CLC number:
On-line Access: 2024-08-27
Received: 2023-10-17
Revision Accepted: 2024-05-08
Crosschecked: 2022-04-22
Cited: 0
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Yuhua LIU, Xiaopeng WAN, Yuan YUAN, Jingjing HUANG, Yijia JIANG, Kaiyue ZHAO, Yan WANG, Yang LIU, Qingqing WANG, Hongchuan JIN. Opposite effects of miR-155 in the initial and later stages of lipopolysaccharide (LPS)-induced inflammatory response[J]. Journal of Zhejiang University Science B, 2021, 22(7): 590-598.
@article{title="Opposite effects of miR-155 in the initial and later stages of lipopolysaccharide (LPS)-induced inflammatory response",
author="Yuhua LIU, Xiaopeng WAN, Yuan YUAN, Jingjing HUANG, Yijia JIANG, Kaiyue ZHAO, Yan WANG, Yang LIU, Qingqing WANG, Hongchuan JIN",
journal="Journal of Zhejiang University Science B",
volume="22",
number="7",
pages="590-598",
year="2021",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2000826"
}
%0 Journal Article
%T Opposite effects of miR-155 in the initial and later stages of lipopolysaccharide (LPS)-induced inflammatory response
%A Yuhua LIU
%A Xiaopeng WAN
%A Yuan YUAN
%A Jingjing HUANG
%A Yijia JIANG
%A Kaiyue ZHAO
%A Yan WANG
%A Yang LIU
%A Qingqing WANG
%A Hongchuan JIN
%J Journal of Zhejiang University SCIENCE B
%V 22
%N 7
%P 590-598
%@ 1673-1581
%D 2021
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2000826
TY - JOUR
T1 - Opposite effects of miR-155 in the initial and later stages of lipopolysaccharide (LPS)-induced inflammatory response
A1 - Yuhua LIU
A1 - Xiaopeng WAN
A1 - Yuan YUAN
A1 - Jingjing HUANG
A1 - Yijia JIANG
A1 - Kaiyue ZHAO
A1 - Yan WANG
A1 - Yang LIU
A1 - Qingqing WANG
A1 - Hongchuan JIN
J0 - Journal of Zhejiang University Science B
VL - 22
IS - 7
SP - 590
EP - 598
%@ 1673-1581
Y1 - 2021
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2000826
Abstract: Although microRNA-155 (miR-155) is considered a pro-inflammatory mediator, cumulative evidence indicates that it also has anti-inflammatory effects in macrophages and dendritic cells. In this study, we identified the dramatic expression changes of more than half of potential miR-155-targeted genes upon lipopolysaccharide (LPS) stimulation; 223 genes were down-regulated and 85 genes were up-regulated, including suppressor of cytokine signaling 1 (SOCS1) and transforming growth factor-β;-activated kinase 1-binding protein 2 (TAB2), two well-known genes involved in miR-155-mediated regulation of the toll-like receptor 4 (TLR4) signaling pathway. We also found that miR-155 acted as an anti-inflammatory mediator in the initial stage of LPS-induced inflammatory response mainly through repressing TAB2 protein translation, and as a pro-inflammatory mediator by down-regulating SOCS1 in the later stage. Meanwhile, overexpression of TAB2 3' untranslated region (UTR) in macrophages promoted the development of endotoxin tolerance by competing for binding with miR-155, which resulted in an elevated expression level of SOCS1 protein. These findings provide new insights for understanding the regulatory mechanisms in fine-tuning of LPS-induced innate immune response.
[1]AndroulidakiA, IliopoulosD, ArranzA, et al., 2009. The kinase Akt1 controls macrophage response to lipopolysaccharide by regulating microRNAs. Immunity, 31(2):220-231.
[2]BossiL, Figueroa-BossiN, 2016. Competing endogenous RNAs: a target-centric view of small RNA regulation in bacteria. Nat Rev Microbiol, 14(12):775-784.
[3]CeppiM, PereiraPM, Dunand-SauthierI, et al., 2009. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci USA, 106(8):2735-2740.
[4]ChenC, LiuJM, LuoYP, 2020. MicroRNAs in tumor immunity: functional regulation in tumor-associated macrophages. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 21(1):12-28.
[5]ChenLQ, SongYJ, HeL, et al., 2016. MicroRNA-223 promotes type I interferon production in antiviral innate immunity by targeting forkhead box protein O3 (FOXO3). J Biol Chem, 291(28):14706-14716.
[6]ChenQY, WangH, LiuY, et al., 2012. Inducible microRNA-223 down-regulation promotes TLR-triggered IL-6 and IL-1β production in macrophages by targeting STAT3. PLoS ONE, 7(8):e42971.
[7]DiwakarBT, YoastR, NettlefordS, et al., 2019. Crth2 receptor signaling down‐regulates lipopolysaccharide‐induced NF‐αB activation in murine macrophages via changes in intracellular calcium. FASEB J, 33(11):12838-12852.
