Online citations, reference lists, and bibliographies.
← Back to Search

Cell Death By Apoptosis During Involution Of The Lactating Breast In Mice And Rats.

N. Walker, R. E. Bennett, J. Kerr
Published 1989 · Biology, Medicine

Cite This
Download PDF
Analyze on Scholarcy
Share
The role of cell death in involution of lactating breast was investigated in mice and rats by light and electron microscopy. Apoptosis, recognized by sharply demarcated compaction of chromatin against the nuclear envelope and by shrinkage and budding of the whole cell to form membrane-bounded apoptotic bodies, was responsible for major loss of cells in both species. In the mouse, rapid involution during the first 2 days was associated with shedding of large numbers of apoptotic bodies derived from alveolar epithelial cells into alveolar lumens. This was followed by more gradual regression, during which the bodies were mostly phagocytosed by macrophages within the epithelium. In the rat, glandular involution was a more gradual and uniform process, with shedding of apoptotic epithelial cells into alveolar lumens being much less conspicuous. Apoptosis of myoepithelial cells was observed in mice, the resulting apoptotic bodies being phagocytosed by intraepithelial macrophages, but was not detected in rats. Apoptosis of capillary endothelial cells caused rapid regression of the capillary beds in both mice and rats. Intraepithelial macrophages increased in number during involution, developed cytoplasmic lipofuscin pigment, and either remained within the epithelium or migrated to the interstitium and regional nodes. Cell loss by apoptosis has been demonstrated during involution and atrophy of a variety of other glands. It characteristically results in shrinkage of a tissue without disruption of its basic architecture.
This paper references
Melanosis coli. A consequence of anthraquinone-induced apoptosis of colonic epithelial cells.
N. Walker (1988)
10.1016/S0074-7696(08)62312-8
Cell death: the significance of apoptosis.
A. Wyllie (1980)
10.1016/0014-4827(71)90167-4
Effects of enforced milk stasis on mammary gland epithelium, with special reference to changes in lysosomes and lysosomal enzymes.
H. Helminen (1971)
10.1002/AJA.1000710102
Normal and experimental mammary involution in the mouse as related to the inception and cessation of lactation
W. L. Williams (1942)
10.1071/AR9570121
The inheritance of flowering time in Trifolium subterraneum L
Ci Davern (1957)
Macrophage recognition of cells undergoing programmed cell death (apoptosis).
E. Duvall (1985)
10.1113/EXPPHYSIOL.1962.SP001574
The absorption of serum albumin and casein from the mammary gland of the merino ewe.
A. Lascelles (1962)
10.1042/BJ1030420
Changes in the enzyme pattern of the mammary gland of the lactating rat after hypophysectomy and weaning.
E. A. Jones (1967)
Removal of basement membrane in the involuting breast.
A. Martinez-Hernandez (1976)
10.1002/AJA.1001560103
Hormonal control of apoptosis in hamster uterine luminal epithelium.
B. Sandow (1979)
Myoepithelium in involuting mammary glands of the rat.
C. Radnor (1972)
10.1095/BIOLREPROD18.5.736
Transepithelial migration of leukocytes in the mammary gland of lactating rats.
L. Seelig (1978)
10.1210/ENDO-122-2-552
Activation of programmed cell death in the rat ventral prostate after castration.
N. Kyprianou (1988)
10.1016/0014-5793(86)80114-4
Expression of the human apolipoprotein AI gene fused to the E. coli gene for β‐galactosidase
Rolando Lorenzetti (1986)
10.1038/bjc.1972.33
Apoptosis: A Basic Biological Phenomenon with Wide-ranging Implications in Tissue Kinetics
J. Kerr (1972)
10.1007/BF00431076
Ultrastructural observations on cell death by apoptosis in the “resting” human breast
D. J. Ferguson (2004)
10.1002/PATH.1711530407
Cell death and cell proliferation during atrophy of the rat parotid gland induced by duct obstruction
N. Walker (1987)
Mechanism of deletion of endothelial cells during regression of the corpus luteum.
