Increasing brain angiotensin converting enzyme 2 activity decreases anxiety-like behavior in male mice by activating central Mas receptors

Neuropharmacology

Volumn 105, Issue , 2016, Pages 114-123

  Wang, Lei ^a   De Kloet, Annette D ^b   Pati, Dipanwita ^a   Hiller, Helmut ^a   Smith, Justin A ^a   Pioquinto, David J ^b   Ludin, Jacob A ^b   Oh, S Paul ^b   Katovich, Michael J ^a   Frazier, Charles J ^a   Raizada, Mohan K ^b   Krause, Eric G ^a  

^a UNIVERSITY OF FLORIDA HEALTH   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

ACE2; Anxiety; Basolateral amygdala; GABA; Mas receptor; Stress

Indexed keywords

4 AMINOBUTYRIC ACID; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN[1-7][7 DEXTRO ALANINE]; DIMINAZENE ACETURATE; MAS RECEPTOR; MESSENGER RNA; PROTEIN FOS; RECEPTOR; UNCLASSIFIED DRUG; 7-ALA-ANGIOTENSIN (1-7); ANGIOTENSIN II; DIPEPTIDYL CARBOXYPEPTIDASE; G PROTEIN COUPLED RECEPTOR; ONCOPROTEIN; PEPTIDE FRAGMENT; PROTEIN C FOS; PROTO-ONCOGENE PROTEINS C-MAS-1;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BASOLATERAL AMYGDALA; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; ENZYME ACTIVITY; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MOUSE; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; STRIA TERMINALIS; TRANQUILIZING ACTIVITY; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; ANXIETY; C57BL MOUSE; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; NERVE CELL; SEPTUM NUCLEUS;

ANGIOTENSIN II; ANIMALS; ANXIETY; BASOLATERAL NUCLEAR COMPLEX; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; NEURONS; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; SEPTAL NUCLEI;

EID: 84955132595     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.12.026     Document Type: Article

References (54)

