Abstract
Neuroinflammation plays a crucial role in the development and progression of neurological disorders. MicroRNA-155 (miR-155), a miR is known to play in inflammatory responses, is associated with susceptibility to inflammatory neurological disorders and neurodegeneration, including Alzheimer’s disease, Parkinson’s disease, multiple sclerosis, and amyotrophic lateral sclerosis as well as epilepsy, stroke, and brain malignancies. MiR-155 damages the central nervous system (CNS) by enhancing the expression of pro-inflammatory cytokines, like IL-1β, IL-6, TNF-α, and IRF3. It also disturbs the blood–brain barrier by decreasing junctional complex molecules such as claudin-1, annexin-2, syntenin-1, and dedicator of cytokinesis 1 (DOCK-1), a hallmark of many neurological disorders. This review discusses the molecular pathways which involve miR-155 as a critical component in the progression of neurological disorders, representing miR-155 as a viable therapeutic target.
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References
Aboulhoda BE, Rashed LA, Ahmed H, Obaya EMM, Ibrahim W, Alkafass MAL, Abd El-Aal SA, ShamsEldeen AM (2021) Hydrogen sulfide and mesenchymal stem cells-extracted microvesicles attenuate LPS-induced Alzheimer’s disease. J Cell Physiol 236(8):5994–6010. https://doi.org/10.1002/jcp.30283
Adly Sadik N, Ahmed Rashed L, Ahmed Abd-El Mawla M (2021) Circulating miR-155 and JAK2/STAT3 axis in acute ischemic stroke patients and its relation to post-ischemic inflammation and associated ischemic stroke risk factors. Int J Gen Med 14:1469–1484. https://doi.org/10.2147/IJGM.S295939
Arena A, Iyer AM, Milenkovic I, Kovacs GG, Ferrer I, Perluigi M, Aronica E (2017) Developmental expression and dysregulation of miR-146a and miR-155 in down’s syndrome and mouse models of down’s syndrome and alzheimer’s disease. Curr Alzheimer Res 14(12):1305–1317. https://doi.org/10.2174/1567205014666170706112701
Asadirad A, Hashemi SM, Baghaei K, Ghanbarian H, Mortaz E, Zali MR, Amani D (2019) Phenotypical and functional evaluation of dendritic cells after exosomal delivery of miRNA-155. Life Sci 219:152–162
Awad H, Bratasz A, Nuovo G, Burry R, Meng X, Kelani H (2018) MiR-155 deletion reduces ischemia-induced paralysis in an aortic aneurysm repair mouse model: Utility of immunohistochemistry and histopathology in understanding etiology of spinal cord paralysis. Ann Diagn Pathol 36:12–20. https://doi.org/10.1016/j.anndiagpath.2018.06.002
Baradaran R, Khoshdel-Sarkarizi H, Kargozar S, Hami J, Mohammadipour A, Sadr-Nabavi A, Peyvandi Karizbodagh M, Kheradmand H, Haghir H (2020) Developmental regulation and lateralisation of the α7 and α4 subunits of nicotinic acetylcholine receptors in developing rat hippocampus. Int J Dev Neurosci 80(4):303–318. https://doi.org/10.1002/jdn.10026
Bigham M, Mohammadipour A, Hosseini M, Malvandi AM, Ebrahimzadeh-Bideskan A (2021) Neuroprotective effects of garlic extract on dopaminergic neurons of substantia nigra in a rat model of Parkinson’s disease: motor and non-motor outcomes. Metab Brain Dis 36(5):927–937. https://doi.org/10.1007/s11011-021-00705-8
Bonifati V, Rizzu P, van Baren MJ, Schaap O, Breedveld GJ, Krieger E (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299(5604):256–259
Bruen R, Fitzsimons S, Belton O (2019) miR-155 in the Resolution of Atherosclerosis. Front Pharmacol 10:463. https://doi.org/10.3389/fphar.2019.00463
Butovsky O, Jedrychowski MP, Cialic R, Krasemann S, Murugaiyan G, Fanek Z (2015) Targeting miR-155 restores abnormal microglia and attenuates disease in SOD1 mice. Ann Neurol 77(1):75–99. https://doi.org/10.1002/ana.24304
Caballero-Garrido E, Pena-Philippides JC, Lordkipanidze T, Bragin D, Yang Y, Erhardt EB, Roitbak T (2015) In Vivo Inhibition of miR-155 Promotes Recovery after Experimental Mouse Stroke. J Neurosci 35(36):12446–12464. https://doi.org/10.1523/JNEUROSCI.1641-15.2015
Caggiu E, Paulus K, Mameli G, Arru G, Sechi GP, Sechi LA (2018) Differential expression of miRNA 155 and miRNA 146a in Parkinson’s disease patients. eNeurologicalSci 13:1–4. doi: https://doi.org/10.1016/j.ensci.2018.09.002.