Azmi Ti (1984)
10.1016/S0344-0338(81)80124-0
Die Regression der Rattenprostata nach Kastration
R. Stiens (1981)
10.1016/0012-1606(75)90244-4
The development of rat palatal shelves in vitro. An ultrastructural analysis of the inhibition of epithelial cell death and palate fusion by the epidermal growth factor.
J. Hassell (1975)
Enzymatic changes associated with the initiation and maintenance of lactation in the rat.
R. Baldwin (1966)
10.1097/00000372-197900120-00003
Apoptosis: Its nature and implications for dermatopathology
D. Weedon (1979)
10.1016/S0022-5320(68)80069-3
Studies on mammary gland involution. I. On the ultrastructure of the lactating mammary gland.
H. Helminen (1968)
10.1677/JOE.0.0510149
Involvement of the macrophage system in the involution of the mammary gland in the albino rat.
R. C. Richards (1971)
10.1002/PATH.1711420112
Chromatin cleavage in apoptosis: Association with condensed chromatin morphology and dependence on macromolecular synthesis
A. Wyllie (1984)
10.1002/IJC.2910360404
An immunohistological study of leukocyte localization in benign and malignant breast tissue
Khin Y. Lwin (1985)
10.1038/ICB.1968.23
The transfer of [131-I]-labelled immunoglobulins and serum albumin from blood into milk of lactating ewes.
Mackenzie Dd (1968)
10.1016/0005-2787(73)90336-5
The effects of testosterone, 5 -dihydrotestosterone and adenosine 3',5'-monophosphate on cell proliferation and differentiation in rat prostate.
B. Lesser (1973)
10.1002/AR.1092080408
The postovulatory cat oviduct and uterus: Correlation of morphological features with progesterone receptor levels
H. Verhage (1984)
10.1007/BF00214253
Involution and regeneration of the endometrium following parturition in the ewe
J. O'Shea (2004)
10.1002/PATH.1711190305
Atrophy and apoptosis in the cyclical human endometrium
D. Hop Wood (1976)
10.1016/0014-4827(68)90406-0
The fine structure of mammary glands of lactating rats, with special reference to the apocrine secretion.
K. Kurosumi (1968)
10.1002/PATH.1711110203
Adrenocortical cell deletion: The role of ACTH
A. Wyllie (1973)
10.1007/BF00433280
The fine structure of the normal, resting terminal ductal-lobular unit of the female breast
J. W. Stirling (2004)
10.1016/S0034-5288(18)34484-9
The importance of macrophages in the removal of fat from the involuting mammary gland.
C. Lee (1969)
Ultrastructure of the rat pancreas after experimental duct ligation. I. The role of apoptosis and intraepithelial macrophages in acinar cell deletion.
N. Walker (1987)
10.1016/S0022-5320(68)80070-X
Studies on mammary gland involution. II. Ultrastructural evidence for auto- and heterophagocytosis.
H. Helminen (1968)
10.1007/BF00303140
An ultrastructural study on the “meconium corpuscles” in rat foetal intestinal epithelium with particular reference to apoptosis
B. Harmon (2004)
10.1038/284555A0
Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation
A. Wyllie (1980)
10.3181/00379727-112-28233
Nucleic Acid Content of Rat Mammary Glands During Post-Lactational Involution.∗
H. Tucker (1963)
10.3181/00379727-110-27557
Hormonal Control of Mammary Gland Involution in the Rat.∗
David R. Griffith (1962)
10.1677/JOE.0.0510137
Structural changes associated with inhibition of involution of the mammary gland in the albino rat.
R. C. Richards (1971)
10.1016/0305-0491(73)90346-5
Dehydrogenases and nucleic acids in rat mammary gland during involution initiated at various stages of lactation.
E. I. Carlsson (1973)
10.1016/0014-5793(86)80115-6
Flow cytometry and biochemical analysis of DNA degradation characteristic of two types of cell death
V. I. Afanas’ev (1986)
10.1016/S0022-5320(68)80072-3
Studies on mammary gland involution. IV. Histochemical and biochemical observations on alterations in lysosomes and lysosomal enzymes.
