Facilitation of hippocampal synaptogenesis and spatial memory by C-terminal truncated Nle 1-angiotensin IV analogs

Journal of Pharmacology and Experimental Therapeutics

Volumn 339, Issue 1, 2011, Pages 35-44

  Benoist, Caroline C ^a   Wright, John W ^a   Zhu, Mingyan ^a   Appleyard, Suzanne M ^a   Wayman, Gary A ^a   Harding, Joseph W ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN DERIVATIVE; ANGIOTENSIN IV [1 NORLEUCINE 2 TYROSINE 3 ISOLEUCINE 4 HISTIDINE 5 PROLINE]; ANGIOTENSIN IV [1 NORLEUCINE 2 TYROSINE 3 ISOLEUCINE 4 HISTIDINE]; ANGIOTENSIN IV [1 NORLEUCINE 2 TYROSINE 3 ISOLEUCINE]; ANGIOTENSIN IV [1 NORLEUCINE 2 TYROSINE]; ANGIOTENSIN IV [1 NORLEUCINE]; ANGIOTENSIN IV [1 NORLEUCINE] DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COGNITION; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITIC SPINE; DRUG MECHANISM; DRUG STRUCTURE; HIPPOCAMPUS; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; SYNAPTOGENESIS;

ANIMALS; BEHAVIOR, ANIMAL; CELL COUNT; CELLS, CULTURED; COGNITION; DENDRITES; DENDRITIC SPINES; DOSE-RESPONSE RELATIONSHIP, DRUG; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MAZE LEARNING; MEMORY; MUSCARINIC ANTAGONISTS; PATCH-CLAMP TECHNIQUES; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ANGIOTENSIN; SCOPOLAMINE HYDROBROMIDE; STRUCTURE-ACTIVITY RELATIONSHIP; SYNAPSES; TRANSFECTION;

EID: 80053147355     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.111.182220     Document Type: Article

References (42)

