Isolation and Characterization of a Spontaneously Immortalized Human Breast Epithelial Cell Line, MCF-10

Cancer Research

Volumn 50, Issue 18, 1990, Pages 6075-6086

  Soule, Herbert D ^a   Maloney, Terry M ^a   Wolman, Sandra R ^a   Brenz, Richard ^a   Russo, Jose ^a   Pauley, Robert J ^a   Jones, Richard F ^a   Brooks, S C ^a   McGrath, Charles M ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BREAST CELL; CELL CULTURE; CELL LINE; CULTURE MEDIUM; CYTOCHEMISTRY; FEMALE; HISTOLOGY; HUMAN; HUMAN CELL; KARYOTYPING; PRIORITY JOURNAL;

ANIMAL; BREAST NEOPLASMS; CELL COUNT; CHROMOSOME ABERRATIONS; FEMALE; GENOTYPE; HUMAN; MICE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENES; RECEPTOR, ERBB-2; SIMIAN VIRUS 40; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.; TUMOR CELLS, CULTURED;

EID: 0025129726     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Stampfer, M. R., Hallowes, R.C., and Hackett, A. J. Growth of normal human mammary cells in culture. In Vitro (Rockville), 16:415–425, 1980.
2. Hammond, S. L., Ham, R. G., and Stampfer, M. R. Serum-free growth of human mammary epithelial cells: rapid clonal growth in defined medium and extended serial passage with pituitary extract. Proc. Natl. Acad. Sci. USA, 81: 5435–5439, 1984.
3. Soule, H. D., and McGrath, C. A simplified method for passage and long-term growth of human mammary cells. In Vitro Cell. Dev. Biol., 22: 6–12, 1986.
4. Hackett, A. J., Smith, H. S., Springer, E. L., Owens, R. B., Nelson Rees, N. A., Riggs, J. L., and Gardner, M. B. Two syngeneic cell lines from human breast tissue: the aneuploid mammary epithelial (Hs 578T) and the diploid myoepithelial (Hs 578Bst) cell lines. J. Natl. Cancer Inst., 58: 1795–1806, 1977.
5. Briand, P., Petersen, O. W., and van Deurs, B. A new diploid nontumorigenic human breast epithelial cell line isolated and propagated in chemically defined medium. In Vitro Cell. Dev. Biol., 23:181–188, 1987.
6. Gaflhey, E. V. A cell line (HBL-100) established from breast milk. Cell Tissue Res., 227: 563–568, 1982.
7. Chang, S. E., Keen, J., Lane, E. B., and Taylor-Papadimitriou, J. Establishment and characterization of SV40-transformed human breast epithelial cell lines. Cancer Res., 42: 2040–2053, 1982.
8. Caron de Fromentel,C., Nardeux, P.C., Soressi, T., Lavialle,C., Estrade, S., Carloni, G., Chandrasekaran, K., and Carsingena, R. Epithelial HBL-100 cell line derived from milk of an apparently healthy woman harbors SV40 genetic information. Exp. Cell Res., 16:83–94, 1985.
9. Stampfer, M. R., and Bartley, J. C. Induction of transformation and continuous cell lines from normal human mammary epithelial cells after exposure to benzo(fl]pyrene. Prcc. Natl. Acad. Sci. USA, 82: 2394–2398, 1984.
10. Band, V., and Sager, R. Distinctive traits of normal and tumor-derived human mammary epithelial cell expressed in a medium that supports long-term growth of both cell types. Proc. Natl. Acad. Sci. USA, 86: 1249–1253, 1989.
11. Band, V., Zajclowski, D., Kulesa, V., and Sager, R. Human papilloma virus DNAs immortalize normal human mammary epithelial cells and reduce their growth factor requirements. Proc. Natl. Acad. Sci. USA, 87:463–467, 1990.
12. Hennings, H., Michael, D., Cheng,C., Steinert, P., Holbrook, K., and Yuspa, S. H. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell, 19:245–254, 1980.
13. Lechner, J., Haugen, A., Autrup, H., McClendon, I., Trump, B., and Harris, C. Clonal growth of epithelial cells from normal human bronchus. Cancer Res., 2294–2304, 1981.
14. Stoner, G., and Babcock, M. Influence of growth factors on proliferation of normal and chemically transformed rat esophageal epithelial cells. Proc. Am. Assoc. Cancer Res., 23:42, 1982.
