Aged endothelial nitric oxide synthase knockout mice exhibit higher mortality concomitant with impaired open-field habituation and alterations in forebrain neurotransmitter levels

Genes, Brain and Behavior

Volumn 1, Issue 4, 2002, Pages 204-213

  Dere, E ^a   De Souza Silva, M A ^a   Topic, B ^a   Fiorillo, C ^b   Li, J S ^a   Sadile, A G ^b   Frisch, C ^a   Huston, J P ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Cerebrovascular disease; eNOS knockout mice; Habituation; Hypertension; Plus maze; Pole test

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; ACETYLCHOLINE; DOPAMINE; NITRIC OXIDE SYNTHASE; SEROTONIN;

ACETYLCHOLINE BRAIN LEVEL; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; ENZYME DEFICIENCY; FRONTAL CORTEX; GENE DISRUPTION; HYPERTENSION; KNOCKOUT MOUSE; MAZE TEST; MORTALITY; MOUSE; NEUROCHEMISTRY; NONHUMAN; NORADRENALIN BRAIN LEVEL; OPEN FIELD BEHAVIOR; PARIETAL LOBE; PRIORITY JOURNAL; SEROTONIN BRAIN LEVEL;

ACETYLCHOLINE; AGING; ANIMALS; BRAIN; HABITUATION, PSYCHOPHYSIOLOGIC; LIFE EXPECTANCY; LONGEVITY; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; NOREPINEPHRINE; ORGAN SPECIFICITY; PAIN; REFERENCE VALUES; SEROTONIN;

ANIMALIA;

EID: 0037499422     PISSN: 16011848     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1601-183X.2002.10402.x     Document Type: Article

References (69)

