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The Junctional Epithelium: from Health to Disease
  1. D.D. Bosshardt*
  2. N.P. Lang


  1. Department of Periodontology and Fixed Prosthodontics, School of Dental Medicine, University
     of Berne, Freiburgstrasse 7, CH-3010 Berne, Switzerland;

  1.   *   corresponding author, dieter.bosshardt@zmk.unibe.ch



Next Section
Abstract
The junctional epithelium is located at a strategically important interface between the gingival
sulcus, populated with bacteria, and the periodontal soft and mineralized connective tissues that
need protection from becoming exposed to bacteria and their products. Its unique structural and
functional adaptation enables the junctional epithelium to control the constant microbiological
challenge. The antimicrobial defense mechanisms of the junctional epithelium, however, do not
preclude the development of gingival and periodontal lesions. The conversion of the junctional to
pocket epithelium, which is regarded as a hallmark in disease initiation, has been the focus of
intense research in recent years. Research has shown that the junctional epithelial cells may play a
much more active role in the innate defense mechanisms than previously assumed. They synthesize
a variety of molecules directly involved in the combat against bacteria and their products. In
addition, they express molecules that mediate the migration of polymorphonuclear leukocytes
toward  the bottom of the gingival sulcus. Periodontopathogens—such as Actinobacillus
actinomycetemcomitans or, in particular, Porphyromonas gingivalis—have developed sophisticated
methods to perturb the structural and functional integrity of the junctional epithelium. Research has
focused on the direct effects of gingipains, cysteine proteinases produced by Porphyromonas
gingivalis, on junctional epithelial cells. These virulence factors may specifically degrade components
of the cell-to-cell contacts. This review will focus on the unique structural organization of the
junctional epithelium, on the nature and functions of the various molecules expressed by its cells,
and on how gingipains may attenuate the junctional epithelium’s structural and functional integrity.


