Skip to main content
SpringerLink
Log in

Functional interplay between extracellular matrix and extracellular matrix-degrading proteinases in the mammary gland: a coordinate system for regulating mammary epithelial function

  • Chapter
Epithelial Organization and Development

Abstract

A critical question in biology is how the organization of epithelial cells is regulated and how tissue-specific gene expression is maintained. It is now evident that, in addition to soluble factors such as hormones and growth factors, the interaction of an epithelial cell with its micro-environment and with adjacent cells is critical in regulating tissue specificity. Earlier studies showed an inductive role of mesenchyme on epithelial growth and organization. In a classic study, Kratchowil (1969) showed that mammary epithelium recombined with salivary mesenchyme developed a growth pattern typical of the salivary rather than the mammary gland, indicating that the inducing mesenchyme had an instructive role in tissue morphogenesis. Based on accumulating literature in the intervening years, it was proposed that the extracellular matrix (ECM) may be an important player in such regulation (Bissell et al., 1982). Many components of the cell microenvironment, including the ECM molecules, have now been defined and characterized (Talhouk et al., 1991a). In addition, recent studies (reviewed by Stoker et al., 1990; Watt, 1991) have described a role for the ECM in directing or maintaining epithelial tissue-specific gene expression in culture.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aggeier, J., Ward, J., Mackenzie Blackie, L., Barcellos-Hoff, M.H., Streuli, C.H. and Bissell, M.J. (1991) Cytodifferentiation of mouse mammary epithelial cells cultured on a reconstituted basement membrane reveals striking similarities to development in vivo. J. Cell Sci., 99, 407–18.

    Google Scholar 

  • Akers, R.M. (1990) Lactation physiology: a ruminant animal perspective. Protoplasma, 159, 96–111.

    Article  Google Scholar 

  • Alexander, C.M. and Werb, Z. (1989) Proteinases and extracellular matrix remodeling. Curr. Op. Cell Biol., 1, 974–82.

    Article  PubMed  CAS  Google Scholar 

  • Alexander, C.M. and Werb, Z. (1991) Extracellular matrix degradation, in Cell Biology of Extracellular Matrix (ed. E.D. Hay), Plenum Press, New York, pp. 255–302.

    Chapter  Google Scholar 

  • Barcellos-Hoff, M.H., Aggeler, J., Ram, T.G. and Bissell, M.J. (1989) Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development, 105, 223–35.

    PubMed  CAS  Google Scholar 

  • Beers, W.H., Strickland, S. and Reich, E. (1975) Ovarian plasminogen activator, relationship to ovulation and hormonal regulation. Cell, 6, 387–94.

    Article  PubMed  CAS  Google Scholar 

  • Bissell, M.J., Hall, H.G. and Parry, G. (1982) How does the extracellular matrix direct gene expression? J. Theor. Biol., 99, 31–68.

    Article  PubMed  CAS  Google Scholar 

  • Blum, J.L., Zeigler, M.E. and Wicha, M.S. (1987) Regulation of rat mammary gene expression by extracellular matrix components. Exp. Cell Res., 173, 322–40.

    Article  PubMed  CAS  Google Scholar 

  • Brenner, C.A., Adler, R.R., Rappolee, D.A., Pederson, R.A. and Werb, Z. (1989) Genes for extracellular matrix-degrading metalloproteinases and their inhibitor, TIMP, are expressed during early mammalian development. Genes Devel., 3, 848–59.

    Article  PubMed  CAS  Google Scholar 

  • Chen, L.-H. and Bissell, M.J. (1989) A novel regulatory mechanism for whey acidic protein gene expression, alveoli-like structures allow expression by sequestering or preventing production of diffusible inhibitor. J. Cell Regul., 1, 45–54.

    CAS  Google Scholar 

  • Coleman, S. and Daniel, C.W. (1990) Inhibition of mouse mammary ductal morphogenesis and down-regulation of the EGF receptor by epidermal growth factor. Devl Biol., 137, 425–33.

    Article  CAS  Google Scholar 

  • Daniel, C.W. and Silberstein, G.B. (1987) Postnatal development of the rodent mammary gland, in The Mammary Gland: development regulation and function (eds M.C. Neville and C.W. Daniel), Plenum Publishing Corp., New York, pp. 3–36.

    Google Scholar 

  • Daniel, C.W., Silberstein, G.B., Van-Horn, K., Strickland, P. and Robinson, S. (1989) TGF-β-1 induced inhibition of mouse mammary ductal growth: developmental specificity and characterization. Devl Biol., 134, 20–30.

    Article  Google Scholar 

  • Ebner, K.E., Hoover, C.R., Hageman, E.C. and Larson, B.L. (1961) Cultivation and properties of bovine mammary cell cultures. Expl Cell Res., 23, 373–85.

