Inhibition of central angiotensin II enhances memory function and reduces oxidative stress status in rat hippocampus

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 43, Issue , 2013, Pages 79-88

  Bild, Walther ^a,c   Hritcu, Lucian ^b   Stefanescu, Cristinel ^a   Ciobica, Alin ^b,c  

^a GRIGORE T POPA UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^b ALEXANDRU IOAN CUZA UNIVERSITY OF IASI   (Romania)

^c Octav Mayer Institute of Mathematics   (Romania)

Author keywords

Angiotensin II; Memory; Oxidative stress

Indexed keywords

1 (4 AMINO 3 METHYLBENZYL) 5 DIPHENYLACETYL 4,5,6,7 TETRAHYDROIMIDAZO[4,5 C]PYRIDINE 6 CARBOXYLIC ACID; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ANGIOTENSIN 2 RECEPTOR ANTAGONIST; ANGIOTENSIN II; CAPTOPRIL; GLUTATHIONE PEROXIDASE; LOSARTAN; MALONALDEHYDE; SODIUM CHLORIDE; SUPEROXIDE DISMUTASE;

AMNESIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; HIPPOCAMPUS; LATENT PERIOD; LIPID PEROXIDATION; LONG TERM MEMORY; MALE; MAZE TEST; MEMORY; NONHUMAN; OXIDATIVE STRESS; PASSIVE AVOIDANCE; RAT; SHORT TERM MEMORY;

ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANGIOTENSIN II TYPE 2 RECEPTOR BLOCKERS; ANGIOTENSIN RECEPTOR ANTAGONISTS; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CAPTOPRIL; GLUTATHIONE PEROXIDASE; HIPPOCAMPUS; IMIDAZOLES; LIPID PEROXIDATION; LOSARTAN; MALE; MALONDIALDEHYDE; MAZE LEARNING; MEMORY; MEMORY, SHORT-TERM; OXIDATIVE STRESS; PSYCHOMOTOR PERFORMANCE; PYRIDINES; RATS; RATS, WISTAR; SUPEROXIDE DISMUTASE;

EID: 84872410904     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2012.12.009     Document Type: Article

References (106)

