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THE ANATOMICAL RECORD 252:301–310 (1998)
Fine Structure of Three Types
of Olfactory Organs in Xenopus laevis
TOSHIHIRO OIKAWA,1* KEIKO SUZUKI,2 TORU R. SAITO,1
KAZUAKI W. TAKAHASHI,1 AND KAZUYUKI TANIGUCHI2
1Department of Laboratory Animal Science, Nippon Veterinary and Animal Science
University, Tokyo 180, Japan
2Department of Veterinary Anatomy, Faculty of Agriculture, Iwate University,
Iwate 020, Japan
ABSTRACT
There is no report on the fine structure of three types of olfactory organs
in Xenopus laevis. Their functional assignments in olfaction are not yet
established. The fine structure of three types of olfactory organs, olfactory
epithelium (OE), vomeronasal organ (VNO), and middle chamber epithelium
(MCE), was examined in Xenopus laevis by light and electron microscopy. The
olfactory cells of the OE and the sensory cells of the VNO were equipped with
cilia and microvilli, respectively, similar to terrestrial animals that possess
both the OE and the VNO. On the other hand, the sensory cells of the MCE
were classified into two types, the sensory cells with cilia and the sensory cells
with microvilli, like those of the OE in fish. These findings suggest that the
OE and the VNO in Xenopus laevis detect different kinds of odoriferous
molecules in air, whereas the MCE is involved in the perception of odorants in
water. Anat. Rec. 252:301–310, 1998. r 1998 Wiley-Liss, Inc.
Key words: olfaction; Xenopus laevis; light and electron microscopy; olfactory
organ types
In vertebrates, at least two types of olfactory organs can
occur, i.e., olfactory epithelium (OE) and vomeronasal
organ (VNO). They perform functional assignments by
perception of general odorants and pheromonal molecules,
respectively (Abbott, 1984; Fleming et al., 1979; Halpern,
1987; Powers and Winans, 1975; Wysocki, 1979). Phylogenically, the OE exists in all vertebrates from fish to mammals (Andres, 1966; Cushieri and Bannister, 1975a,b;
Graziadei, 1973,1977; Parsons, 1967). On the other hand,
the VNO is absent in fish and first appears in amphibians
as a diverticulum of the nasal cavity (Bertmar, 1981;
Bruner, 1984; Burton et al., 1990; Kolnberger, 1971a). In
reptiles, the VNO is well developed in terrestrial species,
such as lizards and snakes (Kratzing, 1975; Parsons, 1970;
Wang and Halpern, 1980a,b), but it is absent in aquatic
crocodiles (Ciges et al., 1977). In mammals, this organ
varies in its development among species. For example, it is
well developed in rodents (Breipohl et al., 1979; Naguro
and Breipohl, 1982; Oikawa et al., 1994; Taniguchi and
Mochizuki, 1982,1983; Vaccarezza et al., 1981) but is
absent in cetaceans adapted to aquatic life style (MackaySim et al., 1982). Thus, olfactory organs are assumed to
undergo morphological modification to take part in different kinds of olfaction according to the life style of a species.
r 1998 WILEY-LISS, INC.
Amphibians are a good choice to examine the functional
significance of these olfactory systems because of their
adaptation to both aquatic and terrestrial life and because
of the first occurrence of the VNO in them. Among amphibians, South African clawed frogs, Xenopus laevis, are
particularly interesting, because they spend their entire
lives in water and seem to be less adapted to terrestrial life
than other anurans. Recent lectin-histochemical examinations revealed the presence of three different types of
olfactory organs, i.e., OE, VNO, and middle chamber
epithelium (MCE) in Xenopus laevis (Hofmann and Meyer,
1991). These olfactory organs are assumed to perform
functional assignments in olfaction to perceive different
kinds of odoriferous molecules. Their assumed functional
assignments may be represented as differences in their
fine structure, although there have been no reports on the
fine structure of olfactory organs in Xenopus laevis.
In the present study, therefore, the fine structure of
three types of olfactory organs was examined in Xenopus
*Correspondence to: Toshihiro Oikawa, Research Laboratories,
Torii Pharmaceutical Co. Ltd., 1–2-1 Ohnodai, Midori-ku, Chibashi, Chiba 267, Japan.
Received 25 October 1997; Accepted 19 May 1998
302
OIKAWA ET AL.
