Cytokeratins 14 and 19 in odontogenic cysts and tumors: a review
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Cytokeratins 14 and 19 in odontogenic cysts and
tumors: a review
Nieves Sabrina*, Apellaniz Delmira*, Tapia Gabriel**, Maglia Alvaro***, Mosqueda-Taylor Adalberto****,
Bologna-Molina Ronell*****.
Abstract
All mammal cells include a cytoplasmic fiber system essential for cell mobility, the
cytoskeleton, formed by three main structural units and associated proteins: microfilaments,
microtubules and intermediate filaments. Cytokeratins are intermediate filaments forming
a complex network which extends from the nucleus surface to the peripheral cell sector,
where they are inserted into desmosomes and hemidesmosomes. Cytokeratins 14 and 19
have been used as diagnosis and prognosis markers in various tumors of epithelial origin,
not only to identify a cell as epithelial, but also to identify different stages during epithelial
differentiation and to characterize the tumor. There are numerous studies in biomedical
literature that have exemplified the utility of cytokeratins 14 and 19 to identify odontogenic
epithelium. This review analyzes the utility of their immunologic expression in the different
cysts and odontogenic tumors.
Keywords: Cytokeratin 14, Cytokeratin 19, Odontogenic cysts, Odontogenic tumors.
* Molecular Pathology Trainee, Facultad de Odontología, UdelaR, Uruguay
** Assistant Professor, Grade 3, Department of Histology, Facultad de Odontología, UdelaR, Uruguay
*** Associate Professor, Grade 5, Department of Histology, Facultad de Odontología, UdelaR, Uruguay
**** Specialist in Pathology and Oral Medicine, Full-time Research Professor, Health Care Department, Universidad Autónoma Metro-
politana, Mexico
***** Specialist in Pathology and Oral Medicine, Doctor in Biological Sciences (Molecular Pathology), Full-time Associate Professor, Grade
5, Molecular Pathology, Facultad de Odontología, UdelaR, Uruguay
Received on: 08.05.14 - Accepted on: 01.09.14
Odontoestomatología / Vol. XVI. Nº 24 / November 2014
45What are cytokeratins? epithelial keratins with variable molecular
weights within the 40-70 kDa range, and sub-
All mammal cells include a cytoplasmic fiber sequently an additional keratin was identified:
system essential for cell mobility: the cytoskel- CK20. They can be divided into low versus
eton. If we try to explain it in a simple and high molecular weight, and into acid or basic
colloquial way, we could compare it to the according to their isoelectric points (2).
steel rods that support the structure of a build- CKs 14 and 19 are type I keratins: CK 19 is
ing: the cytoskeleton plays a key role as it sup- the smallest one and it is exceptional because,
ports the plasma membrane and presents paths unlike other cytokeratins, it lacks the typical
along which organelles and other cytosol ele- domain (no alpha helix) (5). CK14 is found in
ments can move. However, unlike the passive the keratinocytes of stratified squamous epi-
frame of a building, the cytoskeleton is con- thelium, both in the epidermis and the nonke-
stantly restructured, which allows for move- ratinized mucosa (4), while CK19 is expressed
ment (1). The cytoskeleton is formed by three in most simple epithelia, in various ductal
main structural units and associated proteins: epithelia, in intestinal epithelia, in the gastric
microfilaments, microtubules and intermedi- foveolar epithelium, and in the mesothelium.
ate filaments. Intermediate filaments are divid- Besides, it is present in most pseudostratified
ed into six types according to their molecular epithelia and urothelial cells, as well as in basal
characteristics. Cytokeratins (CK) are type I cells of nonkeratinized stratified squamous
and type II intermediate filaments (2, 3). epithelium (4).
Moll et al. (4) classified a total of 19 human
Fig. 1. Epithelial cells. Disposition of cytokeratins from the cytoplasmic plaque toward the nuclear periphery.
