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Development of the articular cavity in the rat temporomandibular joint with special reference to the behavior of endothelial cells and macrophages.

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THE ANATOMICAL RECORD PART A 286A:908 –916 (2005)
Development of the Articular Cavity
in the Rat Temporomandibular Joint
With Special Reference to the
Behavior of Endothelial Cells and
Macrophages
AKIKO SUZUKI,*1 KAYOKO NOZAWA-INOUE,1 NOBUYUKI IKEDA,2
NORIO AMIZUKA,1,3 KAZUHIRO ONO,2 RITSUO TAKAGI,2 AND
TAKEYASU MAEDA1,3
1
Division of Oral Anatomy, Department of Oral Biological Science, Niigata
University Graduate School of Medical and Dental Sciences, Niigata, Japan
2
Division of Oral Maxillofacial Surgery, Department of Oral Health Science, Niigata
University Graduate School of Medical and Dental Sciences, Niigata, Japan
3
Center for Transdisciplinary Research, Niigata University, Niigata, Japan
ABSTRACT
Previous developmental studies on the temporomandibular joint (TMJ) have proposed several hypotheses on the
formation of its articular cavity. However, detailed information is meager. The present study examined the formation
process of the articular cavity in the rat TMJ by immunocytochemistry for CD31, RECA-1, and ED1, which are useful
cellular markers for endothelial cells and monocyte/macrophage lineages, respectively. The upper articular cavity
formation had begun by embryonic day 21 (E21) and was completed at postnatal day 1 (P1) in advance of the lower
cavitation; the latter took place from P1 to P3. The occurrence and distribution pattern of the CD31-, RECA-1-, and
ED1-positive cells differed between the upper and lower articular cavity-forming areas: the ED1-positive cells exclusively occurred in the area of the prospective upper articular cavity prior to its formation, while no ED1-positive cell
appeared in the lower cavity-forming area. In contrast, the CD31- and RECA-1-positive endothelial cells were restricted
to the lower cavity-forming area (never the prospective upper cavity) at E19 and diminished thereafter. Throughout the
cavity formation, we failed to find any apoptotic cells in the cavity formation area, indicating no involvement of
apoptosis in the cavity formation in TMJ. The present findings on the behaviors of endothelial cells and ED1-positive
cells show a possibility of different mechanism in the cavity formation between the upper and lower articular cavities
in the rat TMJ. The appearance of ED1-reactive cells and temporal vascularization may play crucial roles in the upper
and lower articular cavity formation, respectively. © 2005 Wiley-Liss, Inc.
Key words: temporomandibular joint; development; articular cavity formation; endothelial cell;
monocyte/macrophage lineages.
The temporomandibular joint (TMJ) is a bilateral synovial arthrosis between the mandibular fossa of the temporal bone and the mandibular condyle. The articular cavity
of TMJ is completely separated by the articular disk to
divide into two cavities, the upper and lower articular
cavities. Both the upper articular cavity and articular disk
involve a sliding movement of the condyle, whereas the
lower one plays a role in the rotation of the condyle
(Walmsley, 1964). These cavities are filled with the viscous synovial fluid, which makes these smooth jaw movements possible.
Previous developmental studies on the TMJ have paid
attention to the general development, including the developmental sequence of compositional elements such as the
mandibular condyle and articular disk, of the TMJ (Symons, 1952; Morimoto et al., 1987; Van der Linden et al.,
©
2005 WILEY-LISS, INC.
1987; Mérida-Velasco et al., 1993). Furthermore, a majority of developmental studies have focused on the individual development of the components— bony elements
Grant sponsor: Japanese Ministry of Education, Culture,
Sports, Science, and Technology; Grant number: 16659498.
*Correspondence to: Akiko Suzuki, Division of Oral Anatomy,
Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, 2-5274 Gakkochodori, Niigata 951-8514, Japan. Fax: 81-25-223-6499.
