Journal of Pathology and Translational Medicine

Original Article

Tongue Growth during Prenatal Development in Korean Fetuses and Embryos: Soo Jeong Hong, Bong Geun Cha, Yeon Sook Kim, Suk Keun Lee, Je Geun Chi; J Pathol Transl Med. 2015;49(6):497-510. Published online October 16, 2015; DOI: https://doi.org/10.4132/jptm.2015.09.17

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Background
Prenatal tongue development may affect oral-craniofacial structures, but this muscular organ has rarely been investigated. Methods: In order to document the physiology of prenatal tongue growth, we histologically examined the facial and cranial base structures of 56 embryos and 106 fetuses. Results: In Streeter’s stages 13–14 (fertilization age [FA], 28 to 32 days), the tongue protruded into the stomodeal cavity from the retrohyoid space to the cartilaginous mesenchyme of the primitive cranial base, and in Streeter’s stage 15 (FA, 33 to 36 days), the tongue rapidly swelled and compressed the cranial base to initiate spheno-occipital synchondrosis and continued to swell laterally to occupy most of the stomodeal cavity in Streeter’s stage 16–17 (FA, 37 to 43 days). In Streeter’s stage 18–20 (FA, 44 to 51 days), the tongue was vertically positioned and filled the posterior nasopharyngeal space. As the growth of the mandible and maxilla advanced, the tongue was pulled down and protruded anteriorly to form the linguomandibular complex. Angulation between the anterior cranial base (ACB) and the posterior cranial base (PCB) was formed by the emerging tongue at FA 4 weeks and became constant at approximately 124°–126° from FA 6 weeks until birth, which was consistent with angulations measured on adult cephalograms. Conclusions: The early clockwise growth of the ACB to the maxillary plane became harmonious with the counter-clockwise growth of the PCB to the tongue axis during the early prenatal period. These observations suggest that human embryonic tongue growth affects ACB and PCB angulation, stimulates maxillary growth, and induces mandibular movement to achieve the essential functions of oral and maxillofacial structures.

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Review

Current Concepts and Occurrence of Epithelial Odontogenic Tumors: II. Calcifying Epithelial Odontogenic Tumor Versus Ghost Cell Odontogenic Tumors Derived from Calcifying Odontogenic Cyst: Suk Keun Lee, Yeon Sook Kim; Korean J Pathol. 2014;48(3):175-187. Published online June 26, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.3.175

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Abstract PDF

Calcifying epithelial odontogenic tumors (CEOTs) and ghost cell odontogenic tumors (GCOTs) are characteristic odontogenic origin epithelial tumors which produce calcifying materials from transformed epithelial tumor cells. CEOT is a benign odontogenic tumor composed of polygonal epithelial tumor cells that show retrogressive calcific changes, amyloid-like deposition, and clear cytoplasm. Differentially, GCOTs are a group of transient tumors characterized by ghost cell presence, which comprise calcifying cystic odontogenic tumor (CCOT), dentinogenic ghost cell tumor (DGCT), and ghost cell odontogenic carcinoma (GCOC), all derived from calcifying odontogenic cysts (COCs). There is considerable confusion about COCs and GCOTs terminology, but these lesions can be classified as COCs or GCOTs, based on their cystic or tumorous natures, respectively. GCOTs include ameloblastomatous tumors derived from dominant odontogenic cysts classified as CCOTs, ghost cell-rich tumors producing dentinoid materials as DGCTs, and the GCOT malignant counterpart, GCOCs. Many authors have reported CEOTs and GCOTs variably express keratins, β-catenin, BCL-2, BSP, RANKL, OPG, Notch1, Jagged1, TGF-β, SMADs, and other proteins. However, these heterogeneous lesions should be differentially diagnosed to allow for accurate tumor progression and prognosis prediction.

