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Cognitive Effects Attributed to Angiotensin II may Result from its Conversion to Angiotensin IV
Jan Jozef Braszko
Department of Clinical Pharmacology, Medical University of Bialystok, J. Waszyngtona 15A, Bialystok 15274, Poland, braszko{at}amb.edu.pl
Anna Walesiuk
Department of Clinical Pharmacology, Medical University of Bialystok, J. Waszyngtona 15A, Bialystok 15274, Poland
Przemyslaw Wielgat
Department of Clinical Pharmacology, Medical University of Bialystok, J. Waszyngtona 15A, Bialystok 15274, Poland
This study tests the hypothesis that the facilitation of learning and improvement of memory observed after an intracerebroventricular (i.c.v.) injection of angiotensin II (Ang II) is, in fact, caused by its derivative angiotensin IV (Ang IV). We ran two memory tests as well as an auxiliary test assessing motor performance in rats injected (i.c.v., 1 nmol in 2 µl saline) with Ang II or Ang IV. There were separate groups receiving peptide or saline five, 10 and 15 minutes before testing. Ang IV significantly increased step-through latencies in a passive avoidance paradigm as well as improved discrimination between familiar and unfamiliar objects in an object recognition test in all groups showing better retrieval of memory of aversive as well as appetitive stimuli in the peptide-treated groups regardless of the time of its injection. In contrast, rats treated with Ang II demonstrated significant improvement of memory of aversive and appetitive stimuli in the same tests only 15 minutes after its i.c.v. injection, with no effect in the groups injected five minutes before testing and slight efficacy in those injected 10 minutes before the test. Numbers of crossings, rearings and bar approaches in an `open' field were similar both in the peptide-treated and control groups making it unlikely that changes in motor performance affected the memory tests. In line with the present views on the intracellular metabolism of Ang II, these results suggest degradation to Ang IV by aminopeptidases A and N is necessary before the cognitive effects can occur.
Key Words: Angiotensins Memory Behaviour Rat
References
- Wright JW, Krebs LT, Stobb JW, Harding JW The angiotensin IV system: functional implications. Front Neuroendocrinol 1995;16:23-52.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Fitzsimons JT Angiotensin, thirst, and sodium appetite. Physiol Rev 1998;78:583-686.[Abstract/Free Full Text]
- Saavedra JM Brain and pituitary angiotensin. Endocr Rev 1992;13:329-80.[Abstract/Free Full Text]
- Baranowska D., Braszko JJ, Wisniewski K. Effect of angiotensin II and vasopressin on acquisition and extinction of conditioned avoidance in rats. Psychopharmacology 1983;81:247-51.[CrossRef][Medline]
[Order article via Infotrieve]
- Braszko JJ AT2 but not AT1 receptor antagonism abolishes angiotensin II increase of the acquisition of conditioned avoidance responses in rats. Behav Brain Res 2002;131:79-86.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Braszko JJ Involvement of D1 dopamine receptors in the cognitive effects of angiotensin IV and des-Phe6 angiotensin IV. Peptides 2004;25:1195-203.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Braszko JJ Valsartan abolishes most of the memory-improving effects of intracerebroventricular angiotensin II in rats. Clin Exp Hypertens 2005;27:635-49.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Braszko JJ, Wisniewski K. Effect of angiotensin II and saralasin on motor activity and the passive avoidance behavior of rats. Peptides 1988;9:475-9.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Braszko JJ, Wisniewski K., Kupryszewski G., Witczuk B. Psychotropic effects of angiotensin II and III in rats: locomotor and exploratory vs. cognitive behaviour. Behav Brain Res 1987;25:195-203.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Braszko JJ, Kupryszewski G., Witczuk B., Wisniewski K. AngiotensinII-(3-8)-hexapeptide affects motor activity, performance of passive avoidance and a conditioned avoidance response in rats. Neuroscience 1988;27:777-83.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Braszko JJ, Wlasienko J., Kupryszewski G., Witczuk B., Wisniewski K. Behavioral effects of angiotensin II and angiotensin II-(4-8)-pentapeptide in rats. Physiol Behav 1988;44:327-32.[CrossRef][Medline]
[Order article via Infotrieve]
- Braszko JJ, Wlasienko J., Koziolkiewicz W., Janecka A., Wisniewski K. The 3-7 fragment of angiotensin II is probably responsible for its psychoactive properties. Brain Res 1991;542:49-54.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Georgiev VP, Yonkov D. Participation of angiotensin II in learning and memory. I. Interaction of angiotensin II with saralasin. Methods Find Exp Clin Pharmacol 1985;7:415-18.[Web of Science][Medline]
[Order article via Infotrieve]