15. McGrath, C. M., and Soule, H. D. Calcium regulation of normal human mammary epithelial cell growth in culture. In Vitro Cell Dev. Biol., 20:652–662, 1984.
16. Soule, H. D., Maloney, T., and Brenz, R. Characterization of long-term growth of normal human mammary epithelial (NHME) cells. Proc. Am. Assoc. Cancer Res., 28: 30, 1987.
17. Ottenbreit, M. J., Halton, D. M., and Peterson, W. D. Jr. Rapid isoenzyme analysis of cell cultures by agarose electrophoresis. II. Intraspecies identification. J. Tissue Culture Methods, 6:107–110, 1982.
18. Seabright, M. A rapid banding technique for human chromosomes. Lancet, 2:971–972, 1971.
19. Wolman, S. R., Smith, H. S., Stampfer, M., and Hackett, A. J. Growth of diploid cells from breast cancers. Cancer Genet. Cytogenet., 16:49–64, 1985.
20. Pauley, R. J., Parks, W. P., and Popko, B. J. Expression and demethylation of germinally-transmitted BALB/c mouse mammary tumor virus DNA in Abelson MuLV B-lymphoid cell lines. Virus Res., 1: 381–400, 1984.
21. Feinberg, A. P., and Vogelstein, B. A technique for radiolabelling DNA restriction fragments to a high specific activity. Anal. Biochem., 132: 6–13, 1983.
22. Vassart, G., Georges, M., Monsieur, R., Brocas, H., Lequarre, A. S., and Christophe, D. A sequence in M13 phage detects hypervariable minisatellites in human and animal DNA. Science (Washington DC), 235:683–684, 1987.
23. Gendler, S. J., Burchell, J. M., Duhig, T., Lamport, D., White, R., Parker, M., and Taylor-Papadimitriou, J. Cloning of partial cDNA encoding differentiation and tumor-associated mucin glycoproteins expressed by human mammary epithelium. Proc. Natl. Acad. Sci. USA, 84:6060–6064, 1987.
24. Yamamoto, T., Ikawa, S., Akiyama, T., Semba, K., Nomura, N., Miyajima, N., Saito, T., and Toyoshima, K. Similarity of protein encoded by the human c-erbB-2 gene to epidermal growth factor receptor. Nature (Lond.), 319:230–234, 1986.
25. Casey, G., Smith, R., McGiliivray, D., Peters, G., and Dickson, C. Characterization and chromosome assignment of the human homolog of i/if-2, a potential proto-oncogene. Mol. Cell. Biol., 6: 502–510, 1986.
26. Jansson, M., Philipson, L., and Vennstrom, B. Isolation and characterization of multiple human genes homologous to the oncogenes of avian erythroblastosis virus. EMBO J., 2: 561–565, 1983.
27. van't Veer, L. J., van Kessel, A. G., van Heerikhuizen, H., van Ooyen, A., and Nusse, R. Molecular cloning and chromosomal assignment of the human homolog of int-U a mouse gene implicated in mammary tumorigenesis. Mol. Cell. Biol., 4: 2532–2534, 1984.
28. Fujita, J., Srivastava, S. K., Kraus, M. H., Rhins, J. S., and Aaronson, S. A. Frequency of molecular alterations affecting ras proto-oncogenes in human urinary tract tumors. Proc. Natl. Acad. Sci. USA, 82: 3849–3853, 1985.
29. Saiki, R. K., Gelfand, D. H., StofTel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B., and Erlich, H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science (Washington DC), 259:487–491, 1988.
30. Capon, D. J., Chen, E. Y., Levinson, A. D., Seeburg, P. H., and Goeddel, D. V. Complete nucleotide sequences of the T24 human bladder carcinoma oncogene and its normal homologue. Nature (Lond.), 302:33–37, 1983.
31. Sanger, F., Nicklen, S., and Coulson, A. R. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA, 74: 5463–5467, 1977.
32. Bachmann, B., Luke, W., and Hunsmann, G. Improvement of PCR amplified DNA sequencing with the aid of detergents. Nucleic Acids Res., 18: 1309, 1990.
33. Harlow, E., Crawford, L. V., Prim, D.C., and Williamson, N. M. Monoclonal antibodies specific for simian virus 40 tumor antigens. J. Virol., 39: 861–869, 1981.
34. Stoker, M., O'Neill, G., Benyman, S., and Waxman, V. Anchorage growth regulation in normal and virus-transformed cells. Int. J. Cancer, 3:683–693, 1968.
