Molecular profiling of phagocytic immune cells in anopheles gambiae reveals integral roles for hemocytes in mosquito innate immunity

Ryan C. Smith, Jonas G. King, Dingyin Tao, Oana A. Zeleznik, Clara Brando, Gerhard G. Thallinger, Rhoel R. Dinglasan

Research output: Contribution to journalArticle

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 falciparum infection promote dramatic shifts in the proteomic profiles of An. gambiae granulocyte 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.

Original languageEnglish (US)
Pages (from-to)3373-3387
Number of pages15
JournalMolecular and Cellular Proteomics
Volume15
Issue number11
DOIs
StatePublished - Nov 1 2016
Externally publishedYes

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Anopheles gambiae
Hemocytes
Phagocytes
Culicidae
Innate Immunity
Blood
Pathogens
Granulocytes
Gene expression
Cell signaling
Proteins
Malaria
Immune system
Proteome
Mass spectrometry
Proteomics
Cells
Parasites
Membranes
Plasmodium falciparum

ASJC Scopus subject areas

  • Analytical Chemistry
  • Biochemistry
  • Molecular Biology

Cite this

Molecular profiling of phagocytic immune cells in anopheles gambiae reveals integral roles for hemocytes in mosquito innate immunity. / Smith, Ryan C.; King, Jonas G.; Tao, Dingyin; Zeleznik, Oana A.; Brando, Clara; Thallinger, Gerhard G.; Dinglasan, Rhoel R.

In: Molecular and Cellular Proteomics, Vol. 15, No. 11, 01.11.2016, p. 3373-3387.

Research output: Contribution to journalArticle

Smith, Ryan C. ; King, Jonas G. ; Tao, Dingyin ; Zeleznik, Oana A. ; Brando, Clara ; Thallinger, Gerhard G. ; Dinglasan, Rhoel R. / Molecular profiling of phagocytic immune cells in anopheles gambiae reveals integral roles for hemocytes in mosquito innate immunity. In: Molecular and Cellular Proteomics. 2016 ; Vol. 15, No. 11. pp. 3373-3387.
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