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The Journal of Neuroscience, February 1, 2002, 22(3):629-634
MINI REVIEW
Neurogenesis in Adult Subventricular Zone
Arturo
Alvarez-Buylla1 and
Jose Manuel
García-Verdugo2
1 Department of Neurological Surgery, Brain Tumor
Research Center, San Francisco, California 94143-0520, and
2 Department of Cellular Biology, Faculty of Biology,
University of Valencia, Valencia, Spain 46100
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ARTICLE |
Much excitement has been generated
by the identification of adult brain regions harboring neural stem
cells and their continual generation of new neurons throughout life.
This is an important departure from traditional views of the germinal
potential of the postnatal brain. However, a more profound
paradigm shift may be emerging. Studies of adult neurogenesis in the
subventricular zone (SVZ) have revealed unexpected properties of
neuronal progenitors and new mechanisms of neuronal migration. Here we
discuss some recent findings that examine the origin, migration, and
function of SVZ-derived new neurons in adult brain and highlight areas that offer exiting opportunities for future research.
Along much of the lateral walls of the lateral ventricles lies the
largest germinal zone of the adult mammalian brain, the SVZ (Doetsch
and Alvarez-Buylla, 1996 ). In fully adult mammals, mew neurons
born in the SVZ of adults migrate anteriorly into the olfactory bulb
(OB), where they mature into local interneurons (Altman, 1969;
Lois and Alvarez-Buylla, 1994; Kornack and Rakic, 2001; Pencea et al.,
2001a) (Fig. 1). SVZ neural stem cells
can be grown in culture with epidermal growth factor (EGF), fibroblast growth factor (FGF), or the two combined (Weiss et al., 1996; Temple and Alvarez-Buylla, 1999; Gage, 2000). As such, the SVZ represents an important reservoir of progenitors in the adult brain,
perhaps harboring cell populations that could be used for neuroregenerative therapy. These findings dramatically change the way
we think about the adult brain. However, a deeper paradigm shift may be
emerging as these discoveries raised basic mechanistic questions not
easily explained by classical views of brain development.
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Figure 1.
The SVZ-OB system. Schematic sagittal view of the
adult rodent brain with the OB to the left and the
cerebellum (CB) to the right. The SVZ is
along the lateral wall of the lateral ventricle (LV,
blue). New neurons are constantly produced throughout the SVZ.
The young neurons (A cells) (Fig. 3) become aligned into long chains
(red lines) (Fig. 2) that form a complex network of
interconnected paths throughout the SVZ. Many of these chains in the
anterior SVZ connect with the RMS, which leads young neurons into the
core of the olfactory bulb. Within the olfactory bulb, cells disperse
radially (dotted lines) as individual cells and complete
their differentiation into granule and periglomerular interneurons.
NC, Neocortex; cc, corpus callosum.
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(1) Which cells give rise to new neurons in adult brain, and how is the
production of these new neurons regulated? (2) How do the young neurons
move through adult brain and find their way into the OB? (3) What is
the function of neuronal replacement in the adult OB? Two decades ago,
it was difficult to imagine that neurogenesis and neuronal migration
could be studied in adult brain. However, the SVZ-OB system has become
an attractive experimental model in which to study neural stem cells,
neurogenesis, the migration of young neurons, and their differentiation
and death. Moreover, the entire process raises basic questions about
how neural circuits benefit from a constant exchange of neurons.
Origins
The continual production of new neurons in the adult SVZ suggests
that neural stem cells persist within this germinal layer. The
SVZ-ependymal region contains at least four different cell types
defined by their morphology, ultrastructure, and molecular markers
(Doetsch et al., 1997) (for the organization of the SVZ, see Fig.
2). The young migrating neurons (type A
cells) form chains ensheathed by astrocytes (type B cells). More
spherical and highly proliferative precursors (type C cells) form
clusters next to the chains of migrating A cells. The SVZ is largely
separated from the ventricle cavity by a layer of ependymal cells (type E cells). B cells interact closely with E cells and occasionally contact the ventricle lumen. Whereas E cells have many long cilia, B
cells contain a single short cilium (Doetsch et al., 1999b) similar to
those of neural progenitors in the embryo.
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Figure 2.
Chain migration. Young neurons within the SVZ
network and in the RMS migrate along each other to form long chains.
