Inhibitory effects of activin on the growth and morphogenesis of primary and transformed mammary epithelial cells

Cancer Research

Volumn 56, Issue 5, 1996, Pages 1155-1163

  Liu, Qiu Yan ^a   Niranjan, Birunthi ^b   Gomes, Peter ^a   Gomm, Jennifer J ^a   Davies, Derek ^c   Coombes, R Charles ^a   Buluwela, Lakjaya ^a  

^a IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER GROWTH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; EPITHELIUM CELL; GROWTH INHIBITION; HUMAN; HUMAN CELL; MICROTUBULE ASSEMBLY; MORPHOGENESIS; MYOEPITHELIUM CELL; PRIORITY JOURNAL;

ACTIVINS; BASE SEQUENCE; BREAST; BREAST NEOPLASMS; CELL DIVISION; FEMALE; HUMANS; INHIBINS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; ORGAN CULTURE TECHNIQUES; TUMOR CELLS, CULTURED;

EID: 0012114501     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Roberts, A R., Flanders, K. C., Heine, U. I., Jakowlew, S., Komdaiah, P., Kim, S. J., and Sporn, M. B Transforming growth factor-β. multifunctional regulator of differentiation and development. Philos. Trans. R. Soc. Lond. B, 327: 145-154, 1990.
2. Gomm, J J., Smith, J. S , Ryall, G. K., Baillie, R , Turnbull, L , and Coombes, R. C. Localisation of basic fibroblast growth factor and transforming growth factor β1 in the human mammary gland. Cancer Res., 51: 4685-4692, 1991.
3. Robinson, S. D., Silberstein, G B , Roberts, A. B., Flanders, K. C., and Daniel, C. W. Regulated expression and growth inhibitory effects of transforming growth factor-β isoforms in mouse mammary gland development. Development (Camb.), 113: 867-878, 1991.
4. Daniel, C. W., Silverstein, G. B., Van Horn, K., Strickland, P., and Robinson, S. TGF-β1 induce inhibition of mouse mammary ductal growth: developmental specificity and characterisation. Dev. Biol., 135: 20-30, 1989.
5. Pierce, D. F , Jr., Johnson, M. D , Matsui, Y., Robinson, S. D , Gold, L. I., Purchio, A F , Daniel, C W., Hogan, B. L. M., and Moses, H. L. Inhibition of mammary duct development but not alveolar outgrowth during pregnancy in transgenic mice expressing active TGF-β1. Genes & Dev., 7: 2308-2317, 1993.
6. Knabbe, C., Lippman, M. E., Wakefield, L M., Flanders, K. C., Kasid, A., Derynck, R , and Dickson, R. B Evidence that transforming growth factor β is a hormonally regulated negative growth factor in human breast cells. Cell, 48: 417-428, 1987.
7. Kingsley, D M. The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes & Dev., 8: 133-146, 1994.
8. Mason, A. J., Hayflick, J. S., Ling, N., Esch, F., Ueno, N., Ying, S., Y., Guillemin, R., Niall, H., and Seeberg, P. H. Complementary DNA sequences of ovarian follicular fluid inhibin show precursor structure and homology with transforming growth factor-β Nature (Lond), 318: 659-663, 1985.
9. Vale, W., Rivier, J., Vaughan, J , MacClintock, R., Corrigan, A., Woo, W., Karr, D., and Speiss, J. Purification and characterisation of an FSH releasing protein from porcine ovarian follicular fluid Nature (Lond.), 231: 776-778, 1986.
10. Robertson, D. M , Foulds, L M , Leversha, L., Mogan, F J., Heara, M. T W , Burger, H. G., Wettenhall, R. E. H., and de Krester, D M. Isolation of inhibin from follicular fluid. Biochem. Biophys. Res. Commun., 133: 120-127, 1985.
11. Ying, S. Y. Inhibins, activins and follistatins: gonadal proteins modulating the secretion of follicle stimulating hormone Endocrinol. Rev., 9: 267-293, 1988.
12. Asashima, M , Nakano, H., Shimada, K., Kinoshita, K., Ismi, K., Shibai, H., and Ueno, N. Mesoderm induction in early amphibian embryos by activin A (erythroid differentiation factor). Roux's Arch. Dev. Biol., 198: 330-335, 1990.
13. Meunier, H. Rivier, C., Evans, R. M., and Vale, W Gonadal and extragonadal expression of inhibin α, βA and βB subunits in various tissues predicts diverse functions Proc. Natl. Acad. Sci. USA, 85: 247-251, 1988.
