β-Arrestins Negatively Regulate the Toll Pathway in Shrimp by Preventing Dorsal Translocation and Inhibiting Dorsal Transcriptional Activity

Sun, Jiejie; Lan, Jiang-Feng; Shi, Xiaoping; Yang, Ming-Chong; Niu, Guo-Juan; Ding, Ding; Zhao, Xiao‐Fan; Yu, Xiao‐Qiang; Wang, Jin-Xing

doi:10.1074/jbc.m115.698134

Cited by 51 publications

(27 citation statements)

References 51 publications

(51 reference statements)

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“…It was also identified as the adaptor protein for clathrin-mediated endocytosis [22, 23]. β-Arrestin1 and 2 were involved in the regulation of shrimp Toll pathway [24]. However, whether β-arrestins participate in the internalization of SRs has not been reported.…”

Section: Introductionmentioning

confidence: 99%

Scavenger Receptor C Mediates Phagocytosis of White Spot Syndrome Virus and Restricts Virus Proliferation in Shrimp

et al. 2016

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Scavenger receptors are an important class of pattern recognition receptors that play several important roles in host defense against pathogens. The class C scavenger receptors (SRCs) have only been identified in a few invertebrates, and their role in the immune response against viruses is seldom studied. In this study, we firstly identified an SRC from kuruma shrimp, Marsupenaeus japonicus, designated MjSRC, which was significantly upregulated after white spot syndrome virus (WSSV) challenge at the mRNA and protein levels in hemocytes. The quantity of WSSV increased in shrimp after knockdown of MjSRC, compared with the controls. Furthermore, overexpression of MjSRC led to enhanced WSSV elimination via phagocytosis by hemocytes. Pull-down and co-immunoprecipitation assays demonstrated the interaction between MjSRC and the WSSV envelope protein. Electron microscopy observation indicated that the colloidal gold-labeled extracellular domain of MjSRC was located on the outer surface of WSSV. MjSRC formed a trimer and was internalized into the cytoplasm after WSSV challenge, and the internalization was strongly inhibited after knockdown of Mjβ-arrestin2. Further studies found that Mjβ-arrestin2 interacted with the intracellular domain of MjSRC and induced the internalization of WSSV in a clathrin-dependent manner. WSSV were co-localized with lysosomes in hemocytes and the WSSV quantity in shrimp increased after injection of lysosome inhibitor, chloroquine. Collectively, this study demonstrated that MjSRC recognized WSSV via its extracellular domain and invoked hemocyte phagocytosis to restrict WSSV systemic infection. This is the first study to report an SRC as a pattern recognition receptor promoting phagocytosis of a virus.

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Section: Introductionmentioning

confidence: 99%

Scavenger Receptor C Mediates Phagocytosis of White Spot Syndrome Virus and Restricts Virus Proliferation in Shrimp

et al. 2016

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“…Moreover, in mammals, βarr1 also recruits tyrosine phosphatase TC45 to Stat1 in the nucleus in response to IFN-gamma stimulation and affects Stat1 phosphorylation35. In shrimp, two β-arrestins (βarr 1 and 2) were identified that regulated the Toll pathway negatively by inhibiting Dorsal translocating into the nucleus40. In the present study, βarr1, but not βarr2, was observed to regulate specifically tyrosine phosphorylation of Stat in shrimp, resulting in decreased AMP expression.…”

Section: Discussionmentioning

confidence: 45%

“…βarrs and Stat were reported in shrimp previously4041. TC45 was first identified in shrimp and submitted to GenBank (no.…”

Section: Resultsmentioning

confidence: 99%

“…The sequences of βarr1 and βarr2 were reported in our previous paper40. Similarity analysis was conducted using BLASTx (http://www.ncbi.nlm.nih.gov/).…”

Section: Methodsmentioning

confidence: 99%

“…Another study also found that GdX (X-linked gene in the G6PD cluster at Xq28, also known as Ubl4A, Ubiquitin-like protein 4A) promotes Stat3 dephosphorylation by mediating the interaction between TC45 and Stat3 specifically37. In shrimp, only one Stat similar to mammalian Stat5a/b3839 and two βarrs (βarr 1 and 2)40 have been identified, but TC45 has not been reported. Furthermore, the functions of βarrs and TC45 in the Jak/Stat pathway remain unknown.…”

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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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Hormonal regulation changes in shrimp infected with Enterocytozoon hepatopenaei: a transcriptomic analysis

Zhang,

Dou

et al. 2023

Aquacult Int

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β-Arrestins Negatively Regulate the Toll Pathway in Shrimp by Preventing Dorsal Translocation and Inhibiting Dorsal Transcriptional Activity

Cited by 51 publications

References 51 publications

Scavenger Receptor C Mediates Phagocytosis of White Spot Syndrome Virus and Restricts Virus Proliferation in Shrimp

Scavenger Receptor C Mediates Phagocytosis of White Spot Syndrome Virus and Restricts Virus Proliferation in Shrimp

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

Hormonal regulation changes in shrimp infected with Enterocytozoon hepatopenaei: a transcriptomic analysis

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