Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-23T03:59:34.358Z Has data issue: false hasContentIssue false
  • English
  • Français

Initiation of chemical studies on the immunoreactive glycolipids of adult Ascaris suum

Published online by Cambridge University Press:  06 April 2009

R. D. Dennis ,
S. Baumeister ,
C. Smuda ,
C. Lochnit ,
T. Waider  and
E. Geyer
R. D. Dennis
Affiliation:
Allgemeine und Medizinische Parasitologie, FB Biologic, Philipps-Universität Marburg, Karl-von-Frisch-Straβe, D-35033 Marburg, Germany
S. Baumeister
Affiliation:
Allgemeine und Medizinische Parasitologie, FB Biologic, Philipps-Universität Marburg, Karl-von-Frisch-Straβe, D-35033 Marburg, Germany
C. Smuda
Affiliation:
Allgemeine und Medizinische Parasitologie, FB Biologic, Philipps-Universität Marburg, Karl-von-Frisch-Straβe, D-35033 Marburg, Germany
C. Lochnit
Affiliation:
Biochemisches Institut am Klinikum der Universität Gieβen, Friedrichstraβe 24, D–35385 Gieβen, Germany
T. Waider
Affiliation:
Allgemeine und Medizinische Parasitologie, FB Biologic, Philipps-Universität Marburg, Karl-von-Frisch-Straβe, D-35033 Marburg, Germany
E. Geyer
Affiliation:
Allgemeine und Medizinische Parasitologie, FB Biologic, Philipps-Universität Marburg, Karl-von-Frisch-Straβe, D-35033 Marburg, Germany
Get access Rights & Permissions [Opens in a new window]

Summary

There is a general lack of basic information concerning one class of glycoconjugate, the glycolipids, from parasitic nematodes. As the prototype, the neutral glycolipid fraction derived from adult males of Ascaris suum was investigated as to its chromatographic, differential chemical staining, antigenic and chemical properties. The thin-layer chromato-graphy-resolved neutral fraction glycolipids could be classified into components of fast and slow migrating band groups. Immunoreactivity was restricted to the latter as detected by IgG and IgM anti-neutral fraction glycolipid antibody levels in serial infection sera of mice. Similarities of chromatography, antigenicity and serological cross-reactivity have been extended to the neutral glycolipid fractions of other parasitic nematodes: Litomosoides carinii and Nippostrongylus brasiliensis. Chemical, differential chemical staining and enzymatic analyses identified the Ascaris suum antigenic, slow migrating band group of components as amphoteric glycosphingolipids, and not the originally hypothesized glyco-glycerolipids or glycosylphosphatidylinositols, that contained typical neutral monosaccharide constituents and a zwitter-ionic phosphodiester linkage, most probably phosphocholine. Glycosphingolipid-immunoreactivity is eliminated on cleavage of the zwitterionic phosphodiester linkage by hydrofluoric acid treatment.

