Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-25T12:35:38.343Z Has data issue: false hasContentIssue false
  • English
  • Français

Mapping fucosylated epitopes on glycoproteins and glycolipids of Schistosoma mansoni cercariae, adult worms and eggs

Published online by Cambridge University Press:  13 December 2004

M. L. M. ROBIJN ,
M. WUHRER ,
D. KORNELIS ,
A. M. DEELDER ,
R. GEYER  and
C. H. HOKKE
M. L. M. ROBIJN
Affiliation:
Department of Parasitology, Centre of Infectious Diseases, Leiden University Medical Centre, P.O. Box 9600, 2300 RC Leiden, The Netherlands
M. WUHRER
Affiliation:
Department of Parasitology, Centre of Infectious Diseases, Leiden University Medical Centre, P.O. Box 9600, 2300 RC Leiden, The Netherlands Institute of Biochemistry, Faculty of Medicine, University of Giessen, Friedrichstrasse 24, D-35392 Giessen, Germany
D. KORNELIS
Affiliation:
Department of Parasitology, Centre of Infectious Diseases, Leiden University Medical Centre, P.O. Box 9600, 2300 RC Leiden, The Netherlands
A. M. DEELDER
Affiliation:
Department of Parasitology, Centre of Infectious Diseases, Leiden University Medical Centre, P.O. Box 9600, 2300 RC Leiden, The Netherlands
R. GEYER
Affiliation:
Institute of Biochemistry, Faculty of Medicine, University of Giessen, Friedrichstrasse 24, D-35392 Giessen, Germany
C. H. HOKKE
Affiliation:
Department of Parasitology, Centre of Infectious Diseases, Leiden University Medical Centre, P.O. Box 9600, 2300 RC Leiden, The Netherlands
Get access Rights & Permissions [Opens in a new window]

Abstract

The developmental expression of the antigenic fucosylated glycan motifs Fucα1-3GalNAcβ1-4GlcNAc (F-LDN), Fucα1-3GalNAcβ1-4(Fucα1-3)GlcNAc (F-LDN-F), GalNAcβ1-4(Fucα1-3)GlcNAc (LDN-F), Galβ1-4(Fucα1-3)GlcNAc (Lewis X), and GalNAcβ1-4(Fucα1-2Fucα1-3)GlcNAc (LDN-DF) in Schistosoma mansoni cercariae, adult worms and eggs, was surveyed using previously defined anti-carbohydrate monoclonal antibodies (mAbs). Lewis X was found both on glycolipids and glycoproteins, yet with completely different expression patterns during the life-cycle: on glycolipids, Lewis X was mainly found in the cercarial stage, while protein-conjugated Lewis X was mainly present in the egg stage. Also protein-conjugated LDN-F and LDN-DF were most highly expressed in the egg-stage. On glycolipids LDN-DF was found in all three examined stages, whereas LDN-F containing glycolipids were restricted to adult worms and eggs. The motifs F-LDN and F-LDN-F were found both on glycoproteins and glycolipids of the cercarial and egg stage, while in the adult stage, they appeared to occur predominantly on glycolipids. Immunofluorescence assays (IFA) showed that these F-LDN and F-LDN-F containing glycolipids were localized in a yet undefined duct or excretory system of adult worms. Murine infection serum showed major reactivity with this adult worm duct-system, which could be fully inhibited by pre-incubation with keyhole limpet haemocyanin (KLH). Clearly, the use of defined mAbs provides a quick and convenient way to map expression profiles of carbohydrate epitopes.

Keywords

Schistosoma mansoniglycoproteinsglycolipidscarbohydratesKLHdifferential expression
Type
Research Article
Information
Parasitology , Volume 130 , Issue 1 , January 2005 , pp. 67 - 77
Copyright
© 2004 Cambridge University Press