                                              junctional epithelium


                                                      tooth


                                                     implant


                                              periodontal diseases




Previous SectionNext Section
This review focuses on the unique structural organization of the junctional epithelium, on the nature
and functions of the various molecules expressed by its cells, and on how gingipains may attenuate
the junctional epithelium’s structural and functional integrity.
Previous SectionNext Section
(I) INTRODUCTION
The junctional epithelium is the epithelial component of the dento-gingival unit that is in contact
with the tooth surface. The innermost cells of the junctional epithelium form and maintain a tight
seal against the mineralized tooth surface, the so-called epithelial attachment (Schroeder and
Listgarten, 1977). The junctional epithelium may be regarded as the most interesting structure of
the gingiva. Its interposition between the underlying soft and mineralized connective tissues of the
periodontium (i.e., gingival connective tissue, periodontal ligament, alveolar bone, and root
cementum) points to its important roles in tissue homeostasis and defense against micro-organisms
and their products (for reviews, see Schroeder, 1996; Schroeder and Listgarten, 1997). Unlike other
appendages—such as scales of reptiles, feathers, hair, fingernails, claws, hoofs, and antlers—teeth
are transmucosal organs. As such, they are permanently exposed to a contaminated environment,
since the permanently wet, warm, and nutrient-rich oral cavity forms a perfect habitat in which
micro-organisms thrive. These micro-organisms form complex ecological systems that adhere to a
glycoprotein layer on solid and non-shedding surfaces and, therefore, are called biofilms. Since a
biofilm quickly forms on the exposed tooth surface, the tissues in the vicinity of this biofilm are
constantly challenged. Such aggravating external circumstances call for a specialized structural and
functional adaptation of the junctional epithelium to control the constant microbiological challenge.
In contrast to most other epithelia, there is no keratinizing epithelial cell layer at the free surface of
the junctional epithelium that could function as a physical barrier. Other structural and functional
characteristics of the junctional epithelium must compensate for the absence of this barrier. The
junctional epithelium fulfills this difficult task with its special structural framework and the
collaboration of its epithelial and non-epithelial cells that provide very potent antimicrobial
mechanisms. However, these defense mechanisms do not preclude the development of extensive
inflammatory lesions in the gingiva, and, occasionally, the inflammatory lesion may eventually
progress to the loss of bone and the connective tissue attachment to the tooth. The conversion of
the junctional epithelium to pocket epithelium is regarded as a hallmark in the progression of
gingivitis to periodontitis. However, data documenting the triggering pathogenic factors and the
subsequent cascade of cell and extracellular events leading to pocket formation are scarce. Recent
studies have shown that the junctional epithelial cells themselves may play a much more active role
in the innate defense system than previously assumed, by synthesizing a variety of molecules
involved in the combat against bacteria and their products. However, the lack of a tight physical seal
by the junctional epithelium may also allow bacteria and their products to penetrate the junctional
epithelium, thereby directly attacking the epithelial cells and attenuating their defense mechanisms.
Bacteria such as, e.g., Porphyromonas gingivalis have developed sophisticated strategies aimed at
perturbing the structural and functional integrity of the junctional epithelium, a mechanism that may
significantly contribute to the initiation of pocket formation and attachment loss. The aim of this
review is to discuss the structural and functional characteristics of this unique epithelial seal around
teeth, with a special focus on host-parasite interactions during the initial development of the
periodontal pocket.
Previous SectionNext Section
(II) THE DEVELOPMENT OF THE JUNCTIONAL
EPITHELIUM
The junctional epithelium forms as the tooth crown erupts into the oral cavity. Prior to the
emergence of the tooth into the oral cavity, the enamel surface is covered by the reduced enamel
epithelium that consists of reduced ameloblasts and the remaining cells of all other layers of the
enamel organ. The stratum intermedium cells of the reduced enamel epithelium and the oral
epithelial cells proliferate following breakdown of the interposed connective tissue (Ten Cate, 1998).
The 2 epithelia eventually fuse to form an epithelial cell mass.
When the tips of the cusps or the incisal edge of the crown breaches the oral mucosa (Ten Cate,
1998), or shortly before the establishment of the first contact between the reduced enamel
epithelium and the oral gingival epithelium (Schroeder, 1996), a slow cell transformation process
develops. Beginning orally and ending at the cemento-enamel junction 1 to 2 (Schroeder and
Listgarten, 1977) or 3 to 4 (Ten Cate, 1998) yrs later, the reduced enamel epithelium gradually
converts into junctional epithelium, a multilayer non-keratinizing squamous epithelium (Glavind and
Zander, 1970; Listgarten, 1972b; Schroeder and Listgarten, 1977; Schroeder, 1996). During the
transformation process, the reduced ameloblasts change their morphology from short columnar to
flattened cells that are oriented parallel to the enamel surface. Also, the cells external to the reduced
ameloblasts undergo a structural change. However, unlike the reduced and transformed ameloblasts,
these external cells regain mitotic activity. These transformed ameloblasts migrate in a coronal
direction, are exfoliated at the bottom of the sulcus, and eventually are replaced by the cells external
to the reduced/transformed ameloblasts (Schroeder, 1996).
It has been proposed that the junctional epithelium, which was originally derived from the reduced
enamel epithelium, may be replaced in time by a junctional epithelium formed by basal cells
originating from the oral gingival epithelium (Ten Cate, 1996). This holds true, at least, for de novo
formation of the junctional epithelium following gingivectomy (Salonen, 1986; Salonen et al., 1989).
However, basal epithelial cells other than those of oral gingival origin may also regenerate a
junctional epithelium (Listgarten, 1967, 1972b; Braga and Squier, 1980; Freeman, 1981).
Previous SectionNext Section
(III) STRUCTURE OF THE JUNCTIONAL EPITHELIUM
Anatomical Aspects
The junctional epithelium is part of the marginal ‘free’ gingiva, forms a collar peripheral to the
cervical region of the tooth, and hence is not visible intra-orally (Fig. 1⇔). In the interproximal area,
the junctional epithelia adjacent to neighboring teeth fuse to form the epithelial lining of the
interdental col. The coronal termination of the junctional epithelium is a free surface and is located
either at the bottom of the sulcus, at the gingival margin, or at the interdental col area. Under
pristine conditions, the epithelial seal extends from the cemento-enamel junction to the gingival
margin, averaging about 2 mm in height (Fig. 1⇔) (Gargiulo et al., 1961). ‘Normal’ gingiva, however,
expresses sub-clinical signs of slight inflammation (Brecx et al., 1987). Therefore, the coronal
termination of the junctional epithelium corresponds usually to the bottom of the gingival sulcus. At
its apical and lateral aspects, the junctional epithelium is bordered by soft connective tissue and, at
its coronal-most portion, also by the sulcular epithelium. The epithelium-connective tissue interface
is smooth, showing an only mild undulation coronally (Figs. 1⇔, 2⇔). Toward the tooth surface, the
junctional epithelial cells form and maintain the epithelial attachment (Schroeder and Listgarten,
1977). At its apical termination, the junctional epithelium—at least in porcine teeth—appears at
frequent intervals to be in continuity with the network of the epithelial rests of Malassez (Grant and
Bernick, 1969; Spouge, 1984).
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Figure 1.
Light microscopic view of human gingiva (from a young, clinically healthy subject) illustrating its
dimensions and relations. ABC, alveolar bone crest; AEFC, acellular extrinsic fiber cementum; CEJ,
cemento-enamel junction; CT, gingival connective tissue; D, dentin; ES, enamel space; GM, gingival
margin; JE, junctional epithelium; OGE, oral gingival epithelium; OSE, oral sulcular epithelium; PL,
periodontal ligament. Courtesy of Dr. H.E. Schroeder.




