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

Journal of Cell Biology

Volumn 125, Issue 3, 1994, Pages 681-693

  Sympson, Carolyn J ^a,b   Talhouk, Rabih S ^a,b,c   Alexander, Caroline M ^b   Chin, Jennie R ^b   Clift, Shirley M ^a,d   Bissell, Mina J ^a   Werb, Zena ^b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^d CELL GENESYS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; MUS MUSCULUS;

BETA CASEIN; COLLAGEN TYPE 4; LAMININ; STROMELYSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CELL; CONTROLLED STUDY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION; INVOLUTION; LACTATION; MAMMARY GLAND FUNCTION; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; TISSUE SPECIFICITY;

ANIMAL; BASE SEQUENCE; BASEMENT MEMBRANE; CASEINS; CELL DIFFERENTIATION; COLLAGEN; DNA PRIMERS; FEMALE; GENE EXPRESSION REGULATION; GENES, STRUCTURAL; LACTATION; LAMININ; MAMMAE; METALLOENDOPEPTIDASES; MICE; MICE, TRANSGENIC; MILK PROTEINS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; PREGNANCY; PROMOTER REGIONS (GENETICS); RESTRICTION MAPPING; STROMELYSIN 1; SUPPORT, U.S. GOV'T, NON-P.H.S.; SUPPORT, U.S. GOV'T, P.H.S.;

EID: 0028302990     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.125.3.681     Document Type: Article

References (59)