H. Helminen (1968)
10.1038/bjc.1981.168
Morphological evaluation of cell turnover in relation to the menstrual cycle in the "resting" human breast.
D. J. Ferguson (1981)
10.1677/JOE.0.0510127
Ultrastructural changes accompanying involution of the mammary gland in the albino rat.
R. C. Richards (1971)
10.1113/jphysiol.1984.sp015387
Exchange area and surface properties of the microvasculature of the rabbit submandibular gland following duct ligation.
G. Clough (1984)
10.1002/PATH.1711050103
Shrinkage necrosis: A distinct mode of cellular death
J. Kerr (1971)
10.1507/ENDOCRJ1954.11.146
MAMMARY INVOLUTION AND ENGORGEMENT AFTER ARREST OF SUCKLING IN LACTATING RATS INDICATED BY THE CONTENTS OF NUCLEIC ACIDS AND MILK PROTEIN OF THE GLAND.
K. Ota (1964)
An Electron-Microscope Study of Cell Deletion in the Anuran Tadpole Tail During Spontaneous Metamorphosis with Special Reference to Apoptosis of Striated Muscle Fibres
J. Kerr (1974)
Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death.
J. Cohen (1984)
10.1007/978-94-011-6921-9_8
Cell death and the disease process. The role of calcium
B. Trump (1981)
10.1016/S0022-5320(68)80071-1
Studies on mammary gland involution. 3. Alterations outside auto- and heterophagocytic pathways for cytoplasmic degradation.
H. Helminen (1968)
Identification of a glucocorticoid-induced nuclease in thymocytes. A potential "lysis gene" product.
M. M. Compton (1987)
10.1002/AJA.1001420207
An ultrastructural study of normal human mammary epithelial cells in culture.
J. Russo (1975)
10.1002/PATH.1711110406
Cell death in the normal neonatal rat adrenal cortex
A. Wyllie (1973)
10.1038/195077B0
Effects of Administration of Oxytocin and Prolactin on Nucleic Acids and Phosphoprotein Contents of Mammary Glands in Lactating Rats
K. Ota (1962)
10.1002/PATH.1711520406
Immunohistochemical analysis of HLA antigens and mononuclear infiltrates of benign and malignant breast
J. Zuk (1987)
10.1016/0014-4827(69)90365-6
Characteristics of cells dissociated from mouse mammary glands. I. Method of separation and morphology of parenchymal cells from lactating glands.
D. Pitelka (1969)
Lysosomes and cellular regressive changes in rat mammary gland involution.
D. Brandes (1969)
10.1038/icb.1968.22
Studies on the transfer of protein across the glandular epithelium of the mammary gland during involution.
D. Mackenzie (1968)
10.1038/1911404A0
Removal of Milk Constituents from the Mammary Gland of the Ewe
A. Lascelles (1961)



This paper is referenced by
10.1007/BF00048064
Active cell death in hormone-dependent tissues
M. Tenniswood (2004)
10.1007/978-1-4757-9534-9_16
Cell Recognition of Apoptotic Cells
C. A. Smith (1993)
10.1002/AR.1092420102
Lipocortin 1 in apoptosis: Mammary regression
J. McKanna (1995)
10.1210/endo.139.2.5683
Testosterone Stimulates Angiogenesis and Vascular Regrowth in the Ventral Prostate in Castrated Adult Rats.
I. Franck-Lissbrant (1998)
10.1074/JBC.275.5.3328
Truncation of the β-Catenin Binding Domain of E-cadherin Precedes Epithelial Apoptosis during Prostate and Mammary Involution*
C. J. Vallorosi (2000)
10.1007/s10495-008-0187-8
Secondary necrosis in multicellular animals: an outcome of apoptosis with pathogenic implications
Manuel T. Silva (2008)
Endotoxin Increases Oxidative Stress And Oxygen Tension While Reducing Milk Protein Gene Expression In The Mammary Gland
Alexander Jonathan Spitzer (2019)
10.1096/fasebj.6.7.1563596
Apoptosis: a different type of cell death
L. Gerschenson (1992)
Apoptosis in the genesis and prevention of cancer.
