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Intercellular contacts of lymphocytes during migration across high-endothelial venules of lymph nodes. An electron microscopic study

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THE ANATOMICAL RECORD 207:643-652 (1983)
Intercellular Contacts of Lymphocytes During Migration
Across High-Endothelial Venules of Lymph Nodes.
An Electron Microscopic Study
FERRELL R. CAMPBELL
Department ofAnutomy, Health Sciences Center, University of Louisville,
Louisville, K Y 40292
ABSTRACT
The migration of lymphocytes across the wall of high-endothelial venules was studied by electron microscopic examination of niurine lymph
nodes fixed with glutaraldehyde and tannic acid. Regions of close membrane
apposition, referred to in the present study as “intercellular contacts,” were
observed between migrating lymphocytes and endothelial cells of the vessel
wall. At high magnification the intercellular contacts resolve into pentalaminar structures resembling gap junctions. However, the location of these contacts suggests that they are regions of membrane adherence utilized for
locomotion of the lymphocytes across the endothelium. At present, it is unclear
whether these intercellular contacts are communicating junctions or sites of
membrane adherence.
In lymph nodes and other lymphatic tissues, lymphocytes migrate from the vascular
bed across the endothelium of venules to enter the lymphatic stroma (Gowans and
Knight, 1964; Howard et al., 1972; Sedgely
and Ford, 1976).The venules involved in this
cellular migration have a n unusually thick
endothelium and are called high-endothelial
venules (HEV) or postcapillary venules
(PCV). Electron microscopic studies on HEV
have described the normal structure of these
vessels (e.g., Anderson, 19761, the effects of
various substances upon HEV (Anderson et
al., 1975; Henry and Beverley, 1976; Kittas
and Henry, 1980), and the route of lymphocytic migration across the endothelium,
whether intercellular (Schoefl, 1972; Wenk et
al., 1974) or transcellular (Farr and DeBruyn, 1975; Cho and DeBruyn, 1979). The
migration of lymphocytes across the walls of
HEV seems to be a highly specific phenomenon involving attachment of lymphocytes by
means of receptors to the endothelial cells
(Stamper and Woodruff, 1976; Chin et al.,
1980a,b; Carey et al., 1981). However, only a
few studies have shown morphological evidence for cellular attachment or interaction
between lymphocytes and endothelial cells.
Anderson and Anderson (1976) and Ohmann
(1980) described regions of decreased intercellular space between lymphocytes and endothelial cells, but according to these authors,
0 1983 ALAN R. LISS, INC
such regions do not resemble any of the usual
intercellular junctions.
Migration of blood cells across the sinusoidal wall of bone marrow is also believed to
be a highly specific phenomenon. Recent
studies (Campbell, 1982) have demonstrated
“intercellular contacts” resembling gap junctions between migrating blood cells and cells
of the sinusoidal wall of bone marrow. In
view of these findings, the present study was
undertaken to determine whether similar intercellular contacts are present between migrating lymphocytes and cells of HEY Tannic
acid-glutaraldehyde fixation was employed,
because this fixative enhances membrane
staining (van Deurs, 1975; Wagner, 1976)and
preserves surface components of the membranes (Chew, 1980).
MATERIALS AND METHODS
Mesenteric and inguinal lymph nodes from
six female Wistar rats weighing 150-200 gm
were used in this study. The thoracic aorta of
anesthetized animals was cannulated, the
vascular system was flushed with isotonic
Krebs’ buffer, pH 6.8, containing 1 unit of
heparin per 100 ml, and then fixative was
perfused into the vascular bed. The perfusion
apparatus has been described previously
(Campbell, 1972). The fixative consisted of
Received March 24, 1983; accepted July 18, 1983.
644
F.R. CAMPBELL
2% glutaraldehyde and 2% tannic acid in 0.1
M cacodylate buffer, pH 6.8. Following perfusion of 100 ml of fixative through the vascular system, lymph nodes were excised, cut
into small blocks, and fixed a n additional 1
hour in 4% glutaraldehyde and 4% tannic
acid in 0.1 M cacodylate buffer, pH 6.5. Tissues were rinsed overnight in 0.1 M cacodylate, osmicated in the same buffer, dehydrated
in a graded series of ethanol, stained with
10%uranyl acetate in methanol, and embedded in Maraglas. Thick sections were stained
with azure I1 and examined to locate highendothelial venules for electron microscopic
study. Thin sections were cut on a PorterBlum MT-2 Ultramicrotome using a diamond knife, stained with lead citrate, and
examined at 60 kv in a Philips EM 200 electron microscope. During the course of the
study, sections through about 400 lymphocytes in various stages of migration across
the endothelium were photographed and the
micrographs of these cells are the basis of the
following observations.
