Chem. Senses 27: 581-582,
2002
© Oxford University Press 2002
SYMPOSIUM: Mechanisms of Differentiation and Migration of Olfactory Progenitors |
Cell Migration in the Rostral Migratory Stream
Dipartimento di Biologia Animale e dell'Uomo, University of Turin, Italy 1 Dipartimento di Morfofisiologia Veterinaria, University of Turin, Italy
Correspondence to be sent to: Aldo Fasolo, Dipartimento di Biologia, University of Turin, via Accademia Albertina 13, 10123 Turin, Italy. e-mail: aldo.fasolo{at}unito.it
Abstract
Adult neurogenesis in the olfactory bulb of rodents is provided by cells which migrate tangentially from their site of genesis into the forebrain subependymal layer (SEL). This migration involves `chains' of neuroblasts sliding into a meshwork of astrocytic cells and processes (glial tubes). The analysis of this process in postnatal rodents and in adult rabbits reveals different types of relationships occurring both among the migrating cells and between these cells and the glial structures of the SEL.
Tangential migration characterizes the subependymal layer (SEL) of adult
rodents. Within the SEL, chains of migrating cells are ensheathed by a
meshwork of astrocytes (glial tubes) that continue into the olfactory bulb,
wherein single neuroblasts spread radially
(Peretto et al.,
1999
). This striking structural plasticity is the model of choice
to unravel mechanisms that allow neurogenesis and cell migration to persist
into the adult mammalian brain. Understanding these mechanisms is crucial from
the perspective of repair of the mature nervous tissue. The unique
organization of glia along the migration pathway led to the hypothesis that
they have a scaffolding function in cell migration and guidance, as previously
established during development in other parts of the nervous system
(Rakic, 1990). Not consistent
with this hypothesis is the finding that during the early postnatal period
tangential migration along the SEL occurs in the absence of chain organization
and glial tubes. In general, migration is orthogonal to the still existing
radial glia, thus suggesting that glial substrates are not essential for cell
displacement into and through the SEL. A comparative approach extended to the
adult rabbit forebrain shows a pattern of cell proliferation and migration
very similar to that previously described in rodents, but occurring within a
different astrocytic organization—one that is devoid of wellformed glial
tubes. In the rabbit, the olfactory ventricles do not close at birth, thus
leaving a ventricular cavity in the area corresponding to the `rostral
extension' of rodents that is characterized by the glial tubes. By contrast,
the olfactory ventricles of the adult rabbit are surrounded by a poorly
defined SEL wherein astrocytes are densely packed but not organized to form
channels. However, some chains of cells immunoreactive for the polysialylated
form of the neural cell adhesion molecule (PSA-NCAM) can be observed. In
rodents, this is a characteristic feature of the long-distance, tangential
cell migration occurring along the glial tubes of the SEL. Thus, the results
obtained in the rabbit SEL seem to confirm that, even in an adult mammalian
brain, specific structures such as the glial tubes are not required to
facilitate cell migration. Ongoing studies in the postnatal rat forebrain show
that the assembly of glial tubes in the SEL occurs around the third postnatal
week, coincidentally with the progressive maturation of the surrounding brain
parenchyma (Peretto et al.,
1998). Indeed, the immunocyto-chemical localization of a variety
of glia- and neuron-associated molecules in the SEL of postnatal and adult
rodents reveals that both cell types show a certain degree of immaturity. In
addition to mature astrocytic markers, cells of the glial tubes also express
the intermediate filament protein vimentin, which is abundant in radial glial
cells. The migrating neuroblasts retain molecules usually expressed during
development, as well as putative regulators of cell migration such as
PSA-NCAM, stathmin and the neuregulin receptor erbB4
(DeMarchis et al.,
2000). The shift from a widespread distribution of these molecules
during the early postnatal period to their very restricted localization in the
SEL occurring at the third postnatal week suggests that glial cells in the
SEL, rather than being directly involved in cell migration and guidance, could
be implicated in the isolation and compartmentalization of a microenvironment
that subserves the persistent neurogenesis which characterizes this region
during adulthood. Moreover, the heterogeneous distribution of glial cells in
the SEL of postnatal versus adult rodents, as well as in the SEL of different
mammalian species, leads us to the conclusion that multiple types of cell
migration can be found in the brain of different mammals, and suggests that
most of them share a behavior that is rather independent of their local glial
substrates.
Acknowledgments
The financial support of Compagnia di San Paolo is acknowledged.
References
De Marchis S., Peretto P., Perroteau I. and Fasolo A. (2000) Expression of the erbB4 neuregulin receptor in the subependymal layer of postnatal and adult rat. Presented at the 30th Annual Meeting of the American Society for Neuroscience.
Peretto, P., Bonfanti, L., Merighi, A. and Fasolo, A. (1998) Carnosine-like immunoreactivity in astrocytes of the glial tubes and in newly-generated cells within the tangential part of the rostral migratory stream of rodents. Neuroscience,85 , 527-542.[Medline]
Peretto, P., Merighi, A., Fasolo, A. and Bonfanti, L. (1999) The subependymal layer in rodents: a site of structural plasticity and cell migration in the adult mammalian brain.Brain Res. Bull. , 49,221 -243.[Web of Science][Medline]
Rakic P. (1990) Principles of neural cell migration. Experientia, 46,882 -891.[Web of Science][Medline]
Accepted May 1, 2002
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