Chains of migrating cells (red) are ensheathed by glial
cells (blue) that have astrocytic characteristics,
including dense bundles of GFAP-containing intermediate filaments and
endings on blood vessel (below). Two chains are illustrated here. In
the bottom chain only some of the astrocytes have been
drawn to illustrate the tight organization of A cell into chains. The
intracellular characteristics of some of the B cells (light
blue) and A cells (yellow) are
illustrated. An A cell in mitosis is illustrated in the
bottom chain to the right.
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In addition to C cells, which are labeled most frequently by
[3H]-thymidine injection, B and A cells,
the SVZ astrocytes and young neurons respectively, also divide. It has
been suggested that muticiliated E cells also divide in vivo
and function as stem cells (Johansson et al., 1999). However, when
labeled cells near the lateral wall of the lateral ventricle are
analyzed with electron microscopy, no evidence of ependymal division is
found (Doetsch et al., 1999a).
The division of B and C cells suggests that one or both of these cell
types could be involved in the generation of the new neurons, the A
cells. Because A cells, themselves, divide (Lois and Alvarez-Buylla,
1994; Menezes et al., 1995; Thomas et al., 1996), it was also
formally possible that they simply generate more A cells. However,
purified A cells in culture do not appear to be self renewing (Lim and
Alvarez-Buylla, 1999). In contrast, a fraction enriched for B/C cells
gives rise to large colonies of A cells. Previous studies had noticed
that the SVZ astrocytes divide, but it was thought that these cells
were simply generating more glia. Quite unexpectedly, more
recent work indicates that B cells, the SVZ astrocytes, are the primary
precursors of new neurons (Doetsch et al., 1999a). After ablation of C
and A cells with antimitotic drugs, SVZ astrocytes divide to generate
new C cells that in turn generate A cells. Labeling specifically SVZ astrocytes with an avian retrovirus resulted in the generation of
labeled neurons that migrated and integrate in the OB. Thus, under
normal conditions and during regeneration, B cells seem to function as
the primary precursors for the new neurons (Fig. 2). These cells are
also capable of generating cells that grow as neural stem cells
in vitro (Doetsch et al., 1999a).
SVZ astrocytes cultured in vitro can also generate FGF- and
EGF-responsive neurospheres (Laywell et al., 2000). Interestingly, this
same study has shown that mouse astrocytes from cortex, cerebellum, and
spinal cord can also behave as stem cells in vitro, but only when isolated before postnatal day 10. Recent work in the adult subgranular layer of the hippocampus indicates that in this region, too, astrocytes function as the primary precursors for new granule neurons (Seri et al., 2001). The neurogenic potential of cells with
astrocytic properties is surprising given the previously unchallenged
idea that neuroglia develop from a lineage separate from that of
neurons. Astrocytes are derived from radial glia during development. In
some species, including the canary, radial glia are retained into adult
life, serving as the primary precursors of new neurons (Alvarez-Buylla
et al., 1990b). Emerging data also indicate that radial glia are neural
stem cells in the developing mammalian neocortex (Malatesta et al.,
2000; Miyata et al., 2001; Noctor et al., 2001). Muller cells have also
been identified as neural precursors in the developing retina (Fischer
and Reh, 2001). Together, these findings have led to the proposition
that neural stem cells lie within the neuroepithelial-radial
glia-astrocyte lineage (Alvarez-Buylla et al., 2001).
Neurogenesis in the adult brain is restricted to particular niches. Is
it the astrocytes, the microenvironment, or both that create an adult
brain germinal region? The identification of reliable molecular markers
to distinguish terminally differentiated astrocytes from those that can
function as neural stem cells remains an important problem for future
research. Most of the signaling molecules that allow neurogenesis to
occur in the SVZ also remain to be discovered. One signaling pathway,
however, has been recently identified. Local neutralization of BMP
signaling, a neurogenesis inhibitor, by ependymal noggin may be
critical for SVZ neurogenesis (Lim et al., 2000) (Fig. 2). Adult
neurogenesis likely results from the interplay of microenvironment with
specific subtypes of astrocytes.
The regulation of proliferation in the SVZ is another particularly
interesting problem. The symmetry of B cell division remains unknown,
as does the number of times C cells divide before A cell production.
The cell cycle of the different cell types in the SVZ needs to be
determined. Previous estimates of cell cycle duration in the SVZ
assumed that the SVZ is composed of a homogenous population of
nonmigratory dividing cells (Morshead et al., 1994). These assumptions
are not met in the SVZ, particularly given the rapid tangential
migration of dividing A cells. More accurate methods are required to
establish the cell cycle duration for the specific cell types in the SVZ.