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

BERGWERFF, A. A., THOMAS-OATES, J. E., VAN OOSTRUM, J., KAMERLING, J. P. & VLIEGENTHART, J. F. ( 1992). 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 Letters 314, 389–394.CrossRefGoogle Scholar
BERGWERFF, A. A., VAN DAM, G. J., ROTMANS, J. P., DEELDER, A. M., KAMERLING, J. P. & VLIEGENTHART, J. F. ( 1994). The immunologically reactive part of immunopurified circulating anodic antigen from Schistosoma mansoni is a threonine-linked polysaccharide consisting of - ->6)-(beta-D-GlcpA-(1- ->3))-beta-D-GalpNAc-(1- ->repeating units. Journal of Biological Chemistry 269, 31510–31517.Google Scholar
BOGERS, J. J., NIBBELING, H. A., SINGH, S. K., DEELDER, A. M. & VAN MARCK, E. A. ( 1995). Ultrastructural immunolocalization of two circulating egg antigens in miracidia of Schistosoma mansoni. Parasitology 110, 365–370.CrossRefGoogle Scholar
BOGERS, J. J., NIBBELING, H. A., VAN MARCK, E. A. & DEELDER, A. M. ( 1994). Immunofluorescent visualization of the excretory and gut system of Schistosoma mansoni by confocal laser scanning microscopy. American Journal of Tropical Medicine and Hygiene 50, 612–619.CrossRefGoogle Scholar
DALTON, J. P., DAY, S. R., DREW, A. C. & BRINDLEY, P. J. ( 1997). A method for the isolation of schistosome eggs and miracidia free of contaminating host tissues. Parasitology 115, 29–32.CrossRefGoogle Scholar
DE GRAAF, T. W., VAN DER STELT, M. E., ANBERGEN, M. G. & VAN DIJK, W. ( 1993). Inflammation-induced expression of sialyl Lewis X-containing glycan structures on alpha 1-acid glycoprotein (orosomucoid) in human sera. Journal of Experimental Medicine 177, 657–666.CrossRefGoogle Scholar
DEELDER, A. M., VAN DAM, G. J., KORNELIS, D., FILLIE, Y. E. & VAN ZEYL, R. J. ( 1996). Schistosoma: analysis of monoclonal antibodies reactive with the circulating antigens CAA and CCA. Parasitology 112, 21–35.CrossRefGoogle Scholar
DUNNE, D. W. & BICKLE, Q. D. ( 1987). Identification and characterization of a polysaccharide-containing antigen from Schistosoma mansoni eggs which cross-reacts with the surface of schistosomula. Parasitology 94, 255–268.CrossRefGoogle Scholar
EBERL, M., LANGERMANS, J. A., VERVENNE, R. A., NYAME, A. K., CUMMINGS, R. D., THOMAS, A. W., COULSON, P. S. & WILSON, R. A. ( 2001). Antibodies to glycans dominate the host response to schistosome larvae and eggs: is their role protective or subversive? Journal of Infectious Diseases 183, 1238–1247.Google Scholar
EL RIDI, R., VELUPILLAI, P. & HARN, D. A. ( 1996). Regulation of schistosome egg granuloma formation: host-soluble L-selectin enters tissue-trapped eggs and binds to carbohydrate antigens on surface membranes of miracidia. Infection and Immunity 64, 4700–4705.Google Scholar
FAVEEUW, C., ANGELI, V., FONTAINE, J., MALISZEWSKI, C., CAPRON, A., VAN KAER, L., MOSER, M., CAPRON, M. & TROTTEIN, F. ( 2002). Antigen presentation by CD1d contributes to the amplification of Th2 responses to Schistosoma mansoni glycoconjugates in mice. Journal of Immunology 169, 906–912.CrossRefGoogle Scholar
FOX, N., DAMJANOV, I., KNOWLES, B. B. & SOLTER, R. D. ( 1983). Immunohistochemical localization of the mouse stage-specific embryonic antigen-1 in human tissues and tumors. Cancer Research 43, 669–678.Google Scholar
GAUSE, W. C., URBAN, J. F. Jr. & STADECKER, M. J. ( 2003). The immune response to parasitic helminths: insights from murine models. Trends in Immunology 24, 269–277.CrossRefGoogle Scholar
GEYER, H., WUHRER, M., KUROKAWA, T. & GEYER, R. ( 2004). Characterization of keyhole limpet hemocyanin (KLH) glycans sharing a carbohydrate epitope with Schistosoma mansoni glycoconjugates. Micron 35, 105–106.CrossRefGoogle Scholar
