Involvement of the AT1 receptor subtype in the effects of angiotensin IV and LVV-haemorphin 7 on hippocampal neurotransmitter levels and spatial working memory

Journal of Neurochemistry

Volumn 112, Issue 5, 2010, Pages 1223-1234

  De Bundel, Dimitri ^a   Demaegdt, Heidi ^a   Lahoutte, Tony ^a   Caveliers, Vicky ^a   Kersemans, Ken ^a   Ceulemans, Ann Gaelle ^a   Vauquelin, Georges ^a   Clinckers, Ralph ^a   Vanderheyden, Patrick ^a   Michotte, Yvette ^a   Smolders, Ilse ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

Angiotensin IV; AT1 receptor; AT4 receptor; IRAP; LVV haemorphin 7; Spatial working memory

Indexed keywords

ACETYLCHOLINE; AMINOPEPTIDASE; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II [3-8]; INSULIN REGULATED AMINOPEPTIDASE; LEUCYLVALYLVALYLHEMORPHIN 7; NEUROPEPTIDE; NEUROTRANSMITTER; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ANGIOTENSIN II; ANGIOTENSIN II, DES ASP(1) DES ARG(2) ILE(5); ANGIOTENSIN II, DES-ASP(1)-DES-ARG(2)-ILE(5)-; DRUG DERIVATIVE; HEMOGLOBIN; IODINE; LVV HEMORPHIN 7; LVV-HEMORPHIN-7; PEPTIDE FRAGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BRAIN LEVEL; COGNITION; CONTROLLED STUDY; DRUG BINDING SITE; DRUG EFFECT; DRUG RECEPTOR BINDING; FEMALE; HIPPOCAMPUS; MALE; MAZE TEST; MICRODIALYSIS; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR INTRINSIC ACTIVITY; SPATIAL MEMORY; TASK PERFORMANCE; WORKING MEMORY; ANIMAL; DEPTH PERCEPTION; DOSE RESPONSE; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; METHODOLOGY; PHYSIOLOGY; PROTEIN BINDING; SCINTISCANNING; SHORT TERM MEMORY; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TISSUE DISTRIBUTION; WISTAR RAT;

RATTUS;

ANGIOTENSIN II; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; HEMOGLOBINS; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; IODINE ISOTOPES; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MICRODIALYSIS; NEUROTRANSMITTER AGENTS; PEPTIDE FRAGMENTS; PROTEIN BINDING; RATS; RATS, WISTAR; RECEPTOR, ANGIOTENSIN, TYPE 1; SPACE PERCEPTION; TISSUE DISTRIBUTION; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON;

EID: 75949128384     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06547.x     Document Type: Article

References (75)

