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Neuroectodermal Antigens Persist in Benign and Malignant Salivary Gland Tumor Cultures

Neuroectodermal Antigens Persist in Benign and Malignant Salivary Gland Tumor Cultures Abstract Objective: To determine whether a heterogeneous collection of salivary gland tumors shared common antigenic characteristics and growth patterns in tissue culture. Design: Cell cultures were derived from benign and malignant salivary gland neoplasms, cultured conservatively, and serially analyzed for epithelial, myoepithelial, and neuroectodermal antigens. Subjects: Nineteen samples reflecting the spectrum of salivary tumor pathologic characteristics were established in tissue culture. Most were derived from benign pleomorphic adenomas, and several were from carcinomas, including carcinoma ex pleomorphic adenoma, and mucoepidermoid and adenoid cystic carcinoma. Results: All cultures were epithelial as determined by morphologic and antigenic examination, using antibodies for cytokeratin. The phenotype of cells derived from benign tumors, especially the pleomorphic adenomas, resembled those in the original neoplasm. Those from carcinomas were similar, with less differentiated characteristics. Manipulation of growth conditions altered the phenotypes shown in culture. Some cultures contained cells expressing vascular smooth-muscle actin and glial fibrillary acidic protein or nestin. Conclusions: This model cell system containing proliferative cells from several tumor types is consistent with a stem-cell theory of salivary gland tumor origin. Our data were not consistent with the bicellular or multicellular theory. We hypothesize a neuroectodermal origin for this group of apparently heterogeneous tumors. These cultured cells will be valuable for in-depth investigation of the loss of proliferation controls in benign and malignant tumors of the salivary gland.(Arch Otolaryngol Head Neck Surg. 1996;122:551-558) References 1. Martinez-Madrigal F, Micheau C. Histology for the major salivary glands . Am J Surg Pathol . 1989;13:879-899.Crossref 2. Johns M, Goldsmith M. Incidence, diagnosis, and classification of salivary gland tumors, 1 . Oncology . 1989;3:47-56. 3. Yoshida H, Azuma M, Yanagawa T, Yura Y, Sato M. Effect of dibutyl cyclic AMP on morphologic features and biologic markers of a human salivary gland adenocarcinoma cell line in culture . Cancer . 1986;57:1011-1018.Crossref 4. Dardick I, Byard R, Carnegie J. A review of the proliferative capacity of major salivary glands and the relationship to current concepts of neoplasia in salivary glands . Oral Surg Oral Med Oral Pathol . 1990;69:53-67.Crossref 5. Burford-Mason A, Byard RW, Dardick I, van Nostrand AWP. The pathobiology of the salivary gland, I: growth and development of rat submandibular gland organoids cultured in a collagen gel matrix . Virchows Arch . 1991;418: 387-400.Crossref 6. Batsakis J, Regezi J, Luna M, el-Naggar A. Histogenesis of salivary gland neoplasms: a postulate with prognostic implications . J Laryngol Otol . 1989;103: 939-944.Crossref 7. Witsell D, Weissler M, Livanos E, Bova-Hill C, Gilmer T. Unique chromosomal rearrangement and mucin production in a novel salivary myoepithelial cell strain . Arch Otolaryngol Head Neck Surg . 1993;119:1151-1157.Crossref 8. Sabatini L, Allen-Hoffman B, Warner T, Azen E. Serial cultivation of epithelial cells from human salivary glands . In Vitro Cell Dev Biol Anim . 1991;27:939-948.Crossref 9. Marmary Y, He X, Hand A, Ship J, Wellner R. Beta-adrenergic responsiveness in a human submandibular tumor cell line . In Vitro Cell Dev Biol Anim . 