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MiR-124 Enriched Exosomes Promoted the M2 Polarization of Microglia and Enhanced Hippocampus Neurogenesis After Traumatic Brain Injury by Inhibiting TLR4 Pathway

Yang, Yongxiang, Ye, Yuqin, Kong, Chuiguang, Su, Xinhong, Zhang, Xin, Bai, Wei, He, Xiaosheng·2019·Neurochemical Research
DOI 10.1007/s11064-018-02714-z
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Abstract

MicroRNA-124 (miR-124) is a brain specific miRNA that is highly expressed in microglia. The upregulation of miR-124 contributes to M2 polarization of microglia, which is beneficial to neurogenesis. Exosomes are lipid membrane vesicles that can deliver miR-124 into the brain. However, whether miR-124 enriched exosomes (Exo-miR-124) can regulate the polarization of microglia and affect hippocampus neurogenesis after traumatic brain injury (TBI) is unknown. To clarify this, the Exo-miR-124 was first constructed, and then was intravenously administrated into rats via tail vein with the dose of 3 × 10 9 particles/each rat at 24 h post TBI. The polarization of microglia in hippocampus was evaluated through measuring the signature genes and cytokines of M1/M2 phenotype by reverse transcription-polymerase chain reaction (RT-PCR) and enzyme-linked immune sorbent assay (ELISA) at 7/14/21/28 days after TBI. Hippocampus neurogenesis was evaluated through detecting the proliferation marker BrdU/SOX2 and differentiation marker BrdU/NeuN by immunofluorescence (IF) at 7 and 28 days after TBI respectively. Neurological function was evaluated by neurological severity score (NSS) and morris water maze (MWM) at 7/14/21/28 and 24-28 days after TBI respectively. To explore the underlying mechanisms, the mRNA expression of TLR4 pathway molecules in hippocampus were measured by RT-PCR, and the polarization of microglia and the activation of TLR4 pathway in BV2 cells were measured after exosome treat…