1. Albiston A. L., McDowall S. G., Matsacos D. et al. (2001) Evidence that the angiotensin IV (AT(4)) receptor is the enzyme insulin-regulated aminopeptidase. J. Biol. Chem. 276, 48623 48626.
2. Albiston A. L., Pederson E. S., Burns P., Purcell B., Wright J. W., Harding J. W., Mendelsohn F. A., Weisinger R. S. Chai S. Y. (2004) Attenuation of scopolamine-induced learning deficits by LVV-hemorphin-7 in rats in the passive avoidance and water maze paradigms. Behav. Brain Res. 154, 239 243.
3. Albiston A. L., Morton C. J., Ng H. L. et al. (2008) Identification and characterization of a new cognitive enhancer based on inhibition of insulin-regulated aminopeptidase. FASEB J. 22, 4209 4217.
4. Ambrogi Lorenzini C. G., Baldi E., Bucherelli C., Sacchetti B. Tassoni G. (1999) Neural topography and chronology of memory consolidation: a review of functional inactivation findings. Neurobiol. Learn. Mem. 71, 1 18.
5. Benveniste H. (1989) Brain microdialysis. J. Neurochem. 52, 1667 1679.
6. Braszko J. J. (2004) Involvement of D1 dopamine receptors in the cognitive effects of angiotensin IV and des-Phe6 angiotensin IV. Peptides 25, 1195 1203.
7. Braszko J. J. (2005) Valsartan abolishes most of the memory-improving effects of intracerebroventricular angiotensin II in rats. Clin. Exp. Hypertens. 27, 635 649.
8. Braszko J. J., Kupryszewski G., Witczuk B. Wisniewski K. (1988) Angiotensin II-(3-8)-hexapeptide affects motor activity, performance of passive avoidance and a conditioned avoidance response in rats. Neuroscience 27, 777 783.
9. Braszko J. J., Walesiuk A. Wielgat P. (2006) Cognitive effects attributed to angiotensin II may result from its conversion to angiotensin IV. J. Renin Angiotensin Aldosterone Syst. 7, 168 174.
10. Braszko J. J., Wielgat P. Walesiuk A. 2008) Effect of D(3) dopamine receptors blockade on the cognitive effects of angiotensin IV in rats. Neuropeptides 42, 301 309.
11. Burgess N., Maguire E. A. O'Keefe J. (2002) The human hippocampus and spatial and episodic memory. Neuron 35, 625 641. (Pubitemid 35223024)
12. Chai S. Y., Bastias M. A., Clune E. F., Matsacos D. J., Mustafa T., Lee J. H., McDowall S. G., Paxinos G., Mendelsohn F. A. Albiston A. L. (2000) Distribution of angiotensin IV binding sites (AT4 receptor) in the human forebrain, midbrain and pons as visualised by in vitro receptor autoradiography. J. Chem. Neuroanat. 20, 339 348.
13. De Bundel D., Smolders I., Vanderheyden P. Michotte Y. (2008) Ang II and Ang IV: unraveling the mechanism of action on synaptic plasticity, memory, and epilepsy. CNS Neurosci. Ther. 14, 315 339.
14. De Bundel D., Smolders I., Yang R., Albiston A. L., Michotte Y. Chai S. Y. (2009) Angiotensin IV and LVV-Haemorphin 7 enhance spatial working memory in rats: effects on hippocampal glucose levels and blood flow. Neurobiol. Learn. Mem. 92, 19 26.
15. Demaegdt H., Laeremans H., De Backer J. P., Mosselmans S., Le M. T., Kersemans V., Michotte Y., Vauquelin G. Vanderheyden P. M. (2004a) Synergistic modulation of cystinyl aminopeptidase by divalent cation chelators. Biochem. Pharmacol. 68, 893 900.
16. Demaegdt H., Vanderheyden P., De Backer J. P., Mosselmans S., Laeremans H., Le M. T., Kersemans V., Michotte Y. Vauquelin G. (2004b) Endogenous cystinyl aminopeptidase in Chinese hamster ovary cells: characterization by [125I]Ang IV binding and catalytic activity. Biochem. Pharmacol. 68, 885 892.
17. Ellis J., Warburton P., Donnelly D. Balmforth A. J. (2006) Conformational induction is the key process for activation of the AT1 receptor. Biochem. Pharmacol. 71, 464 471.
18. Faure S., Oudart N., Javellaud J., Fournier A., Warnock D. G. Achard J. M. (2006) Synergistic protective effects of erythropoietin and olmesartan on ischemic stroke survival and post-stroke memory dysfunctions in the gerbil. J. Hypertens. 24, 2255 2261.
19. Fitzsimons J. T. 1998) Angiotensin, thirst, and sodium appetite. Physiol. Rev. 78 (3 583 686. Review.
