Exosomal miR-224 contributes to hemolymph microbiota homeostasis during bacterial infection in crustacean

Gong, Yi; Wei, Xiaoyuan; Sun, Wanwei; Ren, Xin; Chen, Jiao; Aweya, Jude Juventus; Ma, Hongyu; Chan, Kok‐Gan; Zhang, Yueling; Li, Shengkang

doi:10.1371/journal.ppat.1009837

Cited by 22 publications

(11 citation statements)

References 52 publications

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“…To date, there are only a few reports on the function of ECSIT gene in invertebrates, namely, two shrimp ECSITs from M. japonicus and Exopalaemon carinicauda (26,47), one mollusk ECSIT from Crassostrea hongkongensis (48), one mud crab ECSIT from Scylla paramamosain, and one Drosophila ECSIT (32,49). Our previous research and the data in this article showed that shrimp ECSIT was necessary for antibacterial signal transduction from MjToll3 to Dorsal.…”

Section: Discussionmentioning

confidence: 68%

“…Additionally, ECSIT was also located in the mitochondrial complex I, and implicated in complex stability and mitochondrial and cellular reactive oxygen species production during bacterial infection, thus contributing to the bactericidal activity of macrophages (52). In arthropods, the interaction of TRAF6 with ECSIT and their role in regulating the expression of AMPs are reported in Drosophila and mud crab (32,49). However, the functional connection of ECSIT and Toll receptors is still unclear.…”

Section: Discussionmentioning

confidence: 99%

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The ECSIT Mediated Toll3-Dorsal-ALFs Pathway Inhibits Bacterial Amplification in Kuruma Shrimp

et al. 2022

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The Toll signaling pathway plays an important role in animal innate immunity. However, its activation and signal transmission greatly differ across species and need to be investigated. Shrimp farming is a worldwide economic activity affected by bacterial disease from the 1990s, which promoted research on shrimp immunity. In this study, we first proved that, among the three identified Toll receptors in Marsupenaeus japonicus kuruma shrimp, Toll 3 plays a pivotal role in initiating the antibacterial response in vivo, especially upon anti-Staphylococcus aureus infection. Further research showed that this result was due to the activation of the Dorsal transcription factor, which induced the expression of two anti-lipopolysaccharide factors (Alfs). Moreover, the evolutionarily conserved signaling intermediate in Toll pathways, ECSIT, was proved to be needed for signal transmission from Toll 3 to Dorsal and the expression of anti-lipopolysaccharide factors. Finally, the mortality assay showed that a Toll3-ECSIT-Dorsal-Alf axis was functional in the anti-S.aureus immunity of M. japonicus shrimp. The results provide new insights into the function and signal transduction of the Toll pathway in aquatic species and offer basic knowledge for shrimp disease control and genetic breeding.

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Section: Discussionmentioning

confidence: 68%

Section: Discussionmentioning

confidence: 99%

The ECSIT Mediated Toll3-Dorsal-ALFs Pathway Inhibits Bacterial Amplification in Kuruma Shrimp

et al. 2022

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“…Crustacean seems possess less phagocytic cells compared with other species, which may be due to its unique endosymbiosis with microbes in its hemolymph, which has been partially unveiled by recent studies (Gong et al, 2021;Zheng et al, 2021) Crustacean hemocytes have been classified into hyalinocytes, semi-granulocytes and granulocytes based on morphology and function for the past decades (Soderhall, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…In human, most of myeloid cells including monocyte, macrophage, dendritic cell, and neutrophil could engulf pathogens(Bassler et al, 2019). Crustacean seems possess less phagocytic cells compared with other species, which may be due to its unique endosymbiosis with microbes in its hemolymph, which has been partially unveiled by recent studies(Gong et al, 2021; Zheng et al, 2021)…”

Section: Discussionmentioning

confidence: 99%

Myeloid cell evolution uncovered by shrimp immune cell analysis at single-cell resolution

