This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Lee, S.K. Articles by Chung, S.I. Search for Related Content PubMed PubMed Citation Articles by Lee, S.K. Articles by Chung, S.I. Social Bookmarking                         What's this?

Expression of Transglutaminase C during the Prenatal Development of Human Submandibular Glands

Department of Pathology, College of Medicine, Seoul National University, Seoul, Korea

J.G. Chi

Department of Pathology, College of Medicine, Seoul National University, Seoul, Korea

Y.J. Jeon

Department of Biochemistry, College of Medicine, Seoul National University, Seoul, Korea

S.C. Park

Department of Biochemistry, College of Medicine, Seoul National University, Seoul, Korea

M. Mori

Department of Oral and Maxillofacial Surgery, School of Dentistry, Asahi University, Gifu, Japan

S.I. Chung

Laboratory of Cellular Development and Oncology, National Institute of Dental Research, National Institutes of Health, Bethesda, Maryland 20892, USA

The involvement of transglutaminase C (TGase C) in morphogenesis and cytodifferentiation during glandular tubule formation was addressed by immunolocalization of the protein at different stages of prenatal human submandibular gland development in 100 fetuses and 20 adult salivary glands. Immunocytochemical detection was carried out using a monospecific antibody to TGase C. The results showed TGase C reactivity in both acini and ducts early in development (from 10 to 14 weeks), followed by a marked increase in ductal activity and a decline in acinar activity up to 32 weeks. During the peak of reactivity at 25 to 32 weeks, staining was concentrated in the apical ends of the columnar cells. In the adult, staining was weakly and diffusely distributed in the striated and excretory ducts. Western blot analysis of the cellular extracts of pooled samples from various stages of salivary gland development showed a single strong band at 76 kDa early in development. This band became weaker after 32 weeks of prenatal development and in the adult. These findings of transient high expression of TGase C, which coincide with the development of tubulo-alveolar structure, suggest that TGase C may play a role in morphogenesis in human salivary gland development.