Cai Z, Li S, Li S, Song F, Zhang Z, Qi G, Li T, Qiu J, Wan J, Sui H, Guo H (2016) Antagonist Targeting microRNA-155 Protects against Lithium-Pilocarpine-Induced Status Epilepticus in C57BL/6 Mice by Activating Brain-Derived Neurotrophic Factor. Front Pharmacol 7:129. https://doi.org/10.3389/fphar.2016.00129
Cao S, Wang Y, Li J, Lv M, Niu H, Tian Y (2016) Tumor-suppressive function of long noncoding RNA MALAT1 in glioma cells by suppressing miR-155 expression and activating FBXW7 function. Am J Cancer Res 6(11):2561–2574
Cardoso AL, Guedes JR, Pereira de Almeida L, Pedroso de Lima MC (2012) miR-155 modulates microglia-mediated immune response by down-regulating SOCS-1 and promoting cytokine and nitric oxide production. Immunology 135(1):73–88. https://doi.org/10.1111/j.1365-2567.2011.03514.x
Ceppi M, Pereira PM, Dunand-Sauthier I, Barras E, Reith W, Santos MA, Pierre P (2009) MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci 106(8):2735–2740
Chai S-D, Li Z-K, Liu R, Liu T, Dong M-F, Tang P-Z, Wang J-T, Ma S-J (2020) The role of miRNA-155 in monocrotaline-induced pulmonary arterial hypertension through c-Fos/NLRP3/caspase-1. Mol Cell Toxicol 16:311–320
Chang Y, Cui M, Fu X, Zhang L, Li X, Li L, Wu J, Sun Z, Zhang X, Li Z (2019) MiRNA-155 regulates lymphangiogenesis in natural killer/T-cell lymphoma by targeting BRG1. Cancer Biol Ther 20(1):31–41
Chen L, Jiang K, Jiang H, Wei P (2014) miR-155 mediates drug resistance in osteosarcoma cells via inducing autophagy. Exp Ther Med 8(2):527–532
Chen J, Li C, Liu W, Yan B, Hu X, Yang F (2019) miRNA-155 silencing reduces sciatic nerve injury in diabetic peripheral neuropathy. J Mol Endocrinol 63(3):227–238
Cunha C, Santos C, Gomes C, Fernandes A, Correia AM, Sebastião AM, Vaz AR, Brites D (2018) Downregulated Glia Interplay and Increased miRNA-155 as Promising Markers to Track ALS at an Early Stage. Mol Neurobiol 55(5):4207–4224. https://doi.org/10.1007/s12035-017-0631-2
Duan W, Chen Y, Wang XR (2018) MicroRNA-155 contributes to the occurrence of epilepsy through the PI3K/Akt/mTOR signaling pathway. Int J Mol Med 42(3):1577–1584
Duan Z, Zhang J, Li J, Pang X, Wang H (2020) Inhibition of microRNA-155 Reduces Neuropathic Pain During Chemotherapeutic Bortezomib via Engagement of Neuroinflammation. Front Oncol 10:416. https://doi.org/10.3389/fonc.2020.00416
D’Urso PI, D’Urso OF, Storelli C, Mallardo M, Gianfreda CD, Montinaro A, Cimmino A, Pietro C, Marsigliante S (2012) miR-155 is up-regulated in primary and secondary glioblastoma and promotes tumour growth by inhibiting GABA receptors. Int J Oncol 41(1):228–234. https://doi.org/10.3892/ijo.2012.1420
Fabian MR, Sonenberg N (2012) The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 19:586–593
Fu H, Cheng Y, Luo H, Rong Z, Li Y, Lu P (2019a) Silencing MicroRNA-155 Attenuates Kainic Acid-Induced Seizure by Inhibiting Microglia Activation. NeuroImmunoModulation 26(2):67–76. https://doi.org/10.1159/000496344
Fu Y, Sun S, Sun H, Peng J, Ma X, Bao L, Ji R, Luo C, Gao C, Zhang X, Jin Y (2019b) Scutellarin exerts protective effects against atherosclerosis in rats by regulating the Hippo-FOXO3A and PI3K/AKT signaling pathways. J Cell Physiol 234(10):18131–18145. https://doi.org/10.1002/jcp.28446
Ge X, Tang P, Rong Y, Jiang D, Lu X, Ji C (2021) Exosomal miR-155 from M1-polarized macrophages promotes EndoMT and impairs mitochondrial function via activating NF-κB signaling pathway in vascular endothelial cells after traumatic spinal cord injury. Redox Biol 41:101932. https://doi.org/10.1016/j.redox.2021.101932
Gerloff D, Grundler R, Wurm A, Bräuer-Hartmann D, Katzerke C, Hartmann J, Madan V, Müller-Tidow C, Duyster J, Tenen DG (2015) NF-κB/STAT5/miR-155 network targets PU. 1 in FLT3-ITD-driven acute myeloid leukemia. Leukemia 29(3):535–547