- de Souza FAM, Sanchis-Segura C., Fukada SY, de Bortoli VCZangrossi, H. Jr, de Oliveira AM Intracerebroventricular effects of angiotensin II on a step-through passive avoidance task in rats. Neurobiol Learn Mem 2004;81:100-03.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Winnicka MM Dopaminergic projection to the nucleus accumbens mediates the memory-enhancing effect of angiotensins in rats. Pharmacol Biochem Behav 1999;62:625-30.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Yonkov DI, Georgiev VP, Opitz MJ Participation of angiotensin II in learning and memory. II. Interactions of angiotensin II with dopaminergic drugs. Methods Find Exp Clin Pharmacol 1986;8:203-06.[Web of Science][Medline]
[Order article via Infotrieve]
- Yonkov DI, Georgiev VP, Kamburova T., Opitz M. Participation of angiotensin II in learning and memory. III. Interactions of angiotensin II with GABAergic drugs. Methods Find Exp Clin Pharmacol 1987;9:205-08.[Web of Science][Medline]
[Order article via Infotrieve]
- Wright JW, Miller-Wing AV, Shaffer MJ et al. Angiotensin II(3-8) (ANG IV) hippocampal binding: potential role in the facilitation of memory. Brain Res Bull 1993;32:497-502.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Hunyady L.G·borik Z.,, Shah BH, Jagadeesh G., Clark AJL, Catt KJ Structural determinants of agonist-induced signalling and regulation of the angiotensin AT1 receptor. Mol Cell Endocrinol 2004;217:89-100.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Wei H., Ahn S., Barnes WG, Lefkowitz RJ Stable interaction between -arrestin 2 and angiotensin type 1A receptor is required for -arrestin 2-mediated activation of extracellular signal-regulated kinases 1 and 2. J Biol Chem 2004;279:48255-61.[Abstract/Free Full Text]
- Cook JL, Re R., Alam J., Hart M., Zhang Z. Intracellular angiotensin II fusion protein alters AT1 receptor fusion protein distribution and activates CREB. J Mol Cell Cardiol 2004;36:75-90.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- G·borik Z., Szasz·k M., Szidonya L. et al. β-arrestin- and dynamin-dependent endocytosis of the AT1 angiotensin receptor. Mol Pharmacol 2001;59:239-47.[Abstract/Free Full Text]
- G·borik Z., Jagadeesh G., Zhang M., Spät A., Catt KJ, Hunyady L. The role of a conserved region of the second intracellular loop in AT1 angiotensin receptor activation and signalling. Endocrinology 2003;144:2220-8.[Abstract/Free Full Text]
- Szasz·k M., G·borik Z., Turu G. et al. Role of the prolinerich domain of dynamin-2 and its interactions with Src homology 3 domains during endocytosis of the AT1 angiotensin receptor. J Biol Chem 2002;277:21650-6.[Abstract/Free Full Text]
- Dale LB, Seachrist JL, Banwah AV, Ferguson SSG. Regulation of angiotensin II type 1 A receptor intracellular retention, degradation, and recycling by Rab5, Rab7, and Rab11 GTPases. J Biol Chem 2004;279:13110-18.[Abstract/Free Full Text]
- Wang JM, Llona I., de Potter WP Receptor-mediated internalization of angiotensin II in bovine adrenal medullary chromaffin cells in primary culture. Regul Pept 1994;53:77-86.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Wang JM, Baudhuin P., Courtoy PJ, de Potter WP Conversion of angiotensin II into active fragments by an endosomal pathway in bovine adrenal medullary cells in primary culture. Endocrinology 1995;136:5274-82.[Abstract]
- McKinley MJ, Albiston AL, Allen AM et al. The brain renin-angiotensin system: location and physiological roles. Int J Biochem Cell Biol 2003;35:901-18.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Chai SY, Fernando R., Peck G. et al. The angiotensin IV/AT4 receptor. Cell Mol Life Sci 2004;61:2728-37.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Wayner MJ, Armstrong DL, Phelix CF, Wright JW, Harding JW Angiotensin IV enhances LTP in rat dentate gyrus in vivo. Peptides 2001;22:1403-14.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Wayner MJ, Polan-Curtain JL, Armstrong DL Dose and time dependency of angiotensin II inhibition of hippocampal long-term potentiation. Peptides 1995;16:1079-82.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- 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;19:1031-6.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Wright JW, Harding JW Important roles for angiotensin III and IV in the brain renin-angiotensin system. Brain Res Rev 1997;25:96-124.[CrossRef][Medline]
[Order article via Infotrieve]
- Pederson ES, Harding JW, Wright JW Attenuation of scopolamine-induced spatial learning impairments by an angiotensin IV analog. Regul Pept 1998;74:97-103.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Stragier B., Sarre S., Vanderheyden P. et al. Metabolism of angiotensin II is required for its in vivo effect on dopamine release in the striatum of the rat. J Neurochem 2004;90:1251-7.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Mendelsohn FA, Jenkins TA, Berkovic SF Effects of angiotensin II on dopamine and serotonin turnover in the striatum in conscious rats. Brain Res 1993;613:221-9.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Cools R. Dopaminergic modulation of cognitive function-implications for L-DOPA treatment in Parkinson's disease. Neurosci Biobehav Rev 2005 (Epub ahead of print).
