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PMID: 12732721 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Rb function in extraembryonic lineages suppresses apoptosis in the CNS of Rb-deficient mice.

de Bruin A, Wu L, Saavedra HI, Wilson P, Yang Y, Rosol TJ, Weinstein M, Robinson ML, Leone G

Abstract

Retinoblastoma (Rb)-deficient embryos show severe defects in neurogenesis, erythropoiesis, and lens development and die at embryonic day 14.5. Our recent results demonstrated a drastic disorganization of the labyrinth layer in the placenta of Rb-deficient embryos, accompanied by reduced placental transport function. When these Rb-/- embryos were supplied with a wild-type placenta by using either tetraploid aggregation or genetic approaches, animals survived until birth. Here we analyze the role of extraembryonic Rb in regulating proliferation, apoptosis, and differentiation in the rescued animals at different developmental stages. Many of the neurological and erythroid abnormalities thought to be responsible for the embryonic lethality of Rb-/- animals, including the ectopic apoptosis in the CNS, were virtually absent in rescued Rb-/- pups. However, rescued animals died at birth with severe skeletal muscle defects. Like in Rb knockout embryos, rescued animals showed a marked increase in DNA replication and cell division in the CNS. In sharp contrast, the typical widespread neuronal apoptosis was absent in Rb-deficient embryos reconstituted with a normal placenta. In lens fiber cells, however, the inappropriate proliferation and apoptosis that is normally observed in Rb-/- embryos continued unabated in rescued animals. These results demonstrate that Rb function in extraembryonic lineages plays an important role in the survival of neuronal cells and in the differentiation of the erythroid lineage, providing mechanistic insight into the cell autonomous and nonautonomous functions of Rb during development.

MeSH Terms
Animals Apoptosis/physiology Central Nervous System/cytology Immunohistochemistry Mice Mice, Knockout Mice, Transgenic Retinoblastoma Protein/genetics,physiology
Chemicals
Retinoblastoma Protein
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
de Bruin Alain
Human Cancer Genetics Program, Department of Molecular Virology, Immunology, and Medical Genetics, Ohio State University, Columbus 43210, USA.
Wu Lizhao
Saavedra Harold I
Wilson Pamela
Yang Ying
Rosol Thomas J
Weinstein Michael
Robinson Michael L
Leone Gustavo
References (32)
32 references, click to expand
  1. The retinoblastoma gene family in differentiation and development.
    Oncogene. 1999 Dec 20;18(55):7873-82 PMID: 10630640
  2. pRb is required for MEF2-dependent gene expression as well as cell-cycle arrest during skeletal muscle differentiation.
    Curr Biol. 1999 May 6;9(9):449-59 PMID: 10322110
  3. Epiblast-restricted Cre expression in MORE mice: a tool to distinguish embryonic vs. extra-embryonic gene function.
    Genesis. 2000 Feb;26(2):113-5 PMID: 10686601
  4. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum.
    Genes Dev. 2000 Apr 15;14(8):994-1004 PMID: 10783170
  5. RB-dependent S-phase response to DNA damage.
    Mol Cell Biol. 2000 Oct;20(20):7751-63 PMID: 11003670
  6. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins.
    Nature. 2000 Oct 5;407(6804):592-8 PMID: 11034201
  7. E2F3 contributes both to the inappropriate proliferation and to the apoptosis arising in Rb mutant embryos.
    Genes Dev. 2001 Feb 15;15(4):386-91 PMID: 11230146
  8. The Rb/E2F pathway and cancer.
    Hum Mol Genet. 2001 Apr;10(7):699-703 PMID: 11257102
  9. Cell-autonomous and non-cell-autonomous functions of the Rb tumor suppressor in developing central nervous system.
    EMBO J. 2001 Jul 2;20(13):3402-13 PMID: 11432828
  10. The retinoblastoma protein acts as a transcriptional coactivator required for osteogenic differentiation.
    Mol Cell. 2001 Aug;8(2):303-16 PMID: 11545733
  11. Early eye development in vertebrates.
    Annu Rev Cell Dev Biol. 2001;17:255-96 PMID: 11687490
  12. Astrocyte inactivation of the pRb pathway predisposes mice to malignant astrocytoma development that is accelerated by PTEN mutation.
    Cancer Cell. 2002 Mar;1(2):157-68 PMID: 12086874
  13. Telencephalon-specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development.
    EMBO J. 2002 Jul 1;21(13):3337-46 PMID: 12093735
  14. Conditional mutation of Rb causes cell cycle defects without apoptosis in the central nervous system.
    Mol Cell Biol. 2003 Feb;23(3):1044-53 PMID: 12529408
  15. Dp1 is required for extra-embryonic development.
    Development. 2003 Apr;130(7):1295-305 PMID: 12588846
  16. Extra-embryonic function of Rb is essential for embryonic development and viability.
    Nature. 2003 Feb 27;421(6926):942-7 PMID: 12607001
  17. A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma.
    Nature. 1986 Oct 16-22;323(6089):643-6 PMID: 2877398
  18. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis.
    Nature. 1992 Sep 24;359(6393):288-94 PMID: 1406932
  19. Effects of an Rb mutation in the mouse.
    Nature. 1992 Sep 24;359(6393):295-300 PMID: 1406933
  20. Requirement for a functional Rb-1 gene in murine development.
    Nature. 1992 Sep 24;359(6393):328-30 PMID: 1406937
  21. Homeotic transformation of the occipital bones of the skull by ectopic expression of a homeobox gene.
    Nature. 1992 Oct 29;359(6398):835-41 PMID: 1359423
  22. Molecular characterization of the retinoblastoma susceptibility gene.
    Biochim Biophys Acta. 1993 May 25;1155(1):43-61 PMID: 8504130
  23. p53-dependent apoptosis suppresses tumor growth and progression in vivo.
    Cell. 1994 Aug 26;78(4):703-11 PMID: 8069917
  24. p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens.
    Nature. 1994 Sep 1;371(6492):72-4 PMID: 8072529
  25. Restricted distribution of tetraploid cells in mouse tetraploid<==>diploid chimaeras.
    Dev Biol. 1995 Jan;167(1):213-26 PMID: 7851644
  26. Tumorigenic and developmental effects of combined germ-line mutations in Rb and p53.
    Cold Spring Harb Symp Quant Biol. 1994;59:449-57 PMID: 7587099
  27. Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle.
    J Cell Biol. 1996 Oct;135(2):441-56 PMID: 8896600
  28. Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs.
    Genes Dev. 1996 Nov 1;10(21):2794-804 PMID: 8946919
  29. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis.
    Genes Dev. 1996 Dec 1;10(23):3051-64 PMID: 8957005
  30. Inhibition of DNA synthesis by RB: effects on G1/S transition and S-phase progression.
    Genes Dev. 1998 Aug 1;12(15):2278-92 PMID: 9694794
  31. Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos.
    Mol Cell. 1998 Sep;2(3):293-304 PMID: 9774968
  32. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2003-05-27
Epub
2003-00-05
Pages
6546-51
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC164483
Subset
IM
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