DOI: 10.1242/dev.118.3.777. Large-scale normal cell death in the developing rat kidney and its reduction by epidermal growth factor

Large-scale normal cell death in the developing rat kidney and its reduction by epidermal growth factor

10.1242/dev.118.3.777

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT Although normal cell death is known to occur in many developing vertebrate organs, it has not been thought to play an important part in the development of the mammalian kidney. We show here that normal cell death is found in both the nephrogenic region and medullary papilla of the developing rat kidney and, in each of these areas, it follows a distinct developmental time course. As many as 3% of the cells in these areas have a typical apoptotic morphology and the dead cells seem to be cleared rapidly (within 1-2 hours) by phagocytosis by neighbouring parenchymal cells. These values are similar to those in vertebrate neural tissues where 50% or more of the cells die during normal development, suggesting that large-scale death is a normal feature of kidney development. We also show that in vivo treatment with epidermal growth factor inhibits cell death in the developing kidney, consistent with the possibility that the cells normally die because they lack sufficient survival factors. Our findings suggest that the extent of normal cell death in developing animals is still greatly underestimated and they raise the possibility that many of these cell deaths may reflect limiting amounts of survival factors.

Bibliography

Coles, H. S. R., Burne, J. F., & Raff, M. C. (1993). Large-scale normal cell death in the developing rat kidney and its reduction by epidermal growth factor. Development, 118(3), 777â784.

Authors 3

Harriet S. R. Coles (first)
Julia F. Burne (additional)
Martin C. Raff (additional)

