Targeting the death machinery in mammary epithelial cells: Implications for breast cancer from transgenic and tissue culture experiments

Critical Reviews in Oncology/Hematology

Volumn 63, Issue 3, 2007, Pages 231-240

  Jäger, Richard ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Apoptosis; Bcl 2; Breast; Cancer; Mammary; MCF 10A; Transgenic mice

Indexed keywords

MYC PROTEIN; PROTEIN BAX; PROTEIN BCL 2; SIMIAN VIRUS 40 T ANTIGEN; UNCLASSIFIED DRUG; VIRUS T ANTIGEN;

APOPTOSIS; BREAST CANCER; BREAST EPITHELIUM; CANCER MODEL; CANCER STAGING; CELL PROLIFERATION; EPITHELIUM CELL; GENE FUNCTION; NONHUMAN; ONCOGENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TISSUE CULTURE; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; DRUG DELIVERY SYSTEMS; EPITHELIAL CELLS; FEMALE; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC;

EID: 34547172201     PISSN: 10408428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2007.05.006     Document Type: Review

References (83)

1. Baehrecke EH. How death shapes life during development. Nat Rev Mol Cell Biol 3 10 (2002) 779-787
2. Richert M.M., Schwertfeger K.L., Ryder J.W., and Anderson S.M. An atlas of mouse mammary gland development. J Mammary Gland Biol Neoplasia 5 2 (2000) 227-241
3. Hinck L., and Silberstein G.B. Key stages in mammary gland development: the mammary end bud as a motile organ. Breast Cancer Res 7 6 (2005) 245-251
4. Humphreys R.C., Krajewska M., Krnacik S., et al. Apoptosis in the terminal endbud of the murine mammary gland: a mechanism of ductal morphogenesis. Development 122 12 (1996) 4013-4022
5. Andres A.C., Zuercher G., Djonov V., Flueck M., and Ziemiecki A. Protein tyrosine kinase expression during the estrous cycle and carcinogenesis of the mammary gland. Int J Cancer 63 2 (1995) 288-296
6. 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 121 7 (1995) 2079-2090
7. Andres A.C., and Strange R. Apoptosis in the estrous and menstrual cycles. J Mammary Gland Biol Neoplasia 4 2 (1999) 221-228
8. Strange R., Li F., Saurer S., Burkhardt A., and Friis R.R. Apoptotic cell death and tissue remodelling during mouse mammary gland involution. Development 115 1 (1992) 49-58
9. Walker N.I., Bennett R.E., and Kerr J.F. Cell death by apoptosis during involution of the lactating breast in mice and rats. Am J Anat 185 1 (1989) 19-32
10. Lund L.R., Romer J., Thomasset N., et al. Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways. Development 122 1 (1996) 181-193
11. Hengartner M.O. The biochemistry of apoptosis. Nature 407 6805 (2000) 770-776
12. Fischer U., Janicke R.U., and Schulze-Osthoff K. Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ 10 1 (2003) 76-100
13. Lavrik I.N., Golks A., and Krammer P.H. Caspases: pharmacological manipulation of cell death. J Clin Invest 115 10 (2005) 2665-2672
14. Slee E.A., Adrain C., and Martin S.J. Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J Biol Chem 276 10 (2001) 7320-7326
15. Riedl S.J., and Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 5 11 (2004) 897-907
16. Krammer P.H. CD95's deadly mission in the immune system. Nature 407 6805 (2000) 789-795
17. Clarkson R.W., Wayland M.T., Lee J., Freeman T., and Watson C.J. Gene expression profiling of mammary gland development reveals putative roles for death receptors and immune mediators in post-lactational regression. Breast Cancer Res 6 2 (2004) R92-R109
18. Marti A., Graber H., Lazar H., et al. Caspases: decoders of apoptotic signals during mammary involution. Caspase activation during involution. Adv Exp Med Biol 480 (2000) 195-201
19. Song J., Sapi E., Brown W., et al. Roles of Fas and Fas ligand during mammary gland remodeling. J Clin Invest 106 10 (2000) 1209-1220
20. Baxter F.O., Came P.J., Abell K., et al. IKKbeta/2 induces TWEAK and apoptosis in mammary epithelial cells. Development 133 17 (2006) 3485-3494
21. Kuwana T., and Newmeyer D.D. Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 15 6 (2003) 691-699
22. Li P., Nijhawan D., Budihardjo I., et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91 4 (1997) 479-489
23. Zou H., Li Y., Liu X., and Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 274 17 (1999) 11549-11556
24. Marti A., Ritter P.M., Jäger R., et al. Mouse mammary gland involution is associated with cytochrome c release and caspase activation. Mech Dev 104 1-2 (2001) 89-98
25. Boudreau N., Sympson C.J., Werb Z., and Bissell M.J. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267 5199 (1995) 891-893
26. Cory S., and Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2 9 (2002) 647-656
