Phurealipids, produced by the entomopathogenic bacteria, Photorhabdus, mimic juvenile hormone to suppress insect immunity and immature development

Ahmed, Shabbir; Hrithik, Md Tafim Hossain; Roy, Miltan Chandra; Bode, Helge B.; Kim, Yonggyun

doi:10.1016/j.jip.2022.107799

Cited by 4 publications

(3 citation statements)

References 29 publications

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“…The role of the CA in E. muscae -induced summiting is consistent with the growing list of examples of parasites exploiting host hormonal axes ( Adamo and Robinson, 2012 ; Beckage, 1997 ; Herbison, 2017 ; Tong et al, 2021 ). The JH pathway, in particular, has been shown to be modulated by a variety of insect parasites, ranging from nematodes to baculoviruses ( Ahmed et al, 2022 ; Jiao et al, 2022 ; Nakai et al, 2016 ; Palli et al, 2000 ; Saito et al, 2015 ; Subrahmanyam and Ramakrishnan, 1980 ; Sun et al, 2019 ; Zhang et al, 2015 ). While there is a clear consensus that JH is involved in a multitude of host physiological and behavioral processes, the extent of JH’s activities in insects is still being uncovered.…”

Section: Discussionmentioning

confidence: 99%

Neural mechanisms of parasite-induced summiting behavior in ‘zombie’ Drosophila

Elya

Lavrentovich

Lee

et al. 2023

eLife

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For at least two centuries, scientists have been enthralled by the 'zombie' behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the recently established Entomophthora muscae-Drosophila melanogaster 'zombie fly' system to reveal the molecular and cellular underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a new, high-throughput behavior assay to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), who are solely responsible for juvenile hormone (JH) synthesis and release. Summiting is a fleeting phenomenon, posing a challenge for physiological and biochemical experiments requiring tissue from summiting flies. We addressed this with a machine learning classifier to identify summiting animals in real time. PI-CA neurons and CA appear to be intact in summiting animals, despite E. muscae cells invading the host brain, particularly in the superior medial protocerebrum (SMP), the neuropil that contains DN1p axons and PI-CA dendrites. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb the fly's hemolymph, activating the neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.

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Section: Discussionmentioning

confidence: 99%

Neural mechanisms of parasite-induced summiting behavior in ‘zombie’ Drosophila

Elya

Lavrentovich

Lee

et al. 2023

eLife

View full text Add to dashboard Cite

show abstract

“…The role of the CA in E. muscae -induced summiting is consistent with the growing list of examples of parasites exploiting host hormonal axes (Adamo and Robinson, 2012; Beckage, 2012; Herbison, 2017; Tong et al, 2021). The JH pathway, in particular, has been shown to be modulated by a variety of insect parasites, ranging from nematodes to baculoviruses (Ahmed et al, 2022; Jiao et al, 2022; Nakai et al, 2016; Palli et al, 2000; Saito et al, 2015; Subrahmanyam and Ramakrishnan, 1980; Sun et al, 2019; Zhang et al, 2015). While there is clear consensus that JH is involved in a multitude of host physiological and behavioral processes, the extent of JH’s activities in insects is still being uncovered.…”

Section: Discussionmentioning

confidence: 99%

Neural mechanisms of parasite-induced summiting behavior in “zombie”Drosophila

Elya

Lavrentovich

Lee

et al. 2022

Preprint

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For at least two centuries, scientists have been enthralled by the zombie behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the recently established Entomophthora muscae-Drosophila melanogaster zombie fly system to reveal the molecular and cellular underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a new, high-throughput behavior assay to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), who are solely responsible for juvenile hormone (JH) synthesis and release. Summiting is a fleeting phenomenon, posing a challenge for physiological and biochemical experiments requiring tissue from summiting flies. We addressed this with a machine learning classifier to identify summiting animals in real time. PI-CA neurons and CA appear to be intact in summiting animals, despite E. muscae cells invading the host brain, particularly in the superior medial protocerebrum (SMP), the neuropil that contains DN1p axons and PI-CA dendrites. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb fly hemolymph, activating the neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.

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“…Phurelipids and juvenoids have a similar molecular structure. Not only did JH and other phurelipids hinder insects' immune responses, but they also prevented pupae from developing into adults [84]. These findings strongly suggest that "CSP" molecules serve a variety of functions in the immune defense system of microbes and arthropods, ranging from the binding of a wide range of exogenous foreign toxic insecticide chemicals to the intracellular transport of endogenous fuel lipids, FAs, and hormones [24,30,31,37,38].…”

Section: Ancestral Functions and Lipoid-binding Propertiesmentioning

confidence: 91%

Renaming ‘Chemosensory’ Proteins (CSPs): ‘Lipoid-Binding Proteins’ — Molecular Nomenclature, Structure, Expression, Evolution, and Intracellular Functions

Liu,

Sun,

Fan

et al. 2024

Preprint

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This is a brief critique of the functions—particularly olfactory functions—specified for the “Chemosensory Protein” (CSPs) molecule family. On the basis of these proteins’ presence in the sensory antennal lymph of locusts, odor chemosensory ligand binding functions have been hypothesized. According to this hypothesis, the entire protein molecule superfamily is referred to as “CSPs”. However, new information and developments in the field of CSP molecular research, such as the expression of CSP genes in the gut, brain, fat body, wings, epidermis, and pheromone gland, as well as gene expression profiling from most early developmental stages—that is, CSP expression well in advance of the appearance of chemical sense nerve cells—strongly suggest that the protein molecule has other roles that are unrelated to chemosensing. Moreover, CSPs are found in bacterial microbial prokaryote organisms in addition to insects and all other arthropods. Thus, we examine the molecule’s name, definition, RNA editing, protein structure, lipid binding properties, DNA interaction, and evolutionary characteristics in brief before referring to this protein family as “Chemosensory Proteins”. As a means of renaming this protein family, this review article discusses the latest findings (“CSP” is attached to the tail of bigger intracellular proteins) and attempts to compel all the data. Because of its highly conserved molecular distinctive feature (four adjacent cysteines), we propose renaming “CSPs” as “4CSPs” (4 Cysteines Soluble Proteins) and use at least for abbreviations for distinctive animal proteins the common peptide 5-letter code, such as “Bommo-4CSPs”.

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Phurealipids, produced by the entomopathogenic bacteria, Photorhabdus, mimic juvenile hormone to suppress insect immunity and immature development

Cited by 4 publications

References 29 publications

Neural mechanisms of parasite-induced summiting behavior in ‘zombie’ Drosophila

Neural mechanisms of parasite-induced summiting behavior in ‘zombie’ Drosophila

Neural mechanisms of parasite-induced summiting behavior in “zombie”Drosophila

Renaming ‘Chemosensory’ Proteins (CSPs): ‘Lipoid-Binding Proteins’ — Molecular Nomenclature, Structure, Expression, Evolution, and Intracellular Functions

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