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PMID: 16436596 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors.

Gil-Perotin S, Marin-Husstege M, Li J, Soriano-Navarro M, Zindy F, Roussel MF, Garcia-Verdugo JM, Casaccia-Bonnefil P

Abstract

The role of multipotential progenitors and neural stem cells in the adult subventricular zone (SVZ) as cell-of-origin of glioblastoma has been suggested by studies on human tumors and transgenic mice. However, it is still unknown whether glial tumors are generated by all of the heterogeneous SVZ cell types or only by specific subpopulations of cells. It has been proposed that transformation could result from lack of apoptosis and increased self-renewal, but the definition of the properties leading to neoplastic transformation of SVZ cells are still elusive. This study addresses these questions in mice carrying the deletion of p53, a tumor-suppressor gene expressed in the SVZ. We show here that, although loss of p53 by itself is not sufficient for tumor formation, it provides a proliferative advantage to the slow- and fast-proliferating subventricular zone (SVZ) populations associated with their rapid differentiation. This results in areas of increased cell density that are distributed along the walls of the lateral ventricles and often associated with increased p53-independent apoptosis. Transformation occurs when loss of p53 is associated with a mutagenic stimulus and is characterized by dramatic changes in the properties of the quiescent adult SVZ cells, including enhanced self-renewal, recruitment to the fast-proliferating compartment, and impaired differentiation. Together, these findings provide a cellular mechanism for how the slow-proliferating SVZ cells can give rise to glial tumors in the adult brain.

