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Neuron addition and neurogenesis in adult dorsal root ganglia (Reply to Farel 2001).

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THE ANATOMICAL RECORD (NEW ANAT.) 265:160, 2001
Neuron Addition and Neurogenesis in Adult Dorsal
Root Ganglia (Reply to Farel, 2001)
T
he letter by Farel (2001) adds
an important point to our recent letter (Geuna et al., 2000).
In fact, we agree that neurogenesis is
not the only possible explanation for
the observed increased number of
neurons in dorsal root ganglia
(DRGs). The alternative possibility
that neuron number increase is due to
the late differentiation of slightly immature neurons (neuron addition)
should also be taken into account, as
we have discussed in more detail in a
recent full-length article that reviewed
the issue of adult neurogenesis
(Geuna et al., 2001). For further development of the discussion raised by
Farel’s letter, we would like to ask two
questions, and try to give an answer to
them. 1) Can true neurogenesis (i.e.,
not only late differentiation of slightly
immature neurons) in DRGs be ruled
out on the basis of existing literature?
2) If true neurogenesis occurred, what
could be the function of the newly
generated DRG neurons?
In regards to the first question, true
neurogenesis in DRGs can be reasonably ruled out because the increase in
the number of neurons in postmetamorphic frogs has been attributed to
evidence that poorly differentiated
neurons complete their differentiation after metamorphosis (Meeker
and Farel, 1997; St. Wecker and Farel,
1994). On the other hand, in regard to
other animal models (especially the
rat), data are still poor and conflicting.
For instance, Ciaroni et al. (2000) detect at least some BrdU-labeled nuclei
of neurons in DRGs of vitamin-E-deficient animals. Considering that they
have injected BrdU just three times a
week (a protocol that is not suitable to
label all dividing cells), the number of
neurons that really synthesize DNA
can be higher. In addition, the recent
advancements on “transdifferentiation”, i.e., the possibility for stem cells
to cross lineage-boundaries (Anderson et al., 2001; Geuna et al., 2001),
makes BrdU and 3H-thymidine stud-
© 2001 Wiley-Liss, Inc.
ies a weaker tool to demonstrate (or
rule out) true neurogenesis (as well as
true genesis in any cell population). In
fact, neuron addition could originate
from the “transdifferentiation” of precursors belonging to other cell lineages (of glial origin, hematogenous
origin, connective origin, etc.) without the need of massive cell division.
Theoretically, a true increase of cells
of any cell lineage can originate without an increase of the total number of
cells (i.e., without cell replication and
thus BrdU or 3H-thymidine uptake)
just because of transdifferentiation
from cell precursors belonging to another cell lineage!
The second question is: If true neurogenesis occurred, what could be the
function of the newly generated DRG
neurons? It is difficult to think that
newly generated neurons in DRGs can
grow axons that, once they reach the
dorsal root of the spinal nerve, will
divide in the central and peripheral
processes and then reach the spinal
cord and the periphery (respectively)
to make functional connections. Alternatively, at least two other hypotheses
can be advanced regarding DRG neurogenesis. First, newly added neurons
could be “abortive”, i.e., without connection with the periphery and functional meaning. Neurogenesis can occur as a general process that is
effective in some regions of the nervous system (such as the hippocampus) and ineffective elsewhere. Second, newly added neurons, though
unconnected (or abortively connected) to the periphery, could act as
local modulators of the DRG environment. In a recent commentary on the
unexplained properties of the dorsal
root ganglion (Devor, 1999), it has
been emphasized that the somata of
DRG neurons are richly endowed with
receptor molecules to a variety of neurotransmitters. In this view, newly
generated neurons can, at least to
some extent, play a “local” neuro-
modulator/neurotrophic
role
by
means, perhaps, of the secretion of
diffusible factors.
In conclusion, we believe that the
recent amazing advancements in stem
cell biology should lead to further research (in multiple directions), with
the aim of elucidating the mechanisms that are the basis of various
conditions where an increase in neuron number has been demonstrated
and/or postulated so far.
LITERATURE CITED
Anderson DJ, Gage FH, Weissman IL.
2001. Can stem cells cross lineage
boundaries? Nature Med 7:393–395.
Ciaroni S, Cecchini T, Cuppini R, Ferri P,
Ambrogini P, Bruno C, Del Grande P.
2000. Are there proliferating neuronal
precursors in adult rat dorsal root ganglia? Neurosci Lett 281:69 –71.
Devor M. 1999. Unexplained pecularities of
the dorsal root ganglion. Pain (Suppl.6):
27–35.
Farel PB. 2001. Neuron addition and neurogenesis are not interchangeable terms.
Anat Rec (New Anat) 265:159.
Geuna S, Borrione P, Fornaro M, Giacobini-Robecchi MG. 2000. Neurogenesis
and stem cells in adult mammalian dorsal root ganglia. Anat Rec (New Anat)
261:139 –140.
Geuna S, Borrione P, Fornaro M, Giacobini-Robecchi MG. 2001. Adult stem
cells and neurogenesis: Historical roots
and state of the art. Anat Rec (New Anat)
265:132–141.
Meeker ML, Farel PB. 1997. Neuron addition during growth of the postmetamorphic bullfrog: Sensory neuron and axon
number. J Comp Neurol 389:569 –576.
St. Wecker PG, Farel PB. 1994. Hindlimb
sensory neuron number increases with
body size. J Comp Neurol 342:430 – 438.
S. Geuna*, P. Borrione,
M. Fornaro,
M.G. Giacobini-Robecchi
*Dipartimento di Scienze Cliniche e
Biologiche
Universitá di Torino
Ospedale San Luigi
Regione Gonzole 10
10043 - Orbassano (TO), Italy
Fax: ⫹39-011-90-38-639
E-mail: stefano.geuna@unito.it
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adults, neurogenesis, dorsal, reply, additional, farex, ganglia, neurons, 2001, roots
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