Norepinephrine and nitric oxide promote cell survival signaling in hippocampal neurons

European Journal of Pharmacology

Volumn 633, Issue 1-3, 2010, Pages 1-9

  Patel, Neha J ^a   Chen, Michael J ^a   Russo Neustadt, Amelia A ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Akt; BDNF; CREB; Hippocampus; Nitric oxide; Norepinephrine

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CLONIDINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE INHIBITOR; NITRITE; NORADRENALIN; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL ASSAY; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; FEMALE; HIPPOCAMPUS; IMMUNOREACTIVITY; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; NUTRIENT; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; CELLS, CULTURED; CLONIDINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FOOD; HIPPOCAMPUS; NEURONS; NEUROPROTECTIVE AGENTS; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITROPRUSSIDE; NOREPINEPHRINE; PREGNANCY; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 77949918047     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2010.01.012     Document Type: Article

References (49)

1. Almeida R., Manadas B.J., Melo C.V., Gomes J.R., Mendes C.S., Carvalho R.F., Carvalho A.P., Duarte C.B. Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ. 2005, 12:1329-1343.
2. Banker G.A., Cowan W.M. Rat hippocampal neurons in dispersed cell culture. Brain Res. Bull. 1977, 126:397-342.
3. Brunet A., Datta S.R., Greenberg M.E. Transcription-dependent and-independent control of neuronal survival by the PI3 kinase-Akt signaling pathway. Curr. Opin. Neurobiol. 2001, 11:297-305.
4. Chen M.J., Russo-Neustadt A.A. Exercise activates the phosphatidylinositol 3-kinase pathway. Mol. Brain Res. 2005, 135:181-193.
5. Chen M.J., Russo-Neustadt A.A. Nitric oxide signaling participates in norepinephrine-induced activity of neuronal intracellular survival pathways. Life Sci. 2007, 81:1280-1290.
6. Chen M.J., Ivy A., Russo-Neustadt A.A. Nitric oxide synthesis is required for exercise-induced increases in hippocampal BDNF and phosphatidylinositol 3 kinase expression. Brain Res. Bull. 2006, 68:257-268.
7. Chen M.J., Nguyen T.V., Pike C.J., Russo-Neustadt A.A. Norepinephrine induces BDNF and activates the PI-3K and MAPK cascades in embryonic hippocampal neurons. Cell. Signal. 2007, 19:114-128.
8. Cheng A., Wang S., Cai J., Rao M.S., Mattson M.P. Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev. Biol. 2003, 258:319-333.
9. Ciani E., Guidi S., Barstesaghi R., Contestabile A. Nitirc oxide regulates cGMP-dependent cAMP-responsive element binding protein phosphorylation and Bcl-2 expression in cerebellar neurons: implications for a survival role of nitric oxide. J. Neurochem. 2002, 82:1282-1289.
10. Ciani E., Virgili M., Contestabile A. Akt pathway mediates a cGMP-dependent survival role of nitric oxide in cerebellar granule neurons. J. Neurochem. 2002, 81:218-228.
11. Chieuh C.C., Andoh T., Lai A.R., Lai E., Krishna G. Neuroprotective strategies in Parkinson's disease: protection against progressive nigral damage induced by free radicals. Neurotox. Res. 2000, 2:293-310.
12. Contestabile A., Ciani E. Role of nitric oxide in the regulation of neuronal proliferation, survival and differentiation. Neurochem. Int. 2004, 45:903-914.
13. Contestabile A., Monti B., Ciani E. Brain nitric oxide and its dual role in neurodegeneration/neuroprotection: understanding molecular mechanisms to devise drug approaches. Curr. Med. Chem. 2003, 10:2147-2174.
14. Culmsee C., Gerling N., Landshamer S., Rickerts B., Duchstein H.-J., Umezawa K., Klumpp S., Krieglstein J. Nitric oxide donors induce neurotrophin-like survival signaling and protect neurons against apoptosis. Mol. Pharmacol. 2005, 68:1006-1017.