MeSH Terms
Animals Apoptosis Brain/radiation effects Brain Neoplasms/chemically induced,etiology,genetics,pathology Cell Count Cell Division Cell Transformation, Neoplastic/genetics Cerebral Ventricles/cytology DNA Damage Ethylnitrosourea/toxicity Female Gene Expression Regulation/radiation effects Genes, p53 Genetic Vectors Glioblastoma/chemically induced,etiology,genetics,pathology Male Mice Mice, Inbred C57BL Mice, Knockout Multipotent Stem Cells/metabolism,pathology,radiation effects Neoplasms, Radiation-Induced/etiology,genetics,pathology Pregnancy Reverse Transcriptase Polymerase Chain Reaction Stem Cells/classification,metabolism,pathology,radiation effects Time Factors Tumor Suppressor Protein p53/deficiency,physiology
Chemicals
Tumor Suppressor Protein p53 Ethylnitrosourea
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Gil-Perotin Sara
Department Neuroscience and Cell Biology, Robert Wood Johnson Medical School, Piscataway, New Jersey 08854, USA.
Marin-Husstege Mireya
Li Jiadong
Soriano-Navarro Mario
Zindy Frederique
Roussel Martine F
Garcia-Verdugo Jose-Manuel
Casaccia-Bonnefil Patricia
References (50)
50 references, click to expand
  1. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain.
    Cell. 1999 Jun 11;97(6):703-16 PMID: 10380923
  2. The subependymal layer in rodents: a site of structural plasticity and cell migration in the adult mammalian brain.
    Brain Res Bull. 1999 Jul 1;49(4):221-43 PMID: 10424843
  3. Multipotent and restricted precursors in the central nervous system.
    Anat Rec. 1999 Aug 15;257(4):137-48 PMID: 10467245
  4. Regeneration of a germinal layer in the adult mammalian brain.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11619-24 PMID: 10500226
  5. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination.
    Eur J Neurosci. 1999 Dec;11(12):4357-66 PMID: 10594662
  6. A mouse model for glioma: biology, pathology, and therapeutic opportunities.
    Toxicol Pathol. 2000 Jan-Feb;28(1):171-7 PMID: 10669005
  7. Preferential inactivation of the p53 tumor suppressor pathway and lack of EGFR amplification distinguish de novo high grade pediatric astrocytomas from de novo adult astrocytomas.
    Brain Pathol. 2000 Apr;10(2):249-59 PMID: 10764044
  8. 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
  9. Radiation-induced apoptosis in the adult central nervous system is p53-dependent.
    Cell Death Differ. 2000 Aug;7(8):712-20 PMID: 10918445
  10. Nf1;Trp53 mutant mice develop glioblastoma with evidence of strain-specific effects.
    Nat Genet. 2000 Sep;26(1):109-13 PMID: 10973261
  11. DNA damage-induced neural precursor cell apoptosis requires p53 and caspase 9 but neither Bax nor caspase 3.
    Development. 2001 Jan;128(1):137-46 PMID: 11092819
  12. Expression of the neural RNA-binding protein Musashi1 in human gliomas.
    Glia. 2001 Apr 1;34(1):1-7 PMID: 11284014
  13. Migration and multipotentiality of PSA-NCAM+ neural precursors transplanted in the developing brain.
    Mol Cell Neurosci. 2001 Jun;17(6):983-1000 PMID: 11414788
  14. Ataxia telangiectasia mutated-dependent apoptosis after genotoxic stress in the developing nervous system is determined by cellular differentiation status.
    J Neurosci. 2001 Sep 1;21(17):6687-93 PMID: 11517258
  15. Neural precursor cell apoptosis and glial tumorigenesis following transplacental ethyl-nitrosourea exposure.
    Oncogene. 2001 Dec 13;20(57):8281-6 PMID: 11781843
  16. Lack of the cell-cycle inhibitor p27Kip1 results in selective increase of transit-amplifying cells for adult neurogenesis.
    J Neurosci. 2002 Mar 15;22(6):2255-64 PMID: 11896165
  17. Transplantation of an indigenous neural stem cell population leading to hyperplasia and atypical integration.
    Cloning Stem Cells. 2002;4(1):3-8 PMID: 12006151
  18. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis.
    Cancer Cell. 2002 Apr;1(3):269-77 PMID: 12086863
  19. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro.
    Glia. 2002 Sep;39(3):193-206 PMID: 12203386
  20. Molecular genetic changes in a series of neuroepithelial tumors of childhood.
    J Neurooncol. 2002 Sep;59(2):117-22 PMID: 12241104
  21. Neural stem cells and neuro-oncology: quo vadis?
    J Cell Biochem. 2003 Jan 1;88(1):11-9 PMID: 12461769
  22. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells.
    Neuron. 2002 Dec 19;36(6):1021-34 PMID: 12495619
  23. EGF-responsive rat neural stem cells: molecular follow-up of neuron and astrocyte differentiation in vitro.
    J Cell Physiol. 2003 May;195(2):220-33 PMID: 12652649
  24. Neural stem cells: an overview.
    Circ Res. 2003 Apr 4;92(6):598-608 PMID: 12676811
  25. Complementary effects of platelet-derived growth factor autocrine stimulation and p53 or Ink4a-Arf deletion in a mouse glioma model.
    Cancer Res. 2003 Aug 1;63(15):4305-9 PMID: 12907595
  26. Shared oligodendrocyte lineage gene expression in gliomas and oligodendrocyte progenitor cells.
    J Neurosurg. 2003 Aug;99(2):344-50 PMID: 12924709
  27. p53 mutations are associated with 17p allelic loss in grade II and grade III astrocytoma.
    Cancer Res. 1992 May 15;52(10):2987-90 PMID: 1349850
  28. Expression of the class VI intermediate filament nestin in human central nervous system tumors.
    Cancer Res. 1992 Oct 1;52(19):5334-41 PMID: 1382841
  29. Distinct roles for p53, p27Kip1, and p21Cip1 during tumor development.
    Oncogene. 2004 Jan 29;23(4):905-13 PMID: 14647411
  30. For the long run: maintaining germinal niches in the adult brain.
    Neuron. 2004 Mar 4;41(5):683-6 PMID: 15003168
  31. Endogenous adult neural stem cells: limits and potential to repair the injured central nervous system.
    J Neurosci Res. 2004 Apr 15;76(2):223-31 PMID: 15048920
  32. Aberrant nestin expression during ethylnitrosourea-(ENU)-induced neurocarcinogenesis.
    Neurobiol Dis. 2004 Apr;15(3):544-52 PMID: 15056462
  33. N-ethyl-N-nitrosourea (ENU) increased brain mutations in prenatal and neonatal mice but not in the adults.
    Toxicol Sci. 2004 Sep;81(1):112-20 PMID: 15159527
  34. Development of gliomas: potential role of asymmetrical cell division of neural stem cells.
    Lancet Oncol. 2004 Aug;5(8):511-4 PMID: 15288241
  35. Molecular genetic analysis of deep-seated glioblastomas.
    Cancer Genet Cytogenet. 2004 Aug;153(1):64-8 PMID: 15325097
  36. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours.
    Nature. 1992 Mar 19;356(6366):215-21 PMID: 1552940
  37. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system.
    Science. 1992 Mar 27;255(5052):1707-10 PMID: 1553558
  38. Ethylnitrosourea induces neural progenitor cell apoptosis after S-phase accumulation in a p53-dependent manner.
    Neurobiol Dis. 2005 Feb;18(1):218-25 PMID: 15649712
  39. Isolation of immortalized, INK4a/ARF-deficient cells from the subventricular zone after in utero N-ethyl-N-nitrosourea exposure.
    J Neurosurg. 2005 Jan;102(1):98-108 PMID: 15658102
  40. Neural stem cells and neurospheres--re-evaluating the relationship.
    Nat Methods. 2005 May;2(5):333-6 PMID: 15846359
  41. Expression profile of an operationally-defined neural stem cell clone.
    Exp Neurol. 2005 Aug;194(2):320-32 PMID: 15992799
  42. The development of experimental brain tumours. A sequential light and electron microscope study of the subependymal plate. I. Early lesions (abnormal cell clusters).
    Acta Neuropathol. 1979 Mar 15;45(3):167-75 PMID: 442982
  43. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells.
    Neuron. 1994 Nov;13(5):1071-82 PMID: 7946346
  44. Long-distance neuronal migration in the adult mammalian brain.
    Science. 1994 May 20;264(5162):1145-8 PMID: 8178174
  45. Molecular pathways in the formation of gliomas.
    Glia. 1995 Nov;15(3):328-38 PMID: 8586467
  46. Silencing of p16/CDKN2 expression in human gliomas by methylation and chromatin condensation.
    Cancer Res. 1996 May 15;56(10):2405-10 PMID: 8625319
  47. Overexpression of the EGF receptor and p53 mutations are mutually exclusive in the evolution of primary and secondary glioblastomas.
    Brain Pathol. 1996 Jul;6(3):217-23; discussion 23-4 PMID: 8864278
  48. Loss of p53 is an early event in induction of brain tumors in mice by transplacental carcinogen exposure.
    Cancer Res. 1997 Feb 15;57(4):646-50 PMID: 9044841
  49. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain.
    J Neurosci. 1997 Jul 1;17(13):5046-61 PMID: 9185542
  50. Tumor-suppressor p53 is expressed in proliferating and newly formed neurons of the embryonic and postnatal rat brain: comparison with expression of the cell cycle regulators p21Waf1/Cip1, p27Kip1, p57Kip2, p16Ink4a, cyclin G1, and the proto-oncogene Bax.
    J Comp Neurol. 1998 Jul 27;397(2):181-98 PMID: 9658283
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2006-01-25
Pages
1107-16
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6674560
Subset
IM
Grants
NCI NIH HHS · CA096832 · United States
NCI NIH HHS · CA71907 · United States
NINDS NIH HHS · NS42925 · United States
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