35. Soule, H. D., Maloney, T., and McGrath, C. M. Phenotypic variance among cells isolated from spontaneous mouse mammary tumors in primary suspension culture. Cancer Res., 41: 1154–1167, 1981.
36. Dexter, D. L., Kowalski, H. M., Blazor, B. A., Fligiel, Z., Vogel, R., and Heppner, G. H. Heterogeneity of tumor cells from a single mouse mammary tumor. Cancer Res., 38: 3174–3181, 1978.
37. Michalopoulos, G., and Pitot, H. C. Primary culture of parenchymal liver cells on collagen membranes. Exp. Cell Res., 94: 70–78, 1975.
38. Yang, J., Richards, J., Bowman, P., Guzman, R., Enami, J., McCormick, K., Hamanoto, S., Pitelka, D., and Nandi, S. Sustained growth and three-dimensional organization of primary mammary tumor epithelial cells embedded in collagen gels. Proc. Natl. Acad. Sci. USA, 76: 3401–3405, 1979.
39. Peters, L. J., and Hewitt, H. B. The influence of fibrin formation on the transplantability of murine tumor cells: implications for the mechanisms of the R'evesz effect. Br. J. Cancer, 29: 279–291, 1974.
40. Dupressoir, T., Vanacker, J. M., Cornel is, J. J., Duponchel, N., and Rom-nelaere, J. Inhibition by parvovirus H-l of the formation of tumors in nude mice and colonies in vitro by transformed human mammary epithelial cells. Cancer Res., 49: 3203–3208, 1989.
41. Yang, J., Balakrishnan, A., Hamamoto, S., Elias, J. J., Rosenau, W., Beattie, C. W., Das Gupta, T. K., Wellings, S. R., and Nandi, S. Human breast epithelial cells in serum-free collagen gel primary culture: growth, morphological, and immunocytochemical analysis. J. Cell. Physiol., 133: 228–234, 1987.
42. An International System for Human Cytogenetic Nomenclature. Basel: S. KargerAG, 1985.
43. Jeffreys, A. J., Wilson, V., and Thein, S. L. Hypervariable minisatellite regions in human DNA. Nature (Lond.), 314:67–73, 1985.
44. Swallow, D. M., Gendler, S., Griffiths, B., Corney, G., Taylor-Papadimitriou, J., and Bramwell, M. E. The human tumour-associated epithelial mucins are coded by an expressed hypervariable gene locus PUM. Nature (Lond.), 328: 82–84, 1987.
45. van de Vijver, M., van de Bersselaar, R., Devilee, P., Cornelisse,C., Peterse, J., and Nusse, R. Amplification of the neu (c-erbB-2) oncogene in human mammary tumors is relatively frequent and is often accompanied by amplification of the linked c-erbA oncogene. Mol. Cell. Biol., 7: 2019–2023, 1987.
46. Lidereau, R., Callahan, R., Dickson,C., Peters, G., Escot,C., and Ali, I. U. Amplification of the int-2 gene in primary human breast tumors. Oncogene Res., 2: 285–291, 1988.
47. Krantiris, T. G., DiMartino, N. A., Colb, M., and Parkinson, D. R. Unique allelic restriction fragments of the Ha-ras locus in leukocyte and tumour DNAs of cancer patients. Nature (Lond.), 313:369–374, 1985.
48. Jensen, F., Koprowski, H., Pagano, J. S., Ponten, J., and Ravdin, R. G. Autologus and homologous implantation of human cells transformed by simian virus 40. J. Natl. Cancer Inst., 32: 917–937, 1964.
49. Hayflick, L., and Moor head, P. S. The cultivation of human diploid cell strains. Exp. Cell Res., 25: 585–621, 1961.
50. Ponten, T. P., and Westermark, B. Cell generation and aging of nontrans-formed glia cells from adult humans. In: S. Fedoroff and L. Hertz (eds.), Advances in Cellular Neurobiology, Vol. 1, pp. 209–227. New York: Academic Press, 1980.
51. Baden, H. P., Kubilus, J., Kvedar, J.C., Steinberg, M. L., and Wolman, S. R. Isolation and characterization of a spontaneously arising long-lived line of human keratinocytes (MM 1). In Vitro Cell. Dev. Biol., 23:205–213, 1987.
52. Woodworth, C. D., Bowden, P. E., Doniger, J., Pirisi, L., Barnes, W., Lancaster, W. D., and DiPaolo, J. A. Characterization of normal human cervical cells immortalized in vitro by papillomavirus types 16 and 18 DNA. Cancer Res., 48:4620–4628, 1988.