1. Akhavan M., Emami-Abarghoie M., Sadighi-Moghaddam B., Safari M., Yousefi Y., Rashidy-Pour A. Hippocampal angiotensin II receptors play an important role in mediating the effect of voluntary exercise on learning and memory in rat. Brain Res 2008, 1232:132-138.
2. Armstrong D.L., Garcia E.A., Ma T., Quinones B., Wayner M.J. Angiotensin II blockade of long-term potentiation at the perforant path-granule cell synapse in vitro. Peptides 1996, 17(4):689-693.
3. Anderson C., Teo K., Gao P., Arima H., Dans A., Unger T. Renin angiotensin system blockade and cognitive function in patients at high risk of cardiovascular disease: analysis of data from the ONTARGET and TRANSCEND studies. Lancet Neurol 2011, 10:43-53.
4. Antelava N., Gongadze N., Gogolauri M., Kezeli T., Pachkoriia K. Comparative characteristic of angiotensin-converting enzyme inhibitor - captopril and the angiotensin II receptor blockers - losartan action on the oxidative metabolism in experimental hyperlipidemia in rabbits. Georgian Med News 2007, 150:57-60.
5. Barnes J., Barnes N., Costall B., Horovitz Z., Ironside J., Naylor R. Angiotensin II inhibits acetylcholine release from human temporal cortex: implications for cognition. Brain Res 1990, 507:341-343.
6. Basso N., Cini R., Pietrelli A., Ferder L., Terragno N. Protective effect of long-term angiotensin II inhibition. Am J Physiol Heart Circ Physiol 2007, 293:1351-1358.
7. Becker C., Jick S., Meier C. Use of antihypertensives and the risk of Parkinson disease. Neurology 2008, 70:1438-1444.
8. Benigni A., Cassis P., Remuzzi G. Angiotensin II revisited: new roles in inflammation, immunology and aging. EMBO Mol Med 2010, 2:247-257.
9. Bild W., Ciobica A. Angiotensin-(1-7) central administration induces anxiolytic-like effects in elevated plus maze and decreased oxidative stress in the amygdala. J Affect Disord 2012, [Epub ahead of print] [PubMed PMID:22868060]. 10.1016/j.jad.2012.07.024.
10. Bonini J., Bevilaqua L., Zinn C., Kerr D., Medina J., Izquierdo I., et al. Angiotensin II disrupts inhibitory avoidance memory retrieval. Horm Behav 2006, 50:308-313.
11. Braszko J. AT(2) but not AT(1) receptor antagonism abolishes angiotensin II increase of the acquisition of conditioned avoidance responses in rats. Behav Brain Res 2002, 131:79-86.
12. Braszko J. Valsartan abolishes most of the memory-improving effects of intracerebroventricular angiotensin II in rats. Clin Exp Hypertens 2005, 27:635-649.
13. Braszko J., Kupryszewski G., Witczuk B., Wiśniewski K. Angiotensin II-(3-8)-hexapeptide affects motor activity, performance of passive avoidance and a conditioned avoidance response in rats. Neuroscience 1988, 27:777-783.
14. Braszko J., Kupryszewski G., Witczuk B., Wisniewski K. Angiotensin II(3-8) hexapeptide affects motor activity, performance of passive avoidance and a conditioned avoidance response in rats. Neuroscience 1988, 27:777-783.
15. Braszko J., Karwowska-Polecka W., Halicka D., Gard P. Captopril and enalapril improve cognition and depressed mood in hypertensive patients. J Basic Clin Physiol Pharmacol 2003, 14:323-343.
16. Braszko J., Kulakowska A., Winnicka M. Effects of angiotensin II and its receptor antagonists on motor activity and anxiety in rats. J Physiol Pharmacol 2003, 54:271-281.
17. Braszko J., Walesiuk A., Wielgat P. Cognitive effects attributed to angiotensin II may result from its conversion to angiotensin IV. J Renin Angiotensin Aldosterone Syst 2006, 7:168-174.
18. Chabrashvili T., Kitiyakara C., Blau J., Karber A., Aslam S., Welch W., et al. Effects of ANG II type 1 and 2 receptors on oxidative stress, renal NADPH oxidase, and SOD expression. Am J Physiol Regul Integr Comp Physiol 2003, 285:117-124.
19. Chalas A., Conway E. No evidence for involvement of angiotensin II in spatial learning in water maze in rats. Behav Brain Res 1996, 81:199-205.
20. Ciobica A., Bild W., Hritcu L., Haulica I. Brain renin-angiotensin system in cognitive function: pre-clinical findings and implications for prevention and treatment of dementia. Acta Neurol Belg 2009, 109:171-180.