27. Willis S.N., and Adams J.M. Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol 17 6 (2005) 617-625
28. Puthalakath H., and Strasser A. Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ 9 5 (2002) 505-512
29. del Peso L., Gonzalez-Garcia M., Page C., Herrera R., and Nunez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278 5338 (1997) 687-689
30. Datta S.R., Dudek H., Tao X., et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91 2 (1997) 231-241
31. Cai B., Chang S.H., Becker E.B., Bonni A., and Xia Z. p38 MAP kinase mediates apoptosis through phosphorylation of BimEL at Ser-65. J Biol Chem 281 35 (2006) 25215-25222
32. Zha J., Harada H., Yang E., Jockel J., and Korsmeyer S.J. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87 4 (1996) 619-628
33. Day C.L., Puthalakath H., Skea G., et al. Localization of dynein light chains 1 and 2 and their pro-apoptotic ligands. Biochem J 377 Pt 3 (2004) 597-605
34. Li H., Zhu H., Xu C.J., and YuanF J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 4 (1998) 491-501
35. Metcalfe A.D., Gilmore A., Klinowska T., et al. Developmental regulation of Bcl-2 family protein expression in the involuting mammary gland. J Cell Sci 112 Pt 11 (1999) 1771-1783
36. Schorr K., Li M., Bar-Peled U., et al. Gain of Bcl-2 is more potent than bax loss in regulating mammary epithelial cell survival in vivo. Cancer Res 59 11 (1999) 2541-2545
37. Strange R., Metcalfe T., Thackray L., and Dang M. Apoptosis in normal and neoplastic mammary gland development. Microsc Res Tech 52 2 (2001) 171-181
38. Heermeier K., Benedict M., Li M., Furth P., Nunez G., and Hennighausen L. Bax and Bcl-xs are induced at the onset of apoptosis in involuting mammary epithelial cells. Mech Dev 56 1-2 (1996) 197-207
39. Walton K.D., Wagner K.U., Rucker III E.B., Shillingford J.M., Miyoshi K., and Hennighausen L. Conditional deletion of the bcl-x gene from mouse mammary epithelium results in accelerated apoptosis during involution but does not compromise cell function during lactation. Mech Dev 109 2 (2001) 281-293
40. Reginato M.J., Mills K.R., Becker E.B., et al. Bim regulation of lumen formation in cultured mammary epithelial acini is targeted by oncogenes. Mol Cell Biol 25 11 (2005) 4591-4601
41. Mailleux A.A., Overholtzer M., Schmelzle T., Bouillet P., Strasser A., and Brugge J.S. BIM regulates apoptosis during mammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev Cell 12 2 (2007) 221-234
42. Salvesen G.S., and Duckett C.S. IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 3 6 (2002) 401-410
43. Eckelman B.P., Salvesen G.S., and Scott F.L. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 7 10 (2006) 988-994
44. Green D.R. Apoptotic pathways: paper wraps stone blunts scissors. Cell 102 1 (2000) 1-4
45. Martins L.M. The serine protease Omi/HtrA2: a second mammalian protein with a Reaper-like function. Cell Death Differ 9 7 (2002) 699-701
46. Olayioye M.A., Kaufmann H., Pakusch M., Vaux D.L., Lindeman G.J., and Visvader J.E. XIAP-deficiency leads to delayed lobuloalveolar development in the mammary gland. Cell Death Differ 12 1 (2005) 87-90
47. Hennighausen L. Mouse models for breast cancer. Breast Cancer Res 2 1 (2000) 2-7
48. 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 alpha but not c-myc-induced tumorigenesis in transgenic mice. Cancer Res 55 17 (1995) 3915-3927
49. Lazar H., Baltzer A., Gimmi C., Marti A., and Jaggi R. Over-expression of erbB-2/neu is paralleled by inhibition of mouse-mammary-epithelial-cell differentiation and developmental apoptosis. Int J Cancer 85 4 (2000) 578-583
50. Aranda V., Haire T., Nolan M.E., et al. Par6-aPKC uncouples ErbB2 induced disruption of polarized epithelial organization from proliferation control. Nat Cell Biol 8 11 (2006) 1235-1245
51. Jäger R., Herzer U., Schenkel J., and Weiher H. Overexpression of Bcl-2 inhibits alveolar cell apoptosis during involution and accelerates c-myc-induced tumorigenesis of the mammary gland in transgenic mice. Oncogene 15 15 (1997) 1787-1795
52. Tzeng Y.J., Gottlob K., Santarelli R., and Graessmann A. The SV40 T-antigen induces premature apoptotic mammary gland involution during late pregnancy in transgenic mice. FEBS Lett 380 3 (1996) 215-218
53. Shibata M.A., Maroulakou I.G., Jorcyk C.L., Gold L.G., Ward J.M., and Green J.E. p53-independent apoptosis during mammary tumor progression in C3(1)/SV40 large T antigen transgenic mice: suppression of apoptosis during the transition from preneoplasia to carcinoma. Cancer Res 56 13 (1996) 2998-3003
54. Knudson C.M., Tung K.S., Tourtellotte W.G., Brown G.A., and Korsmeyer S.J. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270 5233 (1995) 96-99
