Identification and functional characterization of the goldfish (Carassius auratus L.) high mobility group box 1 (HMGB1) chromatin-binding protein

Xie, Jiasong; Hodgkinson, Jordan W.; Li, Chao; Kovačević, Nikolina; Belosevic, Miodrag

doi:10.1016/j.dci.2013.12.015

Cited by 32 publications

(35 citation statements)

References 53 publications

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“…1,6 Recent discoveries illustrate that HMGBs, particularly HMGB1, function as cytokines or pro-inflammatory factors, playing a pivotal role in crosslinking innate and adaptive immunity. [7][8][9] Various studies have also highlighted the novel feature of HMGBs that function as universal sentinels for nucleic-acid-mediated innate immune responses. 7,10 Some of these studies have shown that HMGBs promiscuously recognize immunogenic nucleic acids and transduce signals to discriminate pattern recognition receptors, such as Toll-like receptors (TLRs), retinoic acid-inducible gene I-like receptors and other cytosolic receptors, to initiate the innate immune response.…”

Section: Introductionmentioning

confidence: 99%

Dynamic localization and the associated translocation mechanism of HMGBs in response to GCRV challenge in CIK cells

Rao

Yang

et al. 2014

Cell Mol Immunol

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High-mobility group box (HMGB) proteins, a family of chromatin-associated nuclear proteins, play amazingly multifaceted roles in the immune system of mammals. Thus far, little is known about the nucleocytoplasmic distribution of HMGBs in teleosts. The present study systematically investigated the dynamic localization of all six HMGB proteins in Ctenopharyngodon idella kidney (CIK) cells. Under basal conditions, all HMGBs exclusively localized to the nucleus. Grass carp reovirus (GCRV), polyinosinic-polycytidylic (poly(I : C)) potassium salt and lipopolysaccharide (LPS) challenge evoked the nuclear export of HMGBs to various degrees: GCRV challenge induced the highest nuclear export of CiHMGB2b, and poly(I : C) and LPS evoked the highest nucleocytoplasmic shuttling of CiHMGB1b. Overall, the nucleocytoplasmic shuttling of CiHMGB2a and CiHMGB3b was rarely induced by these challenges. Dynamic imaging uncovered that the nucleocytoplasmic GCRV-induced relocation of CiHMGB2b occurred in cells undergoing karyotheca rupture, apoptosis or proliferation. Western blot analyses were used to examine HMGB-EGFP fusion proteins in whole cell lysates, cytosol, nuclear fractions and culture medium. Further investigation demonstrated the nuclear retention of N-terminal HMG-boxes and the nucleocytoplasmic distribution of the C-terminal acidic tails. Comparative analyses of the dynamic relocation of full-length, truncated or chimeric HMGBs confirmed that the intramolecular interaction between HMG-boxes and C-tail domains mediated the nucleocytoplasmic translocation of HMGBs. These results not only provide an overall understanding of the subcellular localization of HMGBs, but also reveal the induction mechanism of the nucleocytoplasmic translocation of HMGBs by GCRV challenge, which lays a foundation for further studies on the interactions among pathogens, HMGBs and pattern recognition receptors in the innate immunity of teleosts. Keywords: grass carp (Ctenopharyngodon idella); grass carp reovirus; HMGBs; innate immunity; subcellular localization INTRODUCTION High-mobility group box (HMGB) proteins are abundant non-histone chromatin components implicated in major DNA transactions. In mammals, there are four family members (HMGB1-4), of which HMGB1, 2 and 3 are characterized by two DNA-binding domains (HMG-box A and B) and a Cterminal acidic tail domain and HMGB4 possesses two HMG-boxes but lacks the acidic tail. 1 In some teleosts, such as fugu (Takifugu), medaka (Oryzias latipes), Tetraodon and stickleback, two paralogous genes were detected for HMGB1 and HMGB2 but not for HMGB3. 2 However, in zebrafish (Danio rerio), salmon (Oncorhynchus), carp (Cyprinus carpio) 2 and grass carp (Ctenopharyngodon idella), 3-5 two paralogs are present within each of the HMGB subfamilies (HMGB1,

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Section: Introductionmentioning

confidence: 99%

Dynamic localization and the associated translocation mechanism of HMGBs in response to GCRV challenge in CIK cells