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Figure 2.
Back-scattered scanning electron micrograph showing the tapering off, in the apical direction, of the
junctional epithelium (JE) in a porcine tooth with a clinically healthy gingiva. CEJ, cemento-enamel
junction; CT, gingival connective tissue; D, dentin; ES, enamel space. Courtesy of Dr. A. Nanci.
The Junctional Epithelial and Interstitial Cells
The junctional epithelium tapers off in the apical direction, and it consists of 15 to 30 cell layers
coronally and only 1 to 3 cell layers at its apical termination (Figs. 1⇔, 2⇔). It is a stratified
squamous non-keratinizing epithelium that is made up of 2 strata only, i.e., a basal layer (the
stratum basale) and a suprabasal layer (the stratum suprabasale). The basal cells face the gingival
connective tissue. The basal cells and the adjacent 1 to 2 suprabasal cell layers are cuboidal to
slightly spindle-shaped. All remaining cells of the suprabasal layer are flat, oriented parallel to the
tooth surface, and closely resemble each other (Fig. 3⇔). The innermost suprabasal cells (facing the
tooth surface) are also called DAT cells (= directly attached to the tooth) (Salonen et al., 1989). They
form and maintain the ‘internal basal lamina’ that faces the tooth surface.




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Figure 3.
Transmission electron micrograph illustrating the epithelial cell morphology in the innermost portion
of the junctional epithelium of a human tooth with a clinically healthy gingiva. ES, enamel space; N,
nuclei of epithelial cells; PMN, polymorphonuclear leukocyte.
Lysosomal bodies are found in large numbers in junctional epithelial cells. Enzymes contained within
these lysosomes participate in the eradication of bacteria (Lange and Schroeder, 1971). While
cytokeratin bundles are scarce, the Golgi fields are large (Fig. 4⇔), the cisternae of the rough
endoplasmic reticulum are abundant, and polyribosomes are numerous. All junctional epithelial cells
express a unique set of cytokeratins, including Nos. 5, 13, 14, and 19, and occasionally also weak
activity for cytokeratins Nos. 8, 16, and 18 (for review, see Schroeder, 1996).
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Figure 4.
Transmission electron micrograph showing a well-developed Golgi apparatus (G) and numerous
mitochondria (M) in the cytoplasm of a junctional epithelial cell in a human tooth with a clinically
healthy gingiva. N, nuclei.
Compared with other epithelia, junctional epithelial cells are interconnected by a few desmosomes
only (Fig. 5⇔), and occasionally by gap junctions (Schroeder, 1969, 1981; Schroeder and Münzel-
Pedrazzoli, 1970; Schroeder and Listgarten, 1977; Yamasaki et al., 1979; Saito et al., 1981; Sasaki et
al., 1981; Hashimoto et al., 1986). The fluid-filled intercellular spaces may vary in width, but are
wider in comparison with the oral gingival or sulcular epithelium (Schroeder and Münzel-Pedrazzoli,
1970). These features account for the junctional epithelium’s remarkable permeability (Figs. 3⇔,
6⇔, 8⇔). A variety of mononuclear leukocytes occupy these interstitial spaces. Neutrophilic
granulocytes (= polymorphonuclear leukocytes or simply neutrophils, PMNs) are found in the central
region of the junctional epithelium and near the tooth surface (Figs. 3⇔, 6⇔) (Schroeder and
Listgarten, 1997). In addition, lymphocytes and macrophages reside in and near the basal cell layer
(Schroeder, 1973, 1977). Antigen-presenting cells and Langerhans and other dendritic cells are
present as well (Juhl et al., 1988). The junctional epithelium, particularly its basal cell layers, is well-
innervated by sensory nerve fibers (Byers and Holland, 1977; Byers et al., 1987; Kondo et al., 1992;
Maeda et al., 1994).
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Figure 5.
Transmission electron micrograph illustrating desmosomes (DES) and cytokeratin filaments (CK) in
the junctional epithelium from a human tooth with a clinically healthy gingiva. N, nucleus of a
junctional epithelial cell.




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Figure 6.
Transmission electron micrograph showing polymorphonuclear leukocytes (PMN) residing in the
intercellular spaces of the junctional epithelium of a human tooth with a clinically healthy gingiva.
ES, enamel space; N, nuclei of junctional epithelial cells.
The Epithelial Attachment
The junctional epithelium faces both the gingival connective tissue ( i.e., the lamina propria of the
gingiva) and the tooth surface (Figs. 1⇔, 2⇔). While a basement membrane, sometimes referred to
as ‘the external basal lamina’ (Schroeder, 1996), is interposed between the basal cells of the
junctional epithelium and the gingival connective tissue, a basal lamina (also known as the internal
basal lamina) forms part of the interfacial matrix between the tooth-facing junctional epithelial cells
(also known as DAT cells; see above) and the tooth surface (Fig. 7⇔). At the apical end of the
junctional epithelium, the basal lamina is continuous with the basement membrane.




