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Characterization of the Ventricular-Subventricular Stem Cell Niche During Human Brain Development Amanda M

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Characterization of the Ventricular-Subventricular Stem Cell Niche During Human Brain Development Amanda M © 2018. Published by The Company of Biologists Ltd | Development (2018) 145, dev170100. doi:10.1242/dev.170100 HUMAN DEVELOPMENT RESEARCH ARTICLE Characterization of the ventricular-subventricular stem cell niche during human brain development Amanda M. Coletti1, Deepinder Singh1, Saurabh Kumar1, Tasnuva Nuhat Shafin1, Patrick J. Briody1, Benjamin F. Babbitt1, Derek Pan1, Emily S. Norton1, Eliot C. Brown1, Kristopher T. Kahle2, Marc R. Del Bigio3 and Joanne C. Conover1,* ABSTRACT (Bruni, 1998; Del Bigio, 1995, 2010; Roales-Buján et al., 2012). In Human brain development proceeds via a sequentially transforming mouse, formation of the epithelial ependymal cells displaces stem cell population in the ventricular-subventricular zone (V-SVZ). An remaining radial glia/stem cell somata to the subventricular zone essential, but understudied, contributor to V-SVZ stem cell niche health (SVZ). These remaining stem cells, referred to as ventricular- is the multi-ciliated ependymal epithelium, which replaces stem cells at subventricular zone (V-SVZ) stem cells, are arrayed in clusters and the ventricular surface during development. However, reorganization maintain only a thin apical process at the ventricle surface (Alvarez- of the V-SVZ stem cell niche and its relationship to ependymogenesis Buylla et al., 1998, 2001; Conover et al., 2000; Doetsch et al., 1999; has not been characterized in the human brain. Based on Kriegstein and Alvarez-Buylla, 2009; Merkle et al., 2004). Stem comprehensive comparative spatiotemporal analyses of cell apical processes surrounded by ependymal cells are referred to ‘ ’ cytoarchitectural changes along the mouse and human ventricle as pinwheels (Mirzadeh et al., 2008) and represent regenerative surface, we uncovered a distinctive stem cell retention pattern in units. Whether human V-SVZ stem cells are organized and humans as ependymal cells populate the surface of the ventricle in an maintained in similar units along the ventricle surface has not occipital-to-frontal wave. During perinatal development, ventricle- been reported. contacting stem cells are reduced. By 7 months few stem cells are After birth in humans, proliferative cells and neurogenesis have detected, paralleling the decline in neurogenesis. In adolescence and been observed along the lateral wall of the lateral ventricle, in the adulthood, stem cells and neurogenesis are not observed along the site of what was formerly the lateral ganglionic eminence. Perinatal lateral wall. Volume, surface area and curvature of the lateral ventricles V-SVZ stem cells appear to be restricted in their neurogenic all significantly change during fetal development but stabilize after 1 potential and migration routes, which include three specific year, corresponding with the wave of ependymogenesis and stem cell pathways within the anterior forebrain: (1) to the frontal lobe in reduction. These findings reveal normal human V-SVZ development, which they distribute as interneurons within the cortical layers (arc highlighting the consequences of disease pathologies such as pathway); (2) along the medial migratory stream (MMS) to the congenital hydrocephalus. medial prefrontal cortex; (3) along the rostral migratory stream (RMS) to the olfactory bulb (Paredes et al., 2016a; Quiñones- KEY WORDS: Stem cell niche, Human brain development, Hinojosa et al., 2006; Sanai et al., 2011, 2004). Neurogenesis and Ependymogenesis, Ventricular-subventricular zone frontal lobe migration is robust for the first several months after birth and then declines dramatically, so that by two years of age there is INTRODUCTION little, or no, observable neurogenesis or migration (Bergmann et al., During early brain development in humans, the lining of the 2012; Paredes et al., 2016b; Quiñones-Hinojosa et al., 2006; Sanai neural tube and subsequently the cerebrospinal fluid (CSF)-filled et al., 2011; Wang et al., 2011, 2014). Postnatal neurogenesis in the ventricular system house a pseudostratified layer of proliferative human forebrain deviates significantly from what is found in mice cells that, in the forebrain, contributes to the robust expansion of and even non-human primates (Kriegstein et al., 2006; LaMonica the cerebral cortex. New neurons are initially generated by et al., 2012; Lui et al., 2011). Many mammals continue to generate neuroepithelial cells, and then by descendant radial glia and outer new neurons via the V-SVZ stem cell niche throughout their radial glia via their progeny, intermediate progenitor cells (Hansen lifetime, with the newly generated neurons migrating exclusively to et al., 2010; LaMonica et al., 2012; Lui et