Download Ultrastructure of cell types of the olfactory epithelium in a catfish

J. Biosci., Vol. 22, Number 2, March 1997, pp 233– 245. © Printed in India.
Ultrastructure of cell types of the olfactory epithelium in
a catfish, Heteropneustesfossilis (Bloch)
N C DATTA* and SHOVAN BANDOPADHYAY
Fishery and Ecology Research Unit, Department of
Calcutta, 35, Ballygunge Circular Road, Calcutta 700019, India
Zoology,
University
of
MS received 21 May 1996; revised 19 December 1996
Abstract.
Transmission electron microscopical study of olfactory epithelium of
a mud-dwelling catfish, Heteropneustes fossilis (Bloch) shows receptor, supporting,
goblet and basal cells. The receptor cells are of ciliated and microvillous type. Both
ciliated and microvillous receptor cells are provided with olfactory knob. The dendrite
of all the receptor cells bears many longitudinally arranged microtubules. Occurrence
of the rod cell and its function is quite debatable. Specialized juctional complexes
between the receptor and adjacent cells are clearly noted. The supporting cells are both
ciliated and nonciliated. The ciliated supporting cells are responsible for water
ventilation in the olfactory chamber as well as in the inter-lamellar spaces. This
facilitates better perception of odours by the receptor cells. In addition to providing
mechanical support to other cells, the nonciliated supporting cells also have a secretory
function which is evident from the present study. The different stages of maturity of
goblet cells are well documented. The presence of white cells in the olfactory
epithelium is a very rare finding.
Keywords. Catfish; olfactory epithelium; receptor cell; rod cell; white cell.
Introduction
Heteropneustes fossilis (Bloch) is primarily a mud dwelling fish of the freshwater bodies
of Indian subcontinent. D ue to this peculiar habitat, its dependence on chemoreceptors
is obvious.
Literature survey indicates that a number of workers (Trujillo Cenoz 1961; Bannister 1965; Kleerekoper 1969; Theisen 1972; Jakubowski 1981; Zielinski and H ara 1992;
Zeiske et al 1992; Singh et al 1995) have described different cell types of the olfactory
epithelium in a number of fishes through the transmission electron microscopy (TEM).
The present study portrays the Ultrastructure of the cell types in the olfactory
epithelium of H. fossilis and an attempt has also been made to ascribe the possible
function of the cells.
Materials and methods
Previously acclimatized in the laboratory, adult specimens of H. fossilis (OrderSiluriformes, Family Heteropneustidae) measuring from 15-20 cm long were taken
*Corresponding author.
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N C Datta and Shovan K Bandyopadhyay
for TEM study. After dissecting out the olfactory rosettes, the lamellae were severed
into small pieces and fixed in 2.5% ice cold glutaraldehyde buffered at 7.4 pH
with 0·1 phosphate buffer for two hours. After rinsing with the same buffer the
tissues were further fixed in 1% OsO4 in 0·1 phosphate buffer (pH 7·4) for l h
at 4°C. During dehydration, pre staining of the tissues was done in saturated
solution of uranyl acetate in 70% alcohol for 15 min. Ultrathin sections of embedded
tissues were cut with a diamond knife on LKB Nova ultrotome and were then contrasted with uranyl acetate for 5 min and lead citrate for 6 min. The sections were
examined in JEOL 100 CX transmission electron microscope operated at emissive
mood at 60 KV. The details of the structural components of various cell types were
then studied and described.
3. Results
The olfactory epithelium of H. fossilis is pseudostratified and therefore the receptor,
supporting, goblet and basal cells are not aligned in the olfactory mucosa.The
unusual white cells (Evans et al 1982) are scantly distributed at the middle position
of the epithelium. The receptor cells are morphologically differentiated into ciliated
and microvillous type. A peculiar rod cell is also present sporadically in the mucosa.
Two types of supporting cells are distinguished: nonciliated and ciliated type
(figure 1).
