Neurotransmitter-Triggered Transfer of Exosomes Mediates Oligodendrocyte–Neuron Communication

Frühbeis, Carsten; Fröhlich, Dominik; Kuo, Wen Ping; Amphornrat, Jesa; Thilemann, Sebastian; Saab, Aiman S.; Kirchhoff, Frank; Möbius, Wiebke; Goebbels, Sandra; Nave, Klaus‐Armin; Schneider, Anja; Simons, Mikael; Klugmann, Matthias; Trotter, Jacqueline; Krämer-Albers, Eva-Maria

doi:10.1371/journal.pbio.1001604

Cited by 685 publications

(668 citation statements)

References 89 publications

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“…Schematic of some main aspects of the roamer type of VT and of its possible implications for integrative actions in the CNS. It was shown inter alia that (i) exosomes can mediate oligodendrocyte -neuron communication [77]; (ii) exosomes can play a role in interconnections between brain and peripheral organs since, for example, cardiac myocytes release exosomes [84] and exosomes can cross the blood -brain barrier [85]; and (iii) exosomes can cause transient cell phenotype changes. Thus, it was shown that exosomes allow intercellular transfer of GPCRs [53].…”

Section: (C) Central Nervous Systemmentioning

confidence: 99%

“…The astrocytic EMVs move into the extracellular space and carry a large number of transfer compounds such as mitochondria, mitochondrial DNA (mtDNA), ATP, Hsp70, functional glutamate transporters, FGF-2, miRNA, etc. (table 3) [68,[73][74][75][76][77][78]. The acceptor cells are both astrocytes and neurons and dependent on the cargo in the EMVs they may produce, for example, neuroprotection or degeneration [68,79,80].…”

Section: (C) Central Nervous Systemmentioning

confidence: 99%

“…Axonally released glutamate activates exosome release from oligodendroglia mediated mainly by glial NMDA receptors [77]. It is linked to the electrical activity of neurons which in turn can internalize the oligodendroglial exosomes.…”

Section: (C) Central Nervous Systemmentioning

confidence: 99%

See 2 more Smart Citations

Extracellular-vesicle type of volume transmission and tunnelling-nanotube type of wiring transmission add a new dimension to brain neuro-glial networks

Agnati

Fuxé

2014

Phil. Trans. R. Soc. B

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Two major types of intercellular communication are found in the central nervous system (CNS), namely wiring transmission (WT; point-to-point communication via private channels, e.g. synaptic transmission) and volume transmission (VT; communication in the extracellular fluid and in the cerebrospinal fluid). Volume and synaptic transmission become integrated because their chemical signals activate different types of interacting receptors in heteroreceptor complexes located synaptically and extrasynaptically in the plasma membrane. In VT, we focus on the role of the extracellular-vesicle type of VT, and in WT, on the potential role of the tunnelling-nanotube (TNT) type of WT. The so-called exosomes appear to be the major vesicular carrier for intercellular communication but the larger microvesicles also participate. Extracellular vesicles are released from cultured cortical neurons and different types of glial cells and modulate the signalling of the neuronal -glial networks of the CNS. This type of VT has pathological relevance, and epigenetic mechanisms may participate in the modulation of extracellular-vesicle-mediated VT. Gerdes and co-workers proposed the existence of a novel type of WT based on TNTs, which are straight transcellular channels leading to the formation in vitro of syncytial cellular networks found also in neuronal and glial cultures.

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Section: (C) Central Nervous Systemmentioning

confidence: 99%

Section: (C) Central Nervous Systemmentioning

confidence: 99%

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Extracellular-vesicle type of volume transmission and tunnelling-nanotube type of wiring transmission add a new dimension to brain neuro-glial networks

Agnati

Fuxé

2014

Phil. Trans. R. Soc. B

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“…These released substances can affect neighbouring cells, either through well-known signalling pathways or, in the case of mRNA and miRNA secretion, by having a direct effect on gene expression [13]. In the nervous system, exosomes have been proposed to participate in myelin formation, neurite outgrowth and neuronal survival [14]. In light of these observations exosomes could be excellent mediators of neuronal-derived signals affecting the development of target organs.…”

Section: Axon-to-target Signallingmentioning

confidence: 99%

Roles of innervation in developing and regenerating orofacial tissues

Pagella

Jiménez-Rojo

Mitsiadis

2014

Cell. Mol. Life Sci.

