Angiotensin type 1 receptor inhibition enhances the extinction of fear memory

Biological Psychiatry

Volumn 75, Issue 11, 2014, Pages 864-872

  Marvar, Paul J ^a,b   Goodman, Jared ^a   Fuchs, Sebastien ^c   Choi, Dennis C ^a   Banerjee, Sunayana ^a   Ressler, Kerry J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

cardiovascular disease; fear memory; PTSD; renin angiotensin; stress

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; LOSARTAN; MESSENGER RNA; ANGIOTENSIN 1 RECEPTOR ANTAGONIST;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANXIETY DISORDER; ARTICLE; BLOOD PRESSURE; CARDIOVASCULAR RESPONSE; CONDITIONING; CONTROLLED STUDY; DRUG EFFECT; ENZYME INHIBITION; FOOTSHOCK; GENE EXPRESSION; IMMOBILIZATION STRESS; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; MINIPUMP; MOUSE; NONHUMAN; ONCOGENE C FOS; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; STRIA TERMINALIS; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; FEAR; REINFORCEMENT; STRESS DISORDERS, POST-TRAUMATIC;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; DISEASE MODELS, ANIMAL; EXTINCTION, PSYCHOLOGICAL; FEAR; LOSARTAN; MALE; MEMORY; MICE; MICE, INBRED C57BL; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84900523528     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.08.024     Document Type: Article

References (77)