1. Barnes, N.M. & Sharp, T. (1999) A review of central 5-HT receptors and their functions. Neuropharmacology 38, 1083-1152.
2. Barthus, R.T., Dean, R.L., Beer, B. & Lippa, A.S. (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408-412.
3. Bohn, H., Brendel, J., Martorana, P.A. & Schonafinger, K. (1995) Cardiovascular actions of the furoxan CAS 1609, a novel nitric oxide donor. Br J Pharmacol 114, 1605-1612.
4. Castoldi, A.F., Manzo, L. & Costa, L.G. (1993) Cyclic GMP formation induced by muscarinic receptors is mediated by nitric oxide synthase in rat cortical primary cultures. Brain Res 610, 57-61.
5. Celik, T., Zagli, Ü., Kayir, H. & Uzbay, I.T. (1999) Nitric oxide synthase inhibition blocks amphetamine-induced locomotor activity in mice. Drug Alcohol Dependence 56, 109-113.
6. Cerbone, A. & Sadile, A.G. (1994) Behavioral habituation to spatial novelty in rats: interference and noninterference studies. Neurosci Biobehav Rev 18, 497-518.
7. Cruce, M., Cruce, R. & Leulescu, C. (1998) Sinteza si efectele monoxidului de azot la nivelul retinei. Oftalmologia 42, 9-12.
8. Damsma, G., Lammerts van Bueren, D., Westerink, B.H.C. & Horn, A.S. (1987) Determination of acetylcholine and choline in the femtomole range by means of HPLC, a post-column enzyme reactor, and electro-chemical detection. Chromatographia 24, 827-831.
9. De la Torre, J.C & Stefano, G.B. (2000) Evidence that Alzheimer's disease is a microvascular disorder: the role of constitutive nitric oxide. Brain Res Rev 34, 119-136.
10. De Souza-Silva, M.A., Hasenöhrl, R.U., Tomaz, C., Schwarting, R.K.W. & Huston, J.P. (2000) Modulation of frontal cortex acetylcholine and behavior by injection of substance P into the ventral pallidum in the freely-moving vs. anesthetized preparation. Synapse 38, 243-253.
11. De Souza-Silva, M.A., Mattern, C., Häcker, R., Nogueira, P.J., Huston, J.P. & Schwarting, R.K. (1997) Intranasal administration of the dopaminergic agonists L-DOPA, amphetamine, and cocaine increases dopamine activity in the neostriatum: a microdialysis study in the rat. J Neurochem 68, 233-239.
12. Demas, G.E., Kriegsfeld, L.J., Blackshaw, S., Huang, R, Gammie, S.C., Nelson, R.J. & Snyder, S.H. (1999) Elimination of aggressive behavior in male mice lacking endothelial nitric oxide synthase. J Neurosci 19, C1-C5.
13. Dere, E., Frisch, C., De Souza Silva, M.A., Gödecke, A., Schrader, J. & Huston, J.P. (2001) Unaltered radial-maze performance and brain acetylcholine of the endothelial nitric oxide synthase knockout mouse. Neuroscience 107, 561-570.
14. Desvignes, C., Bert, L., Vinet, L., Denoroy, L., Renaud, B. & Lambas-Senas, L. (1999) Evidence that the neuronal nitric oxide synthase inhibitor 7-nitroindazole inhibits monoamine oxidase in the rat: in vivo effects on extracellular striatal dopamine and 3,4-dihydroxyphenylacetic acid. Neurosci Lett 264, 5-8.
15. Duchen, M.R. (2000) Mitochondria and calcium: from cell signalling to cell death. J Physiol. 529, Part 157-168.
16. Dzoljic, E., De Vries, R. & Dzoljic, M.R. (1997) New and potent inhibitors of nitric oxide synthase reduce motor activity in mice. Behav Brain Res 87, 209-212.
17. Faraci, F.M. & Sobey, C.G. (1999) Role of soluble guanylate cyclase in dilator responses of the cerebral microcirculation. Brain Res 821, 368-373.
18. Farkas, E., De-Jong, G.I., Apro, E., De-Vos, R.A., Steur, E.N. & Luiten, P.G. (2000) Similar ultrastructural breakdown of cerebrocortical capillaries in Alzheimer's disease, Parkinson's disease, and experimental hypertension. What is the functional link? Ann NY Acad Sci 90, 372-382.
19. Feelisch, M. (1998) The use of nitric oxide donors in pharmacological studies. Naunyn-Schmiedeberg's Arch Pharmacol 358, 113-122.
20. -/- mouse together with monoamine changes in cerebellum and ventral striatum. J Neurosci 20, 6694-6700.
21. Gerlach, M., Reichmann, H. & Riederer, P. (2000) Pathophysiological mechanisms underlying Parkinson's disease and neuroprotective approaches. Nervenheilkunde 19, 496-503.
22. Gerlai, R. (1996) Gene targeting studies of mammalian behavior: Is it the mutation or the background genotype? TINS 19, 177-181