    Article  CAS  Google Scholar 

  • Ekblom, P., Vestweber, D. and Kemler, R. (1986) Cell-matrix interactions and cell adhesions during development. A. Rev. Cell Biol., 2, 27–47.

    Article  CAS  Google Scholar 

  • Emerman, J.T. and Pitelka, D.R. (1977) Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro, 13, 316–28.

    Article  PubMed  CAS  Google Scholar 

  • Emerman, J.T., Bartley, J.C. and Bissell, M.J. (1981) Glucose metabolite patterns as markers of functional differentiation in freshly isolated and cultured mouse mammary epithelial cells. Expl Cell Res., 134, 241–50.

    Article  CAS  Google Scholar 

  • Ervin, P.R., Kaminski, M.S., Cody, R.L. and Wicha, M.S. (1989) Production of mammostatin, a tissue-specific growth inhibitor, by normal human mammary cells. Science, 244, 1585–7.

    Article  PubMed  CAS  Google Scholar 

  • Ferguson, J.E., Schor, A.M., Howell, A. and Ferguson, M.W. (1990) Tenascin distribution in the normal human breast is altered during the menstrual cycle and in carcinoma. Differentiation, 42, 199–207.

    Article  PubMed  CAS  Google Scholar 

  • Frisch, S.M. and Werb, Z. (1989) Molecular biology of collagen degradation, in Collagen, Vol. IV, Molecular Biology (eds B.R. Olsen and M.E. Nimni), CRC Press, Boca Raton, FL, pp. 85–107.

    Google Scholar 

  • Haeuptle, M.-T., Suard, Y.L.M., Bogenmann, E., Reggio, H., Racine, L. and Kraehenbuhl, J.-P. (1983) Effect of cell shape change on the function and differentiation of rabbit mammary cells in culture. J. Cell Biol., 96, 1425–34.

    Article  PubMed  CAS  Google Scholar 

  • Haslam, S.Z. (1991) Stromal—epithelial interactions in normal and neoplastic mammary gland. Cancer Treat. Res., 53, 401–20.

    Article  PubMed  CAS  Google Scholar 

  • Hennighausen, L. (1990) The mammary gland as a bioreactor: production of foreign proteins in milk. Protein Expression and Purification, 1, 3–8.

    Article  PubMed  CAS  Google Scholar 

  • Howeedy, A.A., Virtanen, I., Laitinen, L., Gould, N.S., Koukoulis, G.K. and Gould, V.E. (1990) Differential distribution of tenascin in the normal, hyperplastic and neoplastic breast, Lab. Inv., 63, 798–806.

    CAS  Google Scholar 

  • Howlett, R.A. and Bissell, M.J. (1990) Regulation of mammary epithelial cell function: a role for stromal and basement membrane matrices. Protoplasma, 159, 85–95.

    Article  Google Scholar 

  • Howlett, R.A. and Bissell, M.J. (1992) The influence of tissue micro-environment, stroma and extracellular matrix, on the development and function of mammary epithelium. Epithelial Cell Biol., in press.

    Google Scholar 

  • Ingber, D.E. and Folkman, J. (1989) How does extracellular matrix control capillary morphogenesis? Cell, 58, 803–5.

    Article  PubMed  CAS  Google Scholar 

  • Knight, C.H. and Peaker, M. (1982) Development of the mammary gland. J. Reprod. Fert., 65, 521–36.

    Article  CAS  Google Scholar 

  • Kratchowil, K. (1969) Organ specificity in mesenchymal induction demonstrated in the embryonic development of the mammary gland of the mouse. Devl Biol., 20, 46–71.

    Article  Google Scholar 

  • Lascelles, A.K. and Lee, C.S. (1978) Involution of the mammary gland, in The Mammary Gland/Human Lactation/Milk Synthesis, Vol. IV (ed. B. L. Larson), Academic Press, New York, pp. 115–72.

    Google Scholar 

  • Lee, E.Y.-H., Lee, W.-H., Kaetzel, C.S., Parry, G. and Bissell, M.J. (1985) Interaction of mouse mammary epithelial cells with collagenous substrata: regulation of casein gene expression and secretion. Proc. Natn. Acad. Sci. U.S.A., 82, 1419–23.

    Article  CAS  Google Scholar 

  • Lee, E.Y.-H., Parry, G. and Bissell, M.J. (1984) Modulation of secreted proteins of mouse mammary epithelial cells by the extracellular matrix. J. Cell Biol., 98, 146–55.

    Article  PubMed  CAS  Google Scholar 

  • Li, M.L., Aggeler, J., Farson, D., Hatier, C., Hassell, J. and Bissell, M.J. (1987) Influence of a reconstituted basement membrane and its components on casein expression and secretion in mouse mammary epithelial cells. Proc. Natn. Acad. Sci. U.S.A., 84, 136–40.

