Identification of a JAK/STAT pathway receptor domeless from Pacific white shrimp Litopenaeus vannamei

Yan, Muting; Li, Chaozheng; Su, Ziqi; Liang, Qianhui; Li, Haoyang; ShiZhong, Liang; Weng, Shaoping; He, Jianguo; Xu, Xiaopeng

doi:10.1016/j.fsi.2015.01.023

Cited by 52 publications

(19 citation statements)

References 38 publications

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“…In mammals, STAT5 participates in the regulation of a wide range of physiological processes of the cell, including proliferation, differentiation, survival, apoptosis, and others [ 42 , 43 ]. A single receptor domeless (Dome), which shares functional and sequence similarity with the mammalian cytokine class I receptors, has been identified in Litopenaeus vannamei [ 44 ]. A JAK has also been reported in L .…”

Section: Discussionmentioning

confidence: 99%

“…vannamei [ 45 ]. Unlike the antiviral function of the JAK/STAT pathway in mammals and insects, white spot syndrome virus (WSSV) uses a shrimp STAT as a transcription factor to enhance viral gene expression in host cells [ 46 ], and the pathway is helpful and beneficial for WSSV replication [ 44 , 47 ]. However, another report has shown that silencing of the shrimp JAK causes higher mortality and increased viral load in L .…”

Section: Discussionmentioning

confidence: 99%

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Binding of a C-type lectin’s coiled-coil domain to the Domeless receptor directly activates the JAK/STAT pathway in the shrimp immune response to bacterial infection

et al. 2017

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C-type lectins (CTLs) are characterized by the presence of a C-type carbohydrate recognition domain (CTLD) that by recognizing microbial glycans, is responsible for their roles as pattern recognition receptors in the immune response to bacterial infection. In addition to the CTLD, however, some CTLs display additional domains that can carry out effector functions, such as the collagenous domain of the mannose-binding lectin. While in vertebrates, the mechanisms involved in these effector functions have been characterized in considerable detail, in invertebrates they remain poorly understood. In this study, we identified in the kuruma shrimp (Marsupenaeus japonicus) a structurally novel CTL (MjCC-CL) that in addition to the canonical CTLD, contains a coiled-coil domain (CCD) responsible for the effector functions that are key to the shrimp's antibacterial response mediated by antimicrobial peptides (AMPs). By the use of in vitro and in vivo experimental approaches we elucidated the mechanism by which the recognition of bacterial glycans by the CTLD of MjCC-CL leads to activation of the JAK/STAT pathway via interaction of the CCD with the surface receptor Domeless, and upregulation of AMP expression. Thus, our study of the shrimp MjCC-CL revealed a striking functional difference with vertebrates, in which the JAK/STAT pathway is indirectly activated by cell death and stress signals through cytokines or growth factors. Instead, by cross-linking microbial pathogens with the cell surface receptor Domeless, a lectin directly activates the JAK/STAT pathway, which plays a central role in the shrimp antibacterial immune responses by upregulating expression of selected AMPs. Funding: This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 31630084, 31130056 and 31472303). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author summaryThe JAK/STAT pathway mediates the effects of a large number of cytokines and growth factors. It is activated following binding of a cytokine or growth factor to its respective receptor. To date, over 50 cytokines and growth factors have been shown to utilize the pathway to regulate cell growth, survival differentiation, motility, and immune responses. The JAK/ STAT pathway is ubiquitous in vertebrates but can also be found as an intact pathway in some invertebrates, including shrimp. However, few cytokines and growth factors like molecules are identified in invertebrates and the function of the pathway in invertebrates is seldom studied. In this study, we identified core components of JAK/STAT pathway in shrimp and found the pathway had an important function in antibacterial immunity. Bacterial pathogens directly activate the JAK/STAT pathway through a secreted C-type lectin containing a coiled coil domain and a C-type lectin domain (MjCC-CL) in shrimp. Working as a cytokine like ligand, the MjCC-CL binds to polysaccharides from bacteria and the ILR domain of Domeles...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Binding of a C-type lectin’s coiled-coil domain to the Domeless receptor directly activates the JAK/STAT pathway in the shrimp immune response to bacterial infection

et al. 2017

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“…Interestingly, STAT is part of the JAK-STAT anti-viral signaling pathway, indicating that WSSV can hijack the host immune response in order to promote expression of its own genes. Knockdown experiments of a cytokine receptor that activates the JAK-STAT pathway in L. vannamei ( LvDOME ) resulted in lower cumulative mortality and fewer WSSV copies, providing further evidence for the interaction between JAK-STAT and WSSV [ 150 ].…”

