J. Cell Set. 2, 137-144 (1967)
Printed in Great Britain
137
FINE STRUCTURE OF THE CYTOPLASM
IN SALIVARY GLANDS OF SIMULIUM
H. C. MACGREGOR AND J. B. MACKIE
Department of Zoology, The University, St Andrews, Fife
SUMMARY
The salivary glands of 3rd or 4th instar larvae of Simulium niditifrons are about 5 mm long and
up to 400 fi wide. They have a capacious lumen which is normally filled with secretion.
The apical (luminal) plasmalemma of the gland cells is thrown into numerous microvilli. The
basal plasmalemma is usually straight but is infolded in places. The infoldings may be complex
near to cell junctions. There is a thick, uniform basement membrane. Contact surfaces of
adjacent cells often interdigitate. A septate junction extends inwards from the lumen for onequarter the depth of the cells. Rough endoplasmic reticulum is distributed evenly throughout
the cytoplasm. Many Golgi complexes with dark membrane-bounded granules are scattered
throughout the cytoplasm. Solitary granules, often more than 1 fi in diameter, lie in the apical
cytoplasm, especially near the apical border of the cell. These granules resemble the larger
Golgi granules and the contents of the lumen. Solitary granules consisting of 2 components
have been seen in various stages of passage through the cell membrane. The 2 components are
present in roughly constant proportions and can be identified in the larger Golgi granules and
in the secretion in the lumen. The nucleus is spherical. The nuclear envelope is smooth in the
larger cells of a gland but may be folded in the smaller cells. There are 80-100 pores//*2 of
nuclear envelope. Each pore appears to have a small granule at its centre. Microtubules,
about 180 A thick, are numerous in the apical cytoplasm, particularly near the luminal border.
Tubules which lie deep in the cytoplasm are flanked by a clear area 100—200 A wide.
The fine structure of a salivary gland cell of Simulium appears to indicate that the major
components of the salivary secretion are synthesized in association with the ribosomes on the
rough endoplasmic reticulum, concentrated in the Golgi regions, formed into secretion granules,
and passed out of the cell into the lumen of the gland by reverse phagocytosis.
INTRODUCTION
It is logical to look for a relationship between the activity of specific genes and the
synthesis of specific proteins in the cytoplasm of a cell. There is equivocal evidence
for such a relationship in the salivary glands of dipteran larvae. The cells of these
glands secrete a silky substance which normally fills the lumen of the gland. This
secretion serves a variety of purposes during larval life and is used in the construction
of a capsule prior to pupation. It is made up of a number of proteins (Laufer &
Nakase, 1965; Phillips & Swift, 1965), and some polysaccharide material (Phillips &
Swift, 1965). It can be identified in the cytoplasm of salivary gland cells in the form of
numerous small granules. In Sciara 3 types of secretion granule have been described (Phillips & Swift, 1965). One of these appears at a specific developmental
stage, another is present throughout development, and the presence of a third is
unpredictable. This pattern of secretion is not yet known to be related to changes in
the appearance or particular regions of the chromosomes of salivary gland cells, but
138
H. C. Macgregor and J. B. Mackie
such a relationship may be anticipated if chromosomal changes in Sciara resemble those
which have been described in Chironomus (Beerman, 1952). In Chironomus some puffs
appear at one developmental stage, others persist over long periods of development,
and some come and go independently of the developmental stage of the larva. In cells
of a special lobe (' Sonderzellen') of the salivary gland in Chironomus palUdivittatus the
presence of one specific Balbiani-ring (BR 4 (SZ)) on the fourth chromosome is
clearly related to the production by these cells of a particular kind of secretion granule
(Beerman, 1961). The Sonderzellen of C. tentans lack the special secretion granules
and show no Balbiani-ring at the locus corresponding to BR 4 (SZ) in C. palUdivittatus.
One might therefore suppose that in C. palUdivittatus the Balbiani-ring at BR 4 (SZ)
is making an informational RNA which serves as a template for the synthesis of a
major component of the salivary secretion.
Some other studies, however, point to a more complex mechanism for the production of salivary secretion. Laufer & Nakase (1965) state that the secretion from salivary
glands of Chironomus thuntmi includes 3 enzymes, trehalase, hyaluronidase, and protease, and 6 antigenic components. None of these enzymes nor the antigens are confined to the salivary glands. All are present in the haemolymph.
