Skip to main content

Advertisement

SpringerLink
Log in

The role of exosomal microRNAs in central nervous system diseases

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNA), endogenous non-coding RNAs approximately 22 nucleotides long, regulate gene expression by mediating translational inhibition or mRNA degradation. Exosomes are a tool for intercellular transmission of information in which miRNA exchange plays an important role. Under pathophysiological conditions in the central nervous system (CNS), cellular transmission of exosomal miRNAs can regulate signaling pathways. Exosomal miRNAs are involved in the occurrence and development of diverse CNS diseases, such as traumatic brain injury, spinal cord injury, stroke, neurodegenerative diseases, epilepsy, and glioma. The use of exosomes as transport vehicles for certain miRNAs provides a novel therapeutic strategy for CNS diseases. Furthermore, the exosomes in body fluids change with the occurrence of diseases, indicating that subtle changes in physiological and pathological processes in vivo could be recognized by analyzing exosomes. Exosomal analysis is expected to act as a novel tool for diagnosis and prediction of neurological diseases. In this review, we present the current understanding of the implications of miRNAs in CNS diseases and summarize the role and mechanism of action of exosomal miRNA in nervous system disease models.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. He C, Zheng S, Luo Y et al (2018) Exosome Theranostics: Biology and Translational Medicine [J]. Theranostics 8(1):237–255

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Urbanelli L, Buratta S, Sagini K et al (2015) Exosome-based strategies for Diagnosis and Therapy [J]. Recent Pat CNS Drug Discov 10(1):10–27

    CAS  PubMed  Google Scholar 

  3. Qing L, Chen H, Tang J et al (2018) Exosomes and Their MicroRNA Cargo: New Players in Peripheral Nerve Regeneration [J]. Neurorehabil Neural Repair 32(9):765–776

    PubMed  PubMed Central  Google Scholar 

  4. Anel A, Gallego-Lleyda A, De Miguel D et al (2019) Role of Exosomes in the Regulation of T-cell Mediated Immune Responses and in Autoimmune Disease [J]. Cells. https://doi.org/10.3390/cells8020154

    Article  PubMed  PubMed Central  Google Scholar 

  5. Wu P, Zhang B, Shi H et al (2018) MSC-exosome: A novel cell-free therapy for cutaneous regeneration [J]. Cytotherapy 20(3):291–301

    PubMed  Google Scholar 

  6. Milane L, Singh A, Mattheolabakis G et al (2015) Exosome mediated communication within the tumor microenvironment [J]. J Control Release 219:278–294

    CAS  PubMed  Google Scholar 

  7. Alenquer M, Amorim MJ (2015) Exosome Biogenesis, Regulation, and Function in Viral Infection [J]. Viruses 7(9):5066–5083

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Yang D, Zhang W, Zhang H et al (2020) Progress, opportunity, and perspective on exosome isolation - efforts for efficient exosome-based theranostics [J]. Theranostics 10(8):3684–3707

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Lu TX, Rothenberg ME (2018) MicroRNA [J]. J Allergy Clin Immunol 141(4):1202–1207

    CAS  PubMed  Google Scholar 

  10. Krichevsky AM, King KS, Donahue CP et al (2003) A microRNA array reveals extensive regulation of microRNAs during brain development [J]. RNA 9(10):1274–1281

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Theis V, Theiss C (2018) Vegf - A Stimulus for Neuronal Development and Regeneration in the CNS and PNS [J]. Curr Protein Pept Sci 19(6):589–597

    CAS  PubMed  Google Scholar 

  12. Vieira MS, Santos AK, Vasconcellos R et al (2018) Neural stem cell differentiation into mature neurons: Mechanisms of regulation and biotechnological applications [J]. Biotechnol Adv 36(7):1946–1970

