Chem. Senses 27: 803-810,
2002
© Oxford University Press 2002
Aggregation of F-Actin in Olfactory Glomeruli: a Common Feature of Glomeruli Across Phyla
ko KuduzPhysiologisches Institut, Universität Göttingen, Humboldtallee 23, 37073 Göttingen, Germany
Correspondence to be sent to (current address): Wolfgang Rössler, Biozentrum der Universität, Zoologie II, Am Hubland, 97074 Würzburg, Germany. e-mail: roessler{at}biozentrum.uni-wuerzburg.de
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Abstract |
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Using fluorophore-conjugated phalloidin, we show that filamentous (F)-actin is strongly aggregated in olfactory glomeruli within primary olfactory centers of vertebrates and insects. Our comparative study demonstrates that aggregation of F-actin is a common feature of glomeruli across phyla, and is independent of glomerular architecture and/or the presence or absence of cellular borders around glomeruli formed by neurons or glial cells. The distribution of F-actin in axonal and dendritic compartments within glomeruli, however, appears different between vertebrates and insects. The potential role of the actin-based cytoskeleton in synaptic and structural plasticity within glomeruli is discussed.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Primary olfactory centers in the brains of vertebrates as well as most advanced invertebrates typically are compartmentalized in spheroidal areas of dense synaptic neuropil called olfactory glomeruli. Recent evidence suggests that glomeruli represent functional units in olfactory information processing (Hildebrand and Shepherd, 1997
; Valverde,
1999; Xu et al.,
2000). In vertebrates, glomerular synapses undergo a lifelong
turnover, resulting from continuous regeneration of axons from olfactory
receptor neurons (ORNs) that are constantly replaced by basal cells in the
olfactory epithelium (Wolff and Missler,
1992; Farbman,
1994; Astic and Saucier,
2001). In insects, individual glomeruli exhibit a high degree of
plasticity during post-embryonic development, as well as activity-dependent
structural changes during adult life
(Winnington et al.,
1996; Sigg et al.,
1997; Rössler et
al., 1999a). Thus, the glomerular synaptic neuropil in both
vertebrates and insects is characterized by a high degree of synaptic and
structural plasticity. To further understand the organization and function of
glomeruli, a comparative approach to structural, molecular and physiological
properties of olfactory glomeruli is particularly promising, and should lead
to the discovery of the most essential features of olfactory glomeruli.
Despite similarities in some general features, anatomical and cellular
attributes of individual glomeruli and the organization of the entire array of
glomeruli can differ markedly across species. For example, in mammals and
insects, glomeruli were shown to be very distinct and clearly separated by
glomerular borders formed by periglomerular neurons and/or glial cells, which
also play an important role during development
(Tolbert and Oland, 1990;
Treolar et al.,
1999). In other species, especially in lower vertebrates, regular
cellular borders around glomeruli are absent, and the glomerular synaptic
neuropil appears much less defined compared with the conditions in mammals
(Byrd and Burd, 1991;
Nezlin and Schild, 2000).
Despite these obvious differences in glomerular organization, the olfactory
system of lower vertebrates, e.g. fish, was shown to perform with high
sensitivity in olfactory discrimination tasks and expresses a remarkable
regenerative capacity (Zippel,
2000).