1. Adams, J. C., and F. M. Watt. 1993. Regulation of development and differentiation by the extracellular matrix. Development. 117:1183-1198.
2. Adams, J. M., and S. Cory. 1991. Transgenic models of tumor development. Science (Wash. DC). 254:1161-1167.
3. Alexander, C. M., and Z. Werb. 1991. Extracellular matrix degradation. In Cell Biology of Extracellular Matrix. 2nd Edition. E. D. Hay, editor. Plenum Publishing Co., New York. 255-302.
4. Bernfield, M., S. D. Banerjee, J. E. Koda, and A. C. Rapraeger. 1984. Remodeling of the basement membrane as a mechanism of morphogenetic tissue interaction. In The Role of Extracellular Matrix in Development. R. Trelstad, editor. Alan R. Liss, New York. 545-572.
5. Bernfield, M., R. Kokenyesi, M. Kato, M. T. Hinkes, J. Spring, R. L. Gallo, and E. J. Lose. 1992. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 8:365-393.
6. Birkedal-Hansen, H., W. G. I. Moore, M. K. Bodden, L. J. Windsor, B. Birkedal-Hansen, A. DeCarlo, and J. A. Engler. 1993. Matrix metallopro teinases: A review. Crit. Rev. Oral Biol. Med. 4:197-250.
7. Bissell, M. J. 1981. The differentiated state of normal and malignant cells or how to define a 'normal' cell in culture. Intern. Rev. Cytol. 70:27-100.
8. Bissell, M. J., H. G. Hall, and G. Parry. 1982. How does the extracellular ma trix direct gene expression? J. Theor. Biol. 99:31-68.
9. Blau, H. M. 1992. Differentiation requires continuous active control. Annu. Rev. Biochem. 61:1213-1230.
10. Campbell, S. M., J. M. Rosen, L. G. Hennighausen, U. Strech-Jurk, and A. E. Sippel. 1984. Comparison of the whey acidic protein genes of the rat and mouse. Nucleic Acids Res. 12:8685-8697.
11. Chen, L-H., and M. J. Bissell. 1989. A novel regulatory mechanism for whey acidic protein gene expression. Cell Regul. 1:45-54.
12. Chin, J. R., G. Murphy, and Z. Werb. 1985. Stromelysin, a connective tissuedegrading metalloendopeptidase secreted by stimulated rabbit synovial fibro blasts in parallel with collagenase. Biosynthesis, isolation, characterization, and substrates. J. Biol. Chem. 260:12367-12376.
13. Dale, T. C., M. J. Krnacik, C. Schmidhauser, C. L. Yang, M. J. Bissell, and J. M. Rosen. 1992. High-level expression of the rat whey acidic protein gene is mediated by elements in the promoter and 31/2 untranslated region. Mol. Cell. Biol. 12:905-914.
14. Damsky, C. H., and Z. Werb. 1992. Signal transduction by integrin receptors for extracellular matrix: cooperative processing of extracellular information. Curr. Opin. Cell Biol. 4:772-781.
15. Daniel, C. W., and G. B. Silberstein. 1987. Postnatal development of the rodent mammary gland. In The Mammary Gland: Development, Regulation and Function. M. C. Neville and C. W. Daniel, editors. Plenum Publishing Corp., New York. 3-36.
16. Daniel, C. W., G. B. Silberstein, K. Van Horn, P. Strickland, and S. Robinson. 1989. TGF-β1-induced inhibition of mouse mammary ductal growth: developmental specificity and characterization. Dev. Biol. 135:20-30.
17. D'Armiento, J., S. S. Dalal, Y. Okada, R. A. Berg, and K. Chada. 1992. Col lagenase expression in the lungs of transgenic mice causes pulmonary emphysema. Cell. 71:955-961.
18. Dickson, R. B., M. M. Gottardis, and G. T. Merlino. 1991. Molecular insights into breast cancer from transgenic mouse models. Bioessays. 13:591-596.
19. Dickson, S. R., and M. J. Warburton. 1992. Enhanced synthesis of gelatinase and stromelysin in myoepithelial cells during involution of the rat mammary gland. J. Histochem. Cytochem. 40:697-703.
20. Edwards, P. A. W., S. E. Hiby, J. Papkoff, and J. M. Bradbury. 1992. Hyperplasia of mouse mammary epithelium induced by expression of the Wnt-1 (int-1) oncogene in reconstituted mammary gland. Oncogene. 7:2041-2051.
21. Ferguson, J. E., A. M. Schor, A. Howell, and M. W. J. Ferguson. 1992. Changes in the extracellular matrix of the normal human breast during the menstrual cycle. Cell Tissue Res. 268:167-177.
22. Fielder, P. J., G. Thordarson, A. English, R. G. Rosenfeld, and F. Talamantes. 1992. Expression of a lactogen-dependent insulin-like growth-factor-binding protein in cultured mouse mammary epithelial cells. Endocrinology. 131: 261-267.
23. Flaumenhaft, R., and D. B. Rifkin. 1991. Extracellular matrix regulation of growth factor and protease activity. Curr. Opin. Cell Biol. 3:817-823.
24. Forsyth, I. A. 1991. The mammary gland. Baillieres Clin. Endo. Metab. 5:809-832.
25. Fukuda, Y., Y. Masuda, J. Kishi, Y. Hashimoto, T. Hayakawa, H. Nogawa, and Y. Nakanishi. 1988. The role of interstitial collagens in cleft formation of mouse embryonic submandibular gland during initial branching. Development. 103:259-267.
26. Gavin, B. J., and A. P. McMahon. 1992. Differential regulation of the Wnt gene family during pregnancy and lactation suggests a role in postnatal development of the mammary gland. Mol. Cell. Biol. 12:2418-2423.
27. Grobstein, C. 1954. Tissue interaction in the morphogenesis of mouse embryonic rudiments in vitro. In Aspects of Synthesis and Order in Growth. D. Rudnick, editor. Princeton University Press, Princeton, NJ. 233-256.
28. Gunzburg, W. H., B. Salmons, B. Zimmerman, M. Muller, V. Erfle, and G. Brem. 1991. A mammary-specific promoter directs expression of growth hormone not only to the mammary gland, but also to Bergman glia cells in transgenic mice. Mol. Endocrinol. 5:123-133.
29. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 353-355.
30. Hay, E. D. 1993. Extracellular matrix alters epithelial differentiation. Curr. Opin. Cell Biol. 5:1029-1035.