Gloire G, Erneux C, Piette J (2007) The role of SHIP1 in T-lymphocyte life and death. Biochem Soc Trans 35(Pt 2):277–280. https://doi.org/10.1042/BST0350277
Gomes C, Sequeira C, Barbosa M, Cunha C, Vaz AR, Brites D (2020) Astrocyte regional diversity in ALS includes distinct aberrant phenotypes with common and causal pathological processes. Exp Cell Res 395(2):112209. https://doi.org/10.1016/j.yexcr.2020.112209
Gracias DT, Stelekati E, Hope JL, Boesteanu AC, Doering TA, Norton J, Mueller YM, Fraietta JA, Wherry EJ, Turner M, Katsikis PD (2013) The microRNA miR-155 controls CD8(+) T cell responses by regulating interferon signaling. Nat Immunol 14(6):593–602. https://doi.org/10.1038/ni.2576
Guedes JR, Santana I, Cunha C, Duro D, Almeida MR, Cardoso AM, de Lima MC, Cardoso AL (2015) MicroRNA deregulation and chemotaxis and phagocytosis impairment in Alzheimer’s disease. Alzheimers Dement (amst) 3:7–17. https://doi.org/10.1016/j.dadm.2015.11.004
Han T, Qin Y, Mou C, Wang M, Jiang M, Liu B (2016) Seizure induced synaptic plasticity alteration in hippocampus is mediated by IL-1β receptor through PI3K/Akt pathway. Am J Transl Res 8(10):4499–4509
Han C, Guo L, Yang Y, Guan Q, Shen H, Sheng Y, Jiao Q (2020) Mechanism of microRNA-22 in regulating neuroinflammation in Alzheimer’s disease. Brain Behav 10(6):e01627. https://doi.org/10.1002/brb3.1627
Harquail J, LeBlanc N, Landry C, Crapoulet N, Robichaud GA (2018) Pax-5 inhibits NF-κB activity in breast cancer cells through IKKε and miRNA-155 effectors. J Mammary Gland Biol Neoplasia 23(3):177–187
Hausser J, Zavolan M (2014) Identification and consequences of miRNA-target interactions-beyond repression of gene expression. Nat Rev Genet 15:599–612
Heidari Z, Mohammadipour A, Haeri P, Ebrahimzadeh-Bideskan A (2019) The effect of titanium dioxide nanoparticles on mice midbrain substantia nigra. Iran J Basic Med Sci 22(7):745–751. https://doi.org/10.22038/ijbms.2019.33611.8018
Henry RJ, Doran SJ, Barrett JP, Meadows VE, Sabirzhanov B, Stoica BA, Loane DJ, Faden AI (2019) Inhibition of miR-155 limits neuroinflammation and improves functional recovery after experimental traumatic brain injury in mice. Neurotherapeutics 16(1):216–230. https://doi.org/10.1007/s13311-018-0665-9
Heyn J, Luchting B, Hinske LC, Hübner M, Azad SC, Kreth S (2016) miR-124a and miR-155 enhance differentiation of regulatory T cells in patients with neuropathic pain. J Neuroinflammation 13(1):1–11
Hou L, Chen J, Zheng Y, Wu C (2016) Critical role of miR-155/FoxO1/ROS axis in the regulation of non-small cell lung carcinomas. Tumor Biol 37(4):5185–5192
Izrael M, Slutsky SG, Revel M (2020) Rising stars: astrocytes as a therapeutic target for ALS disease. Front Neurosci 14:824. https://doi.org/10.3389/fnins.2020.00824
Jiang K, Yang J, Guo S, Zhao G, Wu H, Deng G (2019) Peripheral circulating exosome-mediated delivery of miR-155 as a novel mechanism for acute lung inflammation. Mol Ther 27(10):1758–1771. https://doi.org/10.1016/j.ymthe.2019.07.003
Kaltschmidt B, Linker RA, Deng J, Kaltschmidt C (2002) Cyclooxygenase-2 is a neuronal target gene of NF-kappaB. BMC Mol Biol 3:16. https://doi.org/10.1186/1471-2199-3-16
Kasper LH, Shoemaker J (2010) Multiple sclerosis immunology: The healthy immune system vs the MS immune system. Neurology 74(Suppl 1):S2-8. https://doi.org/10.1212/WNL.0b013e3181c97c8f
Kim JH, Jou I, Joe EH (2014) Suppression of miR-155 expression in IFN-γ-treated astrocytes and microglia by DJ-1: a possible mechanism for maintaining SOCS1 expression. Exp Neurobiol 23(2):148–154. https://doi.org/10.5607/en.2014.23.2.148
