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Insights into the Critical Role of Exosomes in the Brain; from Neuronal Activity to Therapeutic Effects

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Abstract

Exo are natural nano-sized vesicles with an endosomal origin that maintain cell-to-cell communications in a paracrine manner. Owing to their physicochemical properties, Exo transfer various types of bioactive metabolites from origin cells to the recipient cells, resulting in induction/inhibition of specific signaling pathways. Like different tissues, Exo are indispensable for the function of neural cells inside the brain parenchyma. Various aspects such as neurogenesis, microglial polarization, and angiogenesis are closely associated with the reciprocal interchanges of Exo between cells in a tightly regulated manner. Similar to physiological conditions, these particles can affect the progression of inflammatory responses following the onset of pathologies. The existence of several uptake exosomal mechanisms, such as receptor-mediated endocytosis, and high penetration capacity into the deep layers of the brain makes Exo promising bio-shuttles for the alleviation of pathological conditions. Like astrocytes, stem cells can release Exo into the surrounding niche with neuroprotective properties regenerative potential. Whether and how Exo can initiate the essential signals required for neurogenesis has not been fully understood. In this review, we will try to elaborate on the putative therapeutic role of Exo in the dynamic activity of neuronal cells.

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Copyright 2021, Stem Cell Research & Therapy) [34]

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Copyright 2017, Stem Cell Research & Therapy) [95]

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Abbreviations

AAV:

Adeno-associated virus

ALS:

Amyotrophic lateral sclerosis

BBB:

Blood–brain-barrier

BDNF:

Brain-derived neurotrophic factor

CNS:

Central nervous system

CSF:

Cerebrospinal fluid

SOD1:

Copper-zinc superoxide dismutase 1

ECs:

Endothelial cells

ESCRT:

Endosomal sorting complexes required for transport

Exo:

Exosomes

ECM:

Extracellular matrix

GFAP:

Glial fibrillary acidic protein

GLT1:

Glutamate transporter 1

hiPSCs:

Human-induced pluripotent stem cells

IFN-γ:

Interferon-gamma

IL-1α:

Interleukin-1 alpha

ILVs:

Intraluminal vesicles

LncRNAs:

Long non-coding RNAs

MSC:

Mesenchymal stem cell

miRNAs:

microRNAs

MVBs:

Multi-vesicular bodies

MCAO:

Middle cerebral artery occlusion

NGF:

Nerve growth factor

NSCs:

Neural stem cells

Nrf2:

Nuclear factor erythroid-derived 2, like 2

(NF-κB):

Nuclear factor-kappa B

RVG:

Rabies viral glycoprotein

siRNAs:

Short interfering RNAs

SNAREs:

Soluble N-ethylmaleimide sensitive factor attachment protein receptors

SCI:

Spinal cord injury

TLR:

Toll-like receptor

TGF-β:

Transforming growth factor-beta

TNF-α:

Tumor necrosis factor-alpha

References

  1. Paul A et al (2017) Transcriptional architecture of synaptic communication delineates GABAergic neuron identity. Cell 171(3):522-539. e20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hughes AN, Appel B (2019) Oligodendrocytes express synaptic proteins that modulate myelin sheath formation. Nat Commun 10(1):1–15

    Article  CAS  Google Scholar 

  3. Schmidt H, Knösche TR (2019) Action potential propagation and synchronisation in myelinated axons. PLoS Comput Biol 15(10):e1007004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Mary N et al (2018) Meiotic synapsis and gene expression altered by a balanced Y-autosome reciprocal translocation in an azoospermic pig. Sex Dev 12(5):256–263

    Article  CAS  PubMed  Google Scholar 

  5. Prada I et al (2018) Glia-to-neuron transfer of miRNAs via extracellular vesicles: a new mechanism underlying inflammation-induced synaptic alterations. Acta Neuropathol 135(4):529–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Pegtel DM, Gould SJ (2019) Exosomes. Annu Rev Biochem 88:487–514

    Article  CAS  PubMed  Google Scholar 

  7. Kalluri R, LeBleu VS (2020) The biology, function, and biomedical applications of exosomes Science 367(6478)

  8. Gassama Y, Favereaux A (2021) Emerging roles of extracellular vesicles in the central nervous system: physiology, pathology, and therapeutic perspectives. Front Cell Neurosci 15:7

