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Title: Identification of Midgut and Salivary Glands as Specific and Distinct Barriers to Efficient Tick-Borne Transmission of Anaplasma marginale

Author
item UETI, MASSARO - WSU
item REAGON, JAMES - WSU
item Knowles Jr, Donald
item Scoles, Glen
item SHKAP, VARDA - KIMRON VETERINARY INST
item PALMER, GUY - WSU

Submitted to: Infection and Immunity
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/30/2007
Publication Date: 6/1/2007
Citation: Ueti, M.W., Reagon, J.O., Knowles Jr, D.P., Scoles, G.A., Shkap, V., Palmer, G.H. 2007. Identification of Midgut and Salivary Glands as Specific and Distinct Barriers to Efficient Tick-Borne Transmission of Anaplasma marginale. Infection and Immunity. 75(6):2959-2964

Interpretive Summary: Control of vector (tick) borne diseases requires a detailed understanding of the relationship between the disease agent and the transmitting (tick) agent. These data showed, remarkably that the ability of the tick to transmit this disease agent (Anaplasma marginale) is controlled at both the gut (entry point) and salivary gland (exit point). An understanding of what genes encode this control within the disease agent will aid in the development of vaccines which induce immunity but aren't transmissible by their tick vectors.

Technical Abstract: Understanding the determinants of efficient tick-borne microbial transmission is needed to better predict the emergence of highly transmissible pathogen strains and disease outbreaks. Although the basic developmental cycle of Anaplasma and Ehrlichia spp. within the tick has been delineated, there are marked differences in the ability of specific strains to be efficiently tick transmitted. Using the highly transmissible St. Maries strain of A. marginale in Dermacentor andersoni as a positive control and two unrelated non-transmissible strains, we identified distinct barriers to efficient transmission within the tick. The Mississippi strain was unable to establish infection at the level of midgut epithelium despite successful ingestion of infected blood following acquisition feeding on a bacteremic animal host. This inability to colonize the midgut epithelium prevented subsequent development within the salivary gland and transmission. In contrast, A. marginale ss. centrale colonized the midgut and then the salivary gland, replicating to a titer indistinguishable from that of the highly transmissible St. Maries strain and at least 100x greater than that previously associated with successful transmission. Nonetheless, A. marginale ss. centrale was not transmitted, even using a large number of infected ticks for transmission feeding. These results establish that there are at least two specific barriers, the midgut and salivary gland, to efficient tick-borne transmission, and highlight the complexity of the pathogen-tick interaction.