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THE ANATOMICAL RECORD 249:486–494 (1997)
Immunohistochemical and Structural Characteristics
of the Reticular Framework of the White Pulp
and Marginal Zone in the Human Spleen
TAKASHI SATOH,* RIKIO TAKEDA, HIROKI OIKAWA, AND RYOICHI SATODATE
Department of Pathology, School of Medicine, Iwate Medical University, Morioka, Japan
ABSTRACT
Background: The reticular framework of the white pulp
(WP) and marginal zone (MZ) consists of reticulum cells and reticulin
fibers. The antigenic heterogeneity of the reticular framework is well
documented in the mouse and rat spleen. The aim of the present study is to
characterize the reticular framework of the WP and MZ of the human
spleen.
Methods: Nine surgically resected human spleens were investigated.
Five of the nine spleens were perfused. Formalin-fixed materials were
embedded in paraffin and serial sections prepared for hematoxylin-eosin,
silver staining, and immunohistochemical examination. Electron and
immuno-electron microscopy were also applied. Using confocal laser
scanning microscopy, the reticular framework was analyzed threedimensionally.
Results: The reticulin fibers of the framework were immunostained for
type IV collagen in the WP and MZ. The WP was three-dimensionally
delimited by the a-smooth muscle actin (a-SMA)-positive reticulum cells.
In the WP, the distribution of a-SMA-positive reticulum cells formed the
reticular framework of the periarteriolar lymphoid sheath (PALS). They
also ensheathed the reticulin fibers. Interdigitating cells (IDCs) were
scattered throughout the framework. A few IDCs attached to the framework. In the lymph follicle (LF), reticulum cells were not a-SMA-positive.
The mesh of follicular dendritic cells (FDCs) was found in the germinal
center. In places, the reticulin fibers were involved in the mesh of the
FDCs and covered by the cytoplasm of FDCs. In the MZ, a-SMA-positive
reticulum cells were arranged in a mesh pattern and ensheathed the fine
reticulin fibers.
Conclusion: The reticular framework of the PALS, LF, and MZ is
specialized into heterogeneous components in the human spleen. The
heterogeneity of the framework may induce the segregation of T and B
lymphocytes. Anat. Rec. 249:486–494, 1997. r 1997 Wiley-Liss, Inc.
Key words: reticular framework; human spleen; white pulp; marginal
zone; heterogeneity
The white pulp (WP) and marginal zone (MZ) constitute the immunologically active compartment of the
spleen. In the WP, there are two distinct regions, the
periarteriolar lymphoid sheath (PALS) and the lymph
follicle (LF). The MZ is located between the WP and the
red pulp. The basic framework of the WP and MZ
consists of reticulum cells and reticulin fibers (Veerman
and Van Ewijk, 1975a; Sasou and Sugai, 1992). However, a distinct microenvironment is formed in the reticular framework of the PALS, LF, and MZ, respectively.
The PALS is a thymus-dependent area in which T
lymphocytes predominate (Parrott et al., 1996; Goldschneider and McGregor, 1973). The LF and MZ are B
lymphocyte areas (Goldschneider and McGregor, 1973;
r 1997 WILEY-LISS, INC.
Kumararatne et al., 1981). However, the cellular composition of the MZ comprises intermediate-sized B lymphocytes, and the immunophenotype of these lymphocytes
is different from the B lymphocytes in the mantle zone
of the LF (Kumararatne et al., 1981; Bazin et al., 1982;
Van Krieken et al., 1989; Satoh, 1991). In the PALS and
LF, interdigitating cells (IDCs) and follicular dendritic
cells (FDCs) create a distinct microenvironment and
play a role in the homing mechanism of T and B
*Correspondence to: Takashi Satoh, M.D., Department of Pathology,
School of Medicine, Iwate Medical University, Uchimaru 19-1, Morioka
020, Japan. E-mail: tsatoh@iwate-med.ac.jp
Received 12 March 1997; Accepted 1 August 1997
487
RETICULAR FRAMEWORK WHITE PULP/MARGINAL ZONE
lymphocytes, respectively (Veerman and Van Ewijk,
1975; Wood et al., 1985).
