Neuronal nitric oxide synthase-derived nitric oxide inhibits neurogenesis in the adult dentate gyrus by down-regulating cyclic AMP response element binding protein phosphorylation

Neuroscience

Volumn 141, Issue 2, 2006, Pages 827-836

  Zhu, X J ^a   Hua, Y ^a   Jiang, J ^a   Zhou, Q G ^a   Luo, C X ^a   Han, X ^a   Lu, Y M ^b   Zhu, D Y ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

7 nitroindazole; hippocampus; MK 801; NMDA receptors; proliferation

Indexed keywords

7 NITROINDAZOLE; BINDING PROTEIN; BROXURIDINE; CYCLIC AMP; DIZOCILPINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DNA RESPONSIVE ELEMENT; DRUG EFFECT; MALE; MOUSE; MOUSE STRAIN; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STEM CELL;

ANIMALS; BLOTTING, WESTERN; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DENTATE GYRUS; DIZOCILPINE MALEATE; DRUG INTERACTIONS; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; IMMUNOHISTOCHEMISTRY; INDAZOLES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PHOSPHORYLATION; SERINE;

EID: 33746310878     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.04.032     Document Type: Article

References (74)

1. Aarts M., Liu Y., Liu L., Besshoh S., Arundine M., Gurd J.W., Wang Y.T., Salter M.W., and Tymianski M. Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science 298 (2002) 846-850
2. Aberg M.A.I., Aberg N.D., Hedbacker H., Oscarsson J., and Eriksson P.S. Peripheral infusion of IGF-1 selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 20 (2000) 2896-2903
3. Altman J., and Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124 (1965) 319-335
4. Arvidsson A., Kokaia Z., and Lindvall O. N-methyl-D-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur J Neurosci 14 (2001) 10-18
5. Baranano D.E., Ferris C.D., and Snyder S.H. A typical neural messengers. Trends Neurosci 24 (2001) 99-106
6. Barnea A., and Nottebohm F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci U S A 91 (1994) 11217-11221
7. Benraiss A., Chmielnicki E., Lerner K., Roh D., and Goldman S.A. Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J Neurosci 21 (2001) 6718-6731
8. Bonni A., Brunet A., West A.E., Datta S.R., Takasu M.A., and Greenberg M.E. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286 (1999) 1358-1362
9. Bredt D.S., Hwang P.M., and Snyder S.H. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347 (1990) 768-770
10. Bush M.A., and Pollack G.M. Pharmacokinetics and protein binding of the selective neuronal nitric oxide synthase inhibitor 7-nitroindazole. Biopharm Drug Dispos 21 (2000) 221-228
11. Cameron H.A., and McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435 (2001) 406-417
12. Cammarota M., Bevilaqua L.R., Ardenghi P., Paratcha G., Levi de Stein M., Izquierdo I., and Medina J.H. Learning-associated activation of nuclear MAPK, CREB and Elk-1, along with Fos production, in the rat hippocampus after a one-trial avoidance learning. abolition by NMDA receptor blockade. Mol Brain Res 76 (2000) 36-46
13. Chen J., Tu Y., Moon C., Matarazzo V., Palmer A.M., and Ronnett G.V. The localization of neuronal nitric oxide synthase may influence its role in neuronal precursor proliferation and synaptic maintenance. Dev Biol 269 (2004) 165-182
14. Cotman C.W., and Berchtold N.C. Exercise. a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25 (2002) 295-301
15. Dayer A.G., Ford A.A., Cleaver K.M., Yassaee M., and Cameron H.A. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460 (2003) 563-572
16. Deisseroth K., Singla S., Toda H., Monje M., Palmer T.D., and Malenka R.C. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42 (2004) 535-552
17. Dinerman J.L., Dawson T.M., Schell M.J., Snowman A., and Snyder S.H. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells. implications for synaptic plasticity. Proc Natl Acad Sci U S A 91 (1994) 4214-4218
18. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., and Gage F.H. Neurogenesis in the adult human hippocampus. Nat Med 4 (1998) 1313-1317
19. Feldman P.L., Griffith O.W., Hong H., and Stuehr D.J. Irreversible inactivation of macrophage and brain nitric oxide synthase by L-NG-methylarginine requires NADPH-dependent hydroxylation. J Med Chem 36 (1993) 491-496
20. Gage F.H., Kemperman G., Palmer T.D., Peterson D.A., and Ray J. Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol 36 (1998) 249-266
21. Garthwaite J., and Boulton C.L. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57 (1995) 683-706