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Figure 7.
Transmission electron micrograph illustrating the basal lamina, consisting of the lamina lucida (LL)
and the lamina densa (LD), and hemidesmosomes (HD) at the interface between the junctional
epithelium and the tooth. The interposed matrix layer (*) may be a dental cuticle or a modified
cementum matrix. The micrograph originates from a healthy but receded gingival site of a human
tooth. AEFC, acellular extrinsic fiber cementum; CK, cytokeratin filaments.
Basement membranes are specialized extracellular matrices that are interposed between connective
tissues and epithelia, endothelia, muscle fibers, and the nervous system. They are thought to play
roles in compartmentalization (physical barrier function), filtration (selective permeability barrier
function or molecular sieve function), cell polarization, migration, adhesion, and differentiation. They
usually consist of a lamina lucida (also known as the lamina rara), a lamina densa, and a lamina
fibroreticularis (also known as the sub-basal lamina). The latter forms a discontinuous layer
consisting of reticular and anchoring fibrils and faces the connective tissue site from which it is
supposed to originate. Typical matrix constituents of the basement membrane are collagen types IV
and VII, laminin, heparan sulfate proteoglycan, fibronectin, nidogen (entactin), and the proteoglycan
perlecan. While the external basement membrane of the junctional epithelium resembles, in its
structure and composition, other basement membranes that are interposed between an epithelium
and a connective tissue, the internal basal lamina has distinctively different structural and molecular
characteristics. It lacks most of the common basement membrane components such as collagen
types IV and VII, most laminin isoforms, perlecan, and a lamina fibroreticularis (Salonen and Santti,
1985; Kogaya et al., 1989; Sawada et al., 1990; Salonen et al., 1991; Oyarzun-Droguett, 1992;
Hormia et al., 2001). Laminin-5, however, appears to be expressed in the internal basal lamina but
not in the external basement membrane of the junctional epithelium, at least in rats (Oksonen et al.,
2001). Thus, the internal basal lamina of the junctional epithelium has its own characteristics and
cannot be regarded as a basement membrane in the true sense.
The basal lamina together with hemidesmosomes (Listgarten, 1966, 1972a; Schroeder, 1969) forms
the interface between the tooth surface and the junctional epithelium and is named ‘epithelial
attachment’ (Schroeder and Listgarten, 1977). The hemidesmosomes consist of an attachment
plaque associated with cytokeratin filaments and the sub-basal dense plate, which is extracellularly
located in the lamina lucida (Fig. 7⇔). The lamina densa directly faces the enamel, dentin, or
cementum (fibrillar or afibrillar) (Figs. 7⇔, 8⇔). A dental cuticle may be interposed between these
tooth matrices (Fig. 9⇔). However, this attachment mechanism has also been demonstrated to exist
on a dental calculus layer in a bacteria-free environment (Listgarten and Ellegaard, 1973). The
elements of the epithelial attachment are produced and renewed by the adjacent DAT cells (Stallard
et al., 1965; Osman and Ruch, 1980) and, hence, are part of the dynamics of the junctional
epithelium.




