Hippocampal neuronal nitric oxide synthase (nNOS) is regulated by nicotine and stress in female but not in male rats

Brain Research

Volumn 1368, Issue , 2011, Pages 134-142

  Keser, Aysegul ^a   Balkan, Burcu ^a   Gozen, Oguz ^a   Kanit, Lutfiye ^a   Pogun, Sakire ^a  

^a EGE UNIVERSITY   (Turkey)

Author keywords

Hippocampus; Nicotine; NNOS; Sexual dimorphism; Stress

Indexed keywords

NEURONAL NITRIC OXIDE SYNTHASE; NICOTINE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BASAL AMYGDALA; CONTROLLED STUDY; FEMALE; FORCED SWIMMING TEST; FRONTAL CORTEX; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; STRESS; WESTERN BLOTTING;

AMYGDALA; ANIMALS; BLOTTING, WESTERN; FEMALE; FRONTAL LOBE; HIPPOCAMPUS; MALE; NEURONS; NEUROPSYCHOLOGICAL TESTS; NICOTINE; NICOTINIC AGONISTS; NITRIC OXIDE SYNTHASE TYPE I; RATS; SEX FACTORS; STRESS, PSYCHOLOGICAL; SWIMMING;

RATTUS;

EID: 78651074123     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.10.090     Document Type: Article

References (84)

