IFN-γ Manipulates NOD1-Mediated Interaction of Autophagy and <i>Edwardsiella piscicida</i> to Augment Intracellular Clearance in Fish

Yin, Licheng; Lv, Mingqi; Qiu, Xingyang; Wang, Xinyan; Zhang, Anying; Yang, Kun; Zhou, Hong

doi:10.4049/jimmunol.2100151

Cited by 10 publications

(5 citation statements)

References 46 publications

(40 reference statements)

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“…Increasing colocalization of A. hydrophila with LC3B puncta in neutrophils was found, and rgcIFN-γ also accelerated the envelopment of bacteria by neutrophil autophagosomes. In fact, previous studies in teleost have reported that rgcIFN-γ promotes monocytes/macrophages autophagy for intracellular E. piscicida clearance [44]. Further involvement of PI3K III and p38 signaling pathways were revealed to mediate rgcIFN-γ-triggered autophagy and drive its bactericidal activity as seen in mammalian macrophages [45].…”

Section: Discussionmentioning

confidence: 94%

IL-12/IFN-γ axis drives skin wound healing via innate defense mechanisms against bacterial invasion in teleost fish

Qiu,

Yang,

Sun

et al. 2023

Preprint

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Objective and design IL-12 is a well-recognized pro-inflammatory cytokine with multi-functions in participating mammalian innate immunity, but little is known regarding the details for protecting skin barrier damage in lower vertebrates. The aim of this study was to evaluate the effects and mechanisms of IL-12 and its key effectors in promoting skin wound repair in teleosts. Material or subjects Recombinant gcIL-12BB (rgcIL-12BB) was employed to investigate IL-12 roles in teleost skin wound healing. Meanwhile, the regulatory effects of rgcIL-12BB on re-epithelialization, inflammation and bacterial clearance at lesion sites were explored. Furthermore, the role of increased IFN-γ and recruited neutrophil in skin wound were uncovered. Finally, the mechanism of neutrophil bacterial clearance triggered by IFN-γ was also elucidated. Results The rgcIL-12BB could promote wound healing, reduce bacterial invasion, and significantly promote epithelial cell proliferation and migration. Moreover, as the main effector of IL-12BB, IFN-γ was observed to exhibit bactericidal activities mainly via recruiting and stimulating autophagic neutrophils in teleosts. In line with findings in mammals, the grass carp guanylate-binding protein 1 (gcGBP1) acts as a downstream effector of the IL-12/IFN-γ axis that interacts with autophagy-related proteins LC3B and P62, which are involved in gcIFN-γ-induced autophagy. Conclusion Collectively, our results highlighted an intrinsic mechanism whereby the IL-12/IFN-γ axis triggers the host's innate defense against bacterial infection, thereby improving skin wound healing in teleosts.

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Section: Discussionmentioning

confidence: 94%

IL-12/IFN-γ axis drives skin wound healing via innate defense mechanisms against bacterial invasion in teleost fish

Qiu,

Yang,

Sun

et al. 2023

Preprint

Self Cite

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“…Noteworthily, crosstalk between glutamine and FoxO elucidated that activation of FoxO3 leads to the accumulation of glutamine, which enforced autophagy beneficial for cellular survival; while suppressed FoxO3-mediated autophagy increased apoptosis [ 55 ]. Appropriate apoptosis and autophagy are essential survival strategies for anti-microbial defense, which are highly engaged in fish anti-pathogen responses [ 57 , 66 , 67 ]. Autophagy also favors homeostasis by removing impaired organelles and self-renewal [ 68 ].…”

Section: Discussionmentioning

confidence: 99%

Integrated Analysis of Transcriptome and Metabolome Reveals Distinct Responses of Pelteobagrus fulvidraco against Aeromonas veronii Infection at Invaded and Recovering Stage

