Hostname: page-component-6bf8c574d5-b4m5d Total loading time: 0 Render date: 2025-02-24T09:45:24.588Z Has data issue: false hasContentIssue false
  • English
  • Français

Histogenesis of salivary gland neoplasms: a postulate with prognostic implications

Published online by Cambridge University Press:  29 June 2007

John G. Batsakis ,
Joseph A. Regezi ,
Mario A. Luna  and
Adel El-Naggar
John G. Batsakis*
Affiliation:
Department of Pathology, The University of Texas MD, Anderson Cancer Center, Houston, Texas
Joseph A. Regezi
Affiliation:
Department of Oral Pathology, University of Michigan Dental School, Ann Arbor, Michigan
Mario A. Luna
Affiliation:
Department of Pathology, The University of Texas MD, Anderson Cancer Center, Houston, Texas
Adel El-Naggar
Affiliation:
Department of Pathology, The University of Texas MD, Anderson Cancer Center, Houston, Texas
*
Dr John G. Batsakis, Department of PathologyThe University of TexasM.D. Anderson Cancer Centre, 1515 Holcombe Boulevard, Houston, Texas 77030.
Get access Rights & Permissions [Opens in a new window]

Abstract

In a continually renewing cell population, stem cells can be regarded as a reservoir of cells with a high capacity for self renewal that give rise to all differentiated progeny. They are the primary source for the generation and maintenance of cellular diversity and tissue homeostasis. In general, neoplasms manifest differentiation pathways similar to those found in the development and renewal of the normal tissues from which they arise. This feature serves as a basis for classification schemes of neoplasms and, as in the normal tissues, there is usually an inverse correlation between proliferative capacity and differentiation within the neoplasms. In our postulate of the histogenesis of salivary gland neoplasia, we evoke the stem cell model to account for the considerable phenotypic heterogeneity seen with these neoplasms. We further consider the neoplasms and, in particular, their myoepithelial constituencies to be manifestations of escape from normal regulatory mechanisms that determine differentiation pathways which a stem cell and its progeny can take. Clinical and basic scientific evidence are presented to support the postulate and also to point to the mitigating role that myoepithelial differentiation has in the biological course of salivary gland neoplasms.