46 Nieves Sabrina, Apellaniz Delmira, Tapia Gabriel, Maglia Alvaro, Mosqueda-Taylor Adalberto, Bologna-Molina RonellWhich are their functions? Utility of cytokeratins as markers
Cytokeratins form a complex network which Not all keratins are synthesized simultane-
extends from the nucleus surface to the pe- ously by a cell, but rather different subsets of
ripheral cell sector, where they are inserted keratins are expressed during terminal differ-
into desmosomes and hemidesmosomes. entiation in different stages of development,
(Figure 1). As they connect the nucleus sur- as well as in different epithelia. Therefore, all
face with the plasma membrane, they provide epithelia (simple and complex) can be clas-
a permanent link that can have important sified according to cytokeratin expression.
implications for cytoplasm organization, cell Simple or monostratified epithelia generally
communication, and perhaps for the trans- express keratins 7, 18, 19 and 20, while com-
portation of information inside and outside plex (stratified) epithelia express keratins 5,
the nucleus (2, 4). Additionally, as they are 6, 10, 14 and 15. When an epithelium un-
inserted into desmosomes and hemidesmo- dergoes malignant transformation, its keratin
somes, they contribute not only to the stabil- profile usually remains constant (2). There-
ity of epithelial cells, but to their union with fore, patterns of keratin expression allow us
the basal membrane and the underlying con- not only to identify a cell as epithelial, but
nective tissue (4, 6). also to determine the phases of epithelial dif-
In recent years there has been agreement re-
ferentiation and to characterize the tumor.
garding the fact that keratins have two funda-
This is why antibodies against several keratins
mental roles in epithelial cells:
are used routinely at immunohistochemistry
a) structural support, without which physical
labs to diagnose carcinoma, especially unclear
trauma leads to loss of integrity, and
metastases (4).
b) regulation of metabolic processes and their
growth, proliferation, migration and apopto- Another clinical application is the detection of
sis. protein fragments of CK8, CK18 and CK19
These two general roles involve regulated in- in the bloodstream of cancer patients. These
teractions with a diverse group of fragments are increasingly used to monitor
proteins (2, 7), which include signaling mol- tumor burden and the progression of the dis-
ecules such as 14-3-3 proteins, apoptosis-re- ease in certain carcinomas such as lung cancer
lated proteins, kinases and phosphatases (8). (15, 16). Besides, it has been observed that
Oriolo et al. (9) say that they can also have a over 95% of lung carcinoma squamous cells
role in epithelial polarity and membrane traf- are positive for CK14 (13, 17).
fic. CK19 is one of the most frequently studied
Cytokeratins have also been linked to wound immunohistochemical markers in thyroid pa-
healing, as they provide a more pliable cyto- thology, which could make it a useful diagno-
skeleton to the cell, which favors the migra- sis and prognosis tool, as it can be determined
tion of keratinocytes for wound closure (10). before the therapeutic procedure in cytologic
As for CK14, mutations in the CK genes are findings (14).
responsible for epidermolysis bullosa simplex Immunohistochemical staining for CK19
(11, 12), a hereditary disease, considered im- facilitates the differential diagnosis between
portant for the physical stability of the epi- papillary carcinoma, which presents strong
dermis (4). In turn, CKs 15 and 20 have been and diffuse staining, and other thyroid can-
used as diagnosis and prognosis markers in cers, which present weak and focal staining.
various tumors of epithelial origin (13, 14). It has also been suggested that it could be a
Cytokeratins 14 and 19 in odontogenic cysts and tumors: a review
47useful predictor of the progression of thyroid nign or malignant myoepithelioma, adenoid
carcinoma (14). cystic carcinoma and pleomorphic adenoma
Tsuruba et al. (18) showed that CK8 and (13, 26, 27).