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Figure 8.
Transmission electron micrograph showing the attachment of the junctional epithelium to the root
cementum (C) from a healthy site of the receded gingiva in a human tooth. The interposed matrix
layer (*) is a modified cementum matrix. N, nuclei of junctional epithelial cells.
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Figure 9.
Transmission electron micrograph illustrating junctional epithelial cells facing a dental cuticle-like
material (DC) in a human tooth. The gingival biopsy originated from a healthy site. ES, enamel space.
Previous SectionNext Section
(IV) DYNAMIC ASPECTS OF THE JUNCTIONAL EPITHELIUM
The cell and extracellular dynamics of the junctional epithelium are essential for its protective and
regenerative functions. The junctional epithelium in primates is known for its high cellular turnover
(Skougaard, 1965, 1970; Demetriou and Ramfjord, 1972). While cell mitosis occurs in the basal and
possibly also in some DAT cells (Salonen, 1994), exfoliation of daughter cells takes place at the free
surface of the junctional epithelium (i.e., at the bottom of the sulcus and the interdental col). Thus,
junctional epithelial cells migrate in the coronal direction toward the free surface, where they
desquamate. Since the surface area occupied by the basal cells is much greater than that of the
sulcus bottom, exfoliation must occur at an extremely high rate (Löe and Karring, 1969; Listgarten,
1972b). Also, the DAT cells are said to migrate toward the sulcus bottom. Since the DAT cells are
connected to the basal lamina via hemidesmosomes, a remodeling of the epithelial attachment must
occur. Thus, the epithelial attachment normally is not static but dynamic.
The intercellular spaces of the junctional epithelium provide a pathway for fluid and transmigrating
leukocytes. In the absence of clinical signs of inflammation, approximately 30,000 PMNs migrate per
minute through the junctional epithelia of all human teeth into the oral cavity (Schiött and Löe,
1970). The tissue fluid transports a variety of molecules through the junctional epithelium to the
bottom of the gingival sulcus. These molecules, together with the leukocytes, represent a host
defense system against the bacterial challenge. Thus, gingival fluid is an exudate that originates
from the sub-epithelial blood vessels of the lamina propria, and its flow rate corresponds to the
degree of inflammation.
Previous SectionNext Section
(V) EXPRESSION OF VARIOUS MOLECULES AND THEIR
FUNCTIONS
Numerous cell and extracellular molecules regulate maintenance of normal tissue architecture and
function. How tissue integrity is maintained is a burning question in view of the many unknown
potential factors that could contribute to the initiation of periodontal diseases. Of particular interest
are the mechanisms that maintain the epithelial attachment to the tooth surface, the epithelial-
connective tissue interface, and the spatial and interactive cell-to-cell relations within the junctional
epithelium itself. In recent years, much emphasis has been placed on the important role of the
epithelial attachment to the tooth surface. The highly dynamic nature of the junctional epithelium,
however, indicates a much more important role for the cells themselves in the maintenance of tissue
integrity (Schroeder, 1996). [The locations and functions of several important molecules associated
with the junctional epithelium are summarized in the Table⇔.]
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Table.
Locations and Functions of Molecular Factors Associated with the Junctional Epithelium
Cells have surface or cell membrane molecules that play a role in cell-matrix and cell-cell
interactions. Junctional epithelial cells express numerous cell adhesion molecules (CAMs), such as
integrins and cadherins (for review, see Juliano, 2002). Integrins are cell-surface receptors that
mediate interactions between cells and the extracellular matrix, and also contribute to cell-cell
adhesion (for reviews, see Graber et al., 1999; Danen and Sonnenberg, 2003). The expression of the
integrin subunits α6β4 (Hormia et al., 1992, 2001; Thorup et al., 1997; Gurses et al., 1999) and
α2β1, α3β1, and α6β1 (Del Castillo et al., 1996) has been documented in the junctional epithelial
cells. Of particular interest are those integrins that interact with the matrix constituents of the
internal basal lamina and the external basement membrane of the junctional epithelium, since
altered expressions of these integrins may adversely influence tissue integrity.
Knowledge about structures and molecules involved in the maintenance of cell-cell contacts is
particularly important in view of the pathological changes that the junctional epithelium undergoes
during its conversion to a pocket lining. The cadherins are responsible for tight contact between
cells (Ivanov et al., 2001; Juliano, 2002). E-cadherin, an epithelium-specific CAM, plays a crucial role
in maintaining the structural integrity. Immunohistochemical staining for E-cadherin reveals a
significant reduction in staining intensity from the oral gingival to the junctional epithelium (Ye et
al., 2000). In contrast, in another study, expression of E-cadherin was not detectable at all in the
junctional epithelium (Heymann et al., 2001). An analysis of the expression of the carcino-embryonic
Ag-related cell adhesion molecule 1 (CEACAM1)—a transmembrane cell-adhesion molecule that is
expressed on leukocytes, epithelia, and blood vessel endothelia—revealed a much stronger cell-
surface staining in the junctional epithelium as compared with the oral sulcular epithelium (Heymann
et al., 2001). Thus, the dynamic cohesion of the junctional epithelial cells may, to a large extent, be
mediated by CEACAM1 (Heymann et al., 2001). Since CEACAM1 is also expressed on the surface of
PMNs, it likewise may play a role in the guidance of these cells through the junctional epithelium
