Publications by authors named "Jiae Lee"

42 Publications

Cytokine-cytokine receptor interactions in the highly pathogenic avian influenza H5N1 virus-infected lungs of genetically disparate Ri chicken lines.

Anim Biosci 2021 Jun 24. Epub 2021 Jun 24.

Department of Animal Science and Technology, Chung-Ang University, Anseong 17546, Republic of Korea.

Objective: The highly pathogenic avian influenza virus (HPAIV) is a threat to the poultry industry as well as the economy and remains a potential source of pandemic infection in humans. Antiviral genes are considered a potential factor for HPAIV resistance. Therefore, in this study, we investigated gene expression related to cytokine-cytokine receptor interactions by comparing resistant and susceptible Ri chicken lines for avian influenza virus infection.

Methods: Ri chickens of resistant (Mx/A; BF2/B21) and susceptible (Mx/G; BF2/B13) lines were selected by genotyping the Mx and BF2 genes. These chickens were then infected with HPAIV H5N1, and their lung tissues were collected for RNA sequencing.

Results: In total, 972 differentially expressed genes (DEGs) were observed between resistant and susceptible Ri chickens, according to the Gene Ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways. In particular, DEGs associated with cytokine-cytokine receptor interactions were most abundant. The expression levels of cytokines (IL-1β, IL-6, IL-8, and IL-18), chemokines (CCL4 and CCL17), interferons (IFN-γ), and IFN-stimulated genes (Mx1, CCL19, OASL, and PRK) were higher in H5N1-resistant chickens than in H5N1-susceptible chickens.

Conclusion: Resistant chickens show stronger immune responses and antiviral activity (cytokines, chemokines, and IFN-stimulated genes) than those of susceptible chickens against HPAIV infection.
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http://dx.doi.org/10.5713/ab.21.0163DOI Listing
June 2021

Flunarizine inhibits osteoclastogenesis by regulating calcium signaling and promotes osteogenesis.

J Cell Physiol 2021 Jun 30. Epub 2021 Jun 30.

Department of Life Science and the Research Center for Cellular Homeostasis, Ewha Womans University, Seoul, Korea.

Many bone diseases such as osteoporosis and periodontitis are caused by hyperactivation of osteoclasts. Calcium (Ca ) signals are crucial for osteoclast differentiation and function. Thus, the blockade of Ca signaling may be a strategy for regulating osteoclast activity and has clinical implications. Flunarizine (FN) is a Ca channel antagonist that has been used for reducing migraines. However, the role of FN in osteoclast differentiation and function remains unknown. Here, we investigated whether FN regulates osteoclastogenesis and elucidated the molecular mechanism. FN inhibited osteoclast differentiation along with decreased expression of nuclear factor of activated T cells, cytoplasmic 1 (NFATc1), and attenuated osteoclast maturation and bone resorption. FN inhibition of osteoclast differentiation was restored by ectopic expression of constitutively active NFATc1. FN reduced calcium oscillations and its inhibition of osteoclast differentiation and resorption function was reversed by ionomycin, an ionophore that binds Ca . FN also inhibited Ca /calmodulin-dependent protein kinase IV (CaMKIV) and calcineurin leading to a decrease in the cAMP-responsive element-binding protein-dependent cFos and peroxisome proliferator-activated receptor-γ coactivator 1β expression, and NFATc1 nuclear translocation. These results indicate that FN inhibits osteoclastogenesis via regulating CaMKIV and calcineurin as a Ca channel blocker. In addition, FN-induced apoptosis in osteoclasts and promoted osteogenesis. Furthermore, FN protected lipopolysaccharide- and ovariectomy-induced bone destruction in mouse models, suggesting that it has therapeutic potential for treating inflammatory bone diseases and postmenopausal osteoporosis.
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http://dx.doi.org/10.1002/jcp.30496DOI Listing
June 2021

Immunomodulatory effects of poly(I:C)-stimulated exosomes derived from chicken macrophages.

Poult Sci 2021 Aug 18;100(8):101247. Epub 2021 May 18.

Department of Animal Science and Technology, Chung-Ang University, Anseong 17546, Republic of Korea. Electronic address:

Exosomes are small membrane vesicles that contain proteins and nucleic acids derived from secretory cells and mediate intracellular communication. Immune cell-derived exosomes regulate immune responses and gene expression of recipient cells. Macrophages recognize viral dsRNA via Toll-like receptor 3, thereby inducing the activation of transcription factors such as interferon regulatory factor 3 and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB). In this study, we aimed to identify the immunomodulatory functions of exosomes derived from chicken macrophages (HD11) stimulated with polyinosinic-polycytidylic acid (poly[I:C]); exosomes were then delivered into HD11 cells and CU91 chicken T cells. Exosomes purified from poly(I:C)-activated macrophages stimulated the expression of type I interferons, proinflammatory cytokines, anti-inflammatory cytokines, and chemokines in HD11 and CU91 cells. Moreover, poly(I:C)-stimulated exosomes induced the NF-κB signaling pathway by phosphorylating TAK1 and NF-κB1. Therefore, we suggest that after the activation of Toll-like receptor 3 ligands following infection with dsRNA virus, chicken macrophages regulate the immune response of naive macrophages and T cells through the NF-κB signaling pathway. Furthermore, poly(I:C)-activated exosomes can be potentially utilized as immunostimulators.
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http://dx.doi.org/10.1016/j.psj.2021.101247DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8242060PMC
August 2021

The effect of body fatness on regional brain imaging markers and cognitive function in healthy elderly mediated by impaired glucose metabolism.

J Psychiatr Res 2021 Aug 11;140:488-495. Epub 2021 Jun 11.