21. Ciobica A., Hritcu L., Nastasa V., Padurariu M., Bild W. Inhibition of central angiotensin converting enzyme exerts anxiolytic effects by decreasing brain oxidative stress. J Med Biochem 2010, 30(2):109-114.
22. Ciobica A., Hritcu L., Bild V., Padurariu M., Bild W. The effects of angiotensin II and its receptor blockers on anxiety status and central oxidative stress in rat. J Neurol 2011, 258:69-70.
23. Ciobica A., Olteanu Z., Padurariu M., Hritcu L. The effects of pergolide on memory and oxidative stress in a rat model of Parkinson's disease. J Physiol Biochem 2012, 68:59-69.
24. Culman J., Baulmann J., Blume A., Unger T. The renin-angiotensin system in the brain: an update. J Renin Angiotensin Aldosterone Syst 2001, 2:96-102.
25. Culman J., Blume A., Gohlke P., Unger T. The renin-angiotensin system in the brain: possible therapeutic implications for AT(1)-receptor blockers. J Hum Hypertens 2002, 16:64-70.
26. Danielyan L., Klein R., Hanson L.R., Buadze M., Schwab M., Gleiter C. Protective effects of intranasal losartan in the APP/PS1 transgenic mouse model of Alzheimer disease. Rejuvenation Res 2010, 13:195-201.
27. Davies N., Kehoe P., Ben-Shlomo Y., Martin R. Associations of antihypertensive treatments with Alzheimer's disease, vascular dementia, and other dementias. J Alzheimers Dis 2011, 26:699-708.
28. Diener H., Sacco R., Yusuf S., Cotton D., Ounpuu S., Lawton W., et al. Effects of aspirin plus extended-release dipyridamole versus clopidogrel and telmisartan on disability and cognitive function after recurrent stroke in patients with ischaemic stroke in the prevention regimen for effectively avoiding second strokes (PRoFESS) trial: a double-blind, active and placebo-controlled study. Lancet Neurol 2008, 7:875-884.
29. Duron E., Hanon O. Antihypertensive treatments, cognitive decline, and dementia. J Alzheimers Dis 2010, 20:903-914.
30. Eckman E., Adams S., Troendle F., Stodola B., Kahn M., Fauq A. Regulation of steady-state beta-amyloid levels in the brain by neprilysin and endothelin-converting enzyme but not angiotensin-converting enzyme. J Biol Chem 2006, 281:30471-30478.
31. Eichenbaum H., Cohen N. Memory, amnesia, and the hippocampal system 1993, MIT Press.
32. Gard P. The role of angiotensin II in cognition and behaviour. Eur J Pharmacol 2002, 438:1-14.
33. Gard P. Cognitive-enhancing effects of angiotensin IV. BMC Neurosci 2008, 9:S15.
34. Gard P.R., Rusted J.M. Angiotensin and Alzheimer's disease: therapeutic prospects. Expert Rev Neurother 2004, 4(1):87-96.
35. Gelband C., Zhu M., Lu D., Reagan L., Fluharty S., Posner P. Functional interactions between neuronal AT1 and AT2 receptors. Endocrinology 1997, 138:2195-2198.
36. Gonzales S., Noriega G., Tomaro M., Peña C. Angiotensin-(1-7) stimulates oxidative stress in rat kidney. Regul Pept 2002, 106:67-70.
37. Griendling K.K., Sorescu D., Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 2000, 86:494-501.
38. Hanif K., Snehlata Pavar C., Arif E., Biswas P., Fahim M., Pasha M., et al. Effect of 3-thienylalanine-ornithine-proline, new sulfur-containing angiotensin-converting enzyme inhibitor on blood pressure and oxidative stress in spontaneously hypertensive rats. J Cardiovasc Pharmacol 2009, 53:145-150.
39. Haulica I., Neamtu C., Stratone A., Petrescu G., Branisteanu D., Rosca V., et al. Evidence for the involvement of cerebral renin-angiotensin system (RAS) in stress analgesia. Pain 1986, 27:237-245.
40. Haulica I., Bild W., Mihaila C.N., Ionita T., Boisteanu C.P., Neagu B. Biphasic effects of angiotensin (1-7) and its interactions with angiotensin II in rat aorta. J Renin Angiotensin Aldosterone Syst 2003, 4:124-128.
41. Haulica I., Bild W., Serban N. Angiotensin peptides and their pleiotropic actions. J Renin Angiotensin Aldosterone Syst 2005, 6:121-131.
42. Hefco V., Yamada K., Hefco A., Hritcu L., Tiron A., Nabeshima T. Role of the mesotelencephalic dopamine system in learning and memory processes in the rat. Eur J Pharmacol 2003, 475:55-60.
43. Hemming M., Selkoe D. Amyloid beta-protein is degraded by cellular angiotensin-converting enzyme (ACE) and elevated by an ACE inhibitor. J Biol Chem 2005, 280:37644-37650.