    Article  CAS  Google Scholar 

  9. Brinker T et al (2014) A new look at cerebrospinal fluid circulation. Fluids and Barriers of the CNS 11(1):10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Caruso Bavisotto C et al (2019) Extracellular vesicle-mediated cell-cell communication in the nervous system: focus on neurological diseases. Int J Mol Sci 20(2):434

    Article  PubMed Central  CAS  Google Scholar 

  11. Bátiz LF, et al (2016) Exosomes as novel regulators of adult neurogenic niches. Front Cell Neurosci 9(501)

  12. Budnik V, Ruiz-Cañada C, Wendler F (2016) Extracellular vesicles round off communication in the nervous system. Nat Rev Neurosci 17(3):160–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hessvik NP, Llorente A (2018) Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 75(2):193–208

    Article  CAS  PubMed  Google Scholar 

  14. Wollert T et al (2009) Membrane scission by the ESCRT-III complex. Nature 458(7235):172–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Juan T, Fürthauer M (2018) Biogenesis and function of ESCRT-dependent extracellular vesicles. In Semin Cell Dev Biol Elsevier.

  16. Ghossoub R et al (2014) Syntenin-ALIX exosome biogenesis and budding into multivesicular bodies are controlled by ARF6 and PLD2. Nat Commun 5(1):1–12

    Article  CAS  Google Scholar 

  17. Gatta AT, Carlton JG (2019) The ESCRT-machinery: closing holes and expanding roles. Curr Opin Cell Biol 59:121–132

    Article  CAS  PubMed  Google Scholar 

  18. Heidarzadeh M et al (2021) Exosomal delivery of therapeutic modulators through the blood–brain barrier; promise and pitfalls. Cell Biosci 11(1):1–28

    Article  Google Scholar 

  19. Andreu Z, Yáñez-Mó M (2014) Tetraspanins in extracellular vesicle formation and function. Front Immunol 5:442

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Larios J, et al (2020) ALIX-and ESCRT-III–dependent sorting of tetraspanins to exosomes. J Cell Biol 219(3)

  21. Kajimoto T et al (2018) Involvement of Gβγ subunits of Gi protein coupled with S1P receptor on multivesicular endosomes in F-actin formation and cargo sorting into exosomes. J Biol Chem 293(1):245–253

    Article  CAS  PubMed  Google Scholar 

  22. Blanc L, Vidal M (2018) New insights into the function of Rab GTPases in the context of exosomal secretion. Small GTPases 9(1–2):95–106

    Article  CAS  PubMed  Google Scholar 

  23. Sinha S et al (2016) Cortactin promotes exosome secretion by controlling branched actin dynamics. J Cell Biol 214(2):197–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Datta A et al (2017) Manumycin A suppresses exosome biogenesis and secretion via targeted inhibition of Ras/Raf/ERK1/2 signaling and hnRNP H1 in castration-resistant prostate cancer cells. Cancer Lett 408:73–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kowal J, Tkach M, Théry C (2014) Biogenesis and secretion of exosomes. Curr Opin Cell Biol 29:116–125

    Article  CAS  PubMed  Google Scholar 

  26. Zhang L, Wrana JL (2014) The emerging role of exosomes in Wnt secretion and transport. Curr Opin Genet Dev 27:14–19

    Article  PubMed  CAS  Google Scholar 

  27. Sharma P, Schiapparelli L, Cline HT (2013) Exosomes function in cell–cell communication during brain circuit development. Curr Opin Neurobiol 23(6):997–1004

    Article  CAS  PubMed  Google Scholar 

  28. Korkut C et al (2009) Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell 139(2):393–404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Korkut C et al (2013) Regulation of postsynaptic retrograde signaling by presynaptic exosome release. Neuron 77(6):1039–1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Frühbeis C et al (2013) Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte–neuron communication. PLoS Biol 11(7):e1001604

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Sharma P et al (2019) Exosomes regulate neurogenesis and circuit assembly. Proc Natl Acad Sci 116(32):16086–16094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Long Q et al (2017) Intranasal MSC-derived A1-exosomes ease inflammation, and prevent abnormal neurogenesis and memory dysfunction after status epilepticus. Proc Natl Acad Sci 114(17):E3536–E3545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Huang J-H et al (2020) Exosomes derived from miR-126-modified MSCs promote angiogenesis and neurogenesis and attenuate apoptosis after spinal cord injury in rats. Neuroscience 424:133–145