1. C.E. Adams, and R. Freedman Nicotinic antagonist alpha-bungarotoxin binding to rat hippocampal neurons containing nitric oxide synthase Brain Res. 776 1997 111 116
2. E.X. Albuquerque, E.F. Pereira, M. Alkondon, and S.W. Rogers Mammalian nicotinic acetylcholine receptors: from structure to function Physiol. Rev. 89 2009 73 120
3. O. Arancio, M. Kiebler, C.J. Lee, V. Lev-Ram, R.Y. Tsien, E.R. Kandel, and R.D. Hawkins Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons Cell 87 1996 1025 1035 (Pubitemid 26427986)
4. M.P. Ashe, J.W. Slaven, S.K. De Long, S. Ibrahimo, and A.B. Sachs A novel eIF2B-dependent mechanism of translational control in yeast as a response to fusel alcohols EMBO J. 20 2001 6464 6474
5. S. Blackshaw, M.J. Eliasson, A. Sawa, C.C. Watkins, D. Krug, A. Gupta, T. Arai, R.J. Ferrante, and S.H. Snyder Species, strain and developmental variations in hippocampal neuronal and endothelial nitric oxide synthase clarify discrepancies in nitric oxide-dependent synaptic plasticity Neuroscience 119 2003 979 990
6. M.I. Boulware, J.P. Weick, B.R. Becklund, S.P. Kuo, R.D. Groth, and P.G. Mermelstein Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein J. Neurosci. 25 2005 5066 5078
7. B. Csillik, J. Nemcsok, I. Boncz, and E. Knyihar-Csillik Nitric oxide synthase and the acetylcholine receptor in the prefrontal cortex: metasynaptic organization of the brain Neurobiology (Bp). 6 1998 383 404
8. J.A. Dani Overview of nicotinic receptors and their roles in the central nervous system Biol. Psychiatry 49 2001 166 174
9. J.M. Daniel, and G.P. Dohanich Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory J. Neurosci. 21 2001 6949 6956
10. R.M. de Oliveira, E. Aparecida Del Bel, M.L. Mamede-Rosa, C.M. Padovan, J.F. Deakin, and F.S. Guimaraes Expression of neuronal nitric oxide synthase mRNA in stress-related brain areas after restraint in rats Neurosci. Lett. 289 2000 123 126
11. M.B. Echeverry, F.S. Guimaraes, and E.A. Del Bel Acute and delayed restraint stress-induced changes in nitric oxide producing neurons in limbic regions Neuroscience 125 2004 981 993
12. D. Forestiero, C.M. Manfrim, F.S. Guimaraes, and R.M. de Oliveira Anxiolytic-like effects induced by nitric oxide synthase inhibitors microinjected into the medial amygdala of rats Psychopharmacology (Berl). 184 2006 166 172
13. R. Gabor, R. Nagle, D.A. Johnson, and R.B. Gibbs Estrogen enhances potassium-stimulated acetylcholine release in the rat hippocampus Brain Res. 962 2003 244 247
14. M. Gao, F. Kondo, T. Murakami, J.W. Xu, N. Ma, X. Zhu, K. Mori, and T. Ishida 1-Aminocyclopropanecarboxylic acid, an antagonist of N-methyl- d-aspartate receptors, causes hypotensive and antioxidant effects with upregulation of heme oxygenase-1 in stroke-prone spontaneously hypertensive rats Hypertens. Res. 30 2007 249 257
15. M. Gimona, J. Vandekerckhove, M. Goethals, M. Herzog, Z. Lando, and J.V. Small Beta-actin specific monoclonal antibody Cell Motil. Cytoskeleton 27 2 1994 108 116
16. R. Girod, N. Barazangi, D. McGehee, and L.W. Role Facilitation of glutamatergic neurotransmission by presynaptic nicotinic acetylcholine receptors Neuropharmacology 39 2000 2715 2725
17. J. Glowinski, and L.L. Iversen Regional studies of catecholamines in the rat brain. I. The disposition of [3H]norepinephrine, [3H]dopamine and [3H]dopa in various regions of the brain J. Neurochem. 13 1966 655 669
18. P.W. Gold, and G.P. Chrousos Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states Mol. Psychiatry 7 2002 254 275
19. O. Gozen, B. Balkan, G. Yararbas, E.O. Koylu, M.J. Kuhar, and S. Pogun Sex differences in the regulation of cocaine and amphetamine-regulated transcript expression in hypothalamic nuclei of rats by forced swim stress Synapse 61 2007 561 568
20. C. Grohe, S. Kann, L. Fink, P.C. Djoufack, M. Paehr, M. van Eickels, H. Vetter, R. Meyer, and K.B. Fink 17 Beta-estradiol regulates nNOS and eNOS activity in the hippocampus NeuroReport 15 2004 89 93
21. S.A. Hart, J.D. Patton, and C.S. Woolley Quantitative analysis of ER alpha and GAD colocalization in the hippocampus of the adult female rat J. Comp. Neurol. 440 2001 144 155
