The extracellular matrix controls gap junction protein expression and function in postnatal hippocampal neural progenitor cells

Imbeault, Sophie; Gauvin, Lianne; Toeg, Hadi; Pettit, Alexandra; Sorbara, Catherine D.; Migahed, Lamiaa; Desroches, R; Menzies, A. Sheila; Nishii, Kanae; Paul, David L.; Simon, Alexander M.; Bennett, Steffany A. L.

doi:10.1186/1471-2202-10-13

Cited by 53 publications

(42 citation statements)

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“…Western analysis was performed as described (10). All procedures were carried out in agreement with the guidelines of the Canadian Council for Animal Care and the University of Ottawa Animal Care Committee.…”

Section: Methodsmentioning

confidence: 99%

“…Cell Culture-Primary NPC cultures were isolated from postnatal day 3 (P3) C57BL/6 mouse hippocampus and expanded as neurospheres for 14 days in vitro (DIV) as described (10). Hippocampal neurons were cultured as previously described (31) for 7 DIV.…”

Section: Methodsmentioning

confidence: 99%

“…Primary antibodies used for Western blots were polyclonal anti-Panx2 (1:800; Aviva Systems Biology, San Diego, CA) previously characterized (26) Confocal Immunofluorescence Microscopy-Neurosphere, P7 and P90 mouse brain cryopreservation, serial 10-m cryosectioning, and immunofluorescence were performed as described (10,11). Antibodies were diluted in 10 mM PBS supplemented with 0.3% Triton X-100 and 3% bovine serum albumin.…”

Section: Methodsmentioning

confidence: 99%

“…One mechanism, the expression of ion-permeable single membrane (ion channels and gap junction hemichannels) as well as double-membrane (gap junction intercellular) channels, is implicated in the control of embryonic and postnatal NPC migration, proliferation, and specification (5)(6)(7)(8)(9)(10)(11). Channel proteins, in part, regulate metabolic coupling, adhesion, and calcium wave propagation between NPCs and adjacent terminally differentiated cells (5)(6)(7)(8)(9)(10)(11). Pannexins are a family of membrane channel proteins discovered through their homology to the invertebrate family of gap junction proteins, the innexins.…”

mentioning

confidence: 99%

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Pannexin 2 Is Expressed by Postnatal Hippocampal Neural Progenitors and Modulates Neuronal Commitment

Swayne

Sorbara²,

Bennett

2010

Journal of Biological Chemistry

113

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The pannexins (Panx1, -2, and -3) are a mammalian family of putative single membrane channels discovered through homology to invertebrate gap junction-forming proteins, the innexins. Because connexin gap junction proteins are known regulators of neural stem and progenitor cell proliferation, migration, and specification, we asked whether pannexins, specifically Panx2, play a similar role in the postnatal hippocampus. We show that Panx2 protein is differentially expressed by multipotential progenitor cells and mature neurons. Both in vivo and in vitro, Type I and IIa stem-like neural progenitor cells express an S-palmitoylated Panx2 species localizing to Golgi and endoplasmic reticulum membranes. Protein expression is down-regulated during neurogenesis in neuronally committed Type IIb and III progenitor cells and immature neurons. Panx2 is re-expressed by neurons following maturation. Protein expressed by mature neurons is not palmitoylated and localizes to the plasma membrane. To assess the impact of Panx2 on neuronal differentiation, we used short hairpin RNA to suppress Panx2 expression in Neuro2a cells. Knockdown significantly accelerated the rate of neuronal differentiation. Neuritic extension and the expression of antigenic markers of mature neurons occurred earlier in stable lines expressing Panx2 short hairpin RNA than in controls. Together, these findings describe an endogenous post-translational regulation of Panx2, specific to early neural progenitor cells, and demonstrate that this expression plays a role in modulating the timing of their commitment to a neuronal lineage. Fig. 4B). The physiological production (and deletion) of these new neurons is implicated in the consolidation of spatial learning and memory (reviewed in Ref. Neural stem and progenitor cells (NPCs2), whereas aberrant or impaired neurogenesis is associated with multiple neurological and cognitive disorders, including epilepsy, mood disorders, neurodegenerative diseases, and ischemia (reviewed in Refs. 3 and 4).The signaling systems that maintain multipotential NPC populations in their "stem-like" state within the adult hippocampal network have only begun to be elucidated (2). One mechanism, the expression of ion-permeable single membrane (ion channels and gap junction hemichannels) as well as double-membrane (gap junction intercellular) channels, is implicated in the control of embryonic and postnatal NPC migration, proliferation, and specification (5-11). Channel proteins, in part, regulate metabolic coupling, adhesion, and calcium wave propagation between NPCs and adjacent terminally differentiated cells (5-11). Pannexins are a family of membrane channel proteins discovered through their homology to the invertebrate family of gap junction proteins, the innexins. Panx1 is expressed in multiple tissues. Panx2 is enriched in the central nervous system. Panx3 is found in skin and cartilage (12)(13)(14). Given their sequence homology with innexins and their structural homology with connexins, pannexins were originally proposed to form ...