The activity of trehalase and hyaluronidase in salivary secretion is depressed by
exposure of larvae to actinomycin D (Laufer, Nakase & Vandenberg, 1964). The concentration of actinomycin D which produces a significant depression is different for
each enzyme. Likewise the dosage of actinomycin D which causes regression of
chromosomal puffing is not the same for all puffs. On the basis of this evidence Laufer
et al. (1964) suggest that trehalase and hyaluronidase are synthesized in the cells of the
salivary glands, and that the continued synthesis and secretion of these enzymes is
dependent upon the production of a template RNA. The 6 antigenic components of the
secretion on the other hand are supposed to be transported intact from the haemolymph
across the cells of the gland and passed into the lumen of the gland as part of the formed
secretion (Laufer & Nakase, 1965). Blood proteins labelled with 14C are transported in
this way and included in the secretion, as are human serum albumin and ferritin. It has
been argued from these observations that at least some of the major components of
the secretion are synthesized outside the salivary glands and that the glands function
in their uptake, transport and secretion.
Laufer's observations raise two questions concerning the structure of salivary gland
cells in dipteran larvae. First, does the cytoplasm of a salivary gland cell show all the
features which one might expect to find in a cell which is actively synthesizing and
secreting large amounts of a few specific proteins? These features have been well
documented for the exocrine cells of the mammalian pancreas (Sjostrand & Hanzon,
1954a, b, c; Ekholm, Zelander & Edlund, 1962; Ekholm & Edlund, 1959; Herman,
Sato & Fitzgerald, 1964), which undoubtedly make their own exportable proteins
(Warshawsky, Leblond & Droz, 1963; Caro & Palade, 1964). Secondly, does a dipteran
salivary gland cell show any features which might betray its supposed role as a transporter cell?
The answer to the first of these questions is already known. Salivary gland cells
from larvae of a variety of Diptera have been shown to possess a highly organized
Cytoplasmic structure in Simulium salivary glands
139
endoplasmic reticulum studded with ribosomes, numerous Golgi regions, various
types of secretion granule, and many conspicuous mitochondria (Jacob & Jurand,
1963, 1965; Phillips & Swift, 1965). The same authors have also remarked upon the
microvillate luminal border of the glands, and a particularly clear account of the gland
cell junction and the basement membrane has been given by Loewenstein & Kanno
(1964) and Wiener, Spiro & Loewenstein (1964). Some other features, including
cytoplasmic microtubules, have been identified by Jacob & Jurand (1965) in the
salivary glands of Smittia.
In the present paper we shall describe the cytoplasmic fine structure of salivary
glands from larvae of the black fly Simulium niditifrons (Edwards), and we shall
discuss our observations in the light of current ideas concerning the origin of the
salivary secretion.
Simulium larvae live in fast-flowing water and use some of their salivary secretion to
form silky threads which act as 'life lines' during local excursions downstream.
Immediately before pupation the larva weaves a stout pupal case entirely from threads
of the salivary secretion. Both of these functions demand an intense production of
secretion, and it was for this reason that we chose Simulium for our investigations.
MATERIALS AND METHODS
Larvae of Simulium niditifrons were collected from the bed of a stream running
through the Lade Braes in St Andrews. Salivary glands were dissected from 3rd or
4th instar larvae which measured 3-5 mm in length. Dissections were performed with
care to avoid displacement of the secretion filling the lumen of the gland. Glands were
immediately drawn into a pool of 1 % osmium tetroxide buffered with veronal acetate
at pH 7-4 (Palade, 1952) and cooled to 2 °C. They were fixed for 1 h, dehydrated in
acetone, and embedded in Vestopal W. Silver-to-grey sections were cut with glass
knives on a Cambridge Ultra-Microtome (A. F. Huxley pattern), and mounted on
Athene 483 grids without supporting films. Sections were double-stained with
2 % uranyl acetate for 5 min and lead citrate (Reynolds, 1963) for 2 min, and examined
with a Siemens Elmiskop 1 (80 kV) at negative magnifications of between 5 coo and
40000.
OBSERVATIONS
The larvae of S. niditifrons are club-shaped. They are about | mm long at
hatching and 6-7 mm long immediately before pupation. The wider rear portion of
the larva accommodates 2 long tubular salivary glands. Each gland is folded back upon
itself once and is connected to the head by a long thin duct (Fig. 1). In transverse
section the glands show a wide lumen filled with secretion and surrounded by flat
relatively narrow cells (Fig. 2). The nuclei of these cells are spherical and in the middle
region of the gland they occupy more than half the width of the cells.
