Angiotensin-(1-7)/Mas axis integrity is required for the expression of object recognition memory

Neurobiology of Learning and Memory

Volumn 97, Issue 1, 2012, Pages 113-123

  Lazaroni, Thiago L N ^a   Raslan, Ana Cláudia S ^a   Fontes, Walkiria R P ^a   de Oliveira, Marilene L ^a   Bader, Michael ^b   Alenina, Natalia ^b   Moraes, Márcio F D ^a   dos Santos, Robson A ^a   Pereira, Grace S ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Angiotensin (1 7); AT1 receptor; Object recognition memory; Receptor Mas

Indexed keywords

1 (4 DIMETHYLAMINO 3 METHYLBENZYL) 5 DIPHENYLACETYL 4,5,6,7 TETRAHYDRO 1H IMIDAZO[4,5 C]PYRIDINE 6 CARBOXYLIC ACID; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN I; ANGIOTENSIN II; ANGIOTENSIN[1-7]; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR MAS; LOSARTAN; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN LEVEL; BRAIN REGION; CONCENTRATION RESPONSE; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; KNOCKOUT MOUSE; MAZE TEST; MOUSE; NONHUMAN; OBJECT RECOGNITION MEMORY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BLOCKING; TASK PERFORMANCE; TISSUE DISTRIBUTION; VISUAL MEMORY;

ANGIOTENSIN I; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANGIOTENSIN II TYPE 2 RECEPTOR BLOCKERS; ANIMALS; HIPPOCAMPUS; IMIDAZOLES; LOSARTAN; MICE; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS; PYRIDINES; RECEPTORS, ANGIOTENSIN; RECEPTORS, G-PROTEIN-COUPLED; RECOGNITION (PSYCHOLOGY);

EID: 84155195033     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2011.10.003     Document Type: Article

References (102)

1. Albasser M.M., Davies M., Futter J.E., Aggleton J.P. Magnitude of the object recognition deficit associated with perirhinal cortex damage in rats: Effects of varying the lesion extent and the duration of the sample period. Behavioral Neuroscience 2009, 123:115-124.
2. Alenina N., Xu P., Rentzsch B., Patkin E.L., Bader M. Genetically altered animal models for Mas and Angiotensin-(1-7). Experimental Physiology 2008, 93:528-537.
3. 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, 17:689-693.
4. Barker G.R., Bird F., Alexander V., Warburton E.C. Recognition memory for objects, place, and temporal order: A disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. Journal of Neuroscience 2007, 27:2948-2957.
5. Becker L.K., Etelvino G.M., Walther T., Santos R.A., Campagnole-Santos M.J. Immunofluorescence localization of the receptor Mas in cardiovascular-related areas of the rat brain. American Journal of Physiology - Heart and Circulatory Physiology 2007, 293:H1416-H1424.
6. Becker L.K., Santos R.A.S., Campagnole-Santos M.J. Cardiovascular effects of angiotensin II and angiotensin-(1-7) at the RVLM of trained normotensive rats. Brain Research 2005, 1040:128-212.
7. Bekinschtein P., Katche C., Slipczuk L., Gonzalez C., Dorman G., Cammarota M., et al. Persistence of long-term memory storage: New insights into its molecular signatures in the hippocampus and related structures. Neurotoxicity Research 2010, 18:377-385.
8. Bekinschtein P., Katche C., Slipczuk L.N., Igaz L.M., Cammarota M., Izquierdo I., et al. mTOR signaling in the hippocampus is necessary for memory formation. Neurobiology of Learning and Memory 2007, 87:303-307.
9. Bernabeu R., Princ F., de Stein M.L., Fin C., Juknat A.A., Batile A., et al. Evidence for the involvement of hippocampal CO production in the acquisition and consolidation of inhibitory avoidance learning. NeuroReport 1995, 6:516-518.
10. Bevilaqua L.R., Kerr D.S., Medina J.H., Izquierdo I., Cammarota M. Inhibition of hippocampal Jun N-terminal kinase enhances short-term memory but blocks long-term memory formation and retrieval of an inhibitory avoidance task. European Journal of Neuroscience 2003, 17:897-902.