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Pannexin 2 Is Expressed by Postnatal Hippocampal Neural Progenitors and Modulates Neuronal Commitment

Swayne

Sorbara²,

Bennett

2010

Journal of Biological Chemistry

113

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“…Despite all the advantages of this methodology, there are nevertheless a certain number of limitations, such as: i) the size of the cells studied, which should be between 7 and 40 µm; ii) the experimental conditions, such as temperature (all the experiments are carried out at 25¼C) or media, are quite restrictive with a potential impact of their viscosity on cell mobility. Indeed, the cell mobility is directly related to the viscosity of their environment and must be between 1 and 1.5 cP; iii) the absence of any extracellular matrix may have an impact on the Gap junction formed (Imbeault et al, 2009). …”

Section: Inhibition Of Gap Junctional Intercellular Communication In mentioning

confidence: 99%

Analysis of gap junctional intercellular communications using a dielectrophoresis-based microchip

Gabriel

Charrier

Royer

et al. 2017

European Journal of Cell Biology

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International audiencePlease cite this article in press as: Tellez-Gabriel, M., et al., Analysis of gap junctional intercellular communications using a dielectrophoresis-based microchip. Gap junctions are transmembrane structures that directly connect the cytoplasm of adjacent cells, making intercellular communications possible. It has been shown that the behaviour of several tumours – such as bone tumours – is related to gap junction intercellular communications (GJIC). Several methodologies are available for studying GJIC, based on measuring different parameters that are useful for multiple applications, such as the study of carcinogenesis for example. These methods nevertheless have several limitations. The present manuscript describes the setting up of a dielectrophoresis (DEP)-based lab-on-a-chip platform for the real-time study of Gap Junctional Intercellular Communication between osteosarcoma cells and the main cells accessible to their microenvironment. We conclude that using the DEParray technology for the GJIC assessment has several advantages comparing to current techniques. This methodology is less harmful for cells integrity; cells can be recovered after interaction to make further molecular analysis; it is possible to study GJIC in real time; we can promote cell interactions using up to five different populations. The setting up of this new methodology overcomes several difficulties to perform experiments for solving questions about GJIC process that we are not able to do with current technics

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The extracellular matrix compartment of neural stem and glial progenitor cells

Faissner

Reinhard

2015

Glia

103

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Neuroepithelial and radial GLIA stem cells generate the majority of the cellular constituents of the central nervous system. Following precisely timed phases of neurogenesis and gliogenesis the stem cells recede, with the exception of adult neural stem cells that persist in two generally accepted canonical neurogenic regions, the subventricular zone of the lateral ventricle and the subgranular zone in the dentate gyrus of the hippocampus. It is believed that adult stem cells reside in privileged stem cell niche environments that provide favorable conditions for self-renewal and maintenance of this cellular compartment. Factors such as morphogens, cytokines, and growth factors influence the developmental pathway of neural stem/progenitor cells. By comparison, less is known about the regulatory roles of glycoproteins and proteoglycans of the extracellular matrix (ECM) and their receptors, although they represent important constituents of the micromolecular environment of the niche. Here, we summarize studies that indicate pivotal roles of the ECM micromilieu for the biology and instrumental use of glial stem and progenitor cells of the CNS. Advancing our understanding of structure-function relationships, signaling motifs and complementary receptors and their signal transduction pathways will be of central importance for the application of these cell types in regenerative medicine.

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The extracellular matrix controls gap junction protein expression and function in postnatal hippocampal neural progenitor cells

Cited by 53 publications

References 54 publications

Pannexin 2 Is Expressed by Postnatal Hippocampal Neural Progenitors and Modulates Neuronal Commitment

Pannexin 2 Is Expressed by Postnatal Hippocampal Neural Progenitors and Modulates Neuronal Commitment

Analysis of gap junctional intercellular communications using a dielectrophoresis-based microchip

The extracellular matrix compartment of neural stem and glial progenitor cells

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