1. Abhold RH and Harding JW (1988) Metabolism of angiotensins II and III by membrane- bound peptidases from rat brain. J Pharmacol Exp Ther 245:171-177.
2. Balschun D, Moechars D, Callaerts-Vegh Z, Vermaercke B, Van Acker N, Andries L, and D'Hooge R (2010) Vesicular glutamate transporter VGLUT1 has a role inhippocampal long-term potentiation and spatial reversal learning. Cereb Cortex 20:684-693.
3. Braszko JJ, Kupryszewski G, Witczuk B, and Wiśniewski 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. (Pubitemid 19025386)
4. Calabrese EJ and Baldwin LA (2003) The hormetic dose-response model is more common than the threshold model in toxicology. Toxicol Sci 71:246-250. (Pubitemid 36285016)
5. Chai SY, Bastias MA, Clune EF, Matsacos DJ, Mustafa T, Lee JH, McDowall SG, Paxinos G, Mendelsohn FA, and Albiston AL (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. (Pubitemid 32162891)
6. Davis CJ, Kramár EA, De A, Meighan PC, Simasko SM, Wright JW, and Harding JW (2006) AT4 receptor activation increases intracellular calcium influx and induces a non-N-methyl-D-aspartate dependent form of long-term potentiation. Neuroscience 137:1369-1379. (Pubitemid 43133160)
7. De Bundel D, Demaegdt H, Lahoutte T, Caveliers V, Kersemans K, Ceulemans AG, Vauquelin G, Clinckers R, Vanderheyden P, Michotte Y, et al. (2010) Involvement of the AT1 receptor subtype in the effects of angiotensin IV and LVV-haemorphin 7 on hippocampal neurotransmitter levels and spatial working memory. J Neurochem 112:1223-1234.
8. De Bundel D, Smolders I, Vanderheyden P, and 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.
9. Faure S, Chapot R, Tallet D, Javellaud J, Achard JM, and Oudart N (2006) Cerebroprotective effect of angiotensin IV in experimental ischemic stroke in the rat mediated by AT4 receptors. J Physiol Pharmacol 57:329-342. (Pubitemid 44543870)
10. Ferreira A and Rapoport M (2002) The synapsins: beyond the regulation of neurotransmitter release. Cell Mol Life Sci 59:589-595. (Pubitemid 34457537)
11. Fisher A, Pittel Z, Haring R, Bar-Ner N, Kliger-Spatz M, Natan N, Egozi I, Sonego H, Marcovitch I, and Brandeis R (2003) M1 muscarinic agonists can modulate some of the hallmarks in Alzheimer's disease: implications in future therapy. J Mol Neurosci 20:349-356. (Pubitemid 38146993)
12. Fyhrquist F and Saijonmaa O (2008) Renin-angiotensin system revisited. J Intern Med 264:224-236.
13. Gard PR (2004) Angiotensin as a target for the treatment of Alzheimer's disease, anxiety and depression. Expert Opin Ther Targets 8:7-14.
14. Gard PR (2008) Cognitive-enhancing effects of angiotensin IV. BMC Neurosci 9 (Suppl 2):S15.
15. Harding JW, Cook VI, Miller-Wing AV, Hanesworth JM, Sardinia MF, Hall KL, Stobb JW, Swanson GN, Coleman JK, and Wright JW (1992) Identification of an AII(3- 8) [AIV] binding site in guinea pig hippocampus. Brain Res 583:340-343.
16. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, and Noguchi J (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33:121-129.
17. Kennedy MB, Beale HC, Carlisle HJ, and Washburn LR (2005) Integration of biochemical signalling in spines. Nat Rev Neurosci 6:423-434. (Pubitemid 40774860)
18. Klausberger T (2009) GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. Eur J Neurosci 30:947-957.
19. Kramár EA, Armstrong DL, Ikeda S, Wayner MJ, Harding JW, and Wright JW (2001) The effects of angiotensin IV analogs on long-term potentiation within the CA1 region of the hippocampus in vitro. Brain Res 897:114-121. (Pubitemid 32244358)
20. Kramár EA, Harding JW, and Wright JW (1997) Angiotensin II- and IV-induced changes in cerebral blood flow. Roles of AT1, AT2, and AT4 receptor subtypes. Regul Pept 68:131-138. (Pubitemid 27138368)
21. Lee J, Albiston AL, Allen AM, Mendelsohn FA, Ping SE, Barrett GL, Murphy M, Morris MJ, McDowall SG, and Chai SY (2004a) Effect of I.C.V. injection of AT4 receptor ligands, NLE1-angiotensin IV and LVV-hemorphin 7, on spatial learning in rats. Neuroscience 124:341-349. (Pubitemid 38229654)
22. Lee KJ, Kim H, Kim TS, Park SH, and Rhyu IJ (2004b) Morphological analysis of spine shapes of Purkinje cell dendrites in the rat cerebellum using high-voltage electron microscopy. Neurosci Lett 359:21-24. (Pubitemid 38446629)
23. Lopez J, Wolff M, Lecourtier L, Cosquer B, Bontempi B, Dalrymple-Alford J, and Cassel JC (2009) The intralaminar thalamic nuclei contribute to remote spatial memory. J Neurosci 29:3302-3306.
24. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, and Unser M (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58:167-176. (Pubitemid 38509178)
25. Mustafa T, Lee JH, Chai SY, Albiston AL, McDowall SG, and Mendelsohn FA (2001) Bioactive angiotensin peptides: focus on angiotensin IV. J Renin Angiotensin Aldosterone Syst 2:205-210. (Pubitemid 33685893)
26. Pederson ES, Krishnan R, Harding JW, and Wright JW (2001) A role for the angiotensin AT4 receptor subtype in overcoming scopolamine-induced spatial memory deficits. Regul Pept 102:147-156. (Pubitemid 33135576)
27. Saneyoshi T, Fortin DA, and Soderling TR (2010) Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways. Curr Opin Neurobiol 20:108-115.
28. Sardinia MF, Hanesworth JM, Krebs LT, and Harding JW (1993) AT4 receptor binding characteristics: D-amino acid- and glycine-substituted peptides. Peptides 14:949-954.
29. Sardinia MF, Hanesworth JM, Krishnan F, and Harding JW (1994) AT4 receptor structure-binding relationship: N-terminal-modified angiotensin IV analogues. Peptides 15:1399-1406. (Pubitemid 24381186)
30. Stubley-Weatherly L, Harding JW, and Wright JW (1996) Effects of discrete kainic acid-induced hippocampal lesions on spatial and contextual learning and memory in rats. Brain Res 716:29-38. (Pubitemid 26156598)
31. Towart LA, Alves SE, Znamensky V, Hayashi S, McEwen BS, and Milner TA (2003) Subcellular relationships between cholinergic terminals and estrogen receptoralpha in the dorsal hippocampus. J Comp Neurol 463:390-401. (Pubitemid 36890523)
32. Tyler WJ and Pozzo-Miller L (2003) Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurones. J Physiol 553: 497-509. (Pubitemid 37527549)
33. Vanderheyden PM (2009) From angiotensin IV binding site to AT4 receptor. Mol Cell Endocrinol 302:159-166.
34. von Bohlen und Halbach O (2003) Angiotensin IV in the central nervous system. Cell Tissue Res 311:1-9.
35. von Bohlen und Halbach O and Albrecht D (2006) The CNS renin-angiotensin system. Cell Tissue Res 326:599-616.
36. von Bohlen und Halbach O, Minichiello L, and Unsicker K (2008) TrkB but not trkC receptors are necessary for postnatal maintenance of hippocampal spines. Neurobiol Aging 29:1247-1255.
37. Wayman GA, Davare M, Ando H, Fortin D, Varlamova O, Cheng HY, Marks D, Obrietan K, Soderling TR, Goodman RH, et al. (2008) An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc Natl Acad Sci USA 105:9093-9098.
38. Wright JW, Clemens JA, Panetta JA, Smalstig EB, Weatherly LA, Kramár EA, Pederson ES, Mungall BH, and Harding JW (1996) 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. (Pubitemid 26155069)
39. Wright JW and Harding JW (2008) The angiotensin AT4 receptor subtype as a target for the treatment of memory dysfunction associated with Alzheimer's disease. J Renin Angiotensin Aldosterone Syst 9:226-237.
40. Wright JW and Harding JW (2010) The brain RAS and Alzheimer's disease. Exp Neurol 223:326-333.
41. Wright JW, Stubley L, Pederson ES, Kramár EA, Hanesworth JM, and Harding JW (1999) Contributions of the brain angiotensin IV-AT4 receptor subtype system to spatial learning. J Neurosci 19:3952-3961. (Pubitemid 29222269)
42. Xu T, Yu X, Perlik AJ, Tobin WF, Zweig JA, Tennant K, Jones T, and Zuo Y (2009) Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462:915-919.