Department of Preventive Medicine, Yonsei University College of Medicine, Seoul, 03722, Republic of Korea; Department of Public Health, Yonsei University Graduate School, Seoul, 03722, Republic of Korea; Institute of Human Complexity and Systems Science, Yonsei University, Incheon, 21983, Republic of Korea. Electronic address:

Brain atrophy is related to vascular risk factors and can increase cognitive dysfunction risk. This community-based, cross-sectional study investigated whether glucose metabolic disorders due to body fatness are linked to regional changes in brain structure and a decline in neuropsychological function in cognitively healthy older adults. From 2016 to 2019, 429 participants underwent measurements for cortical thickness and subcortical volume using 3 T magnetic resonance imaging and for cognitive function using the neuropsychological screening battery. The effects of body fatness mediated by impaired glucose metabolism on neuroimaging markers and cognitive function was investigated using partial least square structural equation modeling. Total grey matter volume (β = -0.020; bias-corrected (BC) 95% confidence interval (CI) = -0.047 to -0.006), frontal (β = -0.029; BC 95% CI = -0.063 to -0.005) and temporal (β = -0.022; BC 95% CI = -0.051 to -0.004) lobe cortical thickness, and hippocampal volume (β = -0.029; BC 95% CI = -0.058 to -0.008) were indirectly related to body fatness. Further, frontal/temporal lobe thinning was associated with recognition memory (β = -0.005; BC 95% CI = -0.012 to -0.001/β = -0.005; BC 95% CI = -0.013 to -0.001) and delayed recall for visual information (β = -0.005; BC 95% CI = -0.013 to -0.001/β = -0.005; BC 95% CI = -0.013 to -0.001). Additionally, the smaller the hippocampal volume, the lower the score in recognition memory (β = -0.005; BC 95% CI = -0.012 to -0.001), delayed recall for visual information (β = -0.005; BC 95% CI = -0.012 to -0.001), and verbal learning (β = -0.008; BC 95% CI = -0.017 to -0.002). Our findings indicate that impaired glucose metabolism caused by excess body fatness affects memory decline as well as regional grey matter atrophy in elderly individuals with no neurological disease.
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http://dx.doi.org/10.1016/j.jpsychires.2021.06.011DOI Listing
August 2021

Tumors overcome the action of the wasting factor ImpL2 by locally elevating Wnt/Wingless.

Proc Natl Acad Sci U S A 2021 Jun;118(23)

Department of Biochemistry, School of Medicine, University of Washington, Seattle, WA 98195;

Tumors often secrete wasting factors associated with atrophy and the degeneration of host tissues. If tumors were to be affected by the wasting factors, mechanisms allowing tumors to evade the adverse effects of the wasting factors must exist, and impairing such mechanisms may attenuate tumors. We use midgut tumor models to show that tumors up-regulate Wingless (Wg) to oppose the growth-impeding effects caused by the wasting factor, ImpL2 (insulin-like growth factor binding protein [IGFBP]-related protein). Growth of Yorkie (Yki)-induced tumors is dependent on Wg while either elimination of or elevation of insulin/insulin-like growth factor signaling in tumors revokes this dependency. Notably, Wg augmentation could be a general mechanism for supporting the growth of tumors with elevated ImpL2 and exploited to attenuate muscle degeneration during wasting. Our study elucidates the mechanism by which tumors negate the action of ImpL2 to uphold their growth during cachexia-like wasting and implies that targeting the Wnt/Wg pathway might be an efficient treatment strategy for cancers with elevated IGFBPs.
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http://dx.doi.org/10.1073/pnas.2020120118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8201939PMC
June 2021

Exosomal miRNA profiling from H5N1 avian influenza virus-infected chickens.

Vet Res 2021 Mar 3;52(1):36. Epub 2021 Mar 3.

Department of Animal Science and Technology, Chung-Ang University, Anseong, 17546, Republic of Korea.

Exosomes are membrane vesicles containing proteins, lipids, DNA, mRNA, and micro RNA (miRNA). Exosomal miRNA from donor cells can regulate the gene expression of recipient cells. Here, Ri chickens were divided into resistant (Mx/A; BF2/B21) and susceptible (Mx/G; BF2/B13) trait by genotyping of Mx and BF2 genes. Then, Ri chickens were infected with H5N1, a highly pathogenic avian influenza virus (HPAIV). Exosomes were purified from blood serum of resistant chickens for small RNA sequencing. Sequencing data were analysed using FastQCv0.11.7, Cutadapt 1.16, miRBase v21, non-coding RNA database, RNAcentral 10.0, and miRDeep2. Differentially expressed miRNAs were determined using statistical methods, including fold-change, exactTest using edgeR, and hierarchical clustering. Target genes were predicted using miRDB. Gene ontology analysis was performed using gProfiler. Twenty miRNAs showed significantly different expression patterns between resistant control and infected chickens. Nine miRNAs were up-regulated and 11 miRNAs were down-regulated in the infected chickens compared with that in the control chickens. In target gene analysis, various immune-related genes, such as cytokines, chemokines, and signalling molecules, were detected. In particular, mitogen-activated protein kinase (MAPK) pathway molecules were highly controlled by differentially expressed miRNAs. The result of qRT-PCR for miRNAs was identical with sequencing data and miRNA expression level was higher in resistant than susceptible chickens. This study will help to better understand the host immune response, particularly exosomal miRNA expression against HPAIV H5N1 and could help to determine biomarkers for disease resistance.
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http://dx.doi.org/10.1186/s13567-021-00892-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7931527PMC
March 2021

Exosomes of lipopolysaccharide-stimulated chicken macrophages modulate immune response through the MyD88/NF-κB signaling pathway.

Dev Comp Immunol 2021 Feb 25;115:103908. Epub 2020 Oct 25.

Department of Animal Science and Technology, Chung-Ang University, Anseong, 17546, Republic of Korea. Electronic address:

Exosomes are small membrane-extracellular vesicles produced from multivesicular bodies and play a role in cell-to-cell signaling. Exosomes from immune cells can regulate immune responses of recipient cells by releasing their contents. In the immune system, macrophages recognize lipopolysaccharides (LPSs) of gram-negative bacteria by toll-like receptor 4 (TLR4) and intracellular pathways, such as NF-κB pathway, are activated, inducing proinflammatory cytokine expression. However, no studies have investigated the functions of exosomes in chicken macrophages. The purpose of this study was to demonstrate the immunoregulatory functions of LPS-activated exosomes in chicken immune systems. Therefore, chicken macrophages cells (HD11) were activated with LPS, and exosomes were purified. The LPS-activated exosomes enhanced the gene expression of cytokines and chemokines, including IL-1β, IFN-γ, IFN-α, IL-4, CCL4, CCL17, and CCL19, in naive chicken macrophages. Furthermore, LPS-activated exosomes induced the MyD88/NF-κB signaling pathway. Therefore, as an immune response against gram-negative bacterial infection, LPS-activated chicken macrophages can release exosomes that are delivered to inactivated macrophages by regulating the expression of immune-related genes and the MyD88/NF-κB signaling pathway. In the future, LPS-stimulated exosomes may be utilized as an immune stimulator.
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http://dx.doi.org/10.1016/j.dci.2020.103908DOI Listing
February 2021

Chicken avian β-defensin 8 modulates immune response via the mitogen-activated protein kinase signaling pathways in a chicken macrophage cell line.