Rao

Yang

et al. 2014

Cell Mol Immunol

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“…The similar results were recorded in report of goldfish HMGB1 (gHMGB1). In addition, the recombinant gHMGB1 also induced TNFa-2 and IL-1b production in goldfish macrophages, suggesting a crucial role of gHMGB1 in inflammatory regulation and antimicrobial response [19]. Our data exhibited that transcripts of Ls-HMGB1 were significantly increased at 18 h (11.8-fold) after V. harveyi challenged compared with control group (Fig.…”

Section: Expression Profiles Of Ls-hmgb1 In Head Kidney (Hk) Responsementioning

confidence: 72%

“…The red drum HMGB1 (SoHMGB1) can promote monocytes/macrophages activation [17]. Additionally, HMGB1 from goldfish induces activation of NF-kB and promotes the production of cytokines, such as TNFa-2 and IL-1b [19]. On the other hand, the requirements of zebrafish HMGB1 during brain development [15] and regeneration after spinal cord injury have been documented as well [20].…”

Section: Introductionmentioning

confidence: 98%

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Molecular cloning and characterization of high mobility group box1 (Ls-HMGB1) from humphead snapper, Lutjanus sanguineus

Cai

Xia

Huang

et al. 2014

Fish & Shellfish Immunology

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“…For immune defense, inflammation induced by brain‐damaging signalling pathways can be activated by proinflammatory cytokines (eg, IL‐1b, TNFα), damage signals (HMGB1), and downstream inflammatory mediators (eg, prostaglandins) . Xie et al identified HMGB1 in goldfish brain and demonstrated the upregulation of HMGB1 transcript and protein during bacterial infection, which induced the activation of the NF‐κB signaling pathway. In a previous study, striped catfish ( Pangasianodon hypophthalmus, S .)…”

Section: Discussionmentioning

confidence: 99%

Transcriptome analysis reveals benzotriazole ultraviolet stabilizers regulate networks related to inflammation in juvenile zebrafish (Danio rerio) brain

Zha

et al. 2018

Environmental Toxicology

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Benzotriazole ultraviolet stabilizers (BUVSs) are widely applied ultraviolet absorbing compounds in industrial materials and personal care products. Due to their ubiquitous use and reports of bio-accumulation in aquatic organisms, these compounds are significant environmental pollutants; however, data are limited for BUVSs toxicity. In this study, juvenile zebrafish (Danio rerio) were exposed to 4 commonly used BUVSs (UV-234, UV-326, UV-329, and UV-P) at one dose of 10 or 100 μg/L for 28 days. To characterize the underlying mechanisms of different BUVSs-induced toxicities, we performed global transcriptome sequencing (RNA-Seq) in the brain (100 μg/L). There were 390, 575, 483, and 470 differentially expressed genes (DEGs) detected following UV-234, UV-326, UV-329, and UV-P exposure at 100 μg/L, respectively. Only 59 genes were identified as DEGs following exposure to each of the BUVSs, suggesting that these chemicals can induce unique responses in fish. Noteworthy was that there were 81 common gene networks (~10%) identified following exposure to BUVSs, many of which were related to inflammation and immune function. Uniquely regulated pathways affected by different BUVSs included those related to mitochondrial respiration, interleukin 1/brain-damaging signaling, dopaminergic signaling, and adrenergic receptor cascades. Furthermore, quantitative PCR (qPCR) results revealed that mgst1 levels were increased in fish from the 100 μg/L UV-329 treatment, while the expression of pck2 was significantly down-regulated in fish from both the 10 and 100 μg/L UV-P treatment.Transcriptomic data suggest that BUVSs can alter mitochondrial bioenergetics, alter expression of a broad range of genes in the oxidative stress response, and can induce pathways related to the immune system in zebrafish brain. K E Y W O R D Sbenzotriazole ultraviolet stabilizers, immune-related pathways, juvenile zebrafish, RNA-Seq

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Identification and functional characterization of the goldfish (Carassius auratus L.) high mobility group box 1 (HMGB1) chromatin-binding protein

Cited by 32 publications

References 53 publications

Dynamic localization and the associated translocation mechanism of HMGBs in response to GCRV challenge in CIK cells

Dynamic localization and the associated translocation mechanism of HMGBs in response to GCRV challenge in CIK cells

Molecular cloning and characterization of high mobility group box1 (Ls-HMGB1) from humphead snapper, Lutjanus sanguineus

Transcriptome analysis reveals benzotriazole ultraviolet stabilizers regulate networks related to inflammation in juvenile zebrafish (Danio rerio) brain

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