11. Bonini J.S., Bevilaqua L.R., Zinn C.G., Kerr D.S., Medina J.H., Izquierdo I., et al. Angiotensin II disrupts inhibitory avoidance memory retrieval. Hormones and Behavior 2006, 50:308-313.
12. Botelho L.M., Block C.H., Khosla M.C., Santos R.A. Plasma Angitensin(1-7) immunoreactivity is increased by salt load, water deprivation, and hemorrhage. Peptides 1994, 15:723-729.
13. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
14. Braszko J.J. AT(2) but not AT(1) receptor antagonism abolishes Angiotensin II increase of the acquisition of conditioned avoidance responses in rats. Behavioural Brain Research 2002, 131:79-86.
15. Braszko J.J. Involvement of D1 dopamine receptors in the cognitive effects of Angiotensin IV and des-Phe6 Angiotensin IV. Peptides 2004, 25:1195-1203.
16. Braszko J.J., Wisniewski K. Effect of Angiotensin II and saralasin on motor activity and the passive avoidance behavior of rats. Peptides 1988, 9:475-479.
17. Bunnemann B., Fuxe K., Metzger R., Mullins J., Jackson T.R., Hanley M.R., et al. Autoradiographic localization of mas proto-oncogene mRNA in adult rat brain using in situ hybridization. Neuroscience Letters 1990, 114:147-153.
18. Cammarota M., Bevilaqua L.R., Rossato J.I., Lima R.H., Medina J.H., Izquierdo I. Parallel memory processing by the CA1 region of the dorsal hippocampus and the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:10279-10284.
19. Cammarota M., Izquierdo I., Wolfman C., Levi de Stein M., Bernabeu R., Jerusalinsky D., et al. Inhibitory avoidance training induces rapid and selective changes in 3[H]AMPA receptor binding in the rat hippocampal formation. Neurobiology of Learning and Memory 1995, 64:257-264.
20. Capettini S.B., Moraes M.F., Prado V.F., Prado M.A., Pereira G.S. Vesicular acetylcholine transporter knock-down mice show sexual dimorphism on memory. Brain Research Bulletin 2011.
21. Carlson S.H., Wyss J.M. Neurohormonal regulation of the sympathetic nervous system: New insights into central mechanisms of action. Current Hypertension Reports 2008, 10:233-240.
22. Carroll J.C., Rosario E.R., Chang L., Stanczyk F.Z., Oddo S., LaFerla F.M., et al. Progesterone and estrogen regulate Alzheimer-like neuropathology in female 3×Tg-AD mice. Journal of Neuroscience 2007, 27:13357-13365.
23. Chappell M.C., Brosnihan K.B., Diz D.I., Ferrario C.M. Identification of Angiotensin-(1-7) in rat brain: Evidence for differential processing of Angiotensin peptides. Journal of Biological Chemistry 1989, 264:16518-16523.
24. Clark R.E., Zola S.M., Squire L.R. Impaired recognition memory in rats after damage to the hippocampus. Journal of Neuroscience 2000, 20:8853-8860.
25. Cohen-Matsliah S.I., Motanis H., Rosenblum K., Barkai E. A novel role for protein synthesis in long-term neuronal plasticity: Maintaining reduced postburst after hyperpolarization. Journal of Neuroscience 2010, 30:4338-4342.
26. Daemen M.J., Lombardi D.M., Bosman F.T., Schwartz S.M. Angiotensin II induces smooth muscle cell proliferation in the normal and injured rat arterial wall. Circulation Research 1991, 68:450-456.
27. Daniels D., Yee D.K., Faulconbridge L.F., Fluharty S.J. Divergent behavioral roles of Angiotensin receptor intracellular signaling cascades. Endocrinology 2005, 146:5552-5560.
28. De Bundel D., Smolders I., Vanderheyden P., Michotte Y. Ang II and Ang IV: Unraveling the mechanism of action on synaptic plasticity, memory, and epilepsy. CNS Neuroscience & Therapeutics 2008, 14:315-339.