Growth factors also probably play an important role in the regulation
of proliferation in the SVZ. EGF, TGF , and FGF can stimulate the
proliferation of SVZ cells in vivo (Morshead et al., 1994;
Craig et al., 1996; Kuhn et al., 1997; Tropepe et al., 1997). SVZ cells
respond to EGF, FGF-forming neurospheres that have characteristics of
neural stem cells in vitro (Morshead et al., 1994; Weiss et
al., 1996). Interestingly, growth factor-amplified SVZ cells appear to
acquire the ability to function as progenitors for other organs as well
(Vescovi et al., 2001). The in vivo role of growth factors
and their receptors is, however, poorly understood. Consequently, the
identity of the EGF-responsive cells in vivo is
controversial. Whereas earlier work suggest that the EGF-responsive cells are relatively quiescent (Morshead et al., 1994), recent experiments suggest that EGF induces the rapidly dividing transient amplifying cells (C cells) to behave as stem cells in vitro
(Doetsch et al., 2001). The FGF-responsive cells have not yet been
identified. Other molecules in concert with classical growth factors
may also regulate proliferation in the SVZ. SVZ astrocytes express
ligands for EphB2. Infusion of EphB2 or ephrinB2 receptor bodies into the brain increases the proliferation of SVZ cells and induces many B
cells to contact the ventricle (Conover et al., 2000). We are still far
from understanding how precise numbers of new neurons and glial cells
are generated in the SVZ. This information is important to determine
the dynamics of cell generation and to draw a precise lineage from the
dividing SVZ stem cells, through the transient amplifying C cells to
the final progeny of young neurons.
Migration
In adult mice, the SVZ is millimeters away from the OB; quite a
journey for a cell that is just 10-30 µm long. The problem is
further compounded if we consider that A cells, the SVZ neuroblasts, originate throughout most of the lateral wall of the lateral ventricle and traverse a complex network of interconnected paths before joining
the rostral migratory stream (RMS) (Doetsch and Alvarez-Buylla, 1996)
(Fig. 1). A similar migration has now been described in much larger
brains, including those of primates (Kornack and Rakic, 2001; Pencea et
al., 2001a). It has also been suggested that similar migrations
may occurs in the infant human brain (Weickert et al., 2000). In these
large brains, the migration of SVZ derived cells is impressively long.
How do these cells move and orient over such long distances and
traverse the dense parenchyma of the adult brain? A migration from the
SVZ to neocortex has also been suggested (Gould et al., 1996; Magavi et
al., 2000), but this migration has not been demonstrated.
In adult rodent SVZ and RMS, A cells move along each other, forming
chains (Fig. 3) (Lois et al., 1996). A
cells have an elongated morphology with a prominent leading process
tipped by a growth cone (Kishi, 1987; Lois and Alvarez-Buylla,
1994; Wichterle et al., 1997). In chains reconstituted in
vitro, neuroblasts move in incremental steps at average speeds of
~120 µm/hr (Wichterle et al., 1997). The cellular machinery that
propels young neurons at these high speeds is not understood. It is
likely that microtubule polymerization and depolymerization plays an
important role in both the exploratory behavior and net translocation
that occurs during a step. Doublecortin, a microtubule-associated
protein important for neuronal migration in development, is expressed prominently by cells in chains of the RMS (Gleeson et al., 1999), suggesting that the migration to the OB in the adult shares key molecular players with migration in the embryo. The prominent growth
cone and the active extension and retraction of the leading process of
A cells (Wichterle et al., 1997), suggest that these cells may use some
of the locomotory mechanisms also used by growing axons.
Accordingly, collapsin response-mediated protein 4, a molecule involved
in axonal guidance, is present in the migrating A cells (Nacher et al.,
2000). Migration of neurons and the growth of axons could differ
in that the former incorporates a mechanism to shuttle the cell body
into the leading process, resulting in the net translocation of the
cell. How the A cell cytoskeleton functions during migration and
what types of signals trigger the cell to advance a step are
particularly interesting problems for future research.
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Figure 3.
Organization and lineage in the SVZ.
Left, Cross section of the anterior rodent brain
indicating the location of the SVZ on the lateral wall of the LV. On
the right is the cellular composition and organization
of the SVZ. Chains of young neurons (A cells, red) are
surrounded by B cells (blue) that have astrocytic
characteristics and form tube-like structures. Clusters of highly
proliferative C cells are associated with the chains of A cells.
