Transcriptional regulation of stromelysin-1 gene expression is altered during progression of mouse mammary epithelial cells from functionally normal to malignant

Matrix Biology

Volumn 18, Issue 5, 1999, Pages 455-467

  Lochter, André ^a   Werb, Zena ^b   Bissell, Mina J ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Actin; Breast cancer; Matrix metalloproteinases; Promoter

Indexed keywords

METALLOPROTEINASE; STROMELYSIN;

ANIMAL CELL; ARTICLE; BREAST DEVELOPMENT; BREAST EPITHELIUM; CELL CULTURE; CELL TRANSFORMATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENETIC TRANSFECTION; IN VITRO STUDY; MOLECULAR CLONING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION;

ACTINS; ANIMALS; CELL SIZE; CELLS, CULTURED; CYTOSKELETON; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; MATRIX METALLOPROTEINASE 3; MICE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; RNA, NEOPLASM; TRANSFECTION;

MURINAE;

EID: 0032745920     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0945-053X(99)00036-0     Document Type: Article

References (60)

1. Adams J.C., Watt F.M. Regulation of development and differentiation by the extracellular matrix. Development. 117:1993;1187-1198.
2. Ashkenas J., Muschler J., Bissell M.J. The extracellular matrix in epithelial biology: shared molecules and common themes in distant phyla. Dev. Biol. 180:1996;433-444.
3. Barcellos-Hoff M.H., Aggeler J., Ram T.G., Bissell M.J. Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development. 105:1989;223-235.
4. Basbaum C.B., Werb Z. Focalized proteolysis: spatial and temporal regulation of extracellular matrix degradation at the cell surface. Curr. Opin. Cell Biol. 8:1996;731-738.
5. Birchmeier C., Birchmeier W., BrandSaberi B. Epithelial-mesenchymal transitions in cancer progression. Acta Anat. 156:1996;216-227.
6. Birkedal-Hansen H., Moore W.G., Bodden M.K. et al. Matrix metalloproteinases: a review. Crit. Rev. Oral Biol. Med. 4:1993;197-250.
7. Delescluse C., Bernard B.A., Furstenberg G et al. Effect of diterpene esters on actin cytoskeleton of SV40-transformed keratinocytes is not reproduced by diacylglycerols. Carcinogenesis. 9:1988;333-334.
8. Desprez P.Y., Roskelley C., Campisi J., Bissell M.J. Isolation of functional cell lines from a mouse mammary epithelial cell strain: The importance of basement membrane and cell-cell interactions. Mol. Cell. Diff. 1:1993;99-110.
9. Dosaka-Akita H., Hommura F., Fujita H. et al. Frequent loss of gelsolin expression in non-small cell lung cancers of heavy smokers. Cancer Res. 58:1998;322-327.
10. Emerman J.T., Pitelka D.R. Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro. 13:1977;316-328.
11. Fisher S.J., Werb Z. Techniques for studying the catabolism of extracellular matrix components. Haralson M.A., Hassel J.R. Extracellular Matrix: A Practical Approach. 1995;261-281 IRL Press Ltd, Oxford.
12. Folkman J., Moscona A. Role of cell shape in growth control. Nature. 273:1978;345-349.
13. Ganser G.L., Stricklin G.P., Matrisian L.M. EGF and TGF influence in vitro lung development by the induction of matrix-degrading metalloproteinases. Int. J. Dev. Biol. 35:1991;453-461.
14. Gilles C., Thompson E. The epithelial to mesenchymal transition and metastatic progression in carcinoma. Breast J. 2:1996;83-96.
15. Hendrix M.J., Seftor E.A., Chu Y.W., Trevor K.T., Seftor R.E. Role of intermediate filaments in migration, invasion and metastasis. Cancer Metastasis Rev. 15:1996;507-525.
16. Hendrix M.J., Seftor E.A., Seftor R.E., Trevor K.T. Experimental co-expression of vimentin and keratin intermediate filaments in human breast cancer cells results in phenotypic interconversion and increased invasive behavior. Am. J. Pathol. 150:1997;483-495.
17. Jones P.L., Schmidhauser C., Bissell M.J. Regulation of gene expression and cell function by extracellular matrix. Crit. Rev. Eukaryot. Gene Expr. 3:1993;137-154.
