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J Comp Neurol
1997 Jan 20;3773:351-64. doi: 10.1002/(sici)1096-9861(19970120)377:3<351::aid-cne4>3.0.co;2-1.
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Xefiltin, a new low molecular weight neuronal intermediate filament protein of Xenopus laevis, shares sequence features with goldfish gefiltin and mammalian alpha-internexin and differs in expression from XNIF and NF-L.
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The nervous system of the postmetamorphic frog Xenopus laevis, like that of other amphibians, shows continued growth and a high capacity for regeneration, especially in its visual system. This characteristic has been attributed, in part, to the retention in adults of traits that in mammals are limited to embryos. In mammals, the progressive maturation of neurons is marked by successive changes in neuronal intermediate filament (nIF) subunit composition. For example, in mammalian forebrain, newly differentiating neurons first express the low molecular weight nIF protein alpha-internexin. As neurons mature, alpha-internexin expression declines, and expression of the low molecular weight neurofilament triplet protein (NF-L) increases. Thus, a systematic examination of the expression of low molecular weight nIF proteins in the postmetamorphic frog might reveal whether the nIF subunit composition of its neurons more closely resembles that of embryonic as opposed to adult mammals. Previously, X. laevis has been shown to express both NF-L and XNIF, a novel low molecular weight nIF protein that most closely resembles mammalian alpha-internexin. We have now discovered a new, low molecular weight nIF protein with even higher homology to alpha-internexin. We named this protein xefiltin, because it shared highest sequence identity with gefiltin, an alpha-internexin-like nIF protein from the goldfish visual system. In situ hybridization with probes to xefiltin, XNIF and NF-L showed that transcripts of all three were expressed widely throughout the post-metamorphic frog nervous system, but with distinctly different patterns of expression. For example, xefiltin was the most abundantly expressed of the three in retinal ganglion cells and in neurons of the habenular nucleus and telencephalon, whereas XNIF and NF-L were found at higher levels than xefiltin in peripheral sensory ganglia and in structures caudal to the mesencephalon. In general, the combined distributions of xefiltin and XNIF paralleled the distribution of alpha-internexin in mammalian embryos. Thus, we speculate that the persistence of alpha-internexin-like nIF proteins in the amphibian nervous system may be important for its continued potential for growth and plasticity.
Fig. 3. Neural-specific expression of xefiltin mRNA as revealed by
Northern blot analysis of total RNA (10 μg for each sample) from
various Xenopus tissues with a 32P-labeled cDNA probe (spanning
nucleotides 297 to 950). Lane 1, juvenile spinal cord; Lane 2, juvenile
retina; Lane 3, juvenile brain; Lane 4, adult (. 3 yr old) brain; Lane
5, muscle; Lane 6, skin; Lane 7, liver; and Lane 8, ovary. Marks
labeled 28S and 18S indicate the positions of the large and small
ribosomal RNAs, respectively.
Fig. 5. Expression of xefiltin (A), XNIF (B) and NF-L (C) transcripts
in the retina of juvenile X. laevis revealed by in situ hybridization
with digoxigenin labeled anti-sense cRNA probes. As a negative
control, one section was hybridized with a labeled cRNA probe
transcribed in the sense orientation of xefiltin (D). In retinal ganglion
cells (examples indicated by unlabeled arrowheads), the level of
xefiltin mRNA was high, whereas that of XNIF was moderate, and
that of NF-L was low. The XNIF probe also occasionally labeled
neurons scattered along the inner margin of the inner nuclear layer
(arrowhead labeled ‘‘i’’ in B). r, retinal ganglion cell layer; i, inner
nuclear layer; p, photoreceptor layer. The scale bar 5 50 μm in D,
applies to all panels.
Fig. 6. Xefiltin, XNIF, and NF-L mRNA expression in forebrain
structures of juvenile X. laevis. In the nucleus habenularis of the
diencephalon (A–C), and the striatum of the telencephalon (D–F),
neurons expressed high levels of xefiltin transcript (A,D), but undetectable
levels of XNIF (B,E) and NF-L (C,F). In the olfactory nuclei of the
telencephalon (G–I), mitral cell neurons expressed moderate levels of
xefiltin (G) and NF-L (I) mRNAs, and barely detectable levels of XNIF
(H). A–C are from the boxed area of Figure 4C. D–F depict the boxed
area of Figure 4B, and G–I are from the boxed area of Figure 4A.
Abbreviations are as in Figure 4. The scale bar570 μm in C, applies to
all panels.
Fig. 7. Xefiltin (A,D), XNIF (B,E), and NF-L (C,F) mRNA expression
in midbrain structures. A–C: Deep layers of the lateral optic
tectum, from the upper boxed region shown in Figure 4D. XNIF (B)
and NF-L (C) staining were intense in some cells and light in others,
whereas that of xefiltin (A) appeared lighter and more homogeneous.
Layers of the tectum are numbered in A. D–F: Cells from the area of
tegmentum that is surrounded by the lower box in Figure 4D. Neurons
in these regions generally expressed comparable levels of mRNAfor all
three of the low molecular weight nIF proteins, although labeling was
heterogeneously distributed among individual cells. Abbreviations are
as in Figure 4D. The scale bar 5 70 μm in A, applies to all panels.
Fig. 8. Xefiltin, XNIF, and NF-L mRNAexpression in the medulla.
In neurons of the dorsal sensory nuclei of the VIIIth (indicated by
arrowheads labeled viii), as well as other sensory nuclei (labeled vi and
ix), and the ventral reticulum (indicated by arrows labeled r), the level
of xefiltin mRNA expression (A) was lower than that of XNIF (B) or
NF-L (C). The photomicrographs are taken from the boxed region of
Figure 4E. Scale bar 5 300 μm in C, applies to all panels.
Fig. 9. Xefiltin, XNIF, and NF-L mRNA expression in the spinal
cord (A–C) and a dorsal root ganglion (D–F). In the spinal cord, both
the sensory and motor neurons expressed moderate levels of xefiltin
mRNA(A) and high levels of XNIF (B) and NF-L (C) mRNAs. In dorsal
root ganglion neurons, xefiltin mRNAexpression was near the threshold
of detection (D), whereas XNIF (E) and NF-L (F) mRNAs were
abundant. Also note that in dorsal root ganglion, XNIF mRNA was
found in both large (arrowhead at l) and small (arrowhead at s)
neurons, in contrast to xefiltin and NF-L mRNAs, which were restricted
to large neurons in the periphery of the ganglion. da, dorsal
area of the gray matter; la, lateral area of the gray matter; mn,
motoneuron; n, nerve emanating from the dorsal root ganglion; sn,
sensory neuron; vh, ventral horn. The area depicted in A–C is from the
boxed region of Figure 4F. In D–F, dorsal is to the right and medial is to
the top. The scale bar 5 70 μm in A, also applies to B, C; whereas the
scale bar 5 150 μm in D, also applies to E, F.