1989; 25:951-958.Crossref 10. Ross DA, Huaman JA, Barsky SH. A study of the heterogeneity of the mucoepidermoid tumor and the implication for future therapies . Arch Otolaryngol Head Neck Surg . 1992;118:1172-1178.Crossref 11. Sens DA, Hintz DS, Rudisill MT, Sens MA, Spicer SS. Explant culture of the human submandibular gland epithelial cells: evidence for ductal origin . Lab Invest . 1985;52:559-567. 12. Kurth BE, Hazen-Martin DJ, Sens MA, DeChamplain RW, Sens DA. Cell culture and characterization of human minor salivary gland duct cells . J Oral Pathol Med . 1989;18:214-219.Crossref 13. Iga H, Azuma M, Nagamine S, et al. Expression of neurofilaments in a neoplastic human salivary intercalated duct cell line or its derivatives and effect of nerve growth factor on the cellular proliferation and phenotype . Cancer . 1989; 49:6708-6719. 14. Keyomarski K, Sandoval L, Band V, Pardee AB. Synchronization of tumor and normal cells from GI to multiple cell cycles by lovastatin . Cancer Res . 1991; 51:3602-3609. 15. Tohyama T, Lee VMY, Rorke LB, Marvin M, McKay RDG, Trojanowski JQ. Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells . Lab Invest . 1992;66:303-313. 16. Chiu F-C, Barnes EA, Das K, et al. Characterization of a novel 66 kd subunit of mammalian neurofilaments . Neuron . 1989;2:1435-1445.Crossref 17. Hirano T, Gluckman J, de Vries E. The expression of alpha vascular smoothmuscle actin in salivary gland tumors . Arch Otolaryngol Head Neck Surg . 1990; 116:692-696.Crossref 18. Stemple DL, Anderson DJ. Isolation of a stem cell for neurons and glia from the mammalian neural crest . Cell . 1992;71:973-985.Crossref 19. Cepko C. Lineage analysis in the vertebrate nervous system by retrovirusmediated gene transfer . Methods Neurosci . 1989;1:367-392. 20. Durban E, Barreto P, Higers J, Sonnenberg A. Cell phenotypes and differentiative transitions in mouse submandibular salivary gland defined with monoclonal antibodies to mammary epithelial cells . J Histochem Cytochem . 1994; 42:185-196.Crossref 21. Hall PA, Watt FM. Stem cells: the generation and maintenance of cellular diversity . Development . 1989;106:619-633. 22. Dardick I. Myoepithelioma: definitions and diagnostic criteria . Ultrastruct Pathol . 1995;19:335-345.Crossref 23. LeDouarin NM, Smith J. Development of the peripheral nervous system from the neural crest . Annu Rev Cell Biol . 1988;4:375-404.Crossref 24. Bronner-Fraser M. Mechanisms of neural crest cell migration . Bioessays . 1993; 15:221-230.Crossref 25. Bronner-Fraser M. Neural crest cell formation and migration in the developing embryo . FASEB J . 1994;8:699-706. 26. Selleck MAJ, Scherson TY, Bronner-Fraser M. Dev Biol . 1993;159:1-11.Crossref 27. Gans C, Northcutt RG. Neural crest and the origin of vertebrates: a new head . Science . 1983;220:268-274.Crossref 28. Sellect MAJ, Bronner-Fraser M. Origins of the avian neural crest: the role of neural palate-epidermal interactions . Development . 1995;121:525-538. 29. Baroffio A, Dupin E, LeDouarin NM. Common precursors for neural or mesectodermal derivatives in the cephalic neural crest . Development . 1991;112: 301-305. 30. Trainor PA, Tan S-S, Tam PPL. Cranial paraxial mesoderm: regionalization of cell fate and impact on craniofacial development in mouse embryos . Development . 1994;120:2397-2408. 31. Couly GF, Coltey PM, LeDouarin NM. The developmental fate of the cephalic mesoderm in quail-chick chimeras . Development . 1992;114:1-15. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Otolaryngology - Head & Neck Surgery American Medical Association

