Shrimp STAT was hijacked by white spot syndrome virus immediate-early protein IE1 involved in modulation of viral genes

Yao, Defu; Ruan, Lingwei; Lu, Huasong; Shi, Hong; Xu, Xun

doi:10.1016/j.fsi.2016.10.051

Cited by 37 publications

(18 citation statements)

References 30 publications

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“…Unlike the potential up-regulation of STAT gene expressions in the early WSSV post-infection time points associated with previously described hijacking mechanism adapted by WSSV for viral replication [35], the MrST gene expressions were down-regulated in the early WSSV post-infection time points (Fig 1) of this study. This infers that MrST was negatively regulated during initial WSSV infection for viral hijacking prevention.…”

Section: Differential Gene Expression Pattern Of Mrst and Pmst During Wssv And V Parahaemolyticus/vp Ahpnd Infectionscontrasting

confidence: 85%

“…For example, M. nipponense had no significant STAT gene expression changes after Aeromonas hydrophila [33] and non-O1 Vibrio cholerae [34] bacterial infections. Interestingly, due to the immune signalling importance of STAT gene, there exists risk of shrimp STAT manipulation by the invading pathogens as demonstrated by the shrimp STAT hijacking by WSSV virus [35].…”

Section: Introductionmentioning

confidence: 99%

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Differential STAT gene expressions of Penaeus monodon and Macrobrachium rosenbergii in response to white spot syndrome virus (WSSV) and bacterial infections: Additional insight into genetic variations and transcriptomic highlights

Soo

Bhassu

2021

PLoS ONE

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Diseases have remained the major issue for shrimp aquaculture industry for decades by which different shrimp species demonstrated alternative disease resistance or tolerance. However, there had been insufficient studies on the underlying host mechanisms of such phenomenon. Hence, in this study, the main objective involves gaining a deeper understanding into the functional importance of shrimp STAT gene from the aspects of expression, sequence, structure, and associated genes. STAT gene was selected primarily because of its vital signalling roles in stress, endocrine, and immune response. The differential gene expressions of Macrobrachium rosenbergii STAT (MrST) and Penaeus monodon STAT (PmST) under White Spot Syndrome Virus (WSSV) and Vibrio parahaemolyticus/VpAHPND infections were identified through qPCR analysis. Notably, during both pathogenic infections, MrST demonstrated significant gene expression down-regulations (during either early or later post-infection time points) whereas PmST showed only significant gene expression up-regulations. Important sequence conservation or divergence was highlighted through STAT sequence comparison especially amino acid alterations at 614 aa [K (Lysine) to E (Glutamic Acid)] and 629 aa [F (Phenylalanine) to V (Valine)] from PmST (AY327491.1) to PmST (disease tolerant strain). There were significant differences observed between in silico characterized structures of MrST and PmST proteins. Important functional differentially expressed genes (DEGs) in the aspects of stress, endocrine, immune, signalling, and structural were uncovered through comparative transcriptomic analysis. The DEGs associated with STAT functioning were identified including inositol 1,4,5-trisphosphate receptor, hsp90, caspase, ATP binding cassette transmembrane transporter, C-type Lectin, HMGB, ALF1, ALF3, superoxide dismutase, glutathione peroxidase, catalase, and TBK1. The main findings of this study are STAT differential gene expression patterns, sequence divergence, structural differences, and associated functional DEGs. These findings can be further utilized for shrimp health or host response diagnostic studies. STAT gene can also be proposed as a suitable candidate for future studies of shrimp innate immune enhancement.

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Section: Differential Gene Expression Pattern Of Mrst and Pmst During Wssv And V Parahaemolyticus/vp Ahpnd Infectionscontrasting

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Differential STAT gene expressions of Penaeus monodon and Macrobrachium rosenbergii in response to white spot syndrome virus (WSSV) and bacterial infections: Additional insight into genetic variations and transcriptomic highlights

Soo

Bhassu

2021

PLoS ONE

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“…As observed above, the LvMKK4-LvJNK-Lvc-Jun cascade was activated at a very early stage of WSSV infection, as illustrated by the increased phosphorylation ratio of LvJNK and Lvc-Jun at 8 hpi (Figures 1D, 1F, and 1G). c-Jun is a transcription factor of the AP-1 family, and the transcription of WSSV IE genes, which are independent of de novo viral protein synthesis, are often driven directly by host transcription factors (Huang et al., 2010, Qiu et al., 2014, Yao et al., 2016). Thus, it is easy to speculate that Lvc-Jun could be hijacked by the WSSV to promote expression of its own genes, such as IE1 .…”

