Three members in JAK/STAT signal pathway from the sea cucumber Apostichopus japonicus: Molecular cloning, characterization and function analysis

Shao, Yina; Li, Chenghua; Zhang, Weiwei; Duan, Xuemei; Li, Ye; Han, Qingxi; Jin, Chunhua

doi:10.1016/j.fsi.2015.07.019

Cited by 31 publications

(6 citation statements)

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“…A complete JAK/STAT pathway is found in Drosophila and mosquito [ 12 , 18 , 27 ]. In mollusks [ 28 ] and echinoderms [ 29 ], only some components have been identified and it remains unclear whether they have a complete JAK/STAT pathway. Other organisms, such as Caenorhabditis elegans and Dictyostelium , do not have a completely functional JAK/STAT cassette, but homologs of some JAK/STAT pathway proteins have been found [ 30 , 31 ].…”

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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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%

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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“…Apostichopus japonicas SOCS2, induced by the bacteria Vibrio splendidus , was found to be a potent negative regulator in the JAK/STAT pathway (Shao et al . ). The present study was limited to studying the immune induction of TmSOCS2 after microorganism challenge.…”

Section: Developmental and Spatial Distribution Of Tmsocs2mentioning

confidence: 97%

“…Immune challenge studies with SOCS2 members reported from other molluscan species, such as Eriocheir sinensis, Pinctada fucata, and Haliotis discus discus-, indicates the potential role of the gene in the antibacterial immune response of molluscans (Zhang et al 2010;De Zoysa & Lee 2009). Apostichopus japonicas SOCS2, induced by the bacteria Vibrio splendidus, was found to be a potent negative regulator in the JAK/STAT pathway (Shao et al 2015). The following Escherichia coli, Staphylococcus aureus, and Candida albicans challenge to the host.…”

Section: Temporal Expression Of Tmsocs2mentioning

confidence: 99%

Molecular cloning and characterization of SOCS2 from the mealworm beetle Tenebrio molitor

Kim

Patnaik

et al. 2019

Entomological Research

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The suppressor of cytokine signaling (SOCS) family of proteins negatively regulate cytokine receptor signaling via the Janus kinase/signal transducer and activator of transcription (STAT) pathway. In this study, we discovered the SOCS2 homolog in the mealworm beetle Tenebrio molitor (TmSOCS2). The full‐length ORF sequence of TmSOCS2 was cloned, and expression pattern in the insect's developmental stages and tissues were investigated. TmSOCS2 encodes 254 amino acid polypeptide consisting of the conserved Src homology 2 (SH2) and SOCS box domains. The amino acid sequence of TmSOCS2 showed maximum 77% identity and minimum evolutionary distance of 0.228 with SOCS2 protein of another related beetle, Tribolium castaneum (TcSOCS2). In the phylogenetic tree, TmSOCS2 and TcSOCS2 formed a separate cluster showing evolutionary relatedness with the hemipteran bug Lygus hesperus SOCS2 (LhSOCS2). TmSOCS2 mRNA was maximally expressed in the egg stage of the insect. High relative expression of TmSOCS2 was observed in the Malpighian tubules during the insect's larval and adult stages. TmSOCS2 mRNA expression was significantly (P < 0.05) upregulated by E. coli challenge in the fat body tissue of T. molitor larvae. In hemocytes, early expression (at 3–6 h) of TmSOCS2 mRNA was observed after S. aureus and C. albicans challenge. Discovery and expression analysis of the SOCS2 homolog from the mealworm beetle T. molitor support transcript's putative involvement in the insect innate immune responses.

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“…Apostichopus japonicus ( A . japonicus ), which belongs to the family Holothuroidea and is mainly distributed on the coasts of China and Japan, is a species with remarkable nutritional and commercial value. , The protein content of the body wall of A. japonicus had been reported to be as high as 70% . Because of the abundance of proteins rich in high-quality peptides, Apostichopus japonicus is widely used as a traditional Chinese medicine, especially for stomachache, hypertension, and erectile dysfunction.…”

Section: Introductionmentioning

confidence: 99%

Dietary Apostichopus japonicus Alleviates Diabetes Symptoms and Modulates Genes Expression in Kidney Tissues of db/db Mice

Dong

Zhang

et al. 2018

J. Agric. Food Chem.

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The effects of Apostichopus japonicus enzymatic hydrolysate on the regulation of dyslipidemia, pathoglycemia, and transcription changes in kidney tissues of db/db mice were evaluated. In this study, the symptoms of diabetes in db/db mice were alleviated after 10 weeks of treatments with low (db/db + LD group) and high dose (db/db + HD group) of Apostichopus japonicus enzymatic hydrolysate, and the high dose treatment showed a better antidiabetic effect. Compared with the db/db group, the fasting blood glucose levels (36.84 ± 7.82 vs 25.18 ± 6.84 mmol/L, P < 0.01), the urine glucose levels (45.44 ± 3.93 vs 22.66 ± 5.58 mmol/L, P < 0.01), and the serum insulin sensitivity index (-4.65 ± 0.43 vs -4.74 ± 0.75, P > 0.05) in the db/db + HD group were decreased, whereas the fasting plasma insulin (3.12 ± 1.08 vs 5.54 ± 1.82 μg/L, P < 0.01) and the serum insulin resistance index (5.01 ± 2.02 vs 5.96 ± 2.49, P < 0.05) were increased. Subsequently, the kidney transcription profiles were measured in the db/db group and db/db + HD group via microarray, and the results show that Apostichopus japonicus hydrolysate induced differential expression of 77 genes. Among these genes, the down-regulation of genes ntrK1 and ptpN5 played vital roles, as this effect induced the further down-regulation of neurotrophin tyrosine kinase, protein tyrosine phosphatase, and other transcription factors, which are involved in the classical mitogen-activated protein kinases (MAPK) and p38MAPK signaling pathways. The inhibited MAPK and p38MAPK signaling pathways are involved in glycometabolism and the control of lipid metabolism, and they regulate the occurrence and development of diabetic nephropathy.

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Three members in JAK/STAT signal pathway from the sea cucumber Apostichopus japonicus: Molecular cloning, characterization and function analysis

Cited by 31 publications

References 48 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 cloning and characterization of SOCS2 from the mealworm beetle Tenebrio molitor

Dietary Apostichopus japonicus Alleviates Diabetes Symptoms and Modulates Genes Expression in Kidney Tissues of db/db Mice

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