3.1 Receptor cell
The receptor cells are typical bipolar neurons. The free surface of the dendrite bulges
out to form a small flask shaped terminal swelling called the olfactory knob (figure 2),
which is more prominent in the microvillous neuron (figure 3). The microvilli on the
olfactory knob range from 0·1 um to 0·15 µm in diameter. The olfactory knob of ciliated
receptor cell distally bears cilia which show the typical 9 + 2 arrangement of the
microtubules. in cross section (figure 2). The diameter of the cilia is approximately
0·3 µm to 0·4 µm. The basal body of the cilia is clearly discernible. The length of both
cilia and microvilli could not be measured because full length of them were not
available in the section.
The dendrites of the receptor cells are elongated and their width usually increase
gradually towards the nucleus. The dendritic regions are mostly separated from each
other by the supporting cells. The axon of the receptor cells does not extend towards the
basement membrane, instead it passes obliquely through the intercellular spaces
between the supporting and basal cells (figure 1). The dendrite contains some
logitudinally arranged microtubules (figure 6). The nuclei of the receptor cells are
usually deeply stained and situated in the lower third of the epithelium towards
basement membrane. These are oval to elongated in shape (figure 7). The heterochromatin material remains scattered and also distributed along the periphery of the
nucleus. Mitochondria are mostly aggregated at the apical part of the dendrite. The
shape varies from round to oblong. Free ribosomes and golgi bodies are observed. The
junctional complex appears to be zonula occludens and present between receptor and
adjacent supporting cells (figures 2,3).
Ultrastructure of olfactory epithelium of H. fossilis
235
Figure 1. H. fossilis. A diagrammatic view of the olfactory epithelium showing different types
of cell, bb, basal body; be, basal cell; bm, basement membrane; c, cilium; cf, collagen fibre; crc,
ciliated receptor cells; esc, ciliated supporting cell; edp, electron dense particle; eov, electron
opaque vesicle; g, golgi complex; gc, goblet cell; id, interdigitation; jc, junctional complex; m,
mitochondria; mrc, microvillous receptor cell; mt, microtubules; mv, microvillous; nsc,
nonciliated supporting cell; ok, olfactory knob; r, rod; rer, rough endoplasmic reticulum; re,
rod cell; ser, smooth endoplasmic reticulum; sv, secretory vesicle; tm, translucent microvesicles; we, white cell.
3.2
Rod cell
The rod cell is occasionally observed in the sensory area of the lamellae. A firm rod like
cilia occupies almost the entire free margin (figure 4) of the cell. The base of the rod is
wide and the diameter is about 1·15 µm. The rod gradually becomes pointed towards
the free end.The length of the rod is 8·15 µm approximately. It contains a number of
parallely oriented microtubules along its long axis (figure 5). The arrangement of these
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N C Datta and Shovan K Bandyopadhyay
Figures 2-5. (2) TEM of surface region of the olfactory epithelium in longitudinal section.
Arrow shows the cross section of the cilia and also the discharging of the secretory products.
(Bar = 0·5 µm). (3) TEM of surface region of the olfactory epithelium in longitudinal section.
(Bar = 1 µm). (b, basal body; c, cilia; cr, ciliated receptor cell; eov, electron opaque vesicle; m,
microvilli; mr, microvillous receptor cell; ok, olfactory knob; sc, supporting cell; z, zonula
occludens). (4) TEM of the olfactory epithelium in oblique section showing rod cell (rc) with
a rod (r). (Bar = 4 µm). (5) A magnified view of the base of the rod. Arrows indicate the
microtubules. (Bar = 0 5 µm).
Ultrastructure of olfactory epithelium of H. fossilis
237
Figure 6. TEM of the dendrite of microvillous receptor cell (mr) surrounded by supporting
cell (sc). Arrows indicate the microtubules. (Bar = 1 µm).
microtubules could not be ascertained because the transverse sectional view of the rod
could not be encountered in the section. The basal bodies of the cilia are very
prominent. The upper cytoplasmic part of the cell resembles dendritic extensions of the
receptor cells. The entire cell takes a deep stain. Aggregation of mitochondria at this
area is also prevalent. The nucleus is placed at the lower third of the cell. Granulated
endoplasmic reticulum is present near the nucleus. Free ribosomes are scattered in the
cytoplasm. The junctional complex form a firm attachment with the adjacent cell.
