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

Abstract

The mammalian ventricular-subventricular zone (V-SVZ) presents the highest neurogenic potential in the brain of the adult individual. In rodents, it is mainly composed of chains of neuroblasts. In humans, it is organized in layers where neuroblasts do not form chains. The aim of this study is to describe the cytoarchitecture of canine V-SVZ (cV-SVZ), to assess its neurogenic potential, and to compare our results with those previously described in other species. We have studied by histology, immunohistochemistry (IHC), electron microscopy and neurosphere assay the morphology, cytoarchitecture and neurogenic potential of cV-SVZ. Age groups of animals were performed. Histological and ultrastructural studies indicated that the cV-SVZ is organized in layers as in humans, but including migratory chains as in rodents. Neural progenitors were organized in niches in the subependymal area and a decline in their number was observed with age. Adult-young dogs contained migratory cells capable to expand and differentiate in vitro according with previous results obtained in rodents, primates, humans, pigs, and dogs. Some adult animals presented perivascular niches outside the V-SVZ. Our observations evidence a great similarity between canine and human V-SVZ indicating that the dog may be better representative of neurogenic events in humans, compared with rodents. Accordingly with our results, we conclude that dogs are a valuable animal model of adult neurogenesis in comparative and preclinical studies.

Age‐related changes in Ki‐67 and DCX expression in the BALB/ c mouse (Mus Musculus) brain

“…Proliferating cells and immature neurons were observed at all ages in the sub ventricular zone of the lateral ventricles, rostral migratory stream, olfactory bulb and sub granular zone of the hippocampal dentate gyrus. Expression of both Ki-67 and DCX confirmed that these brain regions are indeed neurogenic sites and these findings extend earlier observations made by previous researchers in mammals (Kuhn et al, 1996;Enwere et al, 2004;Kondo et al, 2010;Nada et al, 2010;Encinas et al, 2011;Jinno, 2011;Kempermann, 2011;Mobley et al, 2014;Olaleye and Ihunwo, 2014;Olude et al, 2014;Fernández-Flores et al, 2018).…”

“…Our results further revealed that there was no period during the first 12 postnatal weeks where neurogenesis was stable over extended periods defining life‐history stages corresponding to juvenile, sub adult and adult. Age‐related decreases in neurogenesis in the SVZ and RMS have been reported previously in laboratory mice (Enwere et al, 2004; Luo et al, 2006; Shook et al, 2012; Mobley et al, 2014), laboratory rats (Chen et al, 2003), the giant African rat (Olude et al, 2014) and more recently dogs (Fernández‐Flores et al, 2018). These age‐related decreases in neurogenesis in the SVZ and RMS have also been proposed to be functionally linked to the olfactory dysfunction that is observed during aging (Enwere et al, 2004).…”

“…The process through which new neurons are added to the brain after birth is termed postnatal or secondary neurogenesis (Thuret et al, 2015). To date, postnatal neurogenesis has been reported in the brains of several laboratory bred and wild living mammalian species including laboratory mice (Kondo et al, 2010; Nada et al, 2010; Encinas et al, 2011; Mobley et al, 2014), four striped mice (Olaleye and Ihunwo, 2014), rats (Kuhn et al, 1996; Jessberger et al, 2009), voles (Amrein et al, 2004), African giant rats (Olude et al, 2014), mole rats (Amrein et al, 2014), bats (Chawana et al, 2013), dogs (Fernández‐Flores et al, 2018) and humans (Eriksson et al, 1998).…”

Adult neurogenesis and gliogenesis in the dorsal and ventral canine hippocampus

“…The canine brain presents many similarities with the human brain in anatomical organization, architectural complexity, gene expression (Griffiths, Duncan, Mcculloch, & Harvey, 1981;Hemsley & Hopwood, 2010;Wenger et al, 1999), physiology (Jung et al, 2010), and agerelated alterations (Cummings et al, 1996;Yu et al, 2011). Recent histological, immunohistochemical, and ultrastructural evidence suggests that the canine brain highly represents the adult human neurogenic events (Fernandez-Flores et al, 2018;Walton, Parmentier, & Wolfe, 2013). The fetal development, cytoarchitecture and neurogenic potential of the canine adult neurogenic niches were shown to share many features in common with humans (Fernandez-Flores et al, 2018;Orechio et al, 2018) establishing canines as excellent animal models for the study of adult hippocampal neurogenesis.…”

“…Recent histological, immunohistochemical, and ultrastructural evidence suggests that the canine brain highly represents the adult human neurogenic events (Fernandez-Flores et al, 2018;Walton, Parmentier, & Wolfe, 2013). The fetal development, cytoarchitecture and neurogenic potential of the canine adult neurogenic niches were shown to share many features in common with humans (Fernandez-Flores et al, 2018;Orechio et al, 2018) establishing canines as excellent animal models for the study of adult hippocampal neurogenesis.…”