Aberrant expression of nitric oxide synthase III in Alzheimer's disease: Relevance to cerebral vasculopathy and neurodegeneration

Neurobiology of Aging

Volumn 21, Issue 2, 2000, Pages 309-319

  De La Monte, S M ^a,b   Lu, B X ^a,b   Sohn, Y K ^a,b   Etienne, D ^a,b   Kraft, J ^a,b   Ganju, N ^a,b   Wands, J R ^a,b  

^a BROWN UNIVERSITY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; ISOENZYME; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN P53;

AGING; ALZHEIMER DISEASE; APOPTOSIS; BRAIN INFARCTION; BRAIN ISCHEMIA; CEREBROVASCULAR DISEASE; CONFERENCE PAPER; DISEASE ASSOCIATION; DISEASE COURSE; ENDOTHELIUM CELL; GENE EXPRESSION; GLIA CELL; HUMAN; MITOCHONDRIAL RESPIRATION; NERVE CELL; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENILE PLAQUE; VASCULAR SMOOTH MUSCLE;

ALZHEIMER DISEASE; CEREBROVASCULAR DISORDERS; HUMANS; NERVE DEGENERATION; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III;

EID: 0034603525     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0197-4580(99)00108-6     Document Type: Conference Paper

References (110)

1. Akiyama H., Mori H., Saido T., Kondo H., Ikeda K., McGeer P.L. Occurrence of the diffuse amyloid beta-protein (Abeta) deposits with numerous Abeta-containing glial cells in the cerebral cortex of patients with Alzheimer's disease. Glia. 25:1999;324-331.
2. Bani D., Failli P., Bello M.G., et al. Relaxin activates the L-arginine-nitric oxide pathway in vascular smooth muscle cells in culture. Hypertension. 31:1998;1240-1247.
3. Belhassen L., Kelly R.A., Smith T.W., Balligand J.L. Nitric oxide synthase (NOS3) and contractile responsiveness to adrenergic and cholinergic agonists in the heart. Regulation of NOS3 transcription in vitro and in vivo by cyclic adenosine monophosphate in rat cardiac myocytes. J Clin Invest. 97:1996;1908-1915.
4. Berk B.C., Corson M.A., Peterson T.E., Tseng H. Protein kinases as mediators of fluid shear stress stimulated signal transduction in endothelial cells a hypothesis for calcium-dependent and calcium-independent events activated by flow . J Biomech. 28:1995;1439-1450.
5. Betard C., Robitaille Y., Gee M., et al. Apo E allele frequencies in Alzheimer's disease, Lewy body dementia, Alzheimer's disease with cerebrovascular disease and vascular dementia. Neuroreport. 5:1994;1893-1896.
6. Boje K., Arora P. Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res. 587:1992;250-256.
7. Braak H., Braak E. Neuropathological staging of Alzheimer-related changes. Acta Neuropath Berl. 82:1991;239-259.
8. Bredt D., Snyder S. Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium. Neuron. 13:1994;301-313.
9. Bredt D.S., Ferris C.D., Snyder S.H. Nitric oxide synthase regulatory sites. Phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase; identification of flavin and calmodulin binding sites. J Biol Chem. 267:1992;10976-10981.
10. Crystal H.A., Dickson D.W., Sliwinski M.J., et al. Pathological markers associated with normal aging and dementia in the elderly. Ann Neurol. 34:1993;566-573.
11. Culcasi M., Lafon-Cazal M., Pietri S., Bockaert J. Glutamate receptors induce a burst of superoxide via activation of nitric oxide synthase in arginine-depleted neurons. J Biol Chem. 269:1994;12589-12593.
12. Dawson V., Kizushi V., Huang P., Snyder S., Dawson T. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J Neurosci. 16:1996;2479-2487.
13. de la Monte S., Bloch K. Aberrant expression of the constitutive endothelial nitric oxide synthase gene in Alzheimer's disease. Mol Chem Neuropathol. 30:1997;139-159.