Poult Sci 2020 Sep 24;99(9):4174-4182. Epub 2020 Jun 24.

Department of Animal Science and Technology, Chung-Ang University, Anseong 17546, Republic of Korea. Electronic address:

Defensins are antimicrobial peptides composed of 3 conserved disulfide bridges, a β-sheet, and both hydrophobic and cationic amino acids. In this study, we aimed to demonstrate the immunomodulation role of avian β-defensin 8 (AvBD8) in a chicken macrophage cell line. Chicken AvBD8 stimulated the expression of proinflammatory cytokines (IL-1β, interferon gamma, and IL-12p40) and chemokines (CCL4, CXCL13, and CCL20) in macrophages. Furthermore, by Western blotting and immunocytochemistry, we confirmed that AvBD8 activated the mitogen-activated protein kinase signaling pathway via extracellular regulated kinases 1/2 and p38 signaling molecules. Overall, AvBD8 plays a crucial role in host defense as not only an antimicrobial peptide but also an immunomodulator by activating the mitogen-activated protein kinase signaling pathway and inducing the expression of proinflammatory cytokines and chemokines.
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http://dx.doi.org/10.1016/j.psj.2020.05.027DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7598012PMC
September 2020

Cinchonine inhibits osteoclast differentiation by regulating TAK1 and AKT, and promotes osteogenesis.

J Cell Physiol 2021 Mar 23;236(3):1854-1865. Epub 2020 Jul 23.

Department of Life Science, Research Center for Cellular Homeostasis, Ewha Womans University, Seoul, South Korea.

Cinchonine (CN) has been known to exert antimalarial, antiplatelet, and antiobesity effects. It was also recently reported to inhibit transforming growth factor β-activated kinase 1 (TAK1) and protein kinase B (AKT) through binding to tumor necrosis factor receptor-associated factor 6 (TRAF6). However, its role in bone metabolism remains largely unknown. Here, we showed that CN inhibits osteoclast differentiation with decreased expression of nuclear factor of activated T-cells, cytoplasmic 1 (NFATc1), a key determinant of osteoclastogenesis. Immunoblot and quantitative real-time polymerase chain reaction analysis as well as the reporter assay revealed that CN inhibits nuclear factor-κB and activator protein-1 by regulating TAK1. CN also attenuated the activation of AKT, cyclic AMP response element-binding protein, and peroxisome proliferator-activated receptor-γ coactivator 1β (PGC1β), an essential regulator of mitochondrial biogenesis. Collectively, these results suggested that CN may inhibit TRAF6-mediated TAK1 and AKT activation, which leads to downregulation of NFATc1 and PGC1β resulting in the suppression of osteoclast differentiation. Interestingly, CN not only inhibited the maturation and resorption function of differentiated osteoclasts but also promoted osteoblast differentiation. Furthermore, CN protected lipopolysaccharide- and ovariectomy-induced bone destruction in mouse models, suggesting its therapeutic potential for treating inflammation-induced bone diseases and postmenopausal osteoporosis.
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http://dx.doi.org/10.1002/jcp.29968DOI Listing
March 2021

Dissemination of Ras-transformed cells requires the mechanosensitive channel Piezo.

Nat Commun 2020 07 16;11(1):3568. Epub 2020 Jul 16.

Department of Biochemistry, University of Washington, Seattle, WA, 98195, USA.

Dissemination of transformed cells is a key process in metastasis. Despite its importance, how transformed cells disseminate from an intact tissue and enter the circulation is poorly understood. Here, we use a fully developed tissue, Drosophila midgut, and describe the morphologically distinct steps and the cellular events occurring over the course of Ras-transformed cell dissemination. Notably, Ras-transformed cells formed the Actin- and Cortactin-rich invasive protrusions that were important for breaching the extracellular matrix (ECM) and visceral muscle. Furthermore, we uncovered the essential roles of the mechanosensory channel Piezo in orchestrating dissemination of Ras-transformed cells. Collectively, our study establishes an in vivo model for studying how transformed cells migrate out from a complex tissue and provides unique insights into the roles of Piezo in invasive cell behavior.
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http://dx.doi.org/10.1038/s41467-020-17341-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7366633PMC
July 2020

Immunomodulatory effects of avian β-defensin 5 in chicken macrophage cell line.

Res Vet Sci 2020 Oct 5;132:81-87. Epub 2020 Jun 5.

Department of Animal Science and Technology, Chung-Ang University, Anseong 17546, Republic of Korea. Electronic address:

Antimicrobial peptides (AMPs) protect host from pathogens as first line of defense. Especially, β-defensins shows antimicrobial activity and immune modulation effects. Avian species also have β-defensins as avian β-defensins (AvBDs) from AvBD1 to AvBD14. In this study, we characterized chicken AvBD5 and demonstrated its immune modulatory functions in chicken macrophage cell line (HD11). Chicken AvBD5 is composed of a signal, pro, and mature peptides containing one α-helix, four β-sheet, and three disulfide bonds. Here, we also showed that chicken AvBD5 induced Th1, Th2, and Th17 cytokines in chicken macrophage cell line and stimulated MAPK signaling pathways through ERK1/2 and p38 molecules. In addition, AvBD5 stimulated MyD88 and CD40 to regulate immune systems. Taken together, chicken AvBD5 can modulate host immune systems by inducing cytokines expression and stimulating MAPK signaling pathway.
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http://dx.doi.org/10.1016/j.rvsc.2020.06.002DOI Listing
October 2020

Benzydamine inhibits osteoclast differentiation and bone resorption down-regulation of interleukin-1 expression.

Acta Pharm Sin B 2020 Mar 8;10(3):462-474. Epub 2019 Nov 8.

