Central administration of angiotensin IV rapidly enhances novel object recognition among mice

Neuropharmacology

Volumn 70, Issue , 2013, Pages 247-253

  Paris, Jason J ^a   Eans, Shainnel O ^a   Mizrachi, Elisa ^a   Reilley, Kate J ^a   Ganno, Michelle L ^a   McLaughlin, Jay P ^a  

^a TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

Author keywords

Angiotensin II(3 8); Cognition; Drug discovery; Learning and memory; Novel object recognition; Renin angiotensin system

Indexed keywords

ANGIOTENSIN II [3-8]; ANGIOTENSIN RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ARTICLE; COGNITION; CONTROLLED STUDY; DOSE RESPONSE; DRUG ACTIVITY; DRUG EFFECT; LOCOMOTION; MALE; MEMORY; MENTAL PERFORMANCE; MENTAL TASK; MOUSE; NONHUMAN; NOVEL OBJECT RECOGNITION; PRIORITY JOURNAL; RECOGNITION; ROTAROD TEST; STATE DEPENDENT LEARNING;

ALANINE; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR ANTAGONISTS; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; INFUSIONS, INTRAVENTRICULAR; MALE; MICE; MOTOR ACTIVITY; NOOTROPIC AGENTS; RECOGNITION (PSYCHOLOGY); TIME FACTORS;

EID: 84877003852     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.01.025     Document Type: Article

References (62)

