992).
Kitazume S, Kitajima K, Inoue S, Troy FA, Cho J-W, Lennarz WJ, Inoue Y, Identification of polysialic acid-containing glycoprotein in the jelly coat of sea urchin eggs. Occurrence of a novel type of polysialic acid structure, J Biol Chem 269, 22712–8 (1994).
Kelm S, Schauer R, Sialic acids in molecular and cellular interactions, In Int Rev Cytology, edited by Jeon KW, Jarvik JW, Vol. 175 (Academic Press, San Diego, 1997), pp. 137–40.
Schauer R, Malykh YN, Krisch B, Gollub M, Shaw L, Biosynthesis and biology of N-glycolylneuraminic acid. In Sialobiology and Other Novel Forms of Glycosylation, edited by Inoue Y, Lee YC, Troy FA II, (Gakushin Publishing Co., Osaka, 1999), pp. 17–27.
Malykh YN, Krisch B, Shaw L, Warner TG, Sinicropi D, Smith R, Chang J, Schauer R, Distribution and localization of CMP-N-acetylneuraminic acid hydroxylase and N-glycolylneuraminic acid-containing glycoconjugates in porcine lymph node and peripheral blood lymphocytes, Eur J Cell Biol 80, 48–58 (2001).
Schauer R, Schoop HJ, Faillard H, Zur Biosynthese der Glykolyl-Gruppe der N-Glykolylneuraminsäure, Hoppe-Seyler's Z Physiol Chem 349, 645–52 (1968).
Shaw L, Schauer R, The biosynthesis of N-glycoloylneuraminic acid occurs by hydroxylation of the CMP-glycoside of N-acetylneuraminic acid, Biol Chem Hoppe-Seyler 369, 477–86 (1988).
Gollub M, Schauer R, Shaw L, Cytidine monophosphate-N-acetylneuraminate hydroxylase in the starfish Asterias rubens and other echinoderms, Comp Biochem Physiol Part B 120, 605–15 (1998).
Lepers A, Shaw L, Schneckenburger P, Cacan R, Verbert A, Schauer R, A study on the regulation of N-glycoloylneuraminic acid biosynthesis and utilization in rat and mouse liver, Eur J Biochem 193, 715–23 (1990).
Chou H-H, Takematsu H, Diaz S, Iber J, Nickerson E, Wright KL, Muchmore EA, Nelson DL, Warren ST, Varki A, A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence, Proc Natl Acad Sci USA 95, 11751–6 (1998).
Irie A, Koyama S, Kozutsumi Y, Kawasaki T, Suzuki A, The molecular basis for the absence of N-glycolylneuraminic acid in humans, J Biol Chem 273, 15866–71 (1998).
Schlenzka W, Shaw L, Kelm S, Schmidt CL, Bill E, Trautwein AX, Lottspeich F, Schauer R, CMP-N-acetylneuraminic acid hydroxylase: the first cytosolic Rieske iron-sulphur protein to be described in Eucarya, FEBS Lett 385, 197–200 (1996).
Nöhle U, Beau J-M, Schauer R, Uptake, metabolism and excretion of orally and intravenously administered, double-labeled N-glycoloylneuraminic acid and single-labeled 2-deoxy-2,3-dehydro-N-acetylneuraminic acid in mousse and rat, Eur J Biochem 126, 543–8 (1982).
Nöhle U, Schauer R, Metabolism of sialic acids from exogeneously administered sialyllactose and mucin in mouse and rat, Hoppe-Seyler's Z Physiol Chem 365, 1457–67 (1984).
Tangvoranuntakul P, Gagneux P, Diaz S, Varki N, Muchmore E, Varki A, Expression of N-glycolyl-neuraminic acid in normal, fetal and malignant human tissues, Glycobiology 10, abstract 53, in press (2000).
Schauer R, Schmid H, Pommerencke J, Iwersen M, Kohla G, Metabolism and role of O-acetylated sialic acids. In Molecular Immunology of Complex Carbohydrates 2, edited by Wu AM, (Plenum, New York, 2001) pp. 325–42.
Schauer R, Biosynthese von N-Acetyl-O-Acetylneuraminsäuren I, Hoppe-Seyler's Z Physiol Chem 351, 595–602 (1970).
Iwersen M, Vandamme-Feldhaus V, Schauer R, Enzymatic 4-Oacetylation of N-acetylneuraminic acid in guinea-pig liver, Glycoconjugate J 15, 895–904 (1998).
Butor C, Diaz S, Varki A, High level O-acetylation of sialic acids on N-linked oligosaccharides of rat liver membranes, J Biol Chem 268, 10197–206 (1993).
