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Stem Cells and Their Niche in the Adult Olfactory Mucosa

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Stem Cells and Their Niche in the Adult Olfactory Mucosa Archives Italiennes de Biologie, 148: 47-58, 2010. Stem cells and their niche in the adult olfactory mucosa A. MACKAY-SIM National Centre for Adult Stem Cell Research, Eskitis Institute for Cell and Molecular Therapies, Griffith University, Brisbane, Australia A bstract It is well known that new neurons are produced in the adult brain, in the hippocampus and in the subventricular zone. The neural progenitors formed in the subventricular zone migrate forward and join in neural circuits as inter- neurons in the olfactory bulb, the target for axons from the olfactory sensory neurons in the nose. These neurons are also continually replaced during adulthood from a stem cell in a neurogenic niche in the olfactory epithelium. The stem cell responsible can regenerate all the cells of the olfactory epithelium if damaged by trauma or toxins. This stem cell, the horizontal basal cell, is in a niche defined by the extra cellular matrix of the basement membrane as well as the many growth factors expressed by surrounding cells and hormones from nearby vasculature. A mul- tipotent cell has been isolated from the olfactory mucosa that can give rise to cells of endodermal and mesodermal origin as well as the expected neural lineage. Whether this is an additional stem cell or the horizontal basal cell is still an open question. Key words Neurogenesis • Adult stem cell • Neural stem cell • Subventricular zone • Olfactory epithelium • Human Introduction large surface area of sensory cilia projecting from the dendrite of the sensory neurons (Fig. 2). The In humans, as in other mammals, there is a continu- human olfactory mucosa is similar in structure to ing neurogenesis in the subventricular zone generat- other vertebrates with the same cell types in a pseu- ing neurons that migrate and become interneurons in dostratified olfactory epithelium (Moran et al., 1982; the olfactory bulb (Curtis et al., 2009). The olfactory Nakashima et al., 1984; Morrison and Costanzo, bulb is that part of the brain which receives axonal 1990; Nakashima et al., 1991). In human adult, com- input from the sensory neurons in the olfactory pared to fetus, there is a loss of olfactory epithelium epithelium in the nose. The olfactory epithelium is from the superior posterior regions of the nasal cavity the most superficial layer of the olfactory mucosa and its replacement with respiratory and squamous which also comprises a lamina propria contain- epithelium (Nakashima et al., 1984). The “olfac- ing the specialized olfactory glands (“Bowman’s tory region” in the adult has a non-contiguous and glands”) and the olfactory sensory axons surrounded patchy distribution of olfactory epithelium (Moran by their specialized glia, the olfactory ensheathing et al., 1982; Nakashima et al., 1984; Morrison and cells (Fig. 1). In mammals, the olfactory mucosa is Costanzo, 1990; Paik et al., 1992). On the other typically located dorsally and posteriorly in the nasal hand, the distribution of olfactory epithelium in adult cavity covering the nasal septum medially, and later- human extends more anteriorly and inferiorly than in ally, covering the turbinate bones, to provide a very the fetus (Feron et al., 1998; Leopold et al., 2000). Corresponding Author: Professor Alan Mackay-Sim, National Centre for Adult Stem Cell Research, Eskitis Institute for Cell and Molecular Therapies, Griffith University, Brisbane, QLD 4111, Australia - Email: [email protected] 48 A. Mackay-SIM Fig. 1. - Olfactory epithelium. The olfactory mucosa is divided into epithelium and lamina propria, separated by the basement membrane. The sensory neurons in the epithelium send a dendrite to the apical surface where their cilia extend into the mucus lining the lumen of the nasal cavity. The sensory axons leave the epithelium and enter the lamina propria where they gather in bundles surrounded by olfactory ensheathing cells. The Bowman’s glands are specialised glands of the olfactory mucosa located in the lamina propria with their ducts open into the lumen. Most of the luminal surface is made up by supporting cells, covered in microvilli, whose end-feet extend to the basement membrane. The horizontal basal cell, the neural stem cell, sits adjacent to the basement membrane. The globose basal cell, a multipotent precursor, migrates away from the basement membrane and gives rise to the sensory neuron. Until now, analysis of human olfactory mucosa has key after toxic damage (Schultz, 1941). Numerous been restricted to sampling of biopsy and autopsy reports confirmed these observations in frog (Smith, material and no systematic and complete distribu- 1951), fish (Westerman and Baumgarten, 1964), tion study of human olfactory mucosa has been cat and dog (Andres, 1966), lamprey (Thornhill, done. The axons of the olfactory sensory neurons 1970), mouse (Moulton et al., 1970; Thornhill, 1970; leave the olfactory epithelium and form bundles and Graziadei and Metcalf, 1971; Smart, 1971), monkey fascicles