Ependymal (E) cells form an epithelial layer that
separates the SVZ from the ventricle (LV). B
cells generate transient amplifying C cells that generate the A cells
(top). Bottom left, BMPs inhibit neurogenesis
and favor glial differentiation (blue). Noggin secreted
by ependymal cells binds BMPs and releases some B cells to become
neurogenic and produce C (green) and A
(red) cells.
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As mentioned above, chains of migrating A cells are ensheathed by
astrocytes (B cells) (Figs. 2, 3) (Jankovski and Sotelo, 1996; Lois et
al., 1996; Peretto et al., 1997). The function of the glial tubes is
not known. Astrocytes are not essential for chain migration (Wichterle
et al., 1997), but factors secreted by astrocytes appear to enhance the
migration of SVZ neuroblasts (Mason et al., 2001). These ensheathing
astrocytes are likely to play important roles. In addition to
enhancement of migration, the glial cells around chains may also
support the survival and/or provide directional information to the A
cells. Additionally, these tubes may prevent A cells from prematurely
escaping normal migratory routes.
Work has begun to identify cell surface adhesion molecules that may be
important for chain migration. 6 1 integrin appears to be required
for chain migration of type A cells (Jacques et al., 1998).
Polysialylated form of neural cell adhesion molecule (PSA-NCAM)
is expressed along the RMS (Bonfanti and Theodosis, 1994) in
migrating A cells (Rousselot et al., 1995), and the rostral migration
of A cells is severely disrupted in animals lacking NCAM or PSA
(Tomasiewicz et al., 1993; Cremer et al., 1994; Ono et al., 1994).
Although initial observations had suggested that PSA was essential for
chain migration (Hu et al., 1996), more recent work indicates that A
cells lacking PSA are less effective in their migration, but capable of
forming chains and moving along the RMS (Cremer et al., 1994). This
study shows that PSA is critically important for the organization of B
cell gliotubes in the RMS. PSA-NCAM may prevent A cells from
establishing tight contacts with glial cells that may hinder
them in their long journey. The extracellular matrix also contributes
to the migratory environment of the RMS. Tenascin and chondroitin
sulfate-containing proteoglycans have been shown to be present in the
RMS (Thomas et al., 1996). Further work is needed to understand
the interplay of surface molecules with the extracellular matrix during
chain migration.
The directionality of migration over the long distance between the SVZ
and the OB is perhaps one of the most fascinating problems in this
system. Presence of the OB is not required for the rostral migration of
A cells (Kirschenbaum et al., 1999), suggesting that, if the OB
secretes chemoattractants, these factors are nonessential for the
rostral migration. Instead, it has been suggested that chemorepulsion
mediated by Slit-Robo signaling may be involved in the migration of
young neurons in the RMS (Hu, 1999; Wu et al., 1999). There is,
however, no information in vivo regarding the role of Slits,
and it is difficult to imagine how stable gradients of repulsive agents
can be established over such a long and complex migratory route.
Moreover, it has been suggested that the source of Slit is the septum,
which lies in the medial wall of the lateral ventricle, opposite to
where the majority of migration occurs. Slits, instead may serve as
general inhibitors of migration (Mason et al., 2001), perhaps
preventing SVZ neuroblasts from migrating into certain regions of the
brain. The directional mechanism of SVZ and RMS migration remains wide
open. Understanding this process may yield novel mechanisms of neuronal orientation.
Once cells reach the core of the OB, they separate from the chains,
individually migrate to more superficial layers, and differentiate into
granule and periglomerular neurons. Nothing is known about the signals
in the OB that induce this change of migration pattern. The mechanism
of radial migration within the bulb is also not known. Interestingly,
in the adult OB, radial glia are no longer present, raising the
question of what guides these young neurons from the OB core to more
superficial layers.
Function
Thousands of young neurons migrate (A cells) into the OB every day
(Lois and Alvarez-Buylla, 1994), but only a fraction of these cells
survive to complete their differentiation. This process is even more
conspicuous in the early postnatal brain, where the RMS is massive
(Luskin, 1993). Why are all these new neurons incorporated into the
olfactory system during postnatal life?
In the adult hippocampus (Barnea and Nottebohm, 1994; Kempermann et
al., 1997; Gould et al., 1999a) and the song control nuclei in adult
birds (Nottebohm, 1985; Alvarez-Buylla et al., 1990a), two systems
where adult neuronal incorporation has been extensively studied, it has
been suggested that new neurons participate in plasticity and learning.
Much less is known about the function of new neurons in the OB of
postnatal animals. Optimal olfactory circuitry may be assembled by the
incorporation of neurons when olfactory circuits are already responding
to environmental signals. The continuous replacement of neurons in the
OB may allow for adjustment of olfactory circuitry as the environment
or relevance of odors change.
