Structural and functional analysis of tunneling nanotubes (TnTs) using <i>g</i>CW STED and <i>g</i>confocal approaches

Bénard, Magalie; Schapman, Damien; Lebon, Alexis; Monterroso, Baptiste; Bellenger, Marine; Foll, Frank Le; Pasquier, Jennifer; Vaudry, Hubert; Vaudry, David; Galas, Ludovic

doi:10.1111/boc.201500004

Cited by 47 publications

(72 citation statements)

References 11 publications

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“…Confocal microscopy allowed the identification of actin-positive and tubulin-negative TNTs containing myosin 10 protein (Additional file 3: Figure S3 d) in neuronal CAD cells. These structures are easily detectable via live imaging in overexpressing systems of actin and tubulin, with a diameter of approximately 400 nm and lengths ranging from 10 to 30 μm (Additional file 4: Figure S4 a), and they are rapidly formed thanks to a “filopodia-like” (Additional file 4: Figure S4 b and d) or a “kiss-and-run” mechanism (Additional file 4: Figure S4 c and e), as previously described [24, 26, 27]. Altogether, these data showed that we have engineered all necessary tools for identifying TNTs.…”

Section: Resultsmentioning

confidence: 64%

Tunneling nanotube (TNT)-mediated neuron-to neuron transfer of pathological Tau protein assemblies

Tardivel

Bégard

Bousset

et al. 2016

acta neuropathol commun

219

185

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A given cell makes exchanges with its neighbors through a variety of means ranging from diffusible factors to vesicles. Cells use also tunneling nanotubes (TNTs), filamentous-actin-containing membranous structures that bridge and connect cells. First described in immune cells, TNTs facilitate HIV-1 transfer and are found in various cell types, including neurons. We show that the microtubule-associated protein Tau, a key player in Alzheimer’s disease, is a bona fide constituent of TNTs. This is important because Tau appears beside filamentous actin and myosin 10 as a specific marker of these fine protrusions of membranes and cytosol that are difficult to visualize. Furthermore, we observed that exogenous Tau species increase the number of TNTs established between primary neurons, thereby facilitating the intercellular transfer of Tau fibrils. In conclusion, Tau may contribute to the formation and function of the highly dynamic TNTs that may be involved in the prion-like propagation of Tau assemblies.Electronic supplementary materialThe online version of this article (doi:10.1186/s40478-016-0386-4) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 64%

Tunneling nanotube (TNT)-mediated neuron-to neuron transfer of pathological Tau protein assemblies

Tardivel

Bégard

Bousset

et al. 2016

acta neuropathol commun

219

185

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“…In contrast, basket/stellate cells coming from the IGL directly cross the PCL without any transient arrest phase [18]. Super-resolution approaches including STimulated Emission Depletion (STED) microscopy [40,41,42] and correlative microscopy [43] could now offer new possibilities to decipher the roles of cell–cell contacts between granule cells, basket/stellate cells, Purkinje cells, and Bergmann glial cells in key steps of cerebellar interneuron migration including the crossing of the PCL.…”

Section: Cellular Highway Network Within the First Two Postnatal mentioning

confidence: 99%

Postnatal Migration of Cerebellar Interneurons

et al. 2017

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Due to its continuing development after birth, the cerebellum represents a unique model for studying the postnatal orchestration of interneuron migration. The combination of fluorescent labeling and ex/in vivo imaging revealed a cellular highway network within cerebellar cortical layers (the external granular layer, the molecular layer, the Purkinje cell layer, and the internal granular layer). During the first two postnatal weeks, saltatory movements, transient stop phases, cell-cell interaction/contact, and degradation of the extracellular matrix mark out the route of cerebellar interneurons, notably granule cells and basket/stellate cells, to their final location. In addition, cortical-layer specific regulatory factors such as neuropeptides (pituitary adenylate cyclase-activating polypeptide (PACAP), somatostatin) or proteins (tissue-type plasminogen activator (tPA), insulin growth factor-1 (IGF-1)) have been shown to inhibit or stimulate the migratory process of interneurons. These factors show further complexity because somatostatin, PACAP, or tPA have opposite or no effect on interneuron migration depending on which layer or cell type they act upon. External factors originating from environmental conditions (light stimuli, pollutants), nutrients or drug of abuse (alcohol) also alter normal cell migration, leading to cerebellar disorders.