    Article  CAS  Google Scholar 

  • Liotta, L. (1986) Tumor invasion and metastases — role of the extracellular matrix. Rhoads Memorial Award lecture. Cancer Res., 46, 1–7.

    Article  PubMed  CAS  Google Scholar 

  • Lyons, J.G., Siew, K. and O’Grady, R.L. (1989) Cellular interactions determining the production of collagenase by a rat mammary carcinoma cell line. Int. J. Cancer, 43, 119–25.

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Hernandez, A., Fink, L.M. and Pierce, G.B. (1976) Removal of basement membrane in the involuting breast. Lab. Invest., 31, 455–62.

    Google Scholar 

  • Matrisian, L.M. (1990) Metalloproteinases and their inhibitors in matrix remodelling. Trends Genetics, 6, 121–5.

    Article  CAS  Google Scholar 

  • Michalopoulus, G. and Pitot, H.C. (1975) Primary cultures of parenchymal liver cells on collagen membranes. Expl Cell Res., 94, 70–8.

    Article  Google Scholar 

  • Monaghan, P., Warburton, M.J., Perusinghe, N. and Rudland, P.S. (1983) Topographical arrangement of basement membrane proteins in lactating rat mammary gland: comparison of the distribution of type IV collagen, laminin, fibronectin, and Thy-1 at the ultra structural level. Proc. Natn. Acad. Sci. U.S.A., 80, 3344–8.

    Article  CAS  Google Scholar 

  • Monteagudo, C., Merino, M.J., San-Juan, J., Liotta, L.A. and Stetler-Stevenson, W.G. (1990) Immunohistochemical distribution of type IV collagenase in normal, benign, and malignant breast tissue. Am. J. Path., 136, 585–92.

    PubMed  CAS  Google Scholar 

  • Neville, M.C. (1987) Mammary cultures on floating gels: a model system for mammary function. News Physiol. Sci., 2, 107–11.

    CAS  Google Scholar 

  • Nicholson, L.J. and Watt, F.M. (1991) Decreased expression of fibronectin and the α5β1 integrin during terminal differentiation of human keratinocytes. J. Cell Sci., 98, 225–32.

    PubMed  CAS  Google Scholar 

  • Ossowski, L. (1988) Plasminogen activator dependent pathways in the dissemination of human tumor cells in the chick embryo. Cell, 52, 321–8.

    Article  PubMed  CAS  Google Scholar 

  • Ossowski, L., Biegel, D. and Reich, E. (1979) Mammary plasminogen activator: correlation with involution, hormonal modulation and comparison between normal and neoplastic tissue. Cell, 16, 929–40.

    Article  PubMed  CAS  Google Scholar 

  • Ozello, L. (1970) Epithelial-stromal junction of normal and dysplastic mammary glands. Cancer, 25, 586–600.

    Article  Google Scholar 

  • Perris, R. and Bronner-Fraser, M. (1989) Recent advances in defining the role of the extracellular matrix in neural crest development. Comm. Dev. Neurobiol., 1, 61–83.

    Google Scholar 

  • Rodriguez-Boulan, E. and Nelson, W.J. (1989) Morphogenesis of the polarized epithelial cell phenotype. Science, 245, 718–25.

    Article  PubMed  CAS  Google Scholar 

  • Schmidhausen C, Bissell, M.J., Myers, C.A. and Casperson, G.F. (1990) Extracellular matrix and hormones transcriptionally regulate bovine β-casein 5′ sequences in stably transfected mouse mammary cells. Proc. Natn. Acad. Sci. U.S.A., 87, 9118–22.

    Article  Google Scholar 

  • Schmidhausen C, Casperson, G.F., Myers, CA., Bolten, S. and Bissell, M.J. (1992) A novel transcriptional enhancer is involved in the prolactin and ECM-dependent regulation of β-casein gene expression. Mol. Biol. Cell (in press).

    Google Scholar 

  • Schmidt, G.H. (1971) Mammary gland involution, in Biology of Lactation (ed. G.W. Salisbury), W.H. Freeman, San Fransisco, CA, pp. 137–48.

    Google Scholar 

  • Silberstein, G.B. and Daniel, C.W. (1982) Glycosaminoglycans in the basal lamina and extracellular matrix of the developing mouse mammary duct. Devl Biol., 90, 215–22.

    Article  CAS  Google Scholar 

  • Simons, J.P., McClenaghan, M. and Clark, A.J. (1987) Alteration of the quality of milk by expression of sheep β-lactoglobulin in transgenic mice. Nature, 328, 530–2.

    Article  PubMed  CAS  Google Scholar 

  • Sloane, B.F., Rozhin, J., Johnson, K., Taylor, H., Crissman, J.D. and Honn, K. (1986) Cathepsin B, association with plasma membrane in metastatic tumors. Proc. Natn. Acad. Sci. U.S.A., 83, 2483–7.

