Publications by authors named "Nicolas Chenouard"

19 Publications

  • Page 1 of 1

Unique dynamics and exocytosis properties of GABAergic synaptic vesicles revealed by three-dimensional single vesicle tracking.

Proc Natl Acad Sci U S A 2021 Mar;118(9)

Division of Life Science, The Hong Kong University of Science and Technology, Clear Water Bay, 999077 Kowloon, Hong Kong;

Maintaining the balance between neuronal excitation and inhibition is essential for proper function of the central nervous system. Inhibitory synaptic transmission plays an important role in maintaining this balance. Although inhibitory transmission has higher kinetic demands compared to excitatory transmission, its properties are poorly understood. In particular, the dynamics and exocytosis of single inhibitory vesicles have not been investigated, due largely to both technical and practical limitations. Using a combination of quantum dots (QDs) conjugated to antibodies against the luminal domain of the vesicular GABA transporter to selectively label GABAergic (i.e., predominantly inhibitory) vesicles together with dual-focus imaging optics, we tracked the real-time three-dimensional position of single GABAergic vesicles up to the moment of exocytosis (i.e., fusion). Using three-dimensional trajectories, we found that GABAergic synaptic vesicles traveled a shorter distance prior to fusion and had a shorter time to fusion compared to synaptotagmin-1 (Syt1)-labeled vesicles, which were mostly from excitatory neurons. Moreover, our analysis revealed that GABAergic synaptic vesicles move more straightly to their release sites than Syt1-labeled vesicles. Finally, we found that GABAergic vesicles have a higher prevalence of kiss-and-run fusion than Syt1-labeled vesicles. These results indicate that inhibitory synaptic vesicles have a unique set of dynamics and exocytosis properties to support rapid synaptic inhibition, thereby maintaining a tightly regulated coordination between excitation and inhibition in the central nervous system.
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http://dx.doi.org/10.1073/pnas.2022133118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7936280PMC
March 2021

An increase in dendritic plateau potentials is associated with experience-dependent cortical map reorganization.

Proc Natl Acad Sci U S A 2021 Mar;118(9)

Department of Basic Neurosciences and the Center for Neuroscience, Centre Médical Universitaire (CMU), University of Geneva, 1211 Geneva, Switzerland;

The organization of sensory maps in the cerebral cortex depends on experience, which drives homeostatic and long-term synaptic plasticity of cortico-cortical circuits. In the mouse primary somatosensory cortex (S1) afferents from the higher-order, posterior medial thalamic nucleus (POm) gate synaptic plasticity in layer (L) 2/3 pyramidal neurons via disinhibition and the production of dendritic plateau potentials. Here we address whether these thalamocortically mediated responses play a role in whisker map plasticity in S1. We find that trimming all but two whiskers causes a partial fusion of the representations of the two spared whiskers, concomitantly with an increase in the occurrence of POm-driven -methyl-D-aspartate receptor-dependent plateau potentials. Blocking the plateau potentials restores the archetypical organization of the sensory map. Our results reveal a mechanism for experience-dependent cortical map plasticity in which higher-order thalamocortically mediated plateau potentials facilitate the fusion of normally segregated cortical representations.
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http://dx.doi.org/10.1073/pnas.2024920118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7936269PMC
March 2021

The integration of Gaussian noise by long-range amygdala inputs in frontal circuit promotes fear learning in mice.

Elife 2020 11 30;9. Epub 2020 Nov 30.

University of Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, Bordeaux, France.

Survival depends on the ability of animals to select the appropriate behavior in response to threat and safety sensory cues. However, the synaptic and circuit mechanisms by which the brain learns to encode accurate predictors of threat and safety remain largely unexplored. Here, we show that frontal association cortex (FrA) pyramidal neurons of mice integrate auditory cues and basolateral amygdala (BLA) inputs non-linearly in a NMDAR-dependent manner. We found that the response of FrA pyramidal neurons was more pronounced to Gaussian noise than to pure frequency tones, and that the activation of BLA-to-FrA axons was the strongest in between conditioning pairings. Blocking BLA-to-FrA signaling specifically at the time of presentation of Gaussian noise (but not 8 kHz tone) between conditioning trials impaired the formation of auditory fear memories. Taken together, our data reveal a circuit mechanism that facilitates the formation of fear traces in the FrA, thus providing a new framework for probing discriminative learning and related disorders.
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http://dx.doi.org/10.7554/eLife.62594DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7704104PMC
November 2020

Synaptic vesicle traffic is supported by transient actin filaments and regulated by PKA and NO.

Nat Commun 2020 10 21;11(1):5318. Epub 2020 Oct 21.

NYU Neuroscience Institute and Department of Neuroscience and Physiology, NYU Langone Medical Center, New York, NY, 10016, USA.

Synaptic vesicles (SVs) can be pooled across multiple synapses, prompting questions about their dynamic allocation for neurotransmission and plasticity. We find that the axonal traffic of recycling vesicles is not supported by ubiquitous microtubule-based motility but relies on actin instead. Vesicles freed from synaptic clusters undergo ~1 µm bouts of active transport, initiated by nearby elongation of actin filaments. Long distance translocation arises when successive bouts of active transport were linked by periods of free diffusion. The availability of SVs for active transport can be promptly increased by protein kinase A, a key player in neuromodulation. Vesicle motion is in turn impeded by shutting off axonal actin polymerization, mediated by nitric oxide-cyclic GMP signaling leading to inhibition of RhoA. These findings provide a potential framework for coordinating post-and pre-synaptic strength, using retrograde regulation of axonal actin dynamics to mobilize and recruit presynaptic SV resources.
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http://dx.doi.org/10.1038/s41467-020-19120-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7578807PMC
October 2020

AMPAR-Dependent Synaptic Plasticity Initiates Cortical Remapping and Adaptive Behaviors during Sensory Experience.

Cell Rep 2020 09;32(9):108097

University of Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297, 33000 Bordeaux, France. Electronic address:

Cortical plasticity improves behaviors and helps recover lost functions after injury. However, the underlying synaptic mechanisms remain unclear. In mice, we show that trimming all but one whisker enhances sensory responses from the spared whisker in the barrel cortex and occludes whisker-mediated synaptic potentiation (w-Pot) in vivo. In addition, whisker-dependent behaviors that are initially impaired by single-whisker experience (SWE) rapidly recover when associated cortical regions remap. Cross-linking the surface GluA2 subunit of AMPA receptors (AMPARs) suppresses the expression of w-Pot, presumably by blocking AMPAR surface diffusion, in mice with all whiskers intact, indicating that synaptic potentiation in vivo requires AMPAR trafficking. We use this approach to demonstrate that w-Pot is required for SWE-mediated strengthening of synaptic inputs and initiates the recovery of previously learned skills during the early phases of SWE. Taken together, our data reveal that w-Pot mediates cortical remapping and behavioral improvement upon partial sensory deafferentation.
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http://dx.doi.org/10.1016/j.celrep.2020.108097DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7487777PMC
September 2020

Neuronal Inactivity Co-opts LTP Machinery to Drive Potassium Channel Splicing and Homeostatic Spike Widening.

Cell 2020 06 2;181(7):1547-1565.e15. Epub 2020 Jun 2.

Department of Neuroscience and Physiology, Neuroscience Institute, NYU Grossman Medical Center, New York, NY 10016, USA; Center for Neural Science, New York University, New York, NY 10003, USA. Electronic address:

Homeostasis of neural firing properties is important in stabilizing neuronal circuitry, but how such plasticity might depend on alternative splicing is not known. Here we report that chronic inactivity homeostatically increases action potential duration by changing alternative splicing of BK channels; this requires nuclear export of the splicing factor Nova-2. Inactivity and Nova-2 relocation were connected by a novel synapto-nuclear signaling pathway that surprisingly invoked mechanisms akin to Hebbian plasticity: Ca-permeable AMPA receptor upregulation, L-type Ca channel activation, enhanced spine Ca transients, nuclear translocation of a CaM shuttle, and nuclear CaMKIV activation. These findings not only uncover commonalities between homeostatic and Hebbian plasticity but also connect homeostatic regulation of synaptic transmission and neuronal excitability. The signaling cascade provides a full-loop mechanism for a classic autoregulatory feedback loop proposed ∼25 years ago. Each element of the loop has been implicated previously in neuropsychiatric disease.
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http://dx.doi.org/10.1016/j.cell.2020.05.013DOI Listing
June 2020

Imaging intraflagellar transport in trypanosomes.