Department of Life Science and the Research Center for Cellular Homeostasis, Ewha Womans University, Seoul 03760, South Korea.

Bone diseases such as osteoporosis and periodontitis are induced by excessive osteoclastic activity, which is closely associated with inflammation. Benzydamine (BA) has been used as a cytokine-suppressive or non-steroidal anti-inflammatory drug that inhibits the production of pro-inflammatory cytokines or prostaglandins. However, its role in osteoclast differentiation and function remains unknown. Here, we explored the role of BA in regulating osteoclast differentiation and elucidated the underlying mechanism. BA inhibited osteoclast differentiation and strongly suppressed interleukin-1 (IL-1) production. BA inhibited osteoclast formation and bone resorption when added to bone marrow-derived macrophages and differentiated osteoclasts, and the inhibitory effect was reversed by IL-1 treatment. The reporter assay and the inhibitor study of IL-1 transcription suggested that BA inhibited nuclear factor-B and activator protein-1 by regulating IB kinase, extracellular signal regulated kinase and P38, resulting in the down-regulation of IL-1 expression. BA also promoted osteoblast differentiation. Furthermore, BA protected lipopolysaccharide- and ovariectomy-induced bone loss in mice, suggesting therapeutic potential against inflammation-induced bone diseases and postmenopausal osteoporosis.
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http://dx.doi.org/10.1016/j.apsb.2019.11.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7049613PMC
March 2020

MicroRNA gga-miR-200a-3p modulates immune response via MAPK signaling pathway in chicken afflicted with necrotic enteritis.

Vet Res 2020 Feb 3;51(1). Epub 2020 Feb 3.

Department of Animal Science and Technology, Chung-Ang University, Anseong, 17546, Republic of Korea.

MicroRNAs (miRNAs) are small non-coding RNAs that contribute to host immune response as post-transcriptional regulation. The current study investigated the biological role of the chicken (Gallus gallus) microRNA-200a-3p (gga-miR-200a-3p), using 2 necrotic enteritis (NE) afflicted genetically disparate chicken lines, 6.3 and 7.2, as well as the mechanisms underlying the fundamental signaling pathways in chicken. The expression of gga-miR-200a-3p in the intestinal mucosal layer of NE-induced chickens, was found to be upregulated during NE infection in the disease-susceptible chicken line 7.2. To validate the target genes, we performed an overexpression analysis of gga-miR-200a-3p using chemically synthesized oligonucleotides identical to gga-miR-200a-3p, reporter gene analysis including luciferase reporter assay, and a dual fluorescence reporter assay in cultured HD11 chicken macrophage cell lines. Gga-miR-200a-3p was observed to be a direct transcriptional repressor of ZAK, MAP2K4, and TGFβ2 that are involved in mitogen-activated protein kinase (MAPK) pathway by targeting the 3'-UTR of their transcripts. Besides, gga-miR-200a-3p may indirectly affect the expression of protein kinases including p38 and ERK1/2 at both transcriptional and translational levels, suggesting that this miRNA may function as an important regulator of the MAPK signaling pathway. Proinflammatory cytokines consisting of IL-1β, IFN-γ, IL-12p40, IL-17A, and LITAF belonging to Th1 and Th17-type cytokines, were upregulated upon gga-miR-200a-3p overexpression. These findings have enhanced our knowledge of the immune function of gga-miR-200a-3p mediating the chicken immune response via regulation of the MAPK signaling pathway and indicate that this miRNA may serve as an important biomarker of diseases in domestic animals.
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http://dx.doi.org/10.1186/s13567-020-0736-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6998359PMC
February 2020

Dehydrocostus lactone inhibits NFATc1 via regulation of IKK, JNK, and Nrf2, thereby attenuating osteoclastogenesis.

BMB Rep 2020 Apr;53(4):218-222

Department of Life Science and the Research Center for Cellular Homeostasis, Ewha Womans University, Seoul 03760, Korea.

Excessive and hyperactive osteoclast activity causes bone diseases such as osteoporosis and periodontitis. Thus, the regulation of osteoclast differentiation has clinical implications. We recently reported that dehydrocostus lactone (DL) inhibits osteoclast differentiation by regulating a nuclear factor of activated T-cells, cytoplasmic 1 (NFATc1), but the underlying mechanism remains to be elucidated. Here we demonstrated that DL inhibits NFATc1 by regulating nuclear factor-κB (NF-κB), activator protein-1 (AP-1), and nuclear factor-erythroid 2- related factor 2 (Nrf2). DL attenuated IκBα phosphorylation and p65 nuclear translocation as well as decreased the expression of NF-κB target genes and c-Fos. It also inhibited c-Jun N-terminal kinase (JNK) but not p38 or extracellular signalregulated kinase. The reporter assay revealed that DL inhibits NF-κB and AP-1 activation. In addition, DL reduced reactive oxygen species either by scavenging them or by activating Nrf2. The DL inhibition of NFATc1 expression and osteoclast differentiation was less effective in Nrf2-deficient cells. Collectively, these results suggest that DL regulates NFATc1 by inhibiting NF-κB and AP-1 via down-regulation of IκB kinase and JNK as well as by activating Nrf2, and thereby attenuates osteoclast differentiation. [BMB Reports 2020; 53(4): 218-222].
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7196184PMC
April 2020

The role of translationally controlled tumor protein in proliferation of intestinal stem cells.

Proc Natl Acad Sci U S A 2019 Dec 16. Epub 2019 Dec 16.

Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA 02115;

Translationally controlled tumor protein (TCTP) is a highly conserved protein functioning in multiple cellular processes, ranging from growth to immune responses. To explore the role of TCTP in tissue maintenance and regeneration, we employed the adult midgut, where multiple signaling pathways interact to precisely regulate stem cell division for tissue homeostasis. Tctp levels were significantly increased in stem cells and enteroblasts upon tissue damage or activation of the Hippo pathway that promotes regeneration of intestinal epithelium. Stem cells with reduced Tctp levels failed to proliferate during normal tissue homeostasis and regeneration. Mechanistically, Tctp forms a complex with multiple proteins involved in translation and genetically interacts with ribosomal subunits. In addition, Tctp increases both Akt1 protein abundance and phosphorylation in vivo. Altogether, Tctp regulates stem cell proliferation by interacting with key growth regulatory signaling pathways and the translation process in vivo.
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http://dx.doi.org/10.1073/pnas.1910850116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6936429PMC
December 2019

MicroRNA gga-miR-10a-mediated transcriptional regulation of the immune genes in necrotic enteritis afflicted chickens.