1. A.L. Albiston, S.G. McDowall, D. Matsacos, P. Sim, E. Clune, T. Mustafa, J. Lee, F.A. Mendelsohn, R.J. Simpson, L.M. Connolly, and S.Y. Chai Evidence that the angiotensin IV (AT(4)) receptor is the enzyme insulin-regulated aminopeptidase J. Biol. Chem. 276 2001 48623 48626
2. J.V. Aldrich, and J.P. McLaughlin Peptide kappa opioid receptor ligands: potential for drug development AAPS J. 11 2009 312 322
3. D. Baranowska, J.J. Braszko, and K. Wiśniewski Effect of angiotensin II and vasopressin on acquisition and extinction of conditioned avoidance in rats Psychopharmacology (Berl) 81 1983 247 251
4. C.C. Benoist, J.W. Wright, M. Zhu, S.M. Appleyard, G.A. Wayman, and J.W. Harding Facilitation of hippocampal synaptogenesis and spatial memory by C-terminal truncated Nle1-angiotensin IV analogs J. Pharmacol. Exp. Ther. 339 2011 35 44
5. J. Birks Cholinesterase inhibitors for Alzheimer's disease Cochrane Database Syst. Rev. 2006 CD005593
6. J.J. Braszko The contribution of AT1 and AT2 angiotensin receptors to its cognitive effects Acta Neurobiol. Exp. (Wars) 56 1996 49 54
7. J.J. Braszko AT(2) but not AT(1) receptor antagonism abolishes angiotensin II increase of the acquisition of conditioned avoidance responses in rats Behav. Brain Res. 131 2002 79 86
8. J.J. Braszko Involvement of D1 dopamine receptors in the cognitive effects of angiotensin IV and des-Phe6 angiotensin IV Peptides 25 2004 1195 1203
9. J.J. Braszko, A. Kułakowska, and W. Karwowska-Polecka CGP 42112A antagonism of the angiotensin II and angiotensin II(3-7) facilitation of recall in rats Pharmacol. Res. 38 1998 461 468
10. J.J. Braszko, G. Kupryszewski, B. Witczuk, and K. Wiśniewski Angiotensin II-(3-8)-hexapeptide affects motor activity, performance of passive avoidance and a conditioned avoidance response in rats Neuroscience 27 1988 777 783
11. J.J. Braszko, P. Wielgat, and A. Walesiuk Effect of D(3) dopamine receptors blockade on the cognitive effects of angiotensin IV in rats Neuropeptides 42 2008 301 309
12. N.J. Broadbent, L.R. Squire, and R.E. Clark Spatial memory, recognition memory, and the hippocampus Proc. Natl. Acad. Sci. U. S. A 101 2004 14515 14520
13. R. Brookmeyer, E. Johnson, K. Ziegler-Graham, and H.M. Arrighi Forecasting the global burden of Alzheimer's disease Alzheimers Dement. 3 2007 186 191
14. A.N. Carey, A.M. Lyons, C.F. Shay, O. Dunton, and J.P. McLaughlin Endogenous kappa opioid activation mediates stress-induced deficits in learning and memory J. Neurosci. 29 2009 4293 4300
15. A.N. Carey, E.I. Sypek, H.D. Singh, M.J. Kaufman, and J.P. McLaughlin Expression of HIV-Tat protein is associated with learning and memory deficits in the mouse Behav. Brain Res. 229 2012 48 56
16. S.Y. Chai, M.A. Bastias, E.F. Clune, D.J. Matsacos, T. Mustafa, J.H. Lee, S.G. McDowall, G. Paxinos, F.A. Mendelsohn, and A.L. Albiston 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 2000 339 348
17. H.L. Chua, S. Jois, M.K. Sim, and M.L. Go Transport of angiotensin peptides across the Caco-2 monolayer Peptides 25 2004 1327 1338
18. J.K. Coleman, L.T. Krebs, T.A. Hamilton, B. Ong, K.A. Lawrence, M.F. Sardinia, J.W. Harding, and J.W. Wright Autoradiographic identification of kidney angiotensin IV binding sites and angiotensin IV-induced renal cortical blood flow changes in rats Peptides 19 1998 269 277
19. D. De Bundel, H. Demaegdt, T. Lahoutte, V. Caveliers, K. Kersemans, A.G. Ceulemans, G. Vauquelin, R. Clinckers, P. Vanderheyden, Y. Michotte, and I. Smolders 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 2010 1223 1234
20. D. De Bundel, I. Smolders, P. Vanderheyden, and Y. Michotte Ang II and Ang IV: unraveling the mechanism of action on synaptic plasticity, memory, and epilepsy CNS Neurosci. Ther. 14 2008 315 339
21. D. De Bundel, I. Smolders, R. Yang, A.L. Albiston, Y. Michotte, and S.Y. Chai Angiotensin IV and LVV-haemorphin 7 enhance spatial working memory in rats: effects on hippocampal glucose levels and blood flow Neurobiol. Learn. Mem. 92 2009 19 26
22. A. Ennaceur, N. Neave, and J.P. Aggleton Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix Exp. Brain Res. 113 1997 509 519
23. S.B. Fonseca, M.P. Pereira, and S.O. Kelley Recent advances in the use of cell-penetrating peptides for medical and biological applications Adv. Drug Deliv. Rev. 61 2009 953 964