14. Tuuri, T., Eramaa, M., Hilden, K., and Ritvos, O. The tissue distribution of activin β A- and β B-subunit and follistatin messenger ribonucleic acids suggest multiple sites of action for the activin-follistatin system during human development. J. Clin Endocnnol. Metab., 78 1521-1524, 1994
15. Smith, J. C., Price, B. M. J., Van Nimmen, K., and Huylebroeck, D. Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature (Lond.), 345: 729-731, 1990.
16. van den Eynden-Van Raaij, A. J. M., van Zoelent, E. J. J., van Nimmen, K , Coster, C. H , Snoek, G. T., Durston, A. J., and Huylebroeck, D. Activin-like factor from Xenopus laevis cell line responsible for mesoderm induction. Nature (Lond.), 345: 732-734, 1990.
17. Green, J. B. A., and Smith, J C. Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature (Lond ), 347: 391-394, 1990.
18. Thomsen, G., Woolf, T , Whitman, M., Sokol, S., Vaughan, J , Vale, W., and Melton, D. A. Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell, 63: 485-493, 1990.
19. Sokol, S , and Melton, D A Preexistent pattern in Xenopus animal pole cells revealed by induction with activin. Nature (Lond.), 351: 409-411, 1991.
20. Matzuk, M. M., Kumar, T. J., Vassalli, A., Bickenbach, J. R., Roop, D. R , Jaenisch, R., and Bradley, A Functional analysis of activins during mammalian development. Nature (Lond ), 374: 354-360, 1995.
21. Schubert, D , Kimura, H., LaCorbiere, M., Vaughan, J , Karr, D., and Fischer, W H. Activin is a nerve cell survival molecule. Nature (Lond.), 344: 868-870, 1990.
22. Hashimoto, M., Kondo, S., Sakurai, T., Etoh, Y., Shibai, H., and Muramatsu, M Activin/EDF as an inhibitor of neural differentiation. Biochem Biophys. Res Commun., 173: 193-200, 1990.
23. Gonzalez-Manchon, C., and Vale, W. Activin A, inhibin and TGF-β modulate growth of two gonadal cell lines Endocrinology, 725: 1666-1672, 1989.
24. Kojima, I., and Ogata, E Dual effect of activin A on cell growth in BALB/c 3T3 cells. Biochem. Biophss. Res. Commun., 159: 1107-1113, 1989.
25. Kojima, I , Mogami, N , Kawamura, N., and Shibata, H. Activin A inhibits cell-cycle progression induced by insulin-like growth factor-I in BALB/c 3T3 cells. J. Endocrinol, 137: 99-105, 1993.
26. Yasuda, H., Mine, T., Shibata, H , Eto, Y., Hasegawa, Y., Takeuchi, T., Asano, S , and Kojima, I. Activin A: an autocrine inhibitor of initiation of DNA synthesis in rat hepatocytes. J. Clin. Invest , 92: 1491-1496, 1993.
27. Murata, M., Eto, Y., Shibai, H., Sakai, M., and Muramatsu, M Erythroid differentiation factor is encoded by the same mRNA as that of the inhibin βA chain. Proc. Natl. Acad. Sci USA, 85: 2434-2438, 1988.
28. Anisano, L., Wrana, J. L , Cheifetz, S., and Massagué, J. Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell, 68 97-108, 1992.
29. Nishimatsu, S., Oda, S , Marakami, K., and Ueno, N. Multiple genes for Xenopus activin receptor expressed during early embryogenesis. FEBS Lett., 303: 81-84, 1992.
30. Kondo, M., Tashiro, K , Fujii, G., Asano, M , Miyoshi, R., Yamada, R., Muramatsu, M., and Shiokawa, K. Activin receptor mRNA is expressed early in Xenopus embryogenesis and the level of the expression affects the body axis formation Biochem. Biophys Res. Commun., 181: 684-690, 1991.
31. Mathews, L S., and Vale, W. W. Expression cloning of an activin receptor: a predicted transmembrane serine kinase. Cell, 65: 973-982, 1991.
32. Lin, H Y., Wang, X., Ng-Eaton, E., Weinberg, R. A., and Lodish, H. F. Expression cloning of the TGF-β Type II receptor: a functional transmembrane serine/threonine kinase. Cell, 68: 775-785, 1992.