Dev Comp Immunol 2020 01 19;102:103472. Epub 2019 Aug 19.

Department of Animal Science and Technology, Chung-Ang University, Anseong, 17546, Republic of Korea. Electronic address:

miRNAs are involved in both adaptive and innate immune systems of host animals; and play important roles in many immune-related pathways. The systemic biological roles of gga-miR-10a-5p chicken microRNA on immune response were investigated in two necrotic enteritis (NE) induced chicken lines, Marek's disease (MD) resistant (line 6.3) and susceptible (line 7.2). We determined the expression patterns of gga-miR-10a in the intestinal mucosal layer of chickens upon NE induction, and identified the target genes (MyD88, and SKP1) related to the host immune response to pathogens. We found that gga-miR-10a expression in the intestinal mucosal layer of MD-resistant chicken line 6.3 gga-miR-10a was significantly down-regulated (p < 0.01) during NE. Overexpression analysis of gga-miR-10a and reporter gene analysis using a wild- or mutant-type MyD88 3' untranslated region (3' UTR)-luciferase construct in chicken macrophage cell line HD11 and chicken fibroblast cell line OU2 showed that gga-miR-10a acted as a direct translational repressor of MyD88 by targeting the 3' UTR of this gene. Furthermore, miR-10a indirectly negatively influenced the expression of signaling molecules related to the MyD88-dependent pathway, including TRAF6, TAK1, and NF-κB1 at both transcriptional and translational levels. Downstream of the MyD88-dependent pathway, several proinflammatory cytokines such as IL-1β, IFN-γ, IL-12p40, TNFSF15, and LITAF were down-regulated by overexpression of gga-miR-10a. These results suggest that gga-miR-10a is an important regulator of the Toll-like receptor signaling pathway. The findings of this study improve our understanding of the biological functions of miR-10a and the mechanisms underlying the TLR signaling pathway upon NE afflicted chickens, as well improving the overall understanding of the immune system function in domestic animals.
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http://dx.doi.org/10.1016/j.dci.2019.103472DOI Listing
January 2020

Dehydrocostus lactone suppresses osteoclast differentiation by regulating NFATc1 and inhibits osteoclast activation through modulating migration and lysosome function.

FASEB J 2019 08 30;33(8):9685-9694. Epub 2019 May 30.

Department of Life Science, Ewha Womans University, Seoul, Republic of Korea.

Excessive osteoclast activity can lead to an imbalance between the synthesis and breakdown of bone, with pathologic consequences that include osteoporosis and periodontitis. Thus, controlling osteoclast differentiation and function has significant therapeutic implications. In this study, we investigated the effects of dehydrocostus lactone (DL) on osteoclast differentiation and activation and elucidated the possible mechanisms underlying these processes. DL suppressed osteoclast differentiation by reducing the expression of the nuclear factor of activated T-cells, cytoplasmic 1. When used to challenge differentiated osteoclasts, DL also effectively inhibited their enlargement and resorption activity, and biochemical approaches revealed that DL attenuates osteoclast activation by inhibiting the migration and lysosome biogenesis and secretion the down-regulation of integrin β, PKC-β, and autophagy related 5 expression. Furthermore, DL prevented bone destruction in inflammation- and ovariectomy-induced osteolytic mouse models. These results indicate that DL has therapeutic potential to treat bone diseases caused by excessive or hyperactive osteoclasts.-Lee, H. I., Lee, J., Hwang, D., Lee, G.-R., Kim, N., Kwon, M., Lee, H., Piao, D., Kim, H. J., Kim, N. Y., Kim, H. S., Seo, E. K., Kang, D., Jeong, W. Dehydrocostus lactone suppresses osteoclast differentiation by regulating NFATc1 and inhibits osteoclast activation through modulating migration and lysosome function.
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http://dx.doi.org/10.1096/fj.201900862RDOI Listing
August 2019

Skullcapflavone II inhibits osteoclastogenesis by regulating reactive oxygen species and attenuates the survival and resorption function of osteoclasts by modulating integrin signaling.

FASEB J 2019 02 14;33(2):2026-2036. Epub 2018 Sep 14.

Department of Life Science, Research Center for Cellular Homeostasis, Ewha Womans University, Seoul, South Korea.

Many bone diseases, such as osteoporosis and rheumatoid arthritis, are attributed to an increase in osteoclast number or activity; therefore, control of osteoclasts has significant clinical implications. This study shows how skullcapflavone II (SFII), a flavonoid with anti-inflammatory activity, regulates osteoclast differentiation, survival, and function. SFII inhibited osteoclastogenesis with decreased activation of MAPKs, Src, and cAMP response element-binding protein (CREB), which have been known to be redox sensitive. SFII decreased reactive oxygen species by scavenging them or activating nuclear factor-erythroid 2-related factor 2 (Nrf2), and its effects were partially reversed by hydrogen peroxide cotreatment or Nrf2 deficiency. In addition, SFII attenuated survival, migration, and bone resorption, with a decrease in the expression of integrin β, Src, and p130 Crk-associated substrate, and the activation of RhoA and Rac1 in differentiated osteoclasts. Furthermore, SFII inhibited osteoclast formation and bone loss in an inflammation- or ovariectomy-induced osteolytic mouse model. These findings suggest that SFII inhibits osteoclastogenesis through redox regulation of MAPKs, Src, and CREB and attenuates the survival and resorption function by modulating the integrin pathway in osteoclasts. SFII has therapeutic potential in the treatment and prevention of bone diseases caused by excessive osteoclast activity.-Lee, J., Son, H. S., Lee, H. I., Lee, G.-R., Jo, Y.-J., Hong, S.-E., Kim, N., Kwon, M., Kim, N. Y., Kim, H. J., Lee, Y. J., Seo, E. K., Jeong, W. Skullcapflavone II inhibits osteoclastogenesis by regulating reactive oxygen species and attenuates the survival and resorption function of osteoclasts by modulating integrin signaling.
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http://dx.doi.org/10.1096/fj.201800866RRDOI Listing
February 2019

The Trajectories of the Number of Pain Sites and Their Associated Factors in Older Adults: Results from the Korean Longitudinal Study of Ageing.

