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Infection and Immunity, October 2001, p. 6074-6083, Vol. 69, No. 10
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.10.6074-6083.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Major Carbohydrate Antigen of Echinococcus multilocularis Induces an Immunoglobulin G Response Independent of ⁺ CD4⁺ T Cells

Wen Juan Dai,^1,* Andrew Hemphill,¹ Andreas Waldvogel,² Katrin Ingold,¹ Peter Deplazes,³ Horst Mossmann,⁴ and Bruno Gottstein^1,*

Institute of Parasitology¹ and Institute of Animal Pathology,² University of Berne, CH-3001 Berne, and Institute of Parasitology, University of Zurich, Zurich,³ Switzerland, and Max Plank Institute for Immunobiology, Freiburg, Germany⁴

Received 11 December 2000/Returned for modification 20 March 2001/Accepted 9 July 2001

Echinococcus multilocularis causes alveolar echinococcosis, one of the most lethal helminthic (accidental) infections in humans, as the life cycle predominantly includes wildlife rodents as intermediate hosts. The physical barrier between the proliferating parasitic metacestode and the host tissue is the acellular laminated layer (LL), which is characterized by its rich high-molecular-weight polysaccharide composition. Conversely to a crude protein-rich vesicular fluid antigen, a major carbohydrate antigen of the LLthe Em2(G11) antigendid not stimulate murine T-cell proliferation in vitro. In fact, the persistent metacestode growth and antigenic stimulation induced a Th2 shift in vivo following conventional infection by intraperitoneal inoculation of 100 metacestode vesicles into C57/BL6 mice. Concurrently, the expression of Th1 cytokines (interleukin-2 and gamma interferon) remained persistently low until the late stage of chronic infection. In comparison to a recombinant proteinic II/3 antigen, the specific immunoglobulin G (IgG) response against the Em2(G11) antigen (including all IgG isotypes) maintained persistently low avidity. Furthermore, the Em2(G11) antigen induced a specific IgM and IgG response in T-cell-deficient athymic nude, TCR^/, major histocompatibility complex class II (MHCII)^/(CD4-deficient), and CD40^/ mice. The Em2(G11)-specific IgG synthesized in nude TCR^/ and MHCII^/ mice was predominantly of the IgG3 and IgG2a isotypes and of the IgG3 and IgG2b isotypes in CD40^/ mice. This finding suggested that in vivo, the IgG response to major carbohydrate antigen Em2(G11) of E. multilocularis could take place independently of ⁺ CD4⁺ T cells and in the absence of CD40-CD40 ligand interactions; thus, the Em2(G11) antigen of the acellular LL represents a T-cell-independent antigen. Functionally, the encapsulating LL, and especially its major carbohydrate antigen, Em2(G11), seems to be one of the key factors in the parasite's survival strategy and acts by modulating the host immune response by virtue of its T-cell-independent nature.

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^* Corresponding author. Mailing address for B. Gottstein: Institute of Parasitology, University of Berne, Länggass-Strasse 122, CH-3012 Berne, Switzerland. Phone: 41 31 631 24 18. Fax: 41 31 631 26 22. E-mail: bruno.gottstein{at}ipa.unibe.ch. Present address for W. J. Dai: Clinic for Rheumatology and Clinical Immunology/Allergology, University Hospital, Inselspital, CH-3010 Bern, Switzerland. Phone: 41 21 632 2245. E-mail: wen.dai{at}dkf6.unibe.ch.

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Infection and Immunity, October 2001, p. 6074-6083, Vol. 69, No. 10
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.10.6074-6083.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

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