E-mail: a-suzuki@dent.niigata-u.ac.jp
Received 3 November 2004; Accepted 20 June 2005
DOI 10.1002/ar.a.20228
Published online 18 August 2005 in Wiley InterScience
(www.interscience.wiley.com).
ARTICULAR CAVITY FORMATION IN TMJ
(Bach-Petersen et al., 1994), lateral pterygoid muscle
(Ögütcen-Toller and Juniper, 1993, 1994), and ligaments
(Ögütcen-Toller, 1995)—around the TMJ in various animals. However, little information is available on the development of articular cavity in TMJ in detail in contrast
to the accumulation of knowledge on joints of other long
bones, such as limb joint.
Several hypotheses have been proposed for the mechanism of articular cavity formation during limb development (cf. Archer et al., 2003). The cavitation may be
caused by several factors, including cell death, enzymatic
degradation in the prospective cavity, differential growth
of opposing elements, differential matrix synthesis, and
mechanical influences (Andersen and Bro-Rasmusen,
1961; Mitrovic, 1977, 1978; Nalin et al., 1995; Abu-Hijleh
et al., 1997). These factors have been considered to adapt
to the mechanism of cavity formation in TMJ (Murray and
Drachman, 1969; Mitrovic, 1977; Linck and Porte, 1978;
Okada et al., 1981; Mérida-Velasco et al., 1999). However,
TMJ that belongs to a category of a secondary cartilage
with covering fibrous tissue is quite different from other
long bone joints at phylogenical and ontogenical aspects,
indicating that data on the other limb joints cannot directly adapt on the TMJ (for review, see Nozawa-Inoue et
al., 2003).
Ohnuki (2000) demonstrated the penetration of blood
vessels into the lower, never upper, articular cavity during
TMJ development in the human fetus by observation of
the serial sections. In our recent developmental study of
the synovial membrane (Ikeda et al., 2004), we noticed
communication between the lower articular cavity and the
surrounding blood vessels during the development of rat
TMJ. These findings indicate the possibility that the vascularization around the TMJ is closely related to the articular cavity formation. However, the involvement of vascularization in the cavity formation in TMJ remains
unclear due to the scarcity of developmental investigations of this issue. On the other hand, Linck and Porte
(1978) suggested crucial roles for macrophage-like type A
cells in the synovial lining layer in the formation of the
articular cavity as they serve in the absorption of cell
fragments and wastes, which are produced through the
articular cavity formation. However, the behavior of the
macrophage-like type A cells during the cavity formation
process in TMJ remains unknown.
The present study was therefore undertaken to investigate the formation process of the articular cavity in the rat
TMJ by immunocytochemistry for cellular markers for
endothelial cells and macrophages during the prenatal
and postnatal stages. It will focus on the chronological
changes in the appearance and distribution pattern of
endothelial cells and macrophages during upper and lower
articular cavity formation. At the early stage of the articular cavity formation, we further applied an Indian-ink
injection method to demonstrate vascularization as well
as in situ identification of fragmented DNA using TdTmediated dUTP-biotin nick end labeling (TUNEL) to detect apoptotic cells.
MATERIALS AND METHODS
All experiments were performed under guidelines of the
Niigata University Faculty of Dentistry Intramural Animal Use and Care Committee.
909
Tissue Preparation
A total of 48 Wistar rats was obtained at embryonic day
18 (E18), E19, and E21 (n ⫽ 10 each), as well as postnatal
day 1 (P1), P3, and P5 (n ⫽ 6 each). The onset of pregnancy
was determined by vaginal smearing, and the day sperm
was found in the smear was regarded as E0. We defined
the day of birth (P1) as 24 – 48 hr after birth. In order to
avoid developmental variations among the animals within
each day, suitable embryos and postnatal rats were selected by their crown-rump length (CRL; E18 ⫽ 19.8 –21.2
mm; E19 ⫽ 24.6 –26.4 mm; E21 ⫽ 33.8 –36.2 mm) and
their body weight (P1 ⫽ 7.0 – 8.0 g; P3 ⫽ 9.0 –11.0 g; P5 ⫽
11.0 –14.0 g) according to a report by González (1932).