Gerontology 2018 3;64(6):532-540. Epub 2018 Jul 3.

Department of Public Health Science, Graduate School of Public Health, Seoul National University, Seoul, Republic of Korea.

Background: The aging of the population will result in an increase in demand for pain management. Pain adversely affects physical and mental functioning in older adults and accounts for a considerable proportion of all medical expenses.

Objectives: This study was performed to investigate the patterns of changes in the trajectories of the number of pain sites in older adults and the factors that affect these patterns according to gender.

Methods: Data were extracted for subjects that participated in the Korean Longitudinal Study of Ageing from 2006 to 2014. The study population consisted of 2,839 individuals (1,190 men and 1,649 women) ≥60 years old. A group-based trajectory model was used to determine the optimal number of subgroups and the trajectories of the number of pain sites according to gender. A multinomial regression analysis was conducted to identify factors that affect the probability of inclusion in each trajectory group.

Results: The trajectories of the number of pain sites were consistent in both genders. Almost all women had one or more pain symptom, and a greater number of pain sites than men. Older age, longest-duration occupation requiring manual labor, lack of physical activity, depressive symptoms, and poor self-rated health were associated with a greater number of pain sites in both genders. A lower level of education, married status, and experience of injury were associated with the number of pain sites in men but not in women, while household income and chronic diseases were associated with the number of pain sites only in women.

Conclusions: The pain status at the early stage is predictive of future pain. In this study, we identified gender differences in the trends of the number of pain sites and associated factors. Further comprehensive studies on pain intensity and duration are required.
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http://dx.doi.org/10.1159/000490051DOI Listing
January 2019

Euphorbia factor L1 inhibits osteoclastogenesis by regulating cellular redox status and induces Fas-mediated apoptosis in osteoclast.

Free Radic Biol Med 2017 11 31;112:191-199. Epub 2017 Jul 31.

Department of Life Science and the Research Center for Cellular Homeostasis, Ewha Womans University, Seoul 120-750, Republic of Korea. Electronic address:

Excessive bone resorption caused by increased osteoclast number or activity leads to a variety of bone diseases including osteoporosis, rheumatoid arthritis and periodontitis. Thus, the therapeutic strategy for these diseases has been focused primarily on the inhibition of osteoclast formation and function. This study shows that euphorbia factor L1 (EFL1), a diterpenoid isolated from Euphorbia lathyris, inhibited osteoclastogenesis and induced osteoclast apoptosis. EFL1 suppressed osteoclast formation and bone resorption at both initial and terminal differentiation stages. EFL1 inhibited receptor activator of NF-κB ligand (RANKL)-induced NFATc1 induction with attenuated NF-κB activation and c-Fos expression. EFL1 decreased the level of reactive oxygen species by scavenging them or activating Nrf2, and inhibited PGC-1β that regulates mitochondria biogenesis. In addition, EFL1 induced apoptosis in differentiated osteoclasts by increasing Fas ligand expression followed by caspase activation. Moreover, EFL1 inhibited inflammation-induced bone erosion and ovariectomy-induced bone loss in mice. These findings suggest that EFL1 inhibits osteoclast differentiation by regulating cellular redox status and induces Fas-mediated apoptosis in osteoclast, and may provide therapeutic potential for preventing or treating bone-related diseases caused by excessive osteoclast.
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http://dx.doi.org/10.1016/j.freeradbiomed.2017.07.030DOI Listing
November 2017

Gender differences in the trajectories and the risk factors of depressive symptoms in later life.

Int Psychogeriatr 2017 09 25;29(9):1495-1505. Epub 2017 May 25.

Department of Public Health Science,Graduate School of Public Health,Seoul National University,Seoul,South Korea.

Background: The present study investigated changes in the trajectories of depressive symptoms in the elderly and attempted to identify risk factors that influence these changes according to gender.

Methods: All data were obtained from a subsample of subjects who participated in the Korean Longitudinal Study of Ageing between 2006 and 2012; 3,667 individuals (1,566 men and 2,101 women) aged 60 years and older were included in the present study. A group-based trajectory model was employed to determine the appropriate number of groups and to observe changes in depressive symptoms according to research year. Following the trajectory analysis, a multinomial regression analysis was performed to examine depressive symptom-related risk factors that influenced membership in the different trajectory groups.

Results: Significant gender differences were found in the trajectories of depressive symptoms among four groups (normal, mild depressed, worsening, and depressed) in men and five groups (normal, mild depressed, worsening, improving, and depressed) in women. Among the trajectory groups, physical health status such as chronic diseases, self-rated health (SRH), and somatic pain showed statistically significant differences in both genders. In addition, employment in men and social participation in women were associated with the trajectories.

Conclusions: The present study suggested that maintaining one's physical health status played an important role in preventing depressive symptoms and that employment in men and social participation in women were preventative against the development of depressive symptoms.
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http://dx.doi.org/10.1017/S1041610217000709DOI Listing
September 2017

Life course indices for social determinants of self-rated health trajectory in Korean elderly.

Arch Gerontol Geriatr 2017 May - Jun;70:186-194. Epub 2017 Feb 7.

Red Cross College of Nursing, Chung-Ang University, Seoul, South Korea. Electronic address:

Objectives: This study investigated the self-rated health trajectories of the Korean older population and revealed life-course factors that affect the trajectories over the life course.

Methods: Around 1000 older adults were randomly allocated by stratified multi-stage sampling based on the population census, and underwent face-to-face interviews. Self-rated health status, socioeconomic variables over the life course, and demographic variables were included in the analysis. A group-based trajectory model was used to investigate the association between self-rated health and explanatory variables.

Results: The enrolled men and women were divided into three groups by trajectory analysis, which showed marked differences in self-rated health trajectories from childhood to senescence. Among older men, those who experienced skipping meals in childhood and those with chronic disease conditions were more likely to be in the lower trajectory groups. Compared to the older men, the likelihood of being in the lower trajectory groups in older women was increased by experience of skipping meals, lower household income, housekeeping labor, receiving Basic Livelihood Security and chronic disease conditions.

