Filarial infection influences mosquito behaviour and fecundity.
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ABSTRACT:
SUBMITTER: Gleave K
PROVIDER: S-EPMC5087081 | biostudies-literature | 2016 Oct
REPOSITORIES: biostudies-literature
Publications
Filarial infection influences mosquito behaviour and fecundity.
Gleave Katherine K Cook Darren D Taylor Mark J MJ Reimer Lisa J LJ
Scientific reports 20161031
Understanding vector-parasite interactions is increasingly important as we move towards the endpoint goals set by the Global Programme for the Elimination of Lymphatic Filariasis (GPELF), as interaction dynamics may change with reduced transmission pressure. Elimination models used to predict programmatic endpoints include parameters for vector-specific transmission dynamics, despite the fact that our knowledge of the host-seeking behaviour of filariasis infected mosquitoes is lacking. We observ ...[more]
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Project description:Human lymphatic filariasis is a mosquito-vectored disease caused by the nematode parasites Wuchereria bancrofti, Brugia malayi and Brugia timori. These are relatively large roundworms that can cause considerable damage in compatible mosquito vectors. In order to assess how mosquitoes respond to infection in compatible mosquito-filarial worm associations, microarray analysis was used to evaluate transcriptome changes in Aedes aegypti at various times during B. malayi development. Changes in transcript abundance in response to the different stages of B. malayi infection were diverse. At the early stages of midgut and thoracic muscle cell penetration, a greater number of genes were repressed compared to those that were induced (20 vs. 8). The non-feeding, intracellular first-stage larvae elicited few differences, with 4 transcripts showing an increased and 9 a decreased abundance relative to controls. Several cecropin transcripts increased in abundance after parasites molted to second-stage larvae. However, the greatest number of transcripts changed in abundance after larvae molted to third-stage larvae and migrated to the head and proboscis (120 induced, 38 repressed), including a large number of putative, immunity-related genes (approximately 13% of genes with predicted functions). To test whether the innate immune system of mosquitoes was capable of modulating permissiveness to the parasite, we activated the Toll and Imd pathway controlled rel family transcription factors Rel1 and Rel2 (by RNA interference knockdown of the pathway's negative regulators Cactus and Caspar) during the early stages of infection with B. malayi. The activation of either of these immune signaling pathways, or knockdown of the Toll pathway, did not affect B. malayi in Ae. aegypti. The possibility of LF parasites evading mosquito immune responses during successful development is discussed.
| S-EPMC2752998 | biostudies-literature
Project description:BackgroundDespite long-term research on dirofilariosis in Slovakia, little attention has thus far been paid to Dirofilaria vectors. The particular aim of the present study was molecular screening for filarioid parasites in two different habitats of Bratislava, the capital city of Slovakia. In addition, the effect of urbanisation on mosquito species abundance and composition, associated with the risk of mosquito-borne infections, was studied and discussed.MethodsMosquitoes were identified by morphological features, and molecular methods were also used for determination of selected individuals belonging to cryptic species from the Anopheles maculipennis and Culex pipiens complexes. The presence of filarioid DNA (Dirofilaria repens, Dirofilaria immitis and Setaria spp.) was detected using standard PCR approaches and sequencing.ResultsA total of 6957 female mosquitoes were collected for the study. Overall, the most abundant mosquito species was Aedes vexans, closely followed by unidentified members of the Cx. pipiens complex and the less numerous but still plentiful Ochlerotatus sticticus species. Further investigation of mosquito material revealed 4.26% relative prevalence of Dirofilaria spp., whereby both species, D. repens and D. immitis, were identified. The majority of positive mosquito pools had their origin in a floodplain area on the outskirts of the city, with a relative prevalence of 5.32%; only two mosquito pools (1.26%) were shown to be positive in the residential zone of Bratislava. Setaria spp. DNA was not detected in mosquitoes within this study.ConclusionsThe study presented herein represents initial research focused on molecular mosquito screening for filarioid parasites in urban and urban-fringe habitats of Bratislava, Slovakia. Molecular analyses within the Cx. pipiens complex identified two biotypes: Cx. pipiens biotype pipiens and Cx. pipiens biotype molestus. To our knowledge, Dirofilaria spp. were detected for the first time in Slovakia in mosquitoes other than Ae. vexans, i.e. D. repens in Anopheles messeae and unidentified members of An. maculipennis and Cx. pipiens complexes, and D. immitis in Coquillettidia richiardii and Cx. pipiens biotype pipiens. Both dirofilarial species were found in Och. sticticus. The suitable conditions for the vectors' biology would represent the main risk factor for dirofilariosis transmission.