14. de la Monte SM, Ganju N, Luong T, et al. Over-expression of nitric oxide synthase-3 and free-radical injury cause apoptosis and phospho-tau accumulation in neuronal cells. J Neuropathol Exp Neurol 1999, in Press.
15. de la Monte S.M., Garner W., Wands J.R. Neuronal thread protein modulation with cerebral infarction. J Cereb Blood Flow Metabol. 17:1997;623-635.
16. de la Monte S.M., Luong T., Wands J.R. Mitochondrial DNA damage as a novel mechanism of cell loss in Alzheimer's disease. Lab Invest. 80:2000;196A.
17. de la Monte S.M., Sohn Y.K., Ganju N., Wands J.R. p53- and CD95-associated apoptosis in neurodegenerative diseases. Lab Invest. 158:1998;1001-1009.
18. de la Monte S.M., Sohn Y.K., Wands J.R. Correlates of p53- and Fas (CD95)-mediated apoptosis in Alzheimer's disease. J Neurol Sci. 152:1997;73-83.
19. de la Torre J. Impaired brain microcirculation may trigger Alzheimer's disease. Neurosci Biobehav Rev. 18:1994;397-401.
20. Delpy E., Coste H., Gouville A.C. Effects of cyclic GMP elevation on isoprenaline-induced increase in cyclic AMP and relaxation in rat aortic smooth muscle role of phosphodiesterase 3 . Br J Pharmacol. 119:1996;471-478.
21. Dickson D.W., Davies P., Bevona C., et al. Hippocampal sclerosis a common pathological feature of dementia in very old (>or = 80 years of age) humans . Acta Neuropathol (Berl). 88:1994;212-221.
22. Dinerman J., Dawson T., Schell M., Snowman A., Snyder S. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells implications for synaptic plasticity . Proc Natl Acad Sci USA. 91:1994;4214-4218.
23. Eseri M.M., Morris J.H.E. The Neuropathology of Dementia. 1997;Cambridge University Press, Oxford.
24. Esiri M.M., Wilcock G.K., Morris J.H. Neuropathological assessment of the lesions of significance in vascular dementia. J Neurol Neurosurg Psychiatry. 63:1997;749-753.
25. Etiene D., Kraft J., Ganju N., et al. Cerebrovascular pathology contributes to the heterogeneity of Alzheimer's Disease. J Alz Dis. 1:1998;48-56.
26. Farinelli S., Park D., Greene L. Nitric oxide delays the death of trophic factor-deprived PC12 cells and sympathetic neurons by a cGMP-mediated mechanism. J Neurosci. 16:1996;2325-2334.
27. Ferriero D., Holtzman D., Black S., Sheldon R. Neonatal mice lacking neuronal nitric oxide synthase are less vulnerable to hypoxic-ischemic injury. Neurobiol Dis. 3:1996;64-71.
28. Frisoni G.B., Beltramello A., Binetti G., et al. Computed tomography in the detection of the vascular component in dementia. Gerontology. 41:1995;121-128.
29. Griscavage J., Fukuto J., Komori Y., Ignarro L. Nitric oxide inhibits neuronal nitric oxide synthase by interacting with the heme prosthetic group. Role of tetrahydrobiopterin in modulating the inhibitory action of nitric oxide. J Biol Chem. 269:1994;21644-21649.
30. Haase J., Halama P., Horr R. Effectiveness of brief infusions with Ginkgo biloba Special Extract EGb 761 in dementia of the vascular and Alzheimer type. Z Gerontol Geriatr. 29:1996;302-309.
31. Hess D., Patterson S., Smith D., Skene J. Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature. 366:1994;562-565.
32. Hooper D., Bagasra O., Marini J., et al. Prevention of experimental allergic encephalomyelitis by targeting nitric oxide and peroxynitrite implications for the treatment of multiple sclerosis . Proc Natl Acad Sci USA. 94:1997;2528-2533.
33. Horr R., Kieser M. Ginkgo biloba special extract EGb 761 - an anti-dementia drug. Fortschr Med. 116:1998;39-40.
34. Huang A., Huang P., Panahian N., Dalkara T., Fishman M., Moskowitz M. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science. 265:1994;1883-1885.