Keywords

nematodeglycolipidsglycosphingolipidsantigenic behaviourchemical properties
Type
Research Article
Information
Parasitology , Volume 110 , Issue 5 , June 1995 , pp. 611 - 623
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Baumeister, S., Dennis, R. D., Klünder, R., Schares, G., Zahner, H. & Geyer, E. (1994). Litomosoides carinii: macrofilariae-derived glycolipids – chromatography, serology and potential in the evaluation of anthelminhic efficacy. Parasite Immunology 16, 629–41.CrossRefGoogle ScholarPubMed
Baumeister, S., Dennis, R. D., Kunz, J., Wiegandt, H. & Geyer, E. (1992). Comparative serological reactivity of Taenia crassiceps, Taenia solium and Taenia saginata metacestode neutral glycolipids to infection serum from Taenia crassiceps-infected mice. Molecular and Biochemical Parasitology 53, 53–62.CrossRefGoogle ScholarPubMed
Blaxter, M. L., Page, A. P., Rudin, W. & Maizels, R. M. (1992). Nematode surface coats: actively evading immunity. Parasitology Today 8, 243–7.CrossRefGoogle ScholarPubMed
Cuellar, C., Fenoy, S. & Guillen, J. L. (1992). Cross-reactions of sera from Toxocara cams-infected mice with Toxascaris leonina and Ascaris suum antigens. International Journal for Parasitology 22, 301–7.CrossRefGoogle ScholarPubMed
Dennis, R. D., Baumeister, S., Geyer, R., Peter-Katalinic, J., Hartmann, R., Egge, H., Geyer, E. & Wiegandt, H. (1992). Glycosphingolipids in cestodes. Chemical structures of ceramide monosaccharide, disaccharide, trisaccharide and tetrasaccharide from metacestodes of the fox tapeworm, Taenia crassiceps (Cestoda: Cyclophyllidea). European Journal of Biochemistry 207, 1053–62.CrossRefGoogle ScholarPubMed
Dennis, R. D., Geyer, R., Egge, H., Menges, H., Stirm, S. & Wiegandt, H. (1985 a). Glycosphingolipids in insects. Chemical structures of ceramide monosaccharide, disaccharide and trisaccharide from pupae of Calliphora vicina (Insecta: Diptera). European Journal of Biochemistry 146, 51–8.CrossRefGoogle ScholarPubMed
Dennis, R. D., Geyer, R., Egge, H., Peter-Katalinic, J., Li, S.-C., Stirm, S. & Wiegandt, H. (1985 b). Glycosphingolipids in insects. Chemical structures of ceramide tetra-, penta-, hexa-, and heptasaccharides from Calliphora vicina pupae (Insecta: Diptera). Journal of Biological Chemistry 260, 5370–5.CrossRefGoogle ScholarPubMed
Dennis, R. D. & Wiegandt, H. (1993). Glycosphingolipids of the Invertebrata as exemplified by a cestode platyhelminth, Taenia crassiceps, and a dipteran insect, Calliphora vicina. In Advances in Lipid Research, Vol. 26, Sphingolipids in Signaling, Part B (ed. Bell, R. M., Hannun, Y. A. & Merrill, A. H.), pp. 321–351. Orlando: Academic Press.Google Scholar
Ferguson, M. A. J. (1992 a). Glycosyl-phosphatidylinositol membrane anchors: the tale of a tail. Biochemical Society Transactions 20, 243–56.CrossRefGoogle ScholarPubMed
Ferguson, M. A. J. (1992 b). Chemical and enzymic analysis of glycosyl-phosphatidylinositol anchors. In Lipid Modification of Proteins. A Practical Approach (ed. Hooper, N. M. & Turner, A. J.), pp. 191–230. Oxford: IRL Press.CrossRefGoogle Scholar
Forsyth, K. P., Spark, R., Kazura, J., Brown, G. V., Peters, P., Heywood, P., Dissanayake, S. & Mitchell, G. F. (1985). A monoclonal antibody-based immunoradiometric assay for detection of circulating antigen in bancroftian filariasis. Journal of Immunology 134, 1172–7.CrossRefGoogle ScholarPubMed
Gerold, P., Dieckmann-Schuppert, A. & Schwarz, R. T. (1994). Glycosylphosphatidylinositols synthesized by asexual erythrocytic stages of the malarial parasite, Plasmodium falciparum. Candidates for plasmodial glycosylphosphatidylinositol membrane anchor precursors and pathogenicity factors. Journal of Biological Chemistry 269, 2597–606.CrossRefGoogle ScholarPubMed