The enzyme histochemical variety of reticulum cells
in the WP of the human spleen has been well documented by Müller-Hermelink et al. (1979). A heterogeneous population of reticulum cells was immunohistochemically observed in the WP of the rat spleen (Van
den Berg et al., 1989). Yoshida et al. (1991) proved the
antigenic heterogeneity of the reticular framework in
the WP of the mouse spleen in relation to lymphoid
subclasses. They discovered that the reticulum cells are
heterogeneous in the PALS and LF. A recent study
TABLE 1. Clinical features
Case
Age
(yr)
Sex
1
2
3
4
5
59
38
73
65
33
m
m
m
f
m
6
7
74
77
m
m
8
33
9
2
Splenic
weight (g)
701
8501
781
651
5001
Perfusion
1
1
1
1
1
2
2
f
100
not
weighed
85
f
40
2
2
Clinical diagnosis
Gastric cancer
Liver cirrhosis
Gastric cancer
Gastric cancer
Hereditary
spherocytosis
Gastric cancer
Gastric cancer
Idiopathic thrombocytopenic purpura
Idiopathic thrombocytopenic purpura
1Before perfusion.
revealed that the reticular mesh localized between the
MZ and WP expresses mucosal addressin cell adhesion
molecule-1 in the mouse spleen and plays an essential
role in the lymphocyte homing and compartmentalization mechanism in the WP (Tanaka et al., 1996).
The aim of the present study is to characterize the
reticular framework of the WP and MZ of human
spleen, using immunohistochemistry, confocal laser
scanning, and electron microscopy.
MATERIALS AND METHODS
Nine surgically resected human spleens were investigated, and their description is summarized in Table 1.
Five spleens were perfused by the arterial and venous
pressure-loading method (Suzuki et al., 1989), using
Ringer’s solution containing heparin (150 IU/l) to wash
out the free cells. The spleens were then fixed by
perfusion with 2.8% glutaraldehyde solution in 0.06 M
phosphate buffer. They were cut into 10 mm slices and
further fixed in 10% buffered formalin solution for 3
days. The other four spleens were not perfused. They
were directly cut into 10 mm slices and fixed in 10%
buffered formalin solution for 2 days. Tissue blocks,
measuring 15 x 10 x 5 mm, were cut from both the
perfusion- and nonperfusion-fixed materials, and then
embedded in paraffin after dehydration in a graded
ethanol series. Serial sections were prepared for hematoxylin-eosin, silver staining (Gomori’s method), and
immunohistochemical examination.
TABLE 2. Antibodies used for immunohistochemistry
Antibodies
Type IV collagen
a-smooth muscle actin
S-100 protein
UCHL-1 (CD45RO)
L26 (CD20/cy)
Ki-M4P
Reactivity
Working dilution
Source
Type IV collagen
a-smooth muscle isoform of actin
Interdigitating cells
T lymphocytes
B lymphocytes
Follicular dendritic cells
1:100
1:100
1:200
1:200
1:100
1:1,000
DAKO
DAKO
DAKO
DAKO
DAKO
Prof. H.J. Radzun
Göttingen, Germany
Fig. 1. (a) Silver impregnation. The number and spatial orientation
of reticulin fibers are different in the PALS, LF, and MZ. In the PALS,
several layers of reticulin fibers run parallel to the central artery. In
the LF, reticulin fibers are sparse. Fine reticulin fibers form a mesh
structure in the MZ. x 100. (b) Immunostaining of type IV collagen.
The reticulin fibers in the PALS, LF, and MZ are immunostained for
type IV collage n. x 250.
488
T. SATOH ET AL.
Fig. 2. Immunostaining of a-SMA (brown). (a) The WP is clearly bordered by a-SMA-positive
spindle-shaped or stellate cells. x 100. (b) A few layers of a-SMA-positive cells (arrowheads) were found at
the border of the LF and MZ. In the MZ, a-SMA-positive cells are arranged in a mesh pattern. x 250.