    Article  CAS  PubMed  Google Scholar 

  34. Zhou W et al (2021) Exosomes derived from human placental mesenchymal stem cells enhanced the recovery of spinal cord injury by activating endogenous neurogenesis. Stem Cell Res Ther 12(1):174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Bátiz LF et al (2016) Exosomes as novel regulators of adult neurogenic niches. Front Cell Neurosci 9:501

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Ma Y et al (2019) Exosomes released from neural progenitor cells and induced neural progenitor cells regulate neurogenesis through miR-21a. Cell Commun Signal 17(1):1–10

    Article  Google Scholar 

  37. Fan L-W, Pang Y (2017) Dysregulation of neurogenesis by neuroinflammation: key differences in neurodevelopmental and neurological disorders. Neural Regen Res 12(3):366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Subramaniyan S, Terrando N (2019) Narrative review article: neuroinflammation and perioperative neurocognitive disorders. Anesth Analg 128(4):781

    Article  PubMed  PubMed Central  Google Scholar 

  39. Osborn LM et al (2016) Astrogliosis: an integral player in the pathogenesis of Alzheimer’s disease. Prog Neurobiol 144:121–141

    Article  CAS  PubMed  Google Scholar 

  40. Pekny M et al (2016) Astrocytes: a central element in neurological diseases. Acta Neuropathol 131(3):323–345

    Article  CAS  PubMed  Google Scholar 

  41. Eng LF, Ghirnikar RS (1994) GFAP and astrogliosis. Brain Pathol 4(3):229–237

    Article  CAS  PubMed  Google Scholar 

  42. Verkhratsky A, Butt A (2013) General pathophysiology of neuroglia. Glial Physiol Pathophysiol 2013:431–450

    Article  Google Scholar 

  43. Pekny M et al (2019) Astrocyte activation and reactive gliosis—a new target in stroke? Neurosci Lett 689:45–55

    Article  CAS  PubMed  Google Scholar 

  44. Liddelow SA et al (2017) Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541(7638):481–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119(1):7–35

    Article  PubMed  Google Scholar 

  46. Bush TG et al (1999) Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23(2):297–308

    Article  CAS  PubMed  Google Scholar 

  47. Levy S (2014) Function of the tetraspanin molecule CD81 in B and T cells. Immunol Res 58(2–3):179–185

    Article  CAS  PubMed  Google Scholar 

  48. Phinney DG, Pittenger MF (2017) Concise review: MSC-derived exosomes for cell-free therapy. Stem Cells 35(4):851–858

    Article  CAS  PubMed  Google Scholar 

  49. Wang L et al (2018) Mesenchymal stem cell-derived exosomes reduce A1 astrocytes via downregulation of phosphorylated NFκB P65 subunit in spinal cord injury. Cell Physiol Biochem 50(4):1535–1559

    Article  CAS  PubMed  Google Scholar 

  50. Liu K et al (2021) Interleukin-1β-treated mesenchymal stem cells inhibit inflammation in hippocampal astrocytes through exosome-activated Nrf-2 signaling. Int J Nanomed 16:1423

    Article  Google Scholar 

  51. Pusic AD (2014) Neuroimmune signaling of environmental enrichment; the role of exosomes in remyelination, The University of Chicago.

  52. Xian P et al (2019) Mesenchymal stem cell-derived exosomes as a nanotherapeutic agent for amelioration of inflammation-induced astrocyte alterations in mice. Theranostics 9(20):5956–5975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Cheli VT et al (2016) L-type voltage-operated calcium channels contribute to astrocyte activation in vitro. Glia 64(8):1396–1415

    Article  PubMed  PubMed Central  Google Scholar 

  54. Men Y et al (2019) Exosome reporter mice reveal the involvement of exosomes in mediating neuron to astroglia communication in the CNS. Nat Commun 10(1):1–18