CK14 can be useful to diagnose tumors in
skin appendices. In general, the following tu- Cytokeratins and odontogenesis
mors test negative for CK8 and positive for
CK14: epidermis, sebaceous glands and hair Patterns of expression of cytokeratins in the
follicles, while tumors derived from eccrine odontogenic epithelium have been described
glands and apocrine sweat glands are CK8 in a very general way. Domingues et al. (28),
positive and CK14 negative. in their immunohistochemical study, showed
Squamous cells carcinoma, as well as malig- that epithelial cells of the tooth germ and in
nant mesothelioma, show a strong expression the remnants of the dental lamina are posi-
of CK14, while adenocarcinomas show none tive for CK14 and CK19 with slight changes
or very little (2, 4, 19). Studies have suggested in their expression pattern, depending on the
that the expression of certain keratins of sim- phase of odontogenesis. For example, they
ple epithelia (like CK19) in squamous cells state that at the inner epithelium of the enam-
carcinomas may indicate a poorly differenti- el organ the expression of CK14 and CK19
ated carcinoma (4). CK19 is detected in the varies in the follicle and bell stages (early bell
epithelium near squamous cells carcinomas, stage according to the author). They observed
which suggests that it could be used as a fun- a strong positive for CK14 while CK 19 had
damental biological agent of the malignant weak staining, which was the opposite at the
progression (20). Clearly these findings can late bell or follicle stage. CK19 has a strong
be applied in the case of oral cavity squamous positive, while the expression of CK14 de-
cells, which shows the utility of these cytoker- creases. Additionally, the most prevalent cy-
atins in the diagnosis and as a possible prog- tokeratin in the remnants of the dental lami-
nosis factor in diverse neoplasms that affect na was CK14, which strongly stained all cells,
the maxillofacial region (21), as well as lesions while CK19 appeared only in some cells of
of the oral mucosa considered potentially ma- the dental lamina, with a non-homogeneous
lignant (22, 23). pattern. CK14 was also observed in the stel-
late reticulum, which was stronger at the early
As for salivary glands tumors, they can be bell phase. CK19 was also expressed but more
divided into two large categories: tumors weakly. The outer epithelium of the enamel
derived from stratified epithelium (pleomor- organ was marked for CK14 and for CK19.
phic adenoma, myoepithelioma, basaloid Crivelini et al. (20), Ferreira Lopes et al. (29),
squamous cells carcinoma, adenoid cystic Leon et al. (30), Kasper et al. (31), Heikin-
carcinoma and mucoepidermoid carcinoma), heimo et al. (32), and Gao et al. (33) also
and tumors that arise from simple epithelia studied the expression of CK14 and CK19 in
(adenocarcinoma NOS, monomorphic ad- tooth germ, although in less detail.
enocarcinoma and acinar cell carcinoma). They found CK14 and CK19 in the enamel
The former express CK14 and CK19, while organ (20, 29–33) and in the dental lamina
the latter do not (24, 25). CK14 is a myoepi- (20, 30, 31).
thelial cells marker, therefore, salivary glands Crivelini et al. and Leon et al. agree with the
tumors with myoepithelial cells are usually findings of Domingues et al. As for CK14, it
positive for CK14. These tumors include be- is gradually replaced by CK19 in the inner
48 Nieves Sabrina, Apellaniz Delmira, Tapia Gabriel, Maglia Alvaro, Mosqueda-Taylor Adalberto, Bologna-Molina Ronellepithelium of the enamel organ: immunoex- toma and in peripheral ameloblastoma. They
pression of CK19 is very positive in pream- conclude that CK19 expression can be used as a
eloblasts (32). tool to differentiate both neoplasms since in the
Given the changes in the expression of CK14 cases of central ameloblastomas studied, CK19
and CK19 in the inner epithelium of the is positive in all the cells, while in peripheral am-
enamel, some researchers have suggested that eloblastoma, there are CK19 negative cells. Gao
CK19 could be considered an effective mark- et al. (33) studied the expression of CK14 and
er of ameloblast differentiation (20, 28). CK19 in the odontogenic epithelium of normal
dental follicles, as well as in the epithelium of
Odontogenic cysts and tumors dentigerous cysts and keratocystic odontogenic
tumors, as they all derive from the odontogenic
The presence of these cytokeratins in tooth de- epithelium of the dental organ. These patterns
velopment suggests that they participate in the were compared with cysts of different origins,
embryonic development of the dental organ, like nasopalatine cysts and epidermoid cysts.