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Case Study

Different Protein Expressions between Peripheral Ameloblastoma and Oral Basal Cell Carcinoma Occurred at the Same Mandibular Molar Area: Yeon Sook Kim, Suk Keun Lee; Korean J Pathol. 2014;48(2):151-158. Published online April 28, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.2.151

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Abstract PDF

Peripheral ameloblastoma (PA) in gingiva is rare and often confused with oral basal cell carcinoma (OBCC). The tissues of one case of PA and one case of OBCC with the same mandibular molar area affected were compared via an immunohistochemical examination using 50 antisera. The PA and OBCC showed similar proliferation of basaloid epithelial strands, but toluidine blue staining revealed that the PA had pinkish juxta-epithelial myxoid tissue, whereas the OBCC was infiltrated by many mast cells. Immunohistochemical comparisons showed that the PA was strongly positive for ameloblastin, KL1, p63, carcinoembryonic antigen, focal adhesion kinase, and cathepsin K, and slightly positive for amelogenin, Krox-25, E-cadherin, and PTCH1, whereas the OBCC was not. On the other hand, the OBCC was strongly positive for EpCam, matrix metalloprotease (MMP)-1, α1-antitrypsin, cytokeratin-7, p53, survivin, pAKT1, transforming growth factor-β1, NRAS, TGase-1, and tumor nescrosis factor-α, and consistently positive for β-catenin, MMP-2, cathepsin G, TGase-2, SOS-1, sonic hedgehog, and the β-defensins-1, -2, -3, while the PA was not. These data suggest that the tumorigeneses of PA and OBCC differ, and that PAs undergo odontogenic differentiation and generate oncogenic signals for infiltrative growth and bone resorption, whereas OBCCs undergo basaloid epidermal differentiation as a result of growth factor/cytokine-related oncogenic signals.

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Review

Current Concepts and Occurrence of Epithelial Odontogenic Tumors: I. Ameloblastoma and Adenomatoid Odontogenic Tumor: Suk Keun Lee, Yeon Sook Kim; Korean J Pathol. 2013;47(3):191-202. Published online June 25, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.3.191

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443 Download
33 Crossref

Abstract PDF

Ameloblastomas and adenomatoid odontogenic tumors (AOTs) are common epithelial tumors of odontogenic origin. Ameloblastomas are clinico-pathologically classified into solid/multicystic, unicystic, desmoplastic, and peripheral types, and also divided into follicular, plexiform, acanthomatous, granular types, etc., based on their histological features. Craniopharyngiomas, derived from the remnants of Rathke's pouch or a misplaced enamel organ, are also comparable to the odontogenic tumors. The malignant transformation of ameloblastomas results in the formation of ameloblastic carcinomas and malignant ameloblastomas depending on cytological dysplasia and metastasis, respectively. AOTs are classified into follicular, extrafollicular, and peripheral types. Ameloblastomas are common, have an aggressive behavior and recurrent course, and are rarely metastatic, while AOTs are hamartomatous benign lesions derived from the complex system of the dental lamina or its remnants. With advances in the elucidation of molecular signaling mechanisms in cells, the cytodifferentiation of epithelial tumor cells in ameloblastomas and AOTs can be identified using different biomarkers. Therefore, it is suggested that comprehensive pathological observation including molecular genetic information can provide a more reliable differential diagnosis for the propagation and prognosis of ameloblastomas and AOTs. This study aimed to review the current concepts of ameloblastomas and AOTs and to discuss their clinico-pathological features relevant to tumorigenesis and prognosis.

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Original Articles

Immunohistochemical Array for Clear Cell Type Mucoepidermoid Carcinoma.: Yeon Sook Kim, Sang Shin Lee, Ji Yong Song, Eun Cheol Kim, Suk Keun Lee; Korean J Pathol. 2010;44(3):284-294.; DOI: https://doi.org/10.4132/KoreanJPathol.2010.44.3.284