Under anesthesia by an intraperitoneal injection of 8%
chloral hydrate (400 mg/kg), the postnatal animals were
perfused with a fixative containing 4% paraformaldehyde
and 0.0125% glutaraldehyde in a 0.1 M phosphate buffer
(pH 7.4). The fetuses were deeply anesthetized in the
same manner, decapitated, and fixed in the same fixative.
The removed heads were decalcified with a 5% ethylene
diamine tetra-acetic acid disodium (EDTA-2 Na) solution
at 4°C. One side of each head was equilibrated in a 30%
sucrose solution at 4°C overnight for cryoprotection and
embedded in an OCT compound (Leica, Nussloch, Germany). Serial sagittal sections were cut at a thickness of
35 ␮m in a cryostat (HM-500; Carl Zeiss, Jena, Germany)
and mounted onto silane-coated glass slides. The other
half of each head was embedded in paraffin. Serial paraffin sections were sagitally cut at a thickness of 5 ␮m. Some
sections were stained with hematoxylin and eosin (H&E)
for histological observations.
Immunohistochemistry
The cryostat sections were processed for immunocytochemistry using the avidin-biotin complex (ABC) method
according to Hsu et al. (1981). After an inhibition of endogenous peroxidase with 0.3% H2O2 in absolute methanol for 30 min, the sections were incubated for 24 hr at 4°C
with the primary antibodies. We used two kinds of monoclonal antibodies to CD31 (1:50; BD Pharmingen, NJ)
(DeLisser et al., 1994; Williams et al., 1996) and rat endothelial cell antigen (RECA-1; 1:80; Serotec, Oxford,
U.K.) (Duijvestijn et al., 1992) for endothelial cells. A
monoclonal ED1 antibody (1:500; Serotec), for detection of
monocyte/macrophage lineages (Dijkstra et al., 1985), was
applied for detection of macrophages. Prior to incubation
with an antibody to CD31, sections were pretreated with
proteinase K (1:10; Dako, Carpinteria, CA) for 20 min at
room temperature. The bound primary antibody was localized using biotinylated antimouse IgG for 2 hr and
subsequently ABC conjugated with peroxidase for 90 min
at room temperature (ABC kit; Vector Lab, Burlingame,
CA). Final visualization used 0.04% 3,3⬘-diaminobenzidine tetrahydrochloride and 0.0125% H2O2 in a 0.05 M
Tris-HCl buffer (pH 7.6). Some immunolabeled sections
were counterstained with methylene blue.
Immunohistochemical Controls
Immunohistochemical controls were performed by replacing the primary antibodies with nonimmune mouse
sera or PBS, and omitting the antimouse IgG or the ABC
conjugated with peroxidase. These control sections did not
reveal any immunoreaction. The characterization of the
antibodies and the origin of antigens have been previously
910
SUZUKI ET AL.
reported elsewhere (cf. Dijkstra et al., 1985; Duijvestijn et
al., 1992; DeLisser et al., 1994).
Vascular Indian-Ink Perfusion
Additional rats at E19, E21, and P1 (n ⫽ 8 each) were
perfused with the same fixative mentioned above and
followed with Indian ink containing 5% gelatin solution
(50°C) via left ventricle under deep anesthesia. The perfused heads were immediately frozen in liquid nitrogen,
embedded in an OCT compound (Leica), and sectioned at
a thickness of 35 ␮m in a cryostat. They were slightly
counterstained with methylene blue.