Along the apical (luminal) border of the cell there are numerous microvilli projecting into the lumen of the gland (Fig. 3). These are bounded by a continuation of the
cell membrane. They are more numerous in cells from older larvae than in cells from
140
H. C. Macgregor andj. B. Mackie
corresponding regions of the gland in young larvae. They are also more numerous in
cells near the base of the gland than in cells of the neck region.
The contact surfaces of adjacent cells are folded and interdigitated. A septate
junction (Fig. 4) extends inwards from the lumen of the gland for about one-quarter
the depth of the cells. The septa are 80-90 A thick and are regularly spaced at intervals
of 40-60 A. We think that in such junctions the septa connect uninterrupted surface
membranes.
The plasma membrane at the base of the cell is generally straight (Fig. 5). It does,
however, fold inwards in some places, and in cells from older larvae these infoldings
may be deep and complex (Fig. 6). The more complex infoldings are usually found
near to a junction between adjacent cells. Sometimes there are membrane-bounded
vesicles, which are relatively empty, inside the folds of the cell membrane (Fig. 6);
such vesicles are extracellular. Similar vesicles may also be enclosed in the underlying
basement 'membrane' (Fig. 6). Some care is needed in interpreting the profiles of
membrane complexes near the base of the cell since these are often the result of
sectioning near to and in the plane of a cell junction, and thereby cutting through the
tips of interdigitations between adjacent cells. In such cases all the compartments of
the complex must necessarily be filled with cytoplasm and bounded by 2 unit
membranes.
Endoplasmic reticulum is distributed evenly throughout the cell (Figs. 3, 7) but is
lacking from regions near the basal and apical borders. The appearance of the endoplasmic reticulum varies from gland to gland. Generally it appears as round, oval, or
elongated profiles. Near the nucleus the elongated profiles lie more or less parallel to
the nuclear envelope (Fig. 7); in the apical regions of the cell they tend to be orientated
radially with respect to the lumen of the gland. The elements of the endoplasmic
reticulum are heavily studded with ribosomes and interspersed with free ribosomes.
In a thin section of a single cell there may be as many as 100 Golgi complexes. These
are scattered uniformly throughout the cell. Each consists of a disorderly collection of
smooth membranes, round vesicles, and granules of dark material (Fig. 8). Each dark
granule is bounded by a membrane. In some cases the membrane compartments
occupied by 2 or more granules are confluent.
Large solitary granules (Figs. 3, 10) are characteristic of the cytoplasm on the
apical side of the nucleus. These resemble the granules in the Golgi regions. Each is
bounded by a membrane. Solitary granules vary in size; the smallest compare with
the larger granules of the Golgi regions, whereas the largest may be more than 1 /i in
diameter. Large solitary granules are most common near the apical border of the cell.
The fate of these granules can be reconstructed from the following observations.
They consist of material which precisely resembles the contents of the lumen of the
gland (Figs. 3, 9). We have seen granules immediately inside and outside the cell
membrane. We have also seen situations similar to that illustrated in Fig. 9. In such
cases the membrane surrounding the granule has fused with the cell membrane and
the granule has been ejected from the confines of the cytoplasm into the lumen. Thereafter the granule probably joins the main mass of secretion in the lumen.
Most solitary granules show 2 components (Fig. 10). The bulk of the granule con-
Cytoplasmic structure in SimuUum salivary glands
141
sists of a compact matrix which appears dark after staining with lead citrate. Embedded
in this matrix are numerous small round light areas which give the whole granule a
spongy appearance. The light areas are not bounded by a membrane. They are
uniformly about 500 A in diameter and spaced 900-1000 A apart. In sections they
often seem to be arranged in a series of concentric rings. The light areas are not confined
to solitary granules; there are usually a few of them in the larger granules of the Golgi
regions (Figs. 7 8).
The nucleus is spherical. The nuclear envelope is often folded in the smaller cells of
a gland but always smooth in the larger cells. The outer and inner membranes of the
nuclear envelope are spaced about 200 A apart. The nuclear pores have an inside
diameter of between 450 and 550 A. Distances between the centres of adjacent pores
range from 850 to 1400 A. There are 80-100 pores//*2 of nuclear envelope. When seen
in surface view, as in sections tangential or oblique to the nuclear envelope, each pore
appears to have a small granule in its centre (Fig. 11). These granules are rarely evident
in transverse sections through the nuclear envelope.
