Signaling between mammalian adiponectin and a mosquito adiponectin receptor reduces Plasmodium transmission

Abstract

ABSTRACT When a female mosquito engorges on a mammalian host, components of the blood meal can affect mosquito fitness and indirectly influence pathogen infectivity. We demonstrate that mammalian adiponectin, ingested during Anopheles gambiae blood feeding, co-localizes within mosquito midguts and decreases Plasmodium infection in the vector. Transcriptomic and RNAi studies reveal that the A. gambiae adiponectin receptor is involved in downregulating lipophorin, a lipid transporter that is important for egg development and Plasmodium infection in mosquitoes. These studies characterize a cross-phyla interaction between the mammalian host and A. gambiae that negatively impacts Plasmodium survival in its arthropod vector. IMPORTANCE When a female mosquito takes a blood meal from a mammalian host, components of the blood meal can affect mosquito fitness and indirectly influence pathogen infectivity. We identified a pathway involving an Anopheles gambiae adiponectin receptor, which, triggered by adiponectin from an incoming blood meal, decreases Plasmodium infection in the mosquito. Activation of this pathway negatively regulates lipophorin expression, an important lipid transporter that both enhances egg development and Plasmodium infection. This is an unrecognized cross-phyla interaction between a mosquito and its vertebrate host. These processes are critical to understanding the complex life cycle of mosquitoes and Plasmodium following a blood meal and may be applicable to other hematophagous arthropods and vector-borne infectious agents.