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Abstract
All vector mosquito species must feed on the blood of a vertebrate host to produce eggs. Multiple cycles of blood feeding also promote frequent contacts with hosts, which enhance the risk of exposure to infectious agents and disease transmission. Blood feeding triggers the release of insulin-like peptides (ILPs) from the brain of the mosquito Aedes aegypti, which regulate blood meal digestion and egg formation. In turn, hemocytes serve as the most important constitutive defense in mosquitoes against pathogens that enter the hemocoel. Prior studies indicated that blood feeding stimulates hemocytes to increase in abundance, but how this increase in abundance is regulated is unknown. Here, we determined that phagocytic granulocytes and oenocytoids express the A. aegypti insulin receptor (AaMIR). We then showed that: 1) decapitation of mosquitoes after blood feeding inhibited hemocyte proliferation, 2) a single dose of insulin-like peptide 3 (ILP3) sufficient to stimulate egg production rescued proliferation, and 3) knockdown of the AaMIR inhibited ILP3 rescue activity. Infection studies indicated that increased hemocyte abundance enhanced clearance of the bacterium Escherichia coli at lower levels of infection. Surprisingly, however, non-blood fed females better survived intermediate and high levels of E. coli infection than blood fed females. Taken together, our results reveal a previously unrecognized role for the insulin signaling pathway in regulating hemocyte proliferation. Our results also indicate that blood feeding enhances resistance to E. coli at lower levels of infection but reduces tolerance at higher levels of infection.
Highlights
Insects primarily rely on an innate immune system for defense against pathogens and other foreign invaders
We have found that insulin-like peptides enhance production of immune cells that serve as the first line of defense against infection
Our results show that loss of signaling from the mosquito brain after blood feeding inhibits the increase in hemocyte abundance that occurs after a blood meal while a single dose of insulin peptide 3 (ILP3), sufficient to stimulate egg development, rescues hemocyte proliferation
Summary
Insects primarily rely on an innate immune system for defense against pathogens and other foreign invaders. ILPs from the brain together with nutrient sensing through the target of rapamycin (TOR) pathway induce the midgut to produce enzymes that digest the protein-rich blood meal into amino acids. These amino acids are transported from the midgut into the hemolymph where they are taken up by the fat body [4,5,6]. ECDs and ILPs together induce the fat body to produce vitellogenin (Vg) and other yolk proteins (YP) [7,8], which are packaged into eggs that the female lays between 72 and 96 h post-blood meal (pbm). Pathogens in a blood meal infect mosquitoes during this same period by moving across the midgut, disseminating through the hemocoel, and invading other organs like the salivary glands or fat body
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