35. Hyman B., Marzloff K., Wenninger J., Dawson T., Bredt D., Snyder S. Relative sparing of nitric oxide synthase-containing neurons in the hippocampal formation in Alzheimer's disease. Ann Neurol. 32:1992;818-820.
36. Ikeda U., Ikeda M., Kano S., Kanbe T., Shimada K. Effect of cilostazol, a cAMP phosphodiesterase inhibitor, on nitric oxide production by vascular smooth muscle cells. Eur J Pharmacol. 314:1996;197-202.
37. Ince P.G., McArthur F.K., Bjertness E., Torvik A., Candy J.M., Edwardson J.A. Neuropathological diagnoses in elderly patients in Oslo Alzheimer's disease, Lewy body disease, vascular lesions . Dementia. 6:1995;162-168.
38. Jendroska K., Hoffmann O.M., Patt S. Amyloid beta peptide and precursor protein (APP) in mild and severe brain ischemia. Ann N Y Acad Sci. 826:1997;401-405.
39. Kalaria R.N., Cohen D.L., Premkumar D.R. Apolipoprotein E alleles and brain vascular pathology in Alzheimer's disease. Ann NY Acad Sci. 777:1996;266-270.
40. Kanowski S., Herrmann W.M., Stephan K., Wierich W., Horr R. Proof of efficacy of the ginkgo biloba special extract EGb 761 in outpatients suffering from mild to moderate primary degenerative dementia of the Alzheimer type or multi-infarct dementia. Pharmacopsychiatry. 29:1996;47-56.
41. Katsunuma H., Shimizu T., Ogawa K., Kubo H., Ishida H., Yoshihama A. Treatment of insomnia by concomitant therapy with Zopiclone and Aniracetam in patients with cerebral infarction, cerebroatrophy, Alzheimer's disease and Parkinson's disease. [In Process Citation] Psychiatry Clin Neurosci. 52:1998;198-200.
42. Kawamura J., Meyer J.S., Terayama Y., Weathers S. Leuko-araiosis and cerebral hypoperfusion compared in elderly normals and Alzheimer's dementia. J Am Geriatr Soc. 40:1992;375-380.
43. Klatt P., Schmidt K., Uray G., Mayer B. Multiple catalytic functions of brain nitric oxide synthase. Biochemical characterization, cofactor requirement, and the role of Nw-hydroxy-L-arginine as an intermediate. J Biol Chem. 268:1993;14781-14787.
44. 2+/calmodulin dependent nitric oxide synthase and a soluble guanylyl cyclase in vertebrate photoreceptor cells. EMBO J. 13:1994;3312-3320.
45. Koprowski H., Zheng Y., Heber-Katz E., et al. In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases. Proc Natl Acad Sci USA. 90:1993;3024-3027.
46. LaFerla F.M., Tinkle B.T., Bieberich C.J., Haudenschild C.C., Jay G. The Alzheimer's A beta peptide induces neurodegeneration and apoptotic cell death in transgenic mice. Nat Genet. 9:1995;21-30.
47. Le Bars P.L., Katz M.M., Berman N., Itil T.M., Freedman A.M., Schatzberg A.F. A placebo-controlled, double-blind, randomized trial of an extract of Ginkgo biloba for dementia. North American EGb Study Group. [see comments] JAMA. 278:1997;1327-1332.
48. Leist M., Fava E., Montecucco C., Nicotera P. Peroxynitrite and nitric oxide donors induce neuronal apoptosis by eliciting autocrine excitotoxicity. Eur J Neurosci. 9:1997;1488-1498.
49. Li L., Wu W., Lin L., Lei M., Oppenheim R., Houenou L. Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc Natl Acad Sci USA. 92:1995;9771-9775.
50. Lipton S., Choi Y., Pan Z., et al. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature. 364:1993;626-632.
51. Lopez O.L., Rabin B.S., Huff F.J., Rezek D., Reinmuth O.M. Serum autoantibodies in patients with Alzheimer's disease and vascular dementia and in nondemented control subjects. Stroke. 23:1992;1078-1083.