Key Words: prenatal development • salivary gland • transglutaminase

REFERENCES

• Avery JK (1987). Oral development and histology: structure and function of salivary glands. Baltimore, MD: Williams and Wilkins.
• Barsigian C., Stern AM, Martinez J. (1991). Tissue (Type II) transglutaminase covalently incorporates itself, fibrinogen, or fibronectin into high molecular weight complexes on the extracellular surface of isolated hepatocytes: use of 2[(2-oxopropyl)thio]-imidazolium derivatives as cellular transglutaminase inactivators. J. Biol Chem 266:22501-22509. Batsakis JG (1980). Salivary gland neoplasia: an outcome of
• Bergamini CM, Signorini M. (1993). Studies on tissue transglutaminases: interaction of erythrocyte type-2 transglutaminase with GTP. Biochem J 291:37-39.[Medline] [Order article via Infotrieve]
• Cardinali M., Uchino R., Chung SI (1990). Interaction of fibrinogen with murine melanoma cells: covalent association with cell membranes and protection against recognition by lymphokine-activated killer cells. Cancer Res 50:8010-8016.[Abstract/Free Full Text]
• Chang SK, Chung SI (1986). Cellular transglutaminase: The particulate-associated transglutaminase from chondrosarcoma and liver. J Biol Chem 261:8112-8121. Chung SI (1972). Comparative studies on tissue transglutaminase and factor XHI. Ann NY Acad Sci 202:240-255.[Medline] [Order article via Infotrieve]
• Chung SI (1975). Multiple molecular forms of transglutaminases in human and guinea pig. Markert CL, Ed. New York: Isozymes Acad. Press, pp. 1259-1274.
• Cocuzzi ET, Chung SI (1986). Cellular transglutaminase: Lung matrix-associated transglutaminase: characterization and activation with sulfhydryls. J Biol Chem 261:8122-8127. Cocuzzi E., Kim HC, Beninati S., Hand AR, Chung SI (1989). Transglutaminase expression in rat parotid gland after isoproterenol stimulation. J Dent Res 68:1474-1478. Connellan JM, Chung SI, Whetzel NK, Bradley LM, Folk JE (1971). Structural properties of guinea pig liver transglutaminase. J Biol Chem 246:1093-1098.[Abstract/Free Full Text]
• Dardick I., van Nostrand AWP (1987). Morphogenesis of salivary gland tumors. A prerequisite to improving classification. Pathol Ann 22:1-53.
• Dardick I., Naiberg J., Leung R., Ramjohn S., Christensen H., Burford-Mason A., et al. (1990). Ultrastructural study of acinar and intercalated duct organization of submandibular and parotid salivary gland. Lab Invest 63:394-404.
• Devi NS, Jacoby F. (1966). The submaxillary gland of the golden hamster and its post-natal development. J Anat (Lond ) 100:269-285.[Medline] [Order article via Infotrieve]
• Eitan S., Solomon A., Lavie V., Yoles E., Hirschberg DL, Bilkin M., et al. (1994). Recovery of visual response of injured adult rat optic nerves treated with transglutaminase. Science 264:1764-1768.[Abstract/Free Full Text]
• Fesus L. (1993). Biochemical events in naturally occurring forms of cell death. FEBS Lett 328:1-5.[CrossRef][Medline] [Order article via Infotrieve]
• Folk JE, Chung SI (1973). Molecular and catalytic properties of transglutaminases. Adv Enzymol Relat Areas Molec Biol 38:109-191.
• Folk JE, Chung SI (1985). Transglutaminases. Meth Enzymol 113:358-375.[Medline] [Order article via Infotrieve]
• Fukuda M. (1967). Histochemical studies on the rat submaxillary gland during post-natal development. Histochemie 8:342-354.[Medline] [Order article via Infotrieve]
• Gentile V., Thomazy VA, Piacentini M., Fesus L., Davies PJ (1992). Expression of tissue transglutaminase in Balb-C 3T3 fibroblasts: effects on cellular morphology and adhesion. J Cell Biol 119:463-474.[Abstract/Free Full Text]
• Gibson MHL (1983). The prenatal human submandibular gland: A histological, histochemical and ultrastructural study. Anat Anz Jena 153:91-105.
• Greenberg CS, Birckbichler PJ, Rice RH ( 1991). Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues. FASEB J 5:3071-3077.[Abstract]
• Gustafsson H., Kjorell U., Ericksson A., Virtanen I., Thornell LE (1988). Distribution of intermediate filament proteins in developing and adult salivary glands in man. Anat Embryol 178:243-251.[Medline] [Order article via Infotrieve]
• Jacoby R., Leeson CR (1959). The postnatal development of the rat submaxillary gland. J Anat (Lond) 93:201-216.[Medline] [Order article via Infotrieve]
• Jamieson JD (1983). The exocrine pancreas and salivary glands. In: Cell and tissue biology. Weiss L, Editor. Baltimore, MD: Urband and Schwarzenberg, pp. 715-736.
• Jiang H., Kochhar DM (1992). Induction of tissue transglutaminase and apoptosis by retinoic acid in the limb bud. Teratology 46:333-340.[CrossRef][Medline] [Order article via Infotrieve]
• Laemmli UK (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277:680-685. Lee KN, Arnold SA, Birckbichler PJ, Patterson MK Jr, Fraij BM, Takeuchi Y., et al. (1993). Site-directed mutagenesis of human tissue transglutaminase: Cys-277 is essential for transglutaminase activity but not for GTPase activity. Biochim Biophys Acta 1202:1-6.[CrossRef][Medline] [Order article via Infotrieve]
• Lee SK, Lim CY, Chi JG, Yamada K., Hashimura K., Kunikata M., et al. (1990). Prenatal development of human major salivary glands and immunohistochemical detection of keratins using monoclonal antibodies. Acta Histochem 89:213-235. Leoncini P., Cintorino M., Vindigni C., Leoncini L., Armellini D., Bugnoli M., et al. (1988). Distribution of cytoskeletal and contractile proteins in normal and tumor bearing salivary and lacrimal glands. Virchows Arch (A) 412:329-337. Martinez-Madrigal F., Micheau C. (1989). Histology of the major salivary glands. Am J Surg Pathol 13:879-899.[Medline] [Order article via Infotrieve]
• Nakaoka H., Perez DM, Baek KJ, Das T., Hurain A., Misono K., et al. (1994). Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science 264:1593-1596.[Abstract/Free Full Text]
• Piacentini M., Fesus L., Melino G. (1993). Multiple cell cycle access to the apoptotic death programmed in human neuroblastoma cells. FEBS Lett 320:150-154.[CrossRef][Medline] [Order article via Infotrieve]
• Redman RS, Sreebny LM (1971). Morphologic and biochemical observations on the development of the rat parotid gland. Dev Biol 25:248-279.[Medline] [Order article via Infotrieve]
• Shackleford JM, Wilborn WH (1970). Ultrastructural aspects of calf submandibular glands. Am J Anat 127:259-279.[Medline] [Order article via Infotrieve]
• Singer MA, Hortsch M., Goodman CS, Bentley D. (1992). Annulin, a protein expressed at limb segment boundaries in the grasshopper embryo, is homologous to protein crosslinking transglutaminases. Dev Biol 154:143-159. Spooner BS, Wessells NK (1972). An analysis of salivary gland morphogenesis: role of cytoplasmic microfilaments and microtubules. Dev Biol 27:38-54.[CrossRef][Medline] [Order article via Infotrieve]
• Testa-Riva F., Puxeddu P., Riva A., Diaz G. ( 1981). The epithelium of the excretory duct of the human submandibular gland: a transmission and scanning electron microscopic study. Am J Anat 160:381-393.[Medline] [Order article via Infotrieve]
• Tyrrell DJ, Sale WS, Slife CW (1986). Localization of a liver transglutaminase and a large molecular weight transglutaminase substrate to a distinct plasma membrane domain. J Biol Chem 261:14833-14836.[Abstract/Free Full Text]

Journal of Dental Research, Vol. 74, No. 11, 1812-1816 (1995)
DOI: 10.1177/00220345950740111501


CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				S. K. Lee, J. G. Chi, S. C. Park, and S. I. Chung Transient Expression of Transglutaminase C During Prenatal Development of Human Muscles J. Histochem. Cytochem., November 1, 2000; 48(11): 1565 - 1574. [Abstract] [Full Text]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Lee, S.K. Articles by Chung, S.I. Search for Related Content PubMed PubMed Citation Articles by Lee, S.K. Articles by Chung, S.I. Social Bookmarking                         What's this?