Here we show that glomeruli in the primary olfactory centers of various species of vertebrates and insects are characterized by strong aggregation of filamentous (F)-actin, independent of the presence or absence of periglomerular borders and differences in the general organization of the glomerular array. The results show that fluorophore-conjugated phalloidin reliably labels glomeruli in a broad range of animal species, allowing distinct mapping of glomeruli even in species that show a very loose or no organization of glomeruli in classical histological preparations. We conclude that distinct aggregation of F-actin in olfactory glomeruli is a fundamental feature of glomeruli across phyla and could play an important role in synaptic and structural plasticity within primary olfactory centers.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Animals and tissue preparation
We used the following species: Xenopus laevis [tadpoles, stages
49-54 (Nieuwkoop and Faber,
1956)], axolotl (Ambystoma mexicanum, from Dr D.L. Meyer,
Göttingen, Germany), goldfish (Carassius auratus, kindly
provided by Dr H.P. Zippel, Göttingen, Germany), tobacco hawkmoth
(Manduca sexta, kindly provided by Dr J. Schachtner, Marburg,
Germany), giant silkmoth (Antherea polyphemus, kindly provided by Dr
E. Kaissling, Seewiesen, Germany), honeybee (Apis mellifera, kindly
provided by Dr J. Rybak, Würzburg, Germany), three species of ant (kindly
provided by Drs. J. Liebig and B. Hölldobler, Würzburg, Germany) and
cricket (Gryllus bimaculatus, laboratory colony, Dr Schürmann,
Göttingen) for the experiments. Dr M. Rickmann (Göttingen, Germany)
provided a perfusion-fixed rat brain and Dr O. Stiedl (Göttingen) a
perfusion-fixed mouse brain (strain C57 BL/6NCrlBR). All animals were
anesthetized and killed using appropriate methods. After dissection, the
brains were immediately transferred to cold solution of 4% formaldehyde in
phosphate buffered saline (PBS), pH 7.2 or 7.4, and fixed over night at
4°C. Brains were washed at least three times in PBS, embedded in 5% low
melting point agarose (Agarose type II, no. 210-815; Amreso, Inc., Solon, OH),
sectioned at 50-300 µm on a Vibratome (Leica VT 1000S) or processed as
whole mounts and sectioned after the staining procedures.
Labeling with phalloidin, immunocytochemistry and nuclear staining with propidium iodide
Sections were stained with Alexa Fluor 488 phalloidin (A-12379, Molecular Probes, Eugene, OR). We obtained the best results when sections were preincubated (1 h at room temperature) in 0.1 M PBS with 0.2% Triton-X and 2% normal goat serum (NGS; no. 191356, ICN Biomedicals GmbH, Orsay, France). Preincubation with Triton and NGS was not always essential and should be tested for any particular species. We observed a reduction in background after preincubating with NGS. Free-floating agarose sections or whole brains were incubated in 0.2 units of Alexa Fluor 488 phalloidin (1 µl methanolic stock solution in 200 µl PBS with 2% NGS) initially for 2-4 h at room temperature (RT), and subsequently overnight or for 2 days at 4°C on a shaker.
Some preparations were double-labeled with antibodies to synaptic proteins.
Antibodies to Synapsin (monoclonal, derived from mouse) were kindly provided
by Dr E. Buchner (Biozentrum, University of Würzburg, Germany)
(Klagges et al.,
1996), antibodies to synaptophysin (polyclonal G113/p38 frog,
derived from rabbit) were generously supplied by Dr R. Jahn (Max Planck
Institute for Biophysical Chemistry, Göttingen, Germany)
(Jahn et al. 1985).
Sections were washed in PBS with 0.2% Triton X-100 (PBST), and nonspecific
binding was blocked with 2% NGS in PBST for 1 h at RT. Then, the tissue was
incubated overnight at 4°C with anti-Synaptophysin (1:1000) or
anti-Synapsin (1:50), diluted in PBS with 2% NGS, together with phalloidin
(see above). Sections were subsequently washed with PBS, and Alexa 488- or
546-conjugated goat anti rabbit or anti mouse secondary antibodies (A 11008
and A 11003; Molecular Probes) were applied at a dilution of 1:250 in 1%
NGS/PBS for 2h at RT. The secondary antibodies were washed in five changes of
PBS.
To stain glial and neuronal cell nuclei, sections (or whole mounts) were incubated for 15-30 min in 25 µg/ml propidium iodide (P-1304, Molecular Probes) in PBS. Finally, preparations were washed in at least five changes of PBS, transferred in 60% glycerol/PBS for at least 1 h, and finally mounted on slides for confocal microscopy in 80% glycerol/PBS.