52. MacGibbon G.A., Lawlor P.A., Sirimanne E.S., et al. Bax expression in mammalian neurons undergoing apoptosis, and in Alzheimer's disease hippocampus. Brain Res. 750:1997;223-234.
53. Merrill J., Ignarro L., Sherman M., Melinek J., Lane T. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J Immunol. 151:1993;2132-2141.
54. Mesenge C., Verrecchia C., Allix M., Boulu R., Plotkine M. Reduction of the neurological deficit in mice with traumatic brain injury by nitric oxide synthase inhibitors. J Neurotrauma. 13:1996;11-16.
55. Mirra S.S., Heyman A., McKeel D., et al. The consortium to establish a registry for Alzheimer's disease (CERAD). II. Standardization of the neuropathological assessment of Alzheimer's disease. Neurology. 41:1991;479-486.
56. Nagata K., Buchan R.J., Yokoyama E., et al. Misery perfusion with preserved vascular reactivity in Alzheimer's disease. Ann NY Acad Sci. 826:1997;272-281.
57. Nagy Z., Esiri M.M., Jobst K.A., et al. The effects of additional pathology on the cognitive deficit in Alzheimer disease. J Neuropathol Exp Neurol. 56:1997;165-170.
58. Nishikawa T., Kirsch J., Koehler R., Bredt D., Snyder S., Traystmann R. Effect of nitric oxide synthase inhibition on cerebral blood flow and injury volume during focal ischemia in cats. Stroke. 24:1993;1717-1724.
59. Norris P., Waldvogel H., Faull R., Love D., Emson P. Decreased neuronal nitric oxide synthase messenger RNA and somatostatin messenger RNA in the striatum of Huntington's disease. Neuroscience. 72:1996;1037-1047.
60. Novikov L., Novikova L., Kellerth J. Brain-derived neurotrophic factor promotes survival and blocks nitric oxide synthase expression in adult rat spinal motoneurons after ventral root avulsion. Neurosci Lett. 200:1995;45-48.
61. Nowicky A., Bindman L. The nitric oxide synthase inhibitor, N-monomethyl-L-arginine blocks induction of a long-term potentiation-like phenomenon in rat medial frontal cortical neurons in vitro. J Neurophysiol. 70:1993;1255-1259.
62. O'Dell T., Huang P., Dawson T., et al. Endothelial NOS and blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science. 265:1994;542-546.
63. Olichney J.M., Hansen L.A., Hofstetter C.R., Grundman M., Katzman R., Thal L.J. Cerebral infarction in Alzheimer's disease is associated with severe amyloid angiopathy and hypertension. Arch Neurol. 52:1995;702-708.
64. Osgawa N. Free radicals and neural cell damage. Rinsho Shinkeigaku. 34:1994;1266-1268.
65. Oury T., Piantadosi C., Crapo J. Cold-induced brain edema in mice Involvement of extracellular superoxide dismutase and nitric oxide . J Biol Chem. 268:1993;15394-15398.
66. Ozawa T. Mitochondrial DNA mutations associated with aging and degenerative diseases. Exp Gerontol. 30:1995;269-290.
67. Ozawa T. Genetic and functional changes in mitochondria associated with aging. Physiol Rev. 77:1997;425-464.
68. Pantoni L., Garcia J.H. Cognitive impairment and cellular/vascular changes in the cerebral white matter. Ann NY Acad Sci. 826:1997;92-102.
69. Pasquier F., Leys D. Why are stroke patients prone to develop dementia? J Neurol. 244:1997;135-142.
70. Peunova N., Enikolopov G. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature. 375:1995;68-73.
71. Pou S., Pou W., Bredt D., Snyder S., Rosen G. Generation of superoxide by purified brain nitric oxide synthase. J Biol Chem. 267:1992;24173-24176.
