Quiescent neural stem cells exit dormancy upon alteration of GABAAR signaling following radiation damage

Stem Cell Research

Volumn 11, Issue 1, 2013, Pages 516-528

  Daynac, Mathieu ^a,b,c   Chicheportiche, Alexandra ^a,b,c   Pineda, Jose R ^a,b,c   Gauthier, Laurent R ^a,b,c   Boussin, François D ^a,b,c   Mouthon, Marc André ^a,b,c  

^a Universite Paris Sud   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Dcx; FUCCI; GFAP; GLAST; LeX; NSC; SVZ; TAC

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; CD15 ANTIGEN; CD24 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; HOE 33342;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; DORMANCY; FLUORESCENCE ACTIVATED CELL SORTING; GAMMA RADIATION; IRRADIATION; MOUSE; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; RADIATION INJURY; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; NEURONS; RECEPTORS, GABA-A; SIGNAL TRANSDUCTION;

MUS;

EID: 84876314854     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.02.008     Document Type: Article

References (40)

1. Alfonso J., Le Magueresse C., Zuccotti A., Khodosevich K., Monyer H. Diazepam binding inhibitor promotes progenitor proliferation in the postnatal SVZ by reducing GABA signaling. Cell Stem Cell 2012, 10(1):76-87.
2. Bellinzona M., Gobbel G.T., Shinohara C., Fike J.R. Apoptosis is induced in the subependyma of young adult rats by ionizing irradiation. Neurosci. Lett. 1996, 208(3):163-166.
3. Ben Abdallah N.M., Slomianka L., Lipp H.P. Reversible effect of X-irradiation on proliferation, neurogenesis, and cell death in the dentate gyrus of adult mice. Hippocampus 2007, 17(12):1230-1240. 10.1002/hipo.20358.
4. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 2003, 467(1):1-10.
5. Calaora V., Chazal G., Nielsen P.J., Rougon G., Moreau H. mCD24 expression in the developing mouse brain and in zones of secondary neurogenesis in the adult. Neuroscience 1996, 73(2):581-594.
6. Capela A., Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002, 35(5):865-875.
7. Carlen M., Meletis K., Goritz C., Darsalia V., Evergren E., et al. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat. Neurosci. 2009, 12(3):259-267.
8. Chevalier F., Chicheportiche A., Daynac M., Depagne J., Bertrand P., Boussin F.D., et al. Identification of factors involved in neurogenesis recovery after irradiation of the adult mouse subventricular zone: a preliminary study. Proteomics - Human Diseases and Protein Functions 2012, vol. 1:327-346. InTech, Rijeka. T.K. Man, R.J. Flores (Eds.).
9. Chow B.M., Li Y.Q., Wong C.S. Radiation-induced apoptosis in the adult central nervous system is p53-dependent. Cell Death Differ. 2000, 7(8):712-720.
10. Costa M.R., Ortega F., Brill M.S., Beckervordersandforth R., Petrone C., Schroeder T., et al. Continuous live imaging of adult neural stem cell division and lineage progression in vitro. Development 2011, 138(6):1057-1068.
11. Doetsch F. The glial identity of neural stem cells. Nat. Neurosci. 2003, 6(11):1127-1134.
12. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97(6):703-716.
13. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(20):11619-11624.
14. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002, 36(6):1021-1034.
15. Fernando R.N., Eleuteri B., Abdelhady S., Nussenzweig A., Andang M., Ernfors P. Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(14):5837-5842.
16. Garcia A.D., Doan N.B., Imura T., Bush T.G., Sofroniew M.V. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 2004, 7(11):1233-1241.
17. Groszer M., Erickson R., Scripture-Adams D.D., Dougherty J.D., Le Belle J., Zack J.A., et al. PTEN negatively regulates neural stem cell self-renewal by modulating G0-G1 cell cycle entry. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(1):111-116.
18. Haydar T.F., Wang F., Schwartz M.L., Rakic P. Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J. Neurosci. 2000, 20(15):5764-5774.