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  1. Xiong Y, Mahmood A, Chopp M (2017) Emerging potential of exosomes for treatment of traumatic brain injury. Neural Regen Res 12:19–22 · DOI · Paper page
  2. Sun D (2016) Endogenous neurogenic cell response in the mature mammalian brain following traumatic injury. Exp Neurol 275(Pt 3):405–410 · DOI
  3. de Miranda AS, Zhang CJ, Katsumoto A, Teixeira AL (2017) Hippocampal adult neurogenesis: does the immune system matter? J Neurol Sci 372:482–495 · DOI
  4. Wu MD, Hein AM, Moravan MJ, Shaftel SS, Olschowka JA, O’Banion MK (2012) Adult murine hippocampal neurogenesis is inhibited by sustained IL-1beta and not rescued by voluntary running. Brain Behav Immun 26:292–300 · DOI
  5. Iosif RE, Ekdahl CT, Ahlenius H, Pronk CJ, Bonde S, Kokaia Z, Jacobsen SE, Lindvall O (2006) Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 26:9703–9712 · DOI
  6. Kiyota T, Ingraham KL, Swan RJ, Jacobsen MT, Andrews SJ, Ikezu T (2012) AAV serotype 2/1-mediated gene delivery of anti-inflammatory interleukin-10 enhances neurogenesis and cognitive function in APP + PS1 mice. Gene Ther 19:724–733 · DOI
  7. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S, Martino G, Schwartz M (2006) Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149–160 · DOI · Paper page
  8. Battista D, Ferrari CC, Gage FH, Pitossi FJ (2006) Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur J Neurosci 23:83–93 · DOI · Paper page
  9. Veremeyko T, Siddiqui S, Sotnikov I, Yung A, Ponomarev ED (2013) IL-4/IL-13-dependent and independent expression of miR-124 and its contribution to M2 phenotype of monocytic cells in normal conditions and during allergic inflammation. PLoS ONE 8:e81774 · DOI · Paper page
  10. Ponomarev ED, Veremeyko T, Weiner HL (2013) MicroRNAs are universal regulators of differentiation, activation, and polarization of microglia and macrophages in normal and diseased CNS. Glia 61:91–103 · DOI · Paper page
  11. Periyasamy P, Liao K, Kook YH, Niu F, Callen SE, Guo ML, Buch S (2018) Cocaine-mediated downregulation of miR-124 activates microglia by targeting KLF4 and TLR4 signaling. Mol Neurobiol 55:3196–3210 · DOI · Paper page
  12. Ning R, Venkat P, Chopp M, Zacharek A, Yan T, Cui X, Seyfried D, Chen J (2017) D-4F increases microRNA-124a and reduces neuroinflammation in diabetic stroke rats. Oncotarget 8:95481–95494 · DOI
  13. Yu A, Zhang T, Duan H, Pan Y, Zhang X, Yang G, Wang J, Deng Y, Yang Z (2017) MiR-124 contributes to M2 polarization of microglia and confers brain inflammatory protection via the C/EBP-alpha pathway in intracerebral hemorrhage. Immunol Lett 182:1–11 · DOI · Paper page
  14. Yang Y, Ye Y, Su X, He J, Bai W, He X (2017) MSCs-derived exosomes and neuroinflammation, neurogenesis and therapy of traumatic brain injury. Front Cell Neurosci 11:55
  15. Zhang Y, Chopp M, Meng Y, Katakowski M, Xin H, Mahmood A, Xiong Y (2015) Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. J Neurosurg 122:856–867 · DOI · Paper page
  16. Zhang Y, Chopp M, Zhang ZG, Katakowski M, Xin H, Qu C, Ali M, Mahmood A, Xiong Y (2017) Systemic administration of cell-free exosomes generated by human bone marrow derived mesenchymal stem cells cultured under 2D and 3D conditions improves functional recovery in rats after traumatic brain injury. Neurochem Int 111:69–81 · DOI
  17. Lee ST, Im W, Ban JJ, Lee M, Jung KH, Lee SK, Chu K, Kim M (2017) Exosome-Based Delivery of miR-124 in a Huntington’s Disease Model. J Mov Disord 10:45–52 · DOI · Paper page
  18. Pinto S, Cunha C, Barbosa M, Vaz AR, Brites D (2017) Exosomes from NSC-34 Cells transfected with hSOD1-G93A are enriched in miR-124 and drive alterations in microglia phenotype. Front Neurosci 11:273 · DOI · Paper page
  19. Yang J, Zhang X, Chen X, Wang L, Yang G (2017) Exosome mediated delivery of miR-124 promotes neurogenesis after ischemia. Mol Ther Nucleic Acids 7:278–287 · DOI · Paper page
  20. Mouihate A (2016) Prenatal activation of toll-like receptor-4 dampens adult hippocampal neurogenesis in An IL-6 dependent manner. Front Cell Neurosci 10:173 · DOI
  21. Seong KJ, Lee HG, Kook MS, Ko HM, Jung JY, Kim WJ (2016) Epigallocatechin-3-gallate rescues LPS-impaired adult hippocampal neurogenesis through suppressing the TLR4-NF-kappaB signaling pathway in mice. Korean J Physiol Pharmacol 20:41–51 · DOI
  22. Keene CD, Chang R, Stephen C, Nivison M, Nutt SE, Look A, Breyer RM, Horner PJ, Hevner R, Montine TJ (2009) Protection of hippocampal neurogenesis from toll-like receptor 4-dependent innate immune activation by ablation of prostaglandin E2 receptor subtype EP1 or EP2. Am J Pathol 174:2300–2309 · DOI
  23. Ahmad A, Crupi R, Campolo M, Genovese T, Esposito E, Cuzzocrea S (2013) Absence of TLR4 reduces neurovascular unit and secondary inflammatory process after traumatic brain injury in mice. PLoS ONE 8:e57208 · DOI
