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Neuronal Regeneration: Lessons from the Olfactory System Richard C seminars in CELL & DEVELOPMENTAL BIOLOGY, Vol 10, 1999: pp. 421]431 Article No. scdb.1999.0329, available online at http:rrwww.idealibrary.com on Neuronal regeneration: Lessons from the olfactory system Richard C. Murray and Anne L. Calof Neuronal regeneration takes place in the primary relay of the offering hope that, by learning how proliferation and olfactory system, the olfactory epithelium() OE ; however, its differentiation of progenitor cells is regulated, it may synaptic target in the central nervous system, the olfactory be possible to identify conditions that promote frank bulb() OB , undergoes continual neurogenesis but not true neuronal regeneration in the CNS. Such information regeneration. In this review, cell interactions and growth would be of considerable medical, as well as scienti- factors regulating neurogenesis in both OE and OB are ®c, signi®cance. discussed. In addition, regulation of regeneration in the OE Interestingly, true neuronal regeneration is known and regulation of neurogenesis in the OB are compared, to occur in adult mammals in the primary relay of with the goal of identifying characteristics that may account odor detection, the olfactory epitheliumŽ. OE . The for the different abilities of these two tissues to regenerate. OE contains undifferentiated progenitor cells that generate new neurons throughout life.3,4 While the Key words: growth factors r neurogenesis r neuronal cell bodies of these neurons, the olfactory receptor progenitor cells r olfactory epithelium r olfactory bulb neuronsŽ. ORNs , remain in the periphery, they send Q1999 Academic Press axons to the OB and their interactions with the bulb are important in regulating OE structure and func- tion. Because of its peripheral location, the OE is readily accessible for study, both in tissue culture and in living animals, and much is known about the cell Introduction interactions and molecular factors that regulate neu- rogenesis and neuron replacement in this tissueŽ re- MANY TISSUES IN adult mammals are able to regener- viewed in refs 5,6. Several principles have emerged ate their characteristic differentiated cell types from such studies, especially with regard to the na- throughout life, but this does not take place in most ture of the signals that initiate neurogenesis and Ž. of the central nervous system CNS . Indeed, the cause it to halt. In this review, we highlight some of inability of the CNS to generate new neurons in these principles and compare them with ideas emerg- order to replace those that have been lost is a ing from studies of neurogenesis in the OB. Our goal formidable obstacle to recovery from neuronal da- is to identify parallels in how these processes are mage caused by injury or neurodegenerative disease, regulated between the OE, a peripheral neural tissue, rendering such insults to the CNS devastating in their and the OB, which is in the CNS. impact. However, there are parts of the CNS where long-term production of neurons takes place. These are the hippocampus and olfactory bulbŽ. OB of the brain, which continue to add new neurons through- Structure of the primary olfactory pathway out life.1,2 This ongoing neurogenesis requires that neuronal progenitor cells exist in the adult brain, The primary olfactory pathway consists of the OE and its CNS target tissue, the OBŽ. Figure 1A .w In addition to this main olfactory system, many vertebrates pos- From the Department of Anatomy and Neurobiology and the sess a separate system for the detection of phero- Developmental Biology Center, 364 Med Surge II, University of mones called the vomeronasal systemŽ reviewed in ref California, Irvine, College of Medicine, Irvine, CA 92697-1275, . x USA. Address reprint requests to [email protected] 7 , which will not be discussed in this review. Odor Q1999 Academic Press detection initiates in the OE, a sensory epithelium 1084-9521r99r040421q11 $30.00r0 that lines the nasal cavity. The OE consists of three 421 R. C. Murray and A. L. Calof found in the middle, largest compartment of the epithelium; and the basal compartmentŽ approxi- mately two cell layers thick. , located adjacent to the basal lamina that separates the epithelium from the underlying lamina propria, contains a mixture of cell types often referred to collectively as basal cellsŽ Fig- ure 1B. ORNs can be further subdivided based on their position in the OE, markers they express, and their level of maturity. Mature ORNs are located more apically and express both the neural cell adhe- sion molecule, NCAM, and olfactory marker protein Ž.OMP , a cytoplasmic protein whose expression ap- pears to be limited to mature ORNs.8,9 Mature ORNs send a dendritic process to the apical surface of the epithelium, and this apical dendrite expands into a knob which projects a number of cilia into the overly- ing mucus. The axons of ORNs project into the lamina propria subjacent to the epithelium, through the cribriform plate of the ethmoid bone, and di- rectly into the CNS where synapse with second order neurons in the OB. Immature ORNs are located underneath mature ORNs in the epithelium, and express both NCAM and the growth associated pro- tein GAP-43, but not OMP.8,10 Immature ORNs have dendrites that do not reach the epithelial surface, Figure 1. A schematic drawing of the primary olfactory and they appear to require sustained contact with the pathway.