The Notch pathway mediates expansion of a progenitor pool and neuronal differentiation in adult neural progenitor cells after stroke

Neuroscience

Volumn 158, Issue 4, 2009, Pages 1356-1363

  Wang, L ^a   Chopp, M ^a,b   Zhang, R L ^a   Zhang, L ^a   LeTourneau, Y ^a   Feng, Y F ^a   Jiang, A ^a   Morris, D C ^c   Zhang, Z G ^a  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

^c HENRY FORD HEALTH SCIENCES CENTER   (United States)

Author keywords

differentiation; neural progenitor cell; Notch pathway; proliferation; rat; stroke

Indexed keywords

GAMMA SECRETASE INHIBITOR; NOTCH RECEPTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR HES 1;

ADULT ANIMAL; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; IMMUNOCYTOCHEMISTRY; INTRACELLULAR MEMBRANE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; STROKE; SUBVENTRICULAR ZONE; WESTERN BLOTTING; WISTAR RAT;

ADULT STEM CELLS; ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL VENTRICLES; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; INFARCTION, MIDDLE CEREBRAL ARTERY; LEUKEMIA INHIBITORY FACTOR; MALE; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; RATS; RATS, WISTAR; RECEPTORS, NOTCH; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION; TRIGLYCERIDES;

EID: 60149094194     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.10.064     Document Type: Article

References (44)