Vandamme-Feldhaus V, Schauer R, Characterization of the enzymatic 7-O-acetylation of sialic acids and evidence for enzymatic O-acetyl migration from C-7 to C-9 in bovine submandibular glands, J Biochem (Tokyo) 124, 111–21 (1998).
Kamerling JP, Schauer R, Shukla AK, Stoll S, van Halbeek H, Vliegenthart JFG, Migration of O-acetyl groups in N,O-acetylneuraminic acids, Eur J Biochem 162, 601–7 (1987).
Shi WX, Chammas R, Varki A, Induction of sialic acid 9-O-acetylation by diverse gene products: implications for the expression cloning of sialic acid O-acetyltransferases, Glycobiology 8, 199–205 (1998).
Kelm A, Shaw L, Schauer R, Reuter G, The biosynthesis of 8-O-methylated sialic acids in the starfish Asterias rubens, Eur J Biochem 251, 874–84 (1998).
Kochetkov NK, Smirnova GP, Chekareva NV, Isolation and structural studies of a sulfated sialosphingolipid from the sea urchin Echinocardium cordatum, Biochim Biophys Acta 424, 274–83 (1976).
Schauer R, Biochemistry of sialic acid diversity. In Carbohydrates in Chemistry and Biology, edited by Ernst B, Hart GW, Sinaÿ P, Vol. 3 (Wiley-VCH, Weinheim, 2000), pp. 227–43.
Schmelter T, Ivanov S, Wember M, Stangier P, Thiem J, Schauer R, Partial purification and characterization of cytidine-5'-monophosphosialate synthase from rainbow trout liver, Biol Chem Hoppe-Seyler 374, 337–42 (1993).
Kleineidam RG, Hofmann O, Reuter G, Schauer R, Indications for the enzymic synthesis of 9-O-lactoyl-N-acetylneuraminic acid in equine liver, Glycoconjugate J 10, 116–9 (1993).
Chammas R, Sonnenburg JL, Watson NE, Tai T, Farquhar MG, Varki NM, Varki A, De-N-acetyl-gangliosides in humans: unusual subcellular distribution of a novel tumor antigen, Cancer Res 59, 1337–46 (1999).
Nakamura T, Urashima T, Nakagawa M, Saito T, Sialyllactose occurs as free lactones in ovine colostrum, Biochim Biophys Acta 1381, 286–92 (1998).
Traving C, Schauer R, Structure, function and metabolism of sialic acids, Cell Mol Life Sci 54, 1330–49 (1998).
Roggentin P, Rothe B, Kaper JB, Galen L, Lawrisuk L, Vimr ER, Schauer R, Conserved sequences in bacterial and viral sialidases, Glycoconjugate J 6, 349–53 (1989).
Roggentin P, Schauer R, Hoyer LL, Vimr ER, The sialidase superfamily and its spread by horizontal gene transfer, Mol Microbiol 9, 915–21 (1993).
Corfield T, Bacterial sialidases–roles in pathogenicity and nutrition, Glycobiology 6, 509–21 (1992).
Roggentin T, Kleineidam RG, Majewski DM, Tirpitz D, Roggentin P, Schauer R, An immunoassay for the rapid and specific detection of three sialidase-producing Clostridia causing gas gangrene, J Immunol Methods 157, 125–33 (1993).
Kleineidam RG, Furuhata K, Ogura H, Schauer R, 4-Methylumbelliferyl-α-glycosides of partially O-acetylated N-acetylneuraminic acids as substrates of bacterial and viral sialidases, Biol Chem Hoppe-Seyler 371, 715–9 (1990).
von Itzstein M, Thomson RJ, The synthesis of noval sialic acids as biological probes. In Topics in Current Chemistry, edited by Driguez H, Thiem J, Vol. 186 (Springer, Berlin, Heidelberg, 1997) pp. 119–70.
Schenkman S, Jiang MS, Hart GW, Nussenzweig V, A novel cell surface transsialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells, Cells 65, 1117–25 (1991).
Previato JO, Andrade AF, Pessolani MC, Mendonca-Previato L, Incorporation of sialic acid into Trypanasoma cruzi macromolecules, Mol Biochem Parasitol 16, 85–96 (1985).
Engstler M, Reuter G, Schauer R, Purification and characterization of a novel sialidase in procyclic culture forms of Trypanosoma brucei, Mol Biochem Parasitol 54, 21–30 (1992).
Buschiazzo A, Tavares GA, Campetella O, Spinelli S, Cremona ML, Pari<q>s G, Fernanda Amaya M, Frasch ACC, Alzari PM, Structural basis of sialyltransferase activity in trypanosomal sialidases, The Embo J 19, 16–24 (2000).