Section: Resultsmentioning

confidence: 99%

“…Another study also showed that in the shrimp Penaeus monodon the thioredoxin protein PmTrx, an important redox regulator, was able to bind to IE1 and restore its DNA-binding activity under oxidizing conditions, indicating a role for IE1 in WSSV pathogenicity (Huang et al., 2012). In addition, WSSV infection was shown to activate several host signaling pathways, and the host transcription factors of these signaling pathways, such as STAT, NF-κB, and AP-1, enhanced the transcription of IE1 (Huang et al., 2010, Yao et al., 2015, Yao et al., 2016). However, the actual mechanism by which the WSSV regulates the activation of the host immune system for its own replication is unknown.…”

Section: Introductionmentioning

confidence: 99%

White Spot Syndrome Virus Establishes a Novel IE1/JNK/c-Jun Positive Feedback Loop to Drive Replication

Wang

Weng

et al. 2020

iScience

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SummaryViruses need to hijack and manipulate host proteins to guarantee their replication. Herein, we uncovered that the DNA virus white spot syndrome virus (WSSV) established a novel positive feedback loop by hijacking the host JNK pathway via its immediate-early 1 (IE1) protein to drive replication. Specifically, the WSSV IE1 bound to host JNK, and enhanced JNK autoactivation by autophosphorylation, and in turn, elevated JNK kinase activity to its substrate c-Jun and induced IE1, which resulted in a viral gene-mediated positive feedback loop. Moreover, the activation of this loop is able to induce wsv056, wsv249, and wsv403, in addition to IE1 itself. Disruption of this loop during WSSV infection by knockdown of JNK, c-Jun or IE1 led to an increased survival rate and lower viral burdens in shrimp. Taken together, this loop may provide a potential target for the development of specific antiviral strategies or agents against WSSV infection.

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“…To this end, the virus hijacks host proteins to facilitate gene transcription. Shrimp NF-kB and STAT were reported to bind the promoter of the WSSV immediate early gene ie1, promoting its expression (11)(12)(13). Viral transcription factor IE1 then drives host JNK autophosphorylation to activate c-Jun and stimulate ie1, wsv056, wsv249, as well as wsv403 expression (14).…”

Section: Introductionmentioning

confidence: 99%

Phosphorylation of Shrimp Tcf by a Viral Protein Kinase WSV083 Suppresses Its Antiviral Effect

et al. 2021

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Nuclear DNA-binding TCF proteins, which act as the main downstream effectors of Wnt signaling, are essential for the regulation of cell fate and innate immunity. However, their role during viral infection in shrimp remains unknown. Herein, we demonstrated that Litopenaeus vannamei TCF (LvTcf) acts independently of Lvβ-catenin to promote interferon-like protein LvVago1 production, thus mounting the response to WSSV infection. Further, we observed that WSV083, a WSSV serine/threonine protein kinase, bound to LvTcf and phosphorylated it. Phosphorylated LvTcf was then recognized and degraded via the ubiquitin-proteasome pathway. Moreover, mass spectrometry analyses indicated that the T39 and T104 residues of LvTcf were target sites phosphorylated by WSV083. Point mutation analyses suggested that additional sites of LvTcf may undergo phosphorylation via WSV083. Taken together, the current work provides valuable insights into host immunity and viral pathogenesis. LvTcf is not only a modulator of shrimp innate immunity but is also an important target for WSSV immune evasion. Thus, the current findings will help improve disease control in shrimps.

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Shrimp STAT was hijacked by white spot syndrome virus immediate-early protein IE1 involved in modulation of viral genes

Cited by 37 publications

References 30 publications

Differential STAT gene expressions of Penaeus monodon and Macrobrachium rosenbergii in response to white spot syndrome virus (WSSV) and bacterial infections: Additional insight into genetic variations and transcriptomic highlights

Differential STAT gene expressions of Penaeus monodon and Macrobrachium rosenbergii in response to white spot syndrome virus (WSSV) and bacterial infections: Additional insight into genetic variations and transcriptomic highlights

White Spot Syndrome Virus Establishes a Novel IE1/JNK/c-Jun Positive Feedback Loop to Drive Replication

Phosphorylation of Shrimp Tcf by a Viral Protein Kinase WSV083 Suppresses Its Antiviral Effect

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