Identification of Transient Glycosylation Alterations of Sialylated Mucin Oligosaccharides During Infection by the Rat Intestinal Parasite Nippostrongylus Brasiliensis

Overview

Journal Biochem J

Specialty Biochemistry

Date 2000 Sep 6

PMID 10970796

Citations 22

Authors

N G Karlsson

F J Olson

P A Jovall

Y Andersch

L Enerback

G C Hansson

Affiliations

Soon will be listed here.

Abstract

The sialylation of the oligosaccharides from small-intestinal mucins during a 13-day infectious cycle was studied in Sprague-Dawley rats with the parasite Nippostrongylus brasiliensis. Sialic acid analysis and release, permethylation and analysis by GC-MS of the sialylated oligosaccharides isolated from the 'insoluble' mucin complex revealed a relative decrease (4-7-fold) of N-glycolylneuraminic acid compared with N-acetylneuraminic acid just before parasite expulsion. Northern blots showed that this effect was due to the decreased expression of a hydroxylase converting CMP-N-acetylneuraminic acid into CMP-N-glycolylneuraminic acid. Analysis of other rat strains showed that this parasite infection also caused the same effect in these animals. Detailed analysis of infected Sprague-Dawley rats revealed four sialylated oligosaccharides not found in the uninfected animals. These new oligosaccharides were characterized in detail and all shown to contain the trisaccharide epitope NeuAc/NeuGcalpha2-3(GalNAcbeta1-4)Galbeta1 (where NeuGc is N-glycolyl neuraminic acid). This epitope is similar to the Sd(a)- and Cad-type blood-group antigens and suggests that the infection causes the induction of a GalNAcbeta1-4 glycosyltransferase. This model for an intestinal infection suggests that the glycosylation of intestinal mucins is a dynamic process being modulated by the expression of specific enzymes during an infection process.

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References

Stellner K, Saito H, HAKOMORI S . Determination of aminosugar linkages in glycolipids by methylation. Aminosugar linkages of ceramide pentasaccharides of rabbit erythrocytes and of Forssman antigen. Arch Biochem Biophys. 1973; 155(2):464-72. DOI: 10.1016/0003-9861(73)90138-0. View

Hounsell E, Davies M, Renouf D . O-linked protein glycosylation structure and function. Glycoconj J. 1996; 13(1):19-26. DOI: 10.1007/BF01049675. View

Blanchard D, Cartron J, Fournet B, Montreuil J, van Halbeek H, Vliegenthart J . Primary structure of the oligosaccharide determinant of blood group Cad specificity. J Biol Chem. 1983; 258(12):7691-5. View

Takeya A, Hosomi O, Kogure T . Identification and characterization of UDP-GalNAc: NeuAc alpha 2-3Gal beta 1-4Glc(NAc) beta 1-4(GalNAc to Gal)N-acetylgalactosaminyltransferase in human blood plasma. J Biochem. 1987; 101(1):251-9. DOI: 10.1093/oxfordjournals.jbchem.a121898. View

Hansson G . Structural aspects of blood group glycosphingolipids in the gastrointestinal tract. Adv Exp Med Biol. 1988; 228:465-94. DOI: 10.1007/978-1-4613-1663-3_17. View

SERAFINI-CESSI F, Malagolini N, DallOlio F . Characterization and partial purification of beta-N-acetylgalactosaminyltransferase from urine of Sd(a+) individuals. Arch Biochem Biophys. 1988; 266(2):573-82. DOI: 10.1016/0003-9861(88)90290-1. View

Karlsson K . Animal glycosphingolipids as membrane attachment sites for bacteria. Annu Rev Biochem. 1989; 58:309-50. DOI: 10.1146/annurev.bi.58.070189.001521. View

Thornton D, Holmes D, Sheehan J, Carlstedt I . Quantitation of mucus glycoproteins blotted onto nitrocellulose membranes. Anal Biochem. 1989; 182(1):160-4. DOI: 10.1016/0003-2697(89)90735-5. View

Gendler S, Lancaster C, Taylor-Papadimitriou J, Duhig T, Peat N, Burchell J . Molecular cloning and expression of human tumor-associated polymorphic epithelial mucin. J Biol Chem. 1990; 265(25):15286-93. View

10.

Baeckstrom D, Hansson G, Nilsson O, Johansson C, Gendler S, Lindholm L . Purification and characterization of a membrane-bound and a secreted mucin-type glycoprotein carrying the carcinoma-associated sialyl-Lea epitope on distinct core proteins. J Biol Chem. 1991; 266(32):21537-47. View

11.

Strecker G, Wieruszeski J, Cuvillier O, Michalski J, Montreuil J . 1H and 13C-NMR assignments for sialylated oligosaccharide-alditols related to mucins. Study of thirteen components from hen ovomucin and swallow nest mucin. Biochimie. 1992; 74(1):39-51. DOI: 10.1016/0300-9084(92)90182-e. View

12.

Nagata Y, Yamashiro S, Yodoi J, LLOYD K, Shiku H, Furukawa K . Expression cloning of beta 1,4 N-acetylgalactosaminyltransferase cDNAs that determine the expression of GM2 and GD2 gangliosides. J Biol Chem. 1992; 267(17):12082-9. View

13.

Ishikawa N, Horii Y, Nawa Y . Immune-mediated alteration of the terminal sugars of goblet cell mucins in the small intestine of Nippostrongylus brasiliensis-infected rats. Immunology. 1993; 78(2):303-7. PMC: 1421791. View

14.

Carlstedt I, Herrmann A, Karlsson H, Sheehan J, Fransson L, Hansson G . Characterization of two different glycosylated domains from the insoluble mucin complex of rat small intestine. J Biol Chem. 1993; 268(25):18771-81. View

15.

Gum Jr J, Hicks J, Toribara N, Siddiki B, Kim Y . Molecular cloning of human intestinal mucin (MUC2) cDNA. Identification of the amino terminus and overall sequence similarity to prepro-von Willebrand factor. J Biol Chem. 1994; 269(4):2440-6. View

16.

SERAFINI-CESSI F, Malagolini N, Guerrini S, Turrini I . A soluble form of Sda-beta 1,4-N-acetylgalactosaminyltransferase is released by differentiated human colon carcinoma CaCo-2 cells. Glycoconj J. 1995; 12(6):773-9. DOI: 10.1007/BF00731238. View

17.

Bry L, Falk P, Midtvedt T, Gordon J . A model of host-microbial interactions in an open mammalian ecosystem. Science. 1996; 273(5280):1380-3. DOI: 10.1126/science.273.5280.1380. View

18.

Kim Y, Gum Jr J, Brockhausen I . Mucin glycoproteins in neoplasia. Glycoconj J. 1996; 13(5):693-707. DOI: 10.1007/BF00702333. View

19.

Karlsson N, Johansson M, Asker N, Karlsson H, Gendler S, Carlstedt I . Molecular characterization of the large heavily glycosylated domain glycopeptide from the rat small intestinal Muc2 mucin. Glycoconj J. 1996; 13(5):823-31. DOI: 10.1007/BF00702346. View

20.

Karlsson N, Herrmann A, Karlsson H, Johansson M, Carlstedt I, Hansson G . The glycosylation of rat intestinal Muc2 mucin varies between rat strains and the small and large intestine. A study of O-linked oligosaccharides by a mass spectrometric approach. J Biol Chem. 1997; 272(43):27025-34. DOI: 10.1074/jbc.272.43.27025. View