44. Hou Y., Wang L., Zhou K., Chen Y., Tian Z., Song J., et al. Altered angiotensin-converting enzyme and its effects on the brain in a rat model of Alzheimer disease. Chin Med J (Engl) 2008, 121:2320-2323.
45. Hritcu L., Clicinschi M., Nabeshima T. Brain serotonin depletion impairs short-term memory, but not long-term memory in rats. Physiol Behav 2007, 91:652-657.
46. Inaba S., Iwai M., Furuno M., Tomono Y., Kanno H., Senba I., et al. Continuous activation of renin-angiotensin system impairs cognitive function in renin/angiotensinogen transgenic mice. Hypertension 2009, 53:356-362.
47. Kerr D., Bevilaqua L., Bonini J., Rossato J.I., Kohler C., Medina J., et al. Angiotensin II blocks memory consolidation through an AT2 receptor-dependent mechanism. Psychopharmacology (Berl) 2005, 179:529-535.
48. Kumaran D., Udayabanu M., Kumar M., Aneja R., Katyal A. Involvement of angiotensin converting enzyme in cerebral hypoperfusion induced anterograde memory impairment and cholinergic dysfunction in rats. Neuroscience 2008, 155:626-639.
49. Laursen J., Rajagopalan S., Galis Z., Tarpey M., Freeman B., Harrison D. Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. Circulation 1997, 95:588-593.
50. Lee E., Ma Y., Wayner M., Armstrong D. Impaired retention by angiotensin-II mediated by the AT(1) receptor. Peptides 1995, 16:1069-1071.
51. Li N., Lee A., Whitmer R., Kivipelto M., Lawler E., Kazis L. Use of angiotensin receptor blockers and risk of dementia in a predominantly male population: prospective cohort analysis. BMJ 2011, 340:b5465.
52. Llorens-Cortes C., Mendelsohn F. Organisation and functional role of the brain angiotensin system. J Renin Angiotensin Aldosterone Syst 2002, 1:39-48.
53. Lopez-Real A., Rey P., Soto-Otero R., Mendez-Alvarez E., Labandeira-Garcia J.L. Angiotensin-reduces oxidative stress and protects dopaminergic neurons in a 6-hydroxydopamine rat model of Parkinsonism. J Neurosci Res 2005, 81:865-873.
54. Machado R., Santos R., Andrade S. Opposing actions of angiotensins on angiogenesis. Life Sci 2000, 66:67-76.
55. Maes M., Fišar Z., Medina M., Scapagnini G., Nowak G., Berk M. New drug targets in depression: inflammatory, cell-mediated immune, oxidative and nitrosative stress, mitochondrial, antioxidant, and neuroprogressive pathways. And new drug candidates - Nrf2 activators and GSK-3 inhibitors. Inflammopharmacology 2012, 20:127-150.
56. Manschot S., Biessels G., Cameron N., Cotter M., Kamal A., Kappelle L., et al. Angiotensin converting enzyme inhibition partially prevents deficits in water maze performance, hippocampal synaptic plasticity and cerebral blood flow in streptozotocin-diabetic rats. Brain Res 2003, 966:274-282.
57. Maul B., Von Bohlen Und Halbach O., Becker A., Sterner-Kock A., Voigt J.P. Impaired spatial memory and altered dendritic spine morphology in angiotensin II type 2 receptor-deficient mice. J Mol Med 2008, 86:563-571.
58. Mavroudis I., Fotiou D., Manani M., Njaou S., Frangou D., Costa V., et al. Dendritic pathology and spinal loss in the visual cortex in Alzheimer's disease: a Golgi study in pathology. Int J Neurosci 2011, 121:347-354.
59. McKinley M., Albiston A., Allen A., Mathai M., May C., McAllen R., et al. The brain renin-angiotensin system: location and physiological roles. Int J Biochem Cell Biol 2003, 35:901-918.
60. Miller S., Norton L., Murphy M., Dalsing M., Unthank J. The role of the renin-angiotensin system and oxidative stress in spontaneously hypertensive rat mesenteric collateral growth impairment. Am J Physiol Heart Circ Physiol 2007, 292:2523-2531.
61. Miners S., Ashby E., Baig S., Harrison R., Tayler H., Speedy E. Angiotensinconverting enzyme levels and activity in Alzheimer's disease: differences in brain and CSF ACE and association with ACE1 genotypes. Am J Transl Res 2009, 1:163-177.
62. Miners J., van Helmond Z., Kehoe P., Love S. Changes with age in the activities of beta-secretase and the Abeta-degrading enzymes neprilysin, insulin-degrading enzyme and angiotensin-converting enzyme. Brain Pathol 2010, 20:794-802.
