Transcriptome analysis provides insights into molecular immune mechanisms of rabbitfish, Siganus oramin against Cryptocaryon irritans infection

Jiang, Biao; Du, Jiang; Li, Yanwei; Ma, Pan; Hu, Yazhou; Li, An‐Xing

doi:10.1016/j.fsi.2019.02.039

Cited by 20 publications

(7 citation statements)

References 40 publications

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“…Knockout and mutation of tap1 and tap2 significantly reduce the number of MHCI complexes, which results in autoimmune disorder and susceptibility to infections ( 66 , 68 ), indicating that timely shipment of antigens to CTLs via TAPs is crucial in preserving the normal functions of the immune system. Previous studies on infected skin of orange spotted grouper ( 12 ) and rabbitfish ( 13 ) showed that tap1 , tap2 , mhci and cd209 were upregulated in infected samples, suggesting that more antigens were displayed to CTLs through increased expression of taps in the defence against pathogens. In zebrafish, cd209 blockade inhibits T cell activation ( 69 ).…”

Section: Discussionmentioning

confidence: 99%

“…So far, lots of fish skin transcription profiles for various species have been obtained including orange-spotted grouper ( Epinephelus coioides ) ( 12 ), rabbitfish ( Siganus oramin ) ( 13 ), yellow croaker ( Larimichthys crocea ) ( 14 ), zebrafish ( 15 ) and rainbow trout ( 6 ). These studies showed that numerous immune-related genes were upregulated upon infection with various pathogens, as is the case for Toll-like receptors ( tlrs ), NOD-like receptors ( nlrs ), janus kinases ( jaks ), transporter ( tap ), signal transducer and activator of transcriptions ( stats ) and interferon regulatory factor 3 ( irf3 ), implying that resistance to stress is proportional to the expression levels of certain immune-related genes.…”

Section: Introductionmentioning

confidence: 99%

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Integrated Analysis of lncRNA and circRNA Mediated ceRNA Regulatory Networks in Skin Reveals Innate Immunity Differences Between Wild-Type and Yellow Mutant Rainbow Trout (Oncorhynchus mykiss)

Huang

et al. 2022

Front. Immunol.

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Fish skin is a vital immune organ that forms the first protective barrier preventing entry of external pathogens. Rainbow trout is an important aquaculture fish species that is farmed worldwide. However, our knowledge of innate immunity differences between wild-type (WR_S) and yellow mutant rainbow trout (YR_S) remains limited. In this study, we performed whole transcriptome analysis of skin from WR_S and YR_S cultured in a natural flowing water pond. A total of 2448 mRNAs, 1630 lncRNAs, 22 circRNAs and 50 miRNAs were found to be differentially expressed (DE). Among these DEmRNAs, numerous key immune-related genes, including ifih1, dhx58, trim25, atp6v1e1, tap1, tap2, cd209, hsp90a.1, nlrp3, nlrc3, and several other genes associated with metabolism (gstp1, nampt, naprt and cd38) were identified. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses of DEmRNAs revealed that many were significantly enriched in innate immune-related GO terms and pathways, including NAD+ADP-ribosyltransferase activity, complement binding, immune response and response to bacterium GO terms, and RIG-I-like receptor signaling, NOD-like receptor signaling and phagosome KEGG pathways. Furthermore, the immune-related competing endogenous RNA networks were constructed, from which we found that lncRNAs MSTRG.11484.2, MSTRG.32014.1 and MSTRG.29012.1 regulated at least three immune-related genes (ifih1, dhx58 and irf3) through PC-5p-43254_34, PC-3p-28352_70 and bta-miR-11987_L-1R-1_1ss8TA, and tap2 was regulated by two circRNAs (circRNA5279 and circRNA5277) by oni-mir-124a-2-p5_1ss13GA. The findings expand our understanding of the innate immune system of rainbow trout, and lay the foundation for further study of immune mechanisms and disease resistance breeding.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Integrated Analysis of lncRNA and circRNA Mediated ceRNA Regulatory Networks in Skin Reveals Innate Immunity Differences Between Wild-Type and Yellow Mutant Rainbow Trout (Oncorhynchus mykiss)

Huang

et al. 2022

Front. Immunol.

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“…Transcriptomic analysis, involving a microarray enriched in immune genes, of spleen, kidney and liver of turbot infected with P. dicentrarchi , revealed strong up-regulation of many immune response genes [ 22 , 23 ] at 1 dpi, but a less intense response than observed in turbot peritoneal cavity in the present study. Sampling times after experimental infection with ciliates were 12 h [ 88 ], 24 h [ 25 ] or 3 dpi [ 24 ] in fish infected experimentally with C. irritans . In the ectoparasite I. multifiliis , sampling was conducted 2 dpi [ 61 ] or 8 dpi [ 27 ].…”

Section: Discussionmentioning

confidence: 99%

Interactions between the Parasite Philasterides dicentrarchi and the Immune System of the Turbot Scophthalmus maximus. A Transcriptomic Analysis