Fig. 3. Double immunostaining of a-SMA (brown) and UCHL-1
(blue). a-SMA-positive cells form the reticular framework of the T
lymphocyte area (PALS).
Fig. 4. Double immunostaining of a-SMA (brown) and L26 (blue). In
the LF, no a-SMA-positive cells are found except for the smooth muscle
cells of the blood vessels. x 100.
Immunohistochemistry for Light Microscopy
technique (Shi et al., 1991) was applied for the retrieval
of the antigen.
For double immunostaining, the first antigen was
visualized in red as described above. After washing by
PBS, the SABC or APAAP method was applied to the
second antigen, which was visualized in blue with the
aid of alkaline phosphatase by incubating sections in 1
mg/ml naphthol AS phosphate (Sigma, St. Louis, MO),
1 mg/ml Fast blue BB salt (Sigma), and 1 mM Levamisole (Sigma) in 0.05 M propandiol buffer, pH 9.75.
The antibodies used in the present study are summarized in Table 2. Commercially available staining kits
(Histofine SAB-PO and SAB-AP, Nichirei, Tokyo, and
DAKO APAAP kit, DAKO, Denmark) were used. After
deparaffinization or silver impregnation, the sections
were immersed in methanol-H2O2 solution for 30 min to
block endogenous peroxidase activity. Nonspecific binding of antibodies was blocked by incubation with normal goat or rabbit serum for 15 min at room temperature. The sections were incubated with primary
antibodies for 2 hr at room temperature, and then
treated using the streptavidin biotin complex (SABC)
method. Each step was followed by repeated washing in
phosphate-buffered saline (PBS) adjusted to pH 7.4.
Coloration was developed in 3-amino-9-ethylcarbazole
solution (Graham et al., 1965). The sections were
counterstained with hematoxylin. In immunostaining
of type IV collagen, the microwave oven heating-
Three-dimensional Analysis of the Reticular Framework
Formalin-fixed spleens were cut into 50 µm slices
with a microslicer (Dosaka, Kyoto, Japan). Sections
were immunostained with anti-a-SMA antibodies using
the SABC method and then incubated with FITCconjugated streptavidine (DAKO). The sections were
attached to glass slides and covered by a coverglass.
Images of the reticular framework were obtained using
RETICULAR FRAMEWORK WHITE PULP/MARGINAL ZONE
489
Fig. 5. Silver impregnation (black) and immunostaining of a-SMA (brown). (a) The distribution of the
a-SMA-positive cells corresponds to that of the reticulin fibers. x 100. (b) a-SMA-positive cells attach to
and ensheath the reticulin fibers. x 250.
Fig. 6. Double immunostaining of a-SMA (brown) and S-100 protein (blue). IDCs attach to the
a-SMA-positive cells. x 500.
Fig. 7. Silver impregnation (black) and immunostaining of Ki-M4P (red). In the germinal center of the
LF, the reticulin fibers are involved in the mesh of the FDCs. x 500.
a confocal laser scanning microscope (LSM-GB 200 type
CLSM Olympus, Tokyo, Japan). Fluorescence of FITC
was obtained using 488 nm argon/krypton laser excitation. Serial sections were analyzed at 0.8 µm intervals.
MICRO VOXEL Ver. 2.2 software (INDEC, Capitola,
CA) was used for the three-dimensional reconstruction.
Immuno-electron Microscopy
Tissue blocks were fixed in 1% glutaraldehyde solution and 4% PLP at 4 °C for 1 day, then cut into 30 µm
slices with a microslicer (Dosaka). The immunostaining
procedure was the same as used for light microscopy.