Ning

Peng

Tang

et al. 2022

IJMS

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Yellow catfish (Pelteobagrus fulvidraco) is an important aquaculture fish susceptible to Aeromonas veronii infection, which causes acute death resulting in huge economic losses. Understanding the molecular processes of host immune defense is indispensable to disease control. Here, we conducted the integrated and comparative analyses of the transcriptome and metabolome of yellow catfish in response to A. veronii infection at the invaded stage and recovering stage. The crosstalk between A. veronii-induced genes and metabolites uncovered the key biomarkers and pathways that strongest contribute to different response strategies used by yellow catfish at corresponding defense stages. We found that at the A. veronii invading stage, the immune defense was strengthened by synthesizing lipids with energy consumption to repair the skin defense line and accumulate lipid droplets promoting intracellular defense line; triggering an inflammatory response by elevating cytokine IL-6, IL-10 and IL-1β following PAMP-elicited mitochondrial signaling, which was enhanced by ROS produced by impaired mitochondria; and activating apoptosis by up-regulating caspase 3, 7 and 8 and Prostaglandin F1α, meanwhile down-regulating FoxO3 and BCL6. Apoptosis was further potentiated via oxidative stress caused by mitochondrial dysfunction and exceeding inflammatory response. Additionally, cell cycle arrest was observed. At the fish recovering stage, survival strategies including sugar catabolism with D-mannose decreasing; energy generation through the TCA cycle and Oxidative phosphorylation pathways; antioxidant protection by enhancing Glutathione (oxidized), Anserine, and α-ketoglutarate; cell proliferation by inducing Cyclin G2 and CDKN1B; and autophagy initiated by FoxO3, ATG8 and ATP6V1A were highlighted. This study provides a comprehensive picture of yellow catfish coping with A. veronii infection, which adds new insights for deciphering molecular mechanisms underlying fish immunity and developing stage-specific disease control techniques in aquaculture.

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“…Cytokines, including interferons (IFNs), interleukins (ILs), tumor necrosis factors (TNFs), colony-stimulating factors, and chemokines, could stimulate T and B cells and antigen-presenting cells, mediating the communication between innate and acquired immune in fish. In rainbow trout, higher cytokine abundance in the spleen correlated strongly with lower F. psychrophilum loads in challenged fish ( 28 ). In the present study, the transcript levels of il1β1 , il1β2 , il6 , and il8 continuously increased in the spleen of fish postexposure to F. psychrophilum (at D3 and D7), whereas tnf-α was upregulated at D3 and downregulated slightly at D7 ( Figure 7 , Table S5 ).…”

Section: Discussionmentioning

confidence: 99%

Time-course transcriptome analyses of spleen in rainbow trout (Oncorhynchus mykiss) post-Flavobacterium psychrophilum infection

et al. 2022

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Flavobacterium psychrophilum, the etiological agent of bacterial coldwater disease and rainbow trout fry syndrome, causes considerable losses in salmonid aquaculture globally. Systemic F. psychrophilum infections in rainbow trout (Oncorhynchus mykiss) lead to a range of clinical signs, including ulcerative lesions in the skin and muscle and splenitis. Previous studies offered an integrative analysis of the skeletal muscle response to F. psychrophilum infection in rainbow trout. However, little is known about the molecular mechanism of immune response in the spleen, which is an important immune organ of rainbow trout. Here, we investigated the time-course splenic transcriptome profiles in uninfected rainbow trout (CK) and F. psychrophilum–infected rainbow trout at day 3 and day 7 (D3, D7) by RNA-seq analyses. Among the 7,170 differentially expressed genes (DEGs) in the three comparisons (D3 vs. CK, D7 vs. CK, D3 vs. D7), 1,286 DEGs showed consistent upregulation or downregulation at D3 and D7 and were associated with pattern recognition, acute-phase response, complement cascade, chemokine and cytokine signaling, and apoptosis. The Real time quantitative PCR (RT-qPCR) analysis of eight DEGs confirmed the accuracy of the RNA-Sequencing (RNA-seq) data. Our results reflected a general process from pathogen recognition to inflammatory cytokine generation and delineated a putative Toll-like receptor signaling pathway in rainbow trout spleen, following F. psychrophilum infection. Taken together, these results provide new insights into the molecular mechanism of the immune response to F. psychrophilum infection and are a valuable resource for future research on the prevention and control of bacterial coldwater disease during salmon culture.

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IFN-γ Manipulates NOD1-Mediated Interaction of Autophagy and Edwardsiella piscicida to Augment Intracellular Clearance in Fish

Cited by 10 publications

References 46 publications

IL-12/IFN-γ axis drives skin wound healing via innate defense mechanisms against bacterial invasion in teleost fish

IL-12/IFN-γ axis drives skin wound healing via innate defense mechanisms against bacterial invasion in teleost fish

Integrated Analysis of Transcriptome and Metabolome Reveals Distinct Responses of Pelteobagrus fulvidraco against Aeromonas veronii Infection at Invaded and Recovering Stage

Time-course transcriptome analyses of spleen in rainbow trout (Oncorhynchus mykiss) post-Flavobacterium psychrophilum infection

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