In Situ Identification of Fragmented DNA Using
TdT-Mediated dUTP-Biotin Nick End Labeling
Dewaxed sections were end-labeled with terminal deoxynucleotidyl transferase using a TACS 2 TdT-Blue Label in situ Apoptosis Detection Kit (Trevigen, Gaithersburg, MD). According to the manufacturer’s instructions,
the sections were treated with proteinase K (1:50) for 15
min, 3% H2O2 in methanol for 5 min, and 1 ⫻ TdT labeling
buffer for 5 min at room temperature; Twenty ␮l labeling
reaction mixture containing TdT, dNTP mix, 50 ⫻ cation
stock (Mn2⫹), TdT enzyme, and 1 ⫻ TdT labeling buffer
was then applied to each specimen at 37°C for 1 hr. The
slides were incubated with a 1 ⫻ TdT stop buffer for 5 min
and subsequently labeled with a streptavidin-HRP solution containing blue-streptavidin diluent and streptavidin-HRP (750 ␮l: 1 ␮l) for 15 min at room temperature.
Finally, they were subjected to the blue label solution. The
specimens were counterstained with nuclear fast red.
RESULTS
Embryonic Day 18
The anlagen of the condyle and the temporal bone were
recognizable as a condensation of the mesenchymal cells,
and the mesenchymal cells were sparsely distributed between their anlagen (Fig. 1a, c, and e). No tissue separation occurred in future joints, indicating the absence of
any formation of the articular cavity at this stage. Observation of the sections showed the presence of a few blood
capillaries filled with red blood cells at the surface of the
developing condyle (Fig. 1b). The endothelial cells of these
capillaries exhibited a weak immunoreaction for CD31
(Fig. 1d) and RECA-1 (data not shown) at this stage.
However, no blood capillaries existed in the mesenchymal
tissue between the anlagen of the condyle and temporal
bone (Fig. 1c). ED1 immunostaining demonstrated a
sparse distribution of immunoreactive cells in the mesenchymal tissue between the anlagen of the condyle and
temporal bone (Fig. 1e). These positive cells, ovoid in
shape, had a rich cytoplasm and large nucleus (Fig. 1f).
surface of the developing condyle. No tissue separation
was found between the prospective articular disk and the
developing condyle. However, we failed to find any
TUNEL-positive cells, indicative of apoptotic cells, in
these areas (Fig. 1m) at this stage, in spite of the existence
of several apoptotic cells at the chondro-osseous junction
of mandible (Fig. 1n). The endothelial cells in some flat
blood capillaries immunopositive for CD31 and RECA-1
were often observed to run along the developing condyle
(Fig. 1g–j). However, no blood capillary was recognizable
in the area between the developing temporal bone and
prospective articular disk. On the other hand, ED1-positive elements increased drastically compared with the
previous stage; numerous ED1-immunoreactive cells occurred in the mesenchymal tissue between the developing
temporal bone and prospective articular disk (Fig. 1k).
These cells changed in their profiles from ovoid to spindle
at this stage (Fig. 1l). Their long axis appeared to lie in
parallel to the convexity of the condylar surface. However,
ED1-positive cells occurred rarely near the surface of the
developing condyle (Fig. 1k), which contained CD31- and
RECA-1-positive endothelial cells (Fig. 1g–j).
Embryonic Day 21
An apparent tissue separation was clearly recognizable
between the mandibular fossa and the condensation of
mesenchymal cells, i.e., prospective articular disk, indicating the commencement of formation of the upper articular
cavity (Fig. 2a and e). However, no formation of such a
tissue separation of the mesenchymal tissues was yet
discernible in the prospective lower articular cavity (Fig.
2a and e). Even at this stage, no apoptotic cell with
TUNEL reaction was identified between the temporal
bone and developing condyle (data not shown). In contrast, several CD31- and RECA-1-immunopositive endothelial cells remained between the surface of the developing condyle and the prospective articular disk (Fig. 2a– c).