(Heymann et al., 2001). In addition, CEACAM1 participates in the regulation of cell proliferation,
stimulation, and co-regulation of activated T-cells (Odin et al., 1988; Kammerer et al., 1998; Singer
et al., 2000). Furthermore, it functions as a cell receptor for a variety of different bacteria (Öbrink,
1997; Hauck et al., 1998). As a consequence, bacterial interactions with CEACAM1 may result in
altered structural organization of the junctional epithelium (Heymann et al., 2001).
Intercellular adhesion molecule-1 (ICAM-1 or CD54) and lymphocyte function antigen-3 (LFA-3) are
additional cell adhesion molecules. Both are members of the immunoglobulin superfamily of
recognition molecules. ICAMs are immunoglobulin-like transmembrane glycoproteins that mediate
cell-cell interactions in inflammatory reactions. They function as ligands for the β2 integrin
molecules present on leukocytes and participate in the control of leukocyte migration to
inflammatory sites. Expression of ICAM-1 and lymphocyte function antigen-3 (LFA-3) has been
demonstrated in the junctional epithelial cells (Crawford and Hopp, 1990; Crawford, 1992; Gao and
Mackenzie, 1992; Tonetti, 1997; Tonetti et al., 1998). The establishment of a gradient of ICAM-1
expression within the junctional epithelium is thought to be an important mechanism for guiding
PMNs toward the bottom of the sulcus, where they could counteract the bacterial challenge (Tonetti,
1997; Tonetti et al., 1998). In this context, the high expression of interleukin-8 (IL-8), a chemotactic
cytokine, in the coronal-most cells of the junctional epithelium may be an additional mechanism of
routing PMNs toward the bacterial challenge (Tonetti et al., 1994, 1998). Other cytokines—such as
interleukin-1α (IL-1α), interleukin-1β (IL-1β), and tumor necrosis factor-α (TNF-α)—are strongly
expressed in the coronal half of the junctional epithelium (Miyauchi et al., 2001). After exposure to
lipopolysaccharide, almost all cells in the junctional epithelium are strongly labeled for these
cytokines (Miyauchi et al., 2001). Staining was attributed to both junctional epithelial cells and
macrophages. Thus, cytokine production by junctional epithelial cells and macrophages in the
coronal half of the junctional epithelium may play a role in the defense against the bacterial
challenge in the gingival sulcus. Hence, from a clinical point of view, it has to be realized that the
junctional epithelium represents a key mechanism in host-parasite interactions, since it actively
participates in the host defense mechanism rather than simply providing an attachment to the tooth
surface.
The level of cellular differentiation can be analyzed by the expression of cell-membrane-associated
blood-group-specific carbohydrates (Dabelsteen et al., 1982). N-acetyllactosamine—the type 2
chain H precursor of the blood group A-specific carbohydrate, which is usually associated with the
lowest level of cell differentiation—is expressed throughout the junctional epithelium (Steffensen et
al., 1987). This, in turn, may support the hypothesis that DAT cells may indeed retain their
proliferative potential.
The expression of growth factors and corresponding receptors has also been studied in the
junctional epithelium. Epidermal growth factor (EGF) is a potent mitogen and is thought to be
involved in epithelial growth, differentiation, and wound healing. The EGF signal is transmitted to the
cell via the EGF receptor. While EGF receptors are poorly expressed or undetectable in junctional
epithelium from the healthy human gingiva, inflamed tissues from patients with chronic periodontitis
revealed an intense labeling in proliferating cells (Nordlund et al., 1991). In the ‘normal’ junctional
epithelium of rat gingiva, immunohistochemical staining for EGF was observed in the cytoplasm
(Tajima et al., 1992).
Expressions of tissue plasminogen activator (t-PA) (Schmid et al., 1991) and its inhibitor PAI-2
(Lindberg et al., 2001a,b) have been detected in the junctional epithelium. The t-PA is a serine
protease that converts plasminogen into plasmin. Plasmin degrades many extracellular matrix
proteins and activates matrix metalloproteinases (MMPs). Matrilysin (matrix metalloproteinase-7;
MMP-7), a proteolytic enzyme found in many mature epithelial cells, is expressed in suprabasal cells
of the human junctional epithelium (Uitto et al., 2002).
The active role the junctional epithelium plays in the innate host defense is also demonstrated by the
production of natural antimicrobial peptides and proteins in response to the bacterial challenge (for
review, see Dale, 2002). Antimicrobial molecules that may contribute to periodontal health include
the α- and β-defensins, the cathelicidin family members (LL-37), and calprotectin. While human β-
defensin 1 (hBD-1) and human β-defensin 2 (hBD-2) are poorly expressed or undetectable in the
junctional epithelium, the α-defensins and LL-37 are present in high amounts. Their expressions are
attributable to the presence of the PMNs that produce these 2 natural antimicrobials. Thus, the PMNs
contribute to the protection of the junctional epithelium by releasing α-defensins and LL-37.
Previous SectionNext Section
(VI) JUNCTIONAL EPITHELIUM ADJACENT TO ORAL
IMPLANTS
The junctional epithelium around implants always originates from epithelial cells of the oral mucosa,
as opposed to the junctional epithelium around teeth which originates from the reduced enamel
epithelium. Hence, it may be questioned whether or not the structural and functional characteristics
of these 2 junctional epithelia are identical. Structurally, the peri-implant epithelium closely
resembles the junctional epithelium around teeth (Berglundh et al., 1991; Listgarten et al., 1991;
Buser et al., 1992; Listgarten, 1996; Koka, 1998; Cochran, 2000), although dissimilarities have also
been reported (Inoue et al., 1997; Ikeda et al., 2000, 2002; Fujiseki et al., 2003; Shimono et al.,