31. Heckel, J. L., E. P. Sandgren, J. L. Degen, R. D. Palmiter, and R. L. Brinster. 1990. Neonatal bleeding in transgenic mice expressing urokinase-type plasminogen activator. Cell. 62:447-456.
32. Hennighausen, L., C. Westphal, L. Sankaran, and C. W. Pittius. 1991. Regulation of expression of genes for milk proteins. Biotechnology. 16:65-74.
33. Hogan, B., F. Costantini, and E. Lacy. 1986. Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 79-204.
34. Jones, J. I., A. Gockerman, W. H. Busby Jr., C. Camacho-Hubner, and D. R. Clemmons. 1993. Extracellular matrix contains insulin-like growth factor binding protein-5: potentiation of the effects of IGF-I. J. Cell Biol. 121: 679-687.
35. Juliano, R. L., and S. Haskill. 1993. Signal transduction from the extracellular matrix. J. Cell Biol. 120:577-585.
36. Knight, C. H., and M. Peaker. 1982. Development of the mammary gland. J. Reprod. Fertil. 65:521-536.
37. Lee, E. Y.-H., W.-H. Lee, C. S. Kaetzel, G. Parry, and M. J. Bissell. 1985. Interaction of mouse mammary epithelial cells with collagen substrata: Regulation of casein gene expression and secretion. Proc. Natl. Acad. Sci. USA. 82:1419-1423.
38. Lefebvre, O., C. Wolf, J. M. Limacher, P. Hutin, C. Wendling, M. Le Meur, P. Basset, and M. C. Rio. 1992. The breast cancer-associated stromelysin-3 gene is expressed during mouse mammary gland apoptosis. J. Cell Biol. 119:997-1002.
39. Lin, C. Q., and M. J. Bissell. 1993. Multi-faceted regulation of cell differentiation by extracellular matrix. FASEB (Fed. Am. Soc. Exp. Biol.) J. 7:737-743.
40. Matrisian, L. M. 1990. Metalloproteinases and their inhibitors in matrix re-modeling. Trends Genet. 6:121-125.
41. Medina, D. 1973. Preneoplastic lesions in mouse mammary tumorigenesis. Methods Cancer Res. 7:3-53.
42. Mignatti, P., and D. B. Rifkin. 1993. Biology and biochemistry of proteinases in tumor invasion. Physiol. Rev. 73:161-195.
43. Nakhasi, H. L., and P. K. Quasba. 1979. Quantitation of milk proteins and their mRNAs in rat mammary gland at various stages of gestation and lactation. J. Biol. Chem. 254:6016-6025.
44. Park, A. J., L. M. Matrisian, A. F. Kell, R. Pearson, Z. Y. Yuan, and M. Navre. 1991. Mutational analysis of the transin (rat stromelysin) autoinhibitor region demonstrates a role for residues surrounding the "cysteine switch." J. Biol. Chem. 266:1584-1590.
45. Pittius, C. W., L. Sankaran, Y. J. Topper, and L. Hennighausen. 1988. Comparison of the regulation of the whey acidic protein gene with that of a hybrid gene containing the whey acidic protein gene promoter in transgenic mice. Mol. Endocrin. 2:1027-1032.
46. Reddy, S. T., A. W. Stoker, and M. J. Bissell. 1991. Expression of Rous sarcoma virus-derived retroviral vectors in the avian blastoderm: potential as stable genetic markers. Proc. Natl. Acad. Sci. USA. 88:10505-10509.
47. Richards, D. A., J. R. Rodgers, S. C. Supowit, and J. M. Rosen. 1981. Construction and preliminary characterization of the rat casein and α-lactalbumin cDNA clones. J. Biol. Chem. 256:526-532.
48. Sanchez-Lopez, R., R. Nicholson, M. C. Gesnel, L. M. Matrisian, and R. Breathnach. 1988. Structure-function relationships in the collagenase family member transin. J. Biol. Chem. 263:11892-11899.
49. Schmidhauser, C., G. F. Casperson, C. A. Myers, K. T. Sanzo, S. Bolten, and M. J. Bissell. 1992. A novel transcriptional enhancer is involved in the prolactin- and extracellular matrix-dependent regulation of β-casein gene expression. Mol. Biol. Cell. 3:699-709.
50. Schmidt, J. W., P. A. Piepenhagen, and W. J. Nelson. 1993. Modulation of epithelial morphogenesis and cell fate by cell-to-cell signals and regulated cell adhesion. Sem. Cell Biol. 4:161-173.
51. Shackleford, G. M., C. A. MacArthur, H. C. Kwan, and H. E. Varmus. 1993. Mouse mammary tumor virus infection accelerates mammary carcinogenesis in Wnt-1 transgenic mice by insertional activation of int-2/Fgf-3 and hst/Fgf-4. Proc. Natl. Acad. Sci. USA. 90:740-744.
52. Silberstein, G. B., K. C. Flanders, A. B. Roberts, and C. W. Daniel. 1992. Regulation of mammary morphogenesis: evidence for extracellular matrix-mediated inhibition of ductal budding by transforming growth factor-β1. Dev. Biol. 152:354-362.
53. Strange, R., F. Li, S. Saurer, A. Burkhardt, and R. R. Friis. 1992. Apoptotic cell death and tissue remodelling during mouse mammary gland involution. Development. 115:49-58.
54. Streuli, C. H., N. Bailey, and M. J. Bissell. 1991. Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. J. Cell Biol. 115:1383-1395.
55. Talhouk, R. S., J. R. Chin, E. N. Unemori, Z. Werb, and M. J. Bissell. 1991. Proteinases of the mammary gland: developmental regulation in vivo and vectorial secretion in culture. Development. 112:439-449.
56. Talhouk, R. S., M. J. Bissell, and Z. Werb. 1992. Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. J. Cell Biol. 118:1271-1282.
57. Tsukamoto, A. S., R. Grosschedl, R. C. Guzman, T. Parslow, and H. E. Varmus, 1988. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell. 55:619-625.
58. Wilhelm, S. M., D. Wunderlich, C. A. Maniglia, A. Z. Eisen, and G. I. Goldberg. 1992. Primary structure and function of stromelysin/transin in cartilage matrix turnover. Matrix Suppl. 1:37-44.
59. Zhou, J., T. Mochizuki, H. Smeets, C. Antignac, P. Laurila, A. de Paepe, K. Tryggvason, and S. T. Reeders. 1993. Deletion of the paired α5 (IV) and α6 (IV) collagen genes in inherited smooth muscle rumors. Science (Wash. DC). 261:1167-1169.