24. P.R. Gard Cognitive-enhancing effects of angiotensin IV BMC Neurosci. 9 2008 S15
25. D. Genoux, U. Haditsch, M. Knobloch, A. Michalon, D. Storm, and I.M. Mansuy Protein phosphatase 1 is a molecular constraint on learning and memory Nature 418 2002 970 975
26. B.J. Golding, A.D. Overall, G. Brown, and P.R. Gard Strain differences in the effects of angiotensin IV on mouse cognition Eur. J. Pharmacol. 641 2010 154 159
27. T.J. Haley, and W.G. McCormick Pharmacological effects produced by intracerebral injection of drugs in the conscious mouse Br. J. Pharmacol. Chemother. 12 1957 12 15
28. R.K. Handa Binding and signalling of angiotensin-(1-7) in bovine kidney epithelial cells involves the AT(4) receptor Peptides 21 2000 729 736
29. J.W. Harding, V.I. Cook, A.V. Miller-Wing, J.M. Hanesworth, M.F. Sardinia, K.L. Hall, J.W. Stobb, G.N. Swanson, J.K. Coleman, J.W. Wright, and E.C. Harding Identification of an AII(3-8) [AIV] binding site in guinea pig hippocampus Brain Res. 583 1992 340 343
30. L.H. Kawas, B.J. Yamamoto, J.W. Wright, and J.W. Harding Mimics of the dimerization domain of hepatocyte growth factor exhibit anti-Met and anticancer activity J. Pharmacol. Exp. Ther. 339 2011 509 518
31. E.A. Kramár, J.W. Harding, and J.W. Wright Angiotensin II- and IV-induced changes in cerebral blood flow. Roles of AT1, AT2, and AT4 receptor subtypes Regul. Pept. 68 1997 131 138
32. E.A. Kramár, D.L. Armstrong, S. Ikeda, M.J. Wayner, J.W. Harding, and J.W. Wright The effects of angiotensin IV analogs on long-term potentiation within the CA1 region of the hippocampus in vitro Brain Res. 897 2001 114 121
33. 4 receptor antagonist Regul. Pept. 67 1996 123 130
34. J. Lee, A.L. Albiston, A.M. Allen, F.A. Mendelsohn, S.E. Ping, G.L. Barrett, M. Murphy, M.J. Morris, S.G. McDowall, and S.Y. Chai Effect of I.C.V. injection of AT4 receptor ligands, NLE1-angiotensin IV and LVV-hemorphin 7, on spatial learning in rats Neuroscience 124 2004 341 349
35. R.A. Lew, T. Mustafa, S. Ye, S.G. McDowall, S.Y. Chai, and A.L. Albiston Angiotensin AT4 ligands are potent, competitive inhibitors of insulin regulated aminopeptidase (IRAP) J. Neurochem. 86 2003 344 350
36. M. Marx Watching peptide drugs grow up Chem. Eng. News 83 2005 847 854
37. A.V. Miller-Wing, J.M. Hanesworth, M.F. Sardinia, K.L. Hall, J.W. Wright, R.C. Speth, K.L. Grove, and J.W. Harding Central angiotensin IV binding sites: distribution and specificity in guinea pig brain J. Pharmacol. Exp. Ther. 266 1993 1718 1726
38. A. Nunomura, G. Perry, and M.A. Smith Prospects for antioxidant Therapy in Mild cognitive impairment and Alzheimer's disease G.A. Qureshi, S.H. Parvez, Oxidative Stress and Neurodegenerative Disorders 2007 Elsevier B.V. Amsterdam 451 466
39. J.J. Paris, K.J. Reilley, and J.P. McLaughlin Kappa opioid receptor-mediated disruption of novel object recognition: Relevance for psychostimulant treatment J. Addict. Res. Ther. S4 2011 1 9
40. E.S. Pederson, R. Krishnan, J.W. Harding, and J.W. Wright A role for the angiotensin AT4 receptor subtype in overcoming scopolamine-induced spatial memory deficits Regul. Pept. 102 2001 147 156
41. P. Raina, P. Santaguida, A. Ismaila, C. Patterson, D. Cowan, M. Levine, L. Booker, and M. Oremus Effectiveness of cholinesterase inhibitors and memantine for treating dementia: evidence review for a clinical practice guideline Ann. Intern. Med. 148 2008 379 397
42. K.A. Roberts, L.T. Krebs, E.A. Kramar, M.J. Shaffer, J.W. Harding, and J.W. Wright Autoradigoraphic identification of brain angiotensin IV binding sites and differential c-Fos expression following intracerebroventricular injection of angiotensin II and IV in rats Brain Res. 682 1995 13 21
43. M.F. Sardinia, J.M. Hanesworth, F. Krishnan, and J.W. Harding AT4 receptor structure-binding relationship: N-terminal-modified angiotensin IV analogues Peptides 15 1994 1399 1406
44. G.W. Small, P.V. Rabins, P.P. Barry, N.S. Buckholtz, S.T. DeKosky, S.H. Ferris, S.I. Finkel, L.P. Gwyther, Z.S. Khachaturian, B.D. Lebowitz, T.D. McRae, J.C. Morris, F. Oakley, L.S. Schneider, J.E. Streim, T. Sunderland, L.A. Teri, and L.E. Tune Diagnosis and treatment of Alzheimer disease and related disorders. Consensus statement of the American Association for Geriatric Psychiatry, the Alzheimer's Association, and the American Geriatrics Society JAMA 278 1997 1363 1371