In the vicinity of the condylar surface, these endothelial
cells were observed either to run along the condylar surface or to climb up perpendicularly in the prospective
fibrous layer of the condyle (Fig. 2b and c). The Indianink-injected sections could confirm such a characteristic
distribution of the blood capillaries (Fig. 2d). A dense
distribution of ED1-positive cells was discernable at the
region of the forming upper articular cavity, notably an
intense immunoreaction in the temporal bone (Fig. 2e).
The ED1-immunoreactivity existed in neither the prospective articular disk nor the area between the condylar
surface and disk, which had endothelial cells. At the upper
anterior region of the articular cavity, the ED1-positive
cells changed their profiles to appear ovoid or irregular in
shape (Fig. 2f), these profiles being similar to those of the
synovial lining cells in the mature synovium (Ikeda et al.,
2004).
Embryonic Day 19
Intramembranous and endochondral ossification had already begun in the temporal bone and the developing
condyle, respectively (Fig. 1g, k, and m). The mesenchymal tissues near the mandibular fossa of the temporal
bone appeared to become sparse due to the expansion of
the intercellular spaces of the mesenchymal cells. The
slender mesenchymal cells aggregated to form a few cell
layers, which might be regarded as a prospective articular
disk (asterisk in Fig. 1g, k, and m), in the vicinity of the
Postnatal Day 1
The upper articular cavity had expanded in the anterior-posterior direction (Fig. 2g and i). The formation of
the lower articular cavity also had begun between the
articular disk and the condyle, being especially prominent
at the anterior and posterior regions (Fig. 2g and i). However, the articular disk was not separated from the condylar surface at the central position of the lower articular
cavity. The blood capillaries with CD31- and RECA-1-
ARTICULAR CAVITY FORMATION IN TMJ
911
Fig. 1. Sagittal sections of the developing rat TMJ at E18 (a–f) and
E19 (g–n). H&E staining (a and b), immunolabeled with antisera against
CD31 (c, d, g, and h), RECA-1 (i and j), and ED1 (e, f, k, and l), and TUNEL
reaction (m and n). The left side of all figures indicates the anterior
direction. a: Mesenchymal cells are observed to gather at the anlagen of
the condyle (C) and the temporal bone (T). Neither the articular cavity nor
the disk is formed at this stage. b: Higher magnification of the boxed
area in a. A capillary with red blood cells is seen to run on the surface of
the condylar anlage. c and d: CD31 immunoreactivity is found in the
endothelial cells with slender profiles near the condylar anlage (C). e: The
mesenchymal tissue between the anlagen of condyle (C) and temporal
bone (T) contains a few ED1-immunopositive cells. f: In a higher-magnified view, the ED1-positive cells display ovoid profiles, and the immunoreactions take on a granular appearance in their cytoplasm. g: Compared with the previous stage, the mesenchymal cells at the superior
portion near the mandibular fossa (T) appear to become sparse due to
the expansion of their intercellular spaces. Near the surface of the
condylar anlage (C), the mesenchymal cells, spindle in shape, form a few
cell layers (asterisk), an analogue to the future articular disk. g–j: The
CD31- (g and h) and RECA-1- (i and j) positive endothelial cells running
between the surface of the developing condyle (C) and the future articular disk (asterisk). RECA-1-positive endothelial cells continue to the
blood capillaries at the posterior portion (j). k and l: The ED1-positive
cells that display irregular or slender shapes (l) increase in number in the
mesenchymal tissue between the temporal bone (T) and the future
articular disk (asterisk). m and n: No TUNEL-positive cell is recognizable
in the mesenchymal tissues between the temporal bone (T) and condylar
anlage (C; m), although a few TUNEL-positive cells (arrows in n) are
scattered only at the chondro-osseous junction of the mandible. Scale
bars ⫽ 150 ␮m (a); 20 ␮m (b, d, f, and l); 100 ␮m (c, e, g, k, m, and n);
and 50 ␮m (h–j).
immunoreactivity drastically decreased in number at the
forming lower articular cavity compared with the previous
stage. Interestingly, the immunopositive endothelial cells
remained in the central portion of the lower articular
cavity, where no cavitation had occurred (Fig. 2g and h).