in the lamina propria before entering the (Graziadei et al., 1980) and human (Wolozin et al., olfactory bulb where they synapse with mitral/tufted 1992; Murrell et al., 1996). The vulnerability of the cells and interneurons, some of which are generated olfactory sensory neurons to environmental factors by neurogenesis in the subventricular zone (Breton- makes neurogenesis in the olfactory epithelium Provencher et al., 2009; Curtis et al., 2009). necessary in order to maintain the sense of smell, Seventy years ago mitotic activity was first observed essential for most aspects of daily life in most ver- in the basal cells of the olfactory epithelium of adult tebrates including food seeking, pathfinding, social mice (Nagahara, 1940) and soon after, regeneration interactions and sexual behaviour. It is worth con- of olfactory sensory neurons was observed in mon- sidering that a primary drive for neurogenesis in the STEM CELL NICHE IN NOSE 49 Fig. 2. - Anatomy of the human olfactory system. In the adult nose, the olfactory mucosa is patchily distributed in the superior-posterior region of the nasal cavity interspersed with respiratory mucosa. The olfactory sensory axons gather in bundles and penetrate the skull at the cribriform plate to synapse in the olfactory bulb lying on the skull base under the forebrain. adult forebrain, that replenishes interneurons in the death (Fig. 1). The dendrites of the olfactory sensory olfactory bulb, is the requirement to provide new neurons penetrate the epithelium and are decorated central circuits because of the continual neurogenesis with multiple cilia containing the sensory transduc- occurring in the periphery. For example, there is evi- tion proteins. These cilia extend into the overlay- dence that olfactory bulb interneurons are lost after ing mucus and may be only a few microns below chemical destruction of the sensory neurons and up- the surface (Menco, 1980). Inhaled toxic gases regulated when sensory innervation returns (Nadi et can destroy the olfactory epithelium and the neu- al., 1981; Baker et al., 1993). The olfactory mucosa rons within it. Inhalation of N-methyl-formimino- is accessible in living adult humans (Feron et al., methylester and methyl bromide lead to reversible 1999b) and so presents an accessible source of tissue loss of the sensory neurons with temporary loss of for understanding the biology of adult neurogenesis smell (Rehn et al., 1981; Schmidt et al., 1984; Hurtt in health and disease (Mackay-Sim and Silburn, et al., 1988). Even nasal lavage with wheat germ 2008). It is also a source of cells for transplantation agglutinin-horse radish peroxidase, induces loss of repair of the nervous system (Feron et al., 2005; sensory neurons from the epithelium and stimulates Mackay-Sim et al., 2008). Understanding the biology basal cell proliferation (Moon and Baker, 1998), of olfactory neural stem cells and their niche will be indicating the potential for large molecules to affect very important for optimizing clinical applications. sensory neuron survival. Olfactory neurons provide a route for viruses and bacteria to enter the brain (Owen et al., 2009) and for this reason they may be The requirement for stem cells vulnerable to apoptosis as a protective mechanism, in olfactory mucosa part of an innate response to infection (Harris et al., 2009). Environmental susceptibility is also sug- A major difference between olfactory sensory neu- gested by evidence that olfactory neurogenesis is rons and other neurons is their proximity to the vulnerable to usage. For example, if over-usage is external environment which increases their risk of induced by closure of one naris in adult mice, the 50 A. Mackay-SIM open side epithelium is reduced in thickness and proliferation of neuronal precursors, the thickness of sensory neurons are lost, with a lack of ability to the olfactory epithelium remains static in the adult maintain regeneration (Maruniak et al., 1989). The rat from 60-330 days of age (Hinds and McNelly, mechanism for this loss is unknown but it may be 1981; Weiler and Farbman, 1997). Without an due to overuse, to toxins or to infections, as indi- increase in epithelial thickness it follows that cell cated by the large number of polymorphonuclear proliferation is balanced by apoptotic cell death. leukocytes on the open side after 7 and 8 months Apoptosis occurs at all stages of olfactory neuron of closure (Maruniak et al., 1990). With increas- development from recently born basal cells through ing age, the proliferative and neurogenic capacity to immature and mature neurons (Carr and Farbman, of the olfactory epithelium declines, especially in 1993; Holcomb et al., 1995; Magrassi and Graziadei, the antero-dorsal region in the rat (Loo et al., 1996; 1995; Mahalik, 1996). Weiler and Farbman, 1997). This may reflect usage, Some of the growth factor signals that regulate stem rather than age, per se, because neurogenesis in the and progenitor proliferation have been identified. posterior nasal cavity is better preserved (Loo et al., Horizontal basal cell proliferation is stimulated by 1996; Weiler and Farbman, 1997).
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