    CAS  PubMed  Google Scholar 

  13. Sim S-E, Bakes J, Kaang B-K (2014) Neuronal activity-dependent regulation of MicroRNAs [J]. Mol Cells 37(7):511–517

    PubMed  PubMed Central  Google Scholar 

  14. Tan L, Yu J-T, Tan L (2015) Causes and Consequences of MicroRNA Dysregulation in Neurodegenerative Diseases [J]. Mol Neurobiol 51(3):1249–1262

    CAS  PubMed  Google Scholar 

  15. Song Y, Li Z, He T et al (2019) M2 microglia-derived exosomes protect the mouse brain from ischemia-reperfusion injury via exosomal miR-124 [J]. Theranostics 9(10):2910–2923

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Li D, Zhang P, Yao X et al (2018) Exosomes Derived From miR-133b-Modified Mesenchymal Stem Cells Promote Recovery After Spinal Cord Injury [J]. Front Neurosci. https://doi.org/10.3389/fnins.2018.00845

    Article  PubMed  PubMed Central  Google Scholar 

  17. Monfared H, Jahangard Y, Nikkhah M et al (2019) Potential Therapeutic Effects of Exosomes Packed With a miR-21-Sponge Construct in a Rat Model of Glioblastoma [J]. Front Oncol. https://doi.org/10.3389/fonc.2019.00782

    Article  PubMed  PubMed Central  Google Scholar 

  18. Vishnoi A, Rani S (2017) MiRNA Biogenesis and Regulation of Diseases: An Overview [J]. Methods Mol Biol. https://doi.org/10.1007/978-1-4939-6524-3_1

    Article  PubMed  Google Scholar 

  19. Lukiw WJ, Pogue AI (2020) Vesicular Transport of Encapsulated microRNA between Glial and Neuronal Cells [J]. Int J Mol Sci. https://doi.org/10.3390/ijms21145078

    Article  PubMed  PubMed Central  Google Scholar 

  20. Yu X, Odenthal M, Fries JWU (2016) Exosomes as miRNA Carriers: Formation-Function-Future [J]. Int J Mol Sci. https://doi.org/10.3390/ijms17122028

    Article  PubMed  PubMed Central  Google Scholar 

  21. Tomasetti M, Lee W, Santarelli L et al (2017) Exosome-derived microRNAs in cancer metabolism: possible implications in cancer diagnostics and therapy [J]. Exp Mol Med 49(1):e285

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Zhang X, Yuan X, Shi H et al (2015) Exosomes in cancer: small particle, big player [J]. J Hematol Oncol. https://doi.org/10.1186/s13045-015-0181-x

    Article  PubMed  PubMed Central  Google Scholar 

  23. Johnson WD, Griswold DP (2017) Traumatic brain injury: a global challenge [J]. Lancet Neurol 16(12):949–950

    PubMed  Google Scholar 

  24. Majdan M, Plancikova D, Brazinova A et al (2016) Epidemiology of traumatic brain injuries in Europe: a cross-sectional analysis [J]. Lancet Public Health 1(2):e76–e83

    PubMed  Google Scholar 

  25. Gao G-Y, Jiang J-Y (2012) Chinese Head Trauma Data Bank: Effect of gender on the outcome of patients with severe traumatic brain injury [J]. J Neurotrauma. https://doi.org/10.1089/neu.2011.2134

    Article  PubMed  PubMed Central  Google Scholar 

  26. Jiang J-Y (2013) Head trauma in China [J]. Injury 44(11):1453–1457

    PubMed  Google Scholar 

  27. Finnie JW (2013) Neuroinflammation: beneficial and detrimental effects after traumatic brain injury [J]. Inflammopharmacology 21(4):309–320

    CAS  PubMed  Google Scholar 

  28. Harrison EB, Hochfelder CG, Lamberty BG et al (2016) Traumatic brain injury increases levels of miR-21 in extracellular vesicles: implications for neuroinflammation [J]. FEBS Open Bio 6(8):835–846