Ž. A : Sagittal view of the caudal nasal cavity and OB in order to mature and survive.11 rostral forebrain of a mouse. The olfactory epitheliumŽ. OE Basal cells of the OE can be subdivided into two lines the nasal cavity and contains olfactory receptor neu- broad morphological subtypes. The horizontalŽ or ronsŽ. ORN , which project through the cribriform plate Ž. Ž. Ž . ¯at. basal cells lie adjacent to the basal lamina and CP to glomeruli G in the olfactory bulb OB within the 8 central nervous systemŽ. CNS . The subventricular zone express keratin intermediate ®laments; these cells Ž.SVZ of the lateral ventricle Ž. LV is the source of progeni- are not part of the neuronal lineage of the OE.12 The tor cells that migrate in the rostral migratory streamŽ. RMS so-called `globose' basal cellsŽ. GBCs lie above hori- to the olfactory bulbŽ OB .Ž. B : A section through the OE zontal basal cells and have been shown to be the illustrating the relative positions of cell types. From apical Ž. progenitor cells that divide and give rise to ORNs in to basal, these include supporting cells SUP , olfactory 12 ] 14 receptor neuronsŽ. ORN , and basal cells Ž. BC . The round vivo. There are at least three types of ORN or globose basal cells consist of at least 3 types of neuronal progenitor cells among the GBCs, which can be q progenitors: stem cellsŽ. black , MASH1 progenitorsŽ. gray , distinguished on the basis of molecular markers and and Immediate Neuronal PrecursorsŽ. white . The OE is proliferative dynamics: these include neuronal Ž. separated from the underlying laminal propria LP by its Ž basement membraneŽ.Ž. BM . C : A section through the OB colony-forming cells putative neuronal stem cells of illustrating the various layers. These include the olfactory the OE. ; MASH1-expressing progenitors; and the Im- nerve layerŽ. ONL , glomerular layer Ž. GL , external plexi- mediate Neuronal PrecursorsŽ.Ž INPs Figure 1B; see form layerŽ. EPL , mitral cell layer Ž. ML , internal plexiform below and ref 6. layerŽ. IPL , granule cell layer Ž GCL . , and subependymal The second relay in the olfactory system, the OB, is Ž. layer SEL ; composition of these layers is discussed in the Ž text. Black stars indicate interneurons in the granule cell also a layered structure Figure 1C; reviewed in ref layer and periglomerular regions that are derived from the 15. The outermost layer, the olfactory nerve layer, SVZ. consists of axons of ORNs and their associatedŽ. glial ensheathing cells. ORN axons extend into the glomerular layer, which contains numerous spherical main cell compartments: the apical compartment structuresŽ. glomeruli consisting of axon terminals contains a single layer of supportingŽ or sustentacu- and the dendritic trees of the second-order neurons lar.Ž. cells; olfactory receptor neurons ORNs are upon which ORNs synapse, the mitral and tufted 422 Neuronal regeneration in the olfactory system cells. Surrounding the glomeruli are interneurons have been interpreted to suggest that turnover of known as periglomerular cells, which also receive ORNs, and by extension the rate of neurogenesis in synaptic input from ORNs. Interestingly, the organi- the OE, is normally regulated by environmental fac- zation of glomeruli within the OB is thought to form tors. Thus, toxins or viruses are thought to cause a sensory map for odorant detection. Odors are de- death of ORNs, which are then replaced by the tected by G protein coupled, seven-transmembrane progenitor cells present in the basal compartment. receptors present on the cilia of ORNs.16,17 Individ- The idea that ORNs are constantly undergoing cell ual odorant receptors are expressed in one of four death is supported by the observation that, in the OE broad zones spanning the OE.18,19 Although ORNs of normal adult mice, apoptosis can be detected in expressing a single odorant receptor are widespread cells at all stages in the ORN differentiation pathway, throughout a given zone in the OE, their axons all with the highest level occurring in mature ORNs.28 As converge on one or a few glomeruli in the OB discussed below, experiments in which levels of ORN Ž.Figure 1A; refs 20]22 . In this fashion each glomeru- death are manipulated have led to the conclusion lus in the OB may be tuned to detect a speci®c set of that the level of cell death and the level of neurogen- odors, forming a spatial odorant map.
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