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Anopheles Mosquito Bites Activate Cutaneous Mast Cells Leading to a Local Inflammatory Response and Lymph Node Hyperplasia¹

Christian E. Demeure^*, Karima Brahimi^2,, Feriel Hacini^2,*, Françoise Marchand^*, Roger Péronet^*, Michel Huerre, Pierre St.-Mezard, Jean-François Nicolas, Paul Brey, Guy Delespesse^¶ and Salaheddine Mécheri^3,*

^* Unités Immuno-Allergie, Biochimie et Biologie Moléculaire des Insectes, and Histotechnologie et Pathologie, Institut Pasteur, Paris, France; INSERM U503 and Allergy Research Laboratory, Lyon, France; and ^¶ Centre de Recherché du Centre Hospitalier Universitaire de Montréal, Montreal, Québec, Canada

When Anopheles mosquitoes probe the skin for blood feeding, they inject saliva in dermal tissue. Mosquito saliva is known to exert various biological activities, but its perception by the immune system and its role in parasite transmission remain poorly understood. In the present study, we report on the cellular changes occurring in the mouse skin and draining lymph nodes after a Anopheles stephensi mosquito bite. We show that mosquito bites induce dermal mast cell degranulation, leading to fluid extravasation and neutrophil influx. This inflammatory response does not occur in mast cell-deficient W/W^v mice, unless these are reconstituted specifically with mast cells. Mast cell activation caused by A. stephensi mosquito bites is followed by hyperplasia of the draining lymph node due to the accumulation of CD3⁺, B220⁺, CD11b⁺, and CD11c⁺ leukocytes. The T cell enrichment of the draining lymph nodes results from their sequestration from the circulation rather than local proliferation. These data demonstrate that mosquito bites and very likely saliva rapidly trigger the immune system, emphasizing the critical contribution of peripheral mast cells in inducing T cell and dendritic cell recruitment within draining lymph nodes, a prerequisite for the elicitation of T and B lymphocyte priming.

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