Laser scanning confocal microscopy
Preparations were viewed using a laser-scanning confocal microscope (Zeiss LSM 510) attached to an inverted microscope (Zeiss Axiovert 100M). A 15 mW argon ion and a 1 mW helium/neon laser were used as light sources. Single optical sections as well as series of sections were imaged at intervals of 0.5-5µm through the depth of the thick sections. They were saved as single optical images or three-dimensional stacks. Two-dimensional projections were generated for each channel and merged with the use of pseudocolors. Where needed, the digitized images were modified only to enhance contrast, to merge images from consecutive sections of the same preparation, or to form montages of images from adjacent regions. Image processing and labeling of figures were performed with one or more of the following programs: Zeiss imaging software (Zeiss, Göttingen, Germany), Corel Photopaint and Corel Draw (Corel Corporation, Ottawa, Ontario, Canada).
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Glomerular aggregation of F-actin: comparison among species
In all species we investigated, olfactory glomeruli became brightly labeled
after phalloidin treatment (Figures
1 and
2). The concentration of
phalloidin within glomeruli was high compared with the surrounding tissue. In
lower and higher vertebrates and in all insects we investigated, staining was
present across the entire volume of individual glomeruli. Only in some cases
did we observe differences in the staining intensity of individual glomeruli
(see below). Labeling of cell nuclei with propidium iodide demonstrates that
glomeruli in the olfactory bulb (OB) of Xenopus laevis
(Figure 1A,B) and Ambystoma
mexicanum (Figure 1E,F)
are not surrounded by a regular border of periglomerular somata of neurons or
glial cells [for X. laevis, see also
(Nezlin and Schild, 2000)].
The distribution of phalloidin, even in these cases, shows a distinct
aggregation of F-actin in a glomerular pattern. In both species, classical
histological techniques show either a very loose glomerular organization
[Xenopus (Byrd and Burd,
1991)] or the complete absence of a glomerular pattern
[Ambystoma (D.L. Meyer, unpublished data)]. F-actin aggregations in
Ambystoma were more separated compared with Xenopus, but
glomeruli were easy to detect in both species
(Figure 1A,B,E,F). In X.
laevis, more homogeneous labeling at lower intensity was present in the
plexiform layer of the OB (Figure
1A,B). In the accessory olfactory bulb of Xenopus laevis,
too, distinct glomerular aggregation of F-actin was present, but glomeruli
were significantly smaller and more irregular in shape
(Figure 1C). In the OB of the
goldfish (Figure 1G), glomeruli
became clearly labeled, but in some areas of the OB glomeruli were less
distinct compared with the conditions in amphibians, and especially compared
with the mammalian OB. In the rat OB, the entire volume of glomeruli was
brightly labeled up to the border formed by periglomerular neurons, and
homogeneous staining was present in the plexiform layer
(Figure 1H). In all
vertebrates, blood vessels were stained with phalloidin, but were easy to
distinguish from neuronal structures. The picture was very similar in the
mouse OB, where the staining intensity was highest in the glomeruli and showed
decreasing levels in the external and internal plexiform layers
(Figure 1L). Taken together,
phalloidin labeling of olfactory glomeruli showed great similarities across
various species of lower and higher vertebrates, despite significant
differences in glomerular shape and volume, and independent of the presence or
absence of cellular borders around glomeruli.
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In insects, too, phalloidin labeling indicates high concentration of
F-actin within glomeruli (Figure
2). As in vertebrates, the entire volume of all glomeruli was
filled with labeled neuronal branches, and staining was absent from
interglomerular spaces. In females of the moth Manduca sexta,
individual identified glomeruli, like the two large, lateral female-specific
glomeruli (LFGs) at the entrance of the antennal lobe (AL), could easily be
recognized [Figure 2A; for
comparison see (Rössler et al.,
1998,
1999a)]. The same was true for
the large glomeruli of the macro-glomerular complex in the AL of male moths
and for other identified glomeruli (data not shown). In the silkmoth
Antherea polyphemus, the pattern was very similar to the conditions
in M. sexta (data not shown). In both species of moths, a prominent
border formed by glial somata surrounds individual glomeruli
[Figure 2C; see also
(Tolbert and Hildebrand, 1981;
Oland and Tolbert, 1996)].
Phalloidin labeling was completely absent from the glial cells forming the
border (Figure 2C) and from
peripheral glial cells within the antennal (olfactory) nerve
(Figure 2B).