55. Burdon T., Sankaran L., Wall R.J., Spencer M., and Hennighausen L. Expression of a whey acidic protein transgene during mammary development. Evidence for different mechanisms of regulation during pregnancy and lactation. J Biol Chem 266 11 (1991) 6909-6914
56. Willis S.N., Chen L., Dewson G., et al. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19 11 (2005) 1294-1305
57. Haldar S., Jena N., and Croce C.M. Inactivation of Bcl-2 by phosphorylation. Proc Natl Acad Sci USA 92 10 (1995) 4507-4511
58. McDonnell T.J., and Korsmeyer S.J. Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14; 18). Nature 349 6306 (1991) 254-256
59. Shibata M.A., Liu M.L., Knudson M.C., et al. Haploid loss of bax leads to accelerated mammary tumor development in C3(1)/SV40-TAg transgenic mice: reduction in protective apoptotic response at the preneoplastic stage. Embo J 18 10 (1999) 2692-2701
60. Li M., Lewis B., Capuco A.V., Laucirica R., and Furth P.A. WAP-TAg transgenic mice and the study of dysregulated cell survival, proliferation, and mutation during breast carcinogenesis. Oncogene 19 8 (2000) 1010-1019
61. Furth P.A., Bar-Peled U., Li M., et al. Loss of anti-mitotic effects of Bcl-2 with retention of anti-apoptotic activity during tumor progression in a mouse model. Oncogene 18 47 (1999) 6589-6596
62. Murphy K.L., Kittrell F.S., Gay J.P., Jäger R., Medina D., and Rosen J.M. Bcl-2 expression delays mammary tumor development in dimethylbenz(a)anthracene-treated transgenic mice. Oncogene 18 47 (1999) 6597-6604
63. Borner C. Diminished cell proliferation associated with the death-protective activity of Bcl-2. J Biol Chem 271 22 (1996) 12695-12698
64. Zinkel S., Gross A., and Yang E. BCL2 family in DNA damage and cell cycle control. Cell Death Differ 13 8 (2006) 1351-1359
65. Adhikary S., and Eilers M. Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol 6 8 (2005) 635-645
66. Askew D.S., Ashmun R.A., Simmons B.C., and Cleveland J.L. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6 10 (1991) 1915-1922
67. Evan G.I., Wyllie A.H., Gilbert C.S., et al. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69 1 (1992) 119-128
68. Juin P., Hueber A.O., Littlewood T., and Evan G. c-Myc-induced sensitization to apoptosis is mediated through cytochrome c release. Genes Dev 13 11 (1999) 1367-1381
69. Mitchell K.O., Ricci M.S., Miyashita T., et al. Bax is a transcriptional target and mediator of c-myc-induced apoptosis. Cancer Res 60 22 (2000) 6318-6325
70. Hemann M.T., Bric A., Teruya-Feldstein J., et al. Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature 436 7052 (2005) 807-811
71. Liao D.J., and Dickson R.B. c-Myc in breast cancer. Endocr Relat Cancer 7 3 (2000) 143-164
72. Stewart T.A., Pattengale P.K., and Leder P. Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell 38 3 (1984) 627-637
73. Liao D.J., and Dickson R.B. Cell death in MMTV-c-myc transgenic mouse mammary tumors may not be typical apoptosis. Lab Invest 83 10 (2003) 1437-1449
74. Hundley J.E., Koester S.K., Troyer D.A., Hilsenbeck S.G., Barrington R.E., and Windle J.J. Differential regulation of cell cycle characteristics and apoptosis in MMTV-myc and MMTV-ras mouse mammary tumors. Cancer Res 57 4 (1997) 600-603
75. Jamerson M.H., Johnson M.D., Korsmeyer S.J., Furth P.A., and Dickson R.B. Bax regulates c-Myc-induced mammary tumour apoptosis but not proliferation in MMTV-c-myc transgenic mice. Br J Cancer 91 7 (2004) 1372-1379
76. Muthuswamy S.K., Li D., Lelievre S., Bissell M.J., and Brugge J.S. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 3 9 (2001) 785-792
77. Debnath J., Mills K.R., Collins N.L., Reginato M.J., Muthuswamy S.K., and Brugge J.S. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111 1 (2002) 29-40
78. Baehrecke E.H. Autophagy: dual roles in life and death?. Nat Rev Mol Cell Biol 6 6 (2005) 505-510
79. Mills K.R., Reginato M., Debnath J., Queenan B., and Brugge J.S. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc Natl Acad Sci USA 101 10 (2004) 3438-3443
80. Krajewski S., Krajewska M., Turner B.C., et al. Prognostic significance of apoptosis regulators in breast cancer. Endocr Relat Cancer 6 1 (1999) 29-40
81. Simin K., Wu H., Lu L., et al. pRb inactivation in mammary cells reveals common mechanisms for tumor initiation and progression in divergent epithelia. PLoS Biol 2 2 (2004) E22
82. Wodarz D., and Komarova N. Can loss of apoptosis protect against cancer?. Trends Genet 23 5 (2007) 232-237
83. Shimizu S., Kanaseki T., Mizushima N., et al. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6 12 (2004) 1221-1228