2003). There is also evidence that several of the mentioned marker molecules involved in the
defense mechanisms against the bacterial challenge are also expressed in the peri-implant
epithelium. In that respect, the presence of t-PA (Schmid et al., 1992), ICAM-1, and a cytokeratin
profile resembling that of gingival junctional epithelium (Mackenzie and Tonetti, 1995) has been
documented. This, in turn, implies that, despite different origins of the 2 epithelia, a functional
adaptation occurs when oral epithelia form an epithelial attachment around implants. Such an
adaptive potential is also observed in the regenerating junctional epithelium around teeth following
gingivectomy.
Previous SectionNext Section
(VII) REGENERATION OF THE JUNCTIONAL EPITHELIUM
Injury of the junctional epithelium may occur through accidental or intentional trauma,
toothbrushing, flossing, or clinical probing. Since the junctional epithelium is located at a
strategically important but also delicate site, it may be expected that it should be very well-adapted
to cope with mechanical insults.
Clinical probing results in a mechanical disruption of the junctional epithelial cells from the tooth.
Whether and how fast a new epithelial attachment reforms have been the objectives of several
studies. In an experimental study in marmosets, following probing, a new and complete attachment
indistinguishable from that in controls was established 5 days after complete separation of the
junctional epithelium from the tooth surface (Taylor and Campbell, 1972). The re-establishment of
the epithelial seal around implants after clinical probing was shown to occur within about the same
time period (Etter et al., 2002). In both studies, persistence of tissue trauma and infection as a result
of probing were not observed. Based on these 2 studies, probing around teeth and implants does
not seem to cause irreversible damage to the soft tissue components.
Oral hygiene practices may be accompanied by undesired trauma to the junctional epithelium as
well. Waerhaug (1981) studied healing of the junctional epithelium following the use of dental floss
at premolars in 12-year-old humans. Detachment of cells persisted for 24 hrs after flossing ceased.
New attachment of junctional epithelial cells started 3 days after flossing ceased. After 2 wks, the
cell populations on the experimental and control surfaces were again indistinguishable from each
other.
In the above studies, the junctional epithelium was never completely removed from the tooth.
However, the application of gingivectomy techniques would completely remove the junctional
epithelium. Subsequently, the formation of a new junctional epithelium must occur from basal cells
of the oral gingival epithelium (Listgarten, 1967; Innes, 1970; Frank et al., 1972; Listgarten and
Ellegaard, 1973; Braga and Squier, 1980). In humans, a new junctional epithelium after gingivectomy
may form within 20 days (Listgarten, 1972a,b; Schroeder and Listgarten, 1977).
These studies show that the junctional epithelium is a highly dynamic and adaptive tissue with a fast
capacity for self-renewal or de novo formation from basal cells of the oral gingival epithelium.
Previous SectionNext Section
(VIII) ROLE OF THE JUNCTIONAL EPITHELIUM IN THE
INITIATION OF POCKET FORMATION
A clinically healthy gingiva exhibits microscopic signs of slight inflammation, including the presence
of an inflammatory infiltrate of very limited extent (Brecx et al., 1987). In that respect, the
importance of the leukocytes, particularly PMNs, migrating through the junctional epithelium has
been recognized as a significant factor contributing to the first line of peripheral host defense (for
review, see Schroeder and Listgarten, 1997). Thus, such inflammatory cells in the sub-epithelial
portion of the lamina propria and in the junctional epithelium itself should be regarded as a part of
normal homeostasis and an essential element of the defense system against continuous bacterial
challenge (for review, see Schroeder and Listgarten, 1997). Also, an acute gingivitis should not be
interpreted as a first step in the development of periodontitis. Usually, the peripheral host defense
system is efficient enough to avoid exacerbation of the developing lesion and progression toward
connective tissue breakdown seen in periodontitis. Since the conversion of the junctional epithelium
to pocket epithelium is regarded as a hallmark in the development of periodontitis, the potential
factors contributing to the initiation of pocket formation deserve particular attention. Schroeder
(1996) pointed to a biologically relevant and clinically important question that still awaits resolution:
‘What happens to the junctional epithelium under conditions of sub-gingival microbial attack, i.e., in
context with pocket formation and deepening?’
Several researchers have attributed pocket formation to a loss of cellular continuity in the coronal-
most portion of the junctional epithelium (Schluger et al., 1977; Schroeder and Listgarten, 1977).
Thus, the initiation of pocket formation may be attributed to the detachment of the DAT cells from
the tooth surface or to the development of an intra-epithelial split. Takata and Donath (1988),
studying pocket formation in humans, observed degenerative changes in the second or third cell
layer of the DAT cells in the coronal-most portion of the junctional epithelium facing the bacterial
biofilm. Similar observations were made in a dog model (Hillmann et al., 1990). Several attempts to
explain the reason for the cleavage within the junctional epithelium have been made. With increasing
degrees of gingival inflammation, both the emigration of PMNs and the rate of gingival crevicular
fluid passing through the intercellular spaces of the junctional epithelium increase (Klinkhamer,
1968; Klinkhamer and Zimmerman, 1969; Attström and Egelberg, 1970; Attström, 1970; Kowashi et
al., 1980). Moderately distended intercellular spaces are not considered to interfere with the