Neuroectodermal Antigens Persist in Benign and Malignant Salivary Gland Tumor Cultures

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/lp/american-medical-association/neuroectodermal-antigens-persist-in-benign-and-malignant-salivary-8kAUGoPYDu
Publisher
American Medical Association
Copyright
Copyright © 1996 American Medical Association. All Rights Reserved.
ISSN
0886-4470
eISSN
1538-361X
DOI
10.1001/archotol.1996.01890170083015
Publisher site
See Article on Publisher Site

Abstract

Abstract Objective: To determine whether a heterogeneous collection of salivary gland tumors shared common antigenic characteristics and growth patterns in tissue culture. Design: Cell cultures were derived from benign and malignant salivary gland neoplasms, cultured conservatively, and serially analyzed for epithelial, myoepithelial, and neuroectodermal antigens. Subjects: Nineteen samples reflecting the spectrum of salivary tumor pathologic characteristics were established in tissue culture. Most were derived from benign pleomorphic adenomas, and several were from carcinomas, including carcinoma ex pleomorphic adenoma, and mucoepidermoid and adenoid cystic carcinoma. Results: All cultures were epithelial as determined by morphologic and antigenic examination, using antibodies for cytokeratin. The phenotype of cells derived from benign tumors, especially the pleomorphic adenomas, resembled those in the original neoplasm. Those from carcinomas were similar, with less differentiated characteristics. Manipulation of growth conditions altered the phenotypes shown in culture. Some cultures contained cells expressing vascular smooth-muscle actin and glial fibrillary acidic protein or nestin. Conclusions: This model cell system containing proliferative cells from several tumor types is consistent with a stem-cell theory of salivary gland tumor origin. Our data were not consistent with the bicellular or multicellular theory. We hypothesize a neuroectodermal origin for this group of apparently heterogeneous tumors. These cultured cells will be valuable for in-depth investigation of the loss of proliferation controls in benign and malignant tumors of the salivary gland.(Arch Otolaryngol Head Neck Surg. 1996;122:551-558) References 1. Martinez-Madrigal F, Micheau C. Histology for the major salivary glands . Am J Surg Pathol . 1989;13:879-899.Crossref 2. Johns M, Goldsmith M. Incidence, diagnosis, and classification of salivary gland tumors, 1 . Oncology . 1989;3:47-56. 3. Yoshida H, Azuma M, Yanagawa T, Yura Y, Sato M. Effect of dibutyl cyclic AMP on morphologic features and biologic markers of a human salivary gland adenocarcinoma cell line in culture . Cancer . 1986;57:1011-1018.Crossref 4. Dardick I, Byard R, Carnegie J. A review of the proliferative capacity of major salivary glands and the relationship to current concepts of neoplasia in salivary glands . Oral Surg Oral Med Oral Pathol . 1990;69:53-67.Crossref 5. Burford-Mason A, Byard RW, Dardick I, van Nostrand AWP. The pathobiology of the salivary gland, I: growth and development of rat submandibular gland organoids cultured in a collagen gel matrix . Virchows Arch . 1991;418: 387-400.Crossref 6. Batsakis J, Regezi J, Luna M, el-Naggar A. Histogenesis of salivary gland neoplasms: a postulate with prognostic implications . J Laryngol Otol . 1989;103: 939-944.Crossref 7. Witsell D, Weissler M, Livanos E, Bova-Hill C, Gilmer T. Unique chromosomal rearrangement and mucin production in a novel salivary myoepithelial cell strain . Arch Otolaryngol Head Neck Surg . 1993;119:1151-1157.Crossref 8. Sabatini L, Allen-Hoffman B, Warner T, Azen E. Serial cultivation of epithelial cells from human salivary glands . In Vitro Cell Dev Biol Anim . 