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Abstract PDF

BACKGROUND
The protein expression profile of clear cell type mucoepidermoid carcinoma (MEC) is not well known.
METHODS
We examined a case of clear cell type MEC by immunohistochemical (IHC) array using 59 antibodies against oncoproteins, proliferation-related proteins, apoptosis-related proteins, growth factor-related proteins, angiogenesis-related proteins, and matrix proteins.
RESULTS
MEC tumor cells showed 40 to 60% more expression of BCL-2 and cyclin-dependent kinase 4 than normal gingival tissue, and 20-40% more expression of BCL-2-associated agonist of cell death, deleted in malignant brain tumors 1, E-cadherin, eIF5A, hypoxia-inducible factor, vimentin, and Wnt-1. Expression of other proteins, including p53, epidermal growth factor receptor, proliferating cell nuclear antigen, survivin, carcinoembryonic antigen, beta-catenin, poly-ADP ribose-polymerase, etc. were relatively weak in MEC tumor cells.
CONCLUSIONS
The IHC array for our MEC contained strong oncogenic signals involving Wnt-1/adenomatous polyposis coli, tumor necrosis factor a/signal transducer and activator of transcription 3/BCL-2, and pAKT pathways, signals that could result in the prolonged survival of clear tumor cells.

Citations

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Adolescent tongue base tumour with diagnostic histopathological dilemma
Mousam Maiti, Ajay Mallick, Debangshu Ghosh, Indranil Chakrabarti
BMJ Case Reports.2024; 17(8): e259570. CrossRef
A review: Immunological markers for malignant salivary gland tumors
P.C. Anila Namboodiripad
Journal of Oral Biology and Craniofacial Research.2014; 4(2): 127. CrossRef
DISPLACEMENT OF MAXILLARY LATERAL INCISOR CAUSED BY IDIOPATHIC GINGIVAL FIBROMATOSIS
Ji-Sook Jung, Ho-Won Park, Ju-Hyun Lee, Hyun-Woo Seo, Suk-Keun Lee
THE JOURNAL OF THE KOREAN ACADEMY OF PEDTATRIC DENTISTRY.2011; 38(3): 296. CrossRef

Gene Expressions of Mouse Submandibular Gland during the Developmental Stage and Their Antisense Inhibition in Organ Culture.: Yeon Sook Kim, Suk Keun Lee, Je G Chi; Korean J Pathol. 2000;34(6):395-412.

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Abstract PDF: This study is aimed to observe the expressions of different genes, including the extracellular matrix proteins, growth factors, and transcription factors during different developmental stages of mouse submandibular gland. Reverse transcription-polymerase chain reaction (RT-PCR) and the antisense inhibition in organ culture system were performed using mouse embryos and newborns. Total 140 mouse embryos (E14(80), E15(20), E16(20), E18(20)) and 30 newborn mice (D2(10), D3(10), D6(10)) obtained from 60 pregnant mice and 3 adult mice (3 weeks old) were used for the cDNA production and the salivary gland organ culture. Syndecan, perlecan, laminin alpha1 chain, TGF beta1, beta 3, and sonic hedgehog mRNAs were expressed in the early stage (E14~E16) of the submandibular gland development, whereas transglutaminase C (TGase C), E-cadherin, epimorphin, laminin beta2 and gamma1 chains, and HGF mRNAs were expressed in the middle and late stages (E16~E18, D2~D6). Antisense inhibition of different genes in the organ culture of E14 mouse embryos of submandibular gland showed specific growth retardation in the development of ductal and acinar cells. Especially, the antisense inhibition of perlecan, E-cadherin, laminin alpha1 chain, laminin beta2 chain, and syndecan mRNA arrested the growth of ductal and acinar cells. While the antisense inhibition of integrin beta5 greatly affected the acinar cell differentiation and also produced cystic dilatation of salivary ducts, the antisense inhibition of fibronectin showed aberrant growth of ectomesenchymal tissues of the mouse submandibular gland.

Molecular Cloning of Novel Genes Related to the Craniofacial Development of Human Embryo.: Young Jun Lee, Tak Soo Go, Hyung Wook Han, Sang Shin Lee, Eun Cheol Kim, Yeon Sook Kim, Suk Keun Lee, Je G Chi; Korean J Pathol. 2000;34(12):961-971.