which is why various authors have studied their The results obtained confirmed the prediction
expression in odontogenic cysts and tumors (20, that development cysts from the odontogenic
29, 30, 32–47). Patterns of expression of kera- epithelium shared the expression of CK14 and
tins allow us to identify a cell as epithelial and CK19, but they were different from the cysts
also to identify different stages during epithelial originated in non-odontogenic epithelium.
differentiation (4). Antibodies against these cy- Therefore, odontogenic epithelium and its de-
tokeratins have been used to elucidate histogen- rivates (cysts and tumors) show certain similari-
esis and to characterize the tumor. Numerous ties in their patterns of expression of CK, but
biomedical studies have illustrated the utility of they differ from nasopalatine cysts for example,
these two cytokeratins to identify odontogenic which derive from epithelial remnants of the
epithelium, and therefore they have been use- nasopalatine duct, and from epidermoid cysts,
ful in the diagnosis of some neoplasms or cysts which arise from the epithelium during embry-
where an odontogenic origin is suspected. They onic development.
have also been useful to determine the possible In Table 1 we summarize the studies which
histogenesis of several cystic or tumoral lesions have focused on the expression of CK14 and/or
of the maxillofacial region that are known to be CK19 in various odontogenic cysts and tumors.
of odontogenic origin (20, 29, 30, 32–34, 37,
40–45, 47). An example of this are the studies
conducted in ameloblastomas (20, 29, 34–36),
where the expression of CK14 and CK19 was
studied to elucidate its possible origin (20, 29).
Other authors have studied these same cytokera-
tins to differentiate them from other lesions, for
example Yoon et al., who studied the expression
of CK14 and CK19 to differentiate it from am-
eloblastic carcinoma. They found that in both
tumors the expression of both cytokeratins is
strong and diffuse. Another interesting study is
that of Pal et al. (35), who studied the expression
of these same cytokeratins in central ameloblas-
Cytokeratins 14 and 19 in odontogenic cysts and tumors: a review
49Table 1.- Expression of CK14/CK19 in odontogenic cysts and tumors. 1989–2013 literature
review.
ODONTOGENIC TUMORS AND
AUTHOR YEAR CK14 expression CK19 expression Origin
CYSTS
Crivelini et al. Remnants of
2003 CK14 positive CK 19 positive
(20) dental lamina
Ferreira Lopes CK14 positive in the CK 19 positive, Remnants of
2005 cells of the periphery of in central and
et al. (29) dental lamina
tumoral nests peripheral cells
CK14 positive in the CK 19 positive,
Ferreira Lopes Remnants of
2005 cells of the periphery of in central and
et al. (29) dental lamina
tumoral nests peripheral cells
Remnants of
Yoon et al.
2011 Strong positive for CK14 Positive for CK19 dental lamina
(34)
(enamel organ)
Follicular: Positive for
CK14 in all basal cells
and in most internal
cells Follicular: Positive
Plexiform: Positive for for CK19 in all cells
CK14 in all basal cells Plexiform: Positive
and in most internal for CK19 in all cells
cells Microcystic: Positive
Microcystic: Positive for for CK19 in all cells
Solid ameloblastoma Pal et al. (35) 2013 -----------------
CK14 in all basal cells Acanthomatous:
and in most internal Positive for CK19 in
cells all cells
Acanthomatous: Positive Granular: Weak
for CK14 in all basal cells positive for CK19
and weak positive in
internal cells
Granular: Negative for
CK14
Follicular: Positive
for CK19 in all cells
Plexiform: Positive
for CK19 in all cells
Acanthomatous:
Positive for CK19 in
Fukumashi et
2002 --------------------- all cells -----------------
al. (36)
Granular: Positive
for CK19 in
basal cells and
weak positive in
suprabasal and
internal cells.