20. Fogari R., Mugellini A., Zoppi A., Derosa G., Pasotti C., Fogari E. Preti P. (2003) Influence of losartan and atenolol on memory function in very elderly hypertensive patients. J. Hum. Hypertens. 17, 781 785.
21. Fogari R., Mugellini A., Zoppi A., Marasi G., Pasotti C., Poletti L., Rinaldi A. Preti P. (2004) Effects of valsartan compared with enalapril on blood pressure and cognitive function in elderly patients with essential hypertension. Eur. J. Clin. Pharmacol. 59, 863 868.
22. Fogari R., Mugellini A., Zoppi A., Lazzari P., Destro M., Rinaldi A. Preti P. (2006) Effect of telmisartan/hydrochlorothiazide vs lisinopril/hydrochlorothiazide combination on ambulatory blood pressure and cognitive function in elderly hypertensive patients. J. Hum. Hypertens. 20, 177 185.
23. de Gasparo M., Catt K. J., Inagami T., Wright J. W. Unger T. (2000) International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol. Rev. 52, 415 472.
24. Georgieva J., Luthman J., Mohringe B. Magnusson O. (1993) Tissue and microdialysate changes after repeated and permanent probe implantation in the striatum of freely moving rats. Brain Res. Bull. 31, 463 470.
25. Gohlke P., Von Kugelgen S., Jurgensen T., Kox T., Rascher W., Culman J. Unger T. (2002) Effects of orally applied candesartan cilexetil on central responses to angiotensin II in conscious rats. J. Hypertens. 20, 909 918. (Pubitemid 34913672)
26. Hasselmo M. E. (2006) The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16, 710 715.
27. Klotz U., Antonin K. H. Bieck P. R. (1976) Pharmacokinetics and plasma binding of diazepam in man, dog, rabbit, guinea pig and rat. J. Pharmacol. Exp. Ther. 199, 67 73.
28. Kulakowska A., Karwowska W., Wisniewski K. Braszko J. J. (1996) Losartan influences behavioural effects of angiotensin II in rats. Pharmacol. Res. 34, 109 115.
29. Laeremans H., Demaegdt H., De Backer J.-P., Le M. T., Kersemans V., Michotte Y., Vauquelin G. Vanderheyden P. M. L. (2005) Metal ion modulation of cystinyl aminopeptidase. Biochem. J. 390, 352 357.
30. Lalonde R. (2002) The neurobiological basis of spontaneous alternation. Neurosci. Biobehav. Rev. 26, 91 104.
31. Lanckmans K., Stragier B., Sarre S., Smolders I. Michotte Y. (2007) Nano-LC-MS/MS for the monitoring of angiotensin IV in rat brain microdialysates: limitations and possibilities. J. Sep. Sci. 30, 2217 2224.
32. Le M. T., Vanderheyden P. M., Szaszak M., Hunyady L. Vauquelin G. (2002) Angiotensin IV is a potent agonist for constitutive active human AT1 receptors. Distinct roles of the N-and C-terminal residues of angiotensin II during AT1 receptor activation. J. Biol. Chem. 277, 23107 23110.
33. Lee J., Chai S. Y., Mendelsohn F. A., Morris M. J. Allen A. M. (2001) Potentiation of cholinergic transmission in the rat hippocampus by angiotensin IV and LVV-hemorphin-7. Neuropharmacology 40, 618 623.
34. Lee J., Albiston A. L., Allen A. M., Mendelsohn F. A., Ping S. E., Barrett G. L., Murphy M., Morris M. J., McDowall S. G. Chai S. Y. (2004) Effect of I.C.V. injection of AT(4) receptor ligands, NLE(1)-angiotensin IV and LVV-hemorphin 7, on spatial learning in rats. Neuroscience 124, 341 349.
35. Lenkei Z., Palkovits M., Corvol P. Llorens-Cortes C. (1996) Distribution of angiotensin II type-2 receptor (AT2) mRNA expression in the adult rat brain. J. Comp. Neurol. 373, 322 339.
36. Lennartz R. C. (2008) The role of extramaze cues in spontaneous alternation in a plus-maze. Learn. Behav. 36, 138 144.
37. Lew R. A., Mustafa T., Ye S., McDowall S. G., Chai S. Y. Albiston A. L. (2003) Angiotensin AT4 ligands are potent, competitive inhibitors of insulin regulated aminopeptidase (IRAP). J. Neurochem. 86, 344 350.
38. Lochard N., Thibault G., Silversides D. W., Touyz R. M. Reudelhuber T. L. (2004) Chronic production of angiotensin IV in the brain leads to hypertension that is reversible with an angiotensin II AT1 receptor antagonist. Circ. Res. 94, 1451 1457.
