The prophenoloxidase system in Drosophila participates in the anti-nematode immune response

Cooper, Dustin; Wuebbolt, Caitlin; Heryanto, Christa; Eleftherianos, Ioannis

doi:10.1016/j.molimm.2019.03.008

Cited by 30 publications

(28 citation statements)

References 37 publications

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“…Previous studies have shown that the species-specific tissue sites of D. immitis and B. malayi larval development can autonomously restrict their development (30,31). Typically, developmental restriction was coincident with larval melanization (10), a process that is important in restricting nematode infections in other insect models (32,33). Our data reveal that activation of Toll and IMD immune pathways in Malpighian tubules is a likely mechanism contributing to this restriction.…”

Section: Discussionsupporting

confidence: 49%

Activation of mosquito immunity blocks the development of transmission-stage filarial nematodes

Edgerton

Mccrea

Berry

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Mosquito-borne helminth infections are responsible for a significant worldwide disease burden in both humans and animals. Accordingly, development of novel strategies to reduce disease transmission by targeting these pathogens in the vector are of paramount importance. We found that a strain of Aedes aegypti that is refractory to infection by Dirofilaria immitis, the agent of canine heartworm disease, mounts a stronger immune response during infection than does a susceptible strain. Moreover, activation of the Toll immune signaling pathway in the susceptible strain arrests larval development of the parasite, thereby decreasing the number of transmission-stage larvae. Notably, this strategy also blocks transmission-stage Brugia malayi, an agent of human lymphatic filariasis. Our data show that mosquito immunity can play a pivotal role in restricting filarial nematode development and suggest that genetically engineering mosquitoes with enhanced immunity will help reduce pathogen transmission.

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Section: Discussionsupporting

confidence: 49%

Activation of mosquito immunity blocks the development of transmission-stage filarial nematodes

Edgerton

Mccrea

Berry

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…Rather, it is dependent upon activation of prophenoloxidase (proPO), which is a proenzyme that is cleaved by prophenoloxidase activating enzyme (PPAE) to its active form phenoloxidase (PO). Phenoloxidase is the catalyst for the oxidation of mono- and diphenols to orthoquinones, which form polymers with melanin non-enzymatically, during which ROS is produced (Cooper et al, 2019; Lemaitre and Hoffmann, 2007). Since the family of FAR proteins is highly conserved among many nematode species it is important to understand whether FARs elicit their immunomodulatory effects in similar ways (Table 1).…”

Section: Discussionmentioning

confidence: 99%

“…Flies were injected with 1,000 CFUs of L. monocytogenes to elicit an immune induced melanization cascade. Phenoloxidase activity was measured as previously described (Binggeli et al, 2014; Cooper et al, 2019). To collect hemolymph, 20-30 flies 4 hours post injection (p.i.)…”

Section: Methodsmentioning

confidence: 99%

Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways

Parks

Nguyen

Nasrolahi

et al. 2021

Preprint

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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 infection, yet little is known about their interactions with host tissues. Leveraging the insect parasitic nematode, Steinernema carpocapsae, we provide the first in vivo study that shows FARs modulate animal immunity, causing an increase in susceptibility to bacterial infection. Next we determined that FARs dampen various aspects of the fly immune response including the phenoloxidase cascade and antimicrobial peptide (AMP) production. Finally, we found 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 a functional immune response. Collectively, these data reveal a complex role for FARs in immunosuppression and provide detailed mechanistic insight into parasitism in phylum Nematoda.

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“…One clotting gene that is most conserved across all organisms is transglutaminase, or factor XIIIa in humans, and has been found to have an anti-nematode effect in Drosophila [16]. In response, EPNs have developed several strategies to overcome immunity and have been reported to secrete peptidases and inhibitors that have specific activity against prophenoloxidases and other clotting genes [35,36]. Other nematode species have developed a protective mechanism against reactive oxygen species from the host [37].…”

Section: Discussionmentioning

confidence: 99%

High-Resolution Infection Kinetics of Entomopathogenic Nematodes Entering Drosophila melanogaster

Dziedziech

Shivankar

Theopold

2020

Insects

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Entomopathogenic nematodes (EPNs) have been a useful model for studying wound healing in insects due to their natural mechanism of entering an insect host either through the cuticle or an orifice. While many experiments have shed light on nematode and host behavior, as well as the host immune response, details regarding early nematode entry and proliferative events have been limited. Using high-resolution microscopy, we provide data on the early infection kinetics of Heterorhabditis bacteriophora and its symbiotic bacteria, Photorhabdus luminescens. EPNs appendage themselves to the host and enter through the host cuticle with a drill-like mechanism while leaving their outer sheath behind. EPNs immediately release their symbiotic bacteria in the host which leads to changes in host behavior and septicemia within 6 h while EPNs travel through the host in a predictable manner, congregating in the anterior end of the host. This paper sheds light on the entry and proliferative events of EPN infection, which will further aid in our understanding of wound healing and host immune activation at a high spatiotemporal resolution.

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The prophenoloxidase system in Drosophila participates in the anti-nematode immune response

Cited by 30 publications

References 37 publications

Activation of mosquito immunity blocks the development of transmission-stage filarial nematodes

Activation of mosquito immunity blocks the development of transmission-stage filarial nematodes

Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways

High-Resolution Infection Kinetics of Entomopathogenic Nematodes Entering Drosophila melanogaster

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