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Dev Growth Differ
2004 Dec 01;466:523-34. doi: 10.1111/j.1440-169x.2004.00767.x.
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Successful reconstitution of the non-regenerating adult telencephalon by cell transplantation in Xenopus laevis.
Yoshino J
,
Tochinai S
.
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The South African clawed frog (Xenopus laevis) can regenerate the anterior half of the telencephalon only during larval life, but such regeneration is no longer possible after metamorphosis. In order to gain a better understanding of differences between larvae and adults that are potentially related to regeneration, several experiments were conducted on larvae and froglets after the partial removal of the telencephalon. As a result, it was found that the cells in the brain proliferated actively, even in non-regenerating froglets, just as was observed in regenerating larvae after the partial removal of the telencephalon. Moreover, it was shown that although the structure was usually imperfect, even isolated single cells derived from the frog brain were able to reconstitute the lost portion when the cells were transplanted to the partially truncated telencephalon. It is therefore likely to be critical for massive organ regeneration that ependymal layer cells promptly cover the cerebral lateral ventricles at an initial stage of wound healing, as is the case observed in larvae. However, in froglets, these cells strongly adhere to one another, and they are therefore unable to move to seal off the exposed ventricle, which in turn is likely to render the froglet brain non-regenerative.
Fig. 1.
Regeneration of larval telencephalon. The anterior half of the telencephalon was removed from stage 53 tadpoles (A,H), and
was then observed macroscopically (AâG) and histologically on horizontally sectioned materials (HâN). Just after the tissue dissection,
the ventricles were open at the anterior end (B,I). As early as 4 days after the operation, the ventricle was completely covered by cells
that had apparently aggregated from the vicinity (D,K). The covered area then gradually increased in thickness with time, and the
regenerated brain was extended anteriorly (L,M). After 30 days, the telencephalon returned to a normal structure with olfactory nerve
bundles, which were connected to the olfactory organs. The arrowheads in (B) indicate the anterior end of the remaining telencephalon
domain. The asterisk in (B) indicates the space created by the partial removal. The arrow in (G) indicates the connection between the
olfactory nerve and the regenerated telencephalon. on, olfactory nerve; t, telencephalon; d, diencephalon; m, mesencephalon; lv,
lateral ventricle; cp, choroid plexus. Bars, 2 mm (AâG); 300 μm (HâN).
Fig. 2.
No regeneration occurred in the adult telencephalon. The anterior half of the telencephalon was removed from froglets 10 days
after metamorphosis (A,D), and the results were observed macroscopically (AâC), and histologically in horizontal sections (DâF). Just
after the tissue dissection, the ventricles were open at the anterior end (BâE). As late as 30 days after the removal of tissue, the
ventricles were still open at the anterior end (C,F). The arrowheads in (B,C) indicate the anterior end of the remaining telencephalon
domain. The asterisks in (B,C) indicate the space created by partial removal. ob, olfactory bulb; cb, cerebrum; d, diencephalon; m,
mesencephalon; lv, lateral ventricle. Bars, 2 mm (AâC); 300 μm DâF.
Fig. 3. Mitotic changes before
and after partial telencephalon
removal. After removing the
anterior half of the telencephalon,
the number of mitotic figures
strikingly increased (compare B,E
with A,D), both in stage 53 larvae
(AâC, red line in G) and in froglets
10 days after metamorphosis
(DâF, blue line in G), as examined
histochemically on crosssectioned
materials (AâF). The
mean mitotic indices shown in
(G) were calculated on BrdUincorporating
cells for all cells on
three randomly selected histological
sections from one animal.
Three animals were used to
illustrate each point. The vertical
bars indicate the SD of nine
samples (three sections from
three animals). lv, lateral ventricle.
Bar, 200 μm.
Fig. 4. Antigenic characterization
of mitotically active ependymal
layer cells surrounding the
lateral ventricle. Intact larvae
(A–F) and froglets (G–L) were
injected with BrdU, and the
telencephalon was examined
histochemically 8 h later (A–L).
Anti-BrdU antibody indicates
replicating cells (green); anti-glial
fibrillary acidic protein (GFAP)
indicates the radial projection of
ependymal layer cells (red); anti-
Musashi1 indicates undifferentiated
neuroblasts (red). In (M–O),
froglets were injected with BrdU
and the telencephalon was
examined 30 days later in order
to determine whether mitotically
active ependymal layer cells
would give rise to differentiated
neurons positive for NeuN antigens.
The right-most panel shows
merged figures showing yellow
cells that are double-positive for
cell proliferation and characteristic
molecules for each cell
type. Each arrowhead in (A–C,
G–I) indicates one replicating
cell having radial projection. The
arrowhead in (M–O) indicates a
cell replicated 30 days ago which
did not differentiate into neuron.
The arrows in (M–O) indicate the
replicated cells 30 days later
differentiated into neuron. lv,
lateral ventricle. Bar, 200 μm.
Fig. 5.
Reconstitution of the
froglet telencephalon by transplantation
of cell suspensions.
Dispersed cells obtained from
larvae (A,D) and froglets (B,E)
were introduced into the space
created in the adult brain by
partially removing the telencephalon.
After 30 days, the reorganized
brain structure consisted
primarily of donor-origin cells
(non-granular nuclei). The rectangles
in (A,B) show the
locations of (D,E), respectively.
Control individuals (no transplantation)
show no indication of
regeneration (C). The dotted line
indicates the hostâgraft boundary,
as distinguished by the
quinacrine stainability of the
nuclei (D,E). The donor cell region
is indicated by asterisks. The
arrowheads in (D,E) indicates
recipient cells found in the donor
cell region. lv, lateral ventricle.
Bars, 200 μm (AâC); 50 μm (D,E).