GRZYCH, J. M., DISSOUS, C., CAPRON, M., TORRES, S., LAMBERT, P. H. & CAPRON, A. ( 1987). Schistosoma mansoni shares a protective carbohydrate epitope with keyhole limpet hemocyanin. Journal of Experimental Medicine 165, 865–878.CrossRefGoogle Scholar
HAMILTON, J. V., CHIODINI, P. L., FALLON, P. G. & DOENHOFF, M. J. ( 1999). Periodate-sensitive immunological cross-reactivity between keyhole limpet haemocyanin (KLH) and serodiagnostic Schistosoma mansoni egg antigens. Parasitology 118, 83–89.CrossRefGoogle Scholar
HOKKE, C. H. & DEELDER, A. M. ( 2001). Schistosome glycoconjugates in host-parasite interplay. Glycoconjugate Journal 18, 573–587.CrossRefGoogle Scholar
JACOBS, W., BOGERS, J. J., TIMMERMANS, J. P., DEELDER, A. M. & VAN MARCK, E. A. ( 1998). Adhesion molecules in intestinal Schistosoma mansoni infection. Parasitology Research 84, 276–280.CrossRefGoogle Scholar
JACOBS, W., DEELDER, A. & VAN MARCK, E. ( 1999). Schistosomal granuloma modulation. II. Specific immunogenic carbohydrates can modulate schistosome-egg-antigen-induced hepatic granuloma formation. Parasitology Research 85, 14–18.CrossRefGoogle Scholar
JORDAN, P., WEBBE, G. & STURROCK, R. F. ( 1993). Human Schistosomiasis. Cambridge University Press, Cambridge.
KANTELHARDT, S. R., WUHRER, M., DENNIS, R. D., DOENHOFF, M. J., BICKLE, Q. & GEYER, R. ( 2002). Fuc(alpha1->3)GalNAc-: major antigenic motif of Schistosoma mansoni glycolipids implicated in infection sera and keyhole limpet hemocyanin cross-reactivity. The Biochemical Journal 366, 217–223.CrossRefGoogle Scholar
KHOO, K. H., CHATTERJEE, D., CAULFIELD, J. P., MORRIS, H. R. & DELL, A. ( 1997 a). Structural characterization of glycosphingolipids from the eggs of Schistosoma mansoni and Schistosoma japonicum. Glycobiology 7, 653–661.Google Scholar
KHOO, K. H., CHATTERJEE, D., CAULFIELD, J. P., MORRIS, H. R. & DELL, A. ( 1997 b). Structural mapping of the glycans from the egg glycoproteins of Schistosoma mansoni and Schistosoma japonicum: identification of novel core structures and terminal sequences. Glycobiology 7, 663–677.Google Scholar
KHOO, K. H., SARDA, S., XU, X., CAULFIELD, J. P., McNEIL, M. R., HOMANS, S. W., MORRIS, H. R. & DELL, A. ( 1995). A unique multifucosylated -3GalNAc beta 1- ->4GlcNAc beta 1- ->3Gal alpha 1-motif constitutes the repeating unit of the complex O-glycans derived from the cercarial glycocalyx of Schistosoma mansoni. Journal of Biological Chemistry 270, 17114–17123.CrossRefGoogle Scholar
KOSTER, B. & STRAND, M. ( 1994). Schistosoma mansoni: immunolocalization of two different fucose-containing carbohydrate epitopes. Parasitology 108, 433–446.CrossRefGoogle Scholar
MARQUES, E. T. Jr ., ICHIKAWA, Y., STRAND, M., AUGUST, J. T., HART, G. W. & SCHNAAR, R. L. ( 2001). Fucosyltransferases in Schistosoma mansoni development. Glycobiology 11, 249–259.CrossRefGoogle Scholar
NAUS, C. W., VAN REMOORTERE, A., OUMA, J. H., KIMANI, G., DUNNE, D. W., KAMERLING, J. P., DEELDER, A. M. & HOKKE, C. H. ( 2003). Specific antibody responses to three schistosome-related carbohydrate structures in recently exposed immigrants and established residents in an area of Schistosoma mansoni endemicity. Infection and Immunity 71, 5676–5681.CrossRefGoogle Scholar
NIBBELING, H. A., KAHAMA, A. I., VAN ZEYL, R. J. & DEELDER, A. M. ( 1998). Use of monoclonal antibodies prepared against Schistosoma mansoni hatching fluid antigens for demonstration of Schistosoma haematobium circulating egg antigens in urine. American Journal of Tropical Medicine and Hygiene 58, 543–550.CrossRefGoogle Scholar