22. Ghosh A., Ginty D.D., Bading H., and Greenberg M.E. Calcium regulation of gene expression in neuronal cells. J Neurobiol 25 (1994) 294-303
23. Gundersen H.J., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., and Pakkenberg. The new stereological tools. disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. Acta Pathol Microbiol Immunol Scand 96 (1988) 857-881
24. Hardingham G.E., Anorld F.J., and Bading H. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat Neurosci 4 (2001) 261-267
25. Hardingham G.E., Chawla S., Cruzalegui F.H., and Bading H. Control of recruitment and transcription-activating function of CBP determines gene regulation by NMDA receptors and L-type calcium channels. Neuron 22 (1999) 789-798
26. Herman M., Schultz C.A., and Claude P. Responses to cAMP depend on stage of neuronal differentiation of NGF-treated adrenal chromaffin cells. Dev Biol 161 (1994) 477-489
27. Hu B.R., Fux C.M., Marton M.E., Zivin J.A., and Ellisman M.H. Persistent phosphorylation of cyclic AMP responsive element-binding protein and activating transcription factor-2 transcription. factors following transient cerebral ischemia in rat brain. Neuroscience 89 (1999) 437-452
28. Hu S.C., Chrivia J., and Ghosh A. Regulation of CBP-mediated transcription by neuronal calcium signaling. Neuron 22 (1999) 799-808
29. Islam A.T., Kuraoka A., and Kawabuchi M. Morphological basis of nitric oxide production and its correlation with the polysialylated precursor cells in the dentate gyrus of the adult guinea pig hippocampus. Anat Sci Int 78 (2003) 98-103
30. Kaplan M.S., and Hinds J.W. Neurogenesis in the adult rat. electron microscopic analysis of light radioautographs. Science 197 (1977) 1092-1094
31. Kempermann G., Kuhn H.G., and Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 386 (1997) 493-495
32. Kornack D.R., and Rakic P. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci U S A 96 (1999) 5768-5773
33. Kuhn H.G., Dickinson-Anson H., and Gage F.H. Neurogenesis in the dentate gyrus of the adult rat. age-related decrease of neuronal progenitor proliferation. J Neurosci 16 (1996) 2027-2033
34. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., and Gage F.H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17 (1997) 5820-5829
35. Lipton S.A., Choi Y.B., Pan Z.H., Lei S.Z., Chen H.S., Sucher N.J., Loscalzo J., Singel D.J., and Stamler J.S. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364 (1993) 626-632
36. Lipton S.A. Neuronal protection and destruction by NO. Cell Death Differ 6 (1999) 943-951
37. Liu S.H., Wang J., Zhu D.Y., Fu Y.P., Lukowiak K., and Lu Y.M. Generation of functional inhibitory neurons in the adult rat hippocampus. J Neurosci 23 (2003) 732-736
38. Liu P.K., Robertson C.S., and Valadka A. The association between neuronal nitric oxide synthase and neuronal sensitivity in the brain after brain injury. Ann N Y Acad Sci 962 (2002) 226-241
39. Lu D., Mahmood A., Zhang R., and Copp M. Upregulation of neurogenesis and reduction in functional deficits following administration of DEtA/NONOate, a nitric oxide donor, after traumatic brain injury in rats. J Neurosurg 99 (2003) 351-361
40. Luo C.X., Zhu X.J., Zhang A.X., Wang W., Yang X.M., Liu S.H., Han X., Sun J., Zhang S.G., Lu Y., and Zhu D.Y. Blockade of L-type voltage-gated Ca channel inhibits ischemia-induced neurogenesis by down-regulating iNOS expression in adult mouse. J Neurochem 94 (2005) 1077-1086
41. Mayr B.M., Canettieri G., and Montminy M.R. Distinct effects of cAMP and mitogenic signals on CREB-binding protein recruitment impart specificity to target gene activation via CREB. Proc Natl Acad Sci U S A 98 (2001) 10936-10941
42. Moreno-López B., Romero-Grimaldi C., Noval J.A., Murillo-Carretero M., Esperanza R., and Matarredona Estrada C. Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J Neurosci 24 (2004) 85-95
43. Moreno-López B., Noval J.A., Gonzalez-Bonet L.G., and Estrada C. Morphological bases for a role of nitric oxide in adult neurogenesis. Brain Res 869 (2000) 244-250
44. Nakagawa S., Kim J.-E., Lee R., Chen J., and Jessica E. Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 26 (2002) 3673-3682
45. Nilsson M., Perfilieva E., Johansson U., Orwar O., and Eriksson P.S. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39 (1999) 569-578
46. Paakkari I., and Lindsberg P. Nitric oxide in the central nervous system. Ann Med 27 (1995) 369-377
47. Packer M.A., Stasiv Y., Benraiss A., Chmielnicki E., Grinberg A., Westphal H., Goldman S.A., and Enikolopov G. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci U S A 100 (2003) 9566-9571