Fig. 1. Light photomicrograph of the olfactory epithelium (OE; a), the vomeronasal organ (VNO; b), and the
middle chamber epithelium (MCE; c). Each epithelium consists of sensory (olfactory) cells (O), supporting cells
(Sp), and basal cells (B). Se, sensory epithelium. Magnification 3600.
laevis by using light and electron microscopy from the
viewpoint of phylogeny to discuss the significance of the
functional assignments of these olfactory organs.
MATERIALS AND METHODS
South African clawed frogs, Xenopus laevis, were obtained from Hmamatsu Teaching Materials, Co. Ltd. (Shizuoka, Japan) and were kept in a glass aquarium maintained at average temperature of 22°C. A total of 11 adult
frogs of both sexes were used for light and electron
microscopic examinations.
For light microscopy, five frogs were anesthetized by
cooling on ice and sacrificed by cardiac perfusion with
Ringer’s solution (0.0125% NaHCo3, 0.0125% CaCl2,
0.0075% KCl, 0.75% NaCl) followed by Bouin’s solution.
The rostral portion of the upper jaw, including the whole
nasal cavity, was removed, immersed in the same fixative
for additional 24 hr, and decalcified in a mixture of 10%
formic acid and 10% formalin. After decalcification, the
materials were embedded in paraffin by using routine
procedures, sectioned serially at 5 µm in the frontal plane,
and stained with hematoxylin and eosin.
For electron microscopy, six frogs were anesthetized as
described above for light microscopy, and they perfused
with Ringer’s solution followed by a modified Karnovsky’s
solution (2% glutaraldehyde and 2.5% paraformaldehyde
in 0.03 M cacodylate buffer, pH 7.4). The materials were
immersed in the same fixative for 2 hr at 4°C, postfixed in
1% osmium tetroxide in 0.06 M cacodylate buffer for 1 hr at
4°C, and then embedded in Quetol-812 (Nisshin-EM, Tokyo,
Japan) by using routine procedures. Ultrathin sections were
cut on a Reichert-Nissei ULTRACUT-S ultramicrotome (Reichert-Jung, Nussloch, Germany), double stained with uranyl
acetate and lead citrate, and examined with a HITACHI
H-7100 (Tokyo, Japan) electron microscope. Semithin sections were cut at 2µm and were stained with 0.5% toluidine blue for light microscopic observations.
RESULTS
Subdivisions of the Nasal Cavity and
Histological Structure of the Sensory Epithelia
The entire nasal cavity in Xenopus laevis consisted of
three chambers communicating with each other, i.e., the
principal, middle, and inferior chambers. The principal
chamber was the largest and opened anteriorly at the
external naris and posteriorly at the choana leading into
the oral cavity. The middle chamber was situated ventrolateral to the rostral half of the principal chamber and was
subdivided into several recesses. The middle chamber
communicated dorsally with the principal chamber through
Fig. 2. Electron photomicrograph of the OE. Supporting cells (Sp) possess a large number of secretory
granules (SG) in the apical cytoplasm. Magnification 33,000.
Fig. 3. Electron photomicrograph of the apical part of the OE. Olfactory cells (O) are covered with cilia (Ci),
and supporting cells (Sp) are covered with microvilli (Mv). Arrows indicate neurotubules. SG, secretory granule.
Magnification 312,000.
304
OIKAWA ET AL.
Fig. 4. Electron photomicrograph of the middle part of the OE. The
olfactory cell extends its dendrite toward the apical surface. Supporting
cells possess well-developed smooth endoplasmic reticulum (sER) in
their cytoplasm. Magnification 37,000.
Fig. 5. Electron photomicrograph of the basal part of the OE. The
axons of olfactory cells penetrate the basement membrane. A, axon of
olfactory cell; B, basal cell. Magnification 37,000.
Fig. 6. Electron photomicrograph of the basal part of the OE. The
basal cell (B) contacts with the basement membrane and surrounds the
axons of olfactory cells (A). Magnification 37,000.
a narrow slit. The inferior chamber was dorsoventrally
flattened, anteroposteriorly elongated, and situated below
the principal chamber. The inferior chamber ended blindly
at its rostral portion and communicated caudally with the
principal chamber. These three chambers possessed different types of sensory epithelia that were separated from
one another by nonsensory respiratory epithelium. The
principal chamber was lined with the OE on its dorsal-tomedial wall, and the inferior chamber was lined with the
VNO on its medial wall. The middle chamber was lined
medially with the MCE and was different from the OE and
the VNO in the thickness of its epithelium.