    Article  CAS  Google Scholar 

  55. Yang Y et al (2009) Presynaptic regulation of astroglial excitatory neurotransmitter transporter GLT1. Neuron 61(6):880–894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Gharbi T, Zhang Z, Yang G-Y (2020) The function of astrocyte mediated extracellular vesicles in central nervous system diseases. Front Cell Dev Biol 8:568889–568889

    Article  PubMed  PubMed Central  Google Scholar 

  57. Zhou X, He X, Ren Y (2014) Function of microglia and macrophages in secondary damage after spinal cord injury. Neural Regen Res 9(20):1787

    Article  PubMed  PubMed Central  Google Scholar 

  58. Zhou T et al (2017) Microglia polarization with M1/M2 phenotype changes in rd1 mouse model of retinal degeneration. Front Neuroanat 11:77

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Zhou L, et al (2020) DHZCP modulates microglial M1/M2 polarization via the p38 and TLR4/NF-κB signaling pathways in LPS-stimulated microglial cells. Front Pharmacol 11.

  60. Thored P et al (2009) Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 57(8):835–849

    Article  PubMed  Google Scholar 

  61. Kwon MJ et al (2013) Contribution of macrophages to enhanced regenerative capacity of dorsal root ganglia sensory neurons by conditioning injury. J Neurosci 33(38):15095–15108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Liu Z et al (2007) Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 38(1):146–152

    Article  CAS  PubMed  Google Scholar 

  63. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8(12):958–969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. David S, Kroner A (2011) Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 12(7):388–399

    Article  CAS  PubMed  Google Scholar 

  65. Hu X et al (2015) Microglial and macrophage polarization—new prospects for brain repair. Nat Rev Neurol 11(1):56–64

    Article  PubMed  Google Scholar 

  66. Liu W 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 Neuroinflammation 17(1):1–22

    Article  CAS  Google Scholar 

  67. Li Y et al (2017) Exosomes secreted by stem cells from human exfoliated deciduous teeth contribute to functional recovery after traumatic brain injury by shifting microglia M1/M2 polarization in rats. Stem Cell Res Ther 8(1):1–11

    Article  CAS  Google Scholar 

  68. Wu J, Wang C, Ding H (2020) LncRNA MALAT1 promotes neuropathic pain progression through the miR-154-5p/AQP9 axis in CCI rat models. Mol Med Rep 21(1):291–303

    CAS  PubMed  Google Scholar 

  69. Cui Y et al (2019) LncRNA Neat1 mediates miR-124-induced activation of Wnt/β-catenin signaling in spinal cord neural progenitor cells. Stem Cell Res Ther 10(1):1–11

    Article  CAS  Google Scholar 

  70. Pinto S et al (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

    Article  PubMed  PubMed Central  Google Scholar 

  71. Madji Hounoum B et al (2016) NSC-34 motor neuron-like cells are unsuitable as experimental model for glutamate-mediated excitotoxicity. Front Cell Neurosci 10:118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Zheng Y et al (2019) Exosomes from LPS-stimulated macrophages induce neuroprotection and functional improvement after ischemic stroke by modulating microglial polarization. Biomater Sci 7(5):2037–2049

    Article  CAS  PubMed  Google Scholar 

  73. Long X et al (2020) Astrocyte-derived exosomes enriched with miR-873a-5p inhibit neuroinflammation via microglia phenotype modulation after traumatic brain injury. J Neuroinflammation 17(1):1–15

    Article  CAS  Google Scholar 

  74. Sohel MH (2016) Extracellular/circulating microRNAs: release mechanisms, functions and challenges. Achiev Life Sci 10(2):175–186

    Google Scholar 

  75. Liu X et al (2021) Bone marrow mesenchymal stem cell-derived exosomes attenuate cerebral ischemia-reperfusion injury-induced neuroinflammation and pyroptosis by modulating microglia M1/M2 phenotypes. Exp Neurol 341:113700

    Article  CAS  PubMed  Google Scholar 

  76. Shao M et al (2020) Exosomes from long noncoding RNA-Gm37494-ADSCs repair spinal cord injury via shifting microglial M1/M2 polarization. Inflammation 43(4):1536–1547

    Article  CAS  PubMed  Google Scholar 

  77. Zhang G, Yang P (2018) A novel cell-cell communication mechanism in the nervous system: exosomes. J Neurosci Res 96(1):45–52

