Characterization of the canine rostral ventricular‐subventricular zone: Morphological, immunohistochemical, ultrastructural, and neurosphere assay studies

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The ventricular‐subventricular zone (V‐SVZ) in the adult brain contains the largest capacity for constitutive regeneration of new neural cells in mammals (Alvarez‐Buylla & Garcia‐Verdugo, 2002; Doetsch, Caille, Lim, García‐Verdugo, & Alvarez‐Buylla, 1999; Sohn et al., 2015). It represents one of the main neurogenic areas of the adult brain together with the subgranular zone of the hippocampus (Alvarez‐Buylla & Garcia‐Verdugo, 2002; Gould, 2007). Adult neurogenesis has been extensively described as an active process that includes processes related with proliferation, maintenance, differentiation, and migration of newformed neural cells to their final destination (Ming & Song, 2005). Neurogenic areas derive from reminiscent embryonic neuroepithelial cells during brain development, allowing continuous turnover of mature neural cells in the adult brain (Conover & Allen, 2002; Doetsch & Alvarez‐Buylla, 1996; Galli, Gritti, Bonfanti, & Vescovi, 2003) from specific reservoirs of neural stem cells (NSCs) (Bernier, Bedard, Vinet, Levesque, & Parent, 2002; Steindler & Pincus, 2002). The maintenance of the stem properties of NSCs has been related with a specific environment provided by structural interactions between both glial and extracellular matrix (ECM) components as well as release of local diffusible factors (Moore et al., 2006; Tavazoie et al., 2008). These areas have been described as neurogenic niches where the stem status is maintained or differentiation in adult neural cells continues. In the V‐SVZ, these cells appear to maintain a low proliferation index during the lifetime of the adult individual in order to generate new neural cells mainly destined to migrate through the rostral migratory stream (RMS) to the olfactory bulb (Cayre, Canoll, & Goldman, 2009; Doetsch & Alvarez‐Buylla, 1996).
The components of these niches have been widely studied by ultrastructure in rodents (Bernier, Vinet, Cossette, & Parent, 2000; Rezza, Sennett, & Rendl, 2014; Weickert et al., 2000). The organization of the V‐SVZ niche is based on four major cell types: ependymal cells (E1 and E2 cells), V‐SVZ astrocytes (B1 and B2 cells), transient amplifying progenitor cells (type C cells), and neuroblasts (type A cells) (Doetsch, Garcı'a‐Verdugo, & Alvarez‐Buylla, 1997; Mirzadeh, Merkle, Soriano‐Navarro, Garcia‐Verdugo, & Alvarez‐Buylla, 2008). B1 are reminiscent embryonic neuroepithelial cells with astrocytic appearance and in contact with the ventricular lumen through the intercellular space between the ependymocytes. These cells proliferate at a slow rate and are considered to be adult resident NSCs. Type B2 cells form a subependymal band and support the migratory neuroblasts that move toward the olfactory bulb. Type C cells are rapidly proliferating transient amplifying cells that arise from B1 cells and produce neuroblasts or type A cells.
In domestic animals, cellular components of the V‐SVZ have been described in oxen (Rodriguez‐Perez, Perez‐Martin, Jimenez, & Fernandez‐Llebrez, 2003), sheep (Low, Faull, Bennet, Gunn, & Curtis, 2013), pigs (Costine et al., 2015), and rabbits (Bonfanti, Aimar, & Ponti, 2006; Bonfanti & Ponti, 2008; Luzzati et al., 2003). Cellular composition and cytoarchitecture of the V‐SVZ have also been studied in humans (Nogueira et al., 2014; Quiñones‐Hinojosa et al., 2006; Sanai, Tramontin, Quinones‐Hinojosa, & Barbaro, 2004) and nonhuman primates (Gil‐Perotin, Duran‐Moreno, Belzunegui, Luquin, & Verdugo, 2009; Sawamoto et al., 2011). Important differences between mammalian species have been described. Thus, in the adult human brain the V‐SVZ is composed of an ependymal cell monolayer, a hypocellular gap and a ribbon of astrocytic cells layers (Quiñones‐Hinojosa et al., 2006; Sanai et al., 2004). Moreover a small amount of proliferating neuroblasts have been identified both in fetal and adult individuals (Wang et al., 2011).
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