Conclusion: Various self-rated health trajectories of the Korean older population were identified, and differed according to socioeconomic variables during their life course. Therefore, socioeconomic variables during the life course should be monitored, and health policies directed at the elderly should focus on initial health status from the perspective of a life-course approach.
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http://dx.doi.org/10.1016/j.archger.2017.02.003DOI Listing
July 2017

An Ionic 1,4-Bis(styryl)benzene-Based Fluorescent Probe for Mercury(II) Detection in Water via Deprotection of the Thioacetal Group.

Sensors (Basel) 2016 Dec 7;16(12). Epub 2016 Dec 7.

Department of Chemistry, Korea University, Seoul 02841, Korea.

Highly sensitive and selective mercury detection in aqueous media is urgently needed because mercury poisoning usually results from exposure to water-soluble forms of mercury by inhalation and/or ingesting. An ionic conjugated oligoelectrolye (M1Q) based on 1,4-bis(styryl)benzene was synthesized as a fluorescent mercury(II) probe. The thioacetal moiety and quaternized ammonium group were incorporated for Hg recognition and water solubility. A neutral Hg probe (M1) was also prepared based on the same molecular backbone, and their sensor characteristics were investigated in a mixture of acetonitrile/water and in water. In the presence of Hg, the thioacetal group was converted to aldehyde functionality, and the resulting photoluminescence intensity decreased. In water, M1Q successfully demonstrated highly sensitive detection, showing a binding toward Hg that was ~15 times stronger and a signal on/off ratio twice as high, compared to M1 in acetonitrile/water. The thioacetal deprotection by Hg ions was substantially facilitated in water without an organic cosolvent. The limit of detection was measured to be 7 nM with a detection range of 10-180 nM in 100% aqueous medium.
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http://dx.doi.org/10.3390/s16122082DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5191063PMC
December 2016

Effective killing of cancer cells and regression of tumor growth by K27 targeting sulfiredoxin.

Free Radic Biol Med 2016 12 5;101:384-392. Epub 2016 Nov 5.

Department of Life Science and the Research Center for Cellular Homeostasis, Ewha Womans University, Seoul 120-750, South Korea. Electronic address:

Cancer cells have been suggested to be more susceptible to oxidative damages and highly dependent on antioxidant capacity in comparison with normal cells, and thus targeting antioxidant enzymes has been a strategy for effective cancer treatment. Sulfiredoxin (Srx) is an enzyme that catalyzes the reduction of sulfinylated peroxiredoxins and thereby reactivates them. In this study we developed a Srx inhibitor, K27 (N-[7-chloro-2-(4-fluorophenyl)-4-quinazolinyl]-N-(2-phenylethyl)-β-alanine), and showed that it induces the accumulation of sulfinylated peroxiredoxins and oxidative stress, which leads to mitochondrial damage and apoptotic death of cancer cells. The effects of K27 were significantly reversed by ectopic expression of Srx or antioxidant N-acetyl cysteine. In addition, K27 led to preferential death of tumorigenic cells over non-tumorigenic cells, and suppressed the growth of xenograft tumor without acute toxicity. Our results suggest that targeting Srx might be an effective therapeutic strategy for cancer treatment through redox-mediated cell death.
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http://dx.doi.org/10.1016/j.freeradbiomed.2016.11.001DOI Listing
December 2016

Immune tolerance to an intestine-adapted bacteria, Chryseobacterium sp., injected into the hemocoel of Protaetia brevitarsis seulensis.

Sci Rep 2016 08 17;6:31722. Epub 2016 Aug 17.

Department of Applied Biology, College of Agriculture and Life Science, Environment Friendly Agriculture Center, Kangwon National University, Chuncheon, Republic of Korea.

To explore the interaction of gut microbes and the host immune system, bacteria were isolated from the gut of Protaetia brevitarsis seulensis larvae. Chryseobacterium sp., Bacillus subtilis, Arthrobacter arilaitensis, Bacillus amyloliquefaciens, Bacillus megaterium, and Lysinibacillus xylanilyticus were cultured in vitro, identified, and injected in the hemocoel of P. brevitarsis seulensis larvae, respectively. There were no significant changes in phagocytosis-associated lysosomal formation or pathogen-related autophagosome in immune cells (granulocytes) from Chryseobacterium sp.-challenged larvae. Next, we examined changes in the transcription of innate immune genes such as peptidoglycan recognition proteins and antimicrobial peptides following infection with Chryseobacterium sp. PGRP-1 and -2 transcripts, which may be associated with melanization generated by prophenoloxidase (PPO), were either highly or moderately expressed at 24 h post-infection with Chryseobacterium sp. However, PGRP-SC2 transcripts, which code for bactericidal amidases, were expressed at low levels. With respect to antimicrobial peptides, only coleoptericin was moderately expressed in Chryseobacterium sp.-challenged larvae, suggesting maintenance of an optimum number of Chryseobacterium sp. All examined genes were expressed at significantly higher levels in larvae challenged with a pathogenic bacterium. Our data demonstrated that gut-inhabiting bacteria, the Chryseobacterium sp., induced a weaker immune response than other pathogenic bacteria, E. coli K12.
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http://dx.doi.org/10.1038/srep31722DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4987663PMC
August 2016

cDNA cloning and molecular characterization of a defensin-like antimicrobial peptide from larvae of Protaetia brevitarsis seulensis (Kolbe).

Mol Biol Rep 2016 May 12;43(5):371-9. Epub 2016 Mar 12.

Department of Applied Biology, Division of Bioresource Science, College of Agriculture and Life Science, Kangwon National University, Kangwon-do, Chuncheon, 200-701, Republic of Korea.

We identified new defensin-like cDNA (called Psdefensin) by searching data set of high-throughput RNA sequencing (RNA-seq) expression profiling of immunized larva of white-spotted flower chafers, Protaetia brevitarsis seulensis. The length of the analyzed new defensin-like sequences were 240 base pair (bp) and encoded the deduced polypeptide of 79 amino acid residues with signal peptides (amino acids 1-20), pro-peptide region (amino acids 21-36), and mature peptide region (amino acids 37-79). The Psdefensin transcript levels were slightly up-regulated at 4 h post-infection and were highly expressed at 8 h post-infection compared to control larvae injected with sterile water. In addition, the Psdefensin did have antimicrobial activity against both Gram-negative bacteria, E. coli and Gram-positive bacteria, B. subtilis suggesting potentially pharmacologic agent.
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http://dx.doi.org/10.1007/s11033-016-3967-1DOI Listing
May 2016

Epidermis-Derived Semaphorin Promotes Dendrite Self-Avoidance by Regulating Dendrite-Substrate Adhesion in Drosophila Sensory Neurons.