3 3 Supporting cell
The nonciliated supporting cells are fairly distributed in the olfactory epithelium. The
cells are columnar which extend from epithelial free margin to the basement membrane.
Usually the cells are broad at the apical region although some narrow cells are also
discernible (figures 1, 2, 8). The distal surface is flat and covered with some irregular
small projections.
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Figures 7-11. (7) TEM showing elongated nucleus of receptor cell. (Bar = 1 µm). (8) TEM
shows a broad supporting cell (sc) with endoplasmic reticulum over the nucleus. (Bar = 1 µm).
(9) TEM of the longitudinal section of the olfactory epithelium showing ciliated supporting cell.
(Bar = 1 µm). (10) Apical margin of the ciliated supporting cell. Arrows indicate the translucent
microvesicles. (Bar = 1 µm). (11) Longitudinal section of the apical region of the olfactory
epithelium showing the immature goblet cell. (Bar = 1·5 µm). (g, golgi complex; id,
interdigitation).
Ultrastructure of olfactory epithelium of H. fossilis
239
The nucleus is almost round and placed at the lower third area of the cell (figures 1, 8).
The amount of euchromatin is comparatively more than that of heterochromatin and
the latter is disposed more near the nuclear envelope. Mitochondria of various shapes
are heaped at the apical region of the cell which consist of a dense matrix with compact
cristae. The endoplasmic reticulum is arranged in the supranuclear region. Some
electron opaque vesicles are present in the marginal area of some of these cells
(figures 1, 2). The size of the vesicles varies approximately from 0·4 µm to 0·7 µm. These
vesicles possess some secretory granules that are released from time to time (figure 2).
The ciliated supporting cells are mainly distributed in the middle region of the
lamella. These cells are also columnar and the free broad end is provided with a number
of cilia (figures 1, 9). The length of the cilia could not be measured but the diameter is
about 0·25 µm. These are typical kinocilia possessing 9 + 2 axial pattern of microtubules. The basal bodies are present but the rootlets are not observed. A few
translucent micro vesicles with smooth surface are scattered at the apical margin of the
cell (figure 10).
The nucleus is oval with well marked heterochromatin. Mitochondria are distributed at the apical region of the cell and the shape varies from round to elongate.
3.4 Goblet cell
These cells are distributed in the distal part of the lamella as well as on the surface layer
of raphe. Immature and mature stages of goblet cells have been identified. In the
immature stage the cell has a prominent golgi complex at the supranuclear region
Figure 12. TEM of a portion of mature goblet cell showing interdigitation (id) and huge
secretory vesicle (sv). (Bar = 1 µm).
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N C Datta and Shovan K Bandyopadhyay
(figure 11). The vesicles with the secretion move towards the free end of the cell and
gradually become accumulated giving a globoid shape to the cell (figures 1,12). Due to
heavy accumulation of the secretory granules the nucleus along with other cell
organelles are pushed towards the bottom of the cell. The nucleus is oval. At the
subsurface area the interdigitation of the cell membrane of both immature and mature
goblet cells with the adjacent supporting cell is quite prominent (figures 1,11,12).
3.5 Basal cell
Basal cells are loosely arranged at the base of the olfactory epithelium and form
a discontinuous layer over the basement membrane. These cells make way to the axons of
the receptor cells to reach the basement membrane. The cells are usually round, oval
or pearshaped (figure 13) and remain interspersed with the bases of receptor, supporting and goblet cells. Nucleus is also of various shapes. Cytoplasm is dense with
scattered mitochondria, rough endoplasmic reticulum and golgi complex (figure 14).
3.6 White cell
It is the most weakly stained cell present in the epithelium intervening the supporting
cell. The cell is polygonal (figures 1,15). The nucleus is comparatively large with well
defined nuclear membrane. The nucleolus is enlarged and dense but the karyoplasmic
particles are very scanty. The cytoplasmic granules are also less. The mitochondria are
swollen and cristae are in degenerated condition. The endoplasmic reticulum is
dialated and shows signs of deterioration (figure 15).
