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Frontiers in Biology

Front. Biol.    2016, Vol. 11 Issue (4) : 261-284     DOI: 10.1007/s11515-016-1407-1
REVIEW |
Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone
Gabrielle Rushing1,Rebecca A. Ihrie2,*()
1. Program in Neuroscience, Vanderbilt University, Nashville, TN 37232, USA
2. Departments of Cancer Biology and Neurological Surgery, Vanderbilt University, Nashville, TN 37232, USA
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Abstract

BACKGROUND: The origin and classification of neural stem cells (NSCs) has been a subject of intense investigation for the past two decades. Efforts to categorize NSCs based on their location, function and expression have established that these cells are a heterogeneous pool in both the embryonic and adult brain. The discovery and additional characterization of adult NSCs has introduced the possibility of using these cells as a source for neuronal and glial replacement following injury or disease. To understand how one could manipulate NSC developmental programs for therapeutic use, additional work is needed to elucidate how NSCs are programmed and how signals during development are interpreted to determine cell fate.

OBJECTIVE: This review describes the identification, classification and characterization of NSCs within the large neurogenic niche of the ventricular-subventricular zone (V-SVZ).

METHODS: A literature search was conducted using Pubmed including the keywords “ventricular-subventricular zone,” “neural stem cell,” “heterogeneity,” “identity” and/or “single cell” to find relevant manuscripts to include within the review. A special focus was placed on more recent findings using single-cell level analyses on neural stem cells within their niche(s).

RESULTS: This review discusses over 20 research articles detailing findings on V-SVZ NSC heterogeneity, over 25 articles describing fate determinants of NSCs, and focuses on 8 recent publications using distinct single-cell analyses of neural stem cells including flow cytometry and RNA-seq. Additionally, over 60 manuscripts highlighting the markers expressed on cells within the NSC lineage are included in a chart divided by cell type.

CONCLUSIONS: Investigation of NSC heterogeneity and fate decisions is ongoing. Thus far, much research has been conducted in mice however, findings in human and other mammalian species are also discussed here. Implications of NSC heterogeneity established in the embryo for the properties of NSCs in the adult brain are explored, including how these cells may be redirected after injury or genetic manipulation.

