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Cell Migration in the Postnatal Subventricular Zone Brazilian Journal of Medical and Biological Research (2002) 35: 1411-1421 Migration in the subventricular zone 1411 ISSN 0100-879X Cell migration in the postnatal subventricular zone J.R.L. Menezes1, M. Marins1, 1Laboratório de Neuroanatomia Celular, Departamento de Anatomia, J.A.J. Alves1, M.M. Fróes1 Instituto de Ciências Biomédicas, and 2Instituto de Biofísica Carlos Chagas Filho, and C. Hedin-Pereira2 Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brasil Abstract Correspondence New neurons are constantly added to the olfactory bulb of rodents Key words J.R.L. Menezes from birth to adulthood. This accretion is not only dependent on · Postnatal neurogenesis Departamento de Anatomia sustained neurogenesis, but also on the migration of neuroblasts and · Chain migration ICB, CCS, Bloco F, UFRJ immature neurons from the cortical and striatal subventricular zone · Rostral migratory stream 21941-590 Rio de Janeiro, RJ (SVZ) to the olfactory bulb. Migration along this long tangential · Astrocytes Brasil pathway, known as the rostral migratory stream (RMS), is in many · Gap junctions Fax: +55-21-290-0587 ways opposite to the classical radial migration of immature neurons: · Radial glia E-mail: [email protected] it is faster, spans a longer distance, does not require radial glial Presented at the IV International guidance, and is not limited to postmitotic neurons. In recent years UNESCO Course on “What the many molecules have been found to be expressed specifically in this Developing Cerebral Cortex Tells pathway and to directly affect this migration. Soluble factors with About the Adult Cortex (and Vice inhibitory, attractive and inductive roles in migration have been Versa)”, Rio de Janeiro, RJ, Brazil, described, as well as molecules mediating cell-to-cell and cell-sub- December 3-7, 2001. strate interactions. However, it is still unclear how the various mol- Research supported by CNPq, TWAS, ecules and cells interact to account for the special migratory behavior FUJB, and FAPERJ. in the RMS. Here we will propose some candidate mechanisms for roles in initiating and stopping SVZ/RMS migration. Received July 12, 2002 Accepted September 17, 2002 Introduction the most extensively studied. In this case, transient glial cells, the radial glia, form a Cell migration is an imperative require- palisade that courses along the cerebral wall ment during development of most CNS re- from the ventricular zone to the pial surface gions. Newly generated neurons must leave serving as a scaffold for the migration of the germinal layers and move, sometimes a young neurons (1). This form of migration is great distance, to reach their final destina- usually referred to as radial migration, al- tion. This migratory behavior can be classi- though alternative types of radial cell move- fied as radial or tangential depending on the ment, independent of radial glia, have been orientation of the cell movement in relation described (4,5). Neuronophilic migration is to the pial surface (1). Alternatively, migra- a less well-studied migratory behavior in tion can be viewed as gliophilic, neurono- which new neurons are associated with axons philic, and homophilic in relation to the cell instead of glial processes during migration substrates of migration (1-3). The glia-de- (1,2). This mode of migration can assume pendent radial migration of immature neu- various orientations, such as the tangential rons, ubiquitous in the embryonic CNS, is movement of ganglionic eminence precur- Braz J Med Biol Res 35(12) 2002 1412 J.R.L. Menezes et al. sors en route to the cerebral cortex in which tion and proliferation (11), as well as a pre- corticofugal axons appear to function as their cocious biochemical differentiation (11). substrate (6). Finally, homophilic migration Recently, there has been a resurgence of was thus termed because in this modality, interest in the SVZ, both in the neonatal and migrating cells, neurons and neuroblasts, use adult brain, where this system has been used each other as substrate, forming long chains in studies ranging from cell migration to of cells in situ and in vitro (3,7). This form of stem cell biology. migration was first described for the cells In brief, new neurons derived from the that leave the anterior subventricular zone SVZ migrate long distances, invade the ma- (SVZ) towards the olfactory bulb (Figure 1) ture nervous tissue and establish new func- and form the rostral migratory stream (RMS; tional circuits with the existing neurons (12). 