Neuron 2016 Feb 4;89(4):741-55. Epub 2016 Feb 4.

Howard Hughes Medical Institute, Departments of Physiology, Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA. Electronic address:

Precise patterning of dendritic arbors is critical for the wiring and function of neural circuits. Dendrite-extracellular matrix (ECM) adhesion ensures that the dendrites of Drosophila dendritic arborization (da) sensory neurons are properly restricted in a 2D space, and thereby facilitates contact-mediated dendritic self-avoidance and tiling. However, the mechanisms regulating dendrite-ECM adhesion in vivo are poorly understood. Here, we show that mutations in the semaphorin ligand sema-2b lead to a dramatic increase in self-crossing of dendrites due to defects in dendrite-ECM adhesion, resulting in a failure to confine dendrites to a 2D plane. Furthermore, we find that Sema-2b is secreted from the epidermis and signals through the Plexin B receptor in neighboring neurons. Importantly, we find that Sema-2b/PlexB genetically and physically interacts with TORC2 complex, Tricornered (Trc) kinase, and integrins. These results reveal a novel role for semaphorins in dendrite patterning and illustrate how epidermal-derived cues regulate neural circuit assembly.
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http://dx.doi.org/10.1016/j.neuron.2016.01.020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4760923PMC
February 2016

Sulfiredoxin inhibitor induces preferential death of cancer cells through reactive oxygen species-mediated mitochondrial damage.

Free Radic Biol Med 2016 Feb 23;91:264-74. Epub 2015 Dec 23.

Department of Life Science and the Research Center for Cellular Homeostasis, Ewha Womans University, Seoul 120-750, South Korea. Electronic address:

Recent studies have shown that many types of cancer cells have increased levels of reactive oxygen species (ROS) and enhance antioxidant capacity as an adaptation to intrinsic oxidative stress, suggesting that cancer cells are more vulnerable to oxidative insults and are more dependent on antioxidant systems compared with normal cells. Thus, disruption of redox homeostasis caused by a decline in antioxidant capacity may provide a method for the selective death of cancer cells. Here we show that ROS-mediated selective death of tumor cells can be caused by inhibiting sulfiredoxin (Srx), which reduces hyperoxidized peroxiredoxins, leading to their reactivation. Srx inhibitor increased the accumulation of sulfinic peroxiredoxins and ROS, which led to oxidative mitochondrial damage and caspase activation, resulting in the death of A549 human lung adenocarcinoma cells. Srx depletion also inhibited the growth of A549 cells like Srx inhibition, and the cytotoxic effects of Srx inhibitor were considerably reversed by Srx overexpression or antioxidants such as N-acetyl cysteine and butylated hydroxyanisol. Moreover, Srx inhibitor rendered tumorigenic ovarian cells more susceptible to ROS-mediated death compared with nontumorigenic cells and significantly suppressed the growth of A549 xenografts without acute toxicity. Our results suggest that Srx might serve as a novel therapeutic target for cancer treatment based on ROS-mediated cell death.
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http://dx.doi.org/10.1016/j.freeradbiomed.2015.12.023DOI Listing
February 2016

Regulation of dendrite growth and maintenance by exocytosis.

J Cell Sci 2015 Dec 19;128(23):4279-92. Epub 2015 Oct 19.

Department of Molecular and Cellular Pharmacology, University of Miami, Miller School of Medicine, Miami, FL 33136, USA

Dendrites lengthen by several orders of magnitude during neuronal development, but how membrane is allocated in dendrites to facilitate this growth remains unclear. Here, we report that Ras opposite (Rop), the Drosophila ortholog of the key exocytosis regulator Munc18-1 (also known as STXBP1), is an essential factor mediating dendrite growth. Neurons with depleted Rop function exhibit reduced terminal dendrite outgrowth followed by primary dendrite degeneration, suggestive of differential requirements for exocytosis in the growth and maintenance of different dendritic compartments. Rop promotes dendrite growth together with the exocyst, an octameric protein complex involved in tethering vesicles to the plasma membrane, with Rop-exocyst complexes and exocytosis predominating in primary dendrites over terminal dendrites. By contrast, membrane-associated proteins readily diffuse from primary dendrites into terminals, but not in the reverse direction, suggesting that diffusion, rather than targeted exocytosis, supplies membranous material for terminal dendritic growth, revealing key differences in the distribution of materials to these expanding dendritic compartments.
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http://dx.doi.org/10.1242/jcs.174771DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4712815PMC
December 2015

Identification of immunity-related genes in the larvae of Protaetia brevitarsis seulensis (Coleoptera: Cetoniidae) by a next-generation sequencing-based transcriptome analysis.

J Insect Sci 2015 8;15. Epub 2015 Oct 8.

Department of Applied Biology, College of Agriculture and Life Science, Environment Friendly Agriculture Center, Kangwon National University, Chuncheon, South Korea

To identify immune-related genes in the larvae of white-spotted flower chafers, next-generation sequencing was conducted with an Illumina HiSeq2000, resulting in 100 million cDNA reads with sequence information from over 10 billion base pairs (bp) and >50× transcriptome coverage. A subset of 77,336 contigs was created, and ∼35,532 sequences matched entries against the NCBI nonredundant database (cutoff, e < 10(-5)). Statistical analysis was performed on the 35,532 contigs. For profiling of the immune response, samples were analyzed by aligning 42 base sequence tags to the de novo reference assembly, comparing levels in immunized larvae to control levels of expression. Of the differentially expressed genes, 3,440 transcripts were upregulated and 3,590 transcripts were downregulated. Many of these genes were confirmed as immune-related genes such as pattern recognition proteins, immune-related signal transduction proteins, antimicrobial peptides, and cellular response proteins, by comparison to published data.
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http://dx.doi.org/10.1093/jisesa/iev120DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4626668PMC
August 2016
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