    Article  CAS  PubMed  Google Scholar 

  78. Heidarzadeh M et al (2021) Exosomal delivery of therapeutic modulators through the blood–brain barrier; promise and pitfalls. Cell Biosci 11(1):142

    Article  PubMed  PubMed Central  Google Scholar 

  79. Yuan D et al (2017) Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials 142:1–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Zhuang X et al (2011) Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther 19(10):1769–1779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Dreyer F, Baur A (2016) Biogenesis and functions of exosomes and extracellular vesicles. Lentiviral Vectors Exosomes Gene Protein Deliv Tools 2016:201–216

    Article  CAS  Google Scholar 

  82. Mingozzi F et al (2013) Overcoming preexisting humoral immunity to AAV using capsid decoys. Sci Transl Med 5(194):194ra92-194ra92

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Orefice NS et al (2019) Real-time monitoring of exosome enveloped-AAV spreading by endomicroscopy approach: a new tool for gene delivery in the brain. Mol Ther-Meth Clin Dev 14:237–251

    Article  CAS  Google Scholar 

  84. Khongkow M et al (2019) Surface modification of gold nanoparticles with neuron-targeted exosome for enhanced blood–brain barrier penetration. Sci Rep 9(1):1–9

    Article  CAS  Google Scholar 

  85. Yang J et al (2020) Therapeutic effects of simultaneous delivery of nerve growth factor mrna and protein via exosomes on cerebral ischemia. Mol Ther-Nucleic Acids 21:512–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Jiang M et al (2018) Exosomes from MiR-30d-5p-ADSCs reverse acute ischemic stroke-induced, autophagy-mediated brain injury by promoting M2 microglial/macrophage polarization. Cell Physiol Biochem 47(2):864–878

    Article  CAS  PubMed  Google Scholar 

  87. Lee M et al (2018) The exosome of adipose-derived stem cells reduces β-amyloid pathology and apoptosis of neuronal cells derived from the transgenic mouse model of Alzheimer’s disease. Brain Res 1691:87–93

    Article  CAS  PubMed  Google Scholar 

  88. Geng W et al (2019) Exosomes from miRNA-126-modified ADSCs promotes functional recovery after stroke in rats by improving neurogenesis and suppressing microglia activation. Am J Transl Res 11(2):780

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Liu M, Hu Y, Chen G (2020) The antitumor effect of gene-engineered exosomes in the treatment of brain metastasis of breast cancer. Front Oncol 10:1453

    Article  PubMed  PubMed Central  Google Scholar 

  90. Rajabi H et al (2019) Current status of used protocols for mesenchymal stem cell differentiation: a focus on insulin producing, osteoblast-like and neural cells. Curr Stem Cell Res Ther 14(7):570–578

    Article  CAS  PubMed  Google Scholar 

  91. Bellavia D et al (2017) Interleukin 3-receptor targeted exosomes inhibit in vitro and in vivo chronic myelogenous leukemia cell growth. Theranostics 7(5):1333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. D’Souza A et al (2021) Targeting the blood-brain barrier for the delivery of stroke therapies. Adv Drug Deliv Rev 171:332–351

    Article  CAS  PubMed  Google Scholar 

  93. Alvarez-Erviti L et al (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29(4):341–345

    Article  CAS  PubMed  Google Scholar 

  94. Grapp M et al (2013) Choroid plexus transcytosis and exosome shuttling deliver folate into brain parenchyma. Nat Commun 4(1):1–13

    Article  CAS  Google Scholar 

  95. Li Y et al (2017) Exosomes secreted by stem cells from human exfoliated deciduous teeth contribute to functional recovery after traumatic brain injury by shifting microglia M1/M2 polarization in rats. Stem Cell Res Ther 8(1):198–198

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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This study was supported by a grant from Koç University.

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M.H., S.S., and M.K. reviewed the literature and prepared a draft. E.S. and R.R. supervised the study.

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Correspondence to Emel Sokullu or Reza Rahbarghazi.

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Heidarzadeh, M., Sokullu, E., Saghati, S. et al. Insights into the Critical Role of Exosomes in the Brain; from Neuronal Activity to Therapeutic Effects. Mol Neurobiol 59, 4453–4465 (2022). https://doi.org/10.1007/s12035-022-02853-z

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