[8]El-SaharAE, ShihaNA, el SayedNS, et al., 2021. Alogliptin attenuates lipopolysaccharide-induced neuroinflammation in mice through modulation of TLR4/MYD88/NF-κB and miRNA-155/SOCS-1 signaling pathways. Int J Neuropsychopharmacol, 24(2):158-169.
[9]FreiseN, BurghardA, OrtkrasT, et al., 2019. Signaling mechanisms inducing hyporesponsiveness of phagocytes during systemic inflammation. Blood, 134(2):134-146.
[10]GattoG, RossiA, RossiD, et al., 2008. Epstein-Barr virus latent membrane protein 1 trans-activates miR-155 transcription through the NF-κB pathway. Nucleic Acids Res, 36(20):6608-6619.
[11]GuoX, ZhengY, 2020. Profiling of miRNAs in mouse peritoneal macrophages responding to Echinococcus multilocularis infection. Front Cell Infect Microbiol, 10:132.
[12]KarrethFA, TayY, PernaD, et al., 2011. In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell, 147(2):382-395.
[13]MartinM, RehaniK, JopeRS, et al., 2005. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat Immunol, 6(8):777-784.
[14]NuzzielloN, LiguoriM, 2019. The microRNA centrism in the orchestration of neuroinflammation in neurodegenerative diseases. Cells, 8(10):1193.
[15]O'ConnellRM, TaganovKD, BoldinMP, et al., 2007. MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA, 104(5):1604-1609.
[16]PiccininiAM, MidwoodKS, 2012. Endogenous control of immunity against infection: tenascin-C regulates TLR4-mediated inflammation via microRNA-155. Cell Rep, 2(4):914-926.
[17]RodriguezA, VigoritoE, ClareS, et al., 2007. Requirement of bic/microRNA-155 for normal immune function. Science, 316(5824):608-611.
[18]RogerT, DavidJ, GlauserMP, et al., 2001. MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature, 414(6866):920-924.
[19]SalmenaL, PolisenoL, TayY, et al., 2011. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell, 146(3):353-358.
[20]SayedAS, el Sayed NSED, 2016. Co-administration of 3-acetyl-11-keto-beta-boswellic acid potentiates the protective effect of celecoxib in lipopolysaccharide-induced cognitive impairment in mice: possible implication of anti-inflammatory and antiglutamatergic pathways. J Mol Neurosci, 59(1):58-67.
[21]SayedAS, GomaaIEO, BaderM, et al., 2018. Role of 3-acetyl-11-keto-beta-boswellic acid in counteracting LPS-induced neuroinflammation via modulation of miRNA-155. Mol Neurobiol, 55(7):5798-5808.
[22]SulOJ, SungYB, RajasekaranM, et al., 2018. MicroRNA-155 induces autophagy in osteoclasts by targeting transforming growth factor β-activated kinase 1-binding protein 2 upon lipopolysaccharide stimulation. Bone, 116:279-289.
[23]TakedaK, KaishoT, AkiraS, 2003. Toll-like receptors. Annu Rev Immunol, 21:335-376.
[24]TangB, XiaoB, LiuZ, et al., 2010. Identification of MyD88 as a novel target of miR-155, involved in negative regulation of Helicobacter pylori-induced inflammation. FEBS Lett, 584(8):1481-1486.
[25]TayY, KatsL, SalmenaL, et al., 2011. Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell, 147(2):344-357.
[26]WanJH, YangXY, RenYP, et al., 2019. Inhibition of miR-155 reduces impaired autophagy and improves prognosis in an experimental pancreatitis mouse model. Cell Death Dis, 10(4):303.
[27]WongD, NielsenTB, BonomoRA, et al., 2017. Clinical and pathophysiological overview of Acinetobacter infections: a century of challenges. Clin Microbiol Rev, 30(1):409-447.
[28]XuCL, RenGW, CaoG, et al., 2013. miR-155 regulates immune modulatory properties of mesenchymal stem cells by targeting TAK1-binding protein 2. J Biol Chem, 288(16):11074-11079.
[29]XuJ, WuKJ, JiaQJ, et al., 2020. Roles of miRNA and lncRNA in triple-negative breast cancer. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 21(9):673-689.
[30]ZhangH, WuZM, YangYP, et al., 2019. Catalpol ameliorates LPS-induced endometritis by inhibiting inflammation and TLR4/NF-κB signaling. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 20(10):816-827.
[31]ZhangM, GillaspyAF, GipsonJR, et al., 2018. Neuroinvasive Listeria monocytogenes infection triggers IFN-activation of microglia and upregulates microglial miR-155. Front Immunol, 9:2751.
[32]ZhangYY, ZhangMY, LiXQ, et al., 2016. Silencing microRNA-155 attenuates cardiac injury and dysfunction in viral myocarditis via promotion of M2 phenotype polarization of macrophages. Sci Rep, 6:22613.
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