29. De Bundel D., Smolders I., Yang R., Albiston A.L., Michotte Y., Chai S.Y. Angiotensin IV and LVV-haemorphin 7 enhance spatial working memory in rats: Effects on hippocampal glucose levels and blood flow. Neurobiology of Learning and Memory 2009, 92:19-26.
30. de Castro B.M., Pereira G.S., Magalhaes V., Rossato J.I., De Jaeger X., Martins-Silva C., et al. Reduced expression of the vesicular acetylcholine transporter causes learning deficits in mice. Genes, Brain and Behaviour 2009, 8:23-35.
31. de Kloet E.R., Oitzl M.S., Joels M. Stress and cognition: Are corticosteroids good or bad guys?. Trends in Neurosciences 1999, 22:422-426.
32. Denny J.B., Polan-Curtain J., Wayner M.J., Armstrong D.L. Angiotensin II blocks hippocampal long-term potentiation. Brain Research 1991, 567:321-324.
33. Dere E., Huston J.P., De Souza Silva M.A. Episodic-like memory in mice: Simultaneous assessment of object, place and temporal order memory. Brain Research Protocol 2005, 16:10-19.
34. Dere E., Huston J.P., De Souza Silva M.A. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neuroscience and Biobehavioral Reviews 2007, 31:673-704.
35. Dias-Peixoto M.F., Santos R.A.S., Gomes E.R.M., Alves M.N.M., Almeida P.W.M., et al. Molecular mechanisms involved in the angiotensin-(1-7)/Mas signaling pathway in cardiomyocytes. Hypertension 2009, 52(3):542-548.
36. Dong X., Han S., Zylka M.J., Simon M.I., Anderson D.J. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 2001, 106:619-632.
37. Feng Y., Xia H., Cai Y., Halabi C.M., Becker L.K., Santos R.A., et al. Brain selective overexpression of human angiotensin-converting enzyme type 2 attenuates neurogenic hypertension. Circulation Research 2010, 106:373-382.
38. Ferry B., Roozendaal B., McGaugh J.L. Basolateral amygdala noradrenergic influences on memory storage are mediated by an interaction between beta- and alpha1-adrenoceptors. Journal of Neuroscience 1999, 19:5119-5123.
39. Fogari R., Mugellini A., Zoppi A., Derosa G., Pasotti C., Fogari E., et al. Influence of losartan and atenolol on memory function in very elderly hypertensive patients. Journal of Human Hypertension 2003, 17:781-785.
40. Fontes M.A., Martins Pinge M.C., Naves V., Campagnole-Santos M.J., Lopes O.U. Cardiovascular effects produced by microinjection of angiotensins and angiotensin antagonists into the ventrolateral medulla of freely moving rats. Brain Research 1997, 750:305-310.
41. Fox W.M. Reflex-ontogeny and behavioral development of the mouse. Animal Behaviour 1965, 13:234-241.
42. Furini C.R., Rossato J.I., Bitencourt L.L., Medina J.H., Izquierdo I., Cammarota M. Beta-adrenergic receptors link NO/sGC/PKG signaling to BDNF expression during the consolidation of object recognition long-term memory. Hippocampus 2010, 20:672-683.
43. Guan Y., Liu Q., Zongxiang T., Srinivasa N., Raja S.N., Anderson D.J., et al. Mas-related G-protein-coupled receptors inhibit pathological pain in mice. PNAS 2010, 107:15933-15938.
44. Hellner K., Walther T., Schubert M., Albrecht D. Angiotensin-(1-7) enhances LTP in the hippocampus through the G-protein-coupled receptor Mas. Molecular and Cellular Neurosciences 2005, 29:427-435.
45. Holscher C. Stress impairs performance in spatial water maze learning tasks. Behavioural Brain Research 1999, 100:225-235.
46. Hughes R.N. The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory. Neuroscience and Biobehavioral Reviews 2004, 28:497-505.
47. Introini-Collison I.B., Miyazaki B., McGaugh J.L. Involvement of the amygdala in the memory-enhancing effects of clenbuterol. Psychopharmacology (Berl) 1991, 104:541-544.
48. Izquierdo I., Bevilaqua L.R., Rossato J.I., Bonini J.S., Da Silva W.C., Medina J.H., et al. The connection between the hippocampal and the striatal memory systems of the brain: A review of recent findings. Neurotoxicity Research 2006, 10:113-121.
