Abstract
Parasitic nematodes cause significant morbidity and mortality globally. Excretory/secretory products (ESPs) such as fatty acid- and retinol- binding proteins (FARs) are hypothesized to suppress host immunity during nematode infection, yet little is known about their interactions with host tissues. Leveraging the insect parasitic nematode, Steinernema carpocapsae, we describe here the first in vivo study demonstrating that FARs modulate animal immunity, causing an increase in susceptibility to bacterial co-infection. Moreover, we show that FARs dampen key components of the fly immune response including the phenoloxidase cascade and antimicrobial peptide (AMP) production. Our data also reveal that FARs deplete lipid signaling precursors in vivo as well as bind to these fatty acids in vitro, suggesting that FARs elicit their immunomodulatory effects by altering the availability of lipid signaling molecules necessary for an efficient immune response. Collectively, these data support a complex role for FARs in immunosuppression in animals and provide detailed mechanistic insight into parasitism in phylum Nematoda.
Highlights
Helminths cause significant morbidity and mortality on a global scale through human disease, sickening of livestock, and a reduction in crop yield [1,2]
Modulation of host biology and the pathology caused by parasitic nematodes is largely effected through the release of proteins and small molecules
We evaluated the presence of fatty acid- and retinol- binding proteins (FARs) in a variety of parasitic nematodes and C. elegans and found a dynamic range of putative FAR-encoding genes among nematode genomes (Table 1)
Summary
Helminths cause significant morbidity and mortality on a global scale through human disease, sickening of livestock, and a reduction in crop yield [1,2]. Parasitic nematodes are responsible for significant human suffering with a striking 1.5 billion people infected with soil-transmitted helminths alone [3]. Protein and small-molecule effectors are crucial for parasites to successfully infect plants, invertebrates, and vertebrate hosts [4,5]. Upon infecting their hosts, nematodes release excretory/secretory products (ESPs) into surrounding tissues, which are the primary point of interaction between the parasite and host and are hypothesized to aid in nematode survival and cause damage to the host. A variety of proteins are found in nematode ESPs, some of which are known to cause tissue damage and modulate host immunity. In C. elegans, FARs are localized in the hypodermis, head and lips which are regularly in contact with the outside environment, as well as the excretory cell connected to the hypodermis [10]
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