Mosquito Transcriptome Profiles and Filarial Worm Susceptibility in Armigeres subalbatus

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 FindingsUtilizing 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/SignificanceHerein, 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.

Involvement of the Anopheles gambiae Nimrod gene family in mosquito immune responses

“…melanogaster draper, nimC1 and eater bind bacteria, and this binding leads to phagocytosis by hemocytes. Often, mosquito genes with immune function are transcriptionally upregulated in response to infection (Aliota et al, 2010;Baton et al, 2009;Choi et al, 2012;Pinto et al, 2009). In the present study, we found that A. gambiae draper, nimrod and eater are all transcriptionally upregulated in response to infection, although the magnitude of the induction varied significantly between the genes (eater upregulation was >11 fold higher than that of draper).…”

Genome-Wide Transcriptional Analysis of <b><i>Drosophila</i></b> Larvae Infected by Entomopathogenic Nematodes Shows Involvement of Complement, Recognition and Extracellular Matrix Proteins

“…Filarial nematodes use insects as vectors to infect vertebrates, such as cattle and humans, sometimes causing debilitating and fatal diseases such as river blindness, and heart and lymphatic filariasis [4]. This has stimulated several systematic studies on the transcriptome changes that occur in vector insects after infection with filarial nematodes [11,12,13]. For example, the innate immune responses against the causative agents of lymphatic filariasis (caused by Brugia pahangi ) were characterized in their insect host (Armigeres subalbatus) , and several putative immune-related molecules were found to be induced [12].…”

“…This has stimulated several systematic studies on the transcriptome changes that occur in vector insects after infection with filarial nematodes [11,12,13]. For example, the innate immune responses against the causative agents of lymphatic filariasis (caused by Brugia pahangi ) were characterized in their insect host (Armigeres subalbatus) , and several putative immune-related molecules were found to be induced [12]. A closely related species (B. malayi) to which Armigeres is resistant showed a distinctly different pattern of induction [12].…”

“…For example, the innate immune responses against the causative agents of lymphatic filariasis (caused by Brugia pahangi ) were characterized in their insect host (Armigeres subalbatus) , and several putative immune-related molecules were found to be induced [12]. A closely related species (B. malayi) to which Armigeres is resistant showed a distinctly different pattern of induction [12]. Ultimately, the hope behind these studies is to increase our understanding of these responses and identify protective factors [4].…”

This De-Wormed World?

“…ASP investigators have played an important role in investigating the basic biological interactions between human helminths and their invertebrate hosts. As just some recent examples, Aliota et al (2010) have shown that distinct transcriptional profiles are generated in mosquitoes following their exposure to filarial worms to which they are susceptible or refractory. This helps not only to understand the complex nature of vector competence and the genes involved, but could lead to new ways to exploit such genes to achieve filariasis control.…”