72. Premkumar D.R., Cohen D.L., Hedera P., Friedland R.P., Kalaria R.N. Apolipoprotein E-epsilon4 alleles in cerebral amyloid angiopathy and cerebrovascular pathology associated with Alzheimer's disease. Am J Pathol. 148:1996;2083-2095.
73. Richter C. Reactive oxygen and DNA damage in mitochondria. Mutat Res. 275:1992;249-255.
74. Richter C. Oxidative damage to mitochondrial DNA and its relationship to ageing. Int J Biochem Cell Biol. 27:1995;647-653.
75. Sayre L.M., Zelasko D.A., Harris P.L., Perry G., Salomon R.G., Smith M.A. 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J Neurochem. 68:1997;2092-2097.
76. Schapira AHV. Mitochondrial dysfunction in neurodegenerative disorders and aging. In: Schapira AHV, DiMauro S, editors. Mitochondrial disorders in neurology. Vol. 14. London: Butterworth-Heinemann Ltd, 1994. p. 227-4.
77. Schmidt H., Walter U. NO at work. Cell. 78:1994;919-925.
78. Sevush S., Durara R., Rivero J., Pascal S., Barker W.W. Clinicopathologic study of probable Alzheimer disease assessment of criteria for excluding cerebrovascular disease . Alzheimer Dis Assoc Disord. 9:1995;208-212.
79. Smith M.A., Harris P.L., Sayre L.M., Perry G. Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc Natl Acad Sci USA. 94:1997;9866-9868.
80. Smith M.A., Perry G. Free radical damage, iron, and Alzheimer's disease. J Neurol Sci. 134:(suppl):1995;92-94.
81. Smith M.A., Sayre L.M., Monnier V.M., Perry G. Oxidative post-translational modifications in Alzheimer disease. A possible pathogenic role in the formation of senile plaques and neurofibrillary tangles. Mol Chem Neuropathol. 28:1996;41-48.
82. Snowdon D.A., Greiner L.H., Mortimer J.A., Riley K.P., Greiner P.A., Markesbery W.R. Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. [see comments] JAMA. 277:1997;813-817.
83. Sohn Y.K., Ganju N., Bloch K.D., Wands J.R., de la Monte S.M. Neuritic sprouting with aberrant expression of the nitric oxide synthase III gene in neurodegenerative diseases. J Neurol Sci. 162:1999;133-151.
84. Son H., Hawkins R., Kiebler M., Huang P., Fishman M., Kandel E. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell. 87:1996;1015-1023.
85. Stamler J. Nitration and related target interactions of nitric oxide. (Review) Cell. 78:1994;931-936.
86. Stamler J. Redox signaling nitration and related target interactions of nitric oxide . (Review) Cell. 78:1994;931-936.
87. Su J.H., Deng G., Cotman C.W. Bax protein expression is increased in Alzheimer's brain correlations with DNA damage, Bcl-2 expression, and brain pathology . J Neuropathol Exp Neurol. 56:1997;86-93.
88. Suttorp N., Hippenstiel S., Fuhrmann M., Krull M., Podzuweit T. Role of nitric oxide and phosphodiesterase isoenzyme II for reduction of endothelial hyperpermeability. Am J Physiol. 270:1996;C778-C785.
89. Thomas T., Sutton E.T., Bryant M.W., Rhodin J.A. In vivo vascular damage, leukocyte activation and inflammatory response induced by beta-amyloid. J Submicrosc Cytol Pathol. 29:1997;293-304.
90. Thomas T., Thomas G., McLendon C., Sutton T., Mullan M. beta-Amyloid-mediated vasoactivity and vascular endothelial damage. [see comments] Nature. 380:1996;168-171.
91. Tohgi H., Yonezawa H., Takahashi S., et al. Cerebral blood flow and oxygen metabolism in senile dementia of Alzheimer's type and vascular dementia with deep white matter changes. Neuroradiology. 40:1998;131-137.
92. Tomimoto H., Akiguchi I., Suenaga T., et al. Alterations of the blood-brain barrier and glial cells in white-matter lesions in cerebrovascular and Alzheimer's disease patients. [see comments] Stroke. 27:1996;2069-2074.