The sections were incubated with antibodies for 4 hr at
room temperature. Coloration was developed in DAB
solution (WAKO, Osaka, Japan) to which H2O2 was
added at 0.015%. After immunostaining, the sections
were postfixed with 1% glutaraldehyde and 1% osmium
tetroxide solution, dehydrated in a graded ethanol
series, and embedded in Epon. Ultrathin sections were
stained with uranyl citrate and examined using an
electron microscope (H-7100 Hitachi, Tokyo, Japan).
Electron Microscopy
For transmission electron microscopy, tissue blocks,
measuring 1 x 1 x 1 mm in size, were prepared from the
perfusion-fixed spleens. They were postfixed in a 1%
osmium tetroxide solution for 2 hr and embedded in
Epon after dehydration in a graded ethanol series.
Ultrathin sections were stained with uranyl acetate
and lead citrate, then examined using a transmission
electron microscope (H-7100 Hitachi).
RESULTS
Light Microscopy
The sections treated by silver impregnation for reticulin fibers (Gomori’s method) revealed a basic reticular
framework in the WP and MZ (Fig. 1a). The number
490
T. SATOH ET AL.
Fig. 8. Three-dimensional analysis of the reticular framework of the WP using a confocal laser scanning
microscope. a-SMA-positive cells clearly demarcate the WP (arrows). In the PALS, a wall-like structure is
formed by a-SMA-positive cells. x 600.
Fig. 9. (a) Ultrastructure of the reticulum cell (R) in the PALS. The reticulum cell has bundles of
microfilaments with dense bodies (arrowheads). The cytoplasm ensheathes the reticulin fibers (rf). x 5250.
(b) Immuno-electron microscopy of a-SMA. The cytoplasm of the reticulum cell (R) is a-SMA-positive
(double arrowheads). x 5000.
RETICULAR FRAMEWORK WHITE PULP/MARGINAL ZONE
491
Fig. 10. Ultrastructure of the IDC. The IDC extends cytoplasmic projections between the lymphocytes
and entwines cytoplasmic projections around the reticulin fibers (arrowheads). x 4500.
and spatial orientation of reticulin fibers were different
in the WP and MZ.
In the PALS, several layers of reticulin fibers ran
parallel to the central artery, which showed a stratiform pattern in longitudinal sections and a circumferential pattern in cross sections. In the LF, reticulin fibers
were sparse. A few layers of reticulin fibers bordered
the LF and MZ.
The reticulin fibers of the MZ were quite fine and
anastomosing, forming a mesh structure.
Immunohistochemistry
The reticulin fibers of the WP and MZ were immunostained for type IV collagen (Fig. lb). The WP was
clearly bordered by a-SMA-positive spindle-shaped or
stellate cells (Figs. 2a,b). They were connected by their
cytoplasmic processes in places. At the border of the LF
and MZ, a few layers of a-SMA-positive cells were found
(Fig. 2b). The distribution of a-SMA-positive cells in the
WP was unique and characteristic. Double immunostaining of a-SMA and UCHL-1 or L26 revealed that
a-SMA-positive cells were selectively distributed in the
PALS (Figs. 3,4). At the perifollicular region, T lymphocytes were found between a-SMA-positive cells (Fig. 3).
Silver impregnation and immunostaining of the a-SMA
disclosed the close relation of a-SMA-positive cells and
reticulin fibers (Fig. 5a). a-SMA-positive cells attached
to and ensheathed the reticulin fibers (Fig. 5b). Interdigitating cells (IDCs) were scattered throughout the reticu-
lar framework. Several IDCs attached to the a-SMApositive cells (Fig.6).
In the LF, no a-SMA-positive spindle-shaped or stellate cells were found except for the smooth muscle cells
of blood vessels (Fig. 4). Immunohistochemistry of
Ki-M4P revealed the mesh of follicular dendritic cells
(FDCs) in the germinal center (Fig. 7). In places, the
reticulin fibers were involved in the mesh of the FDCs
and ensheathed by the cytoplasm of the FDCs (Fig. 7).
a-SMA-positive cells were arranged in a mesh pattern in the MZ (Fig. 2b). The fine reticulin fibers of the
MZ were covered by the cytoplasm of the a-SMApositive cells (Fig. 5b).
