Role of the Parasite-derived Prostaglandin D2 in the Inhibition of Epidermal Langerhans Cell Migration during Schistosomiasis Infection

doi:10.1084/jem.193.10.1135

Published online 14 May 2001.

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© The Rockefeller University Press, 0022-1007/2001/5/1135/ $5.00
The Journal of Experimental Medicine, Volume 193, Number 10, May 21, 2001 1135-1148

Original Article

Role of the Parasite-derived Prostaglandin D₂ in the Inhibition of Epidermal Langerhans Cell Migration during Schistosomiasis Infection

Véronique Angeli^a, Christelle Faveeuw^a, Olivier Roye^b, Josette Fontaine^a, Elisabeth Teissier^c, André Capron^a, Isabelle Wolowczuk^b, Monique Capron^a, and François Trottein^a
^a Centre d'Immunologie et de Biologie Parasitaire, Institut National de la Santé et de la Recherche Médicale (INSERM) U547,
^b Centre National de la Recherche Scientifique 8527, Institut de Biologie de Lille
^c INSERM U545, Institut Pasteur de Lille, Lille 59019, France

Correspondence to: François Trottein, Centre d'Immunologie et de Biologie Parasitaire, INSERM U547, Institut Pasteur de Lille, 1 rue du Professeur Calmette, 59019 Lille Cedex, France. Tel:33-3-20-877-885 Fax:33-3-20-877-888 E-mail:francois.trottein{at}pasteur-lille.fr.

Epidermal Langerhans cells (LCs) play a key role in immune defensemechanisms and in numerous immunological disorders. In thisreport, we show that percutaneous infection of C57BL/6 micewith the helminth parasite Schistosoma mansoni leads to theactivation of LCs but, surprisingly, to their retention in theepidermis. Moreover, using an experimental model of LC migrationinduced by tumor necrosis factor (TNF)- ${alpha}$ , we show that parasitestransiently impair the departure of LCs from the epidermis andtheir subsequent accumulation as dendritic cells in the draininglymph nodes. The inhibitory effect is mediated by soluble lipophilicfactors released by the parasites and not by host-derived antiinflammatorycytokines, such as interleukin-10. We find that prostaglandin(PG)D₂, but not the other major eicosanoids produced by theparasites, specifically impedes the TNF- ${alpha}$ –triggered migrationof LCs through the adenylate cyclase–coupled PGD₂ receptor(DP receptor). Moreover, the potent DP receptor antagonist BWA868C restores LC migration in infected mice. Finally, in amodel of contact allergen-induced LC migration, we show thatactivation of the DP receptor not only inhibits LC emigrationbut also dramatically reduces the contact hypersensitivity responsesafter challenge. Taken together, we propose that the inhibitionof LC migration could represent an additional stratagem forthe schistosomes to escape the host immune system and that PGD₂may play a key role in the control of cutaneous immune responses.

Key Words: dendritic cells, migration, Schistosoma, eicosanoids, cAMP

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