8). This tangential migratory movement of This is exactly the behavior one would wish neurons and neuroblasts is directly associ- from a source of new neurons that could be ated with the neurogenesis of olfactory bulb used to substitute neuron depletion. The un- interneurons that occurs postnatally in the derstanding of the mechanisms by which SVZ- SVZ, a highly proliferative layer in the early derived cells migrate may be then as important postnatal animal that persists well into adult- as understanding how this region sustains con- hood (7-10). tinued neurogenesis throughout adulthood. Besides the unusual mode of migration, Here we will review the special characteris- cells within the SVZ/RMS display other un- tics of this tangential migration and the cel- usual features, such as simultaneous migra- lular interactions that drive this behavior. Figure 1. Summary of subven- tricular zone/rostral migratory stream (SVZ/RMS) tangential mi- gration towards the olfactory bulb (OB) in a parasagittal representa- tion of the anterior forebrain in Progenitors Neuroblast or immature neuron the early postnatal animal. Migra- tion in the RMS can be divided Mitosis Periglomerular cell into three overlapping phases that correspond roughly to differ- Granular cell ent portions of the pathway (num- Radial glia Cx cc bers in circles). 1) Initially cells go through a phase in which they lv migrate but are still able to divide. Radially migrating neuron That happens mostly in regions 1 of the SVZ close to the lateral ventricles where mitosis is more frequent. 2) At a given moment, AOB St already within the RMS, cells defi- 3 nitely abandon the cell cycle and continue migration towards the OB. 3) Upon reaching the OB, cells switch from tangential to ra- dial migration and invade the OB 2 MOB parenchyma, turning on their dif- Tu ferentiation into granular and periglomerular cells. In early post- natal life radial glia form a scaffold for this pathway as represented with a few examples (more details can be obtained in Ref. 16). Radial glia in the OB were omitted for simplicity. Although only the early postnatal period is represented in this figure, migration in the adult SVZ/RMS appears to obey similar phases and pattern. Note also that, although not represented, chain migration can also occur from more caudal regions. The SVZ/RMS is represented in stipples. AOB, accessory olfactory bulb; Cx, cerebral cortex; cc, corpus callosum; lv, lateral ventricle; MOB, main olfactory bulb; St, striatum; Tu, olfactory tubercle. Braz J Med Biol Res 35(12) 2002 Migration in the subventricular zone 1413 Cellular composition of the SVZ (14). Additional evidence for this comes postnatal SVZ from infusion of truncated ephrins that by disturbing proliferation cause the appearance The SVZ is not a homogeneous and of large islands of proliferating cells (22). The stable region throughout the life of an ani- relevance of these discrete compartments is mal. The cellular composition of young and still not fully understood. They may reflect the adult SVZ differs little except for relative segregated distribution of specific cells and/or numbers, with both containing immature neu- growth factors with proliferation-inducing ca- rons, neuroblasts, undifferentiated precur- pacities. Alternatively, they may arise from the sor cells, astrocytes and microglia (13,14). A preferential adhesion between homophilic main difference is that in the young SVZ the migrating cells, thus excluding proliferating major glial component is the radial glia, cells from the migratory chains. absent in the adult (15,16). The astrocytes of the adult SVZ/RMS surround the migrating Tangential migration within the cells providing an astrocytic scaffold to the SVZ/RMS SVZ that forms long cylinders denominated glial tubes (7,17). Recently, we have demon- The migration of neuroblasts and young strated that such a scaffold does in fact exist neurons generated in the SVZ can also be in the young SVZ formed by the cell bodies divided into three phases, independent of the and processes of transforming radial glia age of the animal (Figure 1). Based on the (17). decreasing caudal-to-rostral proliferative gra- dient of the RMS (8,19,23,24) we can infer Compartments in the postnatal SVZ that cells go through a phase switch, in which first migration and proliferation can occur Proliferation in the SVZ was thought to simultaneously, to another, when migrating occur homogeneously, in contrast to, for cells do not reenter the cell cycle. The exact example, the embryonic ventricular zone, time and place where this transition occurs where a characteristic nuclear movement are yet to be determined, although this must segregates cells in different stages of the cell happen somewhere along the RMS. This cycle (18). Recently, we have demonstrated transition appears to become more spatially that the S-phase cells in the young SVZ/ restricted with age, when cell division is RMS are preferentially concentrated in the mostly restricted to the region overlying the periphery of the SVZ/RMS tube-like struc- lateral ventricles. The third phase occurs ture spatially segregated from migratory cells within the bulb, where the cells go through (19). A similar periphery-to-core pattern of another phase switch, this time from a tan- distribution was recently described for the gential to a radial migratory mode (10,23). It expression of zebrin II (20), which rein- is possible that the glial cells in the olfactory forces the idea that the early postnatal SVZ is bulb provide the necessary signals for the organized in discrete cellular compartments.
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