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- Title
Mosquito Transcriptome Profiles and Filarial Worm Susceptibility in Armigeres subalbatus.
- Authors
Aliota, Matthew T.; Fuchs, Jeremy F.; Rocheleau, Thomas A.; Clark, Amanda K.; Hillyer, Julián F.; Chen, Cheng-Chen; Christensen, Bruce M.
- Abstract
Background: Armigeres subalbatus is a natural vector of the filarial worm Brugia pahangi, but it kills Brugia malayi microfilariae by melanotic encapsulation. Because B. malayi and B. pahangi are morphologically and biologically similar, comparing Ar. subalbatus-B. pahangi susceptibility and Ar. subalbatus-B. malayi refractoriness could provide significant insight into recognition mechanisms required to mount an effective anti-filarial worm immune response in the mosquito, as well as provide considerable detail into the molecular components involved in vector competence. Previously, we assessed the transcriptional response of Ar. subalbatus to B. malayi, and now we report transcriptome profiling studies of Ar. subalbatus in relation to filarial worm infection to provide information on the molecular components involved in B. pahangi susceptibility. Methodology/Principal Findings: Utilizing microarrays, comparisons were made between mosquitoes exposed to B. pahangi, B. malayi, and uninfected bloodmeals. The time course chosen facilitated an examination of key events in the development of the parasite, beginning with the very start of filarial worm infection and spanning to well after parasites had developed to the infective stage in the mosquito. At 1, 3, 6, 12, 24 h post infection and 2–3, 5–6, 8–9, and 13–14 days post challenge there were 31, 75, 113, 76, 54, 5, 3, 13, and 2 detectable transcripts, respectively, with significant differences in transcript abundance (increase or decrease) as a result of parasite development. Conclusions/Significance: Herein, we demonstrate that filarial worm susceptibility in a laboratory strain of the natural vector Ar. subalbatus involves many factors of both known and unknown function that most likely are associated with filarial worm penetration through the midgut, invasion into thoracic muscle cells, and maintenance of homeostasis in the hemolymph environment. The data show that there are distinct and separate transcriptional patterns associated with filarial worm susceptibility as compared to refractoriness, and that an infection response in Ar. subalbatus can differ significantly from that observed in Ae. aegypti, a common laboratory model. Author Summary: In general, organisms can use two different strategies when confronted with pathogens, tolerance and/or resistance. Resistance reduces the fitness of the invading pathogen, whereas tolerance reduces the damage caused by the pathogen to the host. Mosquitoes that transmit the parasites that cause human lymphatic filariasis generally are tolerant to the parasite, whereas those that do not transmit the parasite are resistant. We examined the effects of filarial worm tolerance and resistance on Armigeres subalbatus by analyzing changes in mosquito gene expression at key stages of parasite development and destruction. Because the gene expression data showed few mosquito transcriptional changes associated with parasite development, we morphologically examined mosquito flight muscle to see if we could identify damage associated with parasite infection. The research described in this manuscript provides a better understanding of the molecular components involved in compatible and incompatible relationships between mosquitoes and the filarial worm parasites that they transmit; and it will provide new insights into the complex biology of vector competence and the origins of host defense, and possibly lead to the functional characterization of previously unknown gene products involved in vector competence.
- Subjects
ARABIAN Peninsula; FILARIAL worms; AEDES aegypti; MOSQUITOES; FILARIASIS; TRANSCRIPTOMES; BIVECTORS
- Publication
PLoS Neglected Tropical Diseases, 2010, Vol 4, Issue 4, p1
- ISSN
1935-2727
- Publication type
Article
- DOI
10.1371/journal.pntd.0000666