49. Izquierdo I., Cammarota M., Medina J.H., Bevilaqua L.R. Pharmacological findings on the biochemical bases of memory processes: A general view. Neural Plasticity 2004, 11:159-189.
50. Jing G., Grammatopoulos T., Ferguson P., Schelman W., Weyhenmeyer J. Inhibitory effects of Angiotensin on NMDA-induced cytotoxicity in primary neuronal cultures. Brain Research Bulletin 2004, 62:397-403.
51. Kerr D.S., Bevilaqua L.R., Bonini J.S., Rossato J.I., Kohler C.A., Medina J.H., et al. Angiotensin II blocks memory consolidation through an AT2 receptor-dependent mechanism. Psychopharmacology (Berl) 2005, 179:529-535.
52. King D.L., Arendash G.W. Behavioral characterization of the Tg2576 transgenic model of Alzheimer's disease through 19 months. Physiology & Behavior 2002, 75:627-642.
53. King D.L., Arendash G.W. Maintained synaptophysin immunoreactivity in Tg2576 transgenic mice during aging: correlations with cognitive impairment. Brain Research 2002, 926:58-68.
54. Kostenis E., Milligan G., Christopoulos A., Sanchez-Ferrer C.F., Heringer-Walther S., Sexton P.M., et al. G-protein-coupled receptor Mas is a physiological antagonist of the Angiotensin II type 1 receptor. Circulation 2005, 111:1806-1813.
55. Kramar E.A., Armstrong D.L., Ikeda S., Wayner M.J., Harding J.W., Wright J.W. The effects of Angiotensin IV analogs on long-term potentiation within the CA1 region of the hippocampus in vitro. Brain Research 2001, 897:114-121.
56. Krizanova O., Kiss A., Zacikova L., Jezova D. Nitric oxide synthase mRNA levels correlate with gene expression of Angiotensin II type-1 but not type-2 receptors, renin or Angiotensin converting enzyme in selected brain areas. Physiological Research 2001, 50:473-480.
57. Lee J., Albiston A.L., Allen A.M., Mendelsohn F.A., Ping S.E., Barrett G.L., et al. Effect of I.C.V. injection of AT4 receptor ligands, NLE1-Angiotensin IV and LVV-hemorphin 7, on spatial learning in rats. Neuroscience 2004, 124:341-349.
58. Lembo P.M., Grazzini E., Groblewski T., O'Donnell D., Roy M.O., Zhang J., et al. Proenkephalin a gene products activate a new family of sensory neuron-specific GPCRs. Nature Neuroscience 2002, 5:201-209.
59. Lister R.G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl) 1987, 92:180-185.
60. Liu D., Gao L., Roy S.K., Cornish K.G., Zucker I.H. Neuronal Angiotensin II type 1 receptor upregulation in heart failure: Activation of activator protein 1 and Jun N-terminal kinase. Circulation Research 2006, 99:1004-1011.
61. Macova M., Pavel J., Saavedra J.M. A peripherally administered, centrally acting Angiotensin II AT2 antagonist selectively increases brain AT1 receptors and decreases brain tyrosine hydroxylase transcription, pituitary vasopressin and ACTH. Brain Research 2009, 1250:130-140.
62. Martin K.A., Grant S.G., Hockfield S. The mas proto-oncogene is developmentally regulated in the rat central nervous system. Brain Research. Developmental Brain Research 1992, 68:75-82.
63. McEwen B.S., Sapolsky R.M. Stress and cognitive function. Current Opinion in Neurobiology 1995, 5:205-216.
64. Metz G.A., Schwab M.E. Behavioral characterization in a comprehensive mouse test battery reveals motor and sensory impairments in growth-associated protein-43 mutant mice. Neuroscience 2004, 129:574-583.
65. Metzger R., Bader M., Ludwig T., Berberich C., Bunnemann B., Ganten D. Expression of the mouse and rat mas proto-oncogene in the brain and peripheral tissues. FEBS Letters 1995, 357:27-32.
