Dynamic expression and activation of ERBB receptors in the developing mouse mammary gland

Cell Growth and Differentiation

Volumn 9, Issue 6, 1998, Pages 451-464

  Schroeder, Joyce A ^a   Lee, David C ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; CELL DIFFERENTIATION; CELL GROWTH; CELL TYPE; DRUG RECEPTOR BINDING; ENZYME ACTIVITY; INVOLUTION; LIGAND BINDING; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

EID: 0031868432     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Lemmon, M. A., and Schlessinger, J. Regulation of signal transduction and signal diversity by receptor oligomerization. Trends Biochem. Sci., 19: 459-463, 1994.
2. erbB3 possesses an impaired tyrosine kinase activity. Proc. Natl. Acad. Sci. USA, 91: 8132-8136, 1994.
3. Toyoda, H., Komurasaki, T., Uchida, D., Takayama, Y., Isobe, T., Okuyama, T., and Hanada, K. Epiregulin: a novel epidermal growth factor with mitogenic activity for rat primary hepatocytes. J. Biol. Chem., 270: 7495-7500, 1995.
4. Lee, D. C., Fenton, S. E., Berkowitz, E. A., and Hissong, M. A. Transforming growth factor a: expression, regulation, and biological activities. Pharmacol. Rev., 47: 51-85, 1995.
5. Wen, D., Suggs, S. V., Karunagaran, D., Liu, N., Cupples, R. L., Luo, Y., Janssen, A. M., Ben-Baruch, N., Trollinger, D. B., Jacobsen, V. L., Meng, S-Y., Lu, H. S., Hu, S., Chang, D., Yang, W., Yanigahara, D., Koski, R. A., and Yarden, Y. Structural and functional aspects of the multiplicity of neu differentiation factors. Mol. Cell. Biol., 14: 1909-1919, 1994.
6. Chang, H., Riese, D. J., II, Gilbert, W., Stern, D. F., and McMahan, U. J. Ligands for ErbB-family receptors encoded by a neuregulin-like gene. Nature (Lond.), 387: 509-512, 1997.
7. Carraway III, K. L., Weber, J. L., Unger, M. J., Ledesma, J., Yu, N., Gassmann, M., and Lai, C. Neuregulin-2, a new ligand of ErbB3/ErbB4-receptor tyrosine kinases. Nature (Lond.), 387: 512-516, 1997.
8. Beerli, R. R., and Hynes, N. E. Epidermal growth factor-related peptides activate distinct subsets of erbB receptors and differ in their biological activities. J. Biol. Chem., 271: 6071-6076, 1996.
9. Elenius, K., Paul, S., Allison, G., Sun, J., and Klagsbrun, M. Activation of HER4 by heparin-binding EGF-like growth factor stimulates chemotaxis but not proliferation. EMBO J., 16: 1268-1278, 1997.
10. Riese, D. J., Bermingham, Y., Raaij, T. M. V., Buckley, S., Plowman, G. D., and Stern, D. F. Betacellulin activates the epidermal growth factor receptor and erbB-4, and induces cellular response patterns distinct from those stimulated by epidermal growth factor or neuregulin-β. Oncogene, 12: 345-353, 1996.
11. neu protein and EGF receptor modulates EGF receptor function. Cell, 61: 1339-1347, 1990.
12. Heldin, C-H. Dimerization of cell surface receptors in signal transduction. Cell, 80: 213-223, 1995.
13. Graus-Porta, D., Beerli, R. R., Daly, J. M., and Hynes, N. E. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J., 16: 1647-1655, 1997.
14. Tzahar, E., Waterman, H., Chen, X., Levkowitz, G., Karunagaran, D., Lavi, S., Ratzkin, B. J., and Yarden, Y. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol., 16: 5276-5287, 1996.
15. Chen, X., Levkowitz, G., Tzahar, W., Karunagaran, D., Lavi, S., Ben-Baruch, N., Leitner, O., Ratzkin, B. J., Bacus, S. S., and Yarden, Y. An immunological approach reveals biological differences between the two NDF/Heregulin receptors, ErbB-3 and ErbB-4. J. Biol. Chem., 277; 7620-7629, 1996.
16. Pinkas-Kramarski, R., Soussan, L., Waterman, H., Levkowitz, G., Alroy, I., Klapper, L., Lavi, S., Seger, R., Ratzkin, B. J., Sela, M., and Yarden, Y. Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. EMBO J., 15: 2452-2467, 1996.