| S-EPMC5937826 | biostudies-literature
Project description:Armigeres subalbatus is a natural vector of the filarial worm Brugia pahangi, but it kills Brugia malayi microfilariae (mf) by melanotic encapsulation. Because B. malayi and B. pahangi are morphologically and biologically similar, this mosquito-parasite system serves as a valuable model for studying resistance mechanisms in mosquito vectors. 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. Accordingly, we initiated transcriptome profiling studies of Ar. subalbatus in relation to filarial worm infection to provide information on the molecular components involved in B. pahangi susceptibility for comparison with our earlier studies on B. malayi refractoriness (Aliota et al., 2007). In addition, these studies also provide information on the infection response of a natural vector, i.e., the overall transcriptional and physiological change that occurs in the mosquito as a result of parasite infection, for comparison with our previous studies that employed a highly susceptible laboratory model, Aedes aegypti (Erickson et al., 2009). 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 infective-stage parasites had completed development in the mosquito. Herein, we demonstrate that filarial worm susceptibility in Ar. subalbatus is a highly complex process during the first 24 hours of infection. It is a process that involves many factors of both known and unknown function which are most likely associated with filarial worm penetration through the midgut lumen, 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, a natural vector, can differ significantly from that observed in Ae. aegypti, a common laboratory model. Finally, the data presented herein provide us with a cadre of information to design wet lab experiments and select candidates for further study to more fully dissect the nature of the anti-filarial worm immune response in this mosquito-parasite system.
2010-04-01 | GSE20205 | GEO
Project description:BackgroundArmigeres 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.
| S-EPMC2857672 | biostudies-literature
Project description:BackgroundArmigeres subalbatus is a natural vector of the filarial worm Brugia pahangi, but it rapidly and proficiently kills Brugia malayi microfilariae by melanotic encapsulation. Because B. malayi and B. pahangi are morphologically and biologically similar, the Armigeres-Brugia system serves as a valuable model for studying the resistance mechanisms in mosquito vectors. We have initiated transcriptome profiling studies in Ar. subalbatus to identify molecular components involved in B. malayi refractoriness.ResultsThese initial studies assessed the transcriptional response of Ar. subalbatus to B. malayi at 1, 3, 6, 12, 24, 48, and 72 hrs after an infective blood feed. In this investigation, we initiated the first holistic study conducted on the anti-filarial worm immune response in order to effectively explore the functional roles of immune-response genes following a natural exposure to the parasite. Studies assessing the transcriptional response revealed the involvement of unknown and conserved unknowns, cytoskeletal and structural components, and stress and immune responsive factors. The data show that the anti-filarial worm immune response by Ar. subalbatus to be a highly complex, tissue-specific process involving varied effector responses working in concert with blood cell-mediated melanization.ConclusionThis initial study provides a foundation and direction for future studies, which will more fully dissect the nature of the anti-filarial worm immune response in this mosquito-parasite system. The study also argues for continued studies with RNA generated from both hemocytes and whole bodies to fully expound the nature of the anti-filarial worm immune response.