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Yin Z, Han Z, Hu T et al (2020) Neuron-derived exosomes with high miR-21–5p expression promoted polarization of M1 microglia in culture [J]. Brain Behav Immun 83:270–282

    CAS  PubMed  Google Scholar 

  30. Yang Y, Ye Y, Kong C et al (2019) MiR-124 Enriched Exosomes Promoted the M2 Polarization of Microglia and Enhanced Hippocampus Neurogenesis After Traumatic Brain Injury by Inhibiting TLR4 Pathway [J]. Neurochem Res 44(4):811–828

    CAS  PubMed  Google Scholar 

  31. Huang S, Ge X, Yu J et al (2018) Increased miR-124-3p in microglial exosomes following traumatic brain injury inhibits neuronal inflammation and contributes to neurite outgrowth their transfer into neurons [J]. FASEB J 32(1):512–528

    CAS  PubMed  Google Scholar 

  32. Long X, Yao X, Jiang Q et al (2020) Astrocyte-derived exosomes enriched with miR-873a-5p inhibit neuroinflammation via microglia phenotype modulation after traumatic brain injury [J]. J Neuroinflammation 17(1):89

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Li D, Huang S, Zhu J et al (2019) Exosomes from MiR-21–5p-Increased Neurons Play a Role in Neuroprotection by Suppressing Rab11a-Mediated Neuronal Autophagy In Vitro After Traumatic Brain Injury [J]. Med Sci Monit 25:1871–1885

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Li D, Huang S, Yin Z et al (2019) Increases in miR-124-3p in Microglial Exosomes Confer Neuroprotective Effects by Targeting FIP200-Mediated Neuronal Autophagy Following Traumatic Brain Injury [J]. Neurochem Res 44(8):1903–1923

    CAS  PubMed  Google Scholar 

  35. Sandrow-Feinberg HR, Houlé JD (2015) Exercise after spinal cord injury as an agent for neuroprotection, regeneration and rehabilitation [J]. Brain Res 1619:12–21

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Friedli L, Rosenzweig ES, Barraud Q et al (2015) Pronounced species divergence in corticospinal tract reorganization and functional recovery after lateralized spinal cord injury favors primates [J]. Sci Transl Med. https://doi.org/10.1126/scitranslmed.aac5811

    Article  PubMed  PubMed Central  Google Scholar 

  37. Hombach S, Kretz M (2016) Non-coding RNAs: Classification, Biology and Functioning [J]. Adv Exp Med Biol. https://doi.org/10.1007/978-3-319-42059-2_1

    Article  PubMed  Google Scholar 

  38. Ding S-Q, Chen J, Wang S-N et al (2019) Identification of serum exosomal microRNAs in acute spinal cord injured rats [J]. Exp Biol Med (Maywood) 244(14):1149–1161

    CAS  Google Scholar 

  39. Li C, Li X, Zhao B et al (2020) Exosomes derived from miR-544-modified mesenchymal stem cells promote recovery after spinal cord injury [J]. Arch Physiol Biochem. https://doi.org/10.1080/13813455.2019.1691601

    Article  PubMed  Google Scholar 

  40. Ji W, Jiang W, Li M et al (2019) miR-21 deficiency contributes to the impaired protective effects of obese rat mesenchymal stem cell-derived exosomes against spinal cord injury [J]. Biochimie 167:171–178

    CAS  PubMed  Google Scholar 

  41. Lu XC, Zheng JY, Tang LJ et al (2015) MiR-133b Promotes neurite outgrowth by targeting RhoA expression [J]. Cell Physiol Biochem 35(1):246–258

    CAS  PubMed  Google Scholar 

  42. Niu M, Xu R, Wang J et al (2016) MiR-133b ameliorates axon degeneration induced by MPP(+) via targeting RhoA [J]. Neuroscience 325:39–49

    CAS  PubMed  Google Scholar 

  43. Wu X, Walker CL, Lu Q et al (2017) RhoA/Rho Kinase Mediates Neuronal Death Through Regulating cPLA Activation [J]. Mol Neurobiol 54(9):6885–6895