53. Rudland, P. S., Hallowes, R.C., Cox, S. A., Ormerod, E. J., and Wasburton, M. J. Loss of production of myoepithelial cells and basement membrane proteins but retention of response to certain growth factors and hormones by a new malignant human breast cancer cell strain. Cancer Res., 45: 3864–3877, 1985.
54. Smith, H. S., Wolman, S. R., Dairkee, S. H., Hancock, M.C., Lippman, M., Leff, A., and Hackett, A. J. Immortalization in culture: occurrence at a late stage in the progression of breast cancer. J. Natl. Cancer Inst., 78:611–615, 1987.
55. San ford, K. K., Handieman, S. L., and Jones, G. M. Morphology and serum dependence of cloned cell lines undergoing spontaneous malignant transformation in culture. Cancer Res., 37:821–830, 1977.
56. Sporn, M. B., and Roberts, A. B. Autocrine growth factors and cancer. Nature (Lond.), 313: 745–747, 1985.
57. Lang, W. E., Tokes, Z. A., Benedict, W. F., and Sargente, N. Anchorage independent growth and plasminogen activator production by bovine endothelial cells. J. Cell. Biol., 84: 281–293, 1980.
58. Soule, H. D., and McGrath, C. M. Estrogen responsive proliferation of clonal human breast carcinoma cells in athymic mice. Cancer Lett., 10: 177–189, 1980.
59. Shafie, S. M., and Giartham, F. H. Role of hormones in the growth and regression of human breast cancer cells (MCF-7) transplanted into athymic mice. J. Natl. Cancer Inst., 67: 51–56, 1981.
60. Kraus, M. H., Yuasa, Y., and Aaronson, S. A. A position 12-activated H-ras oncogene in all HS578T mammary carcinosarcoma cells but not normal mammary cells of the same patient. Proc. Natl. Acad. Sci. USA, 81: 5384–5388, 1984.
61. Sukumar, S., Carney, W. P., and Barbacid, M. Independent molecular pathways in initiation and loss of hormone responsiveness of breast carcinomas. Science (Washington DC), 240: 524–526, 1988.
62. Yuspa, S. H., Kilkenny, A. E., Stanley, J., and Lichti, U. Harvey and Kirsten sarcoma viruses block keratinocytes in an early, phorbol ester responsive stage of terminal differentiation. Nature (Lond.), 314:459–467, 1985.
63. Brown, K., Quintanilla, M., Ramsden, M., Kerr, I. B., and Blamain, A. \-ras genes from Harvey and Balb murine sarcoma viruses can act as initiators of two-stage mouse skin carcinogenesis. Cell, 46:447–456, 1986.
64. Sinn, E., Muller, W., Pattengale, P., Tepler, I., Wallace, R., and Leder,P. Coexpression of MMTVN-Ha-ros and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo. Cell, 49:465–475, 1987.
65. Zarbl, H., Sukumar, S., Arthur, A. V., Martin-Zanca, D., and Barbacid, M. Direct mutagenesis of Ha-ras-1 oncogenes by JV-nitroso-AT-methylurea. Nature (Lond.), 315: 382–385, 1985.
66. Barbacid, M. ras genes. Annu. Rev. Biochem., 56: 779–827, 1987.
67. Rochlitz, C. F., Scott, G. K., Dodson, J. M., Liu, E., Dollbaum,C., Smith, H. S., and Benz, C. C. Incidence of activating ras oncogene mutations associated with primary and metastatic human breast cancer. Cancer Res., 49:357–360, 1989.
68. Yang, J., Elias, J. J., Petrolis, L., Wellings, S. R., and Nandi, S. Effects of hormones and growth factors on human mammary epithelial cells in collagen gel cultures. Cancer Res., 41: 1021–1027, 1981.
69. Balakrishnan, A., Cramer, S., Bandyopadhyay, G. K., Imagawa, W., Yang, J., Elias, J., Beattie, C. W., Das Gupta, T. K., and Nandi, S. Differential proliferative response to linoleate in cultures of epithelial cells from normal human breast and fibroadenomas. Cancer Res., 49:857–862, 1989.
70. Rudland, P. S. Stem cells and the development of mammary cancers in experimental rats and in humans. Cancer Metastasis Rev., 6: 55–83, 1987.
71. Cowell, J. K. Double minutes and homogeneously staining regions: gene amplification in mammalian cells. Annu. Rev. Genet., 16:21–59, 1982.