Three-dimensional Analysis of Reticular Framework
a-SMA-positive cells clearly demarcated the WP. In
the PALS, they extended their cytoplasm three-dimensionally and formed a wall-like structure (Fig. 8). A
mesh structure was formed by a-SMA-positive cells in
the MZ.
Electron and Immuno-electron Microscopy
Free cells remained in the WP after perfusion,
whereas they were partly washed away in the MZ. The
number and spatial orientation of the reticulin fibers
were different as seen by light microscopy.
The framework of the WP was constructed of reticulin fibers and reticulum cells. The cytoplasm of the
reticulum cells ensheathed the reticulin fibers (Fig. 9a),
492
T. SATOH ET AL.
Fig. 11. Immuno-electron microscopy of Ki-M4P. The dendritic processes of the FDCs (arrowheads)
extend between the lymphocytes and ensheath the reticulin fibers (rf). x 4500.
although some reticulin fibers were not enclosed. Reticulum cells in the PALS had bundles of microfilaments
with dense bodies (Fig. 9a). Immmuno-electron microscopy revealed that the reticulum cells in the PALS were
a-SMA-positive (Fig. 9b). IDCs extended their cytoplasmic projections between the lymphocytes in the PALS.
In places, the cytoplasm of IDCs attached to reticulum
cells. Several IDCs directly entwined their cytoplasmic
processes around reticulin fibers (Fig. 10). The reticulum cells in the LF were a-SMA-negative. FDCs elongated their slender cytoplasmic processes among the
lymphocytes and covered the reticulin fibers (Fig. 11).
In the MZ, reticulin fibers and reticulum cells formed
the framework of the MZ (Fig. 12a). The reticulin fibers
were ensheathed by the cytoplasm of the reticulum
cells, which were a-SMA-positive. The cytoplasm of the
reticulum cells contained bundles of microfilaments
with dense bodies and was connected with that of other
reticulum cells. An intermediate junction was observed
between their cytoplasms (Fig. 12b).
DISCUSSION
In the lymphatic tissues, reticulum cells and reticulin
fibers form the basic reticular framework. T and B
lymphocyte areas are involved in the reticular framework, and a specific microenvironment is prepared for
the lymphocytes in each area, respectively.
The spleens of human and rodent have an open
circulation (Weiss, 1984; Sasou et al., 1986; Satodate et
al., 1986a). The splenic arteries terminate in the splenic
cord and the marginal zone (MZ). The marginal zone
bridging channel was first described by Mitchell (1973),
especially as an exit pathway from the PALS to the red
pulp. However, this channel also has been described by
other authors (Van Ewijk and Van der Kwast, 1980;
Brelińska et al., 1984; Pellas and Weiss, 1990; Satoh,
1991) as an entrance pathway of T and B lymphocytes
from the red pulp to the PALS. T and B lymphocytes
from the blood are segregated during intrasplenic migration and are selectively sorted in the reticular framework according to the distinct microenvironment. Among
the various stromal cells of the lymphatic tissues, the
dendritic cells are thought to provide a microenvironment specific for lymphoid subclasses. IDCs and FDCs
are found in the T and B lymphocyte area, respectively
(Veerman and Van Ewijk, 1975a; Wood et al., 1985).
Dijkstra et al. (1982) demonstrated that during the
regeneration process of heterotropic autotransplanted
splenic implants, T and B lymphocytes show a specific
homing pattern in the developing WP and that the
newly formed reticulum determines the distribution of
the homing lymphocytes.