Methods Cell Biol 2015 7;127:487-508. Epub 2015 Mar 7.

Trypanosome Cell Biology Unit, Institut Pasteur & CNRS URA2581, Paris, France.

Trypanosoma brucei is a flagellated eukaryotic pathogen responsible for sleeping sickness in central Africa. Because of the presence of a long motile flagellum (>20 μm) and its amenity to genetic manipulation, it is becoming an attractive model to study the assembly and the functions of cilia and flagella. In recent years, several aspects have been investigated, especially intraflagellar transport (IFT) that has been exhaustively characterized at the light microscopy level. In this manuscript, we review various methods to express fluorescent fusion proteins and to record IFT in living trypanosomes in normal or mutant contexts. We present an approach for separating anterograde and retrograde IFT, hence facilitating quantification of train speed, frequency, and size. A statistical analysis to discriminate different subpopulations of IFT trains is also summarized. These methods have proven their efficiency for the study of IFT in trypanosomes and could be applied to any other organism.
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http://dx.doi.org/10.1016/bs.mcb.2015.01.005DOI Listing
January 2016

Stressed mycobacteria use the chaperone ClpB to sequester irreversibly oxidized proteins asymmetrically within and between cells.

Cell Host Microbe 2015 Feb 22;17(2):178-90. Epub 2015 Jan 22.

Department of Microbiology and Immunology, Weill Cornell Medical College, New York, NY 10065, USA. Electronic address:

Mycobacterium tuberculosis (Mtb) defends itself against host immunity and chemotherapy at several levels, including the repair or degradation of irreversibly oxidized proteins (IOPs). To investigate how Mtb deals with IOPs that can neither be repaired nor degraded, we used new chemical and biochemical probes and improved image analysis algorithms for time-lapse microscopy to reveal a defense against stationary phase stress, oxidants, and antibiotics--the sequestration of IOPs into aggregates in association with the chaperone ClpB, followed by the asymmetric distribution of aggregates within bacteria and between their progeny. Progeny born with minimal IOPs grew faster and better survived a subsequent antibiotic stress than their IOP-burdened sibs. ClpB-deficient Mtb had a marked recovery defect from stationary phase or antibiotic exposure and survived poorly in mice. Treatment of tuberculosis might be assisted by drugs that cripple the pathway by which Mtb buffers, sequesters, and asymmetrically distributes IOPs.
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http://dx.doi.org/10.1016/j.chom.2014.12.008DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5707119PMC
February 2015

Objective comparison of particle tracking methods.

Nat Methods 2014 Mar 19;11(3):281-9. Epub 2014 Jan 19.

1] Department of Medical Informatics, Erasmus University Medical Center, Rotterdam, The Netherlands. [2] Department of Radiology, Erasmus University Medical Center, Rotterdam, The Netherlands. [3].

Particle tracking is of key importance for quantitative analysis of intracellular dynamic processes from time-lapse microscopy image data. Because manually detecting and following large numbers of individual particles is not feasible, automated computational methods have been developed for these tasks by many groups. Aiming to perform an objective comparison of methods, we gathered the community and organized an open competition in which participating teams applied their own methods independently to a commonly defined data set including diverse scenarios. Performance was assessed using commonly defined measures. Although no single method performed best across all scenarios, the results revealed clear differences between the various approaches, leading to notable practical conclusions for users and developers.
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http://dx.doi.org/10.1038/nmeth.2808DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4131736PMC
March 2014

Multiple hypothesis tracking for cluttered biological image sequences.

IEEE Trans Pattern Anal Mach Intell 2013 Nov;35(11):2736-3750

New York University School of Medicine, New York.