    Article  CAS  Google Scholar 

  • Stoker, A.W., Streuli, C.H., Martins-Green, M. and Bissell, M.J. (1990) Designer microenvironments for the analysis of cell and tissue function. Curr. Op. Cell Biol., 2, 864–74.

    Article  PubMed  CAS  Google Scholar 

  • Streuli, C.H. and Bissell, M J. (1990a) Expression of extracellular matrix components is regulated by substratum. J. Cell Biol., 110, 1405–15.

    Article  PubMed  CAS  Google Scholar 

  • Streuli, C.H. and Bissell, M.J. (1990b) Mammary epithelial cells, extracellular matrix and gene expression, in Breast Cancer: cellular and molecular biology, Vol. 2 (eds M.E. Lippman and R. Dickson), Kluwer Academic Publishers, Boston, pp. 365–81.

    Google Scholar 

  • Streuli, C.H., Bailey, N. and Bissell, M.J. (1991) Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interactions and morphological polarity. J. Cell Biol., 115, 1383–95.

    Article  PubMed  CAS  Google Scholar 

  • Takeichi, M. (1991) Cadherin cell adhesion receptors as a morphogenetic regulator. Science, 251, 1451–5.

    Article  PubMed  CAS  Google Scholar 

  • Talhouk, R.S., Alexander, C.M., Clift, S.M., Sympson, C.J., Bissell, M.J. and Werb, Z. (1991c) A critical balance between ECM-degrading proteinases and their inhibitors regulates tissue specific function. J. Cell Biol., 115, 137a.

    Google Scholar 

  • Talhouk, R.S., Bissell, M.J. and Werb, Z. (1990) Expression of extracellular matrix-degrading proteinases and their inhibitors during involution of the mammary gland of CD-1mice. J. Cell Biol., 111, 14a (abstract).

    Google Scholar 

  • 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., (in press).

    Google Scholar 

  • Talhouk, R.S., Chin, J.R., Unemori, E.N., Werb, Z. and Bissell, M.J. (1991b) Proteinases of the mammary gland: developmental regulation in vivo and vectorial secretion in culture. Development, 112, 439–49.

    PubMed  CAS  Google Scholar 

  • Talhouk, R.S., Streuli, C.H., Barcellos-Hoff, M.H. and Bissell, M.J. (1991a) The extracellular matrix, in Fundamentals of Medical Cell Biology (ed. E.E. Bittar), JAI Press Inc., Greenwich, Connecticut, vol. 2, pp. 137–78.

    Google Scholar 

  • Thiery, J.P., Duband, J.-L., Dufour, S., Savanger, P. and Imhof, B.A. (1988) Roles of fibronectin in embryogenesis, in Fibronectin (ed. D.F. Mosher) Academic Press, New York, pp. 181-212.

    Google Scholar 

  • Warburton, M.J., Mitchell, D., Ormerod, E.J. and Rudland, P. (1982) Distribution of myoepithelial cells and basement membrane proteins in the resting, pregnant, lactating, and involuting rat mammary gland. J. Histochem. Cytochem., 30, 667–76.

    Article  PubMed  CAS  Google Scholar 

  • Watt, F.M. (1991) Cell culture models of differentiation. FASEB J., 5, 287–94.

    PubMed  CAS  Google Scholar 

  • Wicha, M.S., Liotta, L.A., Vonderhaar, B.K. and Kidwell, W.R. (1980) Effects of inhibition of basement membrane collagen deposition on rat mammary gland development. Devl Biol., 80, 253–66.

    Article  CAS  Google Scholar 

  • Wilde, C.J., Knight, C.H., Addey C.V.P. et al. (1990) Autocrine regulation of mammary cell differentiation. Protoplasma, 159, 112–17.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Radiobiology and Environmental Health, University of California, USA

    Zena Werb

  2. Division of Cell and Molecular Biology, Lawrence Berkeley Laboratory, USA

    Rabih S. Talhouk & Mina J. Bissell

Authors
  1. Rabih S. Talhouk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zena Werb
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mina J. Bissell
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Biology, School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton, SO9 3TU, UK

    Tom P. Fleming

Rights and permissions

Reprints and permissions

Copyright information

© 1992 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Talhouk, R.S., Werb, Z., Bissell, M.J. (1992). Functional interplay between extracellular matrix and extracellular matrix-degrading proteinases in the mammary gland: a coordinate system for regulating mammary epithelial function. In: Fleming, T.P. (eds) Epithelial Organization and Development. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-2354-9_12

Download citation

  • DOI: https://doi.org/10.1007/978-94-011-2354-9_12

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-5040-1

  • Online ISBN: 978-94-011-2354-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation