Apoptosis in the terminal endbud of the murine mammary gland: A mechanism of ductal morphogenesis

Development

Volumn 122, Issue 12, 1996, Pages 4013-4022

  Humphreys, Robin C ^a   Krajewska, Maryla ^b   Krnacik, Susanne ^a   Jæger, Richard ^c   Weiher, Hans ^c   Krajewski, Stanislaw ^b   Reed, John C ^b   Rosen, Jeffrey M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b BURNHAM INSTITUTE   (United States)

^c KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Apoptosis; Bax; Bcl 2; Bcl x; DNA synthesis; Mammary gland; Mouse; p53; Terminal endbud; WAP Bcl 2

Indexed keywords

DNA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST DEVELOPMENT; BREAST DUCT; CELL DEATH; CONTROLLED STUDY; DNA SYNTHESIS; FEMALE; IMMUNOHISTOCHEMISTRY; MAMMARY GLAND; MORPHOGENESIS; MORPHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENE;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; FEMALE; GENES, P53; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; MORPHOGENESIS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; TISSUE DISTRIBUTION;

EID: 0030452907     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Andersnn, C. H. and Beattie, C. W. (1992). Cellular kinetics of rat mammary gland terminal end bud epithelium exposed to N-methyl-N-nitrosourea in vivo. Cancer Res. 52, 5076-5081.
2. Barres, B. A., Hart, I. K., Coles, H. S., Burne, J. F., Voyvodic, J. T., Richardson, W. D. and Raff, M. C. (1992). Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31-46.
3. Berges, R. R., Furuya, Y., Remington, L., English, H. F., Jacks, T. and Isaacs, J. T. (1993). Cell proliferation. DNA repair, and p53 function are not required for programmed death of prostatic glandular cells induced by androgen ablation. Proc. Natl. Acad. Sci. USA 90, 8910-8914.
4. Boise, L. H., Gonzalez, G. M., Postema, C. E., Ding, L., Lindsten, T., Turka, L. A., Mao, X., Nunez, G. and Thompson, C. B. (1993). bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74, 597-608.
5. Boudreau, N., Sympson, C. J., Werb, Z. and Bissell, M. J. (1995). Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267, 891-893.
6. Chao, D. T., Linette, G. P., Boise, L. H., White, L. S., Thompson, C. B. and Korsmeyer, S. J. (1995). Bcl-XL and Bcl-2 repress a common pathway of cell death. J. Exp. Med. 182, 821-828.
7. Coleman, S., Silberstein, G, B. and Daniel, C. W. (1988). Ductal morphogenesis in the mouse mammary gland: evidence supporting a role for epidermal growth factor. Dev. Biol. 127, 304-315.
8. Coles, H., Burne, J. F. and Raff, M. C. (1993). Large scale normal cell death in the developing rat kidney and its reduction by epidermal growth factor. Development 118. 777-784.
9. Colombel, M., Radvanyi, F., Blanche, M., Abbou, C., Buttyan, R., Donehower, L. A., Chopin, D. and Thiery, J. P. (1995). Androgen suppressed apoptosis is modified in p53 deficient mice. Oncogene 10, 1269-1274.
10. Coucouvanis, E. and Martin, G. R. (1995). Signals for cell death and survival: A two step mechanism for cavitation in the vertabrate embryo. Cell 83. 279-287.
11. Daniel, C. W. and Silberstein, G. B. (1985). Postnatal development of the rodent mammary gland. In The Mammary Gland: Development. Regulation and Function (ed. M. C. Neville and C. W. Daniel), pp. 3-36. New York: Plenum Publishing.
12. Daniel, C. W., Silberstein, G. B. and Strickland, P. (1987). Direct action of 17 beta-estradiol on mouse mammary ducts analyzed by sustained release implants and steroid autoradiography. Cancer Res. 47, 6052-6057.
13. Daniel, C. W., Strickland, P. and Friedmann, Y. (1995). Expression and functional role of E- and P-cadherins in mouse mammary ductul morphogenesis and growth. Dev. Biol. 169, 511-519.
14. Donehower, L. A., Harvey, M., Slagle, B. L., McArthur, M. J., Montgomery, C. A. J., Butel, J. S. and Bradley, A. (1992). Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356, 215-221.
15. Dulbecco, R., Allen, W. R., Bologna, M. and Bowman, M. (1986). Marker evolution during the development of the rat mammary gland: stem cells identified by markers and the role of myoepithelial cells. Cancer Res. 46, 2449-2456.
16. Dulbecco, R., Henahan, M. and Armstrong, B. (1982). Cell types and morphogenesis in the mammary gland. Proc. Natl. Acad. Sci. USA 79. 7346-7350.
17. Dulbecco, R., Unger, M., Armstrong, B., Bowman, M. and Syka, P. (1983) Epithelial cell types and their evolution in the rat mammary gland determined by immunological markers. Proc. Natl. Acad. Sci. USA 80, 1033-1037.
18. Frisch, S. M. and Francis, H. (1994). Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124, 619-26.
19. Garcia, I., Martinou, I., Tsujimoto, Y. and Martinou, J.-C. (1992). Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene. Science 258, 302-304.
20. Gavrieli, Y., Sherman, Y. and Ben, S. S. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
21. Glucksmann, A. (1951). Cell death in normal vetebrate ontogeny. Biol. Rev. 26, 59-86.
22. Heermeier, K., Benedict, M., Li, M. L., Furth, P., Nunez, G. and Henninghausen, L, (1996). Bax and bcl-x(s) are induced at the onset of apoptosis in involuting mammary epithelial cells. Mech. Devel. 56, 197-207.
23. Knight, C. H. and Peaker, M. (1982). Development of the mammary gland. J. Reprod. Fertil. 65, 521-536.
24. Knudson, C. M., Tung, K. S., Tourtellotte, W. G., Brown, G. A. and Korsmeyer, S. J. (1995). Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270, 96-99.
25. Krajewski, S., Krajewska, M., Shabaik, A., Wang, H. G., Irie. S., Fong, L. and Reed, J. C. (1994a). Immunohistochemical analysis of in vivo patterns of Bcl-X expression. Cancer Res. 54, 5501-5507.
26. Krajewski, S., Krajewska, M., Shabaik, A., Miyashita, T., Wang, H. G. and Reed, J. C. (1994b). Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am. J. Pathol. 145, 1323-1336.
27. Li, B., Kittrell, F. S., Medina, D. and Rosen, J. M. (1995). Delay of dimethylbenz[a]anthracene-induced mammary tumorigenesis in transgenic mice by apoptosis induced by an unusual mutant p53 protein. Molecular Carcinogenesis 14, 75-83.
28. Li, M., Hu, J., Heermeier, K., Hennighausen, L. and Furth, P. (1996a). Expression of a viral oncoprotein during mammary gland development alters cell fate and function: Induction of p53-independent apoptosis is followed by impaired milk production in surviving cells. Cell Growth & Differ. 7, 7-11.
29. Li, M., Hu, J., Heermeier, K., Henninghausen, L. and Furth, P. (1996b). Apoptosis and remoldeling of mammary gland tissue during involution proceeds through p53-independent pathways. Cell Growth & Differ. 7, 13-20.
30. Lund, L. R., Romer, J., Thomasset, N., Solberg, H., Pyke, C., Bissell, M. J., Dano, K. and Werb, Z. (1996). Two distinct phases of apoptosis in mamamry gland involution: proteinase-independent and -dependent pathways. Development 122, 181-193.
31. Merlo, G. R., Basolo, F., Fiore, L., Duboc, L. and Hynes, N. E. (1995). p53-dependent and p53-independent activation of apoptosis in mammary epithelial cells reveals a survival function of EGF and insulin. J. Cell Biol. 128, 1185-1196.
32. Middleton, G., Nunez, G. and Davies, A. M. (1996). Bax promotes neuronal survival and antagonises the survival effects of neurotrophic factors. Development 122, 695-701.
33. Miyashita, T., Krajewski, S., Krajewska, M., Wang, H. G., Lin, H. K., Liebermann, D. A., Huffman, B. and Reed, J. C. (1994). Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9, 1799-1805.
34. Oltvai, Z. N., Milliman, C. L. and Korsmeyer, S. J. (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609-619.
35. Pullan, S., Wilson, J., Metcalfe, A., Edwards, G. M., Goberdhan, N., Tilly, J., Hickman, J. A., Dive, C. and Streuli, C. H. (1996). Requirement of basement membrane for the suppression of programmed cell death in mammary epithelium. J. Cell Sci. 109, 631-642.
36. Quarrie, L. H., Addey, C. V. and Wilde, C. J. (1995). Apoptosis in lactating and involuting mouse mammary tissue demonstrated by nick-end DNA labelling. Cell Tissue Res. 281, 413-419.
37. Reed, J. C. (1994). Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124, 1-6.
38. Reed, J. C., Cuddy, M., Haldar, S., Croce, C., Nowell, P., Makover, D. and Bradley, K. (1990). BCL2-mediated tumorigenicity of a human T-lymphoid cell line: synergy with MYC and inhibition by BCL2 antisense. Proc. Natl. Acad. Set. USA 87, 3660-3664.
39. Ruoslahti, E. and Reed, J. C. (1994). Anchorage dependence, integrins, and apoptosis. Cell 77, 477-478.
40. Russo, I. H. and Russo, J. (1978a). Developmental stage of the rat mammary gland as determinant of its susceptibility to 7, 12-dimethylbenz[a]anthracene. J. Natl. Cancer Inst. 61, 1439-1449.
41. Russo, J. and Russo, I. H. (1978b). DNA labeling index and structure of the rat mammary gland as determinants of its susceptibility to carcinogenesis. J. Natl. Cancer Inst. 61, 1451-1459.
42. Sapino, A., Macri, L., Gugliotta, P. and Bussolati, G. (1990). Immunocytochemical identification of proliferating cell types in mouse mammary gland. J. Histochem. Cylochem. 38, 1541-1547.
43. Saunders, J. W. (1966). Death in embryonic systems. Science 154, 604-612.
44. Sedlak, T. W., Oltvai, Z. N., Yang, E., Wang, K., Boise, L. H., Thompson, C. B. and Korsmeyer, S. J. (1995). Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc. Natl. Acad. Sci. USA 92, 7834-7838.
45. Shaw, P., Bovey, R., Tardy, S., Sahli, R., Sordat, B. and Costa, J. (1992). Induction ot apoptosis by wild-type p53 in a human colon tumor-derived cell line. Proc. Natl. Acad. Sci. USA 89, 4495-4499.
46. Strange, R., Li, F., Saurer, S., Burkhardt, A. and Friis, R. R. (1992). Apoptotic cell death and tissue remodelling during mouse mammary gland involution. Development 115, 49-58.
47. Strasser, A., Harris, A. W. and Cory, S. (1991). bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 67, 889-899.
48. Sympson, C. J., Talhouk, R. S., Alexander, C. M., Chin, J. R., Clift, S. M., Bissell, M. J. and Werb, Z. (1994). Targeted expression of stromelysin-1 in mammary gland provides evidence for a role of proteinases in branching morphogenesis and the requirement for an intact basement membrane for tissue-specific gene expression. J. Cell Biol. 125, 681-693.
49. Takayama, S., Takaaki, S., Krajewski. S., Kochel, K., Irie, S., Millan, J. A. and Reed, J. C. (1995). Cloning and functional analysis of Bag-1: A novel Bcl-2 binding protein with anti-cell death activity. Cell 80, 279-284.
50. Topper, Y. J. and Freeman, C. S. (1980). Multiple hormone interactions in the developmental biology of the mammary gland. Physiol. Rev. 60. 1049-1106.
51. Vaux, D. L., Cory, S. and Adams, J. M. (1988). Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335, 440-442.
52. Vonderhaar, B. K. (1987). Local effects of EGF, alpha-TGF, and EGF-like growth factors on lobuloalveolar development of the mouse mammary gland in vivo. J. Cell. Physiol. 132, 581-584.
53. Williams, J. M. and Daniel, C. W. (1983). Mammary ductal elongation: differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev. Biol. 97, 274-290.
54. Witty, J. P., Lempka, T., Coffey, R. J. and Matrisian, L. M. (1995). Decreased tumor formation in 7, 12-dimethylbenzanthracene-treated stromelysin-1 transgenic mice is associated with alterations in mammary epithelial cell apoptosis. Cancer Res. 55, 1401-1406.
55. Yang, E., Zha, J., Jockel, J., Boise, L. H., Thompson, C. B. and Korsmeyer, S. J. (1995). Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80, 285-291.
56. Yonish, R. E., Grunwald, D., Wilder, S., Kimchi, A., May, E., Lawrence, J. J., May, P. and Oren, M. (1993). p53-mediated cell death: relationship to cell cycle control. Mol Cell Biol. 13, 1415-1423.
57. Zhan, Q., Carrier, F. and Fornace, A. J. (1993). Induction of cellular p53 activity by DNA-damaging agents and growth arrest. Mol. Cell Biol. 13, 4242-4250.
58. Zhang, Z., Vuori, K., Reed, J. C. and Ruoslahti, E. (1995). The alpha 5 beta 1 integrin supports survival of cells on fibronectin and up-regulates Bcl-2 expression. Proc. Natl Acad. Sci. USA 92, 6161-6165.