Cytoplasmic microtubules (Slautterback, 1963; Ledbetter & Porter, 1963; Porter,
Ledbetter & Badenhausen, 1964) are common in the salivary glands of SimuUum
larvae. They appear in side view as 2 parallel dark lines and have an average thickness
of 180 ±30 A (Figs. 12, 13). They usually appear straight, never branch, and are
most numerous in the apical half of the cell, particularly near the luminal border.
Elsewhere they are sparse. Unlike Jacob & Jurand (1965) we have never seen microtubules near the adjoining membranes of neighbouring cells. Microtubules which lie
deep in the cytoplasm are particularly easy to see on account of a clear area which
extends for 100-200 A on either side of the tubule (Fig. 13). This area contrasts
sharply with the surrounding congestion of ribosomes and endoplasmic reticulum.
Such clear areas are less evident around microtubules near the luminal border.
DISCUSSION
In the exocrine cells of the mammalian pancreas, digestive enzymes are synthesized
on ribosomes.attached to the limiting membranes of the rough endoplasmic reticulum
(Siekevitz & Palade, i960). They are then transported across these membranes, segregated within the cisternae of the endoplasmic reticulum (Redman, Siekevitz & Palade,
1966), and move to small peripheral vesicles of the Golgi region (Jamieson & Palade,
1966). Thereafter they are concentrated into the condensation vacuoles of the Golgi
regions and formed into individual secretion granules (Caro & Palade, 1964). The
granules move towards the apical border of the cell and are thence discharged into the
lumen of the acinus.
In SimuUum salivary glands, formed secretion granules lying near to the apical
border of the cell consist of material which, in our electron micrographs, looks exactly
like the material occupying the lumen of the gland. We therefore think that the lumen
contents are wholly derived from the visible intracellular secretion granules. If any
other material is secreted by the cells into the lumen then it is not detectable in our
electron micrographs and can only be a minor component of the final secretion.
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H. C. Macgregor and J. B. Mackie
The material of the solitary secretion granules looks exactly like the material in the
condensing vacuoles of the Golgi regions; and these condensing vacuoles are surrounded first by smooth vesicles and then by rough endoplasmic reticulum which is
often highly organized. Accordingly it seems reasonable to regard the salivary gland
cell of a Simulium larva as a large version of an exocrine pancreas cell, making large
quantities of one or a few specific materials and exporting them, by reverse phagocytosis, to the lumen of the gland.
In our opinion there would appear no reason for supposing that any of the major proteins of the secretion are regularly imported from the haemolymph and merely transported across the cells of the gland. The structure of the salivary gland cells in
Simulium gives no indication of a transporting function beyond that of transporting
secretion granules from their site of formation to the apical border of the cell. Laufer &
Goldsmith (1965) have reported 'specializations' of the basal plasmalemma in Chironomus salivary glands which suggest that these cells are engaged in micropinocytosis.
The salivary glands of Simulium show no such specializations. In these cells the basal
plasmalemma is occasionally infolded and in glands from older larvae such infoldings
may be deep and complex. Infoldings of the basal plasmalemma in secretory cells are
not uncommon, however, and they need not be interpreted as indications of pinocytotic
activity. They have been described in mammalian pancreas (Ekholm et al. 1962), in
Brunner's gland in the mouse (Friend, 1965), and in certain cells of mammalian
gastric mucosa (Ito & Winchester, 1963); yet there is nothing to suggest that any of
these cells function by transporting rather than synthesizing their respective products.
The salivary glands of Simulium make only one type of secretion granule. These
granules consist of 2 microscopically distinct components, the dark material and the
light areas in our electron micrographs, and these components are present in roughly
constant proportions. These observations contrast with the findings of Phillips & Swift
(1965) who found, in Sciara, 3 different types of secretion granule. However, we have
not yet been able to look at the salivary glands of a larva which is in the act of making
its pupal capsule, and the secretion used to make this capsule may well differ from that
which is produced intermittently throughout the larval life.
We think that the microtubules in salivary gland cells of Simulium larvae may be
concerned with movement of materials through the cytoplasm of these cells. Such a
role has already been suggested for microtubules in cultured mammalian cells by
Freed (1965). The clear area surrounding microtubules which lie deep in the cytoplasm can be interpreted as a passage through the dense endoplasmic reticulum
created by a flow of non-particulate material along the outside of the tubule. The most
likely role for tubules near the luminal border is that of propelling the larger secretory
granules towards the lumen. This idea is upheld by the fact that some secretory
granules have microtubules clustered around them (Fig. 10).
We are indebted to Dr Lewis Davies for his generous help in identifying the species and the
stages of the larvae used in this work.
Cytoplasmic structure in Simulium salivary glands
143
REFERENCES
BKERMAN, W. (1952). Chromomerenkonstanz und spezifische Modifikationen der Chromosomenstruktur in der Entwicklung und Organ-differenzierung von Chironomus tentans. Chromosoma 5, 139-198.
BEEKMAN, W. (1961). Ein Balbiani-Ring als Locus einer Speicheldriisen-Mutation. Chromosoma
12,
1-25.
L. G. & PALADE, G. E. (1964). Protein synthesis, storage, and discharge in the pancreatic
exocrine cell. J. Cell Biol. 20, 473-495.
EKHOLM, R. & EDLUND, Y. (1959). infrastructure of the human exocrine pancreas. J. Ultrastruct. Res. 2, 453-481.
EKHOLM, R., ZELANDBR, T. & EDLUND, Y. (1962). The ultrastructural organization of the rat
exocrine pancreas. J. Ultrastruct. Res. 7, 61-72.
FREED, J. J. (1965). Microtubules and saltatory movements of cytoplasmic elements in cultured
cells. Jf. Cell Biol. 27, 29A.
FRIEND, D. S. (1965). The fine structure of Brunner's glands in the mouse. J. Cell Biol. 25,
563-576.
HERMAN, L., SATO, T. & FITZGERALD, P. J. (1964). The pancreas. In Electron Microscope
Anatomy (ed. S. M. Kurtz), pp. 59-95. New York and London: Academic Press.
ITO, S. & WINCHESTER, R. J. (1963). Thefinestructure of the gastric mucosa in the bat. J. Cell
Biol. 16, 541-577JACOB, J. & JURAND, A. (1963). Electron microscope studies on salivary gland cells of Bradysia
mycorum Frey (Sciaridae). III. The structure of the cytoplasm. J. Insect Physiol. 9, 849—
857JACOB, J. & JURAND, A. (1965). Electron microscope studies on salivary gland cells. V. The
cytoplasm of Smittia parthenogenetica (Chironomidae). J. Insect Physiol. u , 1337-1343.
JAMIESON, J. D. & PALADE, G. E. (1966). Role of the Golgi complex in the intracellular transport of secretory proteins. Proc. natn. Acad. Sci. U.S.A. 55, 424-431.
LAUFER, H. & GOLDSMITH, M. (1965). Ultrastructural evidence for a protein transport system
in Chironomus salivary glands and its implication for chromosomal puffing, jf. Cell Biol. 27,
57 A.
LAUFER, H. & NAKASE, Y. (1965). Salivary gland secretion and its relation to chromosomal
puffing in the dipteran, Chironomus ihummi. Proc. natn. Acad. Sci. U.S.A. 53, 511-516.
LAUFER, H., NAKASE, Y. & VANDENBEKG, J. (1964). Developmental studies of the dipteran
salivary gland. I. The effects of actinomycin D on larval development, enzyme activity, and
chromosomal differentiation in Chironomus ihummi. Devi Biol. 9, 367-384.
LEDBETTER, M. C. & PORTER, K. R. (1963). A microtubule in plant cell fine structure. J. Cell
Biol. 19, 239-250.
LOEWENSTEIN, W. R. & KANNO, Y. (1964). Studies on an epithelial (gland) cell junction. I.
Modifications of surface membrane permeability. J. Cell Biol. 22, 565-598.
PALADE, G. E. (1952). A study of fixation for electron microscopy. J. exp. Med. 95, 285-298.
PHILLIPS, D. M. & SWIFT, H. (1965). Cytoplasmic fine structure of Sciara salivary glands. I.
Secretion. J. Cell Biol. 27, 395-409.
PORTER, K. R., LEDBETTER, M. C. & BADENHAUSEN, S. (1964). The microtubule in cell fine
structure as a constant accompaniment of cytoplasmic movements. In Proceedings of the Third
European Regional Conference on Electron Microscopy (ed. M. Titlbach), pp. 119-120.
Prague: Publishing House of the Czechoslovak Academy of Sciences.