Kishino et al. 2007 Positive for CK14 Positive for CK19 Remnants of
(37) odontogenic
epithelium
Peripheral ameloblastoma Pal et al. (35) 2013 ---------------------- Positive for CK19, -----------------
although some
negative cells were
found at internal
and basal levels.
50 Nieves Sabrina, Apellaniz Delmira, Tapia Gabriel, Maglia Alvaro, Mosqueda-Taylor Adalberto, Bologna-Molina RonellPal et al. (35) 2013 ------------------------ Positive for CK19, ------------------
although some
negative cells were
found at internal
and basal levels.
Desmoplastic ameloblastoma Fukumashi et 2002 --------------------- Positive for CK 19 -----------------
al. (36) in all internal and
suprabasal cells
Bologna- 2010 Positive for CK14 in Negative for CK19 -------------------
Molina et al. some suprabasal cells
(38) and in central cells
Calcifying epithelial odontogenic
tumor Crivelini et al. 2003 Positive for CK14 in all Weak positive for Remnants of
(20) cells CK19 Hertwig's sheath
Crivelini et al. 2003 Positive for CK14 in all Negative for CK19. Reduced enamel
(20) tumoral epithelial cells epithelium
Leon et al. 2005 Positive for CK14 in all Positive for CK19 Reduced enamel
(30) cells Some negative less intense than epithelium
cases for clear cells positive for CK14
Adenomatoid odontogenic
(cells in the center of Negative in fusiform
tumor
nodes) cells (peripheral to
the nodes)
Ferreira Lopes 2005 Positive for CK14 Positive for CK 19 in Reduced enamel
et al. (29) positive in duct and duct cells epithelium
plexiform cells
Martínez- 2008 Positive for CK14 Partially positive for ------------------
Odontogenic myxoma Mata et al. CK19
(39)
Crivelini et al. 2003 Positive for CK14 in all Negative for CK19 Remnants of
Ameloblastic fibroma
(20) the epithelium dental lamina
Bologna- 2013 ------------------------ Strong positive for Odontogenic
Ameloblastic fibrodentinoma Molina et al. CK19 epithelium
(40)
Gao et al. (33) 1989 Positive for CK14. Positive for CK 19 Remnants of
(irregular staining in dental lamina
suprabasal cells and
in some basal cells)
Dos Santos et 2009 Positive for CK14 in all Strong positive for Remnants of
Keratocystic odontogenic tumor al. (41) epithelial layers CK19 (in suprabasal dental lamina
and intermediate
cells)
Aragaki et al. 2010 -------------------- Strong positive for From remnants
(42) CK19 (in basal and of the dental
suprabasal cells) lamina
Gao et al. (33) 1989 Positive for CK14 Strong positive for Reduced enamel
CK19 epithelium
Tsuji et al. 2013 ------------------- Positive for CK 19 Odontogenic
(43) (in the basal layer of epithelium
Dentigerous cysts
squamous epithelial
cells)
Stoll et al. (44) 2005 ------------------- Positive for CK19 Odontogenic
epithelium
Cytokeratins 14 and 19 in odontogenic cysts and tumors: a review
51Lukinmaa et 1997 Strong positive for CK14 Strong positive for Odontogenic
al. (45) CK19 (cells of the epithelium
basal layer of the
epithelium)
Calcifying epithelial odontogenic Murakami et 2003 --------------------- Positive for CK19 (in ------------------
cyst al. (46) basal cells of oral
mucosa).
Fregnani et 2003 Positive for CK14 (in Positive for CK19 (in Odontogenic
al. (47) basal cells of lining suprabasal cells of epithelium
epithelium) epithelium)
In conclusion, various studies and recent re-
search increasingly ascribe cytokeratins a role
which goes well beyond the mere construction
of the cytoskeleton. Several groups are current-
ly studying the influence of their structural and
regulatory functions in various diseases, and
the molecular interactions of these proteins in
various normal and pathological processes are
becoming increasingly clear. These new find-
ings highlight the importance of this family of
intermediate filaments as useful biomarkers for
the prognosis and diagnosis of various human
tumors, including those in the oral maxillofa-
cial region.
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