39. Loening A. M. Gambhir S. S. (2003) AMIDE: a free software tool for multimodality medical image analysis. Mol. Imaging 2, 131 137.
40. Martial F. P., Thornton S. N., Lienard F., Mousseau M. C. Nicolaidis S. (1994) Tonic neuronal inhibition by AII revealed by iontophoretic application of Losartan, a specific antagonist of AII type-1 receptors. Brain Res. Bull. 34 (6 533 539.
41. McKinley M. J., Badoer E., Vivas L. Oldfield B. J. (1995) Comparison of c-fos expression in the lamina terminalis of conscious rats after intravenous or intracerebroventricular angiotensin. Brain Res. Bull. 37 (2 131 137.
42. Meek J. L. Neff N. H. (1973) Is cerebrospinal fluid the major avenue for the removal of 5-hydroxyindoleacetic acid from the brain? Neuropharmacology 12, 497 499.
43. Moeller I., Paxinos G., Mendelsohn F. A., Aldred G. P., Casley D. Chai S. Y. (1996) Distribution of AT4 receptors in the Macaca fascicularis brain. Brain Res. 712, 307 324.
44. Moeller I., Lew R. A., Mendelsohn F. A., Smith A. I., Brennan M. E., Tetaz T. J. Chai S. Y. (1997) The globin fragment LVV-hemorphin-7 is an endogenous ligand for the AT4 receptor in the brain. J. Neurochem. 68, 2530 2537.
45. Moser E., Moser M. B. Andersen P. (1993) Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J. Neurosci. 13, 3916 3925.
46. Myhrer T. (2003) Neurotransmitter systems involved in learning and memory in the rat: a meta-analysis based on studies of four behavioral tasks. Brain Res. Brain Res. Rev. 41, 268 287.
47. O'Keefe J. (1983) Two spatial systems in the rat brain - implications for the neural basis of learning and memory. Prog. Brain Res. 58, 453 464.
48. Olson M. L., Olson E. A., Qualls J. H., Stratton J. J., Harding J. W. Wright J. W. (2004) Norleucine1-angiotensin IV alleviates mecamylamine-induced spatial memory deficits. Peptides 25, 233 241.
49. Pederson E. S., Harding J. W. Wright J. W. (1998) Attenuation of scopolamine-induced spatial learning impairments by an angiotensin IV analog. Regul. Pept. 74, 97 103.
50. Pederson E. S., Krishnan R., Harding J. W. Wright J. W. (2001) A role for the angiotensin AT4 receptor subtype in overcoming scopolamine-induced spatial memory deficits. Regul. Pept. 102, 147 156.
51. Pych J. C., Chang Q., Colon-Rivera C. Gold P. E. (2005) Acetylcholine release in hippocampus and striatum during testing on a rewarded spontaneous alternation task. Neurobiol. Learn. Mem. 84, 93 101.
52. Raghavendra V., Chopra K. Kulkarni S. K. (1998) Involvement of cholinergic system in losartan-induced facilitation of spatial and short-term working memory. Neuropeptides 32, 417 421.
53. Ragozzino M. E., Unick K. E. Gold P. E. (1996) Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. Proc. Natl. Acad. Sci. U S A 93, 4693 4698.
54. Rogers J. L. Kesner R. P. (2003) Cholinergic modulation of the hippocampus during encoding and retrieval. Neurobiol. Learn. Mem. 80, 332 342.
55. Saavedra J. M. (2005) Brain angiotensin II: new developments, unanswered questions and therapeutic opportunities. Cell. Mol. Neurobiol. 25, 485 512.
56. Saxby B. K., Harrington F., Wesnes K. A., McKeith I. G. Ford G. A. (2008) Candesartan and cognitive decline in older patients with hypertension: a substudy of the SCOPE trial. Neurology 70, 1858 1866.
57. Smolders I., Clinckers R., Meurs A., De Bundel D., Portelli J., Ebinger G. Michotte Y. (2008) Direct enhancement of hippocampal dopamine or serotonin levels as a pharmacodynamic measure of combined antidepressant-anticonvulsant action. Neuropharmacology 54, 1017 1028.
58. Srinivasan J., Jayadev S., Kumaran D., Ahamed K. F., Suresh B. Ramanathan M. (2005) Effect of losartan and enalapril on cognitive deficit caused by Goldblatt induced hypertension. Indian J. Exp. Biol. 43, 241 246.