Reuter G, Schauer R, Prioli R, Pereira MEA, Isolation and properties of a sialidase from Trypanosoma rangeli, Glycoconjugate J 4, 339–48 (1987).
Smith LE, Eichinger D, Directed mutagenesis of the Trypanosoma cruzi trans-sialidase enzyme identifies two domains involved in its sialyltransferase activity, Glycobiology 7, 445–51 (1997).
Engstler M, Schauer R, Brun R, Distribution and developmentally regulated trans-sialidases in the Kinetoplastida and characterization of a shed trans-sialidase activity from procyclic Trypanosoma congolense, Acta Tropica 59, 117–29 (1995).
Pereira-Chioccola VL, Schenkman S, Biological role of Trypanosoma cruzi trans-sialidase, Biochem Soc Trans 27, 516–8 (1999).
Carrillo MB, Gao W, Herrera M, Alroy J, Moore JB, Beverley SM, Pereira MA, Heterologous expression of Trypanosoma cruzi trans-sialidase in Leishmania major enhances virulence, Infect Immun 68, 2728–34 (2000).
Tertov VV, Kaplun VV, Sobenin IA, Orekhov AN, Low-density Lipoprotein modification occurring in human plasma. Possible mechanism of in vivo lipoprotein desialylation as a primary step of atherogenic modification, Atherosclerosis 138, 183–95 (1998).
Chou M-Y, Li S-C, Li Y-T, Cloning and expression of sialidase L, a NeuAc?2-3Gal-specific sialidase from the leech, Macrobdella decora, J Biol Chem 271, 19219–24 (1996).
Hasegawa T, Yamaguchi K, Wada T, Takeda A, Itoyama Y, Miyagi T, Molecular cloning of mouse ganglioside sialidase and its increased expression in Neuro2a cell differentiation, J Biol Chem 275, 8007–15 (2000).
Kleineidam RG, Kruse S, Roggentin P, Schauer R, Elucidation of the role of functional amino acid residues of the 'small’ sialidase from Clostridium perfringens by site-directed mutagenesis, Biol Chem 382, 313–9 (2001).
Schauer R, Sommer U, Kruger D, van Unen H, Traving C, The terminal enzymes of sialic acid metabolism: Acylneuraminate pyruvate-lyases, Bioscience Reports 19, 373–83 (1999).
Izard T, Lawrence MC, Malby RL, Lilley GG, Colman PM, The three-dimensional structure of N-acetylneuraminate lyase from Escherichia coli, Structure 2, 361–9 (1994).
Sander M, Veh RW, Schauer R, (1979) Partial purification and further characterization of glycoprotein-specific neuraminidase from horse liver. In Glycoconjugates, Proc Fifth Int Symp Glycoconjugates, edited by Schauer R, Boer P, Buddecke E, Kramer MF, Vliegenthart JFG, Wiegandt H, (Georg Thieme Publ, Stuttgart, 1979), pp. 44–5.
Schauer R, Reuter G, Stoll S, Sialate-O-acetylesterases: key enzymes in sialic acid catabolism, Biochimie 70, 1511–9 (1988).
Herrler U, Rott R, Klenk H-D, Müller H-P, Shukla AK, Schauer R, The receptor destroying enzyme of influenza C virus is neuraminate-O-acetylesterase, EMBO J 4, 1503–6 (1985).
Rosenthal PB, Zhang X, Formanowski F, Fitz W, Wong C-H, Meier-Ewert H, Skehel JJ, Wiley DC, Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus, Nature 396, 92–6 (1998).
Hubl U, Ishida H, Kiso M, Hasegawa A, Schauer R, Studies on the specificity and sensitivity of the influenza C virus binding assay for O-acetylated sialic acids and its application to human melanomas, J Biochem 27, 1021–31 (2000).
Fahr C, Schauer R, Detection of sialic acids and gangliosides with special reference to 9-O-acetylated species in basaliomas and normal human skin, J Invest Dermatol 116, 254–60 (2001).
Regl G, Kaser A, Iwersen M, Schmid H, Kohla G, Strobl B, Vilas U, Schauer R, Vlasak R, The hemagglutinin-esterase of mouse hepatitis virus strain S is a sialate-4-O-acetylesterase, J Virol 73, 4721–7 (1999).
Mitsuoka C, Ohmori K, Kimura N, Kanamori A, Komba S, Ishida H, Kiso M, Kannagi R, Regulation of selectin binding activity by cyclization of sialic acid moiety of carbohydrate ligands on human leukocytes, Proc Natl Acad Sci USA 96, 1597–602 (1999).