17. Karunagaran, D., Tzahar, E., Liu, N., Wen, D., and Yarden, Y. Neu differentiation factor inhibits EGF binding. J. Biol. Chem., 270: 9982-9990, 1995.
18. Vonderhaar, 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.
19. 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.
20. Jones, F. E., Jerry, D. J., Guarino, B. C., Andrews, G. C., and Stern, D. F. Heregulin induces in vivo proliferation and differentiation of mammary epithelium into secretory lobuloalveoli. Cell Growth Differ., 7: 1031-1038, 1996.
21. Kenney, N. J., Smith, G. H., Rosenberg, K., Cutler, M. L., and Dickson, R. B. Induction of ductal morphogenesis and lobular hyperplasia by amphiregulin in the mouse mammary gland. Cell Growth Differ., 7: 1769-1781, 1996.
22. Sandgren, E. P., Schroeder, J. A., Qui, T. H., Palmiter, R. D., Brinster, R. L., and Lee, D. C. Inhibition of mammary gland involution is associated with transforming growth factor α but not c-myc-induced tumorigenesis in transgenic mice. Cancer Res., 55: 3915-3927, 1995.
23. Haslam, S. Z., Counterman, L. J., and Nummy, K. A. EGF receptor regulation in normal mouse mammary gland. J. Cell. Physiol., 152: 553-557, 1992.
24. Edery, M., Pang, K., Larson, L., Colosi, T., and Nandi, S. Epidermal growth factor receptor levels in mouse mammary glands in various physiological states. Endocrinology, 117: 405-411, 1985.
25. Bussmann, L. E., Bussmann, I. M., and Charreau, E. H. Role of receptors for epidermal growth factor and insulin-like growth factors I and II in the differentiation of rat mammary glands from lactogenesis I to lactogenesis II. J. Reprod. Fertil., 107: 307-314, 1996.
26. Herrington, E. E., Ram, T. G., Salomon, D. S., Johnson, G. R., Gullick, W. J., Kenney, N., and Hosick, H. L. Expression of epidermal growth factor-related proteins in the aged adult mouse mammary gland and their relationship to tumorigenesis. J. Cell. Physiol., 170: 47-56, 1997.
27. Snedeker, S. M., Brown, C. F., and DiAugustine, R. P. Expression and functional properties of transforming growth factor α and epidermal growth factor during mouse mammary gland ductal morphogenesis. Proc. Natl. Acad. Sci. USA, 88: 276-280, 1991.
28. Luetteke, N. C., Phillips, H. K., Qiu, T. H., Copeland, N. G., Earp, H. S., Jenkins, N. A., and Lee, D. C. The mouse waved-2 phenotype results from a point mutation in the EGF receptor tyrosine kinase. Genes Dev., 8: 399-413, 1994.
29. Fowler, K. J., Walker, F., Alexander, W., Hibbs, M. L., Nice, E. C., Bohmer, R. M., Mann, G. B., Thumwood, C., Maglitto, R., Danks, J. A., Chetty, R., Burgess, A. W., and Dunn, A. R. A mutation in the epidermal growth factor receptor in waved-2 mice has a profound effect on receptor biochemistry that results in impaired lactation. Proc. Natl. Acad. Sci. USA, 92: 1465-1469, 1995.
30. Xie, W., Paterson, A. J., Chin, E., Nabell, L. M., and Kudlow, J. E. Targeted expression of a dominant negative epidermal growth factor receptor in the mammary gland of transgenic mice inhibits pubertal mammary duct development. Mol. Endocrinol., 11: 1766-1781, 1997.
31. Fox, S. B., Smith, K., Hollyer, J., Greenall, M., Hastrich, D., and Harris, A. L. The epidermal growth factor receptor as a prognostic marker: results of 370 patients and review of 3009 patients. Breast Cancer Res. Treat., 29: 41-49, 1994.
32. Slamon, D. J., Clark, D. M., Wong, S. G., Levin, W. J., Ullrich, A., and McGuire, W. L. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science (Washington DC), 235: 177-182, 1987.
33. Chakrabarty, S., Huang, S., Moskal, T. L., and Fritsche, H. A., Jr. Elevated serum levels of transforming growth factor-α in breast cancer patients. Cancer Lett., 79: 157-160, 1994.
34. LeJeune, N., Leek, R., Horak, E., Plowman, G., Greenall, M., and Harris, A. L. Amphiregulin, epidermal growth factor receptor, and estrogen receptor expression in human primary breast cancer. Cancer Res., 53: 3597-3602, 1993.