1991;27:939-948.Crossref 9. Marmary Y, He X, Hand A, Ship J, Wellner R. Beta-adrenergic responsiveness in a human submandibular tumor cell line . In Vitro Cell Dev Biol Anim . 1989; 25:951-958.Crossref 10. Ross DA, Huaman JA, Barsky SH. A study of the heterogeneity of the mucoepidermoid tumor and the implication for future therapies . Arch Otolaryngol Head Neck Surg . 1992;118:1172-1178.Crossref 11. Sens DA, Hintz DS, Rudisill MT, Sens MA, Spicer SS. Explant culture of the human submandibular gland epithelial cells: evidence for ductal origin . Lab Invest . 1985;52:559-567. 12. Kurth BE, Hazen-Martin DJ, Sens MA, DeChamplain RW, Sens DA. Cell culture and characterization of human minor salivary gland duct cells . J Oral Pathol Med . 1989;18:214-219.Crossref 13. Iga H, Azuma M, Nagamine S, et al. Expression of neurofilaments in a neoplastic human salivary intercalated duct cell line or its derivatives and effect of nerve growth factor on the cellular proliferation and phenotype . Cancer . 1989; 49:6708-6719. 14. Keyomarski K, Sandoval L, Band V, Pardee AB. Synchronization of tumor and normal cells from GI to multiple cell cycles by lovastatin . Cancer Res . 1991; 51:3602-3609. 15. Tohyama T, Lee VMY, Rorke LB, Marvin M, McKay RDG, Trojanowski JQ. Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells . Lab Invest . 1992;66:303-313. 16. Chiu F-C, Barnes EA, Das K, et al. Characterization of a novel 66 kd subunit of mammalian neurofilaments . Neuron . 1989;2:1435-1445.Crossref 17. Hirano T, Gluckman J, de Vries E. The expression of alpha vascular smoothmuscle actin in salivary gland tumors . Arch Otolaryngol Head Neck Surg . 1990; 116:692-696.Crossref 18. Stemple DL, Anderson DJ. Isolation of a stem cell for neurons and glia from the mammalian neural crest . Cell . 1992;71:973-985.Crossref 19. Cepko C. Lineage analysis in the vertebrate nervous system by retrovirusmediated gene transfer . Methods Neurosci . 1989;1:367-392. 20. Durban E, Barreto P, Higers J, Sonnenberg A. Cell phenotypes and differentiative transitions in mouse submandibular salivary gland defined with monoclonal antibodies to mammary epithelial cells . J Histochem Cytochem . 1994; 42:185-196.Crossref 21. Hall PA, Watt FM. Stem cells: the generation and maintenance of cellular diversity . Development . 1989;106:619-633. 22. Dardick I. Myoepithelioma: definitions and diagnostic criteria . Ultrastruct Pathol . 1995;19:335-345.Crossref 23. LeDouarin NM, Smith J. Development of the peripheral nervous system from the neural crest . Annu Rev Cell Biol . 1988;4:375-404.Crossref 24. Bronner-Fraser M. Mechanisms of neural crest cell migration . Bioessays . 1993; 15:221-230.Crossref 25. Bronner-Fraser M. Neural crest cell formation and migration in the developing embryo . FASEB J . 1994;8:699-706. 26. Selleck MAJ, Scherson TY, Bronner-Fraser M. Dev Biol . 1993;159:1-11.Crossref 27. Gans C, Northcutt RG. Neural crest and the origin of vertebrates: a new head . Science . 1983;220:268-274.Crossref 28. Sellect MAJ, Bronner-Fraser M. Origins of the avian neural crest: the role of neural palate-epidermal interactions . Development . 1995;121:525-538. 29. Baroffio A, Dupin E, LeDouarin NM. Common precursors for neural or mesectodermal derivatives in the cephalic neural crest . Development . 1991;112: 301-305. 30. Trainor PA, Tan S-S, Tam PPL. Cranial paraxial mesoderm: regionalization of cell fate and impact on craniofacial development in mouse embryos . Development . 1994;120:2397-2408. 31. Couly GF, Coltey PM, LeDouarin NM. The developmental fate of the cephalic mesoderm in quail-chick chimeras . Development . 1992;114:1-15.

Journal

Archives of Otolaryngology - Head & Neck SurgeryAmerican Medical Association

Published: May 1, 1996

References

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