22. R.G. Hunter, E.B. Bloss, K.J. McCarthy, and B.S. McEwen Regulation of the nicotinic receptor alpha7 subunit by chronic stress and corticosteroids Brain Res. 1325 2010 141 146
23. Y. Ishizuka, Y. Ishida, Q. Jin, K. Kato, T. Kunitake, Y. Mitsuyama, and H. Kannan Differential profiles of nitric oxide and norepinephrine releases in the paraventricular nucleus region in response to mild footshock in rats Brain Res. 862 2000 17 25
24. Y. Ishizuka, H. Abe, H. Nakane, H. Kannan, and Y. Ishida Different response between production of free radicals induced by central and peripheral administration of interleukin-1beta in conscious rats Neurosci. Res. 60 2008 10 14
25. M.H. Jang, M.C. Shin, B.V. Lim, J.H. Chung, H.S. Kang, S.A. Kang, R.W. Choue, E.H. Kim, and C.J. Kim Nicotine administration decreases nitric oxide synthase expression in the hypothalamus of food-deprived rats Neurosci. Lett. 322 2002 29 32
26. L. Kanit, E.O. Koylu, G. Yararbas, J.J. Furedy, and S. Pogun The effect of nitric oxide synthase inhibition on cognitive ability and strategies employed for place learning in the water maze: sex differences Brain Res. Bull. 62 2003 151 159
27. E.O. Koylu, L. Kanit, D. Taskiran, T. Dagci, B. Balkan, and S. Pogun Effects of nitric oxide synthase inhibition on spatial discrimination learning and central DA2 and mACh receptors Pharmacol. Biochem. Behav. 81 2005 32 40
28. T.L. Krukoff Central actions of nitric oxide in regulation of autonomic functions Brain Res. Brain Res. Rev. 30 1999 52 65
29. T.L. Krukoff, and P. Khalili Stress-induced activation of nitric oxide-producing neurons in the rat brain J. Comp. Neurol. 377 1997 509 519
30. Y. Kubota, R. Hattori, and Y. Yui Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex Brain Res. 649 1994 159 173
31. E.K. Lambe, M.R. Picciotto, and G.K. Aghajanian Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex Neuropsychopharmacology 28 2003 216 225
32. J.C. Leza, E. Salas, G. Sawicki, J.C. Russell, and M.W. Radomski The effects of stress on homeostasis in JCR-LA-cp rats: the role of nitric oxide J. Pharmacol. Exp. Ther. 286 1998 1397 1403
33. M.O. Lopez-Figueroa, K. Itoi, and S.J. Watson Regulation of nitric oxide synthase messenger RNA expression in the rat hippocampus by glucocorticoids Neuroscience 87 1998 439 446
34. V.N. Luine Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats Exp. Neurol. 89 2 1985 484 490
35. V.N. Luine, and B.S. McEwen Sex differences in cholinergic enzymes of diagonal band nuclei in the rat preoptic area Neuroendocrinology 36 1983 475 482
36. L. Luo, and R.X. Tan Fluoxetine inhibits dendrite atrophy of hippocampal neurons by decreasing nitric oxide synthase expression in rat depression model Acta Pharmacol. Sin. 22 2001 865 870
37. L. Mao, Q. Tang, S. Samdani, Z. Liu, and J.Q. Wang Regulation of MAPK/ERK phosphorylation via ionotropic glutamate receptors in cultured rat striatal neurons Eur. J. Neurosci. 19 2004 1207 1216
38. M.B. Mathews, N. Sonenberg, and J.W.B. Hershey Origins and principles of translational control N. Sonenberg, J.W.B. Hershey, M.B. Mathews, Translational Control of Gene Expression, Cold Spring Harbor Laboratory Press 2000 Cold Spring Harbor New York 1 32
39. A.J. McDonald, D.R. Payne, and F. Mascagni Identification of putative nitric oxide producing neurons in the rat amygdala using NADPH-diaphorase histochemistry Neuroscience 52 1993 97 106
40. M.M. Mesulam, E.J. Mufson, B.H. Wainer, and A.I. Levey Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6) Neuroscience 10 1983 1185 1201
41. D.D. Murphy, and M. Segal Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones J. Neurosci. 16 1996 4059 4068
42. L. Musazzi, M. Milanese, P. Farisello, S. Zappettini, D. Tardito, V.S. Barbiero, T. Bonifacino, A. Mallei, P. Baldelli, G. Racagni, M. Raiteri, F. Benfenati, G. Bonanno, and M. Popoli Acute stress increases depolarization- evoked glutamate release in the rat prefrontal/frontal cortex: the dampening action of antidepressants PLoS One 5 2010 e8566
43. K. Nakamura, T. Takahashi, M. Taniuchi, C.X. Hsu, and C. Owyang Nicotinic receptor mediates nitric oxide synthase expression in the rat gastric myenteric plexus J. Clin. Invest. 101 1998 1479 1489 (Pubitemid 28166846)