Peng

Chen

Huang

et al. 2022

Preprint

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How myeloid cells evolved from invertebrate to vertebrate is still a mystery. Here we collected circulating hemocytes from a marine invertebrate-Penaeus vannamei via gradient centrifugation and identified prohemocyte, monocytic hemocyte and granulocyte as three major types of cells in shrimp hemolymph by single-cell mRNA sequencing. Additional pseudotime trajectory analysis revealed that shrimp monocytic hemocytes and granulocytes were differentiated from a common progenitor which was similar with that of human myeloid cells. More interestingly, we identified that MH2, a terminal differentiated monocytic hemocyte, was a macrophage-like phagocytic cell which could engulf fluorescein labelled Vibrio parahaemolyticus and shared nine marker genes including inflammasome components Nlrp3 and Casp1 with human macrophage. After that, we compared our classification with traditional shrimp hemocytes classification and found that hyalinocyte included both prohemocyte and monocytic hemocyte while semi-granulocyte included both monocytic hemocyte and granulocyte. In general, our results redefine shrimp hemocyte classification based on functional marker genes and unveil evolutionary trace of myeloid cells in marine invertebrate.

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“…Drosophila Schneider 2 (S2) cells (Invitrogen), a cell line that is widely used in marine invertebrate-related research ( 57 , 58 ), were cultured at 27°C in Express Five serum-free medium (SFM) (Invitrogen). Then, the constructed pIZ/V5 plasmid combinations bearing a Flag or HA tag were cotransfected into S2 cells using the Cellfectin II reagent (Invitrogen, USA).…”

Section: Methodsmentioning

confidence: 99%

p53 Ubiquitination Comediated by HUWE1 and TRAF6 Contributes to White Spot Syndrome Virus Infection in Crustacean

Gong

Kong

Aweya

et al. 2022

J Virol

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p53, the guardian of the genome, is a short-lived protein that is tightly controlled at low levels by constant ubiquitination and proteasomal degradation in higher organisms. p53 stabilization and activation are early crucial events to cope with external stimuli in cells. However, the role of p53 ubiquitination and its relevant molecular mechanisms have not been addressed in invertebrates. In this study, our findings revealed that both HUWE1 (HECT, UBA, and WWE domain-containing E3 ubiquitin-protein ligase 1) and TRAF6 (TNF receptor associated factor 6) could serve as E3 ubiquitin ligases for p53 in mud crab ( Scylla paramamosain ). Moreover, the expressions of HUWE1 and TRAF6 were significantly down-regulated during WSSV (White spot syndrome virus) infection, and therefore the ubiquitination of p53 was interrupted, leading to the activation of apoptosis and ROS (Reactive oxygen species) signals through p53 accumulation, which eventually suppressed viral invasion in mud crab. To the best of our knowledge, this is the first study to reveal the p53 ubiquitination simultaneously induced by two E3 ligases in arthropods, which provides a novel molecular mechanism of invertebrates in resistance to viral infection. Importance p53, which is a well-known tumor suppressor that has been widely studied in higher animals, has been reported to be tightly controlled at low levels by Ubiquitin-dependent proteasomal degradation. However, the recent p53 ubiquitination-relevant research is mainly involved in an individual E3 ubiquitin ligase, whether there exist other mechanisms that need to be explored. The results of this study showed that HUWE1 and TRAF6 could serve as p53 E3 ubiquitin ligases, and synchronously mediate p53 ubiquitination in mud crab, which confirmed the diversity of the p53 ubiquitination regulatory pathway. In addition, the effects of p53 ubiquitination are mainly focused on tumorigenesis, but few on the host immune defense in invertebrates. Our findings revealed that p53 ubiquitination could affect ROS and apoptosis signals to cope with WSSV infection in mud crab, which firstly clarified the immunologic functions and mechanisms of p53 ubiquitination in invertebrates.

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Exosomal miR-224 contributes to hemolymph microbiota homeostasis during bacterial infection in crustacean

Cited by 22 publications

References 52 publications

The ECSIT Mediated Toll3-Dorsal-ALFs Pathway Inhibits Bacterial Amplification in Kuruma Shrimp

The ECSIT Mediated Toll3-Dorsal-ALFs Pathway Inhibits Bacterial Amplification in Kuruma Shrimp

Myeloid cell evolution uncovered by shrimp immune cell analysis at single-cell resolution

p53 Ubiquitination Comediated by HUWE1 and TRAF6 Contributes to White Spot Syndrome Virus Infection in Crustacean

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