Type
Main Articles
Information
The Journal of Laryngology & Otology , Volume 103 , Issue 10 , October 1989 , pp. 939 - 944
Copyright
Copyright © JLO (1984) Limited 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Azuma, M., Yoshida, H., Kawamata, H., Yanagawa, T., Furumoto, N. and Sato, M. (1988) Cellular proliferation and ras oncogene of p21 21,000 expression in relation to the intracellular cyclic adenosine 3′:5′—monophosphate levels of a human salivary gland adenocarcinoma cell line in culture. Cancer Research, 49: 2898–2903.Google Scholar
Batsakis, J. G. (1980) Salivary gland neoplasia: an outcome of modified morphogenesis and cytodifferentiation. Oral Surgery, Oral Medicine, Oral Pathology, 49: 229–232.CrossRefGoogle ScholarPubMed
Batsakis, J. G., Kraemer, B. B. and Sciubba, J. J. (1983) The pathology of head and neck tumours: the myoepithelial cell and its participation in salivary gland neoplasia. Part 17. Head and Neck Surgery, 5: 222–233.CrossRefGoogle ScholarPubMed
Batsakis, J. G., Ordonez, N. G., Meis, J. M. and Bruner, J. M. (1986) S-100 protein and myoepithelial neoplasms. Journal of Laryngology and Otology, 100: 687–698.CrossRefGoogle ScholarPubMed
Brown, G., Bunce, C. M., Lord, J. M. and McConnell, F. M. (1988) The development of cell lineages: A sequential model. Differentiation, 39: 83–89.CrossRefGoogle ScholarPubMed
Caselitz, J. Das pleomorphe Adenom der Speicheldrüsen. Histogenese, zelluläre Differenzierung, Tumormarker. Gustav Fisher Verlag. Stuttgart, 1987.Google Scholar
Caselitz, J., Osborn, M., Hamper, K., Wustrow, J., Rauchfus, A. and Weber, K. (1986) Pleomorphic adenomas, adenoid cystic carcinomas and adenolymphomas of salivary glands analyzed by a monoclonal antibody against myoepithelial/basal cells. An immunohistochemical study. Virchows Archiv für Pathologische Anatomie und Physiologie, 409: 805–816.CrossRefGoogle Scholar
Chaudhry, A. P., Schmutz, J. A., Cutler, L. S. and Sunderraj, M. (1983) Prenatal and postnatal histogenesis of myoepithelium in hamster submandibular gland. Journal of Submicroscopic Cytology, 15: 787–798.Google ScholarPubMed
Chaudhry, A. P., Cutler, L. S., Schmutz, J. A., Yamane, G. M., Sunderraj, M. and Pierri, L. K. (1985) Development of the hamster submandibular gland. I. The acinar intercalated duct complex. Journal of Submicroscopic Cytology, 17: 555–567.Google ScholarPubMed
Cutler, L. S. (1980) The dependent and independent relationship between cytodifferentiation and morphogenesis in developing salivary gland secretory cells. Anatomical Record, 196: 341–347.CrossRefGoogle ScholarPubMed
Dardick, I. and van Nostrand, P. (1987) Morphogenesis of salivary gland tumors. A prerequisite to improving classification. Pathology Annual, 22: (part 1) 1–53.Google ScholarPubMed
Dulbecco, R., Unger, M., Armstrong, B., Bowman, M. and Syka, P. (1982) Epithelial cell types and their evolution in rat mammary gland determined by immunological markers. Proceedings of the National Academy of Science U.S.A., 79: 7346–7350.CrossRefGoogle Scholar
Dulbecco, R., Allen, W. R., Bologna, M. and Bowman, M. (1986) Marker evolution during the development of the rat mammary gland: stem cells identified by markers and the role of myoepithelial cells. Cancer Research, 46: 2449–2456.Google ScholarPubMed
Dunnington, J., Kim, U., Hughes, C. M., Monaghan, P., Ormerod, E. J. and Rudland, P. S. (1984) Study of myoepithelial cell characteristics in metastasizing mammary tumours relative to their nonmetastasizing counterparts. Journal of the National Cancer Institute, 72: 455–461.Google Scholar
Elsasser, H-P., Lutcke, H. and Kern, H. F. (1986) In The Exocrine Pancreas: Biology, Pathobiology, and Diseases Go, V. Y., Gardner, J. D., Brooks, F. P., Lebenthal, E., DiMagno, E. P. and Scheele, G. A., eds., 45–53, Raven Press, New York, N.Y.Google Scholar
Eversole, L. R. (1971) Histogenic classification of salivary tumors. Archives of Pathology, 92: 433–443.Google ScholarPubMed
Gibson, H. M. L. (1983) The prenatal human submandibular gland: A histological, histochemical and ultrastructural study. Anatomischer Anzeiger Jena, 153: 91–105.Google ScholarPubMed
Johns, M. E., Mills, S. E. and Thompson, K. K. (1983) Colony-forming assay of human salivary gland tumors. Applications for chemosensitivity and histogenetic studies. Archives of Otolaryngology, 109: 709–714.CrossRefGoogle ScholarPubMed
Joshi, K., Smith, J. A., Persusinghe, N. and Monoghan, P. (1986) Cell proliferation in human mammary epithelium. Differential contribution by epithelial and myoepithelial cells. American Journal of Pathology, 124: 199–206.Google ScholarPubMed