structural and functional integrity of the junctional epithelium (Schroeder and Listgarten, 1997).
However, an increased number of mononuclear leukocytes, i.e., T- and B-lymphocytes and
monocytes/macrophages, together with PMNs, are considered as factors that contribute to the focal
disintegration of the junctional epithelium (Schroeder and Listgarten, 1997). Apart from the view that
the host itself is the major source of factors contributing to the disintegration of the junctional
epithelium, other possibilities have to be considered as well.
The junctional epithelium is an ‘open system’ that allows cells and substances to emigrate from the
gingival connective tissue into the sulcus, thereby clearing and counteracting the continuous
bacterial challenge. In contrast, the bacteria and their products also have the opportunity to enter
the junctional epithelium. It has already been hypothesized that pocket formation is the result of
subgingival spreading of bacteria under impaired defense conditions (Schroeder and Attström,
1980). Particular attention has been paid to elucidating the mechanisms by which Actinobacillus
actinomycetemcomitans and Porphyromonas gingivalis (P. gingivalis), 2 pathogens implicated as
major etiological agents in aggressive and chronic periodontitis, adhere to, invade, and replicate in
epithelial cells (Lamont et al., 1992, 1995; Sandros et al., 1994; Madianos et al., 1996; Meyer et al.,
1997; Njoroge et al., 1997; Deshpande et al., 1998; Huard-Delcourt et al., 1998; Lamont and
Jenkinson, 1998; Fives-Taylor et al., 1999; Forng et al., 2000; Quirynen et al., 2001). Among the
virulence factors produced by P. gingivalis, the cysteine proteinases, referred to as gingipains, have
been the focus of research over the last few years (Potempa et al., 2000; Curtis et al., 2001;
Imamura, 2003). Recently, a new effect of gingipains has emerged. It has been shown that gingipains
specifically degrade components of the epithelial cell-to-cell junctional complexes (Wang et al.,
1999; Katz et al., 2000, 2002; Chen et al., 2001; Hintermann et al., 2002). Epithelial cells challenged
by P. gingivalis exhibit proteolysis of focal contact components, adherens junction proteins, and
adhesion signaling molecules (Hintermann et al., 2002). Furthermore, epithelial cells exposed to P.
gingivalis, or to proteinases derived from it, showed reduced adhesion to extracellular matrices,
changes in morphology, impaired motility, and apoptosis. The recent observation that gingipains
may also disturb the ICAM-1-dependent adhesion of PMNs to oral epithelial cells, an immune
evasion mechanism by P. gingivalis, points to the importance of these molecules for the
disintegration of the junctional epithelium (Tada et al., 2003). Thus, bacterial products penetrating
the junctional epithelium at the bottom of the sulcus may directly perturb the structural and
functional integrity of the junctional epithelium. The proteolytic disruption of the epithelial integrity
may not only be a significant factor in the initiation of pocket formation, but may also pave the way
for bacterial invasion into the sub-epithelial connective tissue in advanced stages of the lesion. The
same mechanisms of destruction of cell-to-cell contacts may further perturb the structural and
functional integrity of the connective tissue. In this regard, degradation of cell adhesion molecules
on fibroblasts and cell death were shown to be induced by the arginine-specific cysteine proteinase
(Arg-gingipain) in vitro (Baba et al., 2001). Whether periodontopathogens use the same strategy in
vivo is an important question that remains to be solved.
Previous SectionNext Section
(IX) CONCLUDING REMARKS
The junctional epithelium is a unique tissue that fulfills a challenging function at the border between
the oral cavity, colonized by bacteria, and the tooth attachment apparatus. It is structurally and
functionally very well-adapted to control the constant presence of bacteria and their products.
However, its antimicrobial defense mechanisms do not preclude the development of inflammatory
lesions in the gingiva. These defense mechanisms may be overwhelmed by bacterial virulence
factors, and the gingival lesion could progress to periodontitis. The conversion of the junctional
epithelium to pocket epithelium is regarded as a hallmark in the development of periodontitis.
Bacteria, such as, e.g., P. gingivalis, may directly perturb the structural and functional integrity of the
junctional epithelium. Recent studies have shed light on the role of gingipains in this process. Such
new information may be used to develop therapeutic strategies aimed at neutralizing the detrimental
effects of these cysteine proteinases.
Previous SectionNext Section
Acknowledgments
The authors are indebted to Mrs. M. Aeberhard for excellent technical assistance. Fig. 1⇔ is
courtesy of Dr. H.E. Schroeder, and Fig. 2⇔ is courtesy of Dr. A. Nanci. This work was supported by
the Clinical Research Foundation (CRF) for the Promotion of Oral Health, University of Berne,
Switzerland.
Previous SectionNext Section
Article Notes

     Received May 12, 2004.
     Accepted October 10, 2004.


     International and American Associations for Dental Research


Previous Section


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1.        Top
2.        Abstract
3.
4.        (I) INTRODUCTION
5.        (II) THE DEVELOPMENT OF THE JUNCTIONAL EPITHELIUM
6.        (III) STRUCTURE OF THE JUNCTIONAL EPITHELIUM
7.        (IV) DYNAMIC ASPECTS OF THE JUNCTIONAL EPITHELIUM
8.        (V) EXPRESSION OF VARIOUS MOLECULES AND THEIR FUNCTIONS
9.        (VI) JUNCTIONAL EPITHELIUM ADJACENT TO ORAL IMPLANTS
10. (VII) REGENERATION OF THE JUNCTIONAL EPITHELIUM
11. (VIII) ROLE OF THE JUNCTIONAL EPITHELIUM IN THE INITIATION OF POCKET FORMATION
12. (IX) CONCLUDING REMARKS
13. Acknowledgments
14. Article Notes
15. REFERENCES


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