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“…Like EVs, TNTs also represent subtypes and heterogeneous morphological structures (Austefjord et al, 2014; Benard et al, 2015). However, biosynthesis of TNTs differs from EVs and is attributed to f-actin polymerization (Gungor-Ordueri et al, 2015; Osteikoetxea-Molnar et al, 2016).…”

Section: Biogenesis and Physicochemical Aspects Of Evs And Tntsmentioning

confidence: 99%

“…However, unlike EVs the TNTs are better known for shipping whole organelles by direct tubular connections between cells, such as mitochondria, lysosomes and Golgi vesicles (Rustom et al, 2002, 2004; Gerdes et al, 2007; Gurke et al, 2008b; Plotnikov et al, 2008; Wang and Gerdes, 2015; Han et al, 2016; Jackson et al, 2016; Torralba et al, 2016). The thicker subset of TNTs may range up to 0.7 microns (Onfelt et al, 2004; Benard et al, 2015), which is more favorable for the transport of larger organelles and lysosomal vesicles (Onfelt et al, 2006). TNTs also transport cytosolic Ca 2+ and electrical signals to neighboring cells (Wang et al, 2010; Smith et al, 2011; Lock et al, 2016).…”

Section: Tnts and Evs: Synergies In Cargo Transfer And Intercellular mentioning

confidence: 99%

Extracellular Vesicles, Tunneling Nanotubes, and Cellular Interplay: Synergies and Missing Links

Nawaz

Fatima

2017

Front. Mol. Biosci.

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The process of intercellular communication seems to have been a highly conserved evolutionary process. Higher eukaryotes use several means of intercellular communication to address both the changing physiological demands of the body and to fight against diseases. In recent years, there has been an increasing interest in understanding how cell-derived nanovesicles, known as extracellular vesicles (EVs), can function as normal paracrine mediators of intercellular communication, but can also elicit disease progression and may be used for innovative therapies. Over the last decade, a large body of evidence has accumulated to show that cells use cytoplasmic extensions comprising open-ended channels called tunneling nanotubes (TNTs) to connect cells at a long distance and facilitate the exchange of cytoplasmic material. TNTs are a different means of communication to classical gap junctions or cell fusions; since they are characterized by long distance bridging that transfers cytoplasmic organelles and intracellular vesicles between cells and represent the process of heteroplasmy. The role of EVs in cell communication is relatively well-understood, but how TNTs fit into this process is just emerging. The aim of this review is to describe the relationship between TNTs and EVs, and to discuss the synergies between these two crucial processes in the context of normal cellular cross-talk, physiological roles, modulation of immune responses, development of diseases, and their combinatory effects in tissue repair. At the present time this review appears to be the first summary of the implications of the overlapping roles of TNTs and EVs. We believe that a better appreciation of these parallel processes will improve our understanding on how these nanoscale conduits can be utilized as novel tools for targeted therapies.

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Structural and functional analysis of tunneling nanotubes (TnTs) using gCW STED and gconfocal approaches

Abstract: Due to large disparity of TnT-like structures in neuronal, immune, cancer or epithelial cells, high- and superresolution approaches can be utilised for full characterisation of these yet poorly understood routes of cell-to-cell communication.

Cited by 47 publications

References 11 publications

Tunneling nanotube (TNT)-mediated neuron-to neuron transfer of pathological Tau protein assemblies

Tunneling nanotube (TNT)-mediated neuron-to neuron transfer of pathological Tau protein assemblies

Postnatal Migration of Cerebellar Interneurons

Extracellular Vesicles, Tunneling Nanotubes, and Cellular Interplay: Synergies and Missing Links

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