In contrast, the endothelial cells diminished in the area in
which the lower articular cavity had been clearly formed
(Fig. 2g). Many immunopositive endothelial cells were
also observed in the synovial membrane. Numerous ED1positive cells were found in the articular disk and the
synovial membrane but not in the lower articular cavityforming area (Fig. 2i).
Postnatal Day 3
The upper and lower articular cavity had further expanded in anterior and posterior directions (Fig. 3a). Since
the lower articular cavity also had been formed at the
central portion, the articular disk was completely separated from the condylar surface at this stage. A part of the
synovial membrane had protruded into the articular cavity in the posterior portion of the upper articular cavity to
form a synovial fold (Fig. 3a, c, and d). A few immunopositive endothelial cells remained in the fibrous layer of
the condylar surface (Fig. 3b) and the synovial membrane
912
SUZUKI ET AL.
Fig. 2. Photomicrographs at E21 (a–f) and P1 (g–i). Sections immunolabeled for CD31 (a, b, g, and h), RECA-1 (c), ED1 (e, f, and i), and
Indian-ink perfusion (d). a: An upper articular cavity (UC) has been
formed between the temporal bone (T) and the articular disk anlage
(asterisk). The blood capillaries with CD31 immunoreaction are found as
either running along the condylar surface or invading the condyle (C). b
and c: Higher magnification of the boxed area in a. The blood capillaries
consisting of CD31- (b) and RECA-1- (c) positive endothelial cells along
the condylar surface anastomose them ascending perpendicularly in the
condylar surface. d: Several blood capillaries containing Indian ink are
recognizable at the mesenchymal tissue between the condyle (C) and
prospective articular disk (asterisk). These capillaries run along the condylar surface (arrow) and climb up into the condyle (arrowhead). e and f:
Many ED1-positive cells are distributed around the upper articular cavity. The area between the articular disk anlage (asterisk) and the condylar
surface (C) does not contain any ED1-positive cells. The ED1-positive
cells in the upper articular cavity-forming area change their profiles from
spindle to ovoid (f). g and h: The enlargement of the upper articular cavity
(UC) has proceeded in the anterior-posterior direction. Formation of the
lower articular cavity has also commenced, but the articular disk (D)
remains in contact with the condyle (C) in the central portion of the
forming lower articular cavity. In comparison with the previous stage, the
CD31-positive cells have decreased in number. The capillaries entering
the condylar surface perpendicularly have disappeared (h). However,
many capillaries with CD31 immunoreaction are observed in both the
anterior and posterior portions of the articular disk and the synovial
membrane. i: In contrast to a dense distribution of ED1-positive cells in
the synovial membrane and the articular disk (D), no positive cells exist
in the lower articular cavity. Scale bars ⫽ 200 ␮m (a, e, g, and i); 50 ␮m
(b– d); 20 ␮m (f); and 40 ␮m (h).
(Fig. 3c). In contrast to the decrease of endothelial cells,
ED1-immunoreactive cells increased in number daily to be
distributed widely in the synovial membrane (Fig. 3d). In
the synovial fold, ED1-immunopositive and -negative cells
were arranged on the synovial surface (Fig. 3d), so we
could easily distinguish the synovial lining layer from the
sublining layer.
previous stage, and ED1-positive cells with ovoid profiles
were arranged there. The behaviors of endothelial cells
and ED1-positive cells during development of the rat TMJ
are given in Figure 4.
