Nitric oxide regulates astrocyte maturation in the hippocampus: Involvement of NOS2

Molecular and Cellular Neuroscience

Volumn 46, Issue 4, 2011, Pages 762-769

  Béchade, Catherine ^a,b   Pascual, Olivier ^a,b   Triller, Antoine ^a,b   Bessis, Alain ^a,b  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b CNRS   (France)

Author keywords

Astrocyte; Astrogenesis; Hippocampus; Nitric oxide; NOS2; Radial glia

Indexed keywords

CARBOXY 2 PHENYL 4,4,5,5 TETRAMETHYL IMIDAZOLINE 1 OXYL 3 OXIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; SCAVENGER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL FATE; CELL MATURATION; CONTROLLED STUDY; GLIA CELL; HIPPOCAMPUS; MOUSE; NERVE CELL MEMBRANE CONDUCTANCE; NONHUMAN; PRIORITY JOURNAL; WESTERN BLOTTING;

EID: 79953044784     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2011.02.009     Document Type: Article

References (48)

1. Akaike T., Yoshida M., Miyamoto Y., Sato K., Kohno M., Sasamoto K., Miyazaki K., Ueda S., Maeda H. Antagonistic action of imidazolineoxyl N-oxides against endothelium-derived relaxing factor/.NO through a radical reaction. Biochemistry 1993, 32:827-832.
2. Angevine J.B. Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol. Suppl. Suppl. 1965, 2:1-70.
3. Anthony T.E., Mason H.A., Gridley T., Fishell G., Heintz N. Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev. 2005, 19:1028-1033.
4. Barry G., Piper M., Lindwall C., Moldrich R., Mason S., Little E., Sarkar A., Tole S., Gronostajski R.M., Richards L.J. Specific glial populations regulate hippocampal morphogenesis. J. Neurosci. 2008, 28:12328-12340.
5. Borán M.S., García A. The cyclic GMP-protein kinase G pathway regulates cytoskeleton dynamics and motility in astrocytes. J. Neurochem. 2007, 102:216-230.
6. Bordey A., Sontheimer H. Postnatal development of ionic currents in rat hippocampal astrocytes in situ. J. Neurophysiol. 1997, 78:461-477.
7. Brahmachari S., Fung Y.K., Pahan K. Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J. Neurosci. 2006, 26:4930-4939.
8. Calabrese V., Mancuso C., Calvani M., Rizzarelli E., Butterfield D.A., Stella A.M.G. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 2007, 8:766-775.
9. Chenn A. A top-NOTCH way to make astrocytes. Dev. Cell 2009, 16:158-159.
10. Covacu R., Danilov A.I., Rasmussen B.S., Hallén K., Moe M.C., Lobell A., Johansson C.B., Svensson M.A., Olsson T., Brundin L. Nitric oxide exposure diverts neural stem cell fate from neurogenesis towards astrogliogenesis. Stem Cells 2006, 24:2792-2800.
11. Demyanenko G.P., Halberstadt A.I., Pryzwansky K.B., Werner C., Hofmann F., Maness P.F. Abnormal neocortical development in mice lacking cGMP-dependent protein kinase I. Brain Res. Dev. Brain Res. 2005, 160:1-8.
12. Domowicz M.S., Sanders T.A., Ragsdale C.W., Schwartz N.B. Aggrecan is expressed by embryonic brain glia and regulates astrocyte development. Dev. Biol. 2008, 315:114-124.
13. Emirandetti A., Simões G.F., Zanon R.G., Oliveira A.L.R. Spinal motoneuron synaptic plasticity after axotomy in the absence of inducible nitric oxide synthase. J. Neuroinflammation 2010, 7:31.
14. Freeman M.R. Specification and morphogenesis of astrocytes. Science 2010, 330:774-778.
15. Giaume C., Koulakoff A., Roux L., Holcman D., Rouach N. Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat. Rev. Neurosci. 2010, 11:87-99.
16. Götz M., Barde Y. Radial glial cells defined and major intermediates between embryonic stem cells and CNS neurons. Neuron 2005, 46:369-372.
17. Hartfuss E., Galli R., Heins N., Götz M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 2001, 229:15-30.
18. Hertz L., Zielke H.R. Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci. 2004, 27:735-743.
19. Jones T.A., Hawrylak N., Greenough W.T. Rapid laminar-dependent changes in GFAP immunoreactive astrocytes in the visual cortex of rats reared in a complex environment. Psychoneuroendocrinology 1996, 21:189-201.
20. Kafitz K.W., Meier S.D., Stephan J., Rose C.R. Developmental profile and properties of sulforhodamine 101-labeled glial cells in acute brain slices of rat hippocampus. J. Neurosci. Meth. 2008, 169:84-92.