In two examples of hymenopteran insects, the honeybee (Apis mellifera) and the ponerine ant (Harpegnathos saltator), glomeruli were not surrounded by glial somata, but also in these cases phalloidin labeling was concentrated in glomeruli and absent from interglomerular spaces (Figure 2D,E,H). The example of the ALs in the ant H. saltator demonstrates that projections from stacks of confocal images allow detailed analyses of the organization and bilateral symmetry of the entire glomerular array, even in small species of insects (Figure 2H).
Distribution of F-actin within glomeruli
To look more closely into the compartmentalization of F-actin within the
glomeruli, we performed double-labeling experiments using antibodies to the
synaptic-vesicle proteins synaptophysin and synapsin. Both proteins are
associated with synaptic vesicles and are restricted to presynaptic
compartments (Jahn et al.,
1985; Klagges et al.,
1996). In the accessory bulb of Xenopus laevis
(Figure 1C,D) and in the main
OB of the rat (Figure 1J,K), at
lower magnification, the distribution of synaptophysin- and
synapsin-immuno-reactivity (IR) and that of phalloidin staining exhibit an
almost similar pattern. At higher magnification, however, a mismatch
synaptic-protein IR and F-actin staining is visible. This is most evident in
peripheral regions of the less densely packed glomeruli in the OB of X.
laevis (Figure 1M). This
indicates that F-actin is located predominantly in postsynaptic dendritic
compartments, which is further supported by the fact that in all vertebrates
staining was completely absent from axons in the nerve layer.
The general distribution of F-actin in pre- and post-synaptic compartments
appears to be different in insects. In contrast to vertebrates, in all insects
we observed light phalloidin labeling along olfactory receptor axons within
the antennal (olfactory) nerve, in addition to strong labeling within the
glomeruli (Figure 2B,D,F,H).
The dendritic branches and processes of neurons and glial cells within the
central core of the ALs of insects were not labeled at all
(Figure 2A,D,H), Axonal
staining was especially prominent in an ORN-axon tract that crosses the
central core of the AL in the honeybee
(Figure 2D). The axonal
staining pattern, as shown, for example, in Manduca sexta
(Figure 2B), can be very useful
in the visualization of the trajectories of axon bundles within the glia-rich
receptor axon sorting zone at the entrance of the olfactory nerve
(Rössler et al.,
1999b). In the honeybee, synapsin-IR and phalloidin labeling show
a differential localization even at lower magnification
(Figure 2F,G). Synapsin was
concentrated exclusively within the glomeruli whereas phalloidin labeling was
also present along the axon tracts of receptor neurons. To further explore the
compartmentalization of F-actin within glomeruli, we traced projection neurons
(PNs) intracellularly with rhodamin-coupled dextrans and stained sections with
phalloidin (Figure 2J). The
example shown in the cricket demonstrates that phalloidin labeling showed only
very little overlap with the dendritic branches of PNs. Phalloidin only
labeled branches with very fine profiles. A partial overlap, however, with the
very fine dendritic tips cannot be excluded, but in the majority of PN
dendrites F-actin appears to be absent. Taken together, the results indicate
that, in contrast to vertebrates, in insects F-actin appears to be localized
predominantly in presynaptic axonal compartments within the glomeruli.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Our results demonstrate that high concentration of F-actin represents a fundamental feature of olfactory glomeruli in species across a broad range of phyla. The compartmentalization of F-actin in axonal and dendritic elements, however, seems to differ in vertebrates and insects. Strong accumulation of F-actin within the glomerular synaptic neuropil indicates that the actin-based cytoskeleton may play an important role in synaptic and structural plasticity within glomeruli (Matus, 1999
;
Morales et al., 2000;
De Camilli et al.,
2001). In addition, our results show that phalloidin-labeling
reveals the intraglomerular cytoarchitecture at excellent resolution and
allows complete mapping of the entire glomerular array in a great variety of
species. This will be especially useful in species for which specific
molecular markers are not available and/or neuronal tracing techniques are
difficult to apply.