44. K.A. Overeem, K.T. Ota, M.S. Monsey, J.E. Ploski, and G.E. Schafe A role for nitric oxide-driven retrograde signaling in the consolidation of a fear memory Front. Behav. Neurosci. 4 2010 2
45. M.A. Packer, Y. Stasiv, A. Benraiss, E. Chmielnicki, A. Grinberg, H. Westphal, S.A. Goldman, and G. Enikolopov Nitric oxide negatively regulates mammalian adult neurogenesis Proc. Natl Acad. Sci. USA 100 2003 9566 9571
46. M.L. Palumbo, M.A. Zorrilla Zubilete, G.A. Cremaschi, and A.M. Genaro Different effect of chronic stress on learning and memory in BALB/c and C57BL/6 inbred mice: involvement of hippocampal NO production and PKC activity Stress 12 2009 350 361
47. G.C. Panzica, C. Viglietti-Panzica, M. Sica, S. Gotti, M. Martini, H. Pinos, B. Carrillo, and P. Collado Effects of gonadal hormones on central nitric oxide producing systems Neuroscience 138 2006 987 995
48. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 1998 Academic Press New York
49. S. Pogun Sex differences in brain and behavior: emphasis on nicotine, nitric oxide and place learning Int. J. Psychophysiol. 42 2001 195 208
50. S. Pogun, and G. Yararbas Sex differences in nicotine action Handb. Exp. Pharmacol. 2009 261 291
51. S. Pogun, S. Demirgoren, D. Taskiran, L. Kanit, O. Yilmaz, E.O. Koylu, B. Balkan, and E.D. London Nicotine modulates nitric oxide in rat brain Eur. Neuropsychopharmacol. 10 2000 463 472
52. Porsolt, R.D., Anton, G., Blavet, N., Jalfre, M., 1978. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol. 15;47(4):379-91.
53. J. Raber, G.F. Koob, and F.E. Bloom Interleukin-2 (IL-2) induces corticotropin-releasing factor (CRF) release from the amygdala and involves a nitric oxide-mediated signaling; comparison with the hypothalamic response J. Pharmacol. Exp. Ther. 272 1995 815 824
54. A.P. Raval, I. Saul, K.R. Dave, R.A. DeFazio, M.A. Perez-Pinzon, and H. Bramlett Pretreatment with a single estradiol-17beta bolus activates cyclic-AMP response element binding protein and protects CA1 neurons against global cerebral ischemia Neuroscience 160 2009 307 318
55. L.P. Reagan, and B.S. McEwen Diabetes, but not stress, reduces neuronal nitric oxide synthase expression in rat hippocampus: implications for hippocampal synaptic plasticity NeuroReport 13 2002 1801 1804
56. L.B. Resstel, and F.M. Correa Medial prefrontal cortex NMDA receptors and nitric oxide modulate the parasympathetic component of the baroreflex Eur. J. Neurosci. 23 2006 481 488
57. L.R. Reznikov, C.A. Grillo, G.G. Piroli, R.K. Pasumarthi, L.P. Reagan, and J. Fadel Acute stress-mediated increases in extracellular glutamate levels in the rat amygdala: differential effects of antidepressant treatment Eur. J. Neurosci. 25 2007 3109 3114
58. C. Rivier Role of gaseous neurotransmitters in the hypothalamic- pituitary-adrenal axis Ann. NY Acad. Sci. 933 2001 254 264
59. L.J. Roman, and B.S. Masters Electron transfer by neuronal nitric-oxide synthase is regulated by concerted interaction of calmodulin and two intrinsic regulatory elements J. Biol. Chem. 281 2006 23111 23118
60. R.D. Romeo, J.B. McCarthy, A. Wang, T.A. Milner, and B.S. McEwen Sex differences in hippocampal estradiol-induced N-methyl- d-aspartic acid binding and ultrastructural localization of estrogen receptor-alpha Neuroendocrinology 81 2005 391 399
61. M. Sasaki, M. Gonzalez-Zulueta, H. Huang, W.J. Herring, S. Ahn, D.D. Ginty, V.L. Dawson, and T.M. Dawson Dynamic regulation of neuronal NO synthase transcription by calcium influx through a CREB family transcription factor-dependent mechanism Proc. Natl Acad. Sci. USA 97 2000 8617 8622
62. D.O. Seo, and C. Rivier Microinfusion of a nitric oxide donor in discrete brain regions activates the hypothalamic-pituitary-adrenal axis J. Neuroendocrinol. 13 2001 925 933
63. Z. Serfozo, J. de Vente, and K. Elekes Thyroid hormone level positively regulates NOS and cGMP in the developing rat cerebellum Neuroendocrinology 89 3 2009 337 350
64. P.J. Shughrue, and I. Merchenthaler Evidence for novel estrogen binding sites in the rat hippocampus Neuroscience 99 2000 605 612
65. P.J. Shughrue, P.J. Scrimo, and I. Merchenthaler Estrogen binding and estrogen receptor characterization (ERalpha and ERbeta) in the cholinergic neurons of the rat basal forebrain Neuroscience 96 2000 41 49