Koch M, Mollenkopf H-J, Klemm U, Meyer TF (2012) Induction of microRNA-155 is TLR-and type IV secretion system-dependent in macrophages and inhibits DNA-damage induced apoptosis. Proc Natl Acad Sci 109:1153–1162
Kong H, Yin F, He F, Omran A, Li L, Wu T, Wang Y, Peng J (2015) The effect of miR-132, miR-146a, and miR-155 on MRP8/TLR4-induced astrocyte-related inflammation. J Mol Neurosci 57(1):28–37. https://doi.org/10.1007/s12031-015-0574-x
Korotkov A, Broekaart DWM, van Scheppingen J, Anink JJ, Baayen JC, Idema S, Gorter JA, Aronica E, van Vliet EA (2018) Increased expression of matrix metalloproteinase 3 can be attenuated by inhibition of microRNA-155 in cultured human astrocytes. J Neuroinflammation 15(1):211. https://doi.org/10.1186/s12974-018-1245-y
Kou X, Chen D, Chen N (2020) The regulation of microRNAs in Alzheimer’s disease. Front Neurol 11:288. https://doi.org/10.3389/fneur.2020.00288
Kouhkan F, Alizadeh S, Kaviani S, Soleimani M, Pourfathollah AA, Amirizadeh N, Abroun S, Noruzinia M, Mohamadi S (2011) miR-155 down regulation by LNA inhibitor can reduce cell growth and proliferation in PC12 cell line. Avicenna J Med Biotechnol 3(2):61–66 (PMID: 23408179)
Krol J, Loedige I, Filipowicz W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11:597–610
Lao G, Liu P, Wu Q, Zhang W, Liu Y, Yang L, Ma C (2014) Mir-155 promotes cervical cancer cell proliferation through suppression of its target gene LKB1. Tumor Biology 35(12):11933–11938
Lashine Y, Salah S, Aboelenein H, Abdelaziz A (2015) Correcting the expression of miRNA-155 represses PP2Ac and enhances the release of IL-2 in PBMCs of juvenile SLE patients. Lupus 24(3):240–247
Lee JY, Han SH, Park MH, Baek B, Song IS, Choi MK (2018) Neuronal SphK1 acetylates COX2 and contributes to pathogenesis in a model of Alzheimer’s Disease. Nat Commun 9(1):1479. https://doi.org/10.1038/s41467-018-03674-2
Li TR, Jia YJ, Wang Q, Shao XQ, Zhang P, Lv RJ (2018) Correlation between tumor necrosis factor alpha mRNA and microRNA-155 expression in rat models and patients with temporal lobe epilepsy. Brain Res 1700:56–65. https://doi.org/10.1016/j.brainres.2018.07.013
Lind EF, Millar DG, Dissanayake D, Savage JC, Grimshaw NK, Kerr WG, Ohashi PS (2015) miR-155 upregulation in dendritic cells is sufficient to break tolerance in vivo by negatively regulating SHIP1. J Immunol 195(10):4632–4640. https://doi.org/10.4049/jimmunol.1302941
Ling N, Gu J, Lei Z, Li M, Zhao J, Zhang HT, Li X (2013) microRNA-155 regulates cell proliferation and invasion by targeting FOXO3a in glioma. Oncol Rep 30(5):2111–2118. https://doi.org/10.3892/or.2013.2685
Liu S, Yang Y, Wu J (2011) TNFα-induced up-regulation of miR-155 inhibits adipogenesis by down-regulating early adipogenic transcription factors. Biochem Biophys Res Commun 414(3):618–624
Liu Q, Zou R, Zhou R, Gong C, Wang Z, Cai T, Tan C, Fang J (2015) miR-155 Regulates glioma cells invasion and chemosensitivity by p38 isforms in vitro. J Cell Biochem 116(7):1213–1221. https://doi.org/10.1002/jcb.25073
Liu N, Jiang F, Han X, Li M, Chen W, Liu Q, Liao C, Lv Y (2018) MiRNA-155 promotes the invasion of colorectal cancer SW-480 cells through regulating the Wnt/beta-catenin. Eur Rev Med Pharmacol Sci 22(1):101–109
Liu D, Zhao D, Zhao Y, Wang Y, Zhao Y, Wen C (2019) Inhibition of microRNA-155 alleviates cognitive impairment in alzheimer’s disease and involvement of neuroinflammation. Curr Alzheimer Res 16(6):473–482. https://doi.org/10.2174/1567205016666190503145207
Lopez-Ramirez MA, Wu D, Pryce G, Simpson JE, Reijerkerk A, King-Robson J (2014) MicroRNA-155 negatively affects blood-brain barrier function during neuroinflammation. FASEB J 28(6):2551–2565. https://doi.org/10.1096/fj.13-248880