4. Discussion
The ciliated and microvillous receptor cells together with rod cell rarely occur in an
olfactory epithelium in H. fossilis. Yamamoto and Ueda (1977, 1978) reported the
occurrence of three types of cell in salmon and in a catfish, Parasilurus asotus. The
identity of rod cell as a receptor neuron has been questioned by Ichikawa and Ueda
(1977) as the cells were found unaffected by the olfactory nerve transection. On the
contrary, Yamamoto and Ueda (1979a, b) suggested that the rod cell is a transformed
ciliated neuron (type 2 ciliated cell) because they observed intermediate form in
Cheilopogon agoo and three species of Perciformes. In a recent study Singh et al (1995)
regarded the rod cell as the receptor cell in Schizothoraichthys progastus and
Schizothorax richardsonii. They have also observed the intermediate stage of rod
cell. The scarcity of the rod cell in the sensory epithelium ofH. fossilis indicates that it is
not a regular type of cell. From the available literature it is evident that the formation of
the rod may be due to the result of fusion of cilia of ciliated neuron. According to
Hernadi (1993) the density of rod cell increases after increased C d2+ exposure which
probably indicates that the environmental factor regulates the density of this kind of
cell. Rowley and Moran (1985) were also of the opinion that the rod cells are the
artefacts of ciliated receptor cell and such transformation is either due to water
pollution or fixation. H. fossilis, a mud dweller, may have to encounter the environmental stress which may necessitate the formation of the rod cell.
Ultrastructure of olfactory epithelium of H. fossilis
Figures 13-15. (13) A basal region of the olfactory epithelium. (Bar = 2 µm). (bc, basal cell;
bm, basement membrane). (14) A magnified portion of the basal cell. Arrows show the rough
endoplasmic reticulum. (Bar = 0·5 µm). (15) TEM of a white cell in the olfactory epithelium.
(Bar= 1µm). (er, endoplasmic reticulum; m, mitochondria; , nucleus; nl, nucleolus; nm,
nuclear membrane).
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N C Datta and Shovan K Bandyopadhyay
Earlier Thornhill (1967) and Wilson and Westerman (1967) believed it as a degenerating sensory cell. Theisen et al (1980) with SEM and TEM micrographs showed
some thick protrusions combining with the cilia in the sensory epithelium of Belone
belone. These protrusions simulate rod cell and they (op. cit.) considered this cell as
a degenerated one. But the present study puts a question to its degenerated status
because it has been observed that the rod cell have well defined nucleus, rough
endoplasmic reticulum and densely populated mitochondria indicating its functional
state, although its real function is yet to be ascertained.
As in other catfishes (Yamamoto and Ueda 1978; Erickson and Caprio 1984; Theisen
et al 1991) the microvillous and ciliated receptor cells are distributed in the sensory area
of the olfactory epithelium ofH. fossilis. The independency of ciliated and microvillous
receptors is now established through a developmental study in rainbow trout by
Zielinski and Hara (1988). They stated that the ciliated receptor cell ontogenetically
precedes the microvular receptor. But previously Theisen et al (1986) mentioned that
the ciliated and microvillous receptor cell develop from identical stem cell and the
development of the centrioles is arrested in microvillous receptors. In H. fossilis no
such centrioles is discernible in microvillous receptors. Hence it can be stated that
ciliated and microvillous neurons develop separately from undifferentiated cell and
also function separately. It is supported by the fact that in some teleosts the ciliated
receptors are altogether absent (Bannister 1965).
In H. fossilis all the receptors have microtubules in their dendrite. Such a condition
has also been reported in many fishes (Andres 1969; Theisen 1972). These microtubules
are probably responsible for maintaining the shape of the dendritic process and
channalizing different transport materials to the particular site. However, Behnke and
Forer (1967) suggested its supportive function and involvement in cytoplasmic streaming. It is generally accepted that the olfactory receptor macromolecules are associated
with the membrane of cilia (Rhein and Cagan 1981; Hara 1992). In H. fossilis it is
evident that not only the cilia and microvilli but also the membrane of the olfactory
knob has the receptor site. This view is supported by the finding of H ara and Zielinski
(1989) that the olfactory knob develops earlier than the cilia or microvilli.