Valle

Leiro

Pereiro

et al. 2020

Biology

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The present study analyses the interactions between Philasterides dicentrarchi (a ciliate parasite that causes high mortalities in cultured flatfish) and the peritoneal cells of the turbot Scophthalmus maximus during an experimental infection. The transcriptomic response was evaluated in the parasites and in the fish peritoneal cells, at 1, 2 and 4 h post-infection (hpi) in turbot injected intraperitoneally (ip) with 107 ciliates and at 12 and 48 hpi in turbot injected ip with 105 ciliates. Numerous genes were differentially expressed (DE) in P. dicentrarchi, relative to their expression in control ciliates (0 hpi): 407 (369 were up-regulated) at 1 hpi, 769 (415 were up-regulated) at 2 hpi and 507 (119 were up-regulated) at 4 hpi. Gene ontology (GO) analysis of the DE genes showed that the most representative categories of biological processes affected at 1, 2 and 4 hpi were biosynthetic processes, catabolic processes, biogenesis, proteolysis and transmembrane transport. Twelve genes of the ABC transporter family and eight genes of the leishmanolysin family were DE at 1, 2 and 4 hpi. Most of these genes were strongly up-regulated (UR), suggesting that they are involved in P. dicentrarchi infection. A third group of UR genes included several genes related to ribosome biogenesis, DNA transcription and RNA translation. However, expression of tubulins and tubulin associated proteins, such as kinesins or dyneins, which play key roles in ciliate division and movement, was down-regulated (DR). Similarly, genes that coded for lysosomal proteins or that participate in the cell cycle mitotic control, glycolysis, the Krebs cycle and/or in the electron transport chain were also DR. The transcriptomic analysis also revealed that in contrast to many parasites, which passively evade the host immune system, P. dicentrarchi strongly stimulated turbot peritoneal cells. Many genes related to inflammation were DE in peritoneal cells at 1, 2 and 4 hpi. However, the response was much lower at 12 hpi and almost disappeared completely at 48 hpi in fish that were able to kill P. dicentrarchi during the first few hpi. The genes that were DE at 1, 2 and 4 hpi were mainly related to the apoptotic process, the immune response, the Fc-epsilon receptor signalling pathway, the innate immune response, cell adhesion, cell surface receptors, the NF-kappaB signalling pathway and the MAPK cascade. Expression of toll-like receptors 2, 5 and 13 and of several components of NF-κB, MAPK and JAK/STAT signalling pathways was UR in the turbot peritoneal cells. Genes expressing chemokines and chemokine receptors, genes involved in prostaglandin and leukotriene synthesis, prostaglandins, leukotriene receptors, proinflammatory cytokines and genes involved in apoptosis were strongly UR during the first four hours of infection. However, expression of anti-inflammatory cytokines such as Il-10 and lipoxygenases with anti-inflammatory activity (i.e., arachidonate 15-lipoxygenase) were only UR at 12 and/or 48 hpi, indicating an anti-inflammatory state in these groups of fish. In conclusion, the present study shows the regulation of several genes in P. dicentrarchi during the early stages of infection, some of which probably play important roles in this process. The infection induced a potent acute inflammatory response, and many inflammatory genes were regulated in peritoneal cells, showing that the turbot uses all the protective mechanisms it has available to prevent the entry of the parasite.

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“…Complement components in serum and mucus are crucial to the rapid immune response against invading pathogens, forming a lytic membrane attack complex. Numerous studies have shown that the rapid activation of the complement system upon parasite infection is universal across different teleost species (Hu et al., 2017; Jiang et al., 2019; Yin et al., 2016; Yin & Qian, 2017). The complement cascade is mainly activated through the alternative pathway (Yin et al., 2016; Yin, Liu, Bao, Jin, et al., 2018), in which the antigen from parasites directly activates C3 and subsequently C5‐C9 to form a lytic membrane attack complex without the existence of an antigen–antibody complex (Boshra et al., 2006).…”

Section: Discussionmentioning

confidence: 99%

The gill transcriptome reveals unique antimicrobial features that protect Nibeaalbiflora from Cryptocaryonirritans infection

Xie

Jiang

Miao

et al. 2021

Journal of Fish Diseases

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Cryptocaryonosis is the greatest threat to most teleost species among all parasitic diseases, causing mass loss to the marine aquaculture industry. Epidemiological investigation of teleost susceptibility to Cryptocaryon irritans infection revealed that yellow drum (Nibea albiflora) is highly resistant. In order to further understand the activation of the immune system in the gill, which is one of the main mucosal‐associated lymphoid tissues and a target of parasites, transcriptome analysis of the yellow drum gill was performed. Gill samples were collected from fish challenged after 24 hr and 72 hr with theronts at a median death rate (2050 theronts per gram fish). Gene expression profiles showed that TLR5 was the only receptor that activated the downstream immune response. The infection activated complement cascade through alternative pathway and increased the expression of C5a anaphylatoxin chemotactic receptor 1. In addition, possible antimicrobial molecules, including lipoprotein and haptoglobin, which are responsible for trypanolysis in humans, were among the top significantly upregulated genes at 24 hr. After 72 hr, the expression of secreted immunoglobulin T‐related genes was induced. These results suggested a rapid innate and adaptive immune response at the mucosal level. In conclusion, the results provide new perspectives on mucosal immune resistance in yellow drum against cryptocaryonosis and provide the possibility of mining resistance genes for future therapy.

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Transcriptome analysis provides insights into molecular immune mechanisms of rabbitfish, Siganus oramin against Cryptocaryon irritans infection

Cited by 20 publications

References 40 publications

Integrated Analysis of lncRNA and circRNA Mediated ceRNA Regulatory Networks in Skin Reveals Innate Immunity Differences Between Wild-Type and Yellow Mutant Rainbow Trout (Oncorhynchus mykiss)

Integrated Analysis of lncRNA and circRNA Mediated ceRNA Regulatory Networks in Skin Reveals Innate Immunity Differences Between Wild-Type and Yellow Mutant Rainbow Trout (Oncorhynchus mykiss)

Interactions between the Parasite Philasterides dicentrarchi and the Immune System of the Turbot Scophthalmus maximus. A Transcriptomic Analysis

The gill transcriptome reveals unique antimicrobial features that protect Nibeaalbiflora from Cryptocaryonirritans infection

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