In this paper, we present a method for simultaneously tracking thousands of targets in biological image sequences, which is of major importance in modern biology. The complexity and inherent randomness of the problem lead us to propose a unified probabilistic framework for tracking biological particles in microscope images. The framework includes realistic models of particle motion and existence and of fluorescence image features. For the track extraction process per se, the very cluttered conditions motivate the adoption of a multiframe approach that enforces tracking decision robustness to poor imaging conditions and to random target movements. We tackle the large-scale nature of the problem by adapting the multiple hypothesis tracking algorithm to the proposed framework, resulting in a method with a favorable tradeoff between the model complexity and the computational cost of the tracking procedure. When compared to the state-of-the-art tracking techniques for bioimaging, the proposed algorithm is shown to be the only method providing high-quality results despite the critically poor imaging conditions and the dense target presence. We thus demonstrate the benefits of advanced Bayesian tracking techniques for the accurate computational modeling of dynamical biological processes, which is promising for further developments in this domain.
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http://dx.doi.org/10.1109/TPAMI.2013.97DOI Listing
November 2013

Spline-based deforming ellipsoids for interactive 3D bioimage segmentation.

IEEE Trans Image Process 2013 Oct 22;22(10):3926-40. Epub 2013 May 22.

Biomedical Imaging Group, École polytechnique fédérale de Lausanne, Lausanne, Switzerland.

We present a new fast active-contour model (a.k.a. snake) for image segmentation in 3D microscopy. We introduce a parametric design that relies on exponential B-spline bases and allows us to build snakes that are able to reproduce ellipsoids. We design our bases to have the shortest-possible support, subject to some constraints. Thus, computational efficiency is maximized. The proposed 3D snake can approximate blob-like objects with good accuracy and can perfectly reproduce spheres and ellipsoids, irrespective of their position and orientation. The optimization process is remarkably fast due to the use of Gauss' theorem within our energy computation scheme. Our technique yields successful segmentation results, even for challenging data where object contours are not well defined. This is due to our parametric approach that allows one to favor prior shapes. In addition, this paper provides a software that gives full control over the snakes via an intuitive manipulation of few control points.
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http://dx.doi.org/10.1109/TIP.2013.2264680DOI Listing
October 2013

Intraflagellar transport proteins cycle between the flagellum and its base.

J Cell Sci 2013 Jan 19;126(Pt 1):327-38. Epub 2012 Sep 19.

Trypanosome Cell Biology Unit, Institut Pasteur and CNRS URA2581, 25 rue du Docteur Roux, 75015 Paris, France.

Intraflagellar transport (IFT) is necessary for the construction of cilia and flagella. IFT proteins are concentrated at the base of the flagellum but little is known about the actual role of this pool of proteins. Here, IFT was investigated in Trypanosoma brucei, an attractive model for flagellum studies, using GFP fusions with IFT52 or the IFT dynein heavy chain DHC2.1. Tracking analysis by a curvelet method allowing automated separation of forward and return transport demonstrated a uniform speed for retrograde IFT (5 µm s(-1)) but two distinct populations for anterograde movement that are sensitive to temperature. When they reach the distal tip, anterograde trains are split into three and converted to retrograde trains. When a fast anterograde train catches up with a slow one, it is almost twice as likely to fuse with it rather than to overtake it, implying that these trains travel on a restricted set of microtubules. Using photobleaching experiments, we show for the first time that IFT proteins coming back from the flagellum are mixed with those present at the flagellum base and can reiterate a full IFT cycle in the flagellum. This recycling is dependent on flagellum length and IFT velocities. Mathematical modelling integrating all parameters actually reveals the existence of two pools of IFT proteins at the flagellum base, but only one is actively engaged in IFT.
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http://dx.doi.org/10.1242/jcs.117069DOI Listing
January 2013

3D steerable wavelets in practice.

IEEE Trans Image Process 2012 Nov 26;21(11):4522-33. Epub 2012 Jun 26.

Biomedical Imaging Group, École Polytechnique Fédérale de Lausanne, Lausanne CH-1015, Switzerland.

