Perturbation of β1-integrin function in involuting mammary gland results in premature dedifferentiation of secretory epithelial cells

Molecular Biology of the Cell

Volumn 13, Issue 10, 2002, Pages 3521-3531

  Faraldo, Marisa M ^a   Deugnier, Marie Ange ^a   Tlouzeau, Sylvie ^a   Thiery, Jean Paul ^a   Glukhova, Marina A ^a  

^a INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PROTEIN; BETA CASEIN; BETA1 INTEGRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; STAT5 PROTEIN; TRANSCRIPTION FACTOR; CD4 ANTIGEN; DNA BINDING PROTEIN; HYBRID PROTEIN; JAK2 PROTEIN, MOUSE; JANUS KINASE 2; MILK PROTEIN; ONCOPROTEIN; PROTEIN TYROSINE KINASE; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FEMALE; GENETIC TRANSCRIPTION; GROWTH DISORDER; INVOLUTION; LACTATION; MAMMARY GLAND; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONTENT; PROTEIN FUNCTION; SECRETORY CELL; TRANSGENIC MOUSE; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; REPORTER GENE; SIGNAL TRANSDUCTION; UDDER;

ANIMALS; ANTIGENS, CD29; ANTIGENS, CD4; APOPTOSIS; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; EPITHELIAL CELLS; FEMALE; GENES, REPORTER; JANUS KINASE 2; LACTATION; MAMMARY GLANDS, ANIMAL; MAMMARY TUMOR VIRUS, MOUSE; MICE; MICE, TRANSGENIC; MILK PROTEINS; NF-KAPPA B; PREGNANCY; PROMOTER REGIONS (GENETICS); PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS;

EID: 0036800344     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-02-0086     Document Type: Article

References (45)