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The head is innervated by 12 cranial nerves (I-XII) that regulate its sensory and motor functions. Cranial nerves are composed of sensory, motor, or mixed neuronal populations. Sensory neurons perceive generally somatic sensations such as pressure, pain, and temperature. These neurons are also involved in smell, vision, taste, and hearing. Motor neurons ensure the motility of all muscles and glands. Innervation plays an essential role in the development of the various orofacial structures during embryogenesis. Hypoplastic cranial nerves often lead to abnormal development of their target organs and tissues. For example, Möbius syndrome is a congenital disease characterized by defective innervation (i.e., abducens (VI) and facial (VII) nerves), deafness, tooth anomalies, and cleft palate. Hence, it is obvious that the peripheral nervous system is needed for both development and function of orofacial structures. Nerves have a limited capacity to regenerate. However, neural stem cells, which could be used as sources for neural tissue maintenance and repair, have been found in adult neuronal tissues. Similarly, various adult stem cell populations have been isolated from almost all organs of the human body. Stem cells are tightly regulated by their microenvironment, the stem cell niche. Deregulation of adult stem cell behavior results in the development of pathologies such as tumor formation or early tissue senescence. It is thus essential to understand the factors that regulate the functions and maintenance of stem cells. Yet, the potential importance of innervation in the regulation of stem cells and/or their niches in most organs and tissues is largely unexplored. This review focuses on the potential role of innervation in the development and homeostasis of orofacial structures and discusses its possible association with stem cell populations during tissue repair.

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“…They showed that activity-dependent release of the neurotransmitter glutamate triggers oligodendroglial exosome secretion mediated by Ca 2þ entry through oligodendroglial NMDA and AMPA receptors. In turn, neurons internalize the released exosomes by endocytosis [59].…”

Section: (I) Additional Data Relating To Exosomesmentioning

confidence: 99%

The role of epigenetic-related codes in neurocomputation: dynamic hardware in the brain

Edelstein

Smythies

2014

Phil. Trans. R. Soc. B

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This paper presents a review of recent work on the role that two epigeneticrelated systems may play in information processing mechanisms in the brain. The first consists of exosomes that transport epigenetic-related molecules between neurons. The second consists of homeoproteins like Otx2 that carry information from sense organs to primary sensory cortex. There is developing evidence that presynaptic neurons may be able to modulate the fine microanatomical structure in the postsynaptic neuron. This may be conducted by three mechanisms, of which the first is well established and the latter two are novel. (i) By the well-established activation of receptors that trigger a chain of signalling molecules (second messengers) that result in the upregulation and/or activation of a transcription factor. The two novel systems are the exosome system and homeoproteins. (ii) Exosomes are small vesicles that are released upon activation of the axon terminal, traverse the synaptic cleft, probably via astrocytes and are taken up by the postsynaptic neuron. They carry a load of signalling proteins and a variety of forms of RNA. These loads may then be transported widely throughout the postsynaptic neuron and engineer modulations in the fine structure of computational machinery by epigenetic-related processes. (iii) Otx2 is a transcription factor that, inter alia, controls the development and survival of PVþ GABAergic interneurons (PV cells) in the primary visual cortex. It is synthesized in the retina and is transported to the cortex by a presently unknown mechanism that probably includes direct cell-to-cell transfer, and may, or may not, include transfer by the dynein and exosome systems in addition. These three mechanisms explain a quantity of data from the field of de-and reafferentation plasticity. These data show that the modality of the presynaptic neuron controls to a large extent the modality of the postsynaptic neuron. However, the mechanism that effects this is currently unknown. The exosome and the homeoprotein hypotheses provide novel explanations to add to the well-established earlier mechanism described above.

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Neurotransmitter-Triggered Transfer of Exosomes Mediates Oligodendrocyte–Neuron Communication

Abstract: Neuronal activity provokes myelinating oligodendrocytes to release exosomes by stimulation of ionotropic glutamate receptors, and that once released, these vesicles are internalized by neurons conveying neuroprotection.

Cited by 685 publications

References 89 publications

Extracellular-vesicle type of volume transmission and tunnelling-nanotube type of wiring transmission add a new dimension to brain neuro-glial networks

Extracellular-vesicle type of volume transmission and tunnelling-nanotube type of wiring transmission add a new dimension to brain neuro-glial networks

Roles of innervation in developing and regenerating orofacial tissues

The role of epigenetic-related codes in neurocomputation: dynamic hardware in the brain

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