Schauer R, Sialic acids and their roles as biological masks, Trends Biochem Sci 10, 357–60 (1985).
Siebert H-C, von der Lieth C-W, Dong X, Reuter G, Schauer R, Gabius H-J, Vliegenthart JFG, Molecular dynamics-derived conformation and intramolecular interaction analysis of the N-acetyl-9-O-acetylneuraminic acid-containing GDIa and NMR-based analysis of its binding to a human polyclonal immunoglobulin G fraction with selectivity for O-acetylated sialic acids, Glycobiology 6, 561–72 (1996).
Ashwell G, Morell AG, The role of surface carbohydrates in the hepatic recognition and transport circulating glycoproteins, Adv Enzymol 41, 99–128 (1974).
Jancik J, Schauer R, Sialic acid – a determinant of the life-time of rabbit erythrocytes, Hoppe-Seyler's Z Physiol Chem 355, 395–400 (1974).
Müller E, Schröder C, Sharon N, Schauer R, Binding and phagocytosis of sialidase-treated rat erythrocytes by a mechanism independent of opsonins, Hoppe-Seyler's Z Physiol Chem 364, 1410–20 (1983).
Bratosin D, Mazurier J, Tissier JP, Estaquier J, Huart JJ, Ameisen JC, Aminoff D, Montreuil J, Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages, Biochimie 80, 173–95 (1998).
Fischer C, Kelm S, Ruch B, Schauer R, Reversible binding of sialidase-treated rat lymphocytes by homologous peritoneal macrophages, Carbohydr Res 213, 263–73 (1991).
Varki A, Sialic acids as ligands in recognition phenomena, The FASEB J 11, 248–55 (1997).
Lee H, Kelm S, Michalski J-C, Schauer R, Influence of sialic acids on the galactose-recognizing receptor of rat peritoneal macrophages, Biol Chem Hoppe-Seyler 371, 307–16 (1990).
Crocker PR, Kelm S, Dubois C, Martin B, McWilliam AS, Shotton DM, Paulson JC, Gordon S, Purification and properties of sialoadhesin, a sialic acid-binding receptor of murine tissue macrophages, EMBO J 10, 1661–9 (1991).
Crocker PR, Clark EA, Filbin M, Gordon S, Jones Y, Kehrl JH, Kelm S, Le Douarin N, Powell L, Roder J, Schnaar RL, Sgroi DC, Stamenkovic I, Schauer R, Schachner M, van den Berg TK, van der Merwe PA, Watt SM, Varki A, Siglecs: a family of sialic-acid binding lectins, Glycobiology 8, V–VI (1998).
Kelm S, Brossmer R, Isecke R, Groß H-J, Strenge K, Schauer R, Functional groups of sialic acids involved in binding to siglecs (sialoadhesins) deduced from interactions with synthetic analogues, Eur J Biochem 255, 663–72 (1998).
Brinkman-Van der Linden ECM, Sjoberg ER, Juneja LR, Crocker PR, Varki N, Varki A, Loss of N-glycolylneuraminic acid in human evolution, J Biol Chem 275, 8633–40 (2000).
Kelm S, Pelz A, Schauer R, Filbin MT, Tang S, de Bellard M-E, Schnaar RL, Mahoney JA, Hartnell A, Bradfield P, Crocker PR, Sialoadhesin, myelin-associated glycoprotein and CD22 define a new family of sialic acid-dependent adhesion molecules of the immunoglobulin superfamily, Curr Biol 4, 965–72 (1994).
Mann B, Klussmann E, Vandamme-Feldhaus V, Iwersen M, Hanski M-L, Riecken E-O, Buhr HJ, Schauer R, Kim YS, Hanski C, Low O-acetylation of sialyl-Lex contributes to its overexpression in colon carcinoma metastases, Int J Cancer 72, 258–64 (1997).
Hirmo S, Kelm S, Iwersen M, Hotta K, Goso Y, Ishihara K, Suguri T, Morita M, Wadström T, Schauer R, Inhibition of Helicobacter pylori sialic acid-specific haemagglutination by human gastrointestinal mucins and milk glycoproteins, FEMS Immunol Med Microbiol 20, 275–81 (1998).
Castillo C, Diaz ME, Balbi D, Thornhill WB, Recio-Pinto E, Changes in sodium channel function during postnatal brain development reflect increases in the level of channel sialidation, Developmental Brain Res 104, 119–30 (1997).
Brückner K, Perez L, Clausen H, Cohen S, Glycosyltransferase activity of Fringe modulates Notch-Delta interactions, Nature 406, 411–5 (2000).