35. Eissa, S., Khalifa, A., El-Hharib, J., Salah, N., and Mohamed, M. K. Multivariate analysis of DNA ploidy, p53, c-erbB-2 proteins, EGFR, and steroid hormone receptors for prediction of poor short term prognosis in breast cancer. Anticancer Res., 17: 1417-1424, 1997.
36. Nicholson, S., Richard, J., Sainsbury, C., Halcrow, P., Kelly, P., Angus, B., Wright, C., Henry, J., Farndon, J. R., and Harris, A. L. Epidermal growth factor receptor (EGFR); results of a 6 year follow-up study in operable breast cancer with emphasis on the node negative subgroup. Br. J. Cancer, 63: 146-150, 1991.
37. Bebok, Z., Markus, B., and Nemeth, P. Prognostic relevance of transforming growth factor alpha (TGF-α) and tumor necrosis factor alpha (TNF-α) detected in breast cancer tissues by immunohistochemistry. Breast Cancer Res. Treat., 29: 229-235, 1994.
38. Schroeder, J. A., and Lee, D. C. Transgenic mice reveal roles for TGFα and EGF receptor in mammary gland development and neoplasia. J. Mammary Gland Biol. Neoplasia, 2: 119-129, 1997.
39. Sainsbury, J. R. C., Farndon, J. R., Needham, G. K., Malcolm, A. J., and Harris, A. L. Epidermal-growth-factor receptor status as predictor of early recurrence of and death from breast cancer. Lancet, i: 1398-1402, 1987.
40. Yamauchi, H., O'Neill, A., Gelman, R., Carney, W., Tenney, D. Y., Hosch, S., and Hayes, D. F. Prediction of response to antiestrogen therapy in advanced breast cancer patients by pretreatment circulating levels of extracellular domain of the HER-2/c-neu protein. J. Clin. Oncol., 15: 2518-2525, 1997.
41. Benz, C. C., Scott, G. K., Sarup, J. C., Johnson, R. M., Tripathy, D., Coronado, E., Shepard, H. M., and Osborne, C. K. Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu. Breast Cancer Res. Treat., 24: 85-95, 1992.
42. Liu, Y., El-Ashry, D., Chen, D., Ding, I. Y. F., and Kern, F. G. MCF-7 breast cancer cells overexpressing transfected c-enbB-2 have an in vitro growth advantage in estrogen-depleted conditions and reduced estrogen-dependence and tamoxifen-sensitivity in vivo. Breast Cancer Res. Treat., 34: 97-117, 1995.
43. Reddy, K. B., Yee, D., Hilesenbeck, S. G., Coffey, R. J., and Osborne, C. K. Inhibition of estrogen-induced breast cancer cell proliferation by reduction in autocrine transforming growth factor α expression. Cell Growth Differ., 5: 1275-1282, 1994.
44. Kenney, N. J., Saeki, T., Gottardis, M., Kim, N., Garcia-Morales, P., Martin, M. B., Normanno, N., Ciardiello, F., Day, A., Cutler, M. L., and Salomon, D. S. Expression of transforming growth factor α antisense mRNA inhibits the estrogen-induced production of TGFα and estrogen-induced proliferation of estrogen-responsive human breast cancer cells. J. Cell. Physiol., 156: 497-514, 1993.
45. Strange, R., Li, F., Saurer, S., Burkhardt, A., and Friis, R. R. Apoptotic cell death and tissue remodelling during mouse mammary gland involution. Development (Camb.), 115: 49-58, 1992.
46. McKnight, R. A., Burdon, T., Pursel, V. G., Shamay, A., Wall, R. J., and Hennighausen, L. The whey acidic protein. In: R. B. Dickson and M. E. Lippman (eds.), Genes, oncogenes, and hormones: advances in cellular and molecular biology of breast cancer, pp. 399-412. Boston: Kluwer Academic Publishers, 1991.
47. Goldsworthy, S. M., Goldsworthy, T. L., Sprankle, C. S., and Butterworth, B. E. Variation in expression of genes used for normalization of Northern blots after induction of cell proliferation. Cell Prolif., 26: 511-517, 1993.
48. Kwan, H., Pecenka, V., Tsukamoto, A., Parslow, T. G., Guzman, R., Lin, T-P., Muller, W. J., Lee, F. S., Leder, P., and Varmus, H. Transgenes expressing the wnt-1 and int-2 proto-oncogenes cooperate during mammary carcinogenesis in doubly transgenic mice. Mol. Cell. Biol., 72: 147-154, 1992.