1. N. Ahmadi, F. Hajsadeghi, H.B. Mirshkarlo, M. Budoff, R. Yehuda, and R. Ebrahimi Post-traumatic stress disorder, coronary atherosclerosis, and mortality Am J Cardiol 108 2011 29 33
2. C.N. Sawchuk, P. Roy-Byrne, J. Goldberg, S. Manson, C. Noonan, J. Beals, and D. Buchwald The relationship between post-traumatic stress disorder, depression and cardiovascular disease in an American Indian tribe Psychol Med 35 2005 1785 1794
3. T.C. Buckley, and D.G. Kaloupek A meta-analytic examination of basal cardiovascular activity in posttraumatic stress disorder Psychosom Med 63 2001 585 594
4. D. Edmondson, and B.E. Cohen Posttraumatic stress disorder and cardiovascular disease Prog Cardiovasc Dis 55 2013 548 556
5. B.A. Wentworth, M.B. Stein, L.S. Redwine, Y. Xue, P.R. Taub, and P. Clopton et al. Post-traumatic stress disorder: A fast track to premature cardiovascular disease? Cardiol Rev 21 2013 16 22
6. S.S. Coughlin Post-traumatic stress disorder and cardiovascular disease Open Cardiovasc Med J 5 2011 164 170
7. J.M. Saavedra Angiotensin II AT(1) receptor blockers as treatments for inflammatory brain disorders Clin Sci 123 2012 567 590
8. J.W. Wright, and J.W. Harding 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 2008 226 237
9. P.R. Gard Angiotensin as a target for the treatment of Alzheimer's disease, anxiety and depression Expert Opin Ther Targets 8 2004 7 14
10. G. Aguilera, A. Kiss, X. Luo, and B.S. Akbasak The renin angiotensin system and the stress response Ann N Y Acad Sci 771 1995 173 186
11. G. Yang, Z.X. Xi, Y. Wan, H. Wang, and G. Bi Changes in circulating and tissue angiotensin II during acute and chronic stress Biol Signals 2 1993 166 172
12. J.M. Saavedra, and J. Benicky Brain and peripheral angiotensin II play a major role in stress Stress 10 2007 185 193
13. I. Armando, S. Volpi, G. Aguilera, and J.M. Saavedra Angiotensin II AT1 receptor blockade prevents the hypothalamic corticotropin-releasing factor response to isolation stress Brain Res 1142 2007 92 99
14. E.C. Dumont, S. Rafrafi, S. Laforest, and G. Drolet Involvement of central angiotensin receptors in stress adaptation Neuroscience 93 1999 877 884
15. C. Bregonzio, A. Seltzer, I. Armando, J. Pavel, and J.M. Saavedra Angiotensin II AT(1) receptor blockade selectively enhances brain AT(2) receptor expression, and abolishes the cold-restraint stress-induced increase in tyrosine hydroxylase mRNA in the locus coeruleus of spontaneously hypertensive rats Stress 11 2008 457 466
16. E.G. Krause, A.D. de Kloet, K.A. Scott, J.N. Flak, K. Jones, and M.D. Smeltzer et al. Blood-borne angiotensin II acts in the brain to influence behavioral and endocrine responses to psychogenic stress J Neurosci 31 2011 15009 15015
17. F. Amenta, F. Mignini, F. Rabbia, D. Tomassoni, and F. Veglio Protective effect of anti-hypertensive treatment on cognitive function in essential hypertension: Analysis of published clinical data J Neurol Sci 203-204 2002 147 151
18. C. Anderson, K. Teo, P. Gao, H. Arima, A. Dans, and T. Unger et al. Renin-angiotensin system blockade and cognitive function in patients at high risk of cardiovascular disease: Analysis of data from the ONTARGET and TRANSCEND studies Lancet Neurol 10 2011 43 53
19. N.M. Khoury, P.J. Marvar, C.F. Gillespie, A. Wingo, A. Schwartz, and B. Bradley et al. The renin-angiotensin pathway in posttraumatic stress disorder: Angiotensin-converting enzyme inhibitors and angiotensin receptor blockers are associated with fewer traumatic stress symptoms J Clin Psychiatry 73 2012 849 855
20. P. Gard Strain differences in the anxiolytic effects of losartan in the mouse Pharmacol Biochem Behav 69 2001 35 40
21. N. Breslau, R.C. Kessler, H.D. Chilcoat, L.R. Schultz, G.C. Davis, and P. Andreski Trauma and posttraumatic stress disorder in the community: The 1996 Detroit Area Survey of Trauma Arch Gen Psychiatry 55 1998 626 632
22. N. Brunello, J.R. Davidson, M. Deahl, R.C. Kessler, J. Mendlewicz, and G. Racagni et al. Posttraumatic stress disorder: Diagnosis and epidemiology, comorbidity and social consequences, biology and treatment Neuropsychobiology 43 2001 150 162
23. T. Jovanovic, and K.J. Ressler How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD Am J Psychiatry 167 2010 648 662
24. B.O. Rothbaum, and M. Davis Applying learning principles to the treatment of post-trauma reactions Ann N Y Acad Sci 1008 2003 112 121
25. M. Davis, K. Ressler, B.O. Rothbaum, and R. Richardson Effects of D-cycloserine on extinction: Translation from preclinical to clinical work Biol Psychiatry 60 2006 369 375
26. T.J. Guzik, N.E. Hoch, K.A. Brown, L.A. McCann, A. Rahman, and S. Dikalov et al. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction J Exp Med 204 2007 2449 2460