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Abstract PDF: In order to obtain novel genes for craniofacial development of human, molecular cloning and sequencing were performed and followed by in situ hybridization in tissue sections. Subtracted cDNA library of craniofacial tissue from 8 weeks old human embryo was made by the subtraction with cDNA of RHEK cells. A total of 231 clones were obtained and their partial sequence data disclosed that 214 clones were nonredundant in Genebank search. We have done in situ hybridization screening on the craniofacial sections of a 10 weeks old human fetus, and found significant positive reaction in 30 clones. Depending on the cell type of similar developmental origin, the positive reactions could be divided into four groups: first group showed an intense positive reaction in neural tube, ganglion, and a part of peripheral nerve tissue, second group relatively diffuse positive reaction in neural tube, cartilage, epithelium, and muscle, third group localized positive reaction in nerve, and muscle, and fourth group positive reaction in almost all kinds of cells of craniofacial tissues. Although every clone showed different expression patterns in the craniofacial development, some of them showed intense mRNA expressions in the characteristic cell type. Because this study also aimed to test a screening methods to find out novel genes related to craniofacial development by the subtracted cDNA library and in situ hybridization, the intense positive reaction of a certain clone by in situ hybridization may indicate its role in the developmental processes. We presumed that 30 clones selected in this study are possibly important new genes for the development of human craniofacial structure.

Improved Technique of Digoxigenin Labeled RNA in situ Hybridization.: Suk Keun Lee, Yeon Sook Kim, In Sun Song, Sang Shin Lee, Young Jun Lee, Woo Ho Kim, Je Geun Chi; Korean J Pathol. 2001;35(2):98-110.

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Abstract PDF: BACKGROUND
A practical RNA in situ hybridization method using digoxigenin labeled RNA probes is described in order to evaluate the technical difficulties and problems in RNA in situ hybridization.
METHODS
The paraffin sections, routinely processed in the Pathology Laboratory, were tested for the possibility of RNA in situ hybridization instead of the RNase free paraffin sections, fixed in 4% paraformaldehyde and prepared using RNase protection procedures.
RESULTS
Most of the paraffin sections, fixed in 10% neutral formalin solution in fresh condition, showed relatively good reaction of RNA in situ hybridization, although the necrotic tissue and autopsy specimens showed poor reaction of RNA in situ hybridization. A refixation procedure using a 4% paraformaldehyde solution was evaluated for optimal expression of mRNA in the paraffin sections.
CONCLUSION
The treatment of 4% paraformaldehyde before the treatment of proteinase K showed better in situ hybridization than did the treatment of 4% paraformaldehyde after the treatment of proteinase K. Also a new Polymerase Chain Reaction (PCR)-based method of RNA probe production showed consistently good results.

Prenatal Development of Human Lip with Immunohistochemical Study.: Su Jung Hong, Young Joon Lee, Yeon Sook Kim, Suk Keun Lee, Je G Chi; Korean J Pathol. 2002;36(4):212-221.

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Abstract PDF: BACKGROUND
This study is aimed to elucidate the developmental pattern of human fetal lip by histological and immunohistochemical examinations.
METHODS
Totally 231 normal human lip tissues obtained from autopsied fetuses were fixed with 10% buffered formalin, sectioned in cross and longitudinal directions, routinely stained for H&E and performed for immunohistochemistry with antibodies of S-100 protein, proliferating cell nuclear antigen (PCNA), transglutaminase C (TGase-C), metalloproteinase (MMP)-3, MMP-10, tenascin, KL1, K8.12, E-cadherin, tissue inhibitors of matrix metalloproteinase (TIMP)-1, TIMP-2 and total keratin (TK).
RESULTS
The lip structure first appeared as an orifice of stomodeum around the 7-8th week of gestation, and a major structure of the midface was observed by the 11-12th week. As the squamous epithelium of the lip became thick and was keratinized, the vermilion border became distinguished in the 15-16th week, and the lip structure was almost completed with the presence of orbicularis oris muscle in the lingual side of vermilion border by the 17-18th week. Immunohistochemically, the vermilion border showed strong reactions for tenascin, E-cadherin and MMP-3 and increased positivity for PCNA, cytokeratins (TK, KL1, K8.12), and TGase-C.
CONCLUSIONS
With the above findings we suppose that the cytodifferentiation of vermilion border epithelium plays an important role for the development of human fetal lip.

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