45. B. Stragier, H. Demaegdt, D. De Bundel, I. Smolders, S. Sarre, G. Vauquelin, G. Ebinger, Y. Michotte, and P. Vanderheyden Involvement of insulin-regulated aminopeptidase and/or aminopeptidase N in the angiotensin IV-induced effect on dopamine release in the striatum of the rat Brain Res. 1131 2007 97 105
46. L. Stubley-Weatherly, J.W. Harding, and J.W. Wright Effects of discrete kainic acid-induced hippocampal lesions on spatial and contextual learning and memory in rats Brain Res. 716 1996 29 38
47. J. Tchekalarova, and D. Albrecht Angiotensin II suppresses long-term depression in the lateral amygdala of mice via L-type calcium channels Neurosci. Lett. 415 2007 68 72
48. L. Toll, T.V. Khroyan, K. Sonmez, A. Ozawa, I. Lindberg, J.P. McLaughlin, S.O. Eans, A.A. Shahien, and D.R. Kapusta Peptides derived from the prohormone proNPQ/spexin are potent central modulators of cardiovascular and renal function and nociception FASEB J. 26 2012 947 954
49. M. Van Heek, D.S. Compton, C.F. France, R.P. Tedesco, A.B. Fawzi, M.P. Graziano, E.J. Sybertz, C.D. Strader, and H.R. Davis Jr. Diet-induced obese mice develop peripheral, but not central, resistance to leptin J. Clin. Invest. 99 1997 385 390
50. P. Vlieghe, V. Lisowski, J. Martinez, and M. Khrestchatisky Synthetic therapeutic peptides: science and market Drug Discov. Today 15 2010 40 56
51. M.J. Wayner, D.L. Armstrong, C.F. Phelix, J.W. Wright, and J.W. Harding Angiotensin IV enhances LTP in rat dentate gyrus in vivo Peptides 22 2001 1403 1414
52. M.J. Wayner, D.L. Armstrong, J.L. Polan-Curtain, and J.B. Denny Role of angiotensin II and AT1 receptors in hippocampal LTP Pharmacol. Biochem. Behav. 45 1993 455 464
53. W.L. Wilson, C. Munn, R.C. Ross, J.W. Harding, and J.W. Wright The role of the AT4 and cholinergic systems in the Nucleus Basalis Magnocellularis (NBM): effects on spatial memory Brain Res. 1272 2009 25 31
54. M.M. Winnicka, J.J. Braszko, and K. Wiśniewski Dopaminergic projection to the septum mediates facilitatory effect of angiotensins on recognition memory in rats Pharmacol. Res. 36 1997 387 394
55. M.M. Winnicka, J.J. Braszko, and K. Wiśniewski 6-OHDA lesions to amygdala and hippocampus attenuate memory-enhancing effect of the 3-7 fragment of angiotensin II Gen. Pharmacol. 30 1998 801 805
56. J.W. Wright, J.A. Clemens, J.A. Panetta, E.B. Smalstig, L.A. Weatherly, E.A. Kramár, E.S. Pederson, B.H. Mungall, and J.W. Harding Effects of LY231617 and angiotensin IV on ischemia-induced deficits in circular water maze and passive avoidance performance in rats Brain Res. 717 1996 1 11
57. J.W. Wright, A.V. Miller-Wing, M.J. Shaffer, C. Higginson, D.E. Wright, J.M. Hanesworth, and J.W. Harding Angiotensin II(3-8) (ANG IV) hippocampal binding: potential role in the facilitation of memory Brain Res. Bull. 32 1993 497 502
58. J.W. Wright, L. Stubley, E.S. Pederson, E.A. Kramár, J.M. Hanesworth, and J.W. Harding Contributions of the brain angiotensin IV-AT4 receptor subtype system to spatial learning J. Neurosci. 19 1999 3952 3961
59. B.J. Yamamoto, P.D. Elias, J.A. Masino, B.D. Hudson, A.T. McCoy, Z.J. Anderson, M.D. Varnum, M.F. Sardinia, J.W. Wright, and J.W. Harding The angiotensin IV analog Nle-Tyr-Leu-ψ-(CH2-NH2)3-4-His-Pro-Phe (norleual) can act as a hepatocyte growth factor/c-Met inhibitor J. Pharmacol. Exp. Ther. 333 2010 161 173
60. R. Yang, I. Smolders, D. De Bundel, R. Fouyn, M. Halberg, H. Demaegdt, P. Vanderheyden, and A.G. Dupont Brain and peripheral angiotensin II type 1 receptors mediate renal vasoconstrictor and blood pressure responses to angiotensin IV in the rat J. Hypertens. 26 2008 998 1007
61. J.E. Zadina, L. Hackler, L.-J. Ge, and A.J. Kastin A potent and selective endogenous agonist for the μ-opiate receptor Nature 386 1997 499 502
62. Y. Zhu, M.A. King, A.G.P. Schuller, J.F. Nitsche, M. Reidl, R.P. Elde, E. Unterwald, G.W. Pasternak, and J.E. Pintar Retention of supraspinal delta-like analgesia and loss of morphine tolerance in δ opioid receptor knockout mice Neuron 24 1999 243 252