H. Thompson (1992)
10.1002/JCB.240580205
Apoptosis and the cell cycle
W. Meikrantz (1995)
Fas expression and function in normal and malignant breast cell lines.
M. Keane (1996)
10.1042/BJ20020026
High expression in involuting reproductive tissues of uterocalin/24p3, a lipocalin and acute phase protein.
J. Ryon (2002)
10.1016/S0006-2952(02)01267-4
Role of the Fas/Fas ligand system in female reproductive organs: survival and apoptosis.
G. Mor (2002)
10.1016/j.febslet.2010.10.046
Secondary necrosis: The natural outcome of the complete apoptotic program
M. Silva (2010)
10.1271/bbb.60142
RETRACTED ARTICLE: Regulation and Functional Relevance of Milk Fat Globules and Their Components in the Mammary Gland
N. Aoki (2006)
10.1158/0008-5472.CAN-07-6453
The Spy1/RINGO family represents a novel mechanism regulating mammary growth and tumorigenesis.
Azadeh Golipour (2008)
10.1016/B978-0-12-394445-0.00035-7
Mammary Gland Morphogenesis and Function during Pregnancy
R. Kommagani (2014)
10.1247/CSF.20.125
Estrogen-depleted condition induces apoptosis of rat mammary cancer cells after entering the S-phase of the cell cycle.
Y. Watanabe (1995)
10.1242/dev.059261
Dual roles for macrophages in ovarian cycle-associated development and remodelling of the mammary gland epithelium
A. C. Chua (2010)
10.1023/A:1006891430596
Biochemical and molecular mechanisms regulating apoptosis
K. Saini (2004)
10.1083/JCB.150.6.1445
Expression and Function of αvβ3 and αvβ5 Integrins in the Developing Pancreas
V. Cirulli (2000)
10.2460/AJVR.2002.63.241
Apoptosis and oxidative stress of infiltrated neutrophils obtained from mammary glands of goats during various stages of lactation.
W. J. Su (2002)
10.1186/bcr753
Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3
Torsten Stein (2003)
10.1016/S1542-0124(12)70070-8
Mechanisms involved in injury and repair of the murine lacrimal gland: role of programmed cell death and mesenchymal stem cells.
D. Zoukhri (2010)
Pubertal mouse mammary gland development - transcriptome analysis and the investigation of Fbln2 expression and function
D. Olijnyk (2011)
10.1210/me.2010-0423
Singleminded-2s (Sim2s) promotes delayed involution of the mouse mammary gland through suppression of Stat3 and NFκB.
Kelly C. Scribner (2011)
10.1007/s10911-007-9037-5
The Fur Seal—a Model Lactation Phenotype to Explore Molecular Factors Involved in the Initiation of Apoptosis at Involution
J. Sharp (2007)
10.1016/1043-2760(92)90087-H
Thymocyte apoptosis a model of programmed cell death
M. M. Compton (1992)
10.1002/(SICI)1097-4652(199609)168:3<559::AID-JCP8>3.0.CO;2-O
Programmed cell death during mammary tissue involution induced by weaning, litter removal, and milk stasis
L. Quarrie (1996)
10.1007/978-1-4612-1944-6_12
The Central Role of Basement Membrane in Functional Differentiation, Apoptosis, and Cancer
M. Bissell (1997)
10.1006/cbir.1996.0098
INVOLUTION OF MOUSE MAMMARY GLANDS DURING WHOLE ORGAN CULTURE OCCURS VIA APOPTOSIS OF EPITHELIAL TISSUE
T. Casey (1996)
10.1074/jbc.273.46.30336
Vascular Endothelial Growth Factor Regulates Endothelial Cell Survival through the Phosphatidylinositol 3′-Kinase/Akt Signal Transduction Pathway
H. Gerber (1998)
See more
Semantic Scholar Logo Some data provided by SemanticScholar