Skip to main content
SpringerLink
Log in

Establishment and characterization of a novel human myoepithelial cell line and matrix-producing xenograft from a parotid basal cell adenocarcinoma

  • Cellular Models
  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Summary

Myoepithelial cells exert important paracrine effects on epithelial morphogenesis and mitogenesis through direct cell-cell interactions and through synthesis of a basement membrane extracellular matrix. To study these effects further, this study established the first immortalized human myoepithelial cell line, HMS-1, and transplantable xenograft, HMS-X, from the rare parotid basal cell adenocarcinoma. The cell line exhibited a fully differentiated myoepithelial phenotype and the xenograft exhibited the rare property of accumulating an abundant extracellular matrix composed of both basement membrane and nonbasement membrane components with the latter predominating. With HMS-1 as a feeder layer, dramatic and specific induction of epithelial morphogenesis (sheroid formation) occurred with selected normal epithelial and primary carcinoma target cells. HMS-1 and HMS-X provide distinct advantages over the conventional murine matrices in existence. They will be invaluable in future studies of human tumor-myoepithelial and matrix interactions important for tumor cell growth, invasion, and metastasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Azuma, M.; Hayashi, Y.; Yoshida, H., et al. Emergence of differentiated subclones from a human salivary adenocarcinoma cell clone in culture after treatment with sodium butyrate. Cancer Res. 46:770–777; 1986.

    PubMed  CAS  Google Scholar 

  2. Azuma, M.; Kawamata, H.; Kasai, Y., et al. Effects of retinoic acid on morphological features and biological markers of a neoplastic human salivary intercalated duct cell line in culture. Cancer Res. 48:7219–7225; 1988.

    PubMed  CAS  Google Scholar 

  3. Azuma, M.; Sato, M. Morphogenesis of normal human salivary gland cellsin vitro. Histol. Histopathol. 9:781–790; 1994.

    PubMed  CAS  Google Scholar 

  4. Azuma, M.; Tamatani, T.; Kasai, Y., et al. Immoralization of normal human salivary gland cells with duct-, myoepithelial-, acinar-, or squamous phenotype by transfection with SV40 Ori mutant deoxyribonucleic acid. Lab. Invest. 69:24–42; 1993.

    PubMed  CAS  Google Scholar 

  5. Baldwin, C. T.; Reginato, A. M.; Smith, C., et al. Structure of cDNA clones coding for human type II procollagen: the α(II) chain is more similar to the α1(I) chain than two other fibrillar collagens. Biochem. J. 262:521–528; 1989.

    PubMed  CAS  Google Scholar 

  6. Bao, L.; Matsumura, Y.; Baban, D., et al. Effects of inoculation site and Matrigel on growth and metastasis of human breast cancer cells. Br. J. Cancer 70:228–232; 1994.

    PubMed  CAS  Google Scholar 

  7. Barsky, S. H.; Layfield, L.; Varki, N., et al. Two human tumors with high basement membrane-producing potential. Cancer 61:1798–1806; 1988.

    Article  PubMed  CAS  Google Scholar 

  8. Caselitz, J.; Schmitt, P.; Seifert, G., et al. Basal membrane associated substances in human salivary glands and salivary gland tumors. Pathol. Res. Pract. 183:386–394; 1988.

    PubMed  CAS  Google Scholar 

  9. Chaudhry, A. P.; Leifert, C.; Cutler, L. S., et al. Histogenesis of adenoid cystic carcinoma of the salivary glands: light and electron microscopic study. Cancer 58:72–82; 1986.

    Article  PubMed  CAS  Google Scholar 

  10. Cheng, J.; Saku, T.; Okabe, H., et al. Basement membranes in adenoidcystic carcinoma: an immunohistochemical study. Cancer 69:2631–2640. 1992.

    Article  PubMed  CAS  Google Scholar 

  11. Dickson, S. R.; Warburton, M. J. Enhanced synthesis of gelatinase and stromelysin by myoepithelial cells during involution of the rat mammary gland. J. Histochem. Cytochem. 40:697–703; 1992.

    PubMed  CAS  Google Scholar 

  12. Ellis, G. L.; Wiscovitch, J. G. Basal cell adenocarcinomas of the major salivary glands. Oral Surg. Oral Med. Oral Pathol. 69:461–469; 1990.