Louafi F, Martinez-Nunez RT, Sanchez-Elsner T (2010) MicroRNA-155 targets SMAD2 and modulates the response of macrophages to transforming growth factor-β. J Biol Chem 285(53):41328–41336
Lu Y, Huang Z, Hua Y, Xiao G (2018) Minocycline promotes BDNF expression of N2a cells via inhibition of miR-155-mediated repression after oxygen-glucose deprivation and reoxygenation. Cell Mol Neurobiol 38(6):1305–1313. https://doi.org/10.1007/s10571-018-0599-0
Ma S, Fan L, Li J, Zhang B, Yan Z (2020) Resveratrol promoted the M2 polarization of microglia and reduced neuroinflammation after cerebral ischemia by inhibiting miR-155. Int J Neurosci 130(8):817–825. https://doi.org/10.1080/00207454.2019.1707817
Maciak K, Dziedzic A, Miller E, Saluk-Bijak J (2021) miR-155 as an important regulator of multiple sclerosis pathogenesis. A Review Int J Mol Sci 22(9):4332. https://doi.org/10.3390/ijms22094332
Manni I, Tunici P, Cirenei N, Albarosa R, Colombo BM, Roz L, Sacchi A, Piaggio G, Finocchiaro G (2002) Mxi1 inhibits the proliferation of U87 glioma cells through down-regulation of cyclin B1 gene expression. Br J Cancer 86(3):477–484. https://doi.org/10.1038/sj.bjc.6600065
Mantzavinos V, Alexiou A (2017) Biomarkers for Alzheimer’s disease diagnosis. Curr Alzheimer Res 14(11):1149–1154. https://doi.org/10.2174/1567205014666170203125942
Mogi M, Togari A, Kondo T, Mizuno Y, Komure O, Kuno S, Ichinose H, Nagatsu T (2000) Caspase activities and tumor necrosis factor receptor R1 (p55) level are elevated in the substantia nigra from parkinsonian brain. J Neural Transm (vienna) 107(3):335–341. https://doi.org/10.1007/s007020050028
Mohammadipour A, Abudayyak M (2021) Hippocampal toxicity of metal base nanoparticles. Is there a relationship between nanoparticles and psychiatric disorders? Rev Environ Health. https://doi.org/10.1515/reveh-2021-0006
Mohammadipour A, Haghir H, Ebrahimzadeh Bideskan A (2020) A link between nanoparticles and Parkinson’s disease. Which nanoparticles are most harmful? Rev Environ Health 35(4):545–556. https://doi.org/10.1515/reveh-2020-0043
Murugaiyan G, Beynon V, Mittal A, Joller N, Weiner HL (2011) Silencing microRNA-155 ameliorates experimental autoimmune encephalomyelitis. J Immunol 187(5):2213–2221. https://doi.org/10.4049/jimmunol.1003952
Nampoothiri SS, Krishnamurthy RG (2016) Commentary: targeted inhibition of miR-155 promotes post-stroke neovascularization and functional recovery. CNS Neurol Disord Drug Targets 15(4):372–374. https://doi.org/10.2174/187152731504160328163830
Nazari-Jahantigh M, Wei Y, Noels H, Akhtar S, Zhou Z, Koenen RR, Heyll K, Gremse F, Kiessling F, Grommes J (2012) MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J Clin Investig 122(11):4190–4202
Nielsen JA, Lau P, Maric D, Barker JL, Hudson LD (2009) Integrating microRNA and mRNA expression profiles of neuronal progenitors to identify regulatory networks underlying the onset of cortical neurogenesis. BMC Neurosci 10:98. https://doi.org/10.1186/1471-2202-10-98
Noorbakhsh F, Ellestad KK, Maingat F, Warren KG, Han MH, Steinman L, Baker GB, Power C (2011) Impaired neurosteroid synthesis in multiple sclerosis. Brain 134(Pt 9):2703–2721. https://doi.org/10.1093/brain/awr200
Oliveira SR, Dionísio PA, Correia Guedes L, Gonçalves N, Coelho M, Rosa MM, Amaral JD, Ferreira JJ, Rodrigues CMP (2020) Circulating inflammatory miRNAs associated with parkinson’s disease pathophysiology. Biomolecules 10(6):945. https://doi.org/10.3390/biom10060945
Paraboschi EM, Soldà G, Gemmati D, Orioli E, Zeri G, Benedetti MD, Salviati A, Barizzone N, Leone M, Duga S, Asselta R (2011) Genetic association and altered gene expression of mir-155 in multiple sclerosis patients. Int J Mol Sci 12(12):8695–8712. https://doi.org/10.3390/ijms12128695