1. L.K. Becker, G.M. Etelvino, T. Walther, R.A. Santos, and M.J. Campagnole-Santos Immunofluorescence localization of the receptor Mas in cardiovascular-related areas of the rat brain Am. J. Physiol. Heart Circ. Physiol. 293 2007 H1416 H1424
2. W. Bild, and A. Ciobica Angiotensin-(1-7) central administration induces anxiolytic-like effects in elevated plus maze and decreased oxidative stress in the amygdala J. Affect Disord. 145 2013 165 171
3. A. Bystritsky Treatment-resistant anxiety disorders Mol. Psychiatry 11 2006 805 814
4. E. Castren, and J.M. Saavedra Repeated stress increases the density of angiotensin II binding sites in rat paraventricular nucleus and subfornical organ Endocrinology 122 1988 370 372
5. P.J. Davern, T.P. Nguyen-Huu, L. La Greca, A. Abdelkader, and G.A. Head Role of the sympathetic nervous system in Schlager genetically hypertensive mice Hypertension 54 2009 852 859
6. M. Davis The role of the amygdala in fear and anxiety Annu. Rev. Neurosci. 15 1992 353 375
7. M. Davis, D.L. Walker, L. Miles, and C. Grillon Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety Neuropsychopharmacology 35 2010 105 135
8. A.D. de Kloet, D. Pati, L. Wang, H. Hiller, C. Sumners, C.J. Frazier, R.J. Seeley, J.P. Herman, S.C. Woods, and E.G. Krause Angiotensin type 1a receptors in the paraventricular nucleus of the hypothalamus protect against diet-induced obesity J. Neurosci. 33 2013 4825 4833
9. A.D. de Kloet, D.J. Pioquinto, D. Nguyen, L. Wang, J.A. Smith, H. Hiller, and C. Sumners Obesity induces neuroinflammation mediated by altered expression of the renin-angiotensin system in mouse forebrain nuclei Physiol. Behav. 136 2014 31 38
10. A.D. de Kloet, L. Wang, J.A. Ludin, J.A. Smith, D.J. Pioquinto, H. Hiller, U.M. Steckelings, D.A. Scheuer, C. Sumners, and E.G. Krause Reporter mouse strain provides a novel look at angiotensin type-2 receptor distribution in the central nervous system, Brain Struct Funct 2014 1 22
11. M.F. Doobay, L.S. Talman, T.D. Obr, X. Tian, R.L. Davisson, and E. Lazartigues Differential expression of neuronal ACE2 in transgenic mice with overexpression of the brain renin-angiotensin system Am. J. Physiol. Regul. Integr. Comp. Physiol. 292 2007 R373 R381
12. S. Duvarci, and D. Pare Glucocorticoids enhance the excitability of principal basolateral amygdala neurons J. Neurosci. 27 2007 4482 4491
13. A.C. Felix-Ortiz, A. Beyeler, C. Seo, C.A. Leppla, C.P. Wildes, and K.M. Tye BLA to vHPC inputs modulate anxiety-related behaviors Neuron 79 2013 658 664
14. A.J. Ferreira, J.A. Hernandez Prada, D.A. Ostrov, and M.K. Raizada Cardiovascular protection by angiotensin-converting enzyme 2: a new paradigm Future Cardiol. 4 2008 175 182
15. K. Franklin, and G. Paxinos The Mouse Brain in Stereotaxic Coordinates 2008
16. C.J. Frazier, D. Pati, H. Hiller, D. Nguyen, L. Wang, J.A. Smith, K. MacFadyen, A.D. de Kloet, and E.G. Krause Acute hypernatremia exerts an inhibitory oxytocinergic tone that is associated with anxiolytic mood in male rats Endocrinology 154 2013 2457 2467
17. M. Freund, T. Walther, von Bohlen, and O. Halbach Immunohistochemical localization of the angiotensin-(1-7) receptor Mas in the murine forebrain Cell Tissue Res. 348 2012 29 35
18. M. Furuhashi, N. Moniwa, T. Mita, T. Fuseya, S. Ishimura, K. Ohno, S. Shibata, M. Tanaka, Y. Watanabe, H. Akasaka, H. Ohnishi, H. Yoshida, H. Takizawa, S. Saitoh, N. Ura, K. Shimamoto, and T. Miura Urinary angiotensin-converting enzyme 2 in hypertensive patients may be increased by olmesartan, an angiotensin II receptor blocker Am. J. Hypertens. 28 2015 15 21
19. H. Gavras, H.R. Brunner, G.A. Turini, G.R. Kershaw, C.P. Tifft, S. Cuttelod, I. Gavras, R.A. Vukovich, and D.N. McKinstry Antihypertensive effect of the oral angiotensin converting-enzyme inhibitor SQ 14225 in man N. Engl. J. Med. 298 1978 991 995