33. Ebner, R., Chen, R H., Shum, L , Lawler, S , Zioncheck, T. F., Lee, A., Lopez, A. R., and Derynck, R. Cloning of a type I TGF-β receptor and its effect on TGF-β binding to the type II receptor. Science (Washington DC), 260: 1344-1348, 1993.
34. Ten Dijke, P , Ichijo, H., Franzén, P., Schulz, P., Saras, J., Toyoshima, H., Heldin, C. H., and Miyazano, K. Activin receptor like kinases: a novel subclass of cell-surface receptors with predicted serine/threonine kinase activity. Oncogene, 8: 2879-2887, 1993.
35. Ten Dijke, P. J., Franzén, P., Yamashita, H , Ichijo, H., Heldin, C. H., and Miyazano, K. Serine/threonine kinase receptors Prog. Growth Factor Res., 5: 55-72, 1994.
36. Kordon, K. C., McKnight, R. A., Jhappan, C , Hennighausen, L , Merlino, G., and Smith, G. H. Ectopic TGF-β1 expression in the secretory mammary epithelium induces early senescence of the epithelial stem cell population. Dev. Biol , 168: 47-61, 1995.
37. Gomm, J. J., Browne, P. J., Coope, R. C , Liu, Q., Buluwela, L., and Coombes, R. C. The isolation of pure populations of epithelial and myoepithehal cells from the normal human mammary gland using immunomagnetic separation with Dynabeads Anal Biochem., 226: 91-99, 1995.
38. Soule, H. D., Maloney, T. M., Wolman, S. R., Peterson, W. D., Jr., Brenz, R., McGrath, C M., Russo, J., Pauley, R. J., Jones, R. F., and Brooks, S. C. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res., 50: 6075-6086, 1990.
39. Clarke, C., Titley, S., Davies, S., and O'Hare, M. J. An immunomagnetic separation method using superparamagnetic (MACS) beads for large-scale purification of human mammary luminal and myoepithelial cell. Epithelial Cell Biol., 3: 38-46, 1994.
40. Boehm, T., Buluwela, L , Williams, D., White, L , and Rabbins, T. H. A cluster of chromosome 11P 13 translocations found via distinct D-D and D-D-J rearrangements of the human T cell receptor δ chain gene. EMBO. J., 7: 2011-2017, 1988.
41. Luqmani, Y. A , Graham, M , and Coombes, R C. Expression of basic fibroblast growth factor, FGR1 and FGR2 in normal and malignant human breast and comparison with other normal tissues. Br J. Cancer, 65: 273-280, 1992.
42. Tanimoto, K., Handa, S., Ueno, N., Murakami, K., and Fukamizu, A. Structure and sequence analysis of the human activin β A subunit gene. DNA Seq., 2: 103-110, 1991.
43. Donaldson, C. J., Mathews, L. S., and Vale, W. W Molecular cloning and binding properties of the human type II activin receptor. Biochem. Biophys. Res. Commun., 184: 310-316, 1992.
44. D'Adamio, L., Shipp, M. A., Masteller, E. L., and Reinherz, E L. Organization of the gene encoding common acute lymphoblastic leukemia antigen (neutral endopeptidase 24.11): multiple miniexons and separate 5′ untranslated regions. Proc. Natl. Acad. Sci. USA, 86: 7103-7107, 1989.
45. Lancaster, C. A , Peat, N., Duhig, T., Wilson, D , Taylor-Papadimitriou, J., and Gendler, S J. Structure and expression of the human polymorphic epithelial mucin gene: an expressed VNTR unit. Biochem Biophys. Res Commun., 173: 1019-1029, 1990
46. Nakajima-Iijima, S., Hamada, H., Reddy, P , and Kakunaga, T. Molecular structure of the human cytoplasmic β-actin gene interspecies homology of sequences in the introns. Proc. Natl Acad Svi. USA, 82: 6133-6137, 1985.
47. Gusterson, B. A., Monaghan, P., Mahendran, R., Ellis, J., and O'Hare, M. J. Identification of myoepithehal cells in human and rat breasts by anti-common acute lymphoblastic leukemia antigen antibody A12. J. Natl Cancer Inst., 77: 343-349, 1986.
48. Roberts, A B , Anzano, M. A., Wakefield, L. M , Roche, N. S., Stern, D. F , and Sporn, M. B. Type β transforming growth factor: a bifunctional regulator of cellular growth. Proc Natl. Acad Sci. USA, 82: 119-123, 1985
49. Arrick, B. A., Korc, M., and Derynck, R. Differential regulation of expression of three transforming growth factor β species in human breast cancer cell lines by estradiol. Cancer Res., 50: 299-303, 1990.