1. Adams, J.C., and Watt, F.M. (1990). Changes in keratinocyte adhesion during terminal differentiation: reduction in fibronectin binding precedes α5β1 integrin loss from the cell surface. Cell 63, 425-435.
2. Ali, S. (1998). Prolactin receptor regulates Stat5 tyrosine phosphorylation and nuclear translocation by two separate pathways. J. Biol. Chem. 273, 7709-7716.
3. Anbazhagan, R., Bartkova, J., Stamp, G., Pignatelli, M., Gusterson, B., and Bartek, J. (1995). Expression of integrin subunits in the human infant breast correlates with morphogenesis and differentiation. J. Pathol. 176, 227-232.
4. Aplin, A.E., Stewart, S.A., Assoian, R.K., and Juliano, R.L. (2001). Integrin-mediated adhesion regulates ERK nuclear translocation and phosphorylation of Elk-1. J. Cell Biol. 153, 273-283.
5. Barkett, M., and Gilmore, T.D. (1999). Control of apoptosis by Rel/NF-κB transcription factors. Oncogene 18, 6910-6924.
6. Bodeau, A.L., Berrier, A.L., Mastrangelo, A.M., Martinez, R., and LaFlamme, S.E. (2001). A functional comparison of mutations in integrin β cytoplasmic domains: effects on the regulation of tyrosine phosphorylation, cell spreading, cell attachment and β1 integrin conformation. J. Cell Sci. 114, 2795-2807.
7. Brakebusch, C., et al. (2000). Skin and hair follicle integrity is crucially dependent on β1 integrin expression on keratinocytes. EMBO J. 19, 3990-4003.
8. Brantley, D.M., Chen, C.L., Muraoka, R.S., Bushdid, P.B., Bradberry, J.L., Kittrell, F., Medina, D., Matrisian, L.M., Kerr, L.D., and Yull, F.E. (2001). Nuclear factor-κB (NF-κB) regulates proliferation and branching in mouse mammary epithelium. Mol. Biol. Cell 12, 1445-1455.
9. Brantley, D.M., Yull, F.E., Muraoka, R.S., Hicks, D.J., Cook, C.M., and Kerr, L.D. (2000). Dynamic expression and activity of NF-κB during post-natal mammary gland morphogenesis. Mech. Dev. 97, 149-155.
10. vβ3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 79, 1157-1164.
11. Campbell, S.M., Rosen, J.M., Hennighausen, L.G., Strech-Jurk, U., and Sippel, A.E. (1984). Comparison of the whey acidic protein genes of the rat and mouse. Nucleic Acids Res. 12, 8685-8697.
12. Clezardin, P., Frappart, L., Clerget, M., Pechoux, C., and Delmas, P.D. (1993). Expression of thrombospondin (TSP1) and its receptors (CD36 and CD51) in normal, hyperplastic, and neoplastic human breast. Cancer Res. 53, 1421-1430.
13. Clarkson, R.W., Heeley, J.L., Chapman, R., Aillet, F., Hay, R.T., Wyllie, A., and Watson, C.J. (2000). NF-κB inhibits apoptosis in murine mammary epithelia. J. Biol. Chem. 275, 12737-12742.
14. de Fougerolles, A.R., Chi-Rosso, G., Bajardi, A., Gotwals, P., Green, C.D., and Koteliansky, V.E. (2000). Global expression analysis of extracellular matrix-integrin interactions in monocytes. Immunity 13, 749-758.
15. Edwards, G.M., Wilford, F.H., Liu, X., Hennighausen, L., Djiane, J., and Streuli, C.H. (1998). Regulation of mammary differentiation by extracellular matrix involves protein-tyrosine phosphatases. J. Biol. Chem. 273, 9495-9500.
16. Faraldo, M.M., Deugnier, M.A., Lukashev, M., Thiery, J.P., and Glukhova, M.A. (1998). Perturbation of β1-integrin function alters the development of murine mammary gland. EMBO J. 17, 2139-2147.
17. Faraldo, M.M., Deugnier, M.A., Thiery, J.P., and Glukhova, M.A. (2001). Growth defects induced by perturbation of β1-integrin function in the mammary gland epithelium result from a lack of MAPK activation via the Shc and Akt pathways. EMBO Rep. 2, 431-437.
18. Furlong, E.E.M., Keon, N.K., Thornton, F.D., Rein, T., and Martin, F. (1996). Expression of a 74-kDa nuclear factor 1 (NF1) protein is induced in mouse mammary gland involution. Involution-enhanced occupation of a twin NF1 binding element in the testosterone-repressed prostate message-2/clusterin promoter. J. Biol. Chem. 271, 29688-29697.
19. Geymayer, S., and Doppler, W. (2000). Activation of NF-κB p50/p65 is regulated in the developing mammary gland and inhibits STAT5-mediated β-casein gene expression. FASEB J. 14, 1159-1170.
20. Giancotti, F.G., and Ruoslahti, E. (1999). Integrin signaling. Science 285, 1028-1032.
21. Groner, B., and Gouilleux, F. (1995). Prolactin-mediated gene activation in mammary epithelial cells. Curr. Opin. Genet. Dev. 5, 587-594.
22. Gupta, P., Rosen, J.M., D'Eustachio, P., and Ruddle, F.H. (1982). Localization of the casein gene family to a single mouse chromosome. J. Cell Biol. 93, 199-204.
23. Li, M., Liu, X., Robinson, G., Bar-Peled, U., Wagner, K.U., Young, W.S., Hennighausen, L., and Furth, P.A. (1997). Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution. Proc. Natl. Acad. Sci. USA 94, 3425-3430.
