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ORIGINAL RESEARCH

miR-146a-5p Promotes the Inflammatory Response in PBMCs Induced by Microcystin-Leucine-Arginine

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Pages 1979-1993 | Received 23 Jan 2023, Accepted 03 May 2023, Published online: 09 May 2023

References

  • Manganelli M, Scardala S, Stefanelli M, et al. Emerging health issues of cyanobacterial blooms. Ann Ist Super Sanita. 2012;48(4):415–428. doi:10.4415/ANN_12_04_09
  • Testai E, Buratti FM, Funari E, et al. Review and analysis of occurrence, exposure and toxicity of cyanobacteria toxins in food. EFSA Support. Publ. 2016;13:998E.
  • Buratti FM, Manganelli M, Vichi S, et al. Cyanotoxins: producing organisms, occurrence, toxicity, mechanism of action and human health toxicological risk evaluation. Arch Toxicol. 2017;91(3):1049–1130. doi:10.1007/s00204-016-1913-6
  • Bormans M, Amzil Z, Mineaud E, et al. Demonstrated transfer of cyanobacteria and cyanotoxins along a freshwater-marine continuum in France. Harmful Algae. 2019;87:101639. doi:10.1016/j.hal.2019.101639
  • Niedermeyer T. Microcystin congeners described in the literature. figshare. 2014. doi:10.6084/m9.figshare.880756.v5
  • Shi L, Du X, Liu H, et al. Update on the adverse effects of microcystins on the liver. Environ Res. 2021;195:110890. doi:10.1016/j.envres.2021.110890
  • Fischer WJ, Altheimer S, Cattori V, et al. Organic anion transporting polypeptides expressed in liver and brain mediate uptake of microcystin. Toxicol Appl Pharmacol. 2005;203(3):257–263. doi:10.1016/j.taap.2004.08.012
  • Svirčev Z, Drobac D, Tokodi N, et al. Toxicology of microcystins with reference to cases of human intoxications and epidemiological investigations of exposures to cyanobacteria and cyanotoxins. Arch Toxicol. 2017;91(2):621–650. doi:10.1007/s00204-016-1921-6
  • Palikova M, Ondrackova P, Mares J, et al. In vivo effects of microcystins and complex cyanobacterial biomass on rats (Rattus norvegicus var. alba): changes in immunological and haematological parameters. Toxicon. 2013;73:1–8. doi:10.1016/j.toxicon.2013.06.016
  • Secombes CJ, Wang T, Hong S, et al. Cytokines and innate immunity of fish. Dev Comp Immunol. 2001;25(8–9):713–723. doi:10.1016/S0145-305X(01)00032-5
  • Ma J, Li Y, Duan H. Chronic exposure of nanomolar MC-LR caused oxidative stress and inflammatory responses in HepG2 cells. Chemosphere. 2018;192:305–317. doi:10.1016/j.chemosphere.2017.10.158
  • Ma Y, Wang J, Xu D, et al. Chronic MC-LR exposure promoted Aβ and p-tau accumulation via regulating Akt/GSK-3β signal pathway. Sci Total Environ. 2021;794:148732. doi:10.1016/j.scitotenv.2021.148732
  • Cao L, Huang F, Massey IY, et al. Effects of microcystin-LR on the microstructure and inflammation-related factors of jejunum in mice. Toxins. 2019;11(9):482. doi:10.3390/toxins11090482
  • Dinarello CA. Interleukin-1. Cytokine Growth Factor Rev. 1997;8(4):253–265. doi:10.1016/S1359-6101(97)00023-3
  • Ksontini R, MacKay SL, Moldawer LL. Revisiting the role of tumor necrosis factor alpha and the response to surgical injury and inflammation. Arch Surg. 1998;133:558–567. doi:10.1001/archsurg.133.5.558
  • Akira S, Taga T, Kishimoto T. Interleukin-6 in biology and medicine. Adv Immunol. 1993;54:1–78. doi:10.1016/s0065-2776(08)60532-5
  • Pulendran B, Artis D. New paradigms in type 2 immunity. Science. 2012;337:431–435. doi:10.1126/science.1221064
  • Liu GJ, Zhang QR, Gao X, et al. MiR-146a ameliorates hemoglobin-induced microglial inflammatory response via TLR4/IRAK1/TRAF6 associated pathways. Front Neurosci. 2020;14:311. doi:10.3389/fnins.2020.00311
  • O’Garra A, Barrat FJ, Castro AG, et al. Strategies for use of IL-10 or its antagonists in human disease. Immunol Rev. 2008;223:114–131. doi:10.1111/j.1600-065X.2008.00635.x
  • Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75(5):843–854. doi:10.1016/0092-8674(93)90529-Y
  • Reinhart BJ, Slack FJ, Basson M, et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature. 2000;403(6772):901–906. doi:10.1038/35002607
  • Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 1993;75(5):855–862. doi:10.1016/0092-8674(93)90530-4
  • Berezikov E, Cuppen E, Plasterk RH. Approaches to microRNA discovery. Nat Genet. 2006;38(Suppl):S2–S7. doi:10.1038/ng1794
  • Ruby JG, Jan C, Player C, et al. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell. 2006;127(6):1193–1207. doi:10.1016/j.cell.2006.10.040
  • Chen M, Wang F, Xia H, et al. MicroRNA-155: regulation of immune cells in sepsis. Mediators Inflamm. 2021;2021:8874854. doi:10.1155/2021/8874854
  • Carissimi C, Fulci V, Macino G. MicroRNAs: novel regulators of immunity. Autoimmun Rev. 2009;8:520–524. doi:10.1016/j.autrev.2009.01.008
  • Ma J, Li Y, Yao L, et al. Analysis of MicroRNA expression profiling involved in MC-LR-induced cytotoxicity by high-throughput sequencing. Toxins. 2017;9(1):23. doi:10.3390/toxins9010023
  • Yang S, Chen L, Wen C, et al. MicroRNA expression profiling involved in MC-LR-induced hepatotoxicity using high-throughput sequencing analysis. J Toxicol Environ Health A. 2018;81(5):89–97. doi:10.1080/15287394.2017.1415580
  • Zhou Y, Wang H, Wang C, et al. Roles of miRNAs in microcystin-LR-induced Sertoli cell toxicity. Toxicol Appl Pharmacol. 2015;287(1):1–8. doi:10.1016/j.taap.2015.05.008
  • Iborra M, Bernuzzi F, Invernizzi P, et al. MicroRNAs in autoimmunity and in flammatory bowel disease: crucial regulators in immune response. Autoimmun Rev. 2012;11:305–314. doi:10.1016/j.autrev.2010.07.002
  • Scrivo R, Vasile M, Bartosiewicz I, et al. Inflammation as “common soil” of the multifactorial diseases. Autoimmun Rev. 2011;10:369–374. doi:10.1016/j.autrev.2010.12.006
  • Friedman RC, Farh KK, Burge CB, et al. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009;19:92–105.
  • Li L, Chen XP, Li YJ. MicroRNA-146a and human disease. Scand J Immunol. 2010;71(4):227–231. doi:10.1111/j.1365-3083.2010.02383.x
  • Chen T, Li Z, Jing T, et al. MicroRNA-146a regulates the maturation process and pro-inflammatory cytokine secretion by targeting CD40L in oxLDL-stimulated dendritic cells. FEBS Lett. 2011;585(3):567–573. doi:10.1016/j.febslet.2011.01.010
  • Zhou C, Zhao L, Wang K, et al. MicroRNA-146a inhibits NF-kB activation and pro-inflammatory cytokine production by regulating IRAK1 expression in THP-1 cells. Exp Ther Med. 2019;18(4):3078–3084. doi:10.3892/etm.2019.7881
  • Sanada T, Sano T, Sotomaru Y, et al. Anti-inflammatory effects of miRNA-146a induced in adipose and periodontal tissues. Biochem Biophys Rep. 2020;22:100757. doi:10.1016/j.bbrep.2020.100757
  • Wang J, Cui Z, Liu L, et al. MiR-146a mimic attenuates murine allergic rhinitis by downregulating TLR4/TRAF6/NF-kB pathway. Immunotherapy. 2019;11(13):1095–1105. doi:10.2217/imt-2019-0047
  • Gram M, Sveinsdottir S, Ruscher K, et al. Hemoglobin induces inflammation after preterm intraventricular hemorrhage by methemoglobin formation. J Neuroinflammation. 2013;10:100.
  • Kwon MS, Woo SK, Kurland DB, et al. Methemoglobin is an endogenous toll-like receptor 4 ligand-relevance to subarachnoid hemorrhage. Int J Mol Sci. 2015;16(3):5028–5046. doi:10.3390/ijms16035028
  • Lin S, Yin Q, Zhong Q, et al. Heme activates TLR4-mediated inflammatory injury via MyD88/TRIF signaling pathway in intracerebral hemorrhage. J Neuroinflammation. 2012;9:46. doi:10.1186/1742-2094-9-46
  • Rey C, Nadjar A, Buaud B, et al. Resolvin D1 and E1 promote resolution of inflammation in microglial cells in vitro. Brain Behav Immun. 2016;55:249–259. doi:10.1016/j.bbi.2015.12.013
  • Taganov KD, Boldin MP, Chang KJ, et al. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA. 2006;103(33):12481–12486. doi:10.1073/pnas.0605298103
  • Campos A, Vasconcelos V. Molecular mechanisms of microcystin toxicity in animal cells. Int J Mol Sci. 2010;11:268–287. doi:10.3390/ijms11010268
  • Redouane EM, El Amrani Zerrifi S, El Khalloufi F, et al. Mode of action and fate of microcystins in the complex soil-plant ecosystems. Chemosphere. 2019;225:270–281. doi:10.1016/j.chemosphere.2019.03.008
  • Chorus Ingrid BJ. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring, and Management. London: Taylor & Francis; 1999.
