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Development, Vol 115, Issue 1 49-58, Copyright © 1992 by Company of Biologists

JOURNAL ARTICLES

Apoptotic cell death and tissue remodelling during mouse mammary gland involution

R Strange, F Li, S Saurer, A Burkhardt and RR Friis
Laboratory for Clinical and Experimental Research, University of Bern, Switzerland.

During post-lactational mammary gland involution, the bulk of mammary epithelium dies and is reabsorbed. This massive cell death and tissue restructuring was found to be accompanied by a specific pattern of gene expression. Northern blot analysis showed that weaning resulted in a dramatic drop in ODC, a gene involved in synthesis of a component of milk, and the nearly simultaneous induction of SGP-2, a gene associated with apoptotic cell death. These changes were followed by decreases in expression of milk protein genes to basal levels and expression of genes associated with regulation of cell proliferation and differentiation, p53, c-myc and TGF-beta 1. Subsequently, additional genes implicated in stress response, tissue remodelling, and apoptotic cell death were transiently expressed, expression peaking at about 6 days post-weaning. A non-random degradation of DNA yielding the oligonucleosomal length fragmentation pattern typical of apoptotic cell death (Wyllie, 1980; Wyllie et al., 1980) was detected in association with morphological changes and gene expression. The correlations between: (a) changes in morphology, (b) pattern of gene expression and (c) changes in DNA integrity suggest that complementary programs for cell death and tissue remodelling direct post-lactational mammary gland involution.
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R. Neve, C. Chang, G. K. Scott, A. Wong, R. R. Friis, N. E. Hynes, and C. C. Benz
The epithelium-specific Ets transcription factor ESX is associated with mammary gland development and involution
FASEB J, November 1, 1998; 12(14): 1541 - 1550.
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 J. Clin. Endocrinol. Metab.Home page
M. Vitale, T. Di Matola, G. Fenzi, M. Illario, and G. Rossi
Fibronectin Is Required to Prevent Thyroid Cell Apoptosis through an Integrin-Mediated Adhesion Mechanism
J. Clin. Endocrinol. Metab., October 1, 1998; 83(10): 3673 - 3680.
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 Am. J. Pathol.Home page
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.
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 EndocrinologyHome page
E. Ahlbom, L. Grandison, B. Zhivotovsky, and S. Ceccatelli
Termination of Lactation Induces Apoptosis and Alters the Expression of the Bcl-2 Family Members in the Rat Anterior Pituitary
Endocrinology, May 1, 1998; 139(5): 2465 - 2471.
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Z Nikolova, V Djonov, G Zuercher, A. Andres, and A Ziemiecki
Cell-type specific and estrogen dependent expression of the receptor tyrosine kinase EphB4 and its ligand ephrin-B2 during mammary gland morphogenesis
J. Cell Sci., January 9, 1998; 111(18): 2741 - 2751.
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 JCBHome page
P. Kueng, Z. Nikolova, V. Djonov, A. Hemphill, V. Rohrbach, D. Boehlen, G. Zuercher, A.-C. Andres, and A. Ziemiecki
A Novel Family of Serine/Threonine Kinases Participating in Spermiogenesis
J. Cell Biol., December 29, 1997; 139(7): 1851 - 1859.
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 JCBHome page
P. L. Jones, J. Crack, and M. Rabinovitch
Regulation of Tenascin-C, a Vascular Smooth Muscle Cell Survival Factor that Interacts with the {alpha}v{beta}3 Integrin to Promote Epidermal Growth Factor Receptor Phosphorylation and Growth
J. Cell Biol., October 6, 1997; 139(1): 279 - 293.
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 JCBHome page
V.M. Weaver, O.W. Petersen, F. Wang, C.A. Larabell, P. Briand, C. Damsky, and M.J. Bissell
Reversion of the Malignant Phenotype of Human Breast Cells in Three-Dimensional Culture and In Vivo by Integrin Blocking Antibodies
J. Cell Biol., April 7, 1997; 137(1): 231 - 245.
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 Proc. Natl. Acad. Sci. USAHome page
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.
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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.
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 Circ. Res.Home page
P. L. Jones and M. Rabinovitch
Tenascin-C Is Induced With Progressive Pulmonary Vascular Disease in Rats and Is Functionally Related to Increased Smooth Muscle Cell Proliferation
Circ. Res., December 1, 1996; 79(6): 1131 - 1142.
[Abstract] [Full Text]

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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.
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S. Pullan, J. Wilson, A. Metcalfe, G. M. Edwards, N. Goberdhan, J. Tilly, J. A. Hickman, C. Dive, and C. H. Streuli
Requirement of basement membrane for the suppression of programmed cell death in mammary epithelium
J. Cell Sci., March 1, 1996; 109(3): 631 - 642.
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P. A. Tilbrook, T. Bittorf, S. J. Busfield, D. Chappell, and S. P. Klinken
Disrupted Signaling in a Mutant J2E Cell Line That Shows Enhanced Viability, but Does Not Proliferate or Differentiate, with Erythropoietin
J. Biol. Chem., February 16, 1996; 271(7): 3453 - 3459.
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 DevelopmentHome page
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.
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 DevelopmentHome page
D. Phippard, S. Weber-Hall, P. Sharpe, M. Naylor, H Jayatalake, R Maas, I Woo, D Roberts-Clark, P. Francis-West, Y. Liu, et al.
Regulation of Msx-1, Msx-2, Bmp-2 and Bmp-4 during foetal and postnatal mammary gland development
Development, January 9, 1996; 122(9): 2729 - 2737.
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 DevelopmentHome page
L. Lund, J Romer, N Thomasset, H Solberg, C Pyke, M. Bissell, K Dano, and Z Werb
Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways
Development, January 1, 1996; 122(1): 181 - 193.
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M. R. Bennett, G. I. Evan, and S. M. Schwartz
Apoptosis of Rat Vascular Smooth Muscle Cells Is Regulated by p53-Dependent and -Independent Pathways
Circ. Res., August 1, 1995; 77(2): 266 - 273.
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 Reproductive SciencesHome page
A. Palumbo and J. Yeh
Apoptosis as a Basic Mechanism in the Ovarian Cycle: Folicular Atresia and Luteal Regression
Reproductive Sciences, May 1, 1995; 2(3): 565 - 573.
[Abstract] [PDF]

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 ScienceHome page
N Boudreau, C. Sympson, Z Werb, and M. Bissell
Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix
Science, February 10, 1995; 267(5199): 891 - 893.
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P. Hall, P. Coates, B Ansari, and D Hopwood
Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis
J. Cell Sci., January 12, 1994; 107(12): 3569 - 3577.
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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.
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