  24. Yao X, Liu S, Ding W, Yue P, Jiang Q, Zhao M, Hu F, Zhang H (2017) TLR4 signal ablation attenuated neurological deficits by regulating microglial M1/M2 phenotype after traumatic brain injury in mice. J Neuroimmunol 310:38–45 · DOI
  25. Huang S, Ge X, Yu J, Han Z, Yin Z, Li Y, Chen F, Wang H, Zhang J, Lei P (2018) Increased miR-124-3p in microglial exosomes following traumatic brain injury inhibits neuronal inflammation and contributes to neurite outgrowth via their transfer into neurons. FASEB J 32:512–528 · DOI · Paper page
  26. Xin H, Katakowski M, Wang F, Qian JY, Liu XS, Ali MM, Buller B, Zhang ZG, Chopp M (2017) MicroRNA cluster miR-17-92 cluster in exosomes enhance neuroplasticity and functional recovery after stroke in rats. Stroke 48:747–753 · DOI
  27. Taupin P (2007) BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev 53:198–214 · DOI · Paper page
  28. Wojtowicz JM, Kee N (2006) BrdU assay for neurogenesis in rodents. Nat Protoc 1:1399–1405 · DOI
  29. Ye Y, Zhao Z, Xu H, Zhang X, Su X, Yang Y, Yu X, He X (2016) Activation of sphingosine 1-phosphate receptor 1 enhances hippocampus neurogenesis in a rat model of traumatic brain injury: an involvement of MEK/Erk signaling pathway. Neural Plast 2016:8072156
  30. Ye Y, Yang Y, Chen C, Li Z, Jia Y, Su X, Wang C, He X (2017) Electroacupuncture improved hippocampal neurogenesis following traumatic brain injury in mice through inhibition of TLR4 signaling pathway. Stem Cells Int 2017:5841814
  31. Beni-Adani L, Gozes I, Cohen Y, Assaf Y, Steingart RA, Brenneman DE, Eizenberg O, Trembolver V, Shohami E (2001) A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice. J Pharmacol Exp Ther 296:57–63
  32. Albert-Weissenberger C, Varrallyay C, Raslan F, Kleinschnitz C, Siren AL (2012) An experimental protocol for mimicking pathomechanisms of traumatic brain injury in mice. Exp Transl Stroke Med 4:1 · DOI
  33. Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1:848–858 · DOI · Paper page
  34. Vorhees CV, Williams MT (2014) Value of water mazes for assessing spatial and egocentric learning and memory in rodent basic research and regulatory studies. Neurotoxicol Teratol 45:75–90 · DOI
  35. Braicu C, Tomuleasa C, Monroig P, Cucuianu A, Berindan-Neagoe I, Calin GA (2015) Exosomes as divine messengers: are they the Hermes of modern molecular oncology? Cell Death Differ 22:34–45 · DOI
  36. Kalani A, Tyagi A, Tyagi N (2014) Exosomes: mediators of neurodegeneration, neuroprotection and therapeutics. Mol Neurobiol 49:590–600 · DOI
  37. Xue F, Shen R, Chen X (2015) Analysis of gene profiles in glioma cells identifies potential genes, miRNAs, and target sites of migratory cells. Tumori 101:542–548 · DOI
  38. Amici SA, Dong J, Guerau-de-Arellano M (2017) Molecular mechanisms modulating the phenotype of macrophages and microglia. Front Immunol 8:1520 · DOI
  39. Sun M, Brady RD, Wright DK, Kim HA, Zhang SR, Sobey CG, Johnstone MR, O’Brien TJ, Semple BD, McDonald SJ, Shultz SR (2017) Treatment with an interleukin-1 receptor antagonist mitigates neuroinflammation and brain damage after polytrauma. Brain Behav Immun 66:359–371 · DOI
  40. Helmy A, Guilfoyle MR, Carpenter KL, Pickard JD, Menon DK, Hutchinson PJ (2014) Recombinant human interleukin-1 receptor antagonist in severe traumatic brain injury: a phase II randomized control trial. J Cereb Blood Flow Metab 34:845–851 · DOI
  41. Richardson RM, Sun D, Bullock MR (2007) Neurogenesis after traumatic brain injury. Neurosurg Clin N Am 18:169–181 · DOI
  42. Sun Y, Li Q, Gui H, Xu DP, Yang YL, Su DF, Liu X (2013) MicroRNA-124 mediates the cholinergic anti-inflammatory action through inhibiting the production of pro-inflammatory cytokines. Cell Res 23:1270–1283 · DOI · Paper page
  43. Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29:341–345 · DOI · Paper page
  44. Braccioli L, van Velthoven C, Heijnen CJ (2014) Exosomes: a new weapon to treat the central nervous system. Mol Neurobiol 49:113–119 · DOI
  45. McDonald SJ, Sun M, Agoston DV, Shultz SR (2016) The effect of concomitant peripheral injury on traumatic brain injury pathobiology and outcome. J Neuroinflam 13:90 · DOI
  46. Sun M, McDonald SJ, Brady RD, O’Brien TJ, Shultz SR (2018) The influence of immunological stressors on traumatic brain injury. Brain Behav Immun 69:618–628 · DOI

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Metadata

Authors
Yang, Y., Ye, Y., Kong, C., Su, X., Zhang, X., Bai, W., & He, X.
Venue
Neurochemical Research
Publisher
Springer Science and Business Media LLC
Published
2019-01-09
Volume
44
Issue
4
Pages
811-828
ISSN
  • 0364-3190
  • 1573-6903
DOI
10.1007/s11064-018-02714-z
Cited by
194
References
6
Language
en
Licence
www.springer.com/tdm (tdm)

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