NOUREL DIN, M. A., KORNELIS, D., VAN ZEYL, R. J. & DEELDER, A. M. ( 1994). Immunologic characterization of two monoclonal antibodies reactive with repetitive carbohydrate epitopes of circulating Schistosoma mansoni egg antigen. American Journal of Tropical Medicine and Hygiene 50, 487–498.CrossRefGoogle Scholar
NYAME, A. K., LEWIS, F. A., DOUGHTY, B. L., CORREA-OLIVEIRA, R. & CUMMINGS, R. D. ( 2003). Immunity to schistosomiasis: glycans are potential antigenic targets for immune intervention. Experimental Parasitology 104, 1–13.CrossRefGoogle Scholar
NYAME, A. K., YOSHINO, T. P. & CUMMINGS, R. D. ( 2002). Differential expression of LacdiNAc, fucosylated LacdiNAc, and Lewis x glycan antigens in intramolluscan stages of Schistosoma mansoni. Journal of Parasitology 88, 890–897.CrossRefGoogle Scholar
OKANO, M., SATOSKAR, A. R., NISHIZAKI, K., ABE, M. & HARN, D. A. ( 1999). Induction of Th2 responses and IgE is largely due to carbohydrates functioning as adjuvants on Schistosoma mansoni egg antigens. Journal of Immunology 163, 6712–6717.Google Scholar
OKANO, M., SATOSKAR, A. R., NISHIZAKI, K. & HARN, D. A. Jr. ( 2001). Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. Journal of Immunology 167, 442–450.CrossRefGoogle Scholar
ROSS, A. G., BARTLEY, P. B., SLEIGH, A. C., OLDS, G. R., LI, Y., WILLIAMS, G. M. & McMANUS, D. P. ( 2002). Schistosomiasis. New England Journal of Medicine 346, 1212–1220.CrossRefGoogle Scholar
STELMA, F. F., TALLA, I., POLMAN, K., NIANG, M., STURROCK, R. F., DEELDER, A. M. & GRYSEELS, B. ( 1993). Epidemiology of Schistosoma mansoni infection in a recently exposed community in northern Senegal. American Journal of Tropical Medicine and Hygiene 49, 701–706.CrossRefGoogle Scholar
STRAND, M., McMILLAN, A. & PAN, X. ( 1982). Schistosoma mansoni: reactivity with infected human sera and monoclonal antibody characterization of a glycoprotein in different developmental stages. Experimental Parasitology 54, 145–156.CrossRefGoogle Scholar
THOMAS, P. G., CARTER, M. R., ATOCHINA, O., DA'DARA, A. A., PISKORSKA, D., McGUIRE, E. & HARN, D. A. ( 2003). Maturation of dendritic cell 2 phenotype by a helminth glycan uses a toll-like receptor 4-dependent mechanism. Journal of Immunology 171, 5837–5841.CrossRefGoogle Scholar
THOMAS, P. G. & HARN, D. A. Jr. ( 2004). Immune biasing by helminth glycans. Cellular Microbiology 6, 13–22.CrossRefGoogle Scholar
THORS, C. & LINDER, E. ( 1998). Cross reacting antibodies against keyhole limpet haemocyanin may interfere with the diagnostics of acute schistosomiasis. Parasite Immunology 20, 489–496.CrossRefGoogle Scholar
THORS, C. & LINDER, E. ( 2003). Localization and identification of Schistosoma mansoni/KLH-crossreactive components in infected mice. Journal of Histochemistry and Cytochemistry 51, 1367–1373.CrossRefGoogle Scholar
VAN DAM, G. J., BERGWERFF, A. A., THOMAS-OATES, J. E., ROTMANS, J. P., KAMERLING, J. P., VLIEGENTHART, J. F. & DEELDER, A. M. ( 1994). The immunologically reactive O-linked polysaccharide chains derived from circulating cathodic antigen isolated from the human blood fluke Schistosoma mansoni have Lewis x as repeating unit. European Journal of Biochemistry 225, 467–482.Google Scholar
VAN DAM, G. J., KORNELIS, D., VAN ZEYL, R. J., ROTMANS, J. P. & DEELDER, A. M. ( 1993). Schistosoma mansoni: analysis of monoclonal antibodies reactive with gut-associated antigens. Parasitology Research 79, 55–62.Google Scholar