18. Kellie S., Holme T.C., Bissell M.J. Interaction of tumour promoters with epithelial cells in culture. An immunofluorescence study. Exp. Cell Res. 160:1985;259-274.
19. Kerr L.D., Magun B.E., Matrisian L.M. The role of c-Fos in growth factor regulation of stromelysin/transin expression. Matrix Suppl. 1:1992;176-183.
20. Ker L.D., Olashaw N.E., Matrisian L.M. Transforming growth factor 1 and cAMP inhibit transcription of epidermal growth factor and oncogene-induced transin RNA. J. Biol. Chem. 263:1988;16999-17005.
21. Kheradmand F., Werner E., Tremble P., Symons M., Werb Z. Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science. 280:1998;898-902.
22. Lelongt B., Trugnan G., Murphy G., Ronco P.M. Matrix metalloproteinases MMP2 and MMP9 are produced in early stages of kidney morphogenesis but only MMP9 is required for renal organogenesis in vitro. J. Cell Biol. 136:1997;1363-1373.
23. Li A.P., Myers C.A., Kaminski D.L. Gene transfer in primary cultures of human hepatocytes. In Vitro Cell Dev. Biol. 28A:1992;373-375.
24. Li M.L., Aggeler J., Farson D.A., Hatier C., Hassell J, Bissell M.J. Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells. Proc. Natl. Acad. Sci. USA. 84:1987;136-140.
25. Lochter A., Bissell M.J. Involvement of extracellular matrix in breast cancer. Semin. Cancer Biol. 6:1995;165-173.
26. Lochter A., Vaughan L., Kaplony A., Prochiantz A., Schachner M., Faissner A. J1/tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth. J. Cell Biol. 113:1991;1159-1171.
27. Lochter A., Galosy S., Muschler J., Freedman N., Werb Z, Bissell M.J. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J. Cell Biol. 139:1997;1862-1872.
28. Lochter A., Srebrow A., Sympson C.J., Terracio N., Werb Z., Bissell M.J. Misregulation of stromelysin-1 expression in mouse mammary tumor cells accompanies acquisition of stromelysin-1-dependent invasive properties. J. Biol. Chem. 272:1997;5007-5015.
29. Lochter A., Sternlicht M.D., Werb Z., Bissell M.J. The significance of matrix metalloproteinases during early stages of tumor progression. Ann. NY Acad. Sci. 857:1998;101-110.
30. Lochter A., Nave M., Werb Z., Bissell M.J. α1 and β2 integrins mediate invasive activity of mouse mammary carcinoma cells through regulation of stromelysin-1 expression. Mol. Biol. Cell. 10:1999;271-282.
31. Lund L.R., Romer J., Thomasset N. et al. Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways. Development. 122:1996;181-193.
32. MacDougall J.R., Kerbel R.S. Constitutive production of 92-kDa gelatinase B can be suppressed by alterations in cell shape. Exp. Cell Res. 218:1995;508-515.
33. MacDougal J.R., Matrisian L.M. Contribution of tumor and stromal matrix metalloproteinases in tumor progression, invasion and metastasis. Cancer Metastasis Rev. 14:1995;351-362.
34. Matrisian L.M., Leroy P., Ruhlmann C., Gesnel M.C., Breathnach R. Isolation of the oncogene and epidermal growth factor-induced transin gene: complex control in rat fibroblasts. Mol. Cell Biol. 6:1986;1679-1686.
35. McClatchey A.L., Saotome I. et al. Mice heterozygous for a mutation at the Nf2 tumor suppressor locus develop a range of highly matastatic tumors. Genes Dev. 12:1998;1121-1133.
36. McDonnell S., Matrisian L.M. Stromelysin in tumor progression and metastasis. Cancer Metastasis Rev. 9:1990;305-319.
37. McDonnell S.E., Kerr L.D., Matrisian L.M. Epidermal growth factor stimulation of stromelysin mRNA in rat fibroblasts requires induction of proto-oncogenes c-fos and c-jun and activation of protein kinase C. Mol. Cell Biol. 10:1990;4284-4293.
38. Medina D., Li M.L., Oborn C.J., Bissell M.J. Casein gene expression in mouse mammary epithelial cell lines: dependence upon extracellular matrix and cell type. Exp. Cell Res. 172:1987;192-203.
39. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Meth. 16:1983;55-63.
40. Myers C.A., Schmidhauser C., Mellentin-Michelotti J. et al. Characterization of BCE-1, a transcriptional enhancer regulated by prolactin and extracellular matrix and modulated by the state of histone acetylation. Mol. Cell. Biol. 18:1998;2184-2195.