    CAS  PubMed  Google Scholar 

  44. Xin H, Li Y, Buller B et al (2012) Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth [J]. Stem Cells 30(7):1556–1564

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Kong F-L, Wang X-P, Li Y-N et al (2018) The role of exosomes derived from cerebrospinal fluid of spinal cord injury in neuron proliferation in vitro [J]. Artif Cells Nanomed Biotechnol 46(1):200–205

    CAS  PubMed  Google Scholar 

  46. Yu T, Zhao C, Hou S et al (2019) Exosomes secreted from miRNA-29b-modified mesenchymal stem cells repaired spinal cord injury in rats [J]. Braz J Med Biol Res 52(12):e8735

    PubMed  PubMed Central  Google Scholar 

  47. Hu X, Xu Y, Zhong Z et al (2016) A Large-Scale Investigation of Hypoxia-Preconditioned Allogeneic Mesenchymal Stem Cells for Myocardial Repair in Nonhuman Primates: Paracrine Activity Without Remuscularization [J]. Circ Res 118(6):970–983

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Liu W, Rong Y, Wang J et al (2020) Exosome-shuttled miR-216a-5p from hypoxic preconditioned mesenchymal stem cells repair traumatic spinal cord injury by shifting microglial M1/M2 polarization [J]. J Neuroinflammation 17(1):47

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Koh S-H, Park H-H (2017) Neurogenesis in Stroke Recovery [J]. Transl Stroke Res. https://doi.org/10.1007/s12975-016-0460-z

    Article  PubMed  Google Scholar 

  50. Xiaolu L, Zhitao F, Lipeng D et al (2019) The Potential Role of MicroRNA-124 in Cerebral Ischemia Injury [J]. Int J Mol Sci. https://doi.org/10.3390/ijms21010120

    Article  Google Scholar 

  51. Smith SD, Eskey CJ (2011) Hemorrhagic stroke [J]. Radiol Clin North Am 49(1):27–45

    PubMed  Google Scholar 

  52. Mei J, Hairong W, Mingming J et al (2018) Exosomes from MiR-30d-5p-ADSCs Reverse Acute Ischemic Stroke-Induced, Autophagy-Mediated Brain Injury by Promoting M2 Microglial/Macrophage Polarization [J]. Cell Physiol Biochem. https://doi.org/10.1159/000490078

    Article  PubMed  Google Scholar 

  53. Song Y, Li Z, He T et al (2019) M2 microglia-derived exosomes protect the mouse brain from ischemia-reperfusion injury via exosomal miR-124 [J]. Theranostics. https://doi.org/10.7150/thno.30879

    Article  PubMed  PubMed Central  Google Scholar 

  54. Yang J, Zhang X, Chen X et al (2017) Exosome Mediated Delivery of miR-124 Promotes Neurogenesis after Ischemia [J]. Mol Ther Nucleic Acids 7:278–287

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Shen H, Yao X, Li H et al (2018) Role of Exosomes Derived from miR-133b Modified MSCs in an Experimental Rat Model of Intracerebral Hemorrhage [J]. J Mol Neurosci 64(3):421–430

    CAS  PubMed  Google Scholar 

  56. Hou K, Li G, Zhao J et al (2020) Bone mesenchymal stem cell-derived exosomal microRNA-29b-3p prevents hypoxic-ischemic injury in rat brain by activating the PTEN-mediated Akt signaling pathway [J]. J Neuroinflammation 17(1):46

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Xin H, Katakowski M, Wang F et al (2017) MicroRNA cluster miR-17-92 Cluster in Exosomes Enhance Neuroplasticity and Functional Recovery After Stroke in Rats [J]. Stroke 48(3):747–753

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Xin H, Wang F, Li Y et al (2017) Secondary Release of Exosomes From Astrocytes Contributes to the Increase in Neural Plasticity and Improvement of Functional Recovery After Stroke in Rats Treated With Exosomes Harvested From MicroRNA 133b-Overexpressing Multipotent Mesenchymal Stromal Cells [J]. Cell Transplant 26(2):243–257

    PubMed  PubMed Central  Google Scholar 

  59. Xin H, Li Y, Liu Z et al (2013) MiR-133b promotes neural plasticity and functional recovery after treatment of stroke with multipotent mesenchymal stromal cells in rats via transfer of exosome-enriched extracellular particles [J]. Stem Cells 31(12):2737–2746

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Yang Y, Cai Y, Zhang Y et al (2018) Exosomes Secreted by Adipose-Derived Stem Cells Contribute to Angiogenesis of Brain Microvascular Endothelial Cells Following Oxygen-Glucose Deprivation In Vitro Through MicroRNA-181b/TRPM7 Axis [J]. J Mol Neurosci 65(1):74–83

    CAS  PubMed  Google Scholar 

  61. Li Q, He Q, Baral S et al (2016) MicroRNA-493 regulates angiogenesis in a rat model of ischemic stroke by targeting MIF [J]. FEBS J 283(9):1720–1733

    CAS  PubMed  Google Scholar 

  62. Wang W, Li D-B, Li R-Y et al (2018) Diagnosis of Hyperacute and Acute Ischaemic Stroke: The Potential Utility of Exosomal MicroRNA-21-5p and MicroRNA-30a-5p [J]. Cerebrovasc Dis 45(5–6):204–212

    CAS  PubMed  Google Scholar 

  63. Luo X, Wang W, Li D et al (2019) Plasma Exosomal miR-450b-5p as a Possible Biomarker and Therapeutic Target for Transient Ischaemic Attacks in Rats [J]. J Mol Neurosci 69(4):516–526

    CAS  PubMed  Google Scholar 

  64. Li D-B, Liu J-L, Wang W et al (2017) Plasma Exosomal miR-422a and miR-125b-2-3p Serve as Biomarkers for Ischemic Stroke [J]. Curr Neurovasc Res 14(4):330–337

    CAS  PubMed  Google Scholar 

  65. Zhou J, Chen L, Chen B et al (2018) Increased serum exosomal miR-134 expression in the acute ischemic stroke patients [J]. BMC Neurol 18(1):198

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Chen F, Du Y, Esposito E et al (2015) Effects of Focal Cerebral Ischemia on Exosomal Versus Serum miR126 [J]. Transl Stroke Res 6(6):478–484

    CAS  PubMed  Google Scholar 

  67. Katsuno M, Sahashi K, Iguchi Y et al (2018) Preclinical progression of neurodegenerative diseases [J]. Nagoya J Med Sci 80(3):289–298

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Matej R, Tesar A, Rusina R (2019) Alzheimer’s disease and other neurodegenerative dementias in comorbidity: A clinical and neuropathological overview [J]. Clin Biochem 73:26–31

    CAS  PubMed  Google Scholar 

  69. Ridolfi B, Abdel-Haq H (2017) Neurodegenerative Disorders Treatment: The MicroRNA Role [J]. Curr Gene Ther 17(5):327–363

    CAS  PubMed  Google Scholar 

  70. Liu C-G, Song J, Zhang Y-Q et al (2014) MicroRNA-193b is a regulator of amyloid precursor protein in the blood and cerebrospinal fluid derived exosomal microRNA-193b is a biomarker of Alzheimer’s disease [J]. Mol Med Rep 10(5):2395–2400

    CAS  PubMed  Google Scholar 

  71. Chen J-J, Zhao B, Zhao J et al (2017) Potential Roles of Exosomal MicroRNAs as Diagnostic Biomarkers and Therapeutic Application in Alzheimer’s Disease [J]. Neural Plast. https://doi.org/10.1155/2017/7027380