Pasquinelli AE (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13:271–282
Pegoraro V, Marozzo R, Angelini C (2020) MicroRNAs and HDAC4 protein expression in the skeletal muscle of ALS patients. Clin Neuropathol 39(3):105–114. https://doi.org/10.5414/NP301233
Rana A, Musto AE (2018) The role of inflammation in the development of epilepsy. J Neuroinflammation 15(1):144. https://doi.org/10.1186/s12974-018-1192-7
Rastegar-Moghaddam SH, Mohammadipour A, Hosseini M, Bargi R, Ebrahimzadeh-Bideskan A (2019) Maternal exposure to atrazine induces the hippocampal cell apoptosis in mice offspring and impairs their learning and spatial memory. Toxin Reviews 38(4):298–306. https://doi.org/10.1080/15569543.2018.1466804
Recio C, Oguiza A, Lazaro I, Mallavia B, Egido J, Gomez-Guerrero C (2014) Suppressor of cytokine signaling 1-derived peptide inhibits Janus kinase/signal transducers and activators of transcription pathway and improves inflammation and atherosclerosis in diabetic mice. Arterioscler Thromb Vasc Biol 34(9):1953–1960. https://doi.org/10.1161/ATVBAHA.114.304144
Rizzuti M, Filosa G, Melzi V, Calandriello L, Dioni L, Bollati V, Bresolin N, Comi GP, Barabino S, Nizzardo M (2018) MicroRNA expression analysis identifies a subset of downregulated miRNAs in ALS motor neuron progenitors. Sci Rep 8:1–12
Sandhu SK, Volinia S, Costinean S, Galasso M, Neinast R, Santhanam R, Parthun MR, Perrotti D, Marcucci G, Garzon R (2012) miR-155 targets histone deacetylase 4 (HDAC4) and impairs transcriptional activity of B-cell lymphoma 6 (BCL6) in the Eµ-miR-155 transgenic mouse model. Proc Natl Acad Sci 109(49):20047–20052
Seddiki N, Brezar V, Ruffin N, Lévy Y, Swaminathan S (2014) Role of miR-155 in the regulation of lymphocyte immune function and disease. Immunology 142(1):32–38. https://doi.org/10.1111/imm.12227
Snow WM, Albensi BC (2016) Neuronal gene targets of NF-κB and their dysregulation in alzheimer’s disease. Front Mol Neurosci 9:118. https://doi.org/10.3389/fnmol.2016.00118
Soria Lopez JA, González HM, Léger GC (2019) Alzheimer’s disease. Handb Clin Neurol 167:231–255. https://doi.org/10.1016/B978-0-12-804766-8.00013-3
Strebovsky J, Walker P, Lang R, Dalpke AH (2011) Suppressor of cytokine signaling 1 (SOCS1) limits NFkappaB signaling by decreasing p65 stability within the cell nucleus. FASEB J 25(3):863–874. https://doi.org/10.1096/fj.10-170597
Sun J, Shi H, Lai N, Liao K, Zhang S, Lu X (2014) Overexpression of microRNA-155 predicts poor prognosis in glioma patients. Med Oncol 31(4):911. https://doi.org/10.1007/s12032-014-0911-x
Sun L, Ji S, Xing J (2019) Inhibition of microRNA-155 alleviates neurological dysfunction following transient global ischemia and contribution of neuroinflammation and oxidative stress in the hippocampus. Curr Pharm Des 25(40):4310–4317. https://doi.org/10.2174/1381612825666190926162229
Tan Y, Yang J, Xiang K, Tan Q, Guo Q (2015) Suppression of microRNA-155 attenuates neuropathic pain by regulating SOCS1 signalling pathway. Neurochem Res 40(3):550–560. https://doi.org/10.1007/s11064-014-1500-2
Tang B, Xiao B, Liu Z, Li N, Zhu ED, Li BS, Xie QH, Zhuang Y, Zou QM, Mao XH (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
Tao Y, Ai R, Hao Y, Jiang L, Dan H, Ji N, Zeng X, Zhou Y, Chen Q (2019) Role of miR-155 in immune regulation and its relevance in oral lichen planus. Exp Ther Med 17(1):575–586. https://doi.org/10.3892/etm.2018.7019
Tarassishin L, Loudig O, Bauman A, Shafit-Zagardo B, Suh HS, Lee SC (2011) Interferon regulatory factor 3 inhibits astrocyte inflammatory gene expression through suppression of the pro-inflammatory miR-155 and miR-155*. Glia 59(12):1911–1922. https://doi.org/10.1002/glia.21233
