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Plasmodium falciparum infection increases Anopheles gambiae attraction to nectar sources and sugar uptake.

ABSTRACT: Plasmodium parasites are known to manipulate the behavior of their vectors so as to enhance transmission. From an evolutionary standpoint, behavior manipulation by the parasite should expose the vector to limited risk of early mortality while ensuring sufficient energy supply for both it and the vector. However, it is unknown whether this vector manipulation also affects vector-plant interaction and sugar uptake. Here, we show that the attraction of Anopheles gambiae s.s. to plant odors increased by 30% and 24% after infection with the oocyst and sporozoite stages of Plasmodium falciparum, respectively, while probing activity increased by 77% and 80%, respectively, when the vectors were infected with the two stages of the parasite. Our data also reveal an increased sugar uptake at the oocyst stage that decreased at the sporozoite stage of infection compared to uninfected An. gambiae, with depletion of lipid reserves at the sporozoite stage. These results point to a possible physiological adjustment by An. gambiae to P. falciparum infection or behavior manipulation of An. gambiae by P. falciparum to enhance transmission. We conclude that the nectar-seeking behavior of P. falciparum-infected An. gambiae appears to be modified in a manner governed by the vector's fight for survival and the parasite's need to advance its transmission.

SUBMITTER: Nyasembe VO

PROVIDER: S-EPMC3935215 | biostudies-literature | 2014 Jan

REPOSITORIES: biostudies-literature

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Plasmodium falciparum infection increases Anopheles gambiae attraction to nectar sources and sugar uptake.

Nyasembe Vincent O VO Teal Peter E A PEA Sawa Patrick P Tumlinson James H JH Borgemeister Christian C Torto Baldwyn B

Current biology : CB 20140109 2

Plasmodium parasites are known to manipulate the behavior of their vectors so as to enhance transmission. From an evolutionary standpoint, behavior manipulation by the parasite should expose the vector to limited risk of early mortality while ensuring sufficient energy supply for both it and the vector. However, it is unknown whether this vector manipulation also affects vector-plant interaction and sugar uptake. Here, we show that the attraction of Anopheles gambiae s.s. to plant odors increase ...[more]

PMID: 24412210

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Project description:Malaria is caused by Plasmodium parasites, which are transmitted via the bites of infected Anopheline mosquitoes. Midgut invasion is a major bottleneck for Plasmodium development inside the mosquito vectors as a rapidly responding immune system recognizes ookinetes and recruits killing factors from the midgut and surrounding tissues, dramatically reducing the population of invading ookinetes before they can successfully traverse the midgut epithelium. Understanding molecular details of the parasite-vector interactions requires precise measurement of nascent protein synthesis in the mosquito during Plasmodium infection. Current expression profiling primarily monitors alterations in steady-state levels of mRNA, but does not address the equally critical issue of whether the proteins encoded by the mRNAs are actually synthesized. In this study, we used sucrose density gradient centrifugation to isolate actively translating Anopheles gambiae mRNAs based upon their association with polyribosomes (polysomes). The proportion of individual gene transcripts associated with polysomes, which is determined by RNA deep sequencing, reflects mRNA translational status. This approach led to identification of 1017 mosquito transcripts that were primarily regulated at the translational level after ingestion of Plasmodium falciparum-infected blood. Caspar, a negative regulator of the NF-kappaB transcription factor Rel2, appears to be substantially activated at the translational levels during Plasmodium infection. In addition, transcripts of Dcr1, Dcr2 and Drosha, which are involved in small RNA biosynthesis, exhibited enhanced associations with polysomes after P. falciparum challenge. This observation suggests that mosquito microRNAs may play an important role in reactions against Plasmodium invasion. We analyzed both total cellular mRNAs and mRNAs that are associated with polysomes to simultaneously monitor transcriptomes and nascent protein synthesis in the mosquito. This approach provides more accurate information regarding the rate of protein synthesis, and identifies some mosquito factors that might have gone unrecognized because expression of these proteins is regulated mainly at the translational level rather than at the transcriptional level after mosquitoes ingest a Plasmodium-infected blood meal.

Project description:The mosquito Anopheles gambiae uses its innate immune system to control bacterial and Plasmodium infection of its midgut tissue. The activation of potent IMD pathway-mediated anti-Plasmodium falciparum defenses is dependent on the presence of the midgut microbiota, which activate this defense system upon parasite infection through a peptidoglycan recognition protein, PGRPLC. We employed transcriptomic and reverse genetic analyses to compare the P. falciparum infection-responsive transcriptomes of septic and aseptic mosquitoes and to determine whether bacteria-independent anti-Plasmodium defenses exist. To examine the impact of P. falciparum infection on the mosquito midgut and carcass transcriptomes in the presence or absence of midgut bacteria, we used A. gambiae whole genome microarrays to compare the mRNA abundance of P. falciparum-infected and -naïve mosquitoes of antibiotic- and non-antibiotic treated cohorts. P. falciparum infection induced changes in the abundance of as many as 2,183 and 2,429 transcripts in whole mosquitoes belonging to a variety of functional groups in aseptic and septic mosquitoes. Ultimately, we were interested in identifying the genes involved in bacteria-independent anti-Plasmodium responses, and therefore we focused on transcripts displaying increased abundance in the parasite-infected aseptic midguts, placing a particular emphasis on those with predicted immune functions. Because of the central role of serine protease cascades in regulating insect immune defenses, we focused the remainder of our analysis on a clip-domain serine protease C2 (CLIPC2, AGAP004317) and a serine protease inhibitor 7 (SRPN7, AGAP007693) that were specifically upregulated in the parasite-infected, aseptic mosquito midgut. We showed that SRPN7 negatively and CLIPC2 positively regulate the anti-Plasmodium defense, independently of the midgut-associated bacteria. Co-silencing assays suggested that these two genes may function together in a signaling cascade. Neither gene was regulated, nor modulated, by infection with the rodent malaria parasite Plasmodium berghei, suggesting that SRPN7 and CLIPC2 are components of a defense system with preferential activity towards P. falciparum. Further analysis using RNA interference determined that these genes do not regulate the anti-Plasmodium defense mediated by the IMD pathway, and both factors act as agonists of the endogenous midgut microbiota, further demonstrating the lack of functional relatedness between these genes and the bacteria-dependent activation of the IMD pathway. This is the first study confirming the existence of a bacteria-independent, anti-P. falciparum defense.

Dataset Information

Plasmodium falciparum infection increases Anopheles gambiae attraction to nectar sources and sugar uptake.

Publications

Plasmodium falciparum infection increases Anopheles gambiae attraction to nectar sources and sugar uptake.

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