23. Gödecke, A, Decking, U.K.M., Ding, Z., Hirchenhain, J., Bidmon, H.J., Gödecke, S. & Schrader, J. (1998) Coronary hemodynamics in endothelial NO synthase knockout mice. Circ Res 82, 186-194.
24. Goldman-Rakic, P.S. & Brown, R.M. (1981) Regional changes of monoamines in cerebral cortex and subcortical structures of aging in rhesus monkey. Neuroscience 6, 177-187.
25. Govers, R. & Rabelink, T.J. (2001) Cellular regulation of endothelial nitric oxide synthase. Am J Physiol Renal Physiol 280, F193-F206.
26. Guevara-Guzman, R., Emson, P.C. & Kendrick, K.M. (1994) Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP. J Neurochem 62, 807-810.
27. Hara, H., Waeber, C., Huang, P.L., Fujii, M., Fishman, M.C. & Moskowitz, M.A. (1996) Brain distribution of nitric oxide synthase in neuronal or endothelial nitric oxide mutant mice using (3H)-L-NG-nitro-argirine autoradiography. Neuroscience 3, 881-890.
28. Haul, S., Gödecke, A., Schrader, J., Haas, H.L. & Luhmann, H.J. (1999) Impairment of neocortical long-term potentiation in mice deficient of endothelial nitric oxide synthase. J Neurophysiol 81, 494-497.
29. Haverkamp, S., Kolb, H. & Cuenca, N. (1999) Endothelial nitric oxide synthase (eNOS) is localized to Muller cells in all vertebrate retinas. Vision Res 39, 2299-2303
30. Hogg, N. & Kalyanaraman, B. (1999) Nitric oxide and lipid peroxidation. Biochim Biophys Acta 1411, 378-384.
31. Huang, P.L. & Fishman, M.C. (1996) Genetic analysis of nitric oxide synthase isoforms: Targeted mutation in mice. Mol Med 74, 415-421.
32. Huang, Z, Huang, P.L., Ma, J., Meng, W., Ayata, C., Fishman, M.C. & Moskowitz, M.A. (1996) Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J Cereb Blood Flow Metab 16, 981-987.
33. Huang, D., Shenoy, A., Cui, J., Huang, W. & Liu, P.K. (2000) In situ detection of AP sites and DNA strand breaks bearing-3′-phosphate termini in ischemic mouse brain. FASEB J 14, 407-417.
34. Kano, T., Shimizu-Sasamata, M., Huang, P.L., Moskowitz, M.A. & Lo, E.H. (1998) Effects of nitric oxide gene knockout on neurotransmitter release in vivo. Neuroscience 86, 695-699.
35. Kimoto-Kinoshita, S., Nishida, S. & Tomura, T.T. (2000) Decrease of endothelial nitric oxide synthase in stroke-prone spontaneously hypertensive rat cerebral cortex. Neurosci Lett 288, 103-106.
36. Kiss, J.P. (2000) Role of nitric oxide in the regulation of monoaminergic neurotransmission. Brain Res Bull 52, 459-466.
37. Kiss, J.P., Hennings, E.C., Zsilla, G. & Vizi, E.S. (1999) A possible role of nitric oxide in the regulation of dopamine transporter function in the striatum. Neurochem Int 34, 345-350.
38. Kojda, G. & Kottenberg, K. (1999) Regulation of basal myocardial function by. Cardiovasc Res 41, 514-523.
39. Kriegsfeld, L.J., Elasson, M.J., Demas, G.E., Blackshaw, S., Dawson, T.M., Nelson, R.J. & Snyder, S.H. (1999) Nocturnal motor coordination deficits in neuronal nitric oxide synthase knock-out mice. Neuroscience 89, 311-315.
40. Lister, R.G. (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92, 180-185.
41. Mashimo, H. & Goyal, R.K. (1999) Lessons from genetically engineered animal models IV Nitric oxide synthase gene knockout mice. Am J Physiol 277, G745-G750.
42. McCann, S.M., Licinio, J. & Wong, M.L., Yu W.H., Karanth, S. & Rettori, V. (1998) The nitric oxide hypothesis of brain aging. Exp Gerontol 33, 813-826.
43. McCarthy, M.F. (2000) Up-regulation of endothelial nitric oxide activity as a central strategy for prevention of ischemic stroke - just say NO to stroke!. Med Hypotheses 55, 386-403.
44. Mendes-Ribeiro, A.C., Brunini, T.M., Ellory, J.C. & Mann, G.E. (2001) Abnormalities in 1-arginine transport and nitric oxide biosynthesis in chronic renal and heart failure. Cardiovasc Res 49, 697-712.
45. Meyer, J.S., Rauch, G.M., Rauch, R.A., Haque, A. & Crawford, K. (2000) Cardiovascular and other risk factors for Alzheimer's disease and vascular dementia. Ann NY Acad Sci 90, 3411-3423.
46. Miyamoto, M. (1997) Characteristics of age-related behavioral changes in senescence-accelerated mouse SAMP8 and SAMP10. Exp Gerontol 32, 139-148.
47. Murashima, Y.L., Yoshii, M. & Suzuki, J. (2000) Role of nitric oxide in the epileptogenesis of EL mice. Epilepsia 41: Suppl 6S195-9.