66. Morilak D.A., Barrera G., Echevarria D.J., Garcia A.S., Hernandez A., Ma S., et al. Role of brain norepinephrine in the behavioral response to stress. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2005, 29:1214-1224.
67. Myskiw J.C., Rossato J.I., Bevilaqua L.R., Medina J.H., Izquierdo I., Cammarota M. On the participation of mTOR in recognition memory. Neurobiology of Learning and Memory 2008, 89:338-351.
68. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 1997, Academic Press, San Diego. 2nd ed.
69. Pereira G.S., Rossato J.I., Sarkis J.J., Cammarota M., Bonan C.D., Izquierdo I. Activation of adenosine receptors in the posterior cingulate cortex impairs memory retrieval in the rat. Neurobiology of Learning and Memory 2005, 83:217-223.
70. Polidori C., Ciccocioppo R., Pompei P., Cirillo R., Massi M. Functional evidence for the ability of Angiotensin AT1 receptor antagonists to cross the blood-brain barrier in rats. European Journal of Pharmacology 1996, 307:259-267.
71. Prado V.F., Martins-Silva C., de Castro B.M., Lima R.F., Barros D.M., Amaral E., et al. Mice deficient for the vesicular acetylcholine transporter are myasthenic and have deficits in object and social recognition. Neuron 2006, 51:601-612.
72. Pych J.C., Kim M., Gold P.E. Effects of injections of glucose into the dorsal striatum on learning of place and response mazes. Behavioural Brain Research 2006, 167:373-378.
73. Raghavendra V., Chopra K., Kulkarni S.K. Comparative studies on the memory-enhancing actions of captopril and losartan in mice using inhibitory shock avoidance paradigm. Neuropeptides 2001, 35:65-69.
74. Roozendaal B., Okuda S., de Quervain D.J., McGaugh J.L. Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 2006, 138:901-910.
75. Rosario E.R., Ramsden M., Pike C.J. Progestins inhibit the neuroprotective effects of estrogen in rat hippocampus. Brain Research 2006, 1099:206-210.
76. Rossato J.I., Bevilaqua L.R., Lima R.H., Medina J.H., Izquierdo I., Cammarota M. On the participation of hippocampal p38 mitogen-activated protein kinase in extinction and reacquisition of inhibitory avoidance memory. Neuroscience 2006, 143:15-23.
77. Rossato J.I., Bevilaqua L.R., Myskiw J.C., Medina J.H., Izquierdo I., Cammarota M. On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory. Learning Memory 2007, 14:36-46.
78. Rowe B.P., Saylor D.L., Speth R.C., Absher D.R. Angiotensin-(1-7) binding at Angiotensin II receptors in the rat brain. Regulatory Peptides 1995, 56:139-146.
79. Sampaio W.O., Henrique de Castro C., Santos R.A., Schiffrin E.L., Touyz R.M. Angiotensin-(1-7) counterregulates Angiotensin II signaling in human endothelial cells. Hypertension 2007, 50:1093-1098.
80. Sango K., McDonald M.P., Crawley J.N., Mack M.L., Tifft C.J., Skop E., et al. Mice lacking both subunits of lysosomal beta-hexosaminidase display gangliosidosis and mucopolysaccharidosis. Nature Genetics 1996, 14:348-352.
81. Santos R.A., Campagnole-Santos M.J., Baracho N.C., Fontes M.A., Silva L.C., Neves L.A., et al. Characterization of a new Angiotensin antagonist selective for Angiotensin-(1-7): Evidence that the actions of Angiotensin-(1-7) are mediated by specific Angiotensin receptors. Brain Research Bulletin 1994, 35:293-298.
82. Santos R.A., Simoes e Silva A.C., Maric C., Silva D.M., Machado R.P., de Buhr I., et al. Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:8258-8263.
83. Schelman W.R., Andres R., Ferguson P., Orr B., Kang E., Weyhenmeyer J.A. Angiotensin II attenuates NMDA receptor-mediated neuronal cell death and prevents the associated reduction in Bcl-2 expression. Brain Research. Molecular Brain Research 2004, 128:20-29.