    Article  PubMed  PubMed Central  Google Scholar 

  72. Yang TT, Liu CG, Gao SC et al (2018) The Serum Exosome Derived MicroRNA-135a, -193b, and -384 Were Potential Alzheimer’s Disease Biomarkers [J]. Biomed Environ Sci 31(2):87–96

    PubMed  Google Scholar 

  73. Wei H, Xu Y, Xu W et al (2018) Serum Exosomal miR-223 Serves as a Potential Diagnostic and Prognostic Biomarker for Dementia [J]. Neuroscience 379:167–176

    CAS  PubMed  Google Scholar 

  74. Mak MKY, Wong-Yu ISK (2019) Exercise for Parkinson’s disease [J]. Int Rev Neurobiol. https://doi.org/10.1016/bs.irn.2019.06.001

    Article  PubMed  Google Scholar 

  75. Vilaça-Faria H, Salgado AJ, Teixeira FG (2019) Mesenchymal Stem Cells-derived Exosomes: A New Possible Therapeutic Strategy for Parkinson’s Disease? [J]. Cells. https://doi.org/10.3390/cells8020118

    Article  PubMed  PubMed Central  Google Scholar 

  76. Shakespear N, Ogura M, Yamaki J et al (2020) Astrocyte-Derived Exosomal microRNA miR-200a-3p Prevents MPP-Induced Apoptotic Cell Death Through Down-Regulation of MKK4 [J]. Neurochem Res 45(5):1020–1033

    CAS  PubMed  Google Scholar 

  77. Saraiva C, Paiva J, Santos T et al (2016) MicroRNA-124 loaded nanoparticles enhance brain repair in Parkinson’s disease [J]. J Control Release 235:291–305

    CAS  PubMed  Google Scholar 

  78. Yao YF, Qu MW, Li GC et al (2018) Circulating exosomal miRNAs as diagnostic biomarkers in Parkinson’s disease [J]. Eur Rev Med Pharmacol Sci 22(16):5278–5283

    PubMed  Google Scholar 

  79. Brown RH, Al-Chalabi A (2017) Amyotrophic Lateral Sclerosis [J]. N Engl J Med 377(2):162–172

    CAS  PubMed  Google Scholar 

  80. Oskarsson B, Gendron TF, Staff NP (2018) Amyotrophic Lateral Sclerosis: An Update for 2018 [J]. Mayo Clin Proc 93(11):1617–1628

    PubMed  Google Scholar 

  81. Yelick J, Men Y, Jin S et al (2020) Elevated exosomal secretion of miR-124–3p from spinal neurons positively associates with disease severity in ALS [J]. Exp Neurol. https://doi.org/10.1016/j.expneurol.2020.113414

    Article  PubMed  PubMed Central  Google Scholar 

  82. Pinto S, Cunha C, Barbosa M et al (2017) Exosomes from NSC-34 Cells Transfected with hSOD1-G93A Are Enriched in miR-124 and Drive Alterations in Microglia Phenotype [J]. Front Neurosci. https://doi.org/10.3389/fnins.2017.00273

    Article  PubMed  PubMed Central  Google Scholar 

  83. Wang L, Zhang L (2020) Circulating Exosomal miRNA as Diagnostic Biomarkers of Neurodegenerative Diseases [J]. Front Mol Neurosci. https://doi.org/10.3389/fnmol.2020.00053

    Article  PubMed  PubMed Central  Google Scholar 

  84. Xu Q, Zhao Y, Zhou X et al (2018) Comparison of the extraction and determination of serum exosome and miRNA in serum and the detection of miR-27a-3p in serum exosome of ALS patients [J]. Intractable Rare Dis Res 7(1):13–18

    PubMed  PubMed Central  Google Scholar 

  85. Fiest KM, Sauro KM, Wiebe S et al (2017) Prevalence and incidence of epilepsy: A systematic review and meta-analysis of international studies [J]. Neurology 88(3):296–303