RESULTS
Following fixation with glutaraldehyde and
tannic acid, the high-endothelial venules appear much as they do with aldehydes alone.
Readily recognized are the thick endothelial
cells and the numerous small lymphocytes in
the process of migrating across the vessel
wall. Various organelles of the endothelial
cells, described in detail by others (e.g., Anderson, 1976),appear well preserved, and the
basal lamina of the endothelial cells is intensely stained (Figs. 3, 6). Tannic acid enhances staining of cellular membranes and,
consequently, accentuates the intercellular
space between lymphocytes and endothelial
cells. Examination of this space shows a variable but appreciable amount of extracellular
material which on occasion is rather electron
dense and largely fills the intercellular space
(arrows, Fig. 6).
After perfusion of fixative through the vascular system, only a few blood cells, mostly
small lymphocytes, remain in the lumina of
HEV. Some of these lymphocytes appear unattached in a given section, but others are
closely apposed to the surface of endothelial
cells (Fig. 1).The intercellular space between
these apparently adherent lymphocytes and
the endothelial cells is variable in width but
a t its narrowest measures 20-30 nm across.
A few lymphocytes lying in the vessel lumina appear to be in a n early stage of endo-
thelial penetration. Figure 2 illustrates this
point; a process of the lymphocyte has invaginated the endothelium. These penetrating
lymphocytes typically have one or more sites,
often associated with villous projections of
the lymphocytes, where the intercellular
space is lacking and the adjacent plasmalemmas are closely apposed (arrowhead, Fig. 2).
At higher magnification these regions of
membrane apposition resolve into pentalaminar structures consisting of a central dense
layer continuous with the outer leaflets of
the membranes and flanked successively by
electron lucent regions and by the dense inner leaflets of the membranes (Fig. 3, see
inset). In the present study, these and similar
pentalaminar regions of close membrane apposition are referred to as “intercellular
contacts.”
Figure 3 shows a lymphocyte (LY1)located
largely within the endothelium of a HEV;
only the blunt uropod of this migrating cell
still lies in the lumen. An intercellular space
of the usual width can be seen around most
of the lymphocyte, located between the lymphocyte and endothelial cells or between this
cell and another lymphocyte (LY2). However,
near the luminal surface of the endothelium,
at the site where the lymphocyte apparently
first penetrated the endothelium, there are
regions where a n intercellular space is lacking (arrowheads). In the inset of Figure 3, the
membranes of the two cells can be observed
coming together to form a pentalaminar region identical to that described above. The
second lymphocyte (LY2) of Figure 3 lacks
intercellular contacts with the endothelial
cell, a t least in this section, even though it is
in a similar stage of endothelial penetration.
This observation is interpreted to indicate
that these intercellular contacts are limited
in extent and do not completely surround the
migrating cell a t the site of initial penetration. Figure 3 also shows a n intercellular
junction between two endothelial cells (arrow) which a t higher magnification (inset)
has a n ultrastructure identical to that of the
intercellular contacts associated with the miFig. l. A lymphocyte (LY) located in the lumen of a
HEV abuts against an endothelial cell (El. The lymphocyte appears to be attached to the endothelium, but no
intercellular contacts are observed. x 26,400.
Fig. 2. A lymphocyte (LY) beginning to penetrate the
endothelium (E) of a HEV. The lymphocyte has a process
(P) invaginating the endothelium and an intercellular
contact (arrowhead) with the endothelial cell. x 20,500.
INTERCELLULAR CONTACTS OF HEV
645
646
F.R. CAMPBELL
647
INTERCELLULAR CONTACTS OF HEV
grating lymphocyte. In view of the morphology of this junction and the cell types
involved, the junction is believed to be a gap
junction. The similarity of this junction to
the intercellular contact between the lymphocyte and endothelial cell is remarkable.
