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Development, Vol 122, Issue 1 181-193, Copyright © 1996 by Company of Biologists
JOURNAL ARTICLES |
LR Lund, J Romer, N Thomasset, H Solberg, C Pyke, MJ Bissell, K Dano and Z Werb
Laboratory of Radiobiology and Environmental Health, University of California, San Francisco 94143-0750, USA.
Postlactational involution of the mammary gland is characterized by two distinct physiological events: apoptosis of the secretory, epithelial cells undergoing programmed cell death, and proteolytic degradation of the mammary gland basement membrane. We examined the spatial and temporal patterns of apoptotic cells in relation to those of proteinases during involution of the BALB/c mouse mammary gland. Apoptosis was almost absent during lactation but became evident at day 2 of involution, when beta-casein gene expression was still high. Apoptotic cells were then seen at least up to day 8 of involution, when beta-casein gene expression was being extinguished. Expression of sulfated glycoprotein-2 (SGP-2), interleukin-1 beta converting enzyme (ICE) and tissue inhibitor of metalloproteinases-1 was upregulated at day 2, when apoptotic cells were seen initially. Expression of the matrix metalloproteinases gelatinase A and stromelysin-1 and the serine proteinase urokinase-type plasminogen activator, which was low during lactation, was strongly upregulated in parallel starting at day 4 after weaning, coinciding with start of the collapse of the lobulo-alveolar structures and the intensive tissue remodeling in involution. The major sites of mRNA synthesis for these proteinases were fibroblast-like cells in the periductal stroma and stromal cells surrounding the collapsed alveoli, suggesting that the degradative phase of involution is due to a specialized mesenchymal-epithelial interaction. To elucidate the functional role of these proteinases during involution, at the onset of weaning we treated mice systemically with the glucocorticoid hydrocortisone, which is known to inhibit mammary gland involution. Although the initial wave of apoptotic cells appeared in the lumina of the gland, the dramatic regression and tissue remodeling usually evident by day 5 was substantially inhibited by systemic treatment with hydrocortisone. mRNA and protein for gelatinase A, stromelysin-1 and uPA were weakly induced, if at all, in hydrocortisone-treated mice. Furthermore, mRNA for membrane-type matrix metalloproteinase decreased after hydrocortisone treatment and paralleled the almost complete inhibition of activation of latent gelatinase A. Concomitantly, the gland filled with an overabundance of milk. Our data support the hypothesis that there are at least two distinct phases of involution: an initial phase, characterized by induction of the apoptosis-associated genes SGP-2 and ICE and apoptosis of fully differentiated mammary epithelial cells without visible degradation of the extracellular matrix, and a second phase, characterized by extracellular matrix remodeling and altered mesenchymal-epithelial interactions, followed by apoptosis of cells that are losing differentiated functions.
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N. Thomasset, A. Lochter, C. J. Sympson, L. R. Lund, D. R. Williams, O. Behrendtsen, Z. Werb, and M. J. Bissell Expression of Autoactivated Stromelysin-1 in Mammary Glands of Transgenic Mice Leads to a Reactive Stroma During Early Development Am. J. Pathol., August 1, 1998; 153(2): 457 - 467. [Abstract] [Full Text] [PDF]
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D. Miller and R. Cagan Local induction of patterning and programmed cell death in the developing Drosophila retina Development, January 6, 1998; 125(12): 2327 - 2335. [Abstract] [PDF]
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Y. Su, Y. Shi, M. A. Stolow, and Y.-B. Shi Thyroid Hormone Induces Apoptosis in Primary Cell Cultures of Tadpole Intestine: Cell Type Specificity and Effects of Extracellular Matrix J. Cell Biol., December 15, 1997; 139(6): 1533 - 1543. [Abstract] [Full Text] [PDF]
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E. Tonner, M. C. Barber, M. T. Travers, A. Logan, and D. J. Flint Hormonal Control of Insulin-Like Growth Factor-Binding Protein-5 Production in the Involuting Mammary Gland of the Rat Endocrinology, December 1, 1997; 138(12): 5101 - 5107. [Abstract] [Full Text] [PDF]
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M. Li, X. Liu, G. Robinson, U. Bar-Peled, K.-U. Wagner, W. S. Young, L. Hennighausen, and P. A. Furth Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution PNAS, April 1, 1997; 94(7): 3425 - 3430. [Abstract] [Full Text] [PDF]
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A. Lochter, A. Srebrow, C. J. Sympson, N. Terracio, Z. Werb, and M. J. Bissell Misregulation of Stromelysin-1 Expression in Mouse Mammary Tumor Cells Accompanies Acquisition of Stromelysin-1-dependent Invasive Properties J. Biol. Chem., February 21, 1997; 272(8): 5007 - 5015. [Abstract] [Full Text] [PDF]
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D Michel, E Moyse, A Trembleau, F Jourdan, and G Brun Clusterin/ApoJ expression is associated with neuronal apoptosis in the olfactory mucosa of the adult mouse J. Cell Sci., January 7, 1997; 110(14): 1635 - 1645. [Abstract] [PDF]
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E. E.M. Furlong, N. K. Keon, F. D. Thornton, T. Rein, and F. Martin 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., November 22, 1996; 271(47): 29688 - 29697. [Abstract] [Full Text] [PDF]
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R. Humphreys, M Krajewska, S Krnacik, R Jaeger, H Weiher, S Krajewski, J. Reed, and J. Rosen Apoptosis in the terminal endbud of the murine mammary gland: a mechanism of ductal morphogenesis Development, January 12, 1996; 122(12): 4013 - 4022. [Abstract] [PDF]
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H. Hathaway and B. Shur Mammary gland morphogenesis is inhibited in transgenic mice that overexpress cell surface beta1,4-galactosyltransferase Development, January 9, 1996; 122(9): 2859 - 2872. [Abstract] [PDF]
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Z. Jiang and E. Zacksenhaus Activation of retinoblastoma protein in mammary gland leads to ductal growth suppression, precocious differentiation, and adenocarcinoma J. Cell Biol., January 7, 2002; 156(1): 185 - 198. [Abstract] [Full Text] [PDF]
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