Postnatal Day 5
No remarkable change in the histological structures
was found at P5 except for the development of the synovial
fold at the posterior-superior portion of the articular cavity. The distribution of CD31- and RECA-1-immunopositive endothelial cells was unchanged; the cells remained
in the fibrous layer of the condylar surface and the synovial membrane. In the surface of the synovial fold, the
synovial lining cell layer thickened compared with the
DISCUSSION
The present immunocytochemical study was clearly
able to demonstrate the formation process of the articular
cavity in the rat TMJ and region-specific expression patterns of CD31, RECA-1, and ED1 immunoreactions in the
cavity-forming area, suggesting the possibility of the different mechanism of the cavitations between the upper
and lower articular cavities.
The mechanism on the formation of the articular cavities is controversial. To date, several hypotheses have
been proposed in limb joints; they include apoptosis, differential growth, vascularization, enzymatic degradation
ARTICULAR CAVITY FORMATION IN TMJ
913
Fig. 3. Micrographs at P3 (a–d) and P5 (e).
Stained with hematoxylin and eosin (a), CD31 (b
and c) and ED1 immunoreactions (d and e). a: Both
upper (UC) and lower articular cavities (LC) have
been widely expanded in the anterior and posterior
directions. A part of the synovial membrane protrudes into the articular cavity in the posterior portion of the upper articular cavity to form a synovial
fold (arrow). b: A few flat capillaries with CD31
immunoreaction (arrow) are observed in the fibrous layer of the condyle (C), but the articular disk
(D) lacks positive cells. c: The sublining tissue of
the synovial membrane in the synovial fold contains many CD31-positive capillaries (arrows). d:
Many ED1-positive cells are widely distributed in
the synovial membrane. In particular, ED1-positive
(arrows) and -negative cells are arranged alternatively in the synovial lining cell layer. The synovial
sublining layer also has many ED1-positive cells
with irregular or ovoid profiles (arrowheads). e: The
thick synovial lining cell layer is clearly distinguishable from the sublining layer. The synovial lining
(arrows) and sublining (arrowhead) layer contain
several ED1-positive cells with irregular profiles.
Scale bars ⫽ 100 ␮m (a); 20 ␮m (b– e).
of the cavity-forming area, and mechanical influences
(Andersen and Bro-Rasmusen, 1961; Mitrovic, 1977, 1978;
Kawai et al., 1982; Kajikawa, 1984; Nalin et al., 1995;
Abu-Hijleh et al., 1997). In spite of lack of detailed information, these hypotheses have been directly adopted on
the mechanism of cavity formation in the TMJ, which is
categorized in secondary cartilaginous joints such as sternoclavicular and acromioclavicular joints. For instance,
many researchers have failed to find apoptosis at the
cavity-forming area in long bone joints (Ballard and Holt,
1968; Murray and Drachman, 1969; Mitrovic, 1977, 1978;
Mori et al., 1995; Nalin et al., 1995; Kimura and Shiota,
1996; Kavanagh et al., 2002), while some studies have
detected it (Abu-Hijleh et al., 1997; Ito and Kida, 2000).
Matsuda et al. (1997) revealed no detection of apoptosis in
this area by biochemical and histochemical analyses with
the TUNEL method in TMJ development, consistent with
the present observations. These evidences lead us to suppose considerably low possibility of the involvement of
apoptosis in cavity formation in TMJ. Therefore, detailed
mechanism remains unclear in the articular cavity formation of the TMJ.
The present immunostaining with the CD31 and
RECA-1 antibodies demonstrated the region- and stage-
specific localizations of blood capillaries throughout the
cavity formation process. Some reports have shown
changes in vascularization during the articular cavity formation; in the knee joint of the mouse and chick embryo,
the capillaries invaded the forming articular cavity from
the surrounding mesenchymal tissue into the prospective
articular cavity, and the endothelial-like cells lining the
cavity developed slender protoplasmic projections to overspread the joint cavity (Kawai et al., 1982; Kajikawa,
1984). In TMJ development, the blood vessels have been
reported to run posteroanteriorly on the lower surface of
the articular disk at the early stages of articular cavity
formation (Morimoto et al., 1987; Ohnuki, 2000) in the
human fetus. In particular, Ohnuki (2000) found the disintegration of the blood vessels as merged with the forming lower articular cavity, suggesting that blood vessels
serve as a partition between the articular disk and the
condyle to produce a space for the lower articular cavity in
the mesenchymal tissue. The current observations by
CD31 and RECA-1 immunocytochemistry and Indian-ink
perfusion techniques suppose the involvement of blood
vessels in the lower articular cavity formation.