Reticulin fibers were commonly positive for type IV
collagen in the WP and MZ in the present study. Type
IV collagen is the major protein in basement membranes (Martinetz-Hernandez and Amenta, 1983). Foidart et al. (1980) suggest that laminin is an ubiquitous
component of basement membranes in addition to type
IV collagen, although the distribution of laminin was
not examined in the present study. Type III collagen,
RETICULAR FRAMEWORK WHITE PULP/MARGINAL ZONE
493
Fig. 12. Ultrastructure of the reticular framework in the MZ. (a)
Reticulum cells (R) and reticulin fibers (rf) form the mesh. The
cytoplasm of each reticulum cell has bundles of microfilaments with
dense bodies and ensheathes the reticulin fibers (small arrowheads).
x 6000. (b) An intermediate junction is observed between the cytoplasms of the reticulum cells (large arrowheads). x 25500.
which is mainly localized in the capsule and trabeculae,
is also contained in matrix proteins of the reticulin
fibers of the WP and MZ, although it is absent in the
early stage of the neonatal development of the WP and
MZ (Macarak et al., 1986; Liakka et al., 1991).
The present study demonstrated that heterogeneous
reticulum cells formed the reticular framework of the
WP and MZ. a-SMA-positive reticulum cells delimited
the WP from the surrounding MZ and were arranged
similar to the marginal metallophil cells of the rat
spleen (Snook, 1964; Satodate et al., 1971) in the
perifollicular region. In the rat spleen, marginal sinuses, formed by the arterial terminals of the WP, also
envelop the WP and bound the inner edge of the MZ
(Snook, 1964; Sasou et al., 1976), although these structures are not found in the human spleen (Sasou et al.,
1986). In the WP, the distribution of a-SMA-positive
reticulum cells corresponded to the types of lymphoid
subclasses and formed the reticular framework of the
T-lymphocyte area.
Actin is an ubiquitous cytoskeletal protein in microfilaments. a-SMA is the isoform of actin and routinely
used as a reliable probe for smooth muscle cell differentiation (Skalli et al., 1986). The ultrastructure and
immunoreactivity of the reticulum cells to a-SMA in the
T lymphocyte area suggest the myofibroblastic differentiation of these cells. In the LF, the reticulum cells
showed no positive reactivity for a-SMA. The mesh of
FDCs involved the reticular framework of the germinal
center. Although the ontogeny of FDCs remains contro-
versial (Parwaresch et al., 1983; Wood et al.,1985; Imai
and Yamakawa, 1996), FDCs seem to play a role in the
formation of the reticular framework of the germinal
center.
The MZ is a discrete compartment and functions as
an immunological filter where blood-borne antigens are
trapped (Veerman and Van Rooijen, 1975b; Satodate et
al., 1977; Satodate et al., 1986b). The major cell population of the MZ is medium-sized B lymphocytes (Van
Krieken et al., 1989). MZ B lymphocytes are CD23-,
KiB3- , IgD-, and enzyme histochemistry reveals the
alkaline phosphatase activity of MZ B lymphocytes
(Kumararatne et al., 1981; Bazin et al., 1982; Van
Krieken et al., 1989; Satoh, 1991). The immunophenotype and enzyme phenotype distinguish them from the
B lymphocytes in the mantle zone of the LF. The
reticulum cells in the MZ were a-SMA-positive and
their immunohistochemical character was different from
those in the LF.
Immunostaining of the a-SMA well characterizes the
reticular framework of the WP and MZ in the human
spleen and is applicable to the further examination of
the reticular framework in other human lymphoid
tissues. The results of the present study demonstrate
that the reticular framework of the PALS and LF in the
human spleen is specialized into heterogeneous components as in the rat and mouse spleen (Van den Berg et
al., 1989; Yoshida et al., 1991). Although the present
study has not yet proceeded to the functional analysis of
the reticular framework regarding the adhesion mol-
494
T. SATOH ET AL.
ecules or their ligand in lymphocyte homing and segregation, the antigenic heterogeneity of the reticular
framework of the PALS and LF may induce the segregation of the lymphoid subclasses.
ACKNOWLEDGMENTS
The authors thank Mr. S. Hayashi, Laboratory of
Electron Microscopy, School of Medicine, Iwate Medical
University, for his technical assistance in the threedimensional analysis.
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