CARO,
REDMAN, C. M., SIEKEVTTZ, P. & PALADE, G. E. (1966). Synthesis and transfer of amylase in
pigeon pancreatic microsomes. J. biol. Chem. 241, 1150-1158.
E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in
electron microscopy. J. Cell Biol. 17, 208—212.
SIEKEVITZ, P. & PALADE, G. E. (i960). A cytochemical study on the pancreas of the guinea pig.
V. In vivo incorporation of leucine-1-C14 into the chymotrypsinogen of various cell fractions.
J. biophys. biochem. Cytol. 7, 619-629.
SjttSTRAND, F. S. & HANZON, V. (1954a). Electron microscopy of the Golgi apparatus of the
exocrine pancreas cell. Experientia 10, 367-369.
REYNOLDS,
144
H.C.MacgregorandJ.B.Mackie
F. S. & HANZON, V. (19546). Membrane structures of cytoplasm and mitochondria
in exocrine cells of mouse pancreas as revealed by high resolution electron microscopy.
Expl Cell Res. 7, 393-414.
SJOSTRAND, F. S. & HANZON, V. (1954c). Ultrastructure of Golgi apparatus of exocrine cells
of mouse pancreas. Expl Cell Res. 7, 415-429.
SLAUTTERBACK, D. B. (1963). Cytoplasmic microtubules. I. Hydra. J. Cell Biol. 18, 367-388.
WARSHAWSKY, H., LEBLOND, C. P. & DROZ, B. (1963). Synthesis and migration of proteins in
the cells of the exocrine pancreas as revealed by specific activity determination from radioautographs, j . Cell Biol. 16, 1-23.
WIENER, J., SPIRO, D. & LOEWENSTEIN, W. R. (1964). Studies on an epithelial (gland) cell
junction. II. Surface structure. J. Cell Biol. 22, 587-598.
SJOSTRAND,
{Received 7 September 1966)
Fig. 1. Photomicrograph showing a salivary gland from a 4th instar Simulium larva
folded as it is when inside the larva. Only the rear portion of the salivary duct (d) is
included in the picture.
Fig. 2. Photomicrograph of a 1-/1 section through a salivary gland in the region immediately behind the fold in the gland (n, nucleus; s, secretion filling the lumen of the
gland).
Fig. 3. Electron micrograph of the apical border of a salivary gland cell and the lumen
of the gland (/, lumen; mv, microvilli; s, secretion; sg, solitary granules).
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H. C. MACGREGOR AND J. B. MACKIE
{Facing p. 144)
Fig. 4. Part of a septate junction between adjacent cells. The arrows indicate regions
where the septa are visible.
Fig. 5. The basal edge of a salivary gland cell showing the basement membrane (b),
the plasma membrane (p), and 2 relatively simple folds (/) in the plasma membrane.
Fig. 6. A complex infolding (/) of the basal plasma membrane at a junction between
2 adjacent cells. Membrane-bounded vesicles (v), which are relatively empty compared
with the cytoplasm, lie within the basement membrane (b) and between adjacent
cell membranes in the infolded region. The area marked sd and similar areas to the
lower left of it are interpreted as sections through the tips of interdigitations between
adjacent cells.
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H. C. MACGREGOR AND J. B. MACKIE
Fig. 7. An area of cytoplasm on the apical side of the nucleus showing the arrangement
of rough endoplasmic reticulum and several Golgi regions (G). The larger granules
of the Golgi regions have a speckled appearance due to the presence of small regularly
arranged light areas within them (ch, chromosomes; nc, nucleolus; mn, nuclear
membrane).
Fig. 8. A typical Golgi region. The largest granules in this region show some of the
light patches which characterize the solitary secretion granules.
Fig. 9. Section through a secretion granule (sg) as it leaves the confines of the cytoplasm and is discharged into the lumen of the gland (s, secretion in the lumen).
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H. C. MACGREGOR AND J. B. MACKIE
Fig. 10. A region near the apical border of a cell showing 3 large secretion granules
(sg) and several smaller ones. Immediately above the large granule on the right are
numerous short profiles of microtubules; /, lumen.
Fig. 11. Oblique section through part of a nuclear envelope. The arrows indicate
pores which have granules visible in their centres.
Fig. 12. A region near the apical border of a cell showing numerous profiles of microtubules. The more distinct profiles are indicated by arrows.
Fig. 13. An enlarged view of a microtubule with a clear area on either side of it.
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H. C. MACGREGOR AND J. B. MACKIE