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

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2016-01-01
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King, Jonas
Tao, Dingyin
Zekeznik, Oana
Brando, Carla
Thallinger, Gerard
Dinglasan, Rhoel
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Smith, Ryan
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Entomology

The Department of Entomology seeks to teach the study of insects, their life-cycles, and the practicalities in dealing with them, for use in the fields of business, industry, education, and public health. The study of entomology can be applied towards evolution and ecological sciences, and insects’ relationships with other organisms & humans, or towards an agricultural or horticultural focus, focusing more on pest-control and management.

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The Department of Entomology was founded in 1975 as a result of the division of the Department of Zoology and Entomology.

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Abstract

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-feeding, and Plasmodium falciparuminfection promote dramatic shifts in the proteomic profiles of An. gambiaegranulocyte populations. Of interest, large numbers of immune proteins were induced in response to blood feeding alone, suggesting that granulocytes have an integral role in priming the mosquito immune system for pathogen challenge. In addition, we identify several granulocyte proteins with putative roles as membrane receptors, cell signaling, or immune components that when silenced, have either positive or negative effects on malaria parasite survival. Integrating existing hemocyte transcriptional profiles, we also compare differences in hemocyte transcript and protein expression to provide new insight into hemocyte gene regulation and discuss the potential that post-transcriptional regulation may be an important component of hemocyte gene expression. These data represent a significant advancement in mosquito hemocyte biology, providing the first comprehensive proteomic profiling of mosquito phagocytic granulocytes during homeostasis blood-feeding, and pathogen challenge. Together, these findings extend current knowledge to further illustrate the importance of hemocytes in shaping mosquito innate immunity and their principal role in defining malaria parasite survival in the mosquito host.

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Published as Smith, Ryan C., Jonas G. King, Dingyin Tao, Oana A. Zeleznik, Clara Brando, Gerhard G. Thallinger, and Rhoel R. Dinglasan. "Molecular profiling of phagocytic immune cells in Anopheles gambiae reveals integral roles for hemocytes in mosquito innate immunity." Molecular & Cellular Proteomics 15, no. 11 (2016): 3373-3387. doi: 10.1074/mcp.M116.060723

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