We introduce a systematic and practical design for steerable wavelet frames in 3D. Our steerable wavelets are obtained by applying a 3D version of the generalized Riesz transform to a primary isotropic wavelet frame. The novel transform is self-reversible (tight frame) and its elementary constituents (Riesz wavelets) can be efficiently rotated in any 3D direction by forming appropriate linear combinations. Moreover, the basis functions at a given location can be linearly combined to design custom (and adaptive) steerable wavelets. The features of the proposed method are illustrated with the processing and analysis of 3D biomedical data. In particular, we show how those wavelets can be used to characterize directional patterns and to detect edges by means of a 3D monogenic analysis. We also propose a new inverse-problem formalism along with an optimization algorithm for reconstructing 3D images from a sparse set of wavelet-domain edges. The scheme results in high-quality image reconstructions which demonstrate the feature-reduction ability of the steerable wavelets as well as their potential for solving inverse problems.
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http://dx.doi.org/10.1109/TIP.2012.2206044DOI Listing
November 2012

Icy: an open bioimage informatics platform for extended reproducible research.

Nat Methods 2012 Jun 28;9(7):690-6. Epub 2012 Jun 28.

Institut Pasteur, Unité d'Analyse d'Images Quantitative, Centre National de la Recherche Scientifique, Unité de Recherche Associée 2582, Paris, France.

Current research in biology uses evermore complex computational and imaging tools. Here we describe Icy, a collaborative bioimage informatics platform that combines a community website for contributing and sharing tools and material, and software with a high-end visual programming framework for seamless development of sophisticated imaging workflows. Icy extends the reproducible research principles, by encouraging and facilitating the reusability, modularity, standardization and management of algorithms and protocols. Icy is free, open-source and available at http://icy.bioimageanalysis.org/.
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http://dx.doi.org/10.1038/nmeth.2075DOI Listing
June 2012

Steerable pyramids and tight wavelet frames in L2(R(d)).

IEEE Trans Image Process 2011 Oct 7;20(10):2705-21. Epub 2011 Apr 7.

Biomedical Imaging Group, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland.

We present a functional framework for the design of tight steerable wavelet frames in any number of dimensions. The 2-D version of the method can be viewed as a generalization of Simoncelli's steerable pyramid that gives access to a larger palette of steerable wavelets via a suitable parametrization. The backbone of our construction is a primal isotropic wavelet frame that provides the multiresolution decomposition of the signal. The steerable wavelets are obtained by applying a one-to-many mapping (Nth-order generalized Riesz transform) to the primal ones. The shaping of the steerable wavelets is controlled by an M×M unitary matrix (where M is the number of wavelet channels) that can be selected arbitrarily; this allows for a much wider range of solutions than the traditional equiangular configuration (steerable pyramid). We give a complete functional description of these generalized wavelet transforms and derive their steering equations. We describe some concrete examples of transforms, including some built around a Mallat-type multiresolution analysis of L(2)(R(d)), and provide a fast Fourier transform-based decomposition algorithm. We also propose a principal-component-based method for signal-adapted wavelet design. Finally, we present some illustrative examples together with a comparison of the denoising performance of various brands of steerable transforms. The results are in favor of an optimized wavelet design (equalized principal component analysis), which consistently performs best.
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http://dx.doi.org/10.1109/TIP.2011.2138147DOI Listing
October 2011

In vivo colocalisation of oskar mRNA and trans-acting proteins revealed by quantitative imaging of the Drosophila oocyte.

PLoS One 2009 Jul 14;4(7):e6241. Epub 2009 Jul 14.

Unité de Biologie Cellulaire du Noyau, Département de Biologie Cellulaire et Infection, Institut Pasteur, Paris, France.

Efficient mRNA transport in eukaryotes requires highly orchestrated relationships between nuclear and cytoplasmic proteins. For oskar mRNA, the Drosophila posterior determinant, these spatio-temporal requirements remain opaque during its multi-step transport process. By in vivo covisualization of oskar mRNA with Staufen, its putative trafficking protein, we find oskar mRNA to be present in particles distinct from Staufen for part of its transport. oskar mRNA stably associated with Staufen near the posterior pole. We observe oskar mRNA to oligomerize as hundreds of copies forming large particles which are necessary for its long range transport and localization. We show the formation of these particles occurs in the nurse cell nucleus in an Hrp48-dependent manner. We present a more refined model of oskar mRNA transport in the Drosophila oocyte.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0006241PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2705681PMC
July 2009

Tracking algorithms chase down pathogens.