al., 2011; Malik et al., the olfactory bulb via the RMS to function in olfaction (Alunni and 2013). Radial glia also generate a monolayer of ependymal cells that Bally-Cuif, 2016; Conover and Shook, 2011; Lledo et al., 2008; lines the ventricles (Jacquet et al., 2009; Mirzadeh et al., 2008; Peretto et al., 1999). Although the exact function of postnatal Spassky et al., 2005) and provides barrier and transport functions inhibitory neurons in the human frontal cortex is unclear, it has been between the interstitial fluid of the brain parenchyma and the CSF proposed that they contribute to neurocognitive maturation and plasticity that is required in infancy (Arshad et al., 2016; Paredes et al., 2016a; Sanai et al., 2011). Disease or injury that disrupts 1Department of Physiology and Neurobiology, University of Connecticut, Storrs, CT proliferation and differentiation of V-SVZ stem cells and migration 06269, USA. 2Department of Neurosurgery, Pediatrics, and Cellular & Molecular of their progeny may contribute to sensorimotor and neurocognitive Physiology, Yale School of Medicine, New Haven, CT 06510, USA. 3Department of Pathology, University of Manitoba, Winnipeg, R3E 3P5, Canada. deficits that are frequently seen in cerebral palsy, autism and fetal- onset hydrocephalus (Arshad et al., 2016; Paredes et al., 2016a; *Author for correspondence ( [email protected]) Sanai et al., 2011). S.K., 0000-0001-8655-9187; J.C.C., 0000-0003-0375-0141 Although the lateral ventricle neuroepithelium drives neurogenesis, overall brain development subsequently influences Received 17 July 2018; Accepted 15 September 2018 the contour of the ventricular system and therefore the V-SVZ stem DEVELOPMENT 1 HUMAN DEVELOPMENT Development (2018) 145, dev170100. doi:10.1242/dev.170100 cell niche. As the ventricles are filled with fluid and lined by a the medial and lateral walls of the lateral ventricle were examined pseudostratified neuroepithelium in early fetal/embryonic using immunohistochemistry to distinguish radial glia [γ-tubulin+ development, the shape of the ventricle may initially be basal body of single cilium, GLAST+ (also known as SLC1A3), compliant. However, late in the second trimester in humans and FOXJ1−], radial glia that are transitioning to immature ependymal around embryonic day (E)13-14 in mouse, V-SVZ stem cells (radial cells (two to five γ-tubulin+ basal bodies of cilia, FOXJ1+), mature glia) generate a monolayer of ependymal cells that line the ventricle ependymal cells (multi-cilia γ-tubulin+ clusters, FOXJ1+) and surface in an occipital-to-frontal gradient (Bruni, 1998; Bruni et al., neural stem cells (single cilium γ-tubulin+ basal body, GFAP+) (see 1985; Del Bigio, 1995; Jacquet et al., 2009; Kyrousi et al., 2015; Fig. S1A) (Jacquet et al., 2009; Mirzadeh et al., 2010b, 2008). Mirzadeh et al., 2008; Paez-Gonzalez et al., 2011; Spassky et al., In Fig. 1, renderings of representative microscope images along 2005). Ependymal cells are multi-ciliated and tightly adherent. They the lateral wall detail cell organization at the ventricle surface provide several crucial functions (Johanson et al., 2011; Mirzadeh (Fig. 1, second column, Fig. S1B). Cell type ratios (Fig. 1, third et al., 2008; Paez-Gonzalez et al., 2011; Spassky et al., 2005). column), the average percentages of each cell type at three locations Motile cilia at their apical surface contribute to laminar flow at the along the lateral wall for each developmental time point, were ventricle surface, and ependymal cells facilitate both barrier and determined based on counts of a 13,567.59 µm2 area for each rostral, transport functions between the interstitial fluid of the brain middle and caudal sample (n=3 animals). Before E13, radial glia parenchyma and the CSF of the ventricular system (Bruni, 1998; cover the surface of the entire ventricular system surface (data not Bruni et al., 1985; Del Bigio, 1995, 2010; Spassky et al., 2005). At shown) (Kriegstein and Alvarez-Buylla, 2009). At E13 and E16 the ventricle surface, ependymal cells are generally cuboidal in (Fig. 1A,B), immature ependymal cells, which make up ∼35% of shape and tightly linked by adherens and tight junction protein total cells at the surface of the ventricle, were found primarily in the complexes (Bruni, 1998; Bruni et al., 1985; Del Bigio, 1995; caudal-most aspects of the lateral ventricle lateral wall. Immature Mirzadeh et al., 2008; Spassky et al., 2005). Stem cells that retain a ependymal cells in the middle and rostral regions comprised only ventricle-contacting apical process also have apical adherens and ∼11% and ∼7%, respectively, of the total cell number. By P1 tight junctions with neighboring ependymal cells and other stem (Fig. 1C), mature ependymal cells, which are characterized by a cells (Jacquet et al., 2009; Mirzadeh et al., 2008; Paez-Gonzalez large tightly clustered array of multiple cilia, cover most of the
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