    PubMed  PubMed Central  Google Scholar 

  86. Thijs RD, Surges R, O’Brien TJ et al (2019) Epilepsy in adults [J]. Lancet 393(10172):689–701

    PubMed  Google Scholar 

  87. Moshé SL, Perucca E, Ryvlin P et al (2015) Epilepsy: new advances [J]. Lancet 385(9971):884–898

    PubMed  Google Scholar 

  88. Pitkänen A, Ndode-Ekane XE, Lapinlampi N et al (2019) Epilepsy biomarkers - Toward etiology and pathology specificity [J]. Neurobiol Dis 123:42–58

    PubMed  Google Scholar 

  89. Yan S, Zhang H, Xie W et al (2017) Altered microRNA profiles in plasma exosomes from mesial temporal lobe epilepsy with hippocampal sclerosis [J]. Oncotarget 8(3):4136–4146

    PubMed  Google Scholar 

  90. Batool A, Hill TDM, Nguyen NT et al (2019) Altered Biogenesis and MicroRNA Content of Hippocampal Exosomes Following Experimental Status Epilepticus [J]. Front Neurosci. https://doi.org/10.3389/fnins.2019.01404

    Article  PubMed  Google Scholar 

  91. Tiwari D, Peariso K, Gross C (2018) MicroRNA-induced silencing in epilepsy: Opportunities and challenges for clinical application [J]. Dev Dyn. https://doi.org/10.1002/dvdy.24582

    Article  PubMed  Google Scholar 

  92. Hu K, Xie Y-Y, Zhang C et al (2012) MicroRNA expression profile of the hippocampus in a rat model of temporal lobe epilepsy and miR-34a-targeted neuroprotection against hippocampal neurone cell apoptosis post-status epilepticus [J]. BMC Neurosci. https://doi.org/10.1186/1471-2202-13-115

    Article  PubMed  PubMed Central  Google Scholar 

  93. Gross C, Yao X, Engel T et al (2016) MicroRNA-Mediated Downregulation of the Potassium Channel Kv4.2 Contributes to Seizure Onset [J]. Cell Rep 17(1):37–45

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Ostrom QT, Bauchet L, Davis FG et al (2014) The epidemiology of glioma in adults: a “state of the science” review [J]. Neuro-oncology 16(7):896–913

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Li Q, Wang A-Y, Xu Q-G et al (2015) In-vitro inhibitory effect of EGFL7-RNAi on endothelial angiogenesis in glioma [J]. Int J Clin Exp Pathol 8(10):12234–12242

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Guo X, Qiu W, Wang J et al (2019) Glioma exosomes mediate the expansion and function of myeloid-derived suppressor cells through microRNA-29a/Hbp1 and microRNA-92a/Prkar1a pathways [J]. Int J Cancer 144(12):3111–3126

    CAS  PubMed  Google Scholar 

  97. Guo X, Qiu W, Liu Q et al (2018) Immunosuppressive effects of hypoxia-induced glioma exosomes through myeloid-derived suppressor cells via the miR-10a/Rora and miR-21/Pten Pathways [J]. Oncogene 37(31):4239–4259

    CAS  PubMed  Google Scholar 

  98. Wang Z-F, Liao F, Wu H et al (2019) Glioma stem cells-derived exosomal miR-26a promotes angiogenesis of microvessel endothelial cells in glioma [J]. J Exp Clin Cancer Res 38(1):201

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Cai Q, Zhu A, Gong L (2018) Exosomes of glioma cells deliver miR-148a to promote proliferation and metastasis of glioblastoma via targeting CADM1 [J]. Bull Cancer 105(7–8):643–651

    PubMed  Google Scholar 

  100. Xu H, Zhao G, Zhang Y et al (2019) Mesenchymal stem cell-derived exosomal microRNA-133b suppresses glioma progression via Wnt/β-catenin signaling pathway by targeting EZH2 [J]. Stem Cell Res Ther 10(1):381