27. P.J. Marvar, S.R. Thabet, T.J. Guzik, H.E. Lob, L.A. McCann, and C Weyand et al. Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension Circ Res 107 2010 263 270
28. P.J. Marvar, A. Vinh, S. Thabet, H.E. Lob, D. Geem, K.J. Ressler, and D.G. Harrison T lymphocytes and vascular inflammation contribute to stress-dependent hypertension Biol Psychiatry 71 2012 774 782
29. S. Pellow, P. Chopin, S.E. File, and M. Briley Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat J Neurosci Methods 14 1985 149 167
30. D.C. Choi, K.A. Maguschak, K. Ye, S.W. Jang, K.M. Myers, and K.J. Ressler Prelimbic cortical BDNF is required for memory of learned fear but not extinction or innate fear Proc Natl Acad Sci U S A 107 2010 2675 2680
31. S.A. Heldt, L. Stanek, J.P. Chhatwal, and K.J. Ressler Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories Mol Psychiatry 12 2007 656 670
32. G. Paxinos, and K. Franklin The Mouse Brain in Stereotaxic Coordinates 2nd ed 2006 Academic Press San Diego
33. G.T. Wang, C.C. Chung, T.F. Holzman, and G.A. Krafft A continuous fluorescence assay of renin activity Anal Biochem 210 1993 351 359
34. H. Xia, Y. Feng, T.D. Obr, P.J. Hickman, and E. Lazartigues Angiotensin II type 1 receptor-mediated reduction of angiotensin-converting enzyme 2 activity in the brain impairs baroreflex function in hypertensive mice Hypertension 53 2008 210 216
35. E.E. Soltis, A.L. Jewell, L.P. Dwoskin, and L.A. Cassis Acute and chronic effects of losartan (DuP 753) on blood pressure and vascular reactivity in normotensive rats Clin Exp Hypertens 15 1993 171 184
36. J.P. Collister, S.L. Soucheray, and J.W. Osborn Chronic hypotensive effects of losartan are not dependent on the actions of angiotensin II at AT 2 receptors J Cardiovasc Pharmacol 39 2002 107 116
37. D. Senador, K. Kanakamedala, M.C. Irigoyen, M. Morris, and K.M. Elased Cardiovascular and autonomic phenotype of db/db diabetic mice Exp Physiol 94 2009 648 658
38. J. Srinivasan, S. Jayadev, D. Kumaran, K.F. Ahamed, B. Suresh, and M. Ramanathan Effect of losartan and enalapril on cognitive deficit caused by Goldblatt induced hypertension Indian J Exp Biol 43 2005 241 246
39. P.C. Wong, W.A. Price, A.T. Chiu, J.V. Duncia, D.J. Carini, and R.R. Wexler et al. Nonpeptide angiotensin II receptor antagonists. VIII. Characterization of functional antagonism displayed by DuP 753, an orally active antihypertensive agent J Pharmacol Exp Ther 252 1990 719 725
40. A.L. Mahan, and K.J. Ressler Fear conditioning, synaptic plasticity and the amygdala: Implications for posttraumatic stress disorder Trends Neurosci 35 2012 24 35
41. L.M. Rattiner Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning J Neurosci 24 2004 4796 4806
42. J.P. Chhatwal, L. Stanek-Rattiner, M. Davis, and K.J. Ressler Amygdala BDNF signaling is required for consolidation but not encoding of extinction Nat Neurosci 9 2006 870 872
43. D.C. Choi, S.L. Gourley, and K.J. Ressler Prelimbic BDNF and TrkB signaling regulates consolidation of both appetitive and aversive emotional learning Transl Psychiatry 2 2012 e205
44. K.S. Sink, D.L. Walker, S.M. Freeman, E.I. Flandreau, K.J. Ressler, and M. Davis Effects of continuously enhanced corticotropin releasing factor expression within the bed nucleus of the stria terminalis on conditioned and unconditioned anxiety Mol Psychiatry 18 2013 308 319
45. J.W. Wright, and J.W. Harding Brain angiotensin receptor subtypes AT1, AT2, and AT4 and their functions Regul Pept 59 1995 269 295
46. P.R. Gard The role of angiotensin II in cognition and behaviour Eur J Pharmacol 438 2002 1 14
47. I. Armando, A. Carranza, Y. Nishimura, K.L. Hoe, M. Barontini, and J.A. Terrón et al. Peripheral administration of an angiotensin II AT(1) receptor antagonist decreases the hypothalamic-pituitary-adrenal response to isolation Stress Endocrinology 142 2001 3880 3889
48. A. Shekhar Angiotensin-II is a putative neurotransmitter in lactate-induced panic-like responses in rats with disruption of GABAergic inhibition in the dorsomedial hypothalamus J Neurosci 26 2006 9205 9215
49. M. Wessa, and H. Flor Failure of extinction of fear responses in posttraumatic stress disorder: Evidence from second-order conditioning Am J Psychiatry 164 2007 1684 1692
50. J. Blechert, T. Michael, N. Vriends, J. Margraf, and F.H. Wilhelm Fear conditioning in posttraumatic stress disorder: Evidence for delayed extinction of autonomic, experiential, and behavioural responses Behav Res Ther 45 2007 2019 2033
51. S.D. Norrholm, T. Jovanovic, I.W. Olin, L.A. Sands, I. Karapanou, B. Bradley, and K.J. Ressler Fear extinction in traumatized civilians with posttraumatic stress disorder: Relation to symptom severity Biol Psychiatry 69 2011 556 563
