J. Cell Biol.
© The Rockefeller University Press
0021-9525/97/04/231/15 $2.00
Volume 137, Number 1, April 7, 1997 231-245

Reversion of the Malignant Phenotype of Human Breast Cells in Three-Dimensional Culture and In Vivo by Integrin Blocking Antibodies

V.M. Weaver,^* O.W. Petersen, F. Wang,^* C.A. Larabell,^* P. Briand,^§ C. Damsky, and M.J. Bissell^*

^* Ernest Orlando Lawrence Berkeley National Laboratory, Berkeley, California 94720;  Structural Cell Biology Unit, Institute of Medical Anatomy, The Panum Institute, DK-2200 Copenhagen N, Denmark; ^§ Department of Tumor Endocrinology, Division of Cancer Biology, Danish Cancer Society, DK-2100, Copenhagen O, Denmark; and  Departments of Stomatology and Anatomy, University of California, San Francisco, California 94143

In a recently developed human breast cancer model, treatment of tumor cells in a 3-dimensional culture with inhibitory 1-integrin antibody or its Fab fragments led to a striking morphological and functional reversion to a normal phenotype. A stimulatory 1-integrin antibody proved to be ineffective. The newly formed reverted acini re-assembled a basement membrane and re-established E-cadherin-catenin complexes, and re-organized their cytoskeletons. At the same time they downregulated cyclin D1, upregulated p21^cip,waf-1, and stopped growing. Tumor cells treated with the same antibody and injected into nude mice had significantly reduced number and size of tumors in nude mice. The tissue distribution of other integrins was also normalized, suggesting the existence of intimate interactions between the different integrin pathways as well as adherens junctions. On the other hand, nonmalignant cells when treated with either 6 or 4 function altering antibodies continued to grow, and had disorganized colony morphologies resembling the untreated tumor colonies. This shows a significant role of the 6/4 heterodimer in directing polarity and tissue structure. The observed phenotypes were reversible when the cells were disassociated and the antibodies removed. Our results illustrate that the extracellular matrix and its receptors dictate the phenotype of mammary epithelial cells, and thus in this model system the tissue phenotype is dominant over the cellular genotype.

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• Aikawa, R., Nagai, T., Kudoh, S., Zou, Y., Tanaka, M., Tamura, M., Akazawa, H., Takano, H., Nagai, R., Komuro, I. (2002). Integrins Play a Critical Role in Mechanical Stress-Induced p38 MAPK Activation. Hypertension 39: 233-238 [Abstract] [Full Text]  
• Schreider, C., Peignon, G., Thenet, S., Chambaz, J., Pincon-Raymond, M. (2002). Integrin-mediated functional polarization of Caco-2 cells through E-cadherin--actin complexes. J. Cell Sci. 115: 543-552 [Abstract] [Full Text]  
• Bhowmick, N. A., Zent, R., Ghiassi, M., McDonnell, M., Moses, H. L. (2001). Integrin beta 1 Signaling Is Necessary for Transforming Growth Factor-beta Activation of p38MAPK and Epithelial Plasticity. J. Biol. Chem. 276: 46707-46713 [Abstract] [Full Text]  
• Seewaldt, V. L., Mrozek, K., Sigle, R., Dietze, E. C., Heine, K., Hockenbery, D. M., Hobbs, K. B., Caldwell, L. E. (2001). Suppression of p53 function in normal human mammary epithelial cells increases sensitivity to extracellular matrix-induced apoptosis. J. Cell Biol. 155: 471-486 [Abstract] [Full Text]  
• Simian, M., Hirai, Y., Navre, M., Werb, Z., Lochter, A., Bissell, M. J. (2001). The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development 128: 3117-3131 [Abstract] [Full Text]  
• 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., Yull, F. E. (2001). Nuclear Factor-{kappa}B (NF-{kappa}B) Regulates Proliferation and Branching in Mouse Mammary Epithelium. Mol. Biol. Cell 12: 1445-1455 [Abstract] [Full Text]  
• Potter, J. D. (2001). Morphostats: A Missing Concept in Cancer Biology. Cancer Epidemiol. Biomarkers Prev. 10: 161-170 [Abstract] [Full Text]  
• Reeves, R., Edberg, D. D., Li, Y. (2001). Architectural Transcription Factor HMGI(Y) Promotes Tumor Progression and Mesenchymal Transition of Human Epithelial Cells. Mol. Cell. Biol. 21: 575-594 [Abstract] [Full Text]  
• Somasiri, A, Howarth, A, Goswami, D, Dedhar, S, Roskelley, C. (2001). Overexpression of the integrin-linked kinase mesenchymally transforms mammary epithelial cells. J. Cell Sci. 114: 1125-1136 [Abstract]  
• Lamb, J., Ladha, M. H., McMahon, C., Sutherland, R. L., Ewen, M. E. (2000). Regulation of the Functional Interaction between Cyclin D1 and the Estrogen Receptor. Mol. Cell. Biol. 20: 8667-8675 [Abstract] [Full Text]  
• Cambier, S., Mu, D.-z., O’Connell, D., Boylen, K., Travis, W., Liu, W.-h., Broaddus, V. C., Nishimura, S. L. (2000). A Role for the Integrin {{alpha}}v{beta}8 in the Negative Regulation of Epithelial Cell Growth. Cancer Res. 60: 7084-7093 [Abstract] [Full Text]  

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