15. Endres M., Gertz K., Lindauer U., Katchanov J., Schultze J., Schröck H., Nickenig G., Kuschinsky W., Dirnagl U., Laufs U. Mechanisms of stroke protection by physical activity. Ann. Neurol. 2003, 54:582-590.
16. Estevez A.G., Spear N., Manuel S.M., Radi R., Henderson C.E., Barbeito L., Beckman J.S. Nitric oxide and superoxide contribute to motor neuron apoptosis induced by trophic factor deprivation. J. Neurosci. 1998, 18:923-931.
17. Garcia C., Chen M.J., Garza A.A., Cotman C.W., Russo-Neustadt A. The influence of specific noradrenergic and serotonergic lesions on the expression of hippocampal brain derived neurotrophic factor transcripts following voluntary physical activity. Neuroscience 2003, 119:721-732.
18. Griffiths C., Wykes V., Bellamy T.C., Garthwaite J. A new and simple method for delivering clamped nitric oxide concentrations in the physiological range: application to activation of guanylyl cyclase-coupled nitric oxide receptors. Mol. Pharmacol. 2003, 64:1349-1356.
19. Ha K.S., Kim K.-M., Kwon Y.-G., Bai S.-K., Nam W.-D., Yoo Y.-M., Kim P.K.M., Chung H.-T., Billiar T.R., Kim Y.-M. Nitric oxide prevents 6-hydroxydopamine-induced apoptosis in PC12 cells through cGMP-dependent PI3 kinase/Akt activation. FASEB J. 2003, 17:1036-1047.
20. Hashiguchi A., Yano S., Morioka M., Hamada J., Ushio Y., Takeuchi Y., Fukunaga K. Up-regulation of endothelia nitric oxide synthase via phosphatidylinositol 3-kinase pathway contributes to ischemic tolerance in the CA1 subfield of the gerbil hippocampus. J. Cereb. Blood Flow Metab. 2004, 24:271-279.
21. Hetman M., Xia Z. Signaling pathways mediating anti-apoptotic action of neurotrophins. Acta Neurobiol. Expr. 2000, 60:531-545.
22. Hetman M., Kanning K., Smith-Cavanaugh J.E., Xia Z. Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular-signal-regulated kinase and phosphatidylinositol-3 kinase. J. Biol. Chem. 1999, 274:22569-22580.
23. Hua Y., Huang X.Y., Zhou L., Zhou O.G., Hu Y., Luo C.X., Li F., Zhu D.Y. DETA/NONOate, a nitric oxide donor, produces antidepressant effects by promoting hippocampal neurogenesis. Psychopharmacology (Berl) 2008, 200:231-242.
24. Ivy A.S., Rodriguez F.G., Garcia C., Chen M.J., Russo-Neustadt A.A. Noradrenergic and serotonergic blockade inhibits BDNF mRNA activation following exercise and antidepressant. Pharmacol. Biochem. Behav. 2003, 75:81-88.
25. Kang Y.-C., Kim P.K., Choi B.-M., Chung H.-T., Ha K.-S., Kwon Y.-G., Kim Y.-M. Regulation of programmed cell death in neuronal cells by nitric oxide. In Vivo 2004, 18:367-376.
26. Kanterewicz B.I., Knapp L.T., Klann E. Stimulation of p42 and p44 mitogen-activated protein kinases by reactive oxygen species and nitric oxide in hippocampus. J. Neurochem. 1998, 70:1009-1016.
27. Kline R.B. Beyond Significance Testing 2005, American Psychological Association, Washington, D.C. first ed.
28. Klöcker N., Kermer P., Gleichmann M., Weller M., Bähr M. Both the neuronal and inducible isoforms contribute to upregulation of retinal nitric oxide synthase activity by brain-derived neurotrophic factor. J. Neurosci. 1999, 19:8517-8527.
29. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
30. Lin Y.-F., Raab-Graham K., Jan Y.N., Jan L.Y. NO stimulation of ATP-sensitive potassium channels: involvement of ras/mitogen-activated protein kinase pathway and contribution to neuroprotection. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7799-7804.
31. Lonart G., Wang J., Johnson K.M. Nitric oxide induces neurotransmitter release from hippocampal slices. Eur. J. Pharmacol. 1992, 220:271-272.