Schauer R, Stoll S, Reuter G, Differences in the amount of N-acetyl-and N-glycoloyl-neuraminic acids, as well as O-acetylated sialic acids, of fetal and adult bovine tissues, Carbohydr Res 213, 353–9 (1991).
Muchmore EA, Developmental sialic acid modifications in rat organs, Glycobiology 4, 337–43 (1992).
Herrler G, Reuter G, Rott R, Klenk H-D, Schauer R, N-Acetyl-9-O-acetylneuraminic acid, the receptor determinant for influenza C virus, is a differentiation marker on chicken erythrocytes, Biol Chem Hoppe-Seyler 368, 451–4 (1987).
Matthijs G, Carbohydrate-deficient glycoprotein syndromes become congenital disorders of glycosylation: an updated nomenclature for CDG, Glycocojugate J 16, 669–71 (1999).
Salhanick Al, Amatruda JM, Role of sialic acid in insulin action and the insulin resistance of diabetes mellitus, Am J Physiol 255, E173–9 (1988).
Sillanaukee P, Pönniö M, Seppä K, Sialic acid: new potential marker of alcohol abuse, Alcohol Clin Exp Res 23, 1039–43 (1999).
Ghosh P, Ender I, Hale EA, Long-term ethanol consumption selectively impairs ganglioside pathway in rat brain, Alcohol Clin Exp Res 22, 1220–6 (1998).
Zuegg J, Gready JE, Molecular dynamics simulation of human prion protein including both N-linked oligosaccharides and the GPI anchor, Glycobiology 10, 959–74 (2000).
Horstkorte R, Nöhring S, Wiechens N, Schwarzkopf M, Danker K, Reutter W, Lucka L, Tissue expression and amino acid sequence of murine UDP-N-acetylglucosamine-2-epimerase/N-acetylmannosamine kinase, Eur J Biochem 260, 923–7 (1999).
Brand Miller J, McVeagh P, Human milk oligosaccharides: 130 reasons to breast-feed, British J Nutrition 82, 333–5 (1999).
Engfer MB, Stahl B, Finke B, Sawatzki G, Daniel H, Human milk oligosaccharides are resistant to enzymatic hydrolysis in the upper gastrointestinal tract, Am J Clin Nutr 71, 1589–96 (2000).
Kikuchi K, Kikuchi H, Tsuiki S, Activities of sialic acidsynthesizing enzymes in rat liver and rat and mouse tumors, Biochim Biophys Acta 252, 357–68 (1971).
Georgopoulou N, Breen KC, Overexpression of ?2,3 sialyltransferase in neuroblastoma cells results in an upset in the glycosylation process, Glycoconjugate J 16, 649–57 (1999).
Krause T, Turner GA, Are selectins involved in metastasis? Clin Exp Metastasis 17, 183–92 (1999).
Kleineidam RG, Schmelter T, Schwarz RT, Schauer R, Studies on the inhibition of sialyl-and galactosyltransferases, Glycoconjugate J 14, 57–66 (1997).
Dufner G, SchwoÈrer R, Müller B, Schmidt RR, Base-and sugar-modified cytidine monophosphate-N-acetylneuraminic acid (CMP-Neu5Ac) analogues–synthesis and studies with ?(2–6)-sialyltransferase from rat liver, Eur J Org Chem 1467–82 (2000).
Rudd PM, Wormald MR, Dwek RA, Glycosylation and the immune system, Trends Glycosci Glycotechnol 11, 1–21 (1999).
Tanemura M, Miyagawa S, Koyota S, Koma M, Matsuda H, Tsuji S, Shirakura R, Taniguchi N, Reduction of the major swine xenoantigen, the ?-galactosyl epitope by transfection of the ?2,3-sialyltransferase gene, J Biol Chem 273, 16421–5 (1998).
Mühlenhoff M, Eckhardt M, Gerardy-Schahn R, Polysialic acid: three-dimensional structure, biosynthesis and function, Current Opinion Struct Biol 8, 558–64 (1998).
Angata K, Suzuki M, McAuliffe J, Ding Y, Hindsgaul O, Fukuda M, 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 ST8SiaIII, J Biol Chem 275, 18594–601 (2000).
Aoki K, Nakahara Y, Yarnada S, Eto K, Role of polysialic acid on outgrowth of rat olfactory receptor neurons, Mechan Develop 85, 103–10 (1999).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Schauer, R. Achievements and challenges of sialic acid research. Glycoconj J 17, 485–499 (2000). https://doi.org/10.1023/A:1011062223612
Issue Date:
DOI: https://doi.org/10.1023/A:1011062223612