41. Nordstrom L.A., Lochner J., Yeung W., Ciment G. The metalloproteinase stromelysin-1 (transin) mediates PC12 cell growth cone invasiveness through basal laminae. Mol. Cell. Neurosci. 6:1995;56-68.
42. Reichmann E., Ball R., Groner B., Friis R.R. New mammary epithelial and fibroblastic cell clones in coculture form structures competent to differentiate functionally. J. Cell Biol. 108:1989;1127-1138.
43. Roskelley C.D., Desprez P.Y., Bissell M.J. Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc. Natl. Acad. Sci. USA. 91:1994;12378-12382.
44. Saarialho-Kere U.K., Pentland A.P., Birkedal-Hansen H., Parks W.C., Welgus H.G. Distinct populations of basal keratinocytes express stromelysin-1 and stromelysin-2 in chronic wounds. J. Clin. Invest. 94:1994;79-88.
45. Schliwa M., Nakamura T., Porter K.R., Euteneuer U. A tumor promoter induces rapid and coordinated reorganization of actin and vinculin in cultured cells. J. Cell Biol. 99:1984;1045-1059.
46. Schmidhauser C., Casperson G.F., Myers C.A., Sanzo K.T., Bolten S., Bissell M.J. A novel transcriptional enhancer is involved in the prolactin and extracellular matrix-dependent regulation of casein gene expression. Mol. Biol. Cell. 3:1992;699-709.
47. Srebrow A., Friedmann Y., Ravanpay A., Daniel C.W., Bissell M.J. Expression of HOXA-1 and HOXB-7 is regulated by ECM-dependent signals in mammary epithelial cells. J. Cell. Biochem. 69:1998;377-391.
48. Sternlicht M.D., Lochter A., Sympson C.S., Huey B., Rougier J.P., Gray J.W., Pinikel D., Bissell M.J., Werb Z. The Stromal Proteinase MMP3/stromelysin-1 promote mammary carcinogenesis. Cell. 98:1999;137-146.
49. Sympson C.J., Talhouk R.S., Alexander C.M. et al. 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. 125:1994;681-693.
50. Sympson C.J., Bissell M.J., Werb Z. Mammary gland tumor formation in transgenic mice over expressing stromelysin-1. Semin. Cancer Biol. 6:1995;159-163.
51. Talhouk R.S., Bissell M.J., Werb Z. Co-ordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. J. Cell Biol. 118:1992;1271-1282.
52. Thomasset N., Lochter A., Sympson C.J. et al. Expression of autoactivated stromelyin-1 in mammary glands of transgenic mice leads to a reactive stroma during early development. Am. J. Pathol. 153:1998;457-466.
53. Tomasek J.J., Halliday N.L., Updike D.L. Gelatinase A activation is regulated by the organization of the polymerized actin cytoskeleton. J. Biol. Chem. 272:1997;7482-7487.
54. Unemori E.N., Werb Z. Reorganization of polymerized actin: a possible trigger for induction of procollagenase in fibroblasts cultured in and on collagen gels. J. Cell Biol. 103:1986;1021-1031.
55. Weaver V.M., Petersen O.W., Wang F. et al. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo using integrin blocking antibodies. J. Cell Biol. 137:1997;231-246.
56. Werb Z. ECM and cell surface proteolysis: Regulating cellular ecology. Cell. 91:1997;439-442.
57. Werb Z., Clark E.J. Phorbol diesters regulate expression of the membrane neutral metalloendopeptidase (EC 3.4.24.11) in rabbit synovial fibroblasts and mammary epithelial cells. J. Biol. Chem. 264:1989;9111-9113.
58. Werb Z., Hembry R.M., Murphy G., Aggeler J. Commitment to expression of the metalloendopeptidases, collagenase and stromelysin: relationship of inducing events to changes in cytoskeletal architecture. J. Cell Biol. 102:1986;697-702.
59. Witty J.P., Wright J.H., Matrisian L.M. Matrix metalloproteinases are expressed during ductal and alveolar mammary morphogenesis, and misregulation of stromelysin-1 in transgenic mice induces unscheduled alveolar development. Mol. Biol. Cell. 6:1995;1287-1303.
60. Ye S., Eriksson P., Hamsten A., Kurkinen M., Humphries S.E., Henney A.M. Progression of coronary atherosclerosis is associated with a common genetic variant of the human stromelysin-1 promoter which results in reduced gene expression. J. Biol. Chem. 271:1996;13055-13060.