Figure 4 illustrates a lymphocyte that has
penetrated the endothelium and now lies
within this layer. An intercellular space of
the usual width is observed around most of
the lymphocyte, but a t one site (arrow) the
membranes lie close together and a n intercellular space is lacking. Higher magnification (Fig. 4,inset) shows that this region is
a n intercellular contact. Intercellular contacts were sometimes seen near the luminal
surface of the endothelium as shown here,
but they were also observed near the abluminal surface of the endothelium and a t intermediate levels. Sections through some
lymphocytes showed no intercellular contacts, while sections through others showed
more than one. Of the lymphocytes photographed and closely examined, about one
quarter had distinct intercellular contacts or,
when the membranes were not cut perpendicularly, regions that were presumed to be
intercellular contacts. Since serial sections
were not examined, it is not known whether
all lymphocytes had intercellular contacts,
but lack of contacts could be due to the plane
of section.
Many lymphocytes in passage across the
endothelium appear to be solitary cells surrounded by endothelial cells as shown in Figure 4, but other lymphocytes form clusters of
two or more cells among the endothelial cells.
In such cases intercellular contacts were
often present between adjacent lymphocytes
(Fig. 5, arrows). In any one section, lymphocytes may have intercellular contacts only
with other lymphocytes, only with endothelial cells, with both endothelial cells and lymphocytes, or no intercellular contacts at all.
Again, because of plane of sectioning effects,
Fig. 3. A lymphocyte (LY1) has largely penetrated the
endothelium (El of a HEV. Intercellular contacts (arrowheads) are seen between lymphocyte and endothelial
cell. A second lymphocyte (LY2) in a similar state of
penetration lacks intercellular contacts, at least in this
section. An intercellular junction between endothelial
cells (arrow), the basal lamina @I) of the endothelium,
and a pericyte (PI are also labeled. X21,300. Inset shows
high magnification of the intercellular contact at the
right between lymphocyte CLY) and endothelial cell (El
and the intercellular junction between the endothelial
cells. x 121,500.
the frequency with which any of these combinations of intercellular contacts occur is
uncertain.
As lymphocytes pass through the endothehum, they penetrate the basal lamina of the
endothelium, come into contact with pericytic cells of the vessel wall, and thereafter lie
among cells of the lymphatic tissue. Figure 6
shows a lymphocyte that has penetrated the
basal lamina of the endothelium and rests
against processes of pericytic cells. Intercellular contacts were not observed during the
course of this study between lymphocytes and
pericytes or between lymphocytes and cells
of the lymphatic tissue, despite the fact that
many lymphocytes in this stage of migration
were closely examined. Figure 6 also illustrates a mass of filamentous material (0 in
the cytoplasm of the migrating lymphocyte.
Similar filamentous material believed to be
microfilaments was frequently observed in
migrating lymphocytes, but its relationship,
if any, to the intercellular contacts is not
known.
DISCUSSION
The direction of lymphocytic migration
across high-endothelial venules has been
shown, using labeled lymphocytes, to be from
the vascular bed into the surrounding lymphatic tissue (Gowans and Knight, 1964;
Howard et al., 1972). The direction of migration can also be surmised in many instances
from the morphology of fixed lymphocytes.
Migrating lymphocytes display a typical configuration, with the nucleus located in the
leading part of the cell and a blunt uropod
containing most of the organelles trailing behind (Lewis, 1931; Norberg et al., 1973; Haston et al., 1982). In the present study, the
expected lymphocytic polarity was evident
among cells that were penetrating the endothelium (Fig. 3). Polarity of lymphocytes was
also apparent among cells that were migrating out of the endothelium, but polarity was
frequently lacking in lymphocytes that were
located within the endothelial layer. This observation and the fact that most of the lymphocytes associated with HEV lie within the
endothelium would seem to indicate that
lymphocytes rapidly penetrate the endothelium, remain within it for a period of time,
and then migrate into the surrounding tissue.
A continuing controversy concerning lymphocytic migration across HEV relates to
whether the lymphocytes penetrate the endothelial cells (Marchesi and Gowans, 1964;
Farr and DeBruyn, 1975) or whether they
648
F.R. CAMPBELL
INTERCELLULAR CONTACTS OF HEV
pass through the intercellular space between
endothelial cells (Schoefl, 1972; Wenk et al.,
1974). The scanning electron microscopic
studies of Cho and DeBruyn (1979) argue
strongly in favor of the former view. This is
a n interesting and possibly important point,
because transcellular migration of lymphocytes in HEV may require cellular interactions between lymphocytes and endothelial
cells. In a similar system, blood cells of bone
marrow have been shown to pass through
pores that penetrate individual endothelial
cells (DeBruyn et al., 1971; Campbell, 1972;
Becker and DeBruyn, 1976). Transcellular
migration is believed by these authors to be
of importance in the screening of blood cells
thought to occur at the sinusoidal wall. In
649
view of these findings, one might expect
transcellular migration and cellular interactions to be involved in the selection that occurs in HEV, i.e., only small lymphocytes
pass in large numbers across these vessels.