Phallotoxins, isolated from the mushroom Amanita phalloides, are
bicyclic peptides that bind the various isoforms of F-actin with high affinity
(Wieland, 1987;
Haugland, 1996). Because of
their small size and low molecular weight (
800 daltons), phalloidin
conjugates penetrate easily into the tissue, thus allowing staining of thick
sections or whole mount preparations for confocal microscopy. In recent years,
various efforts were made to provide a more or less complete spatial map of
olfactory glomeruli within primary olfactory centers [e.g. in the honeybee
Apis mellifera (Flanagan and
Mercer, 1989; Galizia et
al., 1999); in the fruit fly Drosophila (Laissue
et al., 1990); in the moth Manduca sexta
(Rospars and Hildebrand,
2000); and in the zebrafish Brachydanio rerio
(Baier and Korsching, 1994)].
Series of histological sections, tracing of the olfactory nerve or
immunocytochemistry tools were used to gain information about the spatial
organization of glomeruli. However, in many `non-model' species
immunocytochemical markers often are not at hand. In other cases, anatomical
features or the small size of animals exclude conventional tracing techniques.
In addition, mass fills of axons or dendrites can be incomplete, and glomeruli
may easily be missed. Phalloidin labeling therefore provides a powerful tool
for spatial mapping of glomeruli, and allows future studies on the
organization and structural plasticity of olfactory glomeruli.
F-actin isoforms are highly conserved across species, and in neurons, actin
microfilaments are most abundant in presynaptic terminals, dendritic spines,
growth cones and the subplasmalemmal cortex
(Berl et al., 1973;
Lee and Cleveland, 1996;
Matus, 1999;
Capani et al., 2001;
De Camilli et al.,
2001). In all species we investigated, phalloidin binds with high
affinity to structures across the entire volume of individual glomeruli. The
results indicate that in insects F-actin predominantly is localized in
terminals of olfactory receptor axons whereas in vertebrates it is absent from
axons and appears to be mostly aggregated in dendritic terminals of olfactory
bulb neurons. To determine the precise distribution at densely packed
glomerular synapses, future investigations at the ultrastructural level are
needed.
F-actin was shown to play an important role during neuronal growth, and
there is strong evidence for a role of the actin-based cytoskeleton in the
regulation of synaptic vesicle dynamics
(Morales et al.,
2000; de Camilli et
al., 2001). Furthermore, studies in vertebrates have shown
that most ion-channel-linked glutamate receptors at spine synapses are closely
associated with the actin cytoskeleton, and therefore indicate an important
role of F-actin in the regulation of postsynaptic plasticity and spine
dynamics [reviewed by Matus (Matus,
1999)]. A possible reason for the difference in the distribution
of F-actin in axonal and dendritic compartments between insects and
vertebrates may be the absence of dendritic spines in insect glomeruli. Thus,
the mechanisms of actin-based synaptic and structural plasticity within
glomeruli may differ between insects and vertebrates.
Aggregation of F-actin within glomeruli is very distinct, even in species
that lack periglomerular cellular borders like in Xenopus laevis
tadpoles, the axolotl and goldfish, resulting in a very loose appearance of
the glomerular organization in histological preparations
(Byrd and Burd, 1991;
Meyer et al., 1996;
Nezlin and Schild, 2000). Also
in these cases, F-actin is clustered in a glomerular fashion and almost
completely absent from interglomerular spaces, even though these spaces are
occupied by bypassing axons and dendrites from other neurons.
In summary, our results demonstrate a consistently high concentration of F-actin in olfactory glomeruli across a broad range of species, indicating that this is an essential feature of olfactory glomeruli that is most likely related to a high degree of synaptic and structural plasticity within the glomerular neuropil of primary olfactory centers.
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Acknowledgments |
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This paper was written in memory of Dr D.L. Meyer. The authors thank Gudrun Federkeil, Malu Obermayer, Mrs Knierim and Alexandra Kneissl for excellent technical assistance, and Drs E. Buchner and R. Jahn for generous supply with antibodies. This work was supported by the DFG, SFB 406, A12.
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Accepted August 23, 2002
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