Grelck, H., Hörchner, F. & Unterholzner, J. (1981). Zur serologischen Differenzierung von Ascaris suum-und Toxocara canis-infektionen beim Schwein. Zeitschrift für Parasitenkunde 65, 277–82.CrossRefGoogle Scholar
Hardy, M. R. (1989). Monosaccharide analysis of glycoconjugates by high-performance anion-exchange chromatography with pulsed amperometric detection. Methods in Enzymology 179, 76–82.CrossRefGoogle ScholarPubMed
Hardy, M. R., Townsend, R. R. & Lee, Y. C. (1988). Monosaccharide analysis of glycoconjugates by anion exchange chromatography with pulsed amperometric detection. Analytical Biochemistry 170, 54–62.CrossRefGoogle ScholarPubMed
Harnett, W., Houston, K. M., Amess, R. & Worms, M. J. (1993). Acanthocheilonema viteae; phosphorylcholine is attached to the major excretory–secretory product via an N-linked glycan. Experimental Parasitology 77, 498–502.CrossRefGoogle Scholar
Helling, F., Dennis, R. D., Weske, B., Nores, G., Peter-Katalinic, J., Dabrowski, U., Egge, H. & Wiegandt, H. (1991). Glycosphingolipids in insects. The amphoteric moiety, N-acetylglucosamine-linked phospho-ethanolamine, distinguishes a group of ceramide oligosaccharides from the pupae of Calliphora vicina (Insecta: Diptera). European Journal of Biochemistry 200, 409–21.CrossRefGoogle Scholar
Hori, T. & Sugita, M. (1993). Sphingolipids in lower animals. Progress in Lipid Research 32, 25–45.CrossRefGoogle ScholarPubMed
Ito, M. & Yamagata, T. (1989 a). Endoglycoceramidase from Rhodococcus species G-74–2. Methods in Enzymology 179, 488–96.CrossRefGoogle ScholarPubMed
Ito, M. & Yamagata, T. (1989 b). Purification and characterization of glycosphingolipid-specific endoglycosidases (endoglycoceramidases) from a mutant strain of Rhodococcus sp. Journal of Biological Chemistry 264, 9510–19.CrossRefGoogle ScholarPubMed
Jenkins, D. c. (1968). Observations on the early migration of larvae of Ascaris suum Goeze, 1782, in white mice. Parasitology 58, 431–40.CrossRefGoogle ScholarPubMed
Kang, S., Cummings, R. D. & McCall, J. W. (1993). Characterization of the N-linked oligosaccharides in glycoproteins synthesized by microfilariae of Dirofilaria immitis. Journal of Parasitology 79, 815–28.CrossRefGoogle ScholarPubMed
Khoo, K. H., Maizels, R. M., Page, A. P., Taylor, G. W., Rendell, N. B. & Dell, A. (1991). Characterization of nematode glycoproteins: the major O-glycans of Toxocara canis excretory-secretory antigens are O-methylated trisaccharides. Glycobiology 1, 163–71.CrossRefGoogle ScholarPubMed
Lal, R. B., Kumaraswami, V., Steel, C. & Nutman, T. B. (1990). Phosphocholine-containing antigens of Brugia malayi nonspecifically suppress lymphocyte function. American Journal of Tropical Medicine and Hygiene 42, 56–64.CrossRefGoogle ScholarPubMed
Levery, S. B., Weiss, J. B., Salyan, M. E., Roberts, C. E., Hakomori, S., Magnani, J. L. & Strand, M. (1992). Characterization of a series of novel fucose-containing glycosphingolipid immunogens from eggs of Schistosoma mansoni. Journal of Biological Chemistry 267, 5542–51.CrossRefGoogle ScholarPubMed
Maizels, R. M., Denham, D. A. & Sutanto, I. (1985). Secreted and circulating antigens of the filarial parasite Brugia malayi: analysis of in vitro released components and detection of parasite products in vivo. Molecular and Biochemical Parasitology 17, 277–88.CrossRefGoogle ScholarPubMed
Maizels, R. M., Kennedy, M. W., Meghji, M., Robertson, B. D. & Smith, H. v. (1987). Shared carbohydrate epitopes on distinct surface and secreted antigens of the parasitic nematode Toxocara canis. Journal of Immunology 139, 207–14.CrossRefGoogle ScholarPubMed
Mayor, S. & Menon, A. K. (1990). Structural analysis of the glycosylinositol phospholipid anchors of membrane proteins. Methods 1, 297–305.CrossRefGoogle Scholar