59. Stragier B., Clinckers R., Meurs A., De Bundel D., Sarre S., Ebinger G., Michotte Y. Smolders I. (2006) Involvement of the somatostatin-2 receptor in the anti-convulsant effect of angiotensin IV against pilocarpine-induced limbic seizures in rats. J. Neurochem. 98, 1100 1113.
60. Swanson G. N., Hanesworth J. M., Sardinia M. F. et al. (1992) Discovery of a distinct binding site for angiotensin II (3-8), a putative angiotensin IV receptor. Regul. Pept. 40, 409 419.
61. Tota S., Kamat P. K., Awasthi H., Singh N., Raghubir R., Nath C. Hanif K. 2008) Candesartan improves memory decline in mice: involvement of AT1 receptors in memory deficit induced by intracerebral streptozotocin. Behav. Brain Res. 199, 235 240.
62. Tracy H. A. Jr., Wayner M. J. Armstrong D. L. (1997) Losartan improves the performance of ethanol-intoxicated rats in an eight-arm radial maze. Alcohol (Fayetteville, NY) 14, 511 517.
63. Van Hemelrijck A., Sarre S., Smolders I. Michotte Y. (2005) Determination of amino acids associated with cerebral ischaemia in rat brain microdialysates using narrowbore liquid chromatography and fluorescence detection. J. Neurosci. Methods 144, 63 71.
64. Vanderheyden P. M., Fierens F. L., De Backer J. P., Fraeyman N. Vauquelin G. (1999) Distinction between surmountable and insurmountable selective AT1 receptor antagonists by use of CHO-K1 cells expressing human angiotensin II AT1 receptors. Br. J. Pharmacol. 126, 1057 1065.
65. Vanhove C., Defrise M., Bossuyt A. Lahoutte T. (2009) Improved quantification in single-pinhole and multiple-pinhole SPECT using micro-CT information. Eur. J. Nucl. Med. Mol. Imaging 36, 1049 1063.
66. Verheijen I., Fierens F. L., Debacker J. P., Vauquelin G. Vanderheyden P. M. (2000) Interaction between the partially insurmountable antagonist valsartan and human recombinant angiotensin II type 1 receptors. Fundam. Clin. Pharmacol. 14, 577 585.
67. White P. F., Marietta M. P., Pudwill C. R., Way W. L. Trevor A. J. (1976) Effects of halothane anesthesia on the biodisposition of ketamine in rats. J. Pharmacol. Exp. Ther. 196, 545 555.
68. Wisniewski K., Borawska M. Car H. (1993) The effect of angiotensin II and its fragments on post-alcohol impairment of learning and memory. Pol. J. Pharmacol. 45, 23 29.
69. Wright J. W., Miller-Wing A. V., Shaffer M. J., Higginson C., Wright D. E., Hanesworth J. M. Harding J. W. (1993) Angiotensin II(3-8) (ANG IV) hippocampal binding: potential role in the facilitation of memory. Brain Res. Bull. 32, 497 502.
70. Wright J. W., Bechtholt A. J., Chambers S. L. Harding J. W. (1996a) Angiotensin III and IV activation of the brain AT1 receptor subtype in cardiovascular function. Peptides 17, 1365 1371.
71. Wright J. W., Clemens J. A., Panetta J. A., Smalstig E. B., Weatherly L. A., Kramar E. A., Pederson E. S., Mungall B. H. Harding J. W. (1996b) Effects of LY231617 and angiotensin IV on ischemia-induced deficits in circular water maze and passive avoidance performance in rats. Brain Res. 717, 1 11.
72. Wright J. W., Stubley L., Pederson E. S., Kramar E. A., Hanesworth J. M. Harding J. W. (1999) Contributions of the brain angiotensin IV-AT4 receptor subtype system to spatial learning. J. Neurosci. 19, 3952 3961.
73. Wright J. W., Yamamoto B. J. Harding J. W. (2008) Angiotensin receptor subtype mediated physiologies and behaviors: new discoveries and clinical targets. Prog. Neurobiol. 84, 157 181.
74. Yan Q., Matheson C., Sun J., Radeke M. J., Feinstein S. C. Miller J. A. (1994) Distribution of intracerebral ventricularly administered neurotrophins in rat brain and its correlation with trk receptor expression. Exp. Neurol. 127, 23 36.
75. Yang R., Smolders I., De Bundel D., Fouyn R., Halberg M., Demaegdt H., Vanderheyden P. Dupont A. G. (2008) Brain and peripheral angiotensin II type 1 receptors mediate renal vasoconstrictor and blood pressure responses to angiotensin IV in the rat. J. Hypertens. 26, 998 1007.