    Article  PubMed  CAS  Google Scholar 

  13. Emerman, J. T.; Vogl, A. W. Cell size and shape changes in the myoepithelium of the mammary gland during differentiation. Anat. Rec. 216:405–415; 1986.

    Article  PubMed  CAS  Google Scholar 

  14. Fridman, R.; Giaccione, G.; Kanemoto, T., et al. Reconstituted basement membrane (Matrigel) and laminin can enhance the tumorigenicity and the drug persistence of small cell lung cancer cell lines. Proc. Natl. Acad. Sci. USA 87:6698–6702; 1990.

    Article  PubMed  CAS  Google Scholar 

  15. Fridman, R.; Kibbey, M. C.; Royce, L. S., et al. Enhanced tumor growth of both primary and established human and murine tumor cells in athymic mice after coinjection with matrigel. J. Natl. Cancer. Inst. 83:769–774; 1991.

    Article  PubMed  CAS  Google Scholar 

  16. Gallimore, A. P.; Spraggs, P. D. R.; Allen, J. P., et al. Basaloid carcinomas of salivary glands. Histopathology 24:139–144; 1994.

    Article  PubMed  CAS  Google Scholar 

  17. Gallo, O.; Bani, D.; Toccafondi, G., et al. Characterization of novel cell line from pleomorphic adenoma of the parotid gland with myoepithelial phenotype and producing interleukin-6 as an autocrine growth factor. Cancer 70:559–568; 1992.

    Article  PubMed  CAS  Google Scholar 

  18. Giard, D. J.; Aaronson, S. A.; Todaro, G. J., et al. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J. Natl. Cancer Inst. 51:1417–1423; 1973.

    PubMed  CAS  Google Scholar 

  19. Guelstein, V. I.; Tchypsheva, T. A.; Ermilova, V. D., et al. Myoepithelial and basement membrane antigens in benign and malignant human breast tumors. Int. J. Cancer 53:269–277; 1993.

    Article  PubMed  CAS  Google Scholar 

  20. Hayashi, Y.; Yoshida, H.; Nagamine, S., et al. Induction of cells with acinar cell phenotype including presence of intracellular amylase: treatment with 12-O-tetradecanoyl-phorbol-13-acwtate in a neoplastic human salivary intercalated duct cell line grown in athymic nude mice. Cancer 60:1000–1008; 1987.

    Article  PubMed  CAS  Google Scholar 

  21. Hayat, M. A. Principles and techniques of electron microscopy: biological applications, 3rd ed. Boca Raton, FL: CRC Press; 1989:137.

    Google Scholar 

  22. Hedley, D. W.; Friedlander, M. L.; Taylor, I. W., et al. Method for analysis of cellular DNA content in paraffin-embedded pathological material using flow cytometry. J. Histochem. Cytochem. 31:1333–1335; 1983.

    PubMed  CAS  Google Scholar 

  23. Jeffreys, A. J.; Wilson, V.; Thein, S. L., et al. Hypervariable “minisatellite” regions in human DNA. Nature 314:67–73; 1985.

    Article  PubMed  CAS  Google Scholar 

  24. Kibbey, M. C.; Grant, D. S.; Kleinman, H. K. Role of the SIKVAV site of laminin in promotion of angiogenesis and tumor growth: an in vivo matrigel model. J. Natl. Cancer Inst. 84:1633–1638; 1992.

    Article  PubMed  CAS  Google Scholar 

  25. Kibbey, M. C.; Royce, L. S.; Dym, M., et al. Glandular-like morphogenesis of the human submandibular tumor cell line A253 on basement membrane components. Exp. Cell Res. 198:343–351; 1992.

    Article  PubMed  CAS  Google Scholar 

  26. Kleinman, H. K.; McGarvey, M. L.; Hassell, J. R., et al. Basement membrane complexes with biological activity. Biochemistry 25:312–318; 1986.

    Article  PubMed  CAS  Google Scholar 

  27. Kleinman, H. K.; McGarvey, M. L.; Liotta, L. A., et al. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21:6188–6193; 1982.