Naris closure decreases the recruitment of new neurons to the OB
(Frazier-Cierpial and Brunjes, 1989; Corotto et al., 1994). It is
possible that only granule cells connected to relatively active mitral
or tufted cells survive, whereas all others undergo apoptosis. Recent
work indicates that soon after new granule cells develop synaptic
connections in the OB, there is a period of intense cell death, perhaps
reflecting this selection process (Petreanu and Alvarez-Buylla, 2001).
What could be the advantage of continual replacement of granule cells?
Granule cell activity is known to extensively shape the activity of
mitral and tufted cells. Modeling experiments indicate that selection
of new granule cells based on their level of activity alone could
continually redistribute odorant representations across the OB (Cecchi
et al., 2001). This model predicts a remarkable improvement in
olfactory discrimination by maximizing differences between similar
odors. Studies in NCAM ( /) mice, in which the number of newly
formed SVZ cells that reach the OB from birth is severely reduced,
olfactory discrimination between odors is impaired, but odor
sensitivity and olfactory memory appear normal (Gheusi et al., 2000).
Thus, experimental and theoretical approaches are beginning to suggest
that new neurons in the OB have some role in olfactory discrimination.
Neurogenesis may in adult animals may allow brain circuitry involved in
sexual behavior to be modified. In birds, steroid hormones play
important roles in regulating the survival of newly generated neurons
in song control nuclei (Rasika et al., 1994, 1999; Burek et al., 1995;
Hidalgo et al., 1995). Similarly, in the adult hippocampus, estrogen
appears to increase the number of dividing cells in the subgranular
layer (Tanapat et al., 1999). New interneurons are also added to the
accessory OB (Bonfanti et al., 1997), a region known to process
olfactory information related to sexual behavior. Interestingly, recent
work in prairie voles shows a dramatic increase in the number of
dividing cells in the RMS during estrous (Smith et al., 2001). BDNF
promotes the survival of A cells (Kirschenbaum and Goldman, 1995;
Pencea et al., 2001b). As in birds, the effects of steroid
hormones on the survival of the new neurons may be mediated through
this trophic factor (Rasika et al., 1999). However, BDNF is thought to
function as a trophic factor for neurons that have matured and are
becoming integrated into functional circuits. It is, therefore, very
intriguing that the survival of a population of migrating precursors
should be regulated in this manner. Moreover, A cells far outnumber the new neurons that become incorporated in the OB; why then is regulation of their survival so critical?
This is just the beginning of our understanding of what is, perhaps,
the most intriguing problem: the role of the new neurons in the OB.
More sensitive behavioral models to test olfactory discrimination are
needed. Animal models in which only a subpopulation of granule cells
born postnatally could be ablated are also required so that
developmental history would not interfere with interpretation of
behavior. In addition, we need a better understanding of the contribution of the new neurons to electrophysiological changes in the OB.
Future perspective
The SVZ-OB system offers a unique opportunity to study, in an
adult organism, the origin, migration, and integration of new neurons
into functional brain circuits. Here we separated the process into
three topics that expose exciting mechanistic data that has recently
emerged. The identification of SVZ astrocytes as neural stem cells is
particularly intriguing. We may learn in the coming years how to
identify those cells with astrocytic properties that can function as
stem cells. This information may open new avenues for the isolation and
genetic modification of stem cells derived from the postnatal brain.
Studies of the molecular mechanisms of cell translocation and
orientation during chain migration are also in their infancy. Very
basic mechanisms may be discovered here, too, as the distances and
speeds of migration baffle those accustomed to thinking of neuronal
migration as a developmental process. Origin and migration are
conceptually interrelated problems. It is likely that advances in our
understanding on these two fronts will provide the essential
ingredients for future studies to elucidate the function of newly
generated cells. This last topic is by far the most challenging and
probably hides behind fundamental principles of brain function.
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FOOTNOTES |
This work was supported by National Institutes of Health Grants NS28478
and HD32116, by the Sandler Family supporting Foundation, and
Fundació la Caixa. We thank Anthony Tramontin and Nader Sanai for
their comments on this manuscript.
Correspondence should be addressed to Dr. Alvarez-Buylla, Department of
Neurological Surgery, Brain Tumor Research Center, Box 0520, 533 Parnassus Avenue, San Francisco, CA 94143-0520. E-mail:
abuylla{at}itsa.ucsf.edu.
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