48. Najarian, T., Marrache, A.M., Dumont, I., Hardy, P., Beauchamp, M.H., Hou, X., Peri, K., Gobeil, F., Varma, D.R. & Chemtob, S. (2000) Prolonged hypercapnia-evoked cerebral hyperemia via K (+) channel- and prostaglandin E(2)-dependent endothelial nitric oxide synthase induction. Circ Res 87, 1149-1156.
49. Nelson, R.J., Demas, G.E., Huang, P.L., Fishman, M.C., Dawson, V.L., Dawson, T.M. & Snyder, S.H. (1995) Behavioural abnormalities in male mice lacking nuronal nitric oxide synthase. Nature 378, 383-386
50. Ogawa, N., Hirose, Y., Ohara, S., Ono, T. & Watanabe, Y. (1985) A simple quantitative bradykinesia test in MPTP-treated mice. Res Commun Chem Pathol Pharmacol 50, 435-441.
51. Pisarska, M., Mulchahey, J.J., Welge, J.A., Geracioti, T.D. & Kasckow, J.W. (2000) Age-related alterations in emotional behaviors and amygdalar corticotropin-releasing factor (CRF) and CRF-binding protein expression in aged Fischer 344 rats. Brain Res 877, 184-190.
52. Potter, P.E., Meek, J.L. & Neff, N.H. (1983) Acetylcholine and choline in neuronal tissue measured by HPLC with electrochemical detection. J Neurochem 41, 188-194.
53. Prast, H. & Philippu, A. (2001) Nitric oxide as modulator of neural function. Prog Neurobiol 64, 51-68.
54. Puumala, T. & Sirvio, J. (1998) Changes in activities of dopamine and serotonin systems in the frontal cortex underlie poor choice accuracy and impulsivity of rats in an attention task. Neuroscience 83, 489-499.
55. Ramasamy, S., Drummond, G.R., Ahn, J., Storek, M., Pohl, J., Parthasarathy, S. & Harrison, D.G. (1999) Modulation of expression of endothelial nitric oxide synthase by nordihydroguaiaretic acid, a phenolic antioxidant in cultured endothelial cells. Mol Pharmacol 56, 116-123.
56. Rehse, K. & König, P. (1995) New NO-donors with antithrombotic and vasodilating activities, XII: Mesoionic oxatriazoles and related noncyclic nitrosohydrazine derivatives. Arch Pharm 328, 137-142.
57. Riedel, W. (2000) Role of nitric oxide in the control of the hypothalamic-pituitary-adrenocortical axis. Z Rheumatol 59: 211/36-42.
58. Rigaud, A.S., Seux, M.L., Staessen, J.A., Birkenhager, W.H. & Forette, F. (2000) Cerebral complications of hypertension. J Hum Hypertens 14, 605-616.
59. Rolls, E.T. (2000) Memory systems in the brain. Ann Rev Psychol 51, 599-630.
60. Roman, G.C. (1999) Vascular dementia today. Rev Neurol 155, S64-S72.
61. Roullet, P., Mele, A. & Ammassari-Teule, M. (1997) Ibotenic lesions of the nucleus accumbens promote reactivity to spatial novelty in nonreactive DBA mice: implications for neural mechanisms subserving spatial information encoding. Behav Neurosci 111, 976-984.
62. Sandi, C., Venero, C. & Guaza, C. (1995) Decreased spontaneous motor activity and startle response in nitric oxide synthase inhibitor-treated rats. Eur J Pharmacol 277, 89-97.
63. Serra, P.A., Esposito, G., Delogu, M.R., Migheli, R., Rocchitta, G., Grella, G., Miele, E., Miele, M. & Desole, M.S. (2000) Analysis of 3-morpholinosyd nonimine and sodium nitroprusside effects on dopamine release in the striatum of freely moving rats: role of nitric oxide, iron and ascorbic acid. Br J Pharmacol 131, 836-842.
64. Sethy, V.M. & Francis, J.W. (1988) Regulation of brain acetylcholine concentration by muscarinic receptors. J Pharmacol Exp Ther 246, 243-248.
65. Sugaya, K. & McKinney, M. (1994) Nitric oxide synthase gene expression in cholinergic neurons in the rat brain examined by combined immuno-cytochemistry and in situ hybridization histochemistry. Mol Brain Res 23, 111-125.
66. Thullier, F., Lalonde, R., Mahler, P., Joyal, C.C. & Lestienne, F. (1996) Dorsal striatal lesions in rats. 1: Effects on exploration and motor coordination. Arch Physiol Biochem 104, 300-306.
67. Weidenfeld, J., Feldman, S., DeKeyser, F.G. & Ovadia, H. (1999) Effect of exogenous nitric oxide and inhibitors of nitric oxide synthase on the hypothalamic pituitary adrenal axis responses to neural stimuli. Neuroendocrinology 70, 153-159.
68. Wner, B.J. (1962) Statistical principles in experimental design. McGraw-Hill, New York.
69. Yamada, K., Noda, Y., Nakayama, S., Komori, Y., Sugihara, H., Hasegawa, T. & Nabeshima, T. (1995) Role of nitric oxide in learning and memory and in monoamine metabolism in the rat brain. Br J Pharmacol 115, 852-858.