Histologically, the OE consisted of olfactory, supporting,
and basal cells (Fig. 1a). Olfactory and supporting cells
were elongated and were arrayed alternatively in the OE,
whereas basal cells were small and were scattered sparsely
on the basement membrane. Oval nuclei of supporting
cells were arranged as a single layer in the upper one-third
of the OE, and round nuclei of olfactory cells accumulated
densely in the lower two-thirds. The VNO and MCE also
consisted of three kinds of cells, i.e., sensory, supporting,
and basal cells. They were conspicuously similar to the OE
in the arrangement of their cells, but they were rather rich
in the number of cells and were thicker than the OE (Fig.
1b,c). The OE, VNO, and MCE were 100 µm, 180 µm, and
140 µm in thickness, respectively. The OE contained
numerous secretory granules in its apical portion and was
equipped with its own associated glands (Bowman’s glands).
The VNO was also equipped with its associated glands
(Jacobson’s glands), whereas the MCE was devoid of such
an associated gland. Nerve fibers issued from the OE and
the VNO to form the olfactory nerve bundle and the
vomeronasal nerve bundle, respectively. Nerve fibers from
the MCE traveled along the olfactory nerve and took part
in the formation of the olfactory nerve bundle.
Fine structure of the OE, VNO and MCE
The olfactory cells of the OE were bipolar neurons, the
same as the sensory cells of the VNO and the MCE.
Dendrites of the olfactory cells protruded their distal ends
beyond the apical surface of adjacent supporting cells to
form olfactory vesicles with long cilia on their apical
surface (Fig. 2). These cilia were embedded in the thick
mucous sheet on the surface of the OE. The olfactory cells
contained numerous neurotubules, ciliary basal bodies,
STRUCTURE OF OLFACTORY ORGANS IN XENOPUS
305
Fig. 7. Electron photomicrograph of the vomeronasal organ (VNO). The apical cytoplasm of the supporting
cells (Sp) was occupied by a large number of mitochondria. Se, sensory cell. Magnification 33,000.
and mitochondria in dendrites (Fig. 3) and contained
rough endoplasmic reticulum (rER), Golgi apparatus, and
lysosomes in the perikarya (Fig. 4). The cytoplasm of the
olfactory cell tapered proximally to the nucleus and penetrated the basement membrane like the axon (Fig. 5).
Columnar supporting cells of the OE were equipped with
short microvilli on their apical surface (Fig. 3). These cells
were characterized by a large number of vesicles with
moderate electron density in the apical cytoplasm. These
vesicles corresponded to the secretory granules that were
observed under light microscopy in the OE. The perinuclear cytoplasm was occupied mostly by excessively
developed smooth endoplasmic reticulum (sER) and also
contained mitochondria, Golgi apparatus, rER, and bundles
of microfilaments (Fig. 4).
The basal cells of the OE were small with scanty
cytoplasm and were almost the same as those of the VNO
and the MCE in their ultrastructural features. They
contained a few mitochondria and other, poorly developed
cytoplasmic organelles, and they often extended their
cytoplasm to surround the axons of olfactory cells (Fig. 6).
On the other hand, the dendrites of the sensory cells of
the VNO protruded slightly into the lumen and were
equipped with a large number of long microvilli on their
apical surface (Fig. 7). These microvilli were in close
contact with mucous substance, which sparsely covered
the VNO. These sensory cells contained centrioles in
dendrites (Fig. 8) and sometimes displayed spirally arranged neurofilaments surrounded by well-developed sER
in perikarya (Fig. 9). The other ultrastructural features
were similar to those of olfactory cells of the OE.
The apical surface of supporting cells of the VNO was
covered with short microvilli in addition to long cilia with
basal bodies and striated rootlets (Fig. 8). The apical
cytoplasm of the supporting cells was occupied by a large
number of mitochondria (Fig. 7), whereas the perinuclear
cytoplasm contained the poorly developed rER and free
ribosomes small in numbers (Fig. 9).
The sensory cells of the MCE were divided into two types
according to their apical morphology (Fig. 10). The first
type of sensory cell (nonciliated sensory cell) was dominant
and possessed microvilli on its apical surface and centrioles in its dendrites, similar to the sensory cells of the VNO
(Figs. 11, 12). The second type of sensory cell (ciliated
sensory cell) was covered with several cilia, similar to the
olfactory cells of the OE, but formed no structure similar to
the olfactory vesicles of the OE (Figs. 11, 12). Mucous
substance was encountered scarcely on the surface of the
MCE. The other ultrastructural features of both types of
sensory cells were in similar to those of olfactory cells of
the OE (Fig. 13).