Leading Article (1989) Stem cells in neoplasia. The Lancet, 1: 701–702.Google Scholar
Luna, M. A., Batsakis, J. G., Ordonez, N. G., Mckay, B. and Tortoledo, M. E. (1987) Salivary gland adenocarcinomas: A clinicopathologic analysis of three distinctive types. Seminars in Diagnostic Pathology, 4: 117–135.Google ScholarPubMed
Mori, M., Tsukitani, K., Ninomiya, T. and Okada, Y. (1987) Various expressions of modified myoepithelial cells in salivary pleomorphic adenomas. Immunhistochemical studies. Pathology, Research, Practice, 182: 632–646.Google Scholar
Mori, M., Ninomiya, T., Okada, Y. and Tsukitani, K. (1989) Myoepitheliomas and myoepithelial adenomas of salivary gland origin. Immunohistochemical evaluation of filament proteins, S-100 a and b, glial fibrillary acidic proteins, neuron-specific enolase, and lactoferrin. Pathology Research Practice, 184: 168–178.CrossRefGoogle Scholar
Nagashima, Y. and Ono, K. (1985) Myoepithelial cell ultrastructure in the submandibular gland of man. Anatomy and Embryology, 171: 259–265.CrossRefGoogle ScholarPubMed
Nagle, R. B., Böcker, W., Davis, J. R., Heid, H. W., Kaufmann, M., Lucas, D. O. and Jarasch, E. D. (1986) Characterization of breast carcinomas by two monoclonal antibodies distinguishing myoepithelial from luminal epithelial cells. Journal of Histochemistry and Cytochemistry, 34: 869–881.CrossRefGoogle ScholarPubMed
Nogawa, H. (1983) Determination of the curvature of epithelial cell mass by mesenchyme in branching morphogenesis of mouse salivary gland. Journal of Embryology and Experimental Morphology, 73: 221–232.Google ScholarPubMed
Ormerod, E. J. and Rudland, P. S. (1982) Mammary gland morphogenesis in vitro: Formation of branched tubules in collagen gels by cloned rat mammary cell line. Developmental Biology, 91: 360–375.CrossRefGoogle ScholarPubMed
Ormerod, E. J. and Rudland, P. S. (1984) Cellular composition and organization of ductal buds in developing rat mammary glands: Evidence for morphological intermediates between epithelial and myoepithelial cells. American Journal of Anatomy, 170: 631–652.CrossRefGoogle ScholarPubMed
Pierce, G. B. (1974) Neoplasms, differentiations, and mutations. American Journal of Pathology, 77: 103–118.Google ScholarPubMed
Pierce, G. B. and Johnson, L. D. (1971) Differentiation and cancer. In Vitro, 7: 140–145.CrossRefGoogle ScholarPubMed
Pound, A. W. and Walker, N. I. (1981) Involution of the pancreas after ligation of the pancreatic ducts: I. A histological study. British Journal of Experimental Pathology, 62: 547–558.Google Scholar
Pour, P. M. (1988) Mechanism of pseudoglandular (tubular) formation during pancreatic carcinogensis in the hamster model. An electron-microscopic and immunohistochemical study. American Journal of Pathology, 130: 335–344.Google Scholar
Regezi, J. A. and Batsakis, J. G. (1977) Histogenesis of salivary gland neoplasms. Otolaryngologic Clinics of North America, 10: 297–307.CrossRefGoogle ScholarPubMed
Rudland, P. S. (1987) Stem cells and the development of mammary cancers in experimental rats and in humans. Cancer and Metastasis Reviews, 6: 55–83.CrossRefGoogle ScholarPubMed
Sciubba, J. J. and Brannon, R. B. (1982) Myoepithelioma of salivary glands: report of 23 cases. Cancer, 49: 562–572.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Shirasuna, K., Watatani, K., Sugiyama, M., Morioka, S. and Miyazaki, T. (1986) Isolation and characterization of different clones including myoepithelial-like variants from a clonal neo-plastic epithelial duct cell line on human salivary gland origin. Cancer Research, 46: 1418–1426.Google Scholar
Sieber-Blum, M. (1989) Commitment of neural crest cells to the sensory neuron lineage. Science, 243: 1608–1610.CrossRefGoogle Scholar
Walker, N. I. and Gobe, G. C. (1987) Cell death and cell proliferation during atrophy of the rat parotid gland induced by duct obstruction. Journal of Pathology, 153: 333–344.CrossRefGoogle ScholarPubMed
Walker, R. A. (1988) Breast myoepithelium—the ignored cell. Journal of Pathology, 156: 5–6.CrossRefGoogle ScholarPubMed
Warburton, M. J., Ferns, S. A. and Rudland, P. S. (1982) Enhanced synthesis of basement membrane proteins during differentiation of rat mammary tumour epithelial cells into myoepithelial-like cells in vitro. Experimental Cell Research, 137: 373–380.CrossRefGoogle ScholarPubMed
Williams, J. M. and Daniel, C. W. (1983) Mammary ductal elongation: Differentiation of myoepithelium and basal lamina during branching morphogenesis. Developmental Biology, 97: 274–290.CrossRefGoogle ScholarPubMed