Keywords ventricular-subventricular zone      neural stem cells      positional identity      single-cell      heterogeneity     
Corresponding Authors: Rebecca A. Ihrie   
Just Accepted Date: 17 June 2016   Online First Date: 08 July 2016    Issue Date: 30 August 2016
 Cite this article:   
Gabrielle Rushing,Rebecca A. Ihrie. Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone[J]. Front. Biol., 2016, 11(4): 261-284.
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http://journal.hep.com.cn/fib/EN/10.1007/s11515-016-1407-1
http://journal.hep.com.cn/fib/EN/Y2016/V11/I4/261
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Gabrielle Rushing
Rebecca A. Ihrie
Marker Cell type labeled Source
Alpha 6 integrin Activated B1 cells C cells Ramalho-Santos et al., 2002; Kokovay et al., 2010
Brain lipid binding protein (BLBP) Radial glia Activated B1 cells Feng et al., 1994; Doetsch, 2003; Kriegstein and Gotz, 2003Giachino et al., 2014
CD44 Astrocyte-restricted precursor cells Liu et al., 2004
Dlx2 C cells A cells Doetsch et al., 2002
Doublecortin (DCX) A cells Doetsch et al., 1999a; Gleeson et al., 1999
E-NCAM Neuronal-restricted precursors Chuong and Edelman, 1984
Epidermal growth factor receptor (EGFR) Activated B1 cells C cells Doetsch et al., 2002; Pastrana et al., 2009; Codega et al., 2014
GD3 Oligodendrocyte precursor cells LeVine and Goldman, 1988a, 1988b
Glial fibrillary acidic protein (GFAP) Neuroepithelial cells Radial glia B1 cells Mature astrocytes Bignami et al., 1972
Glutamate aspartate transporter (GLAST) Radial glia Shibata et al., 1997; Hartfuss et al., 2001; Doetsch, 2003; Kriegstein and Gotz, 2003
Mature astrocytes Shibata et al., 1997; Ullensvang et al., 1997
Activated B1 cells C cells Pastrana et al., 2009
ITGA6/CD49f B1 cells C cells Ramalho-Santos et al., 2002; Shen et al., 2008; Kokovay et al., 2010
LeX (CD15) B1 cells Capela and Temple, 2002
MAG Mature oligodendrocytes Quarles and Trapp, 1984
MAP2 Mature neurons Garner et al., 1988
Mash1 (Ascl1) Activated B cells Pastrana et al., 2009
C cells Parras et al., 2004; Pastrana et al., 2009
mCD24 (aka heat-stable antigen, HSA) E cells Calaora et al., 1996
A cells (transiently) Rougon et al., 1991; Nedelec et al., 1992; Calaora et al., 1996
Myelin basic protein (MBP) Mature oligodendrocytes Poduslo and Braun, 1975; Golds and Braun, 1976; Omlin et al., 1982
Nestin Neuroepithelial cells Lendahl et al., 1990
Ependymal cells Lendahl et al., 1990; Doetsch et al., 1997
Radial glia Hockfield and McKay, 1985
Activated B1 cells Codega et al., 2014
Neuronal nuclear antigen (NeuN) Mature neurons Mullen et al., 1992
Neuron-specific enolase (NSE) Mature neurons Kirino et al., 1983
NG2 Oligodendrocyte precursor cells Stallcup and Beasley, 1987; Nishiyama et al., 1996; Ong and Levine, 1999
O4 Mature oligodendrocytes Sommer and Schachner, 1981
Pax6 Cortical radial glia Gotz et al., 1998; Englund et al., 2005
Polysialylated neural cell adhesion molecule (PSA-NCAM) A cells Doetsch et al., 1997
Prominin-1 (CD133) Ependymal cells Coskun et al., 2008
Primary cilia of B1 cells Uchida et al., 2000; Marzesco et al., 2005; Pinto et al., 2008; Beckervordersandforth et al., 2010
Platelet-derived growth factor receptor α (PDGFRα) Oligodendrocyte precursor cells Hart et al., 1989; Pringle et al., 1992; Hall et al., 1996
RC1 Neuroepithelial cells Radial glia Edwards et al., 1990
RC2 Neuroepithelial cells Radial glia Misson et al., 1988; Chanas-Sacre et al., 2000; Hartfuss et al., 2001
SOX2 (SRY-Box 2) Embryonic NSCs (radial glia) Zappone et al., 2000
B1 cells Ellis et al., 2004; Ferri et al., 2004
S100-β Mature astrocytes (Not all astrocytes express it) Wang and Bordey, 2008
Ependymal cells Didier et al., 1986
Tbr1 Intermediate progenitor cells Englund et al., 2005; Hevner, 2006; Hevner et al., 2006
Tbr2 Mature neurons (cortex) Englund et al., 2005; Hevner, 2006; Hevner et al., 2006
Tuj1 (βIII Tubulin) A cells Doetsch et al., 1997; Pastrana et al., 2009
VCAM-1 Quiescent B1 cells Kokovay et al., 2012; Codega et al., 2014
Vimentin Radial glia Schnitzer and Schachner, 1981; Zecevic, 2004
Ependymal cells
Tab.1  Marker expression on cell types within the V-SVZ and its precursor regions
Fig.1  Development of the mouse ventricular-subventricular zone. Representative coronal sections of mouse brain at indicated developmental times are shown at top. Colors in the coronal sections represent domains of transcription factor expression within the developing V-SVZ. At bottom, representative schematics of developing V-SVZ corresponding to red box within the coronal section above. Note that the size of coronal sections and corresponding representative images of cell types are not to scale. (A) Neuroepithelial cells (NECs; dark blue) fold in to form the neural tube. These cells contact both the pial and ventricular surfaces of the developing brain (below) and divide to form a densely packed VZ. (B) In developing telencephalon, NECs give rise to radial glia (RG; light blue), which retain properties of NECs (see text), including contact with the ventricular and pial surfaces. At this stage, the RG divide asymmetrically, producing a daughter RG and a daughter intermediate progenitor cell (IPC; green) located away from the ventricular surface in a subventricular zone (SVZ). Newborn neurons (red) use the RG processes as a scaffold for migration to their final destinations. (C) In the neonatal brain, the RG are retained until approximately postnatal day 7. After postnatal day 2, they begin to retract their basal (pial) processes and will give rise to ependymal (E) cells (grey; shown in (D)), B1 cells (teal; shown in (D)) and B2 cells (yellow; shown in (D)) in the mature brain. (D) In the adult brain, B1 cells are the NSCs. They have basal processes that wrap around blood vessels (dark red) and a single primary cilium that extends between the tightly connected E cells. The multiple motile cilia of E cells push CSF through the ventricles. Note the presence of transit-amplifying C cells (green), migrating neuroblasts (A cells, red) and parenchymal astrocytes (B2 cells, orange). This structure in the adult is termed the ventricular-subventricular zone (V-SVZ). Note that other cell types exist in the region that are not discussed within this review including microglia and local and distant innervating neurons.
Fig.2  Embryonic neural cell lineage and marker expression profiles. Neuroepithelial cells (NECs) are the earliest neural progenitors discussed here. These cells produce neurons but also give rise to radial glia cells (RG), which in turn act as the primary progenitors during cortical development. These cells can produce oligodendrocytes, astrocytes and neurons. While precursors for oligodendrocytes and neurons have been characterized, it is still debated whether an astrocyte-restricted precursor cell exists. RG cells also produce pre-B1 cells between E13.5-15.5 that remain relatively quiescent until postnatal reactivation (see text).
Fig.3  Postnatal neural cell lineage and marker expression profiles. *Radial glia persist only during the first postnatal week and are non-self-renewing during this time. They retract their processes after postnatal day 2 in the mouse and give rise to parenchymal astrocytes (orange), ependymal cells (grey), oligodendrocytes (purple) and astrocyte-like adult neural stem cells (B1 cells, teal). B1 cells are self-renewing and also give rise to transit amplifying progenitors (green), which in turn produce neuroblasts (red) that will mature into neurons (yellow). **These markers are primarily expressed by activated B1 cells. ***CD133 is present on the primary cilia of B1 cells, as well as ependymal cells. ****VCAM-1 is expressed on quiescent B1 cells. # Note that Nestin is not expressed on all RG and B1 cells but rather, is dynamically regulated (see text).
Persisting Questions
• Is regional transcription factor expression controlled in the same manner throughout development and in the postnatal brain?
• Which transcription factors are permissive for multiple fates vs. instructive for a specific one?
• How is regional identity maintained postnatally?
• Is there a signaling or transcriptional threshold to induce plasticity of NSCs?
• Is there a ‘gradient of identity” or sharp cutoffs within the V-SVZ?
• How do signals within the developing V-SVZ affect specific TFs to determine the ultimate fate of an NSC?
• Can we mathematically model the input of signals experienced by NSCs that drive fate determination?
• Do SGZ NSCs have a positional identity?
• Does positional identity exist in the human brain?
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