84. Schelman W.R., Kurth J.L., Berdeaux R.L., Norby S.W., Weyhenmeyer J.A. Angiotensin II type-2 (AT2) receptor-mediated inhibition of NMDA receptor signalling in neuronal cells. Brain Research. Molecular Brain Research 1997, 48:197-205.
85. Sirett N.E., Bray J.J., Hubbard J.I. Localization of immunoreactive Angiotensin II in the hippocampus and striatum of rat brain. Brain Research 1981, 217:405-411.
86. Strawn W.B., Ferrario C.M., Tallant E.A. Angiotensin-(1-7) reduces smooth muscle growth after vascular injury. Hypertension 1999, 33:207-211.
87. Sumners C., Fleegal M.A., Mingyan Z. Angiotensin AT1 receptor signalling pathways in neurons. Clinical and Experimental Pharmacology and Physiology 2002, 29:483-490.
88. Tallant E.A., Ferrario C.M., Gallagher P.E. Angiotensin-(1-7) inhibits growth of cardiac myocytes through activation of the mas receptor. American Journal of Physiology - Heart and Circulatory Physiology 2005, 289:H1560-H1566.
89. Tota S., Kamat P.K., Awasthi H., Singh N., Raghubir R., Nath C., et al. Candesartan improves memory decline in mice: Involvement of AT1 receptors in memory deficit induced by intracerebral streptozotocin. Behavioural Brain Research 2009, 199:235-240.
90. Voikar V., Polus A., Vasar E., Rauvala H. Long-term individual housing in C57BL/6J and DBA/2 mice: Assessment of behavioral consequences. Genes, Brain and Behaviour 2005, 4:240-252.
91. 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, 19:1031-1036.
92. von Bohlen und Halbach O., Albrecht D. The CNS renin-Angiotensin system. Cell and Tissue Research 2006, 326:599-616.
93. Von Bohlen und Halbach O., Walther T., Bader M., Albrecht D. Interaction between Mas and the Angiotensin AT1 receptor in the amygdala. Journal of Neurophysiology 2000, 83:2012-2021.
94. Walther T., Balschun D., Voigt J.P., Fink H., Zuschratter W., Birchmeier C., et al. Sustained long term potentiation and anxiety in mice lacking the Mas protooncogene. Journal of Biological Chemistry 1998, 273:11867-11873.
95. Wang J.M., Tan J., Leenen F.H. Central nervous system blockade by peripheral administration of AT1 receptor blockers. Journal of Cardiovascular Pharmacology 2003, 41:593-599.
96. Wayner M.J., Polan-Curtain J., Armstrong D.L. Dose and time dependency of Angiotensin II inhibition of hippocampal long-term potentiation. Peptides 1995, 16:1079-1082.
97. Winters B.D., Forwood S.E., Cowell R.A., Saksida L.M., Bussey T.J. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: Heterogeneity of function within the temporal lobe. Journal of Neuroscience 2004, 24:5901-5908.
98. Xia H., Lazartigues E. Angiotensin-converting enzyme 2 in the brain: properties and future directions. Journal of Neurochemistry 2008, 107:1482-1494.
99. Yang H., Raizada M.K. Role of phosphatidylinositol 3-kinase in Angiotensin II regulation of norepinephrine neuromodulation in brain neurons of the spontaneously hypertensive rat. Journal of Neuroscience 1999, 19:2413-2423.
100. Yang R.F., Yin J.X., Li Y.L., Zimmerman M.C., Schultz H.D. Angiotensin-(1-7) increases neuronal potassium current via a nitric oxide-dependent mechanism. American Journal of Physiology - Heart and Circulatory Physiology 2011, 300:C58-C64.
101. Young D., O'Neill K., Jessell T., Wigler M. Characterization of the rat mas oncogene and its high-level expression in the hippocampus and cerebral cortex of rat brain. Proceedings of the National Academy of Sciences of the United States of America 1988, 85:5339-5342.
102. Zhou L., Shi Z., Gao J., Han Y., Yuan N., Gao X., et al. Angiotensin-(1-7) and angiotension II in the rostral ventrolateral medulla modulate the cardiac sympathetic afferent reflex and sympathetic activity in rats. Pflügers Archiv - European Journal of Physiology 2010, 459:681-688.