References 32 Referenced 296

10.1002/ar.1090940210 / Anat. Rec / Estimation of nuclear population from microtome sections by Abercrombie (1946)
10.1016/S0959-437X(05)80177-7 / Curr. Opin. Genet. Dev / The development of the mouse kidney—embryogenesis writ small by Bard (1992)
10.1016/0896-6273(89)90040-8 / Neuron / Trophic factors and neuronal survival by Barde (1989)
10.1016/0092-8674(92)90531-G / Cell / Cell death and control of cell survival in the oligodendrocyte lineage by Barres (1992)
{'volume-title': 'The Biology of Cell Reproduction. Cambridge, MA: Harvard University Press', 'year': '1985', 'author': 'Baserga', 'key': '2024121723015218500_DEVELOP_118_3_777C5'} / The Biology of Cell Reproduction. Cambridge, MA: Harvard University Press by Baserga (1985)
10.1007/BF00174615 / Anat. Embryol / Developmental cell death: morphological diversity and multiple mechanisms by Clarke (1990)
10.1126/science.6474175 / Science / Regressive events in neurogenesis by Cowan (1984)
10.1073/pnas.87.7.2579 / Proc. Natl. Acad. Sci. USA / Kinetics of mature T-cell development in the thymus by Egerton (1990)
10.1007/978-3-642-71837-3_8 / Mesenchymal-Epithelial Interactions in Neural Development / Cell interactions during kidney development by Ekblom (1987)
10.1146/annurev.cb.07.110191.003311 / Annu. Rev. Cell Biol / Mechanisms and functions of cell death by Ellis (1991)
10.1146/annurev.ph.51.030189.000435 / Annu. Rev. Physiol / Epidermal growth factor in the kidney by Fisher (1989)
10.1111/j.1469-185X.1951.tb00774.x / Biol. Rev / Cell deaths in normal vertebrate ontogeny by Glucksmann (1951)
10.1002/cyto.990060604 / Cytometry / A monoclonal antibody reactive with 5-bromo-2-deoxyuridine that does not require DNA denaturation by Gonchoroff (1985)
10.1002/ajh.2830200311 / Am. J. Hemat / Immunofluorescent plasma cell labelling indices (LI) using a monoclonal antibody (BU-1) by Greipp (1985)
10.1523/JNEUROSCI.01-01-00060.1981 / J. Neurosci / Neural death in the spinal ganglion of the chick embryo and its reduction by nerve growth factor by Hamburger (1981)
10.1002/jez.1401110308 / J. Exp. Zool / Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions by Hamburger (1949)
10.1016/0014-4827(77)90240-3 / Exp. Cell Res / Elevated levels of cAMP alter the effect of epidermal growth factor in vitro on programmed cell death in the secondary palatal epithelia by Hassell (1977)
10.1038/331261a0 / Nature / Brain-derived neurotrophic factor prevents neural death in vivo by Hofer (1988)
10.1038/bjc.1972.33 / Br. J. Cancer / Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics by Kerr (1972)
10.1083/jcb.119.5.1327 / J. Cell Biol / Apoptosis in metanephric development by Koseki (1992)
{'key': '2024121723015218500_DEVELOP_118_3_777C21', 'article-title': 'Neuronal cell death and some related regressive phenomena during neurogenesis: a selective historical review and progress report', 'volume-title': 'Studies in Developmental Neurobiology', 'author': 'Oppenheim', 'year': '1981'} / Studies in Developmental Neurobiology / Neuronal cell death and some related regressive phenomena during neurogenesis: a selective historical review and progress report by Oppenheim (1981)
10.1126/science.3363373 / Science / Reduction of naturally occuring motor neuron death in vivo by a target-derived neurotrophic factor by Oppenheim (1988)
10.1146/annurev.ne.14.030191.002321 / Annu. Rev. Neurosci / Cell death during development of the nervous system by Oppenheim (1991)
10.1002/cne.902190309 / J. Comp. Neurol / Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat by Perry (1983)
{'volume-title': 'Body and Brain: A Trophic Theory of Neural Connections', 'year': '1988', 'author': 'Purves', 'key': '2024121723015218500_DEVELOP_118_3_777C25'} / Body and Brain: A Trophic Theory of Neural Connections by Purves (1988)
10.1038/356397a0 / Nature / Social controls on cell survival and cell death by Raff (1992)
10.1017/CBO9780511565083 / Organogenesis of the Kidney. (Developmental and Cell Biology Series) by Saxen (1987)
10.1007/BF00849241 / Pediatr. Nephrol / Early organogenesis of the kidney by Saxen (1987)
{'key': '2024121723015218500_DEVELOP_118_3_777C29', 'first-page': '3', 'article-title': 'The generation and fate of thymocytes', 'volume': '2', 'author': 'Shortman', 'year': '1990', 'journal-title': 'Semin. in Immunol'} / Semin. in Immunol / The generation and fate of thymocytes by Shortman (1990)
{'volume-title': 'Ph.D. Thesis, University of Aberdeen', 'year': '1975', 'author': 'Wyllie', 'key': '2024121723015218500_DEVELOP_118_3_777C30'} / Ph.D. Thesis, University of Aberdeen by Wyllie (1975)
10.1016/S0074-7696(08)62312-8 / Int. Rev. Cytol / Cell death: significance of apoptosis by Wyllie (1980)
{'key': '2024121723015218500_DEVELOP_118_3_777C32', 'first-page': '11', 'article-title': 'Preparation of cat kidney for ultrastructural studies', 'volume': '25', 'author': 'Yun', 'year': '1976', 'journal-title': 'J Electron Microsc'} / J Electron Microsc / Preparation of cat kidney for ultrastructural studies by Yun (1976)

Dates

Type	When
Created	4 years, 3 months ago (April 25, 2021, 9:20 p.m.)
Deposited	8 months, 1 week ago (Dec. 17, 2024, 6:02 p.m.)
Indexed	2 days, 2 hours ago (Aug. 23, 2025, 1:22 a.m.)
Issued	32 years, 1 month ago (July 1, 1993)
Published	32 years, 1 month ago (July 1, 1993)
Published Online	32 years, 1 month ago (July 1, 1993)
Published Print	32 years, 1 month ago (July 1, 1993)

Funders 0

None

BibTeX

@article{Coles_1993, title={Large-scale normal cell death in the developing rat kidney and its reduction by epidermal growth factor}, volume={118}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.118.3.777}, DOI={10.1242/dev.118.3.777}, number={3}, journal={Development}, publisher={The Company of Biologists}, author={Coles, Harriet S. R. and Burne, Julia F. and Raff, Martin C.}, year={1993}, month=jul, pages={777–784} }

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