Mitchell, G. F., Hogarth-Scott, R. S., Edwards, R. D., Lewers, H. M., Cousins, G. & Moore, T. (1976). Studies on immune responses to parasite antigens in mice. I Ascaris suum larvae numbers and antiphosphorylcholine responses in infected mice of various strains and in hypothymic nu/nu mice. International Archives of Allergy and Applied Immunology 52, 64–78.CrossRefGoogle ScholarPubMed
Noda, N., Tanaka, R., Miyahara, K. & Kawasaki, T. (1992). Two novel galactosylceramides from Marphysa sanguinea. Tetrahedron Letters 33, 7527–30.CrossRefGoogle Scholar
Noda, N., Tanaka, R., Miyahara, K. & Kawasaki, T. (1993 a). Three glycosphingolipids having the phosphocholine group from the crude drug ‘jiryu’ (the earthworm, Pheretima asisatica). Chemical and Pharmaceutical Bulletin 41, 1733–7.CrossRefGoogle Scholar
Noda, N., Tanaka, R., Miyahara, K. & Kawasaki, T. (1993 b). Isolation and characterization of a novel type of glycosphingolipid from Neanthes diversicolor. Biochimica et Biophysica Acta 1169, 30–8.Google ScholarPubMed
Page, A. P., Hamilton, A. J. & Maizels, A. M. (1992). Toxocara cants: monoclonal antibodies to carbohydrate epitopes of secreted (TES) antigens localize to different secretion-related structures in infective larvae. Experimental Parasitology 75, 56–71.CrossRefGoogle Scholar
Page, A. P., Rudin, W., Fluri, E., Blaxter, M. L. & Maizels, R. M. (1992). Toxocara canis: a labile antigenic surface coat overlying the epicuticle of infective larvae. Experimental Parasitology 75, 72–86.CrossRefGoogle ScholarPubMed
Persat, F., Bouhours, J. F., Mojon, M. & Petavy, A. F. (1992). Glycosphingolipids with Galβ1–6Gal sequences in metacestodes of the parasite Echinococcus multilocularis. Journal of Biological Chemistry 267, 8764–9.CrossRefGoogle Scholar
Pery, P., Petit, A., Poulain, J. & Luffau, G. (1974). Phosphorylcholine-bearing components in homogenates of nematodes. European Journal of Immunology 4, 637–9.CrossRefGoogle ScholarPubMed
Politz, S. M. & Philipp, M. (1992). Caenorhabditis elegans as a model for parasitic nematodes: a focus on the cuticle. Parasitology Today 8, 6–12.CrossRefGoogle Scholar
Pritchard, D. I., Quinnell, R. J., Mckean, P. G., Walsh, L., Leggett, K. V., Slater, A. F. G., Raiko, A., Dale, D. D. s. & Keymer, A. E. (1991). Antigenic cross-reactivity between Necator americanus and Ascaris lumbricoides in a community in Papua New Guinea infected predominantly with hookworm. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 511–14.CrossRefGoogle Scholar
Saito, T. & Hakomori, S. (1971). Quantitative isolation of total glycosphingolipids from animal cells. Journal of Lipid Research 12, 257–9.CrossRefGoogle ScholarPubMed
Skipski, V. P. & Barclay, M. (1969). Thin-layer chromatography of lipids. Methods in Enzymology 14, 530–98.CrossRefGoogle Scholar
Stadler, J., Keenan, T., Bauer, G. & Gerisch, G. (1989). The contact site A glycoprotein of Dictyostelium discoideum carries a phospholipid anchor of a novel type. EMBO Journal 8, 371–7.CrossRefGoogle Scholar
Sugita, M., Fujii, H., Inagaki, F., Suzuki, M., Hayata, C. & Hori, T. (1992). Polar glycosphingolipids in Annelida. A novel series of glycosphingolipids containing choline phosphate from the earthworm, Pheretima hilgendorfi. Journal of Biological Chemistry 267, 22595–8.CrossRefGoogle Scholar
Turner, A. P., Brown, D., Heasman, J., Cook, G. M. W., Evans, J., Vickers, L. & Wylie, C. C. (1992). Involvement of a neutral glycolipid in differential cell adhesion in the Xenopus blastula. EMBO Journal 11, 3845–55.CrossRefGoogle ScholarPubMed
Williams, M. A. & McCluer, R. H. (1980). The Use of Sep-Pak™ C18 cartridges during the isolation of gangliosides. Journal of Neurochemistry 35, 266–9.CrossRefGoogle ScholarPubMed