  • Christen V, Meili N, Fent K. Microcystin-LR induces endoplasmatic reticulum stress and leads to induction of NF-kB, interferon-alpha, and tumor necrosis factor-alpha. Environ Sci Technol. 2013;47(7):3378–3385. doi:10.1021/es304886y
  • Chen L, Zhang X, Chen J, et al. NF-kB plays a key role in microcystin-RR induced HeLa cell proliferation and apoptosis. Toxicon. 2014;87:120–130. doi:10.1016/j.toxicon.2014.06.002
  • Zhang XX, Fu Z, Zhang Z, et al. Microcystin-LR promotes melanoma cell invasion and enhances matrix metalloproteinase-2/-9 expression mediated by NF-κB activation. Environ Sci Technol. 2012;46(20):11319–11326. doi:10.1021/es3024989
  • Essandoh K, Li Y, Huo J, et al. MiRNA-mediated macrophage polarization and its potential role in the regulation of inflammatory response. Shock. 2016;46(2):122–131. doi:10.1097/SHK.0000000000000604
  • Fei Y, Chaulagain A, Wang T, et al. MiR-146a down-regulates inflammatory response by targeting TLR3 and TRAF6 in Coxsackievirus B infection. RNA. 2020;26(1):91–100. doi:10.1261/rna.071985.119
  • Yan F, Wufuer D, Ding J, et al. MicroRNA miR-146a-5p inhibits the inflammatory response and injury of airway epithelial cells via targeting TNF receptor-associated factor 6. Bioengineered. 2021;12(1):1916–1926. doi:10.1080/21655979.2021.1927545
  • Akdis CA. Therapies for allergic inflammation: refining strategies to induce tolerance. Nat Med. 2012;18(5):736–749. doi:10.1038/nm.2754
  • Garo LP, Ajay AK, Fujiwara M, et al. MicroRNA-146a limits tumorigenic inflammation in colorectal cancer. Nat Commun. 2021;12(1):2419. doi:10.1038/s41467-021-22641-y
  • Chen L, Yu L, Zhang R, et al. Correlation of microRNA-146a/b with disease risk, biochemical indices, inflammatory cytokines, overall disease severity, and prognosis of sepsis. Medicine. 2020;99(22):e19754. doi:10.1097/MD.0000000000019754
  • Bauernfeind FG, Horvath G, Stutz A, et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol. 2009;183:787–791. doi:10.4049/jimmunol.0901363
  • Monteleone M, Stow JL, Schroder K. Mechanisms of unconventional secretion of IL-1 family cytokines. Cytokine. 2015;74:213–218. doi:10.1016/j.cyto.2015.03.022
  • Minnone G, De Benedetti F, Bracci-Laudiero L. NGF and its receptors in the regulation of inflammatory response. Int J Mol Sci. 2017;18(5):1028. doi:10.3390/ijms18051028
  • Yi XM, Li M, Chen YD, et al. Reciprocal regulation of IL-33 receptor-mediated inflammatory response and pulmonary fibrosis by TRAF6 and USP38. Proc Natl Acad Sci USA. 2022;119(10):e2116279119. doi:10.1073/pnas.2116279119
  • Daskalaki MG, Tsatsanis C, Kampranis SC. Histone methylation and acetylation in macrophages as a mechanism for regulation of inflammatory responses. J Cell Physiol. 2018;233(9):6495–6507. doi:10.1002/jcp.26497
  • Kumar A, Sharma N, Singh S, et al. Oral vaccine antigen induced immune response signalling pathways: current and future perspectives. J Vaccines Vaccin. 2014;5(3):1–6.
  • Viana I, Roussel S, Defrêne J, et al. Innate and adaptive immune responses toward nanomedicines. Acta Pharm Sin B. 2021;11(4):852–870. doi:10.1016/j.apsb.2021.02.022
  • Bolen CR, Uduman M, Kleinstein SH. Cell subset prediction for blood genomic studies. BMC Bioinform. 2011;12:258. doi:10.1186/1471-2105-12-258
  • Mohr S, Liew CC. The peripheral-blood transcriptome: new insights into disease and risk assessment. Trends Mol Med. 2007;13:422–432. doi:10.1016/j.molmed.2007.08.003
  • Lechner J, Chen M, Hogg RE, et al. Peripheral blood mononuclear cells from neovascular age-related macular degeneration patients produce higher levels of chemokines CCL2 (MCP-1) and CXCL8 (IL-8). J Neuroinflammation. 2017;14(1):42. doi:10.1186/s12974-017-0820-y
  • Ramírez-Pérez S, Hernández-Palma LA, Oregon-Romero E, et al. Downregulation of inflammatory cytokine release from IL-1β and LPS-stimulated PBMC orchestrated by ST2825, a MyD88 dimerisation inhibitor. Molecules. 2020;25(18):4322. doi:10.3390/molecules25184322