63. Mogi M., Iwanami Jun, Jing Fei, Tsukuda Kana, Horiuchi Masatsugu Co-treatment with memantine and compound 21, an angiotensin II type 2 receptor agonist, prevents cognitive decline in type 2 diabetic mice. Alzheimers Dement 2012, 8:P707.
64. Morgan J., Routtenberg A. Angiotensin injected into the neostriatum after learning disrupts retention performance. Science 1977, 196:87-89.
65. Munzel T., Keaney J.F. Are ACE inhibitors a "magic bullet" against oxidative stress?. Circulation 2001, 104:1571-1574.
66. Nikolova J., Getova D., Nikolov F. Effects of ACE inhibitors on learning and memory processes in rats. Folia Med (Plovdiv) 2000, 42:47-51.
67. Ohrui T., Matsui M., Yamaya H., Arai S., Ebihara M., Maruyama H. Angiotensin-converting enzyme inhibitors and incidence of Alzheimer's disease in Japan. J Am Geriatr Soc 2004, 52:649-650.
68. Padurariu M., Ciobica A., Dobrin I., Stefanescu C. Evaluation of antioxidant enzymes activities and lipid peroxidation in schizophrenic patients treated with typical and atypical antipsychotics. Neurosci Lett 2010, 479:317-320.
69. Padurariu M., Ciobica A., Hritcu L., Stoica B., Bild W., Stefanescu C. Changes of some oxidative stress markers in the serum of patients with mild cognitive impairment and Alzheimer's disease. Neurosci Lett 2010, 469:6-10.
70. Patrick G., Gordon K.W. Is inhibition of the renin-angiotensin system a new treatment option for Alzheimer's disease?. Lancet Neurol 2007, 6:373-378.
71. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2006, Academic Press Elsevier, San Diego. 6th ed.
72. Pedreanez A., Arcaya J.L., Carrizo E., Mosquera J. Forced swimming test increases superoxide anion positive cells and angiotensin II positive cells in the cerebrum and cerebellum of the rat. Brain Res Bull 2006, 71:18-22.
73. Raghavendra V., Chopra K., Kulkarni S. Comparative studies on the memory-enhancing actions of captopril and losartan in mice using inhibitory shock avoidance paradigm. Neuropeptides 2001, 35:65-69.
74. Rajagopalan S., Kurz S., Münzel T., Tarpey M., Freeman B., Griendling K., et al. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. J Clin Invest 1996, 97:1916-1923.
75. Rosenberg P., Mielke M., Tschanz J., Cook L., Corcoran C., Hayden K., et al. Effects of cardiovascular medications on rate of functional decline in Alzheimer disease. Am J Geriatr Psychiatry 2008, 16:883-892.
76. Saavedra J. Brain angiotensin II: new developments, unanswered questions and therapeutic opportunities. Cell Mol Neurobiol 2005, 25:485-512.
77. Saavedra J. Angiotensin II AT(1) receptor blockers ameliorate inflammatory stress: a beneficial effect for the treatment of brain disorders. Cell Mol Neurobiol 2012, 32:667-681.
78. Santos R.A.S., Campagnole-Santos M.J., Andrade S.P. Angiotensin-(1-7): an update. Regul Pept 2000, 91:45-62.
79. Savaskan K.C., Hock G., Olivieri S., Bruttel C., Rosenberg C., Hulette F., et al. Cortical alterations of angiotensin converting enzyme, angiotensin II and AT1 receptor in Alzheimer's dementia. Neurobiol Aging 2001, 22:541-546.
80. Sharma B., Singh N. Experimental hypertension induced vascular dementia: pharmacological, biochemical and behavioral recuperation by angiotensin receptor blocker and acetylcholinesterase inhibitor. Pharmacol Biochem Behav 2012, 102:101-108.
81. Shepherd J., Bill D., Dourish C., Grewal S., Mclenachan A., Stanhope K. Effects of the selective angiotensin II receptor antagonists losartan and PD123177 in animal models of anxiety and memory. Psychopharmacology (Berl) 1996, 126:206-218.
82. Sies H. Oxidative stress: oxidants and antioxidants. Exp Physiol 1997, 82:291-295.
83. Sleegers K.T., Heijer E.J., van Dijk A., Hofman A.M., Bertoli-Avella P.J., Koudstaal M.M., et al. ACE gene is associated with Alzheimer's disease and atrophy of hippocampus and amygdala. Neurobiol Aging 2005, 26:1153-1159.
84. Stefanescu C., Ciobica A. The relevance of oxidative stress status in first episode and recurrent depression. J Affect Disord 2012, 143(1-3):34-38.
85. Tchekalarova J., Albrecht D. Angiotensin II suppresses long-term potentiation in the lateral amygdala of mice via L-type calcium channels. Neurosci Lett 2007, 415:68-72.