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Project description:BackgroundA variety of studies have reported that malaria parasites alter the behaviour of mosquitoes. These behavioural alterations likely increase transmission because they reduce the risk of vector death during parasite development and increase biting after parasites become infectious.MethodsA mathematical model is used to investigate the potential impact of these behavioural alterations on the lifetime number of infectious bites delivered. The model is used to explore the importance of assumptions about the magnitude and distribution of mortality as well as the importance of extrinsic incubation period and gonotrophic cycle length. Additionally, the model is applied to four datasets taken from actual transmission settings.ResultsThe impact of behavioural changes on the relative number of lifetime bites is highly dependent on assumptions about the distribution of mortality over the mosquito-feeding cycle. Even using fairly conservative estimates of these parameters and field collected data, the model outputs suggest that altered feeding could easily cause a doubling in the force of infection.ConclusionsInfection-induced behavioural alterations have their greatest impact on the lifetime number of infectious bites in environments with high feeding-related adult mortality and many pre-infectious feeding cycles. Interventions that increase feeding-associated mortality are predicted to amplify the relative fitness benefits and hence enhance the strength of selection for behavioural alteration.
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Project description:Mosquito-borne helminth infections are responsible for a significant worldwide disease burden in both humans and animals. Accordingly, development of novel strategies to reduce disease transmission by targeting these pathogens in the vector are of paramount importance. We found that a strain of Aedes aegypti that is refractory to infection by Dirofilaria immitis, the agent of canine heartworm disease, mounts a stronger immune response during infection than does a susceptible strain. Moreover, activation of the Toll immune signaling pathway in the susceptible strain arrests larval development of the parasite, thereby decreasing the number of transmissionstage larvae. Notably, this strategy also blocks transmission stage Brugia malayi, an agent of human lymphatic filariasis. Our data show that mosquito immunity can play a pivotal role in restricting filarial nematode development and suggest that genetically engineering mosquitoes with enhanced immunity will help reduce disease transmission.
2020-02-01 | GSE142155 | GEO
Project description:A Zika virus (ZIKV) pandemic started soon after the first autochthonous cases in Latin America. Although Aedes aegypti is pointed as the primary vector in Latin America, little is known about the fitness cost due to ZIKV infection. We investigated the effects of ZIKV infection on the life-history traits of Ae. aegypti females collected in three districts of Rio de Janeiro, Brazil (Barra, Deodoro, and Porto), equidistant ~25 km each other. Aedes aegypti mosquitoes were classified into infected (a single oral challenge with ZIKV) and superinfected (two ZIKV-infected blood meals spaced by 7 days each other). ZIKV infection reduced Ae. aegypti survival in two of the three populations tested, and superinfection produced a sharper increase in mortality in one of those populations. We hypothesized higher mortality with the presence of more ZIKV copies in Ae. aegypti females from Porto. The number of eggs laid per clutch was statistically similar between vector populations and infected and uninfected mosquitoes. Infection by ZIKV not affected female oviposition success. ZIKV infection impacted Ae. aegypti vectorial capacity by reducing its lifespan, although female fecundity remained unaltered. The outcome of these findings to disease transmission intensity still needs further evaluation.
| S-EPMC6305470 | biostudies-literature
Project description:Mosquito-borne helminth infections are responsible for a significant worldwide disease burden in both humans and animals. Accordingly, development of novel strategies to reduce disease transmission by targeting these pathogens in the vector are of paramount importance. We found that a strain of Aedes aegypti that is refractory to infection by Dirofilaria immitis, the agent of canine heartworm disease, mounts a stronger immune response during infection than does a susceptible strain. Moreover, activation of the Toll immune signaling pathway in the susceptible strain arrests larval development of the parasite, thereby decreasing the number of transmission-stage larvae. Notably, this strategy also blocks transmission-stage Brugia malayi, an agent of human lymphatic filariasis. Our data show that mosquito immunity can play a pivotal role in restricting filarial nematode development and suggest that genetically engineering mosquitoes with enhanced immunity will help reduce pathogen transmission.
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