Dataset Information

Proteogenomic analysis of Anopheles gambiae phagocytic hemocyte populations reveals an anticipatory innate immune response in the absence of pathogen challenge

ABSTRACT: The innate immune response to a broad class of pathogens is highly conserved across all eukaryotes and has been studied in great detail at the cellular and transcriptomic level in several insect species. However, the commensurate cellular proteomic response, especially of hemocytes, the primary immune cell population in insects, has remained poorly understood. We report on the comprehensive proteogenomic analysis of a phagocyte subpopulation from Anopheles gambiae, the primary malaria mosquito vector in Sub-Saharan Africa. We leveraged the innate phagocytic response of mosquito granulocytes to achieve targeted enrichment for these cells to facilitate the examination of their proteomic response profiles following sugar feeding, as well as non-infectious and infectious blood feeding with Plasmodium falciparum. A comparative integrative-OMICs analysis of existing transcriptomic profiles combined with these proteomic data permitted the delineation of the functional genome of anopheline granulocytes. We observed that phagocytosis, blood feeding, and P. falciparum infection induced dramatic shifts in granulocyte protein expression indicative of broad changes in cellular proliferation and innate immune response priming. Importantly, we identified a large number of hemocyte immune proteins that respond to blood feeding alone, suggesting that granulocytes may play an integral role in an anticipatory immune response prior to immune challenge.

INSTRUMENT(S): 6520 Quadrupole Time-of-Flight LC/MS

ORGANISM(S): Anopheles Gambiae (african Malaria Mosquito)

TISSUE(S): Whole Body

DISEASE(S): Plasmodium Falciparum Malaria

SUBMITTER: Dingyin Tao

LAB HEAD: Rhoel R. Dinglasan

PROVIDER: PXD001507 | Pride | 2016-09-26

REPOSITORIES: Pride

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Publications

Molecular Profiling of Phagocytic Immune Cells in Anopheles gambiae Reveals Integral Roles for Hemocytes in Mosquito Innate Immunity.

Smith Ryan C RC King Jonas G JG Tao Dingyin D Zeleznik Oana A OA Brando Clara C Thallinger Gerhard G GG Dinglasan Rhoel R RR

Molecular & cellular proteomics : MCP 20160913 11

The innate immune response is highly conserved across all eukaryotes and has been studied in great detail in several model organisms. Hemocytes, the primary immune cell population in mosquitoes, are important components of the mosquito innate immune response, yet critical aspects of their biology have remained uncharacterized. Using a novel method of enrichment, we isolated phagocytic granulocytes and quantified their proteomes by mass spectrometry. The data demonstrate that phagocytosis, blood- ...[more]

PMID: 27624304

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Project description:A deeper understanding of malaria parasite development inside the Anopheles mosquito may lead to the identification of processes that can be targeted by transmission-blocking interventions. Paraquat (1,1'-dimethyl-4,4'-bipyridylium dichloride) is a potent superoxide-inducing agent that impacts Plasmodium ookinete development, especially at higher concentrations. Compounds like Paraquat can potentially induce an oxidative imbalance in the mosquito midgut during ookinete maturation, essentially super-stressing the parasite leading to the arrested development of ookinetes, the only stage that can invade through a mosquito midgut cell to establish an oocyst infection in the mosquito. The mosquito midgut has evolved to handle the natural production of reactive oxygen and nitrogen species (ROS and RNS, respectively) as a result of feeding on blood. The addition of Paraquat to a bloodmeal is expected to induce a cognate response in the midgut to handle the excess ROS/RNS, and high concentrations of this compound can potentially overwhelm the midgut response leading to mosquito death. While several studies have explored the effect of Paraquat on malaria parasites, a fundamental understanding of the mosquito response to this compound remains unknown. Here, we quantified the mosquito midgut proteomic response to a Paraquat-laced sugar meal to understand the intrinsic midgut response (in the absence of a bloodmeal). We then carried out transcriptomic analysis of the mosquito midgut for several antioxidants of the Trx and GSH pathways to compare concordance or discordance between protein and its transcripts during different oxidative stress conditions. Finally, we determined whether the same Trx and GSH pathways are upregulated following infection with either P. falciparum or P. berghei at 24 hrs post-blood feeding, coinciding with the time point for maximal ookinete traversal of the midgut. We discuss the potential selective action of Paraquat on the parasite and the intrinsic tolerance of the mosquito midgut to Paraquat-mediated oxidative stress.

Dataset Information

Proteogenomic analysis of Anopheles gambiae phagocytic hemocyte populations reveals an anticipatory innate immune response in the absence of pathogen challenge

Publications

Molecular Profiling of Phagocytic Immune Cells in Anopheles gambiae Reveals Integral Roles for Hemocytes in Mosquito Innate Immunity.

Similar Datasets

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