21. Kressin K., Kuprijanova E., Jabs R., Seifert G., Steinhäuser C. Developmental regulation of Na+ and K+ conductances in glial cells of mouse hippocampal brain slices. Glia 1995, 15:173-187.
22. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32:149-184.
23. Kuzin B., Roberts I., Peunova N., Enikolopov G. Nitric oxide regulates cell proliferation during Drosophila development. Cell 1996, 87:639-649.
24. Lee S., Park J., Lee W., Kim H., Park H., Mori K., Suk K. Lipocalin-2 is an autocrine mediator of reactive astrocytosis. J. Neurosci. 2009, 29:234-249.
25. Li W.E., Nagy J.I. Connexin43 phosphorylation state and intercellular communication in cultured astrocytes following hypoxia and protein phosphatase inhibition. Eur. J. Neurosci. 2000, 12:2644-2650.
26. MacMicking J.D., Nathan C., Hom G., Chartrain N., Fletcher D.S., Trumbauer M., Stevens K., Xie Q.W., Sokol K., Hutchinson N. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 1995, 81:641-650.
27. Matthias K., Kirchhoff F., Seifert G., Hüttmann K., Matyash M., Kettenmann H., Steinhäuser C. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J. Neurosci. 2003, 23:1750-1758.
28. Miller F.D., Gauthier A.S. Timing is everything: making neurons versus glia in the developing cortex. Neuron 2007, 54:357-369.
29. Moreno-López B., Romero-Grimaldi C., Noval J.A., Murillo-Carretero M., Matarredona E.R., Estrada C. Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J. Neurosci. 2004, 24:85-95.
30. Müller C.M. Dark-rearing retards the maturation of astrocytes in restricted layers of cat visual cortex. Glia 1990, 3:487-494.
31. Nakahira E., Yuasa S. Neuronal generation, migration, and differentiation in the mouse hippocampal primoridium as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation. J. Comp. Neurol. 2005, 483:329-340.
32. Noctor S.C., Martínez-Cerdeño V., Kriegstein A.R. Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J. Comp. Neurol. 2008, 508:28-44.
33. Norenberg M.D., Martinez-Hernandez A. Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res. 1979, 161:303-310.
34. Oliet S.H., Piet R., Poulain D.A. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 2001, 292:923-926.
35. Packer M.A., Stasiv Y., Benraiss A., Chmielnicki E., Grinberg A., Westphal H., Goldman S.A., Enikolopov G. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9566-9571.
36. Peunova N., Enikolopov G. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 1995, 375:68-73.
37. Peunova N., Scheinker V., Cline H., Enikolopov G. Nitric oxide is an essential negative regulator of cell proliferation in Xenopus brain. J. Neurosci. 2001, 21:8809-8818.
38. Reif A., Schmitt A., Fritzen S., Chourbaji S., Bartsch C., Urani A., Wycislo M., Mössner R., Sommer C., Gass P., Lesch K. Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behaviour. Eur. J. Neurosci. 2004, 20:885-895.
39. Rouach N., Glowinski J., Giaume C. Activity-dependent neuronal control of gap-junctional communication in astrocytes. J. Cell Biol. 2000, 149:1513-1526.
40. Scemes E., Giaume C. Astrocyte calcium waves: what they are and what they do. Glia 2006, 54:716-725.
41. Seifert G., Carmignoto G., Steinhäuser C. Astrocyte dysfunction in epilepsy. Brain Res. Rev. 2010, 63:212-221.
42. Tang X., Falls D.L., Li X., Lane T., Luskin M.B. Antigen-retrieval procedure for bromodeoxyuridine immunolabeling with concurrent labeling of nuclear DNA and antigens damaged by HCl pretreatment. J. Neurosci. 2007, 27:5837-5844.
43. Theodosis D.T., Poulain D.A., Oliet S.H.R. Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol. Rev. 2008, 88:983-1008.
44. Volterra A., Meldolesi J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 2005, 6:626-640.
45. Wakselman S., Béchade C., Roumier A., Bernard D., Triller A., Bessis A. Developmental neuronal death in hippocampus requires the microglial CD11b integrin and DAP12 immunoreceptor. J. Neurosci. 2008, 28:8138-8143.
46. Wang D.D., Bordey A. The astrocyte odyssey. Prog. Neurobiol 2008, 86:342-367.
47. Zhou M., Schools G.P., Kimelberg H.K. Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J. Neurophysiol. 2006, 95:134-143.
48. Zhu D.Y., Liu S.H., Sun H.S., Lu Y.M. Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J. Neurosci. 2003, 23:223-229.