19. Kippin T.E., Martens D.J., van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev. 2005, 19(6):756-767.
20. Lazarini F., Mouthon M.A., Gheusi G., de Chaumont F., Olivo-Marin J.C., Lamarque S., et al. Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS One 2009, 4(9):e7017.
21. Liu X., Wang Q., Haydar T.F., Bordey A. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat. Neurosci. 2005, 8(9):1179-1187.
22. Lois C., Garcia-Verdugo J.M., Alvarez-Buylla A. Chain migration of neuronal precursors. Science 1996, 271(5251):978-981.
23. LoTurco J.J., Owens D.F., Heath M.J., Davis M.B., Kriegstein A.R. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 1995, 15(6):1287-1298.
24. Michelot D., Melendez-Howell L.M. Amanita muscaria: chemistry, biology, toxicology, and ethnomycology. Mycol. Res. 2003, 107(Pt 2):131-146.
25. Mori T., Tanaka K., Buffo A., Wurst W., Kuhn R., Gotz M. Inducible gene deletion in astroglia and radial glia - a valuable tool for functional and lineage analysis. Glia 2006, 54(1):21-34.
26. Morshead C.M., Reynolds B.A., Craig C.G., McBurney M.W., Staines W.A., Morassutti D., et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 1994, 13(5):1071-1082.
27. Mouthon M.-A., Fouchet P., Mathieu C., Sii-Felice K., Etienne O., et al. Neural stem cells from mouse forebrain are contained in a population distinct from the 'side population'. J. Neurochem. 2006, 99(3):807-817.
28. Nguyen L., Malgrange B., Breuskin I., Bettendorff L., Moonen G., et al. Autocrine/paracrine activation of the GABA(A) receptor inhibits the proliferation of neurogenic polysialylated neural cell adhesion molecule-positive (PSA-NCAM+) precursor cells from postnatal striatum. J. Neurosci. 2003, 23(8):3278-3294.
29. Obermair F.J., Fiorelli R., Schroeter A., Beyeler S., Blatti C., et al. A novel classification of quiescent and transit amplifying adult neural stem cells by surface and metabolic markers permits a defined simultaneous isolation. Stem Cell Res. 2010, 5(2):131-143.
30. Parras C.M., Galli R., Britz O., Soares S., Galichet C., Battiste J., et al. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 2004, 23(22):4495-4505.
31. Pastrana E., Cheng L.C., Doetsch F. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(15):6387-6392.
32. Pineda J.R., Daynac M., Chicheportiche A., Cebrian-Silla A., Sii-Felice K., Garcia-Verdugo J.-M., et al. Vascular-derived TGF-β increases in stem cell niche and perturbs neurogenesis during aging and irradiation in the adult mouse brain. EMBO Mol. Med. 2013, 10.1002/emmm.201202197.
33. Platel J.C., Stamboulian S., Nguyen I., Bordey A. Neurotransmitter signaling in postnatal neurogenesis: the first leg. Brain Res. Rev. 2010, 63(1-2):60-71.
34. Ren S., Rollins B.J. Cyclin C/cdk3 promotes Rb-dependent G0 exit. Cell 2004, 117(2):239-251.
35. Sakaue-Sawano A., Kurokawa H., Morimura T., Hanyu A., Hama H., Osawa H., et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 2008, 132(3):487-498.
36. Shinohara C., Gobbel G.T., Lamborn K.R., Tada E., Fike J.R. Apoptosis in the subependyma of young adult rats after single and fractionated doses of X-rays. Cancer Res. 1997, 57(13):2694-2702.
37. Sii-Felice K., Etienne O., Hoffschir F., Mathieu C., Riou L., Barroca V., et al. Fanconi DNA repair pathway is required for survival and long-term maintenance of neural progenitors. EMBO J. 2008, 27(5):770-781.
38. Song J., Zhong C., Bonaguidi M.A., Sun G.J., Hsu D., Gu Y., et al. Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 2012, 10.1038/nature11306.
39. Tada E., Yang C., Gobbel G.T., Lamborn K.R., Fike J.R. Long-term impairment of subependymal repopulation following damage by ionizing irradiation. Exp. Neurol. 1999, 160(1):66-77.
40. Wang D.D., Krueger D.D., Bordey A. GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J. Physiol. 2003, 550(Pt 3):785-800.