The mechanical support to the surrounding receptor cell by the supporting cell is
now an established phenomena. But in H. fossilis some vesicles filled with secretory
granules suggest the secretory function of the supporting cell. The micrograph clearly
shows the discharging of the secretory material (figure 2). The secretory function of the
supporting cell was also proposed earlier by Thornhill (1967), Bertmar (1973) and
Zeiske et al (1979), although Yamamoto (1982) had a doubt on such function due to
lack of evidence.
The ciliated supporting cell in H. fossilis can easily be distinguished from the ciliated
receptor cell as it does not have any olfactory knob. The long cilia are inclined at the
same direction indicating their role in water ventilation in the olfactory chamber as well
as in the interlamellar spaces which obviously promotes better odour perception by the
receptor cells. Aggregation of mitochondria at the apical region of the cell indicates that
they are providing the required energy for the movement of cilia.
The immature and mature state of goblet cells of H. fossilis have been clearly identified.
The interdigitation of goblet cell with the adjacent supporting cell helps it to
be in its position firmly during profuse secretion. But it is interesting to note that no
report of such type of interdigitation is available. However, Thornhill (1967) mentioned the
interdigitation of supporting cell with basement membrane, other supporting cell,
Ultrastructure of olfactory epithelium of H. fossilis
243
basal or sensory cell. Gemne and Doving (1969) and Zeiske et al (1979) reported the
interdigitation between supporting and receptor cell. Regarding the function, Hornung
and Mozell (1981) proposed that the secretion helps in facilitating the odorant removal.
In H. fossilis, as it is a mud dweller the secretion of the goblet cell helps in binding the
microscopic debris that enter in the olfactory chamber with water current and finally it
exit through the nasal aperture. It also helps in decreasing the friction of water in the
chamber as well as protecting the epithelium from coming in contact with the
hazardous material to some extent.
The junctional complex in H. fossilis, the zonula occludens is prominent between
receptor and supporting cell which is also reported by Gemne and Doving (1969) and
Theisen (1972). Thornhill (1967) mentioned the junctional complex in lamprey as
zonula adherens and stated it acts as a barrier to prevent the influx and eflux of
substances into and out of the interlamellar spaces. But Gemne and Doving (1969)
stated that the "Z onula occludentes" protects the epithelial lining in the fresh water fish,
Lota lota against the osmotic pressure. The basal cell is believed as the progenitor of
receptor or the supporting cell as its mitotic condition is observed by Breucker et al
(1979) and Zeiske et al (1992). The rough endoplasmic reticulum and mitochondria also
support its functional state.
Occurrence of white cell is reported by Evans et al (1982) in the neuroepithelium of
rainbow trout. A similar kind of cell named X cell is also described by Peters et al (1984)
in the epithelial tumour tissue of Platichthys stellatus. Although the microanatomical
description of the X cell is very similar to that of the white cell, it is assumed that the
white cell is quite different from the X cell. This is because the X cells are densely
distributed in the epithelial tumours (Peters et al 1984) where as the white cell is
scarcely found in the olfactory epithelium ofH. fossilis. As all its organelles are found in
degenerating condition it is obviously a degenerating cell. However, presence of
degenerating cell in the olfactory epithelium of teleosts and other vertebrates is a very
common feature as mentioned by Thornhill (1967) and Bertmar (1973) which is
corroborated by the present study.
Acknowledgements
Thanks are due to Dr (Mrs) S Majumdar and Mr Sailen Dey, Biophysics Division,
Indian Institute of Chemical Biology, Calcutta for the technical assistance in the
transmission electron microscopical study. Prof. S G Pal and Dr Biswas, Biophysics
Laboratory of the Calcutta University also deserve thanks for valuable suggestions.
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Corresponding editor: SAMIR BHATTACHARYA