93. Tomimoto H., Akiguchi I., Wakita H., Suenaga T., Nakamura S., Kimura J. Regressive changes of astroglia in white matter lesions in cerebrovascular disease and Alzheimer's disease patients. Acta Neuropathol (Berl). 94:1997;146-152.
94. Van Nostrand W.E., Davis S.J., Saporito I.S. Amyloid beta-protein induces the cerebrovascular cellular pathology of Alzheimer's disease and related disorders. Ann NY Acad Sci. 777:1996;297-302.
95. Victoroff J., Mack W.J., Lyness S.A., Chui H.C. Multicenter clinicopathological correlation in dementia. Am J Psychiatry. 152:1995;1476-1484.
96. Vodovotz Y., Lucia M., Flanders K., et al. Inducible nitric oxide synthase in tangle-bearing neurons of patients with Alzheimer's disease. J Exp Med. 184:1996;1425-1433.
97. Ward S., Shuttleworth C., Kenyon J. Dorsal root ganglion neurons of embryonic chicks contain nitric oxide synthase and respond to nitric oxide. Brain Res. 648:1994;249-258.
98. Wisniewski H.M., Maslinska D. Beta-protein immunoreactivity in the human brain after cardiac arrest. Folia Neuropathol. 34:1996;65-71.
99. Wolf G., Henschke G., Wurdig S. Glutamate agonist-induced hippocampal lesion and nitric oxide synthase/NADPH-diaphorase a light and electron microscopical study in the rat . Neurosci Lett. 161:1993;49-52.
100. Wu H.M., Yuan Y., Zawieja D.C., Tinsley J., Granger H.J. Role of phospholipase C, protein kinase C, and calcium in VEGF-induced venular hyperpermeability. Am J Physiol. 276:1999;H535-H542.
101. Wu W., Liuzzi F., Schinco F., et al. Neuronal nitric oxide synthase is induced in spinal neurons by traumatic injury. Neuroscience. 61:1994;719-726.
102. Xia Y., Dawson V., Dawson T., Snyder S., Zweier J. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc Natl Acad Sci USA. 93:1996;6770-6774.
103. Yamatsuji T., Okamoto T., Shizu T., Murayama Y., Tanaka N., Nishimoto I. Expression of V642 APP mutant causes cellular apoptosis as Alzheimer train-linked phenotype. EMBO J. 15:1996;498-509.
104. Yan S.D., Yan S.F., Chen X., et al. Non-enzymatically glycated tau in Alzheimer's disease induces neuronal oxidant stress resulting in cytokine gene expression and release of amyloid beta-peptide. Nat Med. 1:1995;693-699.
105. Yezierski R., Liu S., Ruenes G., Busto R., Dietrich W. Neuronal damage following intraspinal injection of a nitric oxide synthase inhibitor in the rat. J Cereb Blood Flow Metab. 16:1996;996-1004.
106. Yoshitake T., Kiyohara Y., Kato I., et al. Incidence and risk factors of vascular dementia and Alzheimer's disease in a defined elderly Japanese population the Hisayama Study . Neurology. 45:1995;1161-1168.
107. Yuan Y., Granger H.J., Zawieja D.C., DeFily D.V., Chilian W.M. Histamine increases venular permeability via a phospholipase C-NO synthase-guanylate cyclase cascade. Am J Physiol. 264:1993;H1734-H1739.
108. Zahner B., Lang C.J., Engelhardt A., Thierauf P., Neundorfer B. A case of Alzheimer's disease with extensive focal white matter changes. Dementia. 6:1995;294-300.
109. Zheng Y., Schafer M.-H., Weihe E., et al. Severity of neurological signs and degree of inflammatory lesions in the brains of rats with Borna disease correlated with induction of nitric oxide synthase. J Virol. 67:1993;5786-5791.
110. Zilles K., Qu M., Schleicher A., Schroeter M., Kraemer M., Witte O.W. Plasticity and neurotransmitter receptor changes in Alzheimer's disease and experimental cortical infarcts. Arzneimittelforschung. 45:1995;361-366.