Thai TH, Calado DP, Casola S, Ansel KM, Xiao C, Xue Y, Murphy A, Frendewey D, Valenzuela D, Kutok JL, Schmidt-Supprian M, Rajewsky N, Yancopoulos G, Rao A, Rajewsky K (2007) Regulation of the germinal center response by microRNA-155. Science 316(5824):604–608. https://doi.org/10.1126/science.1141229
Thome AD, Harms AS, Volpicelli-Daley LA, Standaert DG (2016) microRNA-155 regulates alpha-synuclein-induced inflammatory responses in models of parkinson disease. J Neurosci 36(8):2383–2390. https://doi.org/10.1523/JNEUROSCI.3900-15.2016
Tiwari S, Atluri V, Kaushik A, Yndart A, Nair M (2019) Alzheimer’s disease: pathogenesis, diagnostics, and therapeutics. Int J Nanomedicine 14:5541–5554. https://doi.org/10.2147/IJN.S200490
Tonacci A, Bagnato G, Pandolfo G, Billeci L, Sansone F, Conte R, Gangemi S (2019) MicroRNA cross-involvement in autism spectrum disorders and atopic dermatitis: a literature review. J Clin Med 8(1):88. https://doi.org/10.3390/jcm8010088
Trotta R, Chen L, Ciarlariello D, Josyula S, Mao C, Costinean S, Yu L, Butchar JP, Tridandapani S, Croce CM (2012) miR-155 regulates IFN-γ production in natural killer cells. Blood J Am Soc Hematol 119(15):3478–3485
Valerio A, Boroni F, Benarese M, Sarnico I, Ghisi V, Bresciani LG, Ferrario M, Borsani G, Spano P, Pizzi M (2006) NF-kappaB pathway: a target for preventing beta-amyloid (Abeta)-induced neuronal damage and Abeta42 production. Eur J Neurosci 23(7):1711–1720. https://doi.org/10.1111/j.1460-9568.2006.04722.x
Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, Marinovich M (2003) Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23(25):8692–8700. https://doi.org/10.1523/JNEUROSCI.23-25-08692.2003
Wang X, Zhao Y, Zhang X, Badie H, Zhou Y, Mu Y (2013) Loss of sorting nexin 27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in Down’s syndrome. Nat Med 19(4):473–480. https://doi.org/10.1038/nm.3117
Wang L, Zhang H, Rodriguez S, Cao L, Parish J, Mumaw C, Zollman A, Kamoka MM, Mu J, Chen DZ (2014a) Notch-dependent repression of miR-155 in the bone marrow niche regulates hematopoiesis in an NF-κB-dependent manner. Cell Stem Cell 15(1):51–65
Wang X, Huang T, Zhao Y, Zheng Q, Thompson RC, Bu G, Zhang YW, Hong W, Xu H (2014b) Sorting nexin 27 regulates Aβ production through modulating γ-secretase activity. Cell Rep 9(3):1023–1033. https://doi.org/10.1016/j.celrep.2014.09.037
Wang D, Tang M, Zong P, Liu H, Zhang T, Liu Y, Zhao Y (2018) MiRNA-155 regulates the Th17/Treg ratio by targeting SOCS1 in severe acute pancreatitis. Front Physiol 9:686
Wen Y, Zhang X, Dong L, Zhao J, Zhang C, Zhu C (2014) Acetylbritannilactone modulates MicroRNA-155-mediated inflammatory response in ischemic cerebral tissues. Mol Med 21(1):197–209. https://doi.org/10.2119/molmed.2014.00199
Woodbury ME, Freilich RW, Cheng CJ, Asai H, Ikezu S, Boucher JD, Slack F, Ikezu T (2015) miR-155 is essential for inflammation-induced hippocampal neurogenic dysfunction. J Neurosci 35(26):9764–9781. https://doi.org/10.1523/JNEUROSCI.4790-14.2015
Wu S, Xie DL, Dai XY (2019) Down-regulation of miR-155 promotes apoptosis of nasopharyngeal carcinoma CNE-1 cells by targeting PI3K/AKT-FOXO3a signaling. Eur Rev Med Pharmacol Sci 23(17):7391–7398. https://doi.org/10.26355/eurrev_201909_18847
Xing G, Luo Z, Zhong C, Pan X, Xu X (2016) Influence of miR-155 on cell apoptosis in rats with ischemic stroke: role of the Ras Homolog Enriched in Brain (Rheb)/mTOR pathway. Med Sci Monit 22:5141–5153. https://doi.org/10.12659/msm.898980
Xu C, Ren G, Cao G, Chen Q, Shou P, Zheng C, Du L, Han X, Jiang M, Yang Q (2013) miR-155 regulates immune modulatory properties of mesenchymal stem cells by targeting TAK1-binding protein 2. J Biol Chem 288(16):11074–11079