50. Petersen, O W., and van Deurs, B Growth factor control of myoepithelial-cell differentiation in cultures of human mammary gland. Differentiation, 39: 197-215, 1988.
51. O'Hare, M. J , Omerod, M G., Monaghan, P., Lane, E. B , and Gusterson, B. A. Characterisation in vitro of luminal and myoepithelial cells isolated from the human mammary gland by cell sorting Differentiation, 46: 209-221, 1991.
52. Dundas, S R., Omerod, M G., Gusterson, B. A., and O'Hare, M. J. Characterisation of luminal and basal cells flow-sorted from the adult rat mammary parenchyma. J. Cell Sci., 100: 459-471, 1991.
53. Caron de Fromentel, C , Nardeux, P. C., Soussi, T., Lavialle, C , Estrade, S , Carloni, G, Chandrasekaran, K., and Cassingena, R. Epithelial HBL-100 cell line derived from milk of an apparently healthy woman harbours SV40 genetic information. Exp. Cell Res., 160: 83-94, 1985.
54. Luqmani, Y A , Smith, J., and Coombes, R. C Polymerase chain reaction-aided analysis of gene expression in frozen tissue sections. Anal Biochem., 200: 291-295, 1992.
55. Valverius, E. M., Walker-Jones, D., Bates, S. E., Stampfer, M. R., Clark, R , McCormick, F., Dickson, R. B., and Lippman, M E. Production of and responsiveness to transforming growth factor-β in normal and oncogene-transformed human mammary epithelial cells Cancer Res., 49: 6269-6274, 1989.
56. Massagué, J The TGF-β family of growth and differentiation factors. Cell, 49: 437-438, 1987.
57. Hosobuchi, M , and Stampfer, M. R. Effects of transforming growth factor β on growth of human mammary epithelial cells in culture. In Vitro Cell. Dev Biol. 25: 705-713, 1989
58. Polyak, K., Lee, M. H., Erdjument-Bromage, H., Koff, A., Roberts, J. M , Tempst, P., and Massagué, J. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell, 78: 59-66, 1994.
59. Toyoshima, H., and Hunter, T p27: a novel inhibitor of G1 cyclin-cdk protein kinase activity is related to p21. Cell, 78: 67-74, 1994
60. Kamb, A , Gruis, N. A., Wever-Feldhaus, J , Liu, Q., Harshman, K , Tavtigian, S V., Stocken, E , Day, R. S , III, Johnson, B. E., and Skolnick, M. H. A cell cycle regulator potentially involved in genesis of many tumour types. Science (Washington DC), 264: 436-440, 1994
61. INK4B is a potential effector of TGF-β-indueed cell cycle arrest. Nature (Lond.), 371: 257-261, 1994.
62. 1 cell cycle arrest. Genes & Dev., 9: 204-217, 1995.
63. 1 phase. J. Cell. Biochem., 50: 255-265, 1992.
64. Sakakura, T. Mammary embryogenesis In: M. C. Neville and C. W. Daniel (eds ), The Mammary Gland Development, Regulation and Function, pp. 37-66 New York: Plenum Publishing Corp., 1987.
65. Daniel, C W., and Silberstein, G. B. Postnatal development of rodent mammary gland. In. M. C. Neville and C. W. Daniel (eds.), The Mammary Gland Development, Regulation and Function, pp 3-36. New York: Plenum Publishing Corp , 1987
66. Vonderharr, B K Local effects of EGF, α-TGF and EGF-like growth factors on lobuloalveolar development of the mouse mammary gland in vivo J. Cell Physiol., 132: 581-584, 1987.
67. Topper, Y. J , and Freeman, C. S. Multiple hormone interactions in the developmental biology of the mammary gland. Physiol. Rev., 60: 1049-1106, 1980.
68. Coleman, S., Silberstein, G. B., and Daniel, C. W. Ductal morphogenesis in the mouse mammary gland: evidence supporting a role for epidermal growth factor Dev Biol., 127 304-315, 1988.
69. Niranjan, B., Buluwela, L , Yant, J., Perusinghe, N., Atherton, A , Phippard, D., Dale, T , Gusterson, B , and Kamalati, T HGF/SF: a potent cytokine for mammary growth, morphogenesis and development. Development (Camb.), 121: 2897-2908, 1995.