Another interesting finding is the disappearance of the
blood capillaries in the lower cavity-forming area after
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SUZUKI ET AL.
Fig. 4. A schematic drawing of the distribution
of endothelial cells and macrophages in the developing rat TMJ.
cavitation. One possible explanation may be the commencement of jaw movements because the capillaries decreased in number in the lower articular cavity after birth.
We can readily suppose that the mechanical pressure from
jaw movements induces the disappearance of endothelial
cells. This idea is supported by findings that spinal cordinjured animals had defective articular cavities (Drachman and Sokoloff, 1966). Thus, we can regard mechanical
stimulus and blood vessels as one of the essential factors
to induce cavitation and to make a space, respectively.
However, mechanism of the elimination process of vascular elements remains unknown.
It is noteworthy that ED1 immunocytochemistry demonstrated the aggregation of monocyte/macrophage lineages in the prospective upper articular cavity in TMJ, in
contrast to the occurrence of CD31- and RECA-1-positive
blood capillaries in the future lower cavity. As far as we
know, this is the first report to demonstrate the aggregation of monocyte/macrophage lineages in the future upper
articular cavity in TMJ. The appearance of an ED1-positive cells seems to be closely related to the period of the
commencement of the upper cavity formation. The predominant distribution of ED1-positive cells suggested the
presence of apoptosis in the upper cavity-forming area. In
spite of careful observations, however, we failed to find
any apoptotic cells in this area, matching the findings by
Matsuda et al. (1997). This means that ED1-positive cells
do not participate in the phagocytosis of apoptotic cells
during the formation of the upper joint cavity. On the
other hand, experimental data have suggested the involvement of hyaluronic acid synthesis in joint cavity formation (Craig et al., 1990; Archer et al., 1994, 2003; Edwards et al., 1994; Pitsillides et al., 1995; Dowthwaite et
al., 1998). Thus, it is better to consider that the ED1positive cells play crucial roles in the elimination of intercellular substances such as a hyaluronic acid, not apoptotic cellular debris, from the upper articular cavity-forming
area.
It is generally accepted that the synovial lining layer
contains two kinds of lining cells, macrophage-like type A
cells and fibroblast-like type B cells, according to their
ultrastructural configurations (Barland et al., 1962;
ARTICULAR CAVITY FORMATION IN TMJ
Graabæk, 1984; Nozawa-Inoue et al., 1998, 2003; Iwanaga
et al., 2000). Observation of the synovial membrane in
osteopetrotic (op/op) mice showed a lack of type A cells
(Naito et al., 1991), strongly suggesting that type A cells
are differentiated from a monocyte lineage. Our previous
report (Ikeda et al., 2004) on the development of the rat
TMJ revealed the first detection of macrophage-like type
A cells in the synovial lining at P3 by electron microscope.
This observation suggests that the ED1-immunopositive
cells arranged on the synovial surface at P3 in this study
might be macrophage-like type A cells.
In conclusion, the region-specific and temporal occurrences of CD31-, RECA-1-, and ED1-positive cells during
development in rat TMJ suggest a possibility of a different
mechanism between the upper and lower cavity formation. Further investigations are needed to clarify the
mechanisms for the disappearance of endothelial cells and
the roles of ED1-positive cells in articular cavity formation.
ACKNOWLEDGMENTS
The authors thank Mr. M. Hoshino and Mr. K. Takeuchi, Division of Oral Anatomy, Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, for their technical assistance.
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