    Article  PubMed  CAS  Google Scholar 

  28. Kondo, T.; Muragishi, H.; Imaizumi, M. A cell line from human salivary gland mixed tumor. Cancer 27:403–410; 1971.

    Article  PubMed  CAS  Google Scholar 

  29. Laemmli, U. K. Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680–685; 1970.

    Article  PubMed  CAS  Google Scholar 

  30. Liotta, L. A.; Rao, C. N.; Barsky, S. H. Tumor invasion and the extracellular matrix. Lab. Invest. 49:636–649; 1983.

    PubMed  CAS  Google Scholar 

  31. Mann, K.; Deutzmann, R.; Paulsson, M., et al. Solubilization of a protein BM-40 from a basement membrane tumor with chelating agents and evidence for its identity with osteonectin and SPARC. FEBS Lett. 218:167–172; 1987.

    Article  PubMed  CAS  Google Scholar 

  32. Martinez-Hernandez, A.; Amenta, P. S. The basement membrane in pathology. Lab. Invest. 48:656–677; 1983.

    PubMed  CAS  Google Scholar 

  33. Murdoch, A. D.; Dodge, G. R.; Cohen, I., et al. Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/perlecan). J. Biol. Chem. 267:8544–8557; 1992.

    PubMed  CAS  Google Scholar 

  34. Nakamura, Y.; Leppert, M.; O'Connell, P., et al. Variable number of tandem repeat (VNTR) markers for human gene mapping. Science 235:1616–1622; 1987.

    Article  PubMed  CAS  Google Scholar 

  35. Nakanishi, K.; Kawai, T.; Suzuki, M., et al. Glycosaminoglycans in pleomorphic adenoma and adenoid cystic carcinoma of the salivary gland. Arch. Pathol. Lab. Med. 114:1227–1231; 1990.

    PubMed  CAS  Google Scholar 

  36. Nara, Y.; Takeuchi, J.; Yoshida, K., et al. Immunohistochemical characterization of extracellular matrix components of salivary gland tumors. Br. J. Cancer 64:307–314; 1991.

    PubMed  CAS  Google Scholar 

  37. Noel, A. C.; Calle, A.; Emonard, H. P., et al. Invasion of reconstituted basement membrane matrix is not correlated to the malignant metastatic phenotype. Cancer Res. 51:405–415; 1991.

    PubMed  CAS  Google Scholar 

  38. Ormos, J.; Halasz, A. Electron microscopic study of adenoid cystic carcinoma. Ultrastruct Pathol. 15:149–157; 1991.

    PubMed  CAS  Google Scholar 

  39. Pan, T. C.; Kluge, M.; Zhang, R. Z., et al. Sequence of extracellular mouse protein BM-90/fibulin and its calcium-dependent binding to other basement-membrane ligands. Eur. J. Biochem. 215:733–740; 1993.

    Article  PubMed  CAS  Google Scholar 

  40. Passaniti, A.; Isaacs, J. T.; Haney, J. A., et al. Stimulation of human prostatic carcinoma tumor growth in athymic mice and control of migration in culture by extracellular matrix. Int. J. Cancer 51:318–324; 1992.

    Article  PubMed  CAS  Google Scholar 

  41. Robinson, L. K.; Murrah, V. A.; Moyer, M. P., et al. Characterization of a novel glycoprotein isolated from the basement membrane matrix of the Engelbreth-Holm-Swarm tumor. J. Biol. Chem. 264:5141–5147; 1989.

    PubMed  CAS  Google Scholar 

  42. Royce, L. S.; Kibbey, M. C.; Mertz, P., et al. Human neoplastic submandibular intercalated duct cells express an acinar phenotype when cultured on a basement membrane matrix. Differentiation 52:247–255; 1993.

    Article  PubMed  CAS  Google Scholar 

  43. Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989.

    Google Scholar 

  44. Sato, M.; Azuma, M.; Hayashi, Y., et al. 5-Azacytidine induction of stable myoepithelial and acinar cells from a human salivary intercalated duct cell clone. Cancer Res. 47:4453–4459; 1987.

    PubMed  CAS  Google Scholar 

  45. Shirasuna, K.; Morioka, S.; Watatani, K., et al. Growth inhibition and differentiation of human salivary adenocarcinoma cells by medium conditioned with normal human fibroblasts. Cancer Res. 48:2819–284; 1988.

    PubMed  CAS  Google Scholar 

  46. Shirasuna, K.; Sato, M.; Miyazaki, T. A myoepithelial cell line established from a human pleomorphic adenoma arising in minor salivary gland. Cancer 45:297–305; 1980.