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Yu L, Gui S, Liu Y et al (2019) Exosomes derived from microRNA-199a-overexpressing mesenchymal stem cells inhibit glioma progression by down-regulating AGAP2 [J]. Aging (Albany NY) 11(15):5300–5318

    CAS  Google Scholar 

  102. Figueroa J, Phillips LM, Shahar T et al (2017) Exosomes from Glioma-Associated Mesenchymal Stem Cells Increase the Tumorigenicity of Glioma Stem-like Cells via Transfer of miR-1587 [J]. Cancer Res 77(21):5808–5819

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Yue X, Lan F, Xia T (2019) Hypoxic Glioma Cell-Secreted Exosomal miR-301a Activates Wnt/β-catenin Signaling and Promotes Radiation Resistance by Targeting TCEAL7 [J]. Mol Ther 27(11):1939–1949

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Yin J, Zeng A, Zhang Z et al (2019) Exosomal transfer of miR-1238 contributes to temozolomide-resistance in glioblastoma [J]. EBioMedicine 42:238–251

    PubMed  PubMed Central  Google Scholar 

  105. Tabibkhooei A, Izadpanahi M, Arab A et al (2020) Profiling of novel circulating microRNAs as a non-invasive biomarker in diagnosis and follow-up of high and low-grade gliomas [J]. Clin Neurol Neurosurg. https://doi.org/10.1016/j.clineuro.2019.105652

    Article  PubMed  Google Scholar 

  106. Shi R, Wang P-Y, Li X-Y et al (2015) Exosomal levels of miRNA-21 from cerebrospinal fluids associated with poor prognosis and tumor recurrence of glioma patients [J]. Oncotarget 6(29):26971–26981

    PubMed  PubMed Central  Google Scholar 

  107. Li S-P, Lin Z-X, Jiang X-Y et al (2018) Exosomal cargo-loading and synthetic exosome-mimics as potential therapeutic tools [J]. Acta Pharmacol Sin 39(4):542–551

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Cheng Q, Shi X, Han M et al (2018) Reprogramming Exosomes as Nanoscale Controllers of Cellular Immunity [J]. J Am Chem Soc 140(48):16413–16417

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Zhan Q, Yi K, Qi H et al (2020) Engineering blood exosomes for tumor-targeting efficient gene/chemo combination therapy [J]. Theranostics 10(17):7889–7905

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Kojima R, Bojar D, Rizzi G et al (2018) Designer exosomes produced by implanted cells intracerebrally deliver therapeutic cargo for Parkinson’s disease treatment [J]. Nat Commun 9(1):1305

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge Editage (www.editage.com) for English language editing.

Funding

This work was supported by the National Natural Science Foundation of China (Grant number 81571199, Grant number 81870974).

Author information

Authors and Affiliations

  1. The Key Laboratory of Pathobiology, Ministry of Education, College of Basic Medical Sciences, Jilin University, Changchun, 130000, People’s Republic of China

    Yifei Yu, Tong Ji, Yangyang Zheng, Jinying Xu & Guangfan Chi

  2. Department of Neurosurgery, The First Hospital of Jilin University, Changchun, 130000, People’s Republic of China

    Kun Hou

  3. Clinical Medical College, Jilin University, Changchun, 130000, People’s Republic of China

    Xishu Wang & Yining Liu

  4. Department of Regeneration Medicine, School of Pharmaceutical Science of Jilin University, Changchun, 130000, People’s Republic of China

    Yi Hou

Authors
  1. Yifei Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kun Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tong Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xishu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yining Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yangyang Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jinying Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yi Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Guangfan Chi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yi Hou or Guangfan Chi.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, Y., Hou, K., Ji, T. et al. The role of exosomal microRNAs in central nervous system diseases. Mol Cell Biochem 476, 2111–2124 (2021). https://doi.org/10.1007/s11010-021-04053-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-021-04053-0

Keywords

Search

Navigation