66. Slotkin, T.A., Freibaum, B.D., Tate, C.A., Thillai, I., Ferguson, S.A., Cada, A.M., Seidler, F.J., 2003. Long-lasting CNS effects of a short-term chemical knockout of ornithine decarboxylase during development: nicotinic cholinergic receptor upregulation and subtle macromolecular changes in adulthood. Brain Res. 15; 981(1-2):118-25.
67. T.A. Slotkin, E.A. MacKillop, C.L. Rudder, I.T. Ryde, C.A. Tate, and F.J. Seidler Permanent, sex-selective effects of prenatal or adolescent nicotine exposure, separately or sequentially, in rat brain regions: indices of cholinergic and serotonergic synaptic function, cell signaling, and neural cell number and size at 6 months of age Neuropsychopharmacology 32 5 2007 1082 1097 Epub 2006 Oct 18
68. D.A. Smith, A.F. Hoffman, D.J. David, C.E. Adams, and G.A. Gerhardt Nicotine-evoked nitric oxide release in the rat hippocampal slice Neurosci. Lett. 255 1998 127 130
69. M.B. Solomon, and J.P. Herman Sex differences in psychopathology: of gonads, adrenals and mental illness Physiol. Behav. 97 2009 250 258
70. P.C. Spolidorio, M.B. Echeverry, M. Iyomasa, F.S. Guimaraes, and E.A. Del Bel Anxiolytic effects induced by inhibition of the nitric oxide-cGMP pathway in the rat dorsal hippocampus Psychopharmacology (Berl). 195 2007 183 192
71. Sunanda, B.S. Rao, and T.R. Raju Restraint stress-induced alterations in the levels of biogenic amines, amino acids, and AChE activity in the hippocampus Neurochem. Res. 25 2000 1547 1552
72. T. Tajima, H. Endo, Y. Suzuki, H. Ikari, M. Gotoh, and A. Iguchi Immobilization stress-induced increase of hippocampal acetylcholine and of plasma epinephrine, norepinephrine and glucose in rats Brain Res. 720 1996 155 158
73. M. Toborek, R. Garrido, A. Malecki, S. Kaiser, M.P. Mattson, B. Hennig, and B. Young Nicotine attenuates arachidonic acid-induced overexpression of nitric oxide synthase in cultured spinal cord neurons Exp. Neurol. 161 2000 609 620 (Pubitemid 30137018)
74. B.H. Tonnessen, S.R. Severson, R.D. Hurt, and V.M. Miller Modulation of nitric-oxide synthase by nicotine J. Pharmacol. Exp. Ther. 295 2000 601 606
75. E. Tribollet, D. Bertrand, A. Marguerat, and M. Raggenbass Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: an autoradiographic study in the rat brain Neuroscience 124 2004 405 420
76. N.G. Weiland Estradiol selectively regulates agonist binding sites on the N-methyl-d-aspartate receptor complex in the CA1 region of the hippocampus Endocrinology 131 1992 662 668
77. M.M. Weissman, and M. Olfson Depression in women: implications for health care research Science 269 1995 799 801
78. E. Weruaga, B. Balkan, E.O. Koylu, S. Pogun, and J.R. Alonso Effects of chronic nicotine administration on nitric oxide synthase expression and activity in rat brain J. Neurosci. Res. 67 2002 689 697
79. T. Xu, W. Jiang, D. Du, Y. Xu, Q. Zhou, X. Pan, Y. Lou, L. Xu, and K. Ma Inhibition of MPEP on the development of morphine antinociceptive tolerance and the biosynthesis of neuronal nitric oxide synthase in rat spinal cord Neurosci. Lett. 436 2008 214 218
80. S.T. Yao, V.R. Antunes, J.F. Paton, and D. Murphy Osmotic regulation of neuronal nitric oxide synthase expression in the rat amygdala: functional role for nitric oxide in adaptive responses? J. Neurosci. Res. 85 2007 410 422
81. O. Yilmaz, L. Kanit, B.E. Okur, E.D. London, and S. Pogun Nitric oxide synthetase inhibition hinders facilitation of active avoidance learning by nicotine in rats Behav. Pharmacol. 11 2000 505 510
82. J.H. Yoo, J.H. Cho, S.Y. Lee, H.H. Loh, I.K. Ho, and C.G. Jang Reduced nNOS expression induced by repeated nicotine treatment in mu-opioid receptor knockout mice Neurosci. Lett. 380 2005 70 74
83. Q.G. Zhou, Y. Hu, Y. Hua, M. Hu, C.X. Luo, X. Han, X.J. Zhu, B. Wang, J.S. Xu, and D.Y. Zhu Neuronal nitric oxide synthase contributes to chronic stress-induced depression by suppressing hippocampal neurogenesis J. Neurochem. 2007
84. W. Zhu, H. Umegaki, J. Yoshimura, N. Tamaya, Y. Suzuki, H. Miura, and A. Iguchi The elevation of plasma adrenocorticotrophic hormone and expression of c-Fos in hypothalamic paraventricular nucleus by microinjection of neostigmine into the hippocampus in rats: comparison with acute stress responses Brain Res. 892 2001 391 395