1. Alexson T.O., Hitoshi S., Coles B.L., Bernstein A., and van der Kooy D. Notch signaling is required to maintain all neural stem cell populations-irrespective of spatial or temporal niche. Dev Neurosci 28 1-2 (2006) 34-48
2. Androutsellis-Theotokis A., Leker R.R., Soldner F., Hoeppner D.J., Ravin R., Poser S.W., Rueger M.A., Bae S.K., Kittappa R., and McKay R.D. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442 (2006) 823-826
3. Arvidsson A., Collin T., Kirik D., Kokaia Z., and Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8 (2002) 963-970
4. Chen J., Zacharek A., Li A., Cui X., Roberts C., Lu M., and Chopp M. Atorvastatin promotes presenilin-1 expression and Notch1 activity and increases neural progenitor cell proliferation after stroke. Stroke 39 (2008) 220-226
5. Chiasson B.J., Tropepe V., Morshead C.M., and van der Kooy D. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci 19 11 (1999) 4462-4471
6. Chigurupati S., Arumugam T.V., Son T.G., Lathia J.D., Jameel S., Mughal M.R., Tang S.C., Jo D.G., Camandola S., Giunta M., Rakova I., McDonnell N., Miele L., Mattson M.P., and Poosala S. Involvement of notch signaling in wound healing. PLoS ONE 2 (2007) e1167
7. Covey M.V., and Levison S.W. Leukemia inhibitory factor participates in the expansion of neural stem/progenitors after perinatal hypoxia/ischemia. Neuroscience 148 (2007) 501-509
8. Curry C.L., Reed L.L., Nickoloff B.J., Miele L., and Foreman K.E. Notch-independent regulation of Hes-1 expression by c-Jun N-terminal kinase signaling in human endothelial cells. Lab Invest 86 (2006) 842-852
9. Felling R.J., Snyder M.J., Romanko M.J., Rothstein R.P., Ziegler A.N., Yang Z., Givogri M.I., Bongarzone E.R., and Levison S.W. Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J Neurosci 26 (2006) 4359-4369
10. Fuentealba R.A., Barria M.I., Lee J., Cam J., Araya C., Escudero C.A., Inestrosa N.C., Bronfman F.C., Bu G., and Marzolo M.P. ApoER2 expression increases Abeta production while decreasing amyloid precursor protein (APP) endocytosis: Possible role in the partitioning of APP into lipid rafts and in the regulation of gamma-secretase activity. Mol Neurodegener 2 (2007) 14
11. Gaiano N., and Fishell G. The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 25 (2002) 471-490
12. Givogri M.I., de Planell M., Galbiati F., Superchi D., Gritti A., Vescovi A., de Vellis J., and Bongarzone E.R. Notch signaling in astrocytes and neuroblasts of the adult subventricular zone in health and after cortical injury. Dev Neurosci 28 (2006) 81-91
13. Gritti A., Parati E.A., Cova L., Frolichsthal P., Galli R., Wanke E., Faravelli L., Morassutti D.J., Roisen F., Nickel D.D., and Vescovi A.L. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 16 (1996) 1091-1100
14. Guentchev M., and McKay R.D. Notch controls proliferation and differentiation of stem cells in a dose-dependent manner. Eur J Neurosci 23 (2006) 2289-2296
15. Gustafsson M.V., Zheng X., Pereira T., Gradin K., Jin S., Lundkvist J., Ruas J.L., Poellinger L., Lendahl U., and Bondesson M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9 (2005) 617-628
16. Hitoshi S.A.T., Tropepe V., Donoviel D., Elia A.J., Nye J.S., Conlon R.A., Mak T.W., Bernstein A., and van der Kooy D. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 16 7 (2002) 846-858
17. Hoe H.S., and Rebeck G.W. Regulation of ApoE receptor proteolysis by ligand binding. Brain Res Mol Brain Res 137 (2005) 31-39
18. Iso T., Kedes L., and Hamamori Y. HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 194 (2003) 237-255
19. Jin G., Omori N., Li F., Nagano I., Manabe Y., Shoji M., and Abe K. Protection against ischemic brain damage by GDNF affecting cell survival and death signals. Neurol Res 25 (2003) 249-253
20. Jones P., May G., Healy L., Brown J., Hoyne G., Delassus S., and Enver T. Stromal expression of Jagged 1 promotes colony formation by fetal hematopoietic progenitor cells. Blood 92 (1998) 1505-1511
21. Kawai T., Takagi N., Nakahara M., and Takeo S. Changes in the expression of Hes5 and Mash1 mRNA in the adult rat dentate gyrus after transient forebrain ischemia. Neurosci Lett 380 (2005) 17-20
22. Liu X.S., Zhang Z., Zhang R., Gregg S.R., Meng H., and Chopp M. Comparison of in vivo and in vitro gene expression profiles in subventricular zone neural progenitor cells from the adult mouse after middle cerebral artery occlusion. Neuroscience 146 (2007) 1053-1061
23. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25 (2001) 402-408
24. Mizutani K., Yoon K., Dang L., Tokunaga A., and Gaiano N. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449 (2007) 351-355
25. Morrison S.J., Perez S.E., Qiao Z., Verdi J.M., Hicks C., Weinmaster G., and Anderson D.J. Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101 (2000) 499-510
26. Morshead C.M., Reynolds B.A., Craig C.G., McBurney M.W., Staines W.A., Morassutti D., Weiss S., and van der Kooy D. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13 (1994) 1071-1082
27. Nagao M., and Nakafuku M. Cross talk between Notch and growth factor/cytokine signaling pathways in neural stem cells. Mol Cell Biol 27 (2007) 3982-3994
28. Nagao M., Sugimori M., and Nakafuku M. Cross talk between notch and growth factor/cytokine signaling pathways in neural stem cells. Mol Cell Biol 27 (2007) 3982-3994
29. Ohtsuka T., Ishibashi M., Gradwohl G., Nakanishi S., Guillemot F., and Kageyama R. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J 18 8 (1999) 2196-2207
30. Olivier A., Lauret E., Gonin P., and Galy A. The Notch ligand delta-1 is a hematopoietic development cofactor for plasmacytoid dendritic cells. Blood 107 (2006) 2694-2701
31. Oya S., Yoshikawa G., Takai K., Tanaka J., Higashiyama S., Saito N., Kirino T., and Kawahara N. Region-specific proliferative response of neural progenitors to exogenous stimulation by growth factors following ischemia. Neuroreport 19 (2008) 805-809
32. Parent J.M., Vexler Z.S., Gong C., Derugin N., and Ferriero D.M. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52 (2002) 802-813
33. Redmond L., Oh S.R., Hicks C., Weinmaster G., and Ghosh A. Nuclear Notch1 signaling and the regulation of dendritic development. Nat Neurosci 3 (2000) 30-40
34. Reynolds B.A., and Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255 (1992) 1707-1710
35. Scholzke M.N., and Schwaninger M. Transcriptional regulation of neurogenesis: potential mechanisms in cerebral ischemia. J Mol Med 85 (2007) 577-588
36. Wang L., Zhang Z., Zhang R., and Chopp M. Activation of the PI3-K/Akt pathway mediates cGMP enhanced-neurogenesis in the adult progenitor cells derived from the subventricular zone. J Cereb Blood Flow Metab 25 (2005) 1150-1158
37. Wang L., Zhang Z., Wang Y., Zhang R., and Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35 (2004) 1732-1737
38. Wang L., Zhang Z., Zhang R., Jiao Z., Wang Y., Pourabdollah-Nejad D.S., LeTourneau Y., Gregg S.R., and Chopp M. Neurogenin 1 mediates erythropoietin enhanced differentiation of adult neural progenitor cells. J Cereb Blood Flow Metab 26 (2006) 556-564
39. Yoon K., and Gaiano N. Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat Neurosci 8 (2005) 709-715
40. Zhang R., Zhang L., Zhang Z., Wang Y., Lu M., Lapointe M., and Chopp M. A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 50 (2001) 602-611
41. Zhang R., Wang L., Zhang L., Chen J., Zhu Z., Zhang Z., and Chopp M. Nitric oxide enhances angiogenesis via the synthesis of vascular endothelial growth factor and cGMP after stroke in the rat. Circ Res 92 (2003) 308-313
42. Zhang R., Zhang Z., Wang L., Wang Y., Gousev A., Zhang L., Ho K.L., Morshead C., and Chopp M. Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 24 (2004) 441-448
43. Zhang R., Zhang Z., Lu M., Wang Y., Yang J.J., and Chopp M. Reduction of the cell cycle length by decreasing G1 phase and cell cycle reentry expand neuronal progenitor cells in the subventricular zone of adult rat after stroke. J Cereb Blood Flow Metab 26 (2006) 857-863
44. Zhang Z., Zhang R., Jiang Q., Raman S.B., Cantwell L., and Chopp M. A new rat model of thrombotic focal cerebral ischemia. J Cereb Blood Flow Metab 17 (1997) 123-135