86. Thone-Reineke C., Zimmermann M., Neumann C., Krikov M., Li J., Gerova N., et al. Are angiotensin receptor blockers neuroprotective?. Curr Hypertens Rep 2004, 6:257-266.
87. Tota S., Kamat P., Saxena G., Hanif K., Najmi A., Nath C. Central angiotensin converting enzyme facilitates memory impairment in intracerebroventricular streptozotocin treated rats. Behav Brain Res 2011, 226:317-330.
88. Tota S., Kamat P., Saxena G., Hanif K., Najmi A., Nath C. Central angiotensin converting enzyme facilitates memory impairment in intracerebroventricular streptozotocin treated rats. Behav Brain Res 2012, 226:317-330.
89. Tota S., Nath C., Najmi A.K., Shukla R., Hanif K. Inhibition of central angiotensin converting enzyme ameliorates scopolamine induced memory impairment in mice: role of cholinergic neurotransmission, cerebral blood flow and brain energy metabolism. Behav Brain Res 2012, 232:66-76.
90. Tzourio C., Anderson N., Chapman M., Woodward B., Neal S., MacMahon J., et al. Effects of blood pressure lowering with perindopril and indapamide therapy on dementia and cognitive decline in patients with cerebrovascular disease. Arch Intern Med 2003, 163:1069-1075.
91. Vargas R., Rincón J., Pedreañez A., Viera N., Hernández-Fonseca J.P., Peña C., et al. Role of angiotensin II in the brain inflammatory events during experimental diabetes in rats. Brain Res 2012, 1453:64-76.
92. von Bohlen und Halbach O., Albrecht D. Angiotensin II inhibits long-term potentiation within the lateral nucleus of the amygdala through AT1 receptors. Peptides 1998, 19(6):1031-1036.
93. von Bohlen und Halbach O., Albrecht D. Identification of angiotensin IV binding sites in the mouse brain by a fluorescent binding study. Neuroendocrinology 2000, 72(4):218-223.
94. von Bohlen und Halbach O. Angiotensin IV in the central nervous system. Cell Tissue Res 2003, 311:1-9.
95. von Bohlen und Halbach O., Albrecht D. The CNS renin-angiotensin system. Cell Tissue Res 2006, 326:599-616.
96. Walther T., Voigt J., Fukamizu A., Fink H., Bader M. Learning and anxiety in angiotensin-deficient mice. Behav Brain Res 1999, 100:1-4.
97. Wang D., Chabrashvili T., Borrego L., Aslam S., Umans J. Angiotensin II infusion alters vascular function in mouse resistance vessels: roles of O and endothelium. J Vasc Res 2006, 43:109-119.
98. Winnicka M., Braszko J., Wiśniewski K. 6-OHDA lesions to amygdala and hippocampus attenuate memory-enhancing effect of the 3-7 fragment of angiotensin II. Gen Pharmacol 1998, 30:801-805.
99. Wright J., Harding J. The brain RAS and Alzheimer's disease. Exp Neurol 2011, 223:326-333.
100. Wyss J., Kadish I., van Groen T. Age-related decline in spatial learning and memory: attenuation by captopril. Clin Exp Hypertens 2003, 25:455-474.
101. Yanagitani Y., Rakugi H., Okamura A., Moriguchi K., Takiuchi S., Ohishi M. Angiotensin II type 1 receptor-mediated peroxide production in human macrophages. Hypertension 1999, 33:335-339.
102. Yao E., Fukuda N., Matsumoto T., Kobayashi N., Katakawa M., Yamamoto C., et al. Losartan improves the impaired function of endothelial progenitor cells in hypertension via an antioxidant effect. Hypertens Res 2007, 30:1119-1128.
103. Yasar S., Zhou J., Varadhan R., Carlson C. The use of angiotensin converting enzyme inhibitors and diuretics is associated with a reduced incidence of impairment on cognition in elderly women. Clin Pharmacol Ther 2008, 84:119-126.
104. Yasar S., Lin F., Fried L., Kawas C., Sink K., DeKosky S., et al. Diuretic use is associated with better learning and memory in older adults in the Ginkgo Evaluation of Memory Study. Alzheimers Dement 2012, 8:188-195. Ginkgo Evaluation of Memory (GEM) Study Investigators.
105. Zhang M., Mao Y., Ramirez S.H., Tuma R.F., Chabrashvili T. Angiotensin II induced cerebral microvascular inflammation and increased blood-brain barrier permeability via oxidative stress. Neuroscience 2010, 171:852-858.
106. Zhang Z., Deng L., Yu H., Shi Y., Bai F., Xie C., Yuan Y., Jia J., Zhang Z. Association of angiotensin-converting enzyme functional gene I/D polymorphism with amnestic mild cognitive impairment. Neurosci Lett 2012, 514(1):131-135.