48. Palmer T., Takahashi J., and Gage F.H. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 8 (1997) 389-404
49. Palmer T., Willhoite A.R., and Gage F.H. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425 (2000) 479-494
50. Parent J.M. Injury-induced neurogenesis in the adult mammalian brain. Neuroscientist 9 (2003) 261-272
51. Park C., Kang M., Kwon Y.K., Chung J.H., Ahn H., and Huh Y. Inhibition of neuronal nitric oxide synthase enhances cell proliferation in the dentate gyrus of the adrenalectomized rat. Neurosci Lett 309 (2001) 9-12
52. Paton J.A., and Nottebohm F. Neurons generated in the adult brain are recruited into functional circuits. Science 225 (1984) 1046-1048
53. Pencea V., Bingaman K.D., Wiegand S.J., and Luskin M.B. Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21 (2001) 6706-6717
54. Peunova N., and Enikolopov G. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 375 (1995) 68-73
55. Peunova N., Scheinker V., Cline H., and Enikolopov G. Nitric oxide is an essential regulator of cell proliferation in Xenopus brain. J Neurosci 21 (2001) 8809-8818
56. Reif A., Schmitt A., Fritzen S., Chourbaji S., Bartsch C., Urani A., Wycislo M., Mossner R., Sommer C., Gass P., and Lesch K.P. Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behaviour. Eur J Neurosci 20 (2004) 885-895
57. Riccio A., Ahn S., Davenport C.M., Blendy J.A., and Ginty D.D. Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286 (1999) 2358-2361
58. Rodrigo J., Springall D.R., Uttenthal O., Bentura M.L., Abadia-Molina F., Riveros-Moreno V., Marti{dotless}nez-Murillo R., Polak J.M., and Moncada S. Localization of nitric oxide synthase in the adult rat brain. Philos Trans R Soc Lond B 345 (1994) 175-221
59. Satoh J., Tabira T., and Kim S.U. Rapidly proliferating glial cells isolated from adult mouse brain have a differentiative capacity in response to cyclic AMP. Neurosci Res 20 (1994) 175-184
60. Shariful Islam A.T., Nakamura K., Seki T., Kuraoka A., Hirata K., Emson P.C., and Kawabuchi M. Expression of NOS, PSA-N-CAM and S100 protein in the granule cell migration pathway of the adult guinea pig forebrain. Brain Res Dev Brain Res 107 (1998) 191-205
61. Shaywitz A.J., and Greenberg M.E. CREB. a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68 (1999) 821-861
62. Storvik M., Linden A.M., Kontkanen O., Lakso M., Castren E., and Wong G. Induction of cAMP response element modulator (CREM) and inducible cAMP early repressor (ICER) expression in rat brain by uncompetitive N-methyl-D-aspartate receptor antagonists. J Pharm Exp Ther 294 (2000) 52-60
63. Sun F.Y., and Guo X. Molecular and cellular mechanisms of neuroprotection by vascular endothelial growth factor. J Neurosci Res 79 (2005) 180-184
64. van Praag H., Schinder A.F., Christis B.R., Toni N., Palmer N., and Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 415 (2002) 1030-1034
65. van Praag H., Christie B.R., Sejnowski T.J., and Gage F.H. Running enhances neurogenesis, learning and long-term potentiation in mice. Proc Natl Acad Sci U S A 96 (1999) 13427-13431
66. van Praag H., Kempermann G., and Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2 (1999) 266-270
67. Wagner J.P., Black I.B., and DiCicco-Bloom E. Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J Neurosci 19 (1999) 6006-6016
68. Walton M.R., and Dragunow M. Is CREB a key to neuronal survival?. Trends Neurosci 23 (2000) 48-53
69. Wang T., FitzGerald T.J., and Haregewoin A. Differential expression of nitric oxide synthases in EGF-responsive mouse neural precursor cells. Cell Tissue Res 296 (1999) 489-497
70. Wang Y., Newton D.C., and Marsden P.A. Neuronal NOS. gene structure, mRNA diversity, and functional relevance. Crit Rev Neurobiol 13 (1999) 21-43
71. 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
72. Zhu D.Y., Deng Q., Yao H.H., Wang D.C., Deng Y., and Liu G.Q. Inducible nitric oxide synthase expression in the ischemic core and penumbra after transient focal cerebral ischemia in mice. Life Sci 71 (2002) 1985-1996
73. Zhu D.Y., Lau L., Wei J.S., Liu S.H., and Lu Y.M. Activation of cAMP-response-element-binding protein (CREB) after focal cerebral ischemia stimulates neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci U S A 101 (2004) 9453-9457
74. Zhu D.Y., Liu S.H., Sun S.H., and Lu Y.M. Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult animal dentate gyrus. J Neurosci 23 (2003) 223-229