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Title: Temporal characterization of the organ-specific Rhipicephalus microplus transcriptional response to Anaplasma marginale infection

Author
item MERCADO-CURIEL, RICARDO - Washington State University
item PALMER, GUY - Washington State University
item Guerrero, Felicito
item BRAYTON, KELLY - Washington State University

Submitted to: International Journal for Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/7/2011
Publication Date: 4/7/2011
Citation: Mercado-Curiel, R.F., Palmer, G.H., Guerrero, F., Brayton, K.A. 2011. Temporal characterization of the organ-specific Rhipicephalus microplus transcriptional response to Anaplasma marginale infection. International Journal for Parasitology. 41:851-860.

Interpretive Summary: Arthropods transmit a variety of important infectious diseases of humans and animals. The development of the infective capacity of the pathogenic organism is tightly linked to the arthropod vector feeding on the mammalian host. Thus, analysis of the genes which are turned off and on in both vector and pathogen during feeding is fundamental in understanding transmission. Using Anaplasma marginale infection of Rhipicephalus microplus as the experimental model, we tested three linked hypotheses regarding gene expression changes during feeding and in response to infection. Numerous R. microplus genes in the midgut and salivary gland were regulated in response to feeding and there was a clear change in regulated gene expression in the salivary gland over time. In contrast, the expression of relatively few tick genes changed in response to A. marginale infection. Unfortunately, most of the genes that changed expression in response to feeding were genes with unknown function. The midgut serves as an initial site of uptake and replication of the A. marginale organisms as blood is ingested, while the salivary gland serves as the final site of replication and secretion of the mature infective A. marginale. The small effect that A. marginale appears to have on the gene expression pattern of the tick host supports the view that the vector-pathogen relationship is well-established with minimal deleterious effect on the tick. The small set of genes whose gene expression pattern was altered by infection suggests that A. marginale is affecting a novel set of tick genes and may provide new opportunities for blocking transmission from the tick.

Technical Abstract: Arthropods transmit a variety of important infectious diseases of humans and animals. Importantly, replication and development of pathogen infectivity is tightly linked to vector feeding on the mammalian host; thus analysis of the transcriptomes of both vector and pathogen during feeding is fundamental in understanding transmission. Using Anaplasma marginale infection of Rhipicephalus microplus as the experimental model, we tested three linked hypotheses exploring the temporal and organ-specific nature of the tick midgut and salivary gland transcriptomes during feeding and in response to infection. Numerous R. microplus genes were regulated in response to feeding. Genes were differentially regulated between the midgut and salivary gland and there was a clear progression in regulated gene expression in the salivary gland over time. In contrast, relatively few tick genes were specifically regulated in response to A. marginale infection. The genes regulated in response to infection were predominantly annotated as hypothetical or were genes of unknown function. Notable among the genes with informative annotation was that several ribosomal proteins were down regulated, suggesting that there may be a corresponding decrease in translation. The hypotheses that R. microplus salivary gland and midgut genes are differentially regulated and that the salivary gland transcriptome is dynamic over time were accepted. This is consistent with and important for understanding the different roles of the two organs, the midgut serving as an initial site of uptake and replication while the salivary gland serves as the final site of replication and secretion. The minimal effect of A. marginale on the tick transcriptome in terms of the numbers of regulated genes and the fold of regulation supports the view that the vector-pathogen relationship is well-established with minimal deleterious effect on the tick. The small set of predominantly hypothetical genes regulated by infection suggests that A. marginale is affecting a novel set of tick genes and may provide new opportunities for blocking transmission from the tick.