20. J.L. Grobe, B.A. Buehrer, A.M. Hilzendeger, X. Liu, D.R. Davis, D. Xu, and C.D. Sigmund Angiotensinergic signaling in the brain mediates metabolic effects of deoxycorticosterone (DOCA)-salt in C57 mice Hypertension 57 2011 600 607
21. K.L. Jackson, K. Palma-Rigo, T.P. Nguyen-Huu, P.J. Davern, and G.A. Head Major contribution of the medial amygdala to hypertension in BPH/2J genetically hypertensive mice Hypertension 63 2014 811 818
22. L. Johannessen, U. Strudsholm, L. Foldager, and P. Munk-Jorgensen Increased risk of hypertension in patients with bipolar disorder and patients with anxiety compared to background population and patients with schizophrenia J. Affect Disord. 95 2006 13 17
23. L.M. Kangussu, A.F. Almeida-Santos, M. Bader, N. Alenina, M.A. Fontes, R.A. Santos, D.C. Aguiar, and M.J. Campagnole-Santos Angiotensin-(1-7) attenuates the anxiety and depression-like behaviors in transgenic rats with low brain angiotensinogen Behav. Brain Res. 257 2013 25 30
24. H. Kayano, S. Koba, T. Matsui, H. Fukuoka, T. Toshida, T. Sakai, Y. Akutsu, K. Tanno, E. Geshi, and Y. Kobayashi Anxiety disorder is associated with nocturnal and early morning hypertension with or without morning surge: ambulatory blood pressure monitoring Circ. J. 76 2012 1670 1677
25. R.C. Kessler, W.T. Chiu, O. Demler, K.R. Merikangas, and E.E. Walters Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication Arch. Gen. Psychiatry 62 2005 617 627
26. N.M. Khoury, P.J. Marvar, C.F. Gillespie, A. Wingo, A. Schwartz, B. Bradley, M. Kramer, and K.J. Ressler 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
27. Y. Kitahara, K. Imataka, H. Nakaoka, M. Ishibashi, T. Yamaji, and J. Fujii Hematocrit increase by mental stress in hypertensive patients Jpn. Heart J. 29 1988 429 435
28. E.G. Krause, A.D. de Kloet, J.N. Flak, M.D. Smeltzer, M.B. Solomon, N.K. Evanson, S.C. Woods, R.R. Sakai, and J.P. Herman Hydration state controls stress responsiveness and social behavior J. Neurosci. 31 2011 5470 5476
29. E.G. Krause, A.D. de Kloet, K.A. Scott, J.N. Flak, K. Jones, M.D. Smeltzer, Y.M. Ulrich-Lai, S.C. Woods, S.P. Wilson, L.P. Reagan, J.P. Herman, and R.R. Sakai Blood-borne angiotensin II acts in the brain to influence behavioral and endocrine responses to psychogenic stress J. Neurosci. 31 2011 15009 15015
30. E.G. Krause, S.J. Melhorn, J.F. Davis, K.A. Scott, L.Y. Ma, A.D. de Kloet, S.C. Benoit, S.C. Woods, and R.R. Sakai Angiotensin type 1 receptors in the subfornical organ mediate the drinking and hypothalamic-pituitary-adrenal response to systemic isoproterenol Endocrinology 149 2008 6416 6424
31. M. Luque, P. Martin, N. Martell, C. Fernandez, K.B. Brosnihan, and C.M. Ferrario Effects of captopril related to increased levels of prostacyclin and angiotensin-(1-7) in essential hypertension J. Hypertens. 14 1996 799 805
32. A. Martins Lima, C.H. Xavier, A.J. Ferreira, M.K. Raizada, G. Wallukat, E.P. Velloso, R.A. dos Santos, and M.A. Fontes Activation of angiotensin-converting enzyme 2/angiotensin-(1-7)/Mas axis attenuates the cardiac reactivity to acute emotional stress Am. J. Physiol. Heart Circ. Physiol. 305 2013 H1057 H1067
33. P.J. Marvar, J. Goodman, S. Fuchs, D.C. Choi, S. Banerjee, and K.J. Ressler Angiotensin type 1 receptor inhibition enhances the extinction of fear memory Biol. Psychiatry 75 2014 864 872
34. F.G. Morrison, and K.J. Ressler From the neurobiology of extinction to improved clinical treatments Depress. Anxiety 31 2014 279 290
35. L. Paul, P. Jeemon, J. Hewitt, L. McCallum, P. Higgins, M. Walters, J. McClure, J. Dawson, P. Meredith, G.C. Jones, S. Muir, A.F. Dominiczak, G. Lowe, G.T. McInnes, and S. Padmanabhan Hematocrit predicts long-term mortality in a nonlinear and sex-specific manner in hypertensive adults Hypertension 60 2012 631 638
36. Y. Qi, J. Zhang, C.T. Cole-Jeffrey, V. Shenoy, A. Espejo, M. Hanna, C. Song, C.J. Pepine, M.J. Katovich, and M.K. Raizada Diminazene aceturate enhances angiotensin-converting enzyme 2 activity and attenuates ischemia-induced cardiac pathophysiology Hypertension 62 2013 746 752