The present observations do not resolve this
controversy, since the intercellular contacts
are of unknown function and could presumably be involved in either route of migration.
From the present study on fixed cells, it
seems possible to reconstruct some of the
events that occur as lymphocytes migrate
from the vascular bed across the wall of HEV.
Lymphocytes in the lumen of the vessels
come into contact with the endothelial cells
and adhere to them. The lymphocytes of the
present study, apparently attached to the en-
Fig. 6. A lymphocyte CLY) has a large process that passes through the basal lamina (bl) of
the endothelium (E) and lies adjacent to the pericytes (P) of the vessel wall. Filamentous
material (0 can be seen in the lymphocyte, and the dense intercellular material often seen
between lymphocytes and endothelial cells is shown (arrows). x 24,100.
Fig. 4. A lymphocyte (LY) surrounded by endothelial
cells (E) of a HEV. An intercellular contact between
lymphocyte and endothelial cell is shown at the arrow.
X 19,800. Inset shows detail of membranes at the intercellular contact. x 146.000.
Fig. 5. Two adjacent lymphocytes (LY) lying in the
endothelium (E) of a HEV. Intercellular contacts (arrows)
are shown between the lymphocytes. X 17,200.
650
F.R. CAMPBELL
dothelium, were separated from the endothelial cells by a n intercellular space measuring
at least 20 nm across. As penetration begins,
intercellular contacts, often associated with
villous projections of the lymphocytes, are
formed with the endothelial cells. As the
lymphocytes penetrate deeper into the endothelium, intercellular contacts are observed
near the site of initial penetration. Once inside the endothelium, intercellular contacts
are present between lymphocytes and endothelial cells and between adjacent lymphocytes. Finally, the basal lamina of the
endothelium is penetrated, and the lymphocytes pass into adjacent tissue. Intercellular
contacts have not been seen between migrating lymphocytes and pericytes or other
nearby cells.
The attachment of lymphocytes to endothelial cells of HEV has been investigated by
several workers. Stamper and Woodruff
(1976) and Butcher et al. (1979) have demonstrated selective binding of small lymphocytes to the surface of endothelial cells of
HEV. More recently Chin et al. (1980a,b) and
Carey et al. (1981)have presented evidence
that lymphocytes possess a surface substance
that mediates their binding to endothelial
cells of HEV. This substance is trypsin-sensitive and appears to be a glycoprotein (Chin
et al., 198Ob). Chin et al. (1980a) feel that the
migration of lymphocytes across HEV consists of two distinct and separate phases: selective binding of lymphocytes to endothelial
cells via their receptors, and then passage of
lymphocytes across the endothelium. The
present observations seem compatible with a
two-phase process of lymphocytic migration
across HEV. Furthermore, it is of interest
and possible importance that attachment
does not appear to involve intercellular contacts, but penetration and movement across
the endothelium do.
One of the most interesting questions
raised by the present study concerns whether
or not the intercellular contacts are gap junctions. The pentalaminar structure of the intercellular contacts appear to be identical to
that of gap junctions of other cells following
fixation with glutaraldehyde and tannic acid
(see van Deurs, 1975; Kalderon et al., 1977;
Gilula et al., 1978).Furthermore, in the present study, the morphology of the intercellular contacts is identical to that of junctions
between endothelial cells. Since endothelial
cells in general (Simionescu et al., 1976) and
endothelial cells of HEV (van Deurs et al.,
1975) may have gap junctions, and since the
morphology seems correct, it would appear
that the junctions described here between
endothelial cells are indeed gap junctions.
That being the case, it would seem to follow
that the intercellular contacts associated
with migrating lymphocytes are likewise gap
junctions. Assuming this is true, then what
are plausible functions of gap junctions a t
these sites? It might be supposed that communicating junctions between endothelial
cells and lymphocytes help determine which
cells migrate across the endothelium. However, the studies of Chin et al. (1980a,b) and
Carey et al. (1981) indicate that binding of
lymphocytes to endothelial cells via receptors is the crucial aspect of specificity, and
the present study shows that intercellular
contacts are not associated with attachment.
Communicating junctions between lymphocytes and endothelial cells or between lymphocytes within the wall of HEV could have
many other functions, but our present knowledge concerning events that may occur during lymphocyte migration across HEV leaves
one at a loss as to what there functions might
be. With the present techniques, the structural similarity of the intercellular contacts
to gap junctions is striking, but beyond that
little can be stated. Examination of the particle distribution on the apposed membranes
by means of freeze-fracture replicas would be
of assistance in determining how closely
these contacts resemble gap junctions, but to
the author’s knowledge such studies have
not been conducted.
Another possibility is that the intercellular
contacts of the present study are sites of
adhesion between lymphocytes and endothelial cell membranes utilized for locomotion of
the lymphocytes across the vessel wall. One
might suppose that, as the lymphocytes begin to penetrate the endothelium, they form
intercellular contacts with the endothelial
cells and use these anchoring sites to invaginate the endothelium. Formation of additional contacts would occur as the lymphocytes penetrate deeper into the endothelium
and these contacts would allow the lymphocytes to eventually pass through the endothelium. The observations of the present
study seem to fit fairly well into such a
schema. To begin with, during initial stages
of penetration, the intercellular contacts are
often associated with villous projections of
the lymphocytes. Villous projections of attached lymphocytes (Anderson and Ander-
INTERCELLULAR CONTACTS OF HEV
son, 1976) and of lymphocytes during early
stages of endothelial penetration (Cho and
DeBruyn, 1979) have been reported previously. An interesting correlate of these observations is that villous projections of
lymphocytes have been shown to contain
high concentrations of actin (Sundqvist et al.,
1980), a substance involved in adhesion and
locomotion of several cell types, including
lymphocytes (reviewed by Parrott and Wilkinson, 1981).If the intercellular contacts are
adherent sites for locomotion of the lymphocytes, one would expect concentration of actin near the contacts. The present study
shows microfilaments in the migrating lymphocytes but does not shown a n association
of microfilaments and intercellular contacts.
However, other techniques such as immunochemistry are better suited to demonstrate
any association of actin and intercellular
contacts. Another interesting observation of
the present study is that the contacts that
form as penetration of the endothelium begins appear to be maintained as penetration
continues, suggesting that the contact sites
may move along the surface of the cell. Capping of membrane components and their
translocation along the membrane during locomotion of lymphocytes has been discussed
by Jarvis et al. (1976) and by Parrott and
Wilkinson (1981).
All these observations suggest that the intercellular contacts described here are involved in attachment and locomotion of the
lymphocytes, but their ultrastructure does
not correlate well with cell to cell contacts
described by others. Cell to cell contacts have
been studied extensively in tissue culture
systems. These contacts (Chen and Singer,
1982), largely on the basis of intermembranous spacing, are currently classified as 1)
focal adhesions (10-20 nm), 2) close contacts
(30-50 nm), and 3) extracellular matrix contacts (100 nm or more). Focal adhesions and
close contacts have submembranous densities associated with them. The intercellular
contacts of the present study do not resemble
any of these contact types; the membrane
spacing is too close (2-4 nm), and submembranous densities are not present. The possibility that gap junctions function as adherent
sites for cellular locomotion has not, to the
author’s knowledge, been reported.
Intercellular contacts identical to those of
the present study have been reported in bone
marrow following fixation with tannic acid
and glutaraldehyde, but their function in
651
marrow is likewise unresolved. In marrow of
mice, these contacts are observed between
developing blood cells and fixed cells of the
marrow (Campbell, 1980) and between migrating blood cells and cells of the sinusoidal
wall (Campbell, 1982). In marrow of chickens, these contacts are observed between the
intravascular erythroblasts and endothelial
cells of the sinusoidal wall (Sorrel1and Weiss,
1982). Possible functions of these contacts in
marrow are discussed by these authors. It
need only be emphasized here that on the
basis of the present study, it is apparent that
identical contacts are involved in the delivery of blood cells from the marrow into the
circulation, on the one hand, and with the
transfer of lymphocytes from the circulation
to lymph nodes, on the other. Both processes
have in common a high degree of cell selectivity and the passage of cells from one compartment to another.
Further studies would seem to be needed
to elucidate the function of these intercellular contacts. At present one can only state
that they are present between lymphocytes
and endothelial cells and between lymphocytes and that they are likely of considerable
importance to the migration of lymphocytes
across the wall of HEV.
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