49. Burdon, T., Sankaran, L., Wall, R. J., Spencer, M., and Hennighausen, L. Expression of a whey acidic protein transgene during mammary development. J. Biol. Chem., 266: 6909-6914, 1991.
50. Robinson, G. W., McKnight, R. A., Smith, G. H., and Hennighausen, L. Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development (Camb.), 121: 2079-2090, 1995.
51. Brown, C. F., Teng, C. T., Pentecost, B. T., and DiAugustine, R. P. Epidermal growth factor precursor in mouse lactating mammary gland alveolar cells. Mol. Endocrinol., 3: 1077-1083, 1989.
52. Fenton, S. E., and Sheffield, L. G. Lactogenic hormones increase epidermal growth factor messenger RNA content of mouse mammary glands. Biochem. Biophys. Res. Commun., 181: 1063-1069, 1991.
53. Gabay, L., Seger, R., and Shilo, B-Z. In situ activation pattern of Drosophila EGF receptor pathway during development. Science (Washington DC), 277: 1103-1106, 1997.
54. r 55,000 substrate with the receptor. Proc. Natl. Acad. Sci. USA, 89: 8477-8481, 1992.
55. Ruff, S. J., Chen, K., and Cohen, S. Peroxovanadate induces tyrosine phosphorylation of multiple signaling proteins in mouse liver and kidney. J. Biol. Chem, 272: 1263-1267, 1997.
56. Burnol, A. F., Loizeau, M., and Girard, J. Insulin receptor activity and insulin sensitivity in mammary gland of lactating rats. Am. J. Phys., 259: E828-E834, 1990.
57. Daly, J. M., Jannot, C. B., Beerli, R. R., Graus-Porta, D., Maurer, F. G., and Hynes, N. E. Neu differentiation factor induces erbB2 down-regulation and apoptosis of erbB2-overexpressing breast tumor cells. Cancer Res., 57: 3804-3811, 1997.
58. Beardmore, J. M., and Richards, R. C. Concentration of epidermal growth factor in mouse milk throughout lactation. J. Endocrinol., 96: 287-292, 1983.
59. Carpenter, G. Epidermal growth factor is a major growth promoting agent in human milk. Science (Washington DC), 270: 198-199, 1980.
60. Dati, C., Maggiora, P., Puech, C., Bortoli, M. D., and Escot, C. Expression of the erbB-2 proto-oncogene during differentiation of the mammary gland in the rat. Cell Tissue Res., 205: 403-410, 1996.
61. Dati, C., Antoniotti, S., Taverna, D., Perroteau, I., and Bortoli, M. D. Inhibition of c-erbB-2 oncogene expression by estrogens in human breast cancer cells. Oncogene, 5: 1001-1006, 1990.
62. Yang, Y., Spitzer, E., Meyer, D., Sachs, M., Niemann, C., Hartmann, G., Weidner, K. M., Birchmeier, C., and Birchmeier, W. Sequential requirement of hepatocyte growth factor and neuregulin in the morphogenesis and differentiation of the mammary gland. J. Cell Biol., 131: 215-226, 1995.
63. Higashiyama, S., Abraham, J. A., Miller, J., Fiddes, J. C., and Klagsbrun, M. A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science (Washington DC), 257: 936-939, 1991.
64. Shoyab, M., Plowman, G. D., McDonald, V. L., Bradley, J. G., and Todaro, G. J. Structure and function of human amphiregulin: a member of the epidermal growth factor family. Science (Washington DC), 243:1074-1076, 1989.
65. Liu, X., Robinson, G. W., and Hennighausen, L. Activation of STAT 5a and STAT 5b by tyrosine phosphorylation is tightly linked to mammary gland differentiation. Mol. Endocrinol., 10: 1496-1506, 1996.
66. Liu, X., Robinson, G. W., Wagner, K-U., Garrett, L, Wynshaw-Boris, A., and Hennighausen, L. Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev., 11: 179-186, 1997.
67. Wartmann, M. K., Cella, N., Hofer, P., Groner, B., Liu, X., Hennighausen, L., and Hynes, N. E. Lactogenic hormone activation of Stat5 and transcription of the β-casein gene in mammary epithelial cells is independent of p42 ERK2 mitogen-activated protein kinase activity. J. Biol. Chem., 277: 31863-31868, 1996.
68. Luetteke, N. C., Qiu, T. H., Peiffer, R. L., Oliver, P., Smithies, O., and Lee, D. C. TGF α deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell, 73: 263-278, 1993.