Yan Z, Che S, Wang J, Jiao Y, Wang C, Meng Q (2015) miR-155 contributes to the progression of glioma by enhancing Wnt/β-catenin pathway. Tumour Biol 36(7):5323–5331. https://doi.org/10.1007/s13277-015-3193-9
Yang L, Li C, Liang F, Fan Y, Zhang S (2017) MiRNA-155 promotes proliferation by targeting caudal-type homeobox 1 (CDX1) in glioma cells. Biomed Pharmacother 95:1759–1764. https://doi.org/10.1016/j.biopha.2017.08.088
Yang L, Liu L, Ying H, Yu Y, Zhang D, Deng H, Zhang H, Chai J (2018) Acute downregulation of miR-155 leads to a reduced collagen synthesis through attenuating macrophages inflammatory factor secretion by targeting SHIP1. J Mol Histol 49(2):165–174. https://doi.org/10.1007/s10735-018-9756-5
Yi J, Wang D, Niu X, Hu J, Zhou Y, Li Z (2015) MicroRNA-155 deficiency suppresses Th17 cell differentiation and improves locomotor recovery after spinal cord injury. Scand J Immunol 81(5):284–290. https://doi.org/10.1111/sji.12276
Ysrafil Y, Astuti I, Anwar SL, Martien R, Sumadi FAN, Wardhana T, Haryana SM (2020) MicroRNA-155-5p diminishes in vitro ovarian cancer cell viability by targeting HIF1α expression. Adv Pharm Bulletin 10(4):630
Zhang J, Cheng Y, Cui W, Li M, Li B, Guo L (2014) MicroRNA-155 modulates Th1 and Th17 cell differentiation and is associated with multiple sclerosis and experimental autoimmune encephalomyelitis. J Neuroimmunol 266(1–2):56–63. https://doi.org/10.1016/j.jneuroim.2013.09.019
Zhang W, Wang L, Pang X, Zhang J, Guan Y (2019) Role of microRNA-155 in modifying neuroinflammation and γ-aminobutyric acid transporters in specific central regions after post-ischaemic seizures. J Cell Mol Med 23(8):5017–5024. https://doi.org/10.1111/jcmm.14358
Zhang W, Li X, Tang Y, Chen C, Jing R, Liu T (2020a) miR-155-5p implicates in the pathogenesis of renal fibrosis via targeting SOCS1 and SOCS6. Oxid Med Cell Longev 2020:1–11. https://doi.org/10.1155/2020/6263921
Zhang W, Wang L, Wang R, Duan Z, Wang H (2020b) A blockade of microRNA-155 signal pathway has a beneficial effect on neural injury after intracerebral haemorrhage via reduction in neuroinflammation and oxidative stress. Arch Physiol Biochem 15:1–7. https://doi.org/10.1080/13813455.2020.1764047
Zheng X, Huang H, Liu J, Li M, Liu M, Luo T (2018) Propofol attenuates inflammatory response in LPS-activated microglia by regulating the miR-155/SOCS1 pathway. Inflammation 41(1):11–19
Zhou J, Wang W, Gao Z, Peng X, Chen X, Chen W (2013) MicroRNA-155 promotes glioma cell proliferation via the regulation of MXI1. PLoS ONE. https://doi.org/10.1371/journal.pone.0083055
Acknowledgements
We express our sincere gratitude for the Vice Chancellor’s support for Research, Mashhad University of Medical Sciences, Iran. AMM received support from funds from ricerca corrente to IRCCS Istituto Ortopedico Galeazzi.
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This work was supported by Mashhad University of medical sciences and IRCCS Istituto Ortopedico Galeazzi.
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Seyed HamidReza Rastegar-moghaddama, Alireza Ebrahimzadeh-Bideskan, and Sara Shahba contributed to the drafting of the manuscript. Amir Mohammad Malvandi and Abbas Mohammadipour contributed to overall conceptual design, drafting and final edits, and approval.
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Rastegar-Moghaddam, S.H., Ebrahimzadeh-Bideskan, A., Shahba, S. et al. Roles of the miR-155 in Neuroinflammation and Neurological Disorders: A Potent Biological and Therapeutic Target. Cell Mol Neurobiol 43, 455–467 (2023). https://doi.org/10.1007/s10571-022-01200-z
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DOI: https://doi.org/10.1007/s10571-022-01200-z