24. Liu, X., Robinson, G.W., Wagner, K.U., Garrett, L., Wynshaw-Boris, A., and Hennighausen, L. (1997). Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev. 11, 179-186.
25. Lukashev, M.E., Sheppard, D., and Pytela, R. (1994). Disruption of integrin function and induction of tyrosine phosphorylation by the autonomously expressed β1 integrin cytoplasmic domain. J. Biol. Chem. 269, 18311-18314.
26. 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 mammary gland involution: proteinase-independent and -dependent pathways. Development 122, 181-193.
27. Luo, G., and Yu-Lee, L. (2000). Stat5b inhibits NF-κB-mediated signaling. Mol. Endocrinol. 14, 114-123.
28. Marcantonio, E.E., and Hynes, R.O. (1988). Antibodies to the conserved cytoplasmic domain of the integrin β1 subunit react with proteins in vertebrates, invertebrates, and fungi. J. Cell Biol. 106, 1765-1772.
29. Mayr, S., Welte, T., Tomasi, J.K., Bruno, P., Cairns, C., Gustafsson, J., and Doppler, W. (1998). Selective coupling of STAT factors to the mouse prolactin receptor. Eur. J. Biochem. 258, 784-793.
30. Muschler, J., Lochter, A., Roskelley, C.D., Yurchenco, P., and Bissell, M.J. (1999). Division of labor among the α6β4 integrin, β1 integrins, and an E3 laminin receptor to signal morphogenesis and β-casein expression in mammary epithelial cells. Mol. Biol. Cell 10, 2817-2828.
31. Musikacharoen, T., Matsuguchi, T., Kikuchi, T., and Yoshikai, Y. (2001). NF-κB, and STAT5 play important roles in the regulation of mouse Toll-like receptor 2 gene expression. J. Immunol. 166, 4516-4524.
32. Pattengale, P.K., Stewart, T.A., Leder, A., Sinn, E., Muller, W., Tepler, I., Schmidt, E., and Leder, P. (1989). Animal models of human disease. Pathology and molecular biology of spontaneous neoplasms occurring in transgenic mice carrying and expressing activated cellular oncogenes. Am. J. Pathol. 135, 39-61.
33. Pfitzner, E., Jahne, R., Wissler, M., Stoecklin, E., and Groner, B. (1998). p300/CREB-binding protein enhances the prolactin-mediated transcriptional induction through direct interaction with the transactivation domain of Stat5, but does not participate in the Stat5-mediated suppression of the glucocorticoid response. Mol. Endocrinol. 12, 1582-1593.
34. Qwarnstrom, E.E., Ostberg, C.O., Turk, G.L., Richardson, C.A., and Bomsztyk, K. (1994). Fibronectin attachment activates the NF-κB p50/p65 heterodimer in fibroblasts and smooth muscle cells. J. Biol. Chem. 269, 30765-30768.
35. Raghavan, S., Bauer, C., Mundschau, G., Li, Q., and Fuchs, E. (2000). Conditional ablation of β1 integrin in skin. Severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J. Cell Biol. 150, 1149-1160.
36. Ramarli, D., Scupoli, M.T., Fiorini, E., Poffe, O., Brentegani, M., Villa, A., Cecchini, G., Tridente, G., and Marchisio, P.C. (1998). Thymocyte contact or monoclonal antibody-mediated clustering of α3β1 or α6β4 integrins activate interleukin-6 (IL-6) transcription factors (NF-κB and NF-IL6) and IL-6 production in human thymic epithelial cells. Blood 92, 3745-3755.
37. Shapiro, D.J., Sharp, P.A., Wahli, W.W., and Keller, M.J. (1988). A high-efficiency HeLa cell nuclear transcription extract. DNA 7, 47-55.
38. Sternlicht, M.D., and Werb, Z. (2001). How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell. Dev. Biol. 17, 463-516.
39. Strange, R., Li, F., Saurer, S., Burkhardt, A., and Friis, R.R. (1992). Apoptotic cell death and tissue remodeling during mouse mammary gland involution. Development 115, 49-58.
40. Streuli, C.H., Edwards, G.M., Delcommenne, M., Whitelaw, C.B., Burdon, T.G., Schindler, C., and Watson, C.J. (1995). Stat5 as a target for regulation by extracellular matrix. J. Biol. Chem. 270, 21639-21644.
41. 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.
42. Talhouk, R.S., Bissell, M.J., and Werb, Z. (1992). Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. J. Cell Biol. 118, 1271-1282.
43. Teglund, S., McKay, C., Schuetz, E., van Deursen, J.M., Stravopodis, D., Wang, D., Brown, M., Bodner, S., Grosveld, G., and Ihle, J.N. (1998). Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 93, 841-850.
44. Walker, N.I., Bennett, R.E., and Kerr, J.F. (1989). Cell death by apoptosis during involution of the lactating breast in mice and rats. Am. J. Anat. 185, 19-32.
45. Zutter, M.M., Mazoujian, G., and Santoro, S.A. (1990). Decreased expression of integrin adhesive protein receptors in adenocarcinoma of the breast. Am. J. Pathol. 137, 863-870.