Biotechnol J 2009 Jun;4(6):838-45

Institut Pasteur, Unité d'Analyse d'Images Quantitative, CNRS URA 2582, Paris, France.

Understanding subcellular dynamic processes governing pathogenic mechanisms is a necessary step towards the development of new drugs and strategies against infectious diseases. Subcellular pathogenic mechanisms, such as viral invasion processes involve highly dynamic nanometric-scale objects and rapid molecular interactions that require the study of individual particle paths. Single-particle tracking methods allow visualizing and characterizing the dynamics of biological objects, and provide a straightforward and accurate means to understand subcellular processes. This review describes a number of particle-tracking methods in time-lapse microscopy sequences and provides examples of using such techniques to investigate mechanisms of host-pathogen interactions.
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http://dx.doi.org/10.1002/biot.200900030DOI Listing
June 2009

Prions hijack tunnelling nanotubes for intercellular spread.

Nat Cell Biol 2009 Mar 8;11(3):328-36. Epub 2009 Feb 8.

Unité de Trafic Membranaire et Pathogénèse, Institut Pasteur, 25 rue du Dr Roux, 75724 Paris Cedex 15, France.

In variant Creutzfeldt-Jakob disease, prions (PrP(Sc)) enter the body with contaminated foodstuffs and can spread from the intestinal entry site to the central nervous system (CNS) by intercellular transfer from the lymphoid system to the peripheral nervous system (PNS). Although several means and different cell types have been proposed to have a role, the mechanism of cell-to-cell spreading remains elusive. Tunnelling nanotubes (TNTs) have been identified between cells, both in vitro and in vivo, and may represent a conserved means of cell-to-cell communication. Here we show that TNTs allow transfer of exogenous and endogenous PrP(Sc) between infected and naive neuronal CAD cells. Significantly, transfer of endogenous PrP(Sc) aggregates was detected exclusively when cells chronically infected with the 139A mouse prion strain were connected to mouse CAD cells by means of TNTs, identifying TNTs as an efficient route for PrP(Sc) spreading in neuronal cells. In addition, we detected the transfer of labelled PrP(Sc) from bone marrow-derived dendritic cells to primary neurons connected through TNTs. Because dendritic cells can interact with peripheral neurons in lymphoid organs, TNT-mediated intercellular transfer would allow neurons to transport prions retrogradely to the CNS. We therefore propose that TNTs are involved in the spreading of PrP(Sc) within neurons in the CNS and from the peripheral site of entry to the PNS by neuroimmune interactions with dendritic cells.
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http://dx.doi.org/10.1038/ncb1841DOI Listing
March 2009

A dual role for actin and microtubule cytoskeleton in the transport of Golgi units from the nurse cells to the oocyte across ring canals.

Mol Biol Cell 2009 Jan 12;20(1):556-68. Epub 2008 Nov 12.

Morphogenesis and Polarity Unit, Institut Jacques Monod, Paris, France.

Axis specification during Drosophila embryonic development requires transfer of maternal components during oogenesis from nurse cells (NCs) into the oocyte through cytoplasmic bridges. We found that the asymmetrical distribution of Golgi, between nurse cells and the oocyte, is sustained by an active transport process. We have characterized actin basket structures that asymmetrically cap the NC side of Ring canals (RCs) connecting the oocyte. Our results suggest that these actin baskets structurally support transport mechanisms of RC transit. In addition, our tracking analysis indicates that Golgi are actively transported to the oocyte rather than diffusing. We observed that RC transit is microtubule-based and mediated at least by dynein. Finally, we show that actin networks may be involved in RC crossing through a myosin II step process, as well as in dispatching Golgi units inside the oocyte subcompartments.
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http://dx.doi.org/10.1091/mbc.e08-04-0360DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2613086PMC
January 2009