    Article  PubMed  CAS  Google Scholar 

  47. Shirasuna, K.; Sato, M.; Miyazaki, T. A neoplastic epithelial duct cell line established from an irradiated human salivary gland. Cancer 48:745–752; 1981.

    Article  PubMed  CAS  Google Scholar 

  48. Shirasuna, K.; Watatani, K.; Furusawa, H., et al. Biological characterization of pseudocyst-forming cell lines from human adenoid cystic carcinomas of minor salivary gland origin. Cancer Res. 50:4139–4145; 1990.

    PubMed  CAS  Google Scholar 

  49. Shirasuna, K.; Watanani, K.; Sugiyama, M., et al. Isolation and characterization of different clones including myoepithelial-like variants from a clonal neoplastic epithelial duct cell line of human salivary gland origin. Cancer Res. 46; 1418–1426; 1986.

    PubMed  CAS  Google Scholar 

  50. Skalova, A.; Leivo, I. Basement membrane proteins in salivary gland tumours: distribution of type IV collagen and laminin. Virchows Archiv. A Pathol. Anat. Histopathol. 420:425–431; 1992.

    Article  CAS  Google Scholar 

  51. Sobue, M.; Takeuchi, J.; Niwa, M., et al. Establishment of a cell line producing basement membrane components from an adenoid cystic carcinoma of the human salivary gland. Virchows Archiv. B Cell. Pathol. 57:203–208; 1989.

    Article  CAS  Google Scholar 

  52. Soini, Y.; Autio-Harmainen, H. Synthesis and degradation of basement membranes in benign and malignant salivary gland tumors. A study byin situ hybridization. J. Pathol. 170:291–296; 1993.

    Article  PubMed  CAS  Google Scholar 

  53. Toth, J.; Sugar, J.; Csuka, O. The role of myoepithelial cells in the morphogenesis of induced mammary tumors. Virchows Arch. A Pathol. Anat. Histol. 385:41–48; 1979.

    Article  PubMed  CAS  Google Scholar 

  54. Tsubura, A.; Shikata, N.; Inui, T., et al. Immunohistochemical localization of myoepithelial cells and basement membrane in normal, benign and malignant human breast lesions. Virchows Arch. A Pathol. Anat. Histopathol. 413:133–139; 1988.

    Article  PubMed  CAS  Google Scholar 

  55. Vukicevic, S.; Kleinman, H. K.; Luyten, F. P., et al. Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp. Cell Res. 202:1–8; 1992.

    Article  PubMed  CAS  Google Scholar 

  56. Witsell, D. L.; Weissler, M. C.; Livanos, E., et al. Unique chromosomal rearrangement and mucin production in a novel salivary myoepithelial cell strain. Arch. Otolaryngol. Head Neck Surg. 119:1151–1157; 1993.

    PubMed  CAS  Google Scholar 

  57. Yoshida, H.; Azuma, M.; Yanagawa, T., et al. Effect of dibutyryl cyclic AMP on morphologic features and biologic markers of a human salivary gland adenocarcinoma cell line in culture. Cancer 57:1011–1018; 1986.

    Article  PubMed  CAS  Google Scholar 

  58. Yoshida, M.; Uchibori, N.; Sato, E., et al. A cell line from a human salivary gland carcinoma. Br. J. Cancer 41:636–639; 1980.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pathology, UCLA School of Medicine, 10833 Le Conte Avenue, 90024-1732, Los Angeles, California

    Mark D. Sternlicht, Suzi Safarians & Sanford H. Barsky

  2. Department of Surgery, Head and Neck Division, UCLA School of Medicine, 10833 Le Conte Avenue, 90024-1732, Los Angeles, California

    Thomas C. Calcaterra

Authors
  1. Mark D. Sternlicht
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Suzi Safarians
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas C. Calcaterra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sanford H. Barsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sternlicht, M.D., Safarians, S., Calcaterra, T.C. et al. Establishment and characterization of a novel human myoepithelial cell line and matrix-producing xenograft from a parotid basal cell adenocarcinoma. In Vitro Cell.Dev.Biol.-Animal 32, 550–563 (1996). https://doi.org/10.1007/BF02722982

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02722982

Key words

Search

Navigation