37. Y. Qi, J. Zhang, L. Wang, V. Shenoy, E. Krause, S.P. Oh, C.J. Pepine, M.J. Katovich, and M.K. Raizada Angiotensin-converting enzyme 2 inhibits high-mobility group box 1 and attenuates cardiac dysfunction post-myocardial ischemia J. Mol. Med. (Berl.) 2015 1 13
38. D.G. Rainnie, E.K. Asprodini, and P. Shinnick-Gallagher Intracellular recordings from morphologically identified neurons of the basolateral amygdala J. Neurophysiol. 69 1993 1350 1362
39. J.M. Saavedra, H. Ando, I. Armando, G. Baiardi, C. Bregonzio, A. Juorio, and M. Macova Anti-stress and anti-anxiety effects of centrally acting angiotensin II AT1 receptor antagonists Regul. Pept. 128 2005 227 238
40. J.M. Saavedra, and J. Benicky Brain and peripheral angiotensin II play a major role in stress Stress 10 2007 185 193
41. J.M. Saavedra, E. Sanchez-Lemus, and J. Benicky Blockade of brain angiotensin II AT1 receptors ameliorates stress, anxiety, brain inflammation and ischemia: therapeutic implications Psychoneuroendocrinology 36 2011 1 18
42. V. Shenoy, A. Gjymishka, Y.P. Jarajapu, Y. Qi, A. Afzal, K. Rigatto, A.J. Ferreira, R.A. Fraga-Silva, P. Kearns, J.Y. Douglas, D. Agarwal, K.K. Mubarak, C. Bradford, W.R. Kennedy, J.Y. Jun, A. Rathinasabapathy, E. Bruce, D. Gupta, A.J. Cardounel, J. Mocco, J.M. Patel, J. Francis, M.B. Grant, M.J. Katovich, and M.K. Raizada Diminazene attenuates pulmonary hypertension and improves angiogenic progenitor cell functions in experimental models Am. J. Respir. Crit. Care Med. 187 2013 648 657
43. J.A. Smith, L. Wang, H. Hiller, C.T. Taylor, A.D. de Kloet, and E.G. Krause Acute hypernatremia promotes anxiolysis and attenuates stress-induced activation of the hypothalamic-pituitary-adrenal axis in male mice Physiol. Behav. 136 2014 91 96
44. P.D. Sorlie, M.R. Garcia-Palmieri, R. Costas Jr., and R.J. Havlik Hematocrit and risk of coronary heart disease: the Puerto Rico Health Program Am. Heart J. 101 1981 456 461
45. R.C. Thurston, M. Rewak, and L.D. Kubzansky An anxious heart: anxiety and the onset of cardiovascular diseases Prog. Cardiovasc Dis. 55 2013 524 537
46. Z. Tian, Y. Wang, N. Zhang, Y.Y. Guo, B. Feng, S.B. Liu, and M.G. Zhao Estrogen receptor GPR30 exerts anxiolytic effects by maintaining the balance between GABAergic and glutamatergic transmission in the basolateral amygdala of ovariectomized mice after stress Psychoneuroendocrinology 38 2013 2218 2233
47. R.R. Townsend T.W. Post, Major Side Effects of Angiotensin-converting Enzyme Inhibitors and Angiotensin II Receptor Blockers 2015 (UpToDate, Waltham, MA)
48. K.M. Tye, R. Prakash, S.Y. Kim, L.E. Fenno, L. Grosenick, H. Zarabi, K.R. Thompson, V. Gradinaru, C. Ramakrishnan, and K. Deisseroth Amygdala circuitry mediating reversible and bidirectional control of anxiety Nature 471 2011 358 362
49. S. Uzun, O. Kozumplik, M. Jakovljevic, and B. Sedic Side effects of treatment with benzodiazepines Psychiatr. Danub. 22 2010 90 93
50. T. Walther, D. Balschun, J.P. Voigt, H. Fink, W. Zuschratter, C. Birchmeier, D. Ganten, and M. Bader Sustained long term potentiation and anxiety in mice lacking the Mas protooncogene J. Biol. Chem. 273 1998 11867 11873
51. H. Xia, and E. Lazartigues Angiotensin-converting enzyme 2: central regulator for cardiovascular function Curr. Hypertens. Rep. 12 2010 170 175
52. P. Xu, S. Sriramula, and E. Lazartigues ACE2/ANG-(1-7)/Mas pathway in the brain: the axis of good Am. J. Physiol. Regul. Integr. Comp. Physiol. 300 2011 R804 R817
53. K. Yamada, S.N. Iyer, M.C. Chappell, D. Ganten, and C.M. Ferrario Converting enzyme determines plasma clearance of angiotensin-(1-7) Hypertension 32 1998 496 502
54. V.K. Yeragani, K.A. Rao, M.R. Smitha, R.B. Pohl, R. Balon, and K. Srinivasan Diminished chaos of heart rate time series in patients with major depression Biol. Psychiatry 51 2002 733 744