The supporting cells of the MCE were also classified into
two types, i.e., ciliated and nonciliated supporting cells
(Figs. 10, 11). Ciliated supporting cells resembled closely
the supporting cells of the VNO in their apical morphology,
long cilia, and short microvilli on their apical surface.
Nonciliated supporting cells protruded into the lumen and
bore several short microvilli on their apical surface. This
306
OIKAWA ET AL.
Fig. 8. Electron photomicrograph of the apical part of the VNO.
Sensory cells (Se) are covered with cilia (Ci), and supporting cells (Sp) are
covered with microvilli (Mv). Arrows indicate neurotubules, and arrowheads indicate centrioles. Magnification 312,000.
Fig. 9. Electron photomicrograph of the somata of the sensory cell of
the VNO. Spirally arranged neurofilaments (Nf) are developed well in the
perinuclear cytoplasm of the sensory cells. G, Golgi apparatus. Magnification 37,000.
type of cell contained concentrically arranged sER in the
supranuclear cytoplasm (Fig. 14). The other cytoplasmic
organelles, such as mitochondria, rER, and Golgi apparatus, were developed moderately in both ciliated and nonciliated supporting cells.
nostril that closed the principal chamber under water,
allowing water exchange between the middle and inferior
chambers, whereas this flap closed the middle and inferior
chambers when outside of the water to enable the principal chamber to make contact with air. More recently,
Hofman and Meyer (1991) distinguished three sets of
olfactory systems, the MCE-ventral part of the MOB
system, the VNO-AOB system, and the OE-dorsal part of
the MOB system, according to their different in binding
affinities to soybean agglutinin (SBA). They speculated
that SBA-positive systems, the MCE-ventral part of the
MOB system and the VNO-AOB system, were involved in
the detection of nonvolatile water-born odors, whereas the
SBA-negative, OE-dorsal part of the MOB system was
involved in the detection of volatile air-born odors. Franceschini et al. (1992) also identified the same three olfactory systems by using SBA, but they did not agree with the
hypothesis of Hofman and Meyer. Although the functional
significance of three olfactory systems has not been established fully to date, at least it can be said that, in Xenopus
laevis, the MCE plays a primary role in olfaction as well as
the OE and the VNO.
In the present study, details of the fine structure of the
OE and the VNO in Xenopus laevis agreed well with those
reported previously in anurans (Bloom, 1954; Burton,
1985; Franceschini et al., 1991; Kolnberger, 1971a,b; Mair
et al., 1982; Menco, 1980; Reese, 1965; Scalia, 1976;
DISCUSSION
In general, vertebrates possess two different types of
olfactory organs, the OE and the VNO. They project
centrally through olfactory and vomeronasal nerves to the
main olfactory bulb (MOB) and the accessory olfactory
bulb (AOB), respectively, and they constitute two distinct
olfactory systems, the OE-MOB system and the VNO-AOB
system (Barber and Raisman, 1974; Salazar et al., 1992;
Scalia and Winans, 1975). The OE-MOB system performs
the usual olfactory perception functions to respond to
general odorants. On the other hand, the VNO-AOB
system is thought to be specialized for the perception of
pheromonal substances and to be involved in reproductive
and/or social behaviors (Abbott, 1984; Fleming et al., 1979;
Halpern, 1987; Powers and Winans, 1975; Saito et al.,
1995; Wysocki, 1979). Thus, these two olfactory systems
seem to play different roles in olfaction.
In Xenopus laevis, the presence of three distinct region
of olfactory mucosa was acknowledged by early authors
(Altner, 1962; Föske, 1934). With regard to the significance
of three nasal chambers, Altner described a skin flap in the
Fig. 10. Electron photomicrograph of the middle chamber epithelium (MCE). Some sensory cells are
covered with cilia and others are covered with microvilli. nSe, nonciliated sensory cell. Magnification 33,000.
Fig. 11. Electron photomicrograph of the apical part of the MCE. The
ciliated supporting cell (cSp) is covered with long cilia with basal bodies
and striated rootlets. The nonciliated supporting cell (nSp) protrudes into
the lumen and bears several short microvilli. Magnification 38,000.
Fig. 12. Electron photomicrograph of the apical part of the MCE.
Centrioles are encountered in the cytoplasm of the nonciliated sensory
cell (nSe). Arrows indicate neurotubules, and arrowheads indicate centrioles. Ci, cilia; Mv, microvilli. Magnification 312,000.