52. E.M. Glover, T. Jovanovic, K.B. Mercer, K. Kerley, B. Bradley, K.J. Ressler, and S.D. Norrholm Estrogen levels are associated with extinction deficits in women with posttraumatic stress disorder Biol Psychiatry 72 2012 19 24
53. R. Andero, and K.J. Ressler Fear extinction and BDNF: Translating animal models of PTSD to the clinic Genes Brain Behav 11 2012 503 512
54. L.H. Lopez, F. Caif, S. Garcia, M. Fraile, A.I. Landa, and G. Baiardi et al. Anxiolytic-like effect of losartan injected into amygdala of the acutely stressed rats Pharmacol Rep 64 2012 54 63
55. J.J. Braszko, D. Wincewicz, and P. Jakubów Candesartan prevents impairment of recall caused by repeated stress in rats Psychopharmacology (Berl) 225 2013 421 428
56. J.J. Braszko Valsartan abolishes most of the memory-improving effects of intracerebroventricular angiotensin II in rats Clin Exp Hypertens 27 2005 635 649
57. A. Kulakowska, W. Karwowska, K. Wisniewski, and J.J. Braszko Losartan influences behavioural effects of angiotensin II in rats Pharmacol Res 34 1997 109 115
58. V. Georgiev, and D. Yonkov Participation of angiotensin II in learning and memory. I. Interaction of angiotensin II with saralasin Methods Find Exp Clin Pharmacol 7 1985 415 418
59. J.J. Braszko, and K. Wisniewski Effect of angiotensin II and saralasin on motor activity and the passive avoidance behavior of rats Peptides 9 1988 475 479
60. F.A.M. DeSouza, C. Sanchis-Segura, S.Y. Fukada, V.C. de Bortoli, H. Zangrossi, and A.M. de Oliveira Intracerebroventricular effects of angiotensin II on a step-through passive avoidance task in rats Neurobiol Learn Mem 81 2004 100 103
61. J.M. Morgan Angiotensin injected into the neostriatum after learning disrupts retention performance Science 196 1977 87 89
62. D.S. Kerr, L.R.M. Bevilaqua, J.S. Bonini, J.I. Rossato, C.A. Köhler, and J.H. Medina et al. Angiotensin II blocks memory consolidation through an AT2 receptor-dependent mechanism Psychopharmacology (Berl) 179 2004 529 535
63. 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
64. N.M. Barnes, S. Champaneria, B. Costall, M.E. Kelly, D.A. Murphy, and R.J. Naylor Cognitive enhancing actions of DuP 753 detected in a mouse habituation paradigm Neuroreport 1 1990 239 242
65. V. Raghavendra, K. Chopra, and S.K. Kulkarni Comparative studies on the memory-enhancing actions of captopril and losartan in mice using inhibitory shock avoidance paradigm Neuropeptides 35 2001 65 69
66. J.S. Bonini, L.R. Bevilaqua, C.G. Zinn, D.S. Kerr, J.H. Medina, I. Izquierdo, and M. Cammarota Angiotensin II disrupts inhibitory avoidance memory retrieval Horm Behav 50 2006 308 313
67. M.R. Tinsley The role of muscarinic and nicotinic cholinergic neurotransmission in aversive conditioning: Comparing Pavlovian fear conditioning and inhibitory avoidance Learn Mem 11 2004 35 42
68. E. Likhtik, J.G. Pelletier, R. Paz, and D. Paré Prefrontal control of the amygdala J Neurosci 25 2005 7429 7437
69. E. Likhtik, D. Popa, J. Apergis-Schoute, G.A. Fidacaro, and D. Paré Amygdala intercalated neurons are required for expression of fear extinction Nature 454 2008 642 645
70. Y. Marc, and C. Llorens-Cortes The role of the brain renin-angiotensin system in hypertension: Implications for new treatment Prog Neurobiol 95 2011 89 103
71. A.D. Gonzalez, G. Wang, E.M. Waters, K.L. Gonzales, R.C. Speth, and T.A. Van Kempen et al. Distribution of angiotensin type 1a receptor-containing cells in the brains of bacterial artificial chromosome transgenic mice Neuroscience 226 2012 489 509
72. D.L. Walker, D.J. Toufexis, and M. Davis Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety Eur J Pharmacol 463 2003 199 216
73. M. Davis, D.L. Walker, and Y. Lee Amygdala and bed nucleus of the stria terminalis: Differential roles in fear and anxiety measured with the acoustic startle reflex Philos Trans R Soc Lond B Biol Sci 352 1997 1675 1687
74. J.W. Wright, and J.W. Harding 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 2008 226 237
75. M. Szekeres, G.L. Nadasy, G. Turu, K. Supeki, L. Szidonya, and L. Buday et al. Angiotensin II-induced expression of brain-derived neurotrophic factor in human and rat adrenocortical cells Endocrinology 151 2010 1695 1703
76. R. Nostramo, A. Tillinger, J.M. Saavedra, A. Kumar, V. Pandey, and L. Serova et al. Regulation of angiotensin II type 2 receptor gene expression in the adrenal medulla by acute and repeated immobilization stress J Endocrinol 215 2012 291 301
77. K.J. Ressler, K.B. Mercer, B. Bradley, T. Jovanovic, A. Mahan, and K. Kerley et al. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor Nature 470 2011 492 497