Microvesicle and tunneling nanotube mediated intercellular transfer of g-protein coupled receptors in cell cultures

Guescini, Michele; Leo, Giuseppina; Genedani, Susanna; Carone, Chiara; Pederzoli, Francesca; Ciruela, Francisco; Guidolin, Diego; Stocchi, Vilberto; Mantuano, M.; Borroto-Escuela, Dasiel O.; Fuxé, Kjell; Agnati, Luigi F.

doi:10.1016/j.yexcr.2012.01.005

Cited by 72 publications

(56 citation statements)

References 68 publications

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“…Consistent with this view is the available experimental evidence on the intercellular transfer of GPCR and GPCR complexes by MVs (Guescini et al, 2012). This process can lead to a transient acquisition of recognition/decoding apparatuses by target cells.…”

Section: Discussionsupporting

confidence: 52%

“…Recently identified direct interactions with RTK (BorrotoEscuela et al, 2012;Di Liberto et al, 2017), indeed, open the possibility that GPCR complexes could modulate structural changes at the level of dendrites and dendritic spines. Furthermore, the reorganization of GPCR complexes in the postjunctional membrane of synapses and their possible stabilization by the interaction with specific adapter proteins could represent a molecular mechanism for learning and memory Fuxe et al, 2014b;Borroto-Escuela et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

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G protein-coupled receptor-receptor interactions give integrative dynamics to intercellular communication

Guidolin

Marcoli

Tortorella

et al. 2018

Reviews in the Neurosciences

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Abstract:The proposal of receptor-receptor interactions (RRIs) in the early 1980s broadened the view on the role of G protein-coupled receptors (GPCR) in the dynamics of the intercellular communication. RRIs, indeed, allow GPCR to operate not only as monomers but also as receptor complexes, in which the integration of the incoming signals depends on the number, spatial arrangement, and order of activation of the protomers forming the complex. The main biochemical mechanisms controlling the functional interplay of GPCR in the receptor complexes are direct allosteric interactions between protomer domains. The formation of these macromolecular assemblies has several physiologic implications in terms of the modulation of the signaling pathways and interaction with other membrane proteins. It also impacts on the emerging field of connectomics, as it contributes to set and tune the synaptic strength. Furthermore, recent evidence suggests that the transfer of GPCR and GPCR complexes between cells via the exosome pathway could enable the target cells to recognize/decode transmitters and/or modulators for which they did not express the pertinent receptors. Thus, this process may also open the possibility of a new type of redeployment of neural circuits. The fundamental aspects of GPCR complex formation and function are the focus of the present review article.

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Section: Discussionsupporting

confidence: 52%

Section: Discussionmentioning

confidence: 99%

G protein-coupled receptor-receptor interactions give integrative dynamics to intercellular communication

Guidolin

Marcoli

Tortorella

et al. 2018

Reviews in the Neurosciences

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“…(ii) Extracellular vesicle-mediated volume transmission signals Studies on cultured cortical nerve cells demonstrate that extracellular membrane vesicles (EMVs) can be released from nerve cells [45], and exosomes were proposed to be a new way of interneuronal communication [19,[46][47][48]. In EMV fractions from the above cultures, GluR2 subunits of the AMPA receptors were found together inter alia with cell adhesion molecule L1 (LICAM).…”

Section: (B) Soma Level (I) Soluble Volume Transmission Signalsmentioning

confidence: 99%

The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural–glial networks

Borroto-Escuela

Agnati

Bechter

et al. 2015

Phil. Trans. R. Soc. B

113

130

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One contribution of 16 to a discussion meeting issue 'Release of chemical transmitters from cell bodies and dendrites of nerve cells'. Two major types of intercellular communication are found in the central nervous system (CNS), namely wiring transmission (point-to-point communication, the prototype being synaptic transmission with axons and terminals) and volume transmission (VT; communication in the extracellular fluid and in the cerebrospinal fluid (CSF)) involving large numbers of cells in the CNS. Volume and synaptic transmission become integrated inter alia through the ability of their chemical signals to activate different types of receptor protomers in heteroreceptor complexes located synaptically or extrasynaptically in the plasma membrane. The demonstration of extracellular dopamine (DA) and serotonin (5-HT) fluorescence around the DA and 5-HT nerve cell bodies with the Falck-Hillarp formaldehyde fluorescence method after treatment with amphetamine and chlorimipramine, respectively, gave the first indications of the existence of VT in the brain, at least at the soma level. There exist different forms of VT. Early studies on VT only involved spread including diffusion and flow of soluble biological signals, especially transmitters and modulators, a communication called extrasynaptic (short distance) and long distance (paraaxonal and paravascular and CSF pathways) VT. Also, the extracellular vesicle type of VT was demonstrated. The exosomes (endosome-derived vesicles) appear to be the major vesicular carriers for VT but the larger microvesicles also participate. Both mainly originate at the soma-dendritic level. They can transfer lipids and proteins, including receptors, Rab GTPases, tetraspanins, cholesterol, sphingolipids and ceramide. Within them there are also subsets of mRNAs and non-coding regulatory microRNAs. At the soma-dendritic membrane, sets of dynamic postsynaptic heteroreceptor complexes (built up of different types of physically interacting receptors and proteins) involving inter alia G protein-coupled receptors including autoreceptors, ion channel receptors and receptor tyrosine kinases are hypothesized to be the molecular basis for learning and memory. At nerve terminals, the presynaptic heteroreceptor complexes are postulated to undergo plastic changes to maintain the pattern of multiple transmitter release reflecting the firing pattern to be learned by the heteroreceptor complexes in the postsynaptic membrane.

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“…Within them, we can also find subsets of mRNAs and non-coding regulatory microRNAs [31,53,54]. They probably have a major role in moving the target cells into a novel but transient phenotypic state.…”

Section: Extracellular-vesicle-mediated Volume Transmission the Roammentioning

confidence: 99%

“…Thus, the ability was investigated whether target cells can recognize and decode signals by means of receptors that they did not previously express [54]. The findings demonstrated that adenosine Figure 2.…”

Section: (C) Central Nervous Systemmentioning

confidence: 99%

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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Microvesicle and tunneling nanotube mediated intercellular transfer of g-protein coupled receptors in cell cultures

Cited by 72 publications

References 68 publications

G protein-coupled receptor-receptor interactions give integrative dynamics to intercellular communication

G protein-coupled receptor-receptor interactions give integrative dynamics to intercellular communication

The role of transmitter diffusion and flow versus extracellular vesicles in volume transmission in the brain neural–glial networks

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

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