308
OIKAWA ET AL.
Fig. 13. Electron photomicrograph of the somata of the sensory cells
of the VNO. These sensory cells contain mitochondria, rough endoplasmic reticulum, and Golgi apparatus in the cytoplasm as the olfactory cells
of the olfactory epithelium. Magnification 37,000.
Fig. 14. Electron photomicrograph of the supporting cells and dendrites of the sensory cells of the MCE. The smooth endoplasmic reticulum
(sER) is arranged concentrically in the perinuclear cytoplasm of the
supporting cell. Magnification 37,000.
Taniguchi et al., 1996). The olfactory cells of the OE were
covered with cilia, and the sensory cells of the VNO were
covered with microvilli in Xenopus laevis, similar to other
species that possess both the OE and the VNO. Because
cilia and microvilli are recognized as receptor sites of
olfaction (Graziadei, 1977; Halpern, 1987), the present
findings seem to suggest that, ultrastructurally, the OE
and the VNO are active in function and perceive general
and pheromonal molecules, respectively, as in other species.
The supporting cells of the OE were covered with
microvilli and were characterized by a large number of
secretory granules in their apical cytoplasm. These granules were also observed in the supporting cells of the OE of
other amphibians, fish, lizards, and birds but not in
mammals (Getchell and Getchell, 1992). In contrast, the
supporting cells of the VNO possessed cilia but no secretory granules in the present study, although they are
generally reported to possess microvilli but to lack cilia in
mammals (Adams, 1986; Adams and Wiekamp, 1984;
Bhatnagar et al., 1982; Kratzing, 1970; Loo and Kanagasuntheram, 1972; Luckhaus, 1969; Oikawa et al., 1994;
Seiffert, 1971; Taniguchi and Mikami, 1985; Taniguchi and
Mochizuki, 1982,1983; Taniguchi et al., 1992; Vaccarezza
et al., 1981). Franceschini et. al. (1991) found ciliated
supporting cells in the VNO of another frog, Rana esculenta, and hypothesized that these cilia play a role in the
transmission of odorants to the VNO in place of the
vomeronasal pump that is observed in some mammals. In
the present study, cilia of the supporting cells of the VNO
were equipped with basal bodies and long rootlets. These
findings may lead to a reconfirmation of their hypothesis.
On the other hand, there is no report on the fine
structure of the MCE in Xenopus laevis. In the present
study, the sensory cells of the MCE were classified into two
types according to their apical morphology. One type of cell
was covered with cilia, similar to those of the OE, and the
other type was covered with microvilli, similar to the VNO.
In fish that lack the VNO, some sensory cells of the OE are
reported to be covered with cilia, whereas others are
covered with microvilli (Breucker et al., 1979; Ichikawa
and Ueda, 1977; Moran et al., 1992; Thommesen, 1983;
Yamamoto and Ueda, 1977; Zeiske et al., 1976). Therefore,
there seems to be a possibility that the primitive OE of fish
remained in the middle chamber of Xenopus laevis as the
MCE to detect odoriferous molecules in water and that it
generated two kinds of olfactory organs, the OE and the
VNO, during its phylogenetical development. Furthermore, the MCE lacked its own associated gland, like the
OE of fish (Getchell and Getchell, 1992; Graziadei, 1973),
and was barely covered by mucous substances on its apical
surface. The secretory substances on the free surface of
olfactory organs were essential for the olfactory perception
of olfactory organs in terrestrial life, because odorants
STRUCTURE OF OLFACTORY ORGANS IN XENOPUS
must be dissolved in the mucous layer covering receptor
sites of olfactory organs to be perceived as olfactory stimuli
(Graziadei, 1977; Halpern, 1987). In fish, because odorants
are dissolved in the surrounding water, the OE does not
have to be covered with secretory substances. In terrestrial
animals, Bowman’s glands and Jacobson’s glands seem to
appear in the OE and the VNO, respectively, to cover the
olfactory organs and to dissolve the odorants in air in
secretory substances. The lack of associated glands in the
MCE seems to suggest that the MCE is involved in
olfactory perception in water. Because Xenopus laevis
remained in aquatic environments after the commencement of respiration with the lung, the primitive OE of fish
may be retained in the middle chamber.
In conclusion, the present findings suggest that, ultrastructurally, the OE and the VNO in Xenopus laevis are
similar in their olfactory functions to those of other species
and detect different kinds of odoriferous molecules in the
air, whereas the MCE is involved in the perception of
odorants in water when the frog stays under water.
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