- Denenberg VH, Kim DS, Palmiter RD The role of dopamine in learning, memory, and performance of a water escape task. Behav Brain Res 2004;148:73-8.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Harley CW Norepinephrine and dopamine as learning signals. Neural Plast 2004;11:191-204.[CrossRef][Medline]
[Order article via Infotrieve]
- Jay TM Dopamine: a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol 2003;69:375-90.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Pezze MA, Feldon J. Mesolimbic dopaminergic pathways in fear conditioning. Prog Neurobiol 2004;74:301-20.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Ader R., Weijnen Jawm, Moleman P. Retention of a passive avoidance responses as a function of the intensity and duration of electric shock. Psychon Sci 1972;26:125-9.[Web of Science]
- Ennaceur A., Meliani K. A new one-trial test for neurobiological studies of memory in rats. III. Spatial vs nonspatial working memory. Behav Brain Res 1992;51:83-92.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Wright JW, Harding JW Regulatory role of brain angiotensins in the control of physiological and behavioral responses. Brain Res Rev 1992;17:227-62.[CrossRef][Medline]
[Order article via Infotrieve]
- Wayner MJ, Armstrong DL, Phelix CF, Wright JW, Harding JW Angiotensin IV enhances LTP in rat dentate gyrus in vivo. Peptides 2001;22:1403-14.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Albiston AL, McDowall SG, Matsacos D. et al. Evidence that the angiotensin IV (AT(4)) receptor is the enzyme insulin-regulated aminopeptidase. J Biol Chem 2001;28:48623-6.
- Campbell DJ The renin-angiotensin and the kallikreinkinin systems. Int J Biochem Cell Biol 2003;35:784-91.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Stragier B., Hristova I., Sarre S., Ebinger G., Michotte Y. In vivo characterization of the angiotensin-(1-7)-induced dopamine and
-aminobutyric acid release in the striatum of the rat. Eur J Neurosci 2005;22:658-64.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve] - Tonnaer JA, Engels GM, Wiegant VM, Burbach JP, De Jong W., De Wied D. Proteolytic conversion of angiotensins in rat brain tissue. Eur J Biochem 1983;15:415-21.
- Ward PE, Bausback HH, Odya CE Kinin and angiotensin metabolism by purified renal post-proline cleaving enzyme. Biochem Pharmacol 1987;1:3187-93.
- Welches WR, Brosnihan KB, Ferrario CM A comparison of the properties and enzymatic activities of three angiotensin processing enzymes: angiotensin converting enzyme, prolyl endopeptidase and neutral endopeptidase 24.11. Life Sci 1993;52:1461-80.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Duncan AM, James GM, Anastasopoulos F., Kladis A., Briscoe TA, Campbell DJ Interaction between neutral endopeptidase and angiotensin converting enzyme inhibition in rats with myocardial infarction: effects on cardiac hypertrophy and angiotensin and bradykinin peptide levels. J Pharmacol Exp Ther 1999;289:295-303.[Abstract/Free Full Text]
- Marin J., Govantes C. Angiotensin-converting enzyme inhibitors and the role of nitric oxide and excitatory amino acids in improvement of cognition and memory. J Auton Pharmacol 1995;15:129-49.[Web of Science][Medline]
[Order article via Infotrieve]
- Braszko JJ, Karwowska-Polecka W., Halicka D., Gard PR Captopril and enalapril improve cognition and depressed mood in hypertensive patients. J Basic Clin Physiol Pharmacol 2003;14:323-43.[Medline]
[Order article via Infotrieve]
- Barnes JM, Barnes NM, Costall B. et al. Angiotensin-converting enzyme inhibition, angiotensin, and cognition. J Cardiovasc Pharmacol 1992;19:563-71.
- Jenkins TA, Chai SY Effect of angiotensin converting enzyme inhibitors on memory. http://fens2006.neurosciences.asso.fr/abstracts/R7/A233_18.html
- Koeller M., Krause HP, Hoffmeister F., Ganten D. Endogenous brain angiotensin II disrupts passive avoidance behavior in rats. Neurosci Lett 1979;14:71-5.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- DeNoble VJ, DeNoble KF, Spencer KR, Chiu AT, Wong PC, Timmermans PB Non-peptide angiotensin II receptor antagonist and angiotensin-converting enzyme inhibitor: effect on a renin-induced deficit of a passive avoidance response in rats. Brain Res 1991;11:230-5.
- Morgan JM, Routtenberg A. Angiotensin injected into the neostriatum after learning disrupts retention performance. Science 1977;1:87-9.
- Kerr DS, Bevilaqua LR, Bonini JS et al. Angiotensin II blocks memory consolidation through an AT2 receptor-dependent mechanism. Psychopharmacology 2005;179:529-35.[CrossRef][Medline]
[Order article via Infotrieve]
Journal of Renin-Angiotensin-Aldosterone System, Vol. 7, No. 3,
168-174 (2006)
DOI: 10.3317/jraas.2006.027

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