VAN DER KLEIJ, D., VAN REMOORTERE, A., SCHUITEMAKER, J. H., KAPSENBERG, M. L., DEELDER, A. M., TIELENS, A. G., HOKKE, C. H. & YAZDANBAKHSH, M. ( 2002). Triggering of innate immune responses by schistosome egg glycolipids and their carbohydrate epitope GalNAc beta 1-4(Fuc alpha 1-2Fuc alpha 1-3)GlcNAc. Journal of Infectious Diseases 185, 531–539.Google Scholar
VAN REMOORTERE, A., HOKKE, C. H., VAN DAM, G. J., VAN DIE, I., DEELDER, A. M. & VAN DEN EIJNDEN, D. H. ( 2000). Various stages of schistosoma express Lewis(x), LacdiNAc, GalNAcbeta1-4 (Fucalpha1-3)GlcNAc and GalNAcbeta1-4(Fucalpha1-2Fucalpha1-3)GlcNAc carbohydrate epitopes: detection with monoclonal antibodies that are characterized by enzymatically synthesized neoglycoproteins. Glycobiology 10, 601–609.CrossRefGoogle Scholar
VAN REMOORTERE, A., VAN DAM, G. J., HOKKE, C. H., VAN DEN EIJNDEN, D. H., VAN DIE, I. & DEELDER, A. M. ( 2001). Profiles of immunoglobulin M (IgM) and IgG antibodies against defined carbohydrate epitopes in sera of Schistosoma-infected individuals determined by surface plasmon resonance. Infection and Immunity 69, 2396–2401.CrossRefGoogle Scholar
VAN REMOORTERE, A., VERMEER, H. J., VAN ROON, A. M., LANGERMANS, J. A., THOMAS, A. W., WILSON, R. A., VAN DIE, I., VAN DEN EIJNDEN, D. H., AGOSTON, K., KEREKGYARTO, J., VLIEGENTHART, J. F., KAMERLING, J. P., VAN DAM, G. J., HOKKE, C. H. & DEELDER, A. M. ( 2003). Dominant antibody responses to Fucalpha1-3GalNAc and Fucalpha1-2Fucalpha1-3GlcNAc containing carbohydrate epitopes in Pan troglodytes vaccinated and infected with Schistosoma mansoni. Experimental Parasitology 105, 219–225.CrossRefGoogle Scholar
VAN DE VIJVER, K. K., HOKKE, C. H., VAN REMOORTERE, A., JACOBS, W., DEELDER, A. M. & VAN MARCK, E. A. ( 2004). Glycans of Schistosoma mansoni and keyhole limpet haemocyanin induce hapatic granulomas in vivo. International Journal for Parasitology 34, 951–961.CrossRefGoogle Scholar
VELUPILLAI, P., DOS REIS, E. A., DOS REIS, M. G. & HARN, D. A. ( 2000). Lewis(x)-containing oligosaccharide attenuates schistosome egg antigen-induced immune depression in human schistosomiasis. Human Immunology 61, 225–232.CrossRefGoogle Scholar
WEISS, J. B., ARONSTEIN, W. S. & STRAND, M. ( 1987). Schistosoma mansoni: stimulation of artificial granuloma formation in vivo by carbohydrate determinants. Experimental Parasitology 64, 228–236.CrossRefGoogle Scholar
WEISS, J. B., MAGNANI, J. L. & STRAND, M. ( 1986). Identification of Schistosoma mansoni glycolipids that share immunogenic carbohydrate epitopes with glycoproteins. Journal of Immunology 136, 4275–4282.Google Scholar
WEISS, J. B. & STRAND, M. ( 1985). Characterization of developmentally regulated epitopes of Schistosoma mansoni egg glycoprotein antigens. Journal of Immunology 135, 1421–1429.Google Scholar
WUHRER, M., DENNIS, R. D., DOENHOFF, M. J., BICKLE, Q., LOCHNIT, G. & GEYER, R. ( 1999). Immunochemical characterisation of Schistosoma mansoni glycolipid antigens. Molecular and Biochemical Parasitology 103, 155–169.CrossRefGoogle Scholar
WUHRER, M., DENNIS, R. D., DOENHOFF, M. J. & GEYER, R. ( 2000). A fucose-containing epitope is shared by keyhole limpet haemocyanin and Schistosoma mansoni glycosphingolipids. Molecular and Biochemical Parasitology 110, 237–246.CrossRefGoogle Scholar
WUHRER, M., KANTELHARDT, S. R., DENNIS, R. D., DOENHOFF, M. J., LOCHNIT, G. & GEYER, R. ( 2002). Characterization of glycosphingolipids from Schistosoma mansoni eggs carrying Fuc(alpha1-3)GalNAc-, GalNAc(beta1-4)[Fuc(alpha1-3)]GlcNAc- and Gal(beta1-4)[Fuc(alpha1-3)]GlcNAc- (Lewis X) terminal structures. European Journal of Biochemistry 269, 481–493.CrossRefGoogle Scholar
YAN, S. B., CHAO, Y. B. & VAN HALBEEK, H. ( 1993). 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 3, 597–608.Google Scholar