Section: Wssv Infectionmentioning

confidence: 99%

Molecular Mechanisms of White Spot Syndrome Virus Infection and Perspectives on Treatments

Verbruggen

Bickley

Aerle

et al. 2016

Viruses

172

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Since its emergence in the 1990s, White Spot Disease (WSD) has had major economic and societal impact in the crustacean aquaculture sector. Over the years shrimp farming alone has experienced billion dollar losses through WSD. The disease is caused by the White Spot Syndrome Virus (WSSV), a large dsDNA virus and the only member of the Nimaviridae family. Susceptibility to WSSV in a wide range of crustacean hosts makes it a major risk factor in the translocation of live animals and in commodity products. Currently there are no effective treatments for this disease. Understanding the molecular basis of disease processes has contributed significantly to the treatment of many human and animal pathogens, and with a similar aim considerable efforts have been directed towards understanding host–pathogen molecular interactions for WSD. Work on the molecular mechanisms of pathogenesis in aquatic crustaceans has been restricted by a lack of sequenced and annotated genomes for host species. Nevertheless, some of the key host–pathogen interactions have been established: between viral envelope proteins and host cell receptors at initiation of infection, involvement of various immune system pathways in response to WSSV, and the roles of various host and virus miRNAs in mitigation or progression of disease. Despite these advances, many fundamental knowledge gaps remain; for example, the roles of the majority of WSSV proteins are still unknown. In this review we assess current knowledge of how WSSV infects and replicates in its host, and critique strategies for WSD treatment.

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“…PIAS can interact directly with p-Stat to inhibit Stat activation31. In shrimp, a Dome42, a Jak43 and a Stat3839 in the Jak/Stat pathway have been identified. Shrimp Stat is similar to mammalian Stat5a/b.…”

Section: Discussionmentioning

confidence: 99%

β-Arrestin 1’s Interaction with TC45 Attenuates Stat signaling by dephosphorylating Stat to inhibit antimicrobial peptide expression

Sun

Yang

Niu

et al. 2016

Sci Rep

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Impaired phosphatase activity leads to the persistent activation of signal transducers and activators of transcription (Stat). In mammals, Stat family members are often phosphorylated or dephosphorylated by the same enzymes. To date, only one Stat similar to mammalian Stat5a/b has been found in crustaceans and there have been few studies in Stat signal regulation in crustaceans. Here, we report that β-arrestin1 interacts with TC45 (45-kDa form of T cell protein tyrosine phosphatase) in the nucleus to attenuate Stat signaling by promoting dephosphorylation of Stat. Initially, we showed that Stat translocates into the nucleus to induce antimicrobial peptide (AMP) expression after bacterial infection. βArr1 enters the nucleus of hemocytes and recruits TC45 to form the βarr1-TC45-Stat complex, which dephosphorylates Stat efficiently. The interaction of TC45 with Stat decreased and Stat phosphorylation increased in βarr1-silenced shrimp (Marsupenaeus japonicus) after challenge with Vibrio anguillarum. βArr1 directly interacts with Stat in nucleus and accelerates Stat dephosphorylation by recruiting TC45 after V. anguillarum challenge. Further study showed that βarr1 and TC45 also affect AMP expression, which is regulated by Stat. Therefore, βarr1 and TC45 are involved in the anti-V. anguillarum immune response by regulating Stat activity negatively to decrease AMP expression in shrimp.

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Identification of a JAK/STAT pathway receptor domeless from Pacific white shrimp Litopenaeus vannamei

Cited by 52 publications

References 38 publications

Binding of a C-type lectin’s coiled-coil domain to the Domeless receptor directly activates the JAK/STAT pathway in the shrimp immune response to bacterial infection

Binding of a C-type lectin’s coiled-coil domain to the Domeless receptor directly activates the JAK/STAT pathway in the shrimp immune response to bacterial infection

Molecular Mechanisms of White Spot Syndrome Virus Infection and Perspectives on Treatments

β-Arrestin 1’s Interaction with TC45 Attenuates Stat signaling by dephosphorylating Stat to inhibit antimicrobial peptide expression

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