32. Lu D., Mahmood A., Zhang R., Copp M. Upregulation of neurogensis and reduction in functional deficits following administration of DEtA/NONOate, a nitric oxide donor, after traumatic brain injury in rats. J. Neurosurg 2003, 99:351-361.
33. Manji H., Quiroz J., Sporn J., Payne L.J., Denicoff K., Gray N.A., Zarate C.A., Charney D.S. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol. Psychiatry 2004, 53:707-742.
34. Mejia-Garcia T.A., Paes-de-Carvalho R. Nitric oxide regulates cell survival in purified cultures of avian retinal neurons: involvement of multiple transduction pathways. J. Neurochem. 2007, 100:382-394.
35. Mohanakumar K.P., Thomas B., Sharma S.M., Muralikrishnan D., Chowdhury R., Chiueh C.C. Nitric oxide: an antioxidant and neuroprotector. Ann. N. Y. Acad. Sci. 2002, 962:389-401.
36. Palumbo M.L., Fosser N.S., Rios H., Zubilete M.A.Z., Guelman L.R., Cremaschi G.A., Genaro A.M. Loss of hippocampal neuronal nitric oxide synthase contributes to the stress-related deficit in learning and memory. J. Neurochem. 2007, 20:1471-4159.
37. Puzzo D., Vitolo O., Trinchese F., Jacob J.P., Palmeri A., Arancio O. Amyloid-β peptide inhibits activation of the nitric oxide/cGMP/cAMP-responsive element-binding protein pathway during hippocampal synaptic plasticity. J. Neurosci. 2005, 25:6887-6897.
38. Rauhala P., Andoh T., Chiueh C.C. Neuroprotective properties of nitric oxide and S-nitrosoglutathione. Toxicol. Appl. Pharmacol. 2005, 207:91-95.
39. Riccio A., Alvania R.S., Lonze B.E., Ramanan N., Kim T., Huang Y., Dawson T.M., Snyder S.H., Ginty D.D. A nitric oxide signaling pathway controls CREB-mediated gene expression in neurons. Mol. Cell 2006, 21:283-294.
40. Russo-Neustadt A.A., Beard R.C., Cotman C.W. Exercise, antidepressant medications, and enhanced brain derived neurotrophic factor expression. Neuropsychopharmacology 1999, 21:679-682.
41. Samdani A.F., Newcamp C., Resink A., Facchinetti F., Hoffman B.E., Dawson V.L., Dawson T.M. Differential susceptibility to neurotoxicity mediated by neurotrophins and neuronal nitric oxide synthase. J. Neurosci. 1997, 17:4633-4641.
42. Satoh S., Kimura T., Toda M., Miyazaki H., Ono S., Narita H., Murayama T., Nomura Y. NO donors stimulate noradrenaline release from rat hippocampus in a calmodulin-dependent manner in the presence of L-cysteine. J. Cell. Physiol. 1996, 169:87-96.
43. 3H]norepinephrine release from rat hippocampal slices. Neuropharmacology 1995, 34:723-729.
44. Tong L., Balazs R., Thornton P.L., Cotman C.W. β-Amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons. J. Neurosci. 2004, 24:6799-6809.
45. Xiong H., Yamada K., Han D., Nabeshima T., Enikolopov G., Carnahan J., Nawa H. Mutual regulation between the intercellular messengers nitric oxide and brain-derived neurotrophic factor in rodent neocortical neurons. Eur. J. Neurosci. 1999, 11:1567-1576.
46. Yu H.M., Xu J., Li C., Zhou C., Zhang F., Han D., Zhang G.Y. Coupling between neuronal nitric oxide synthase and glutamate receptor 6-mediated c-Jun N-terminal kinase signaling pathway via S-nitrosylation contributes to ischemia neuronal death. Neuroscience 2008, 115:1120-1132.
47. Zhang R., Zhang L., Zhang Z., Wang Y., Lu M., LaPointe M., Chopp M. A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann. Neurol. 2001, 50:602-611.
48. Zheng W.-H., Quirion R. Comparative signaling pathways of insulin-like growth factor-1 and brain-derived neurotrophic factor in hippocampal neurons and the role of the PI3 kinase pathway in cell survival. J. Neurochem. 2004, 89:844-852.
49. Zheng W.-H., Quirion R. Glutamate acting on N-methyl-D-aspartate receptors attenuates insulin-like growth factor-1 receptor tyrosine phosphorylation and its survival signaling properties in rat hippocampal neurons. J. Biol. Chem. 2009, 284:855-861.