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Review Article

Neuropsychiatric Properties of the ACE2/Ang-(1-7)/Mas Pathway: A Brief Review

Author(s): Leonardo Augusto de Melo and Ana Flávia Almeida-Santos*

Volume 27, Issue 6, 2020

Page: [476 - 483] Pages: 8

DOI: 10.2174/0929866527666191223143230

Price: $65

Abstract

The current pharmacological strategies for the management of anxiety disorders and depression, serious conditions which are gaining greater prevalence worldwide, depend on only two therapeutic classes of mood-stabilizing drugs: Serotonin Reuptake Inhibitors (SSRIs) and Serotonin-Norepinephrine Reuptake Inhibitors (SNRIs). Although first line agents with proven efficacy, their clinical success in the management of anxiety disorders and depression is still considered highly complex due to the multifaceted nature of such conditions. Several studies have shown a possible therapeutic target could be found in the form of the Angiotensin-Converting Enzyme [ACE] type 2 (ACE2), Angiotensin [Ang]-(1-7) and Mas receptor pathway of the Renin- Angiotensin System (RAS), which as will be discussed, has been described to exhibit promising therapeutic properties for the management of anxiety disorders and depression. In this article, the literature to describe recent findings related to the role of the RAS in anxiety and depression disorders was briefly revised. The literature used covers a time range from 1988 to 2019 and were acquired from the National Center for Biotechnology Information’s (NCBI) PubMed search engine. The results demonstrated in this review are promising and encourage the development of new research for the treatment of anxiety and depression disorders focusing on the RAS. In conclusion, the ACE2/Ang-(1-7)/Mas pathway may exhibit anxiolytic and anti-depressive effects through many possible biochemical mechanisms both centrally and peripherally, and result in highly promising mental health benefits which justifies further investigation into this system as a possible new therapeutic target in the management of neuropsychiatric disorders, including any as of yet undescribed risk-benefit analysis compared to currently-implemented pharmacological strategies.

Keywords: Anxiety, depression, pharmacotherapy, ACE2/Ang-(1-7)/Mas pathway, renin-angiotensin system, moodstabilizing drugs.

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[1]
Omran, A.R. The epidemiologic transition: a theory of the epidemiology of population change. 1971. Milbank Q., 2005, 83(4), 731-757.
[http://dx.doi.org/10.1111/j.1468-0009.2005.00398.x] [PMID: 16279965]
[2]
Prados-Torres, A.; Poblador-Plou, B.; Gimeno-Miguel, A.; Calderón-Larrañaga, A.; Poncel-Falcó, A.; Gimeno-Feliú, L.A.; González-Rubio, F.; Laguna-Berna, C.; Marta-Moreno, J.; Clerencia-Sierra, M.; Aza-Pascual-Salcedo, M.; Bandrés-Liso, A.C.; Coscollar-Santaliestra, C.; Pico-Soler, V.; Abad-Díez, J.M. Cohort profile: The epidemiology of chronic diseases and multimorbidity. The EpiChron Cohort Study. Int. J. Epidemiol., 2018, 47(2), 382-384f.
[http://dx.doi.org/10.1093/ije/dyx259] [PMID: 29346556]
[3]
Ionescu, D.F.; Niciu, M.J.; Henter, I.D.; Zarate, C.A. Defining anxious depression: a review of the literature. CNS Spectr., 2013, 18(5), 252-260.
[http://dx.doi.org/10.1017/S1092852913000114] [PMID: 23507190]
[4]
Khoury, N.M.; Marvar, P.J.; Gillespie, C.F.; Wingo, A.; Schwartz, A.; Bradley, B.; Kramer, M.; Ressler, K.J. 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, 2012, 73(6), 849-855.
[http://dx.doi.org/10.4088/JCP.11m07316] [PMID: 22687631]
[5]
Saavedra, J.M. Angiotensin II AT(1) receptor blockers as treatments for inflammatory brain disorders. Clin. Sci. (Lond.), 2012, 123(10), 567-590.
[http://dx.doi.org/10.1042/CS20120078] [PMID: 22827472]
[6]
Gironacci, M.M.; Vicario, A.; Cerezo, G.; Silva, M.G. The depressor axis of the renin-angiotensin system and brain disorders: a translational approach. Clin. Sci. (Lond.), 2018, 132(10), 1021-1038.
[http://dx.doi.org/10.1042/CS20180189] [PMID: 29802208]
[7]
Bild, W.; Ciobica, A. Angiotensin-(1-7) central administration induces anxiolytic-like effects in elevated plus maze and decreased oxidative stress in the amygdala. J. Affect. Disord., 2013, 145(2), 165-171.
[PMID: 22868060]
[8]
Liu, F.; Havens, J.; Yu, Q.; Wang, G.; Davisson, R.L.; Pickel, V.M.; Iadecola, C. The link between angiotensin II-mediated anxiety and mood disorders with NADPH oxidase-induced oxidative stress., Int. J. Physiol. Pathophysiol. Pharmacol., 2012, 4(1), 28-35.
[PMID: 22461954]
[9]
Marvar, P.J.; Goodman, J.; Fuchs, S.; Choi, D.C.; Banerjee, S.; Ressler, K.J. Angiotensin type 1 receptor inhibition enhances the extinction of fear memory. Biol. Psychiatry, 2014, 75(11), 864-872.https://dx.doi.org/10.1016%2Fj.biopsych.2013.08.024
[PMID: 24094510]
[10]
Etelvino, G.M.; Peluso, A.A.; Santos, R.A. New components of the renin-angiotensin system: Alamandine and the MAS-related G protein-coupled receptor D. Curr. Hypertens. Rep., 2014, 16(6), 433.
[PMID: 24760442]
[11]
von Bohlen und Halbach, O.; Albrecht, D. The CNS renin-angiotensin system. Cell Tissue Res., 2006, 326(2), 599-616.
[http://dx.doi.org/10.1007/s00441-006-0190-8] [PMID: 16555051]
[12]
Becker, L.K.; Etelvino, G.M.; Walther, T.; Santos, R.A.; Campagnole-Santos, M.J. Immunofluorescence localization of the receptor Mas in cardiovascular-related areas of the rat brain. Am. J. Physiol. Heart Circ. Physiol., 2007, 293(3), H1416-H1424.
[http://dx.doi.org/10.1152/ajpheart.00141.2007] [PMID: 17496218]
[13]
Santos, R.A. Angiotensin-(1-7). Hypertension, 2014, 63(6), 1138-1147.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.113.01274] [PMID: 24664288]
[14]
Wright, J.W.; Harding, J.W. Brain angiotensin receptor subtypes in the control of physiological and behavioral responses. Neurosci. Biobehav. Rev., 1994, 18(1), 21-53.
[http://dx.doi.org/10.1016/0149-7634(94)90034-5] [PMID: 8170622]
[15]
Doobay, M.F.; Talman, L.S.; Obr, T.D.; Tian, X.; Davisson, R.L.; Lazartigues, E. Differential expression of neuronal ACE2 in transgenic mice with overexpression of the brain renin-angiotensin system. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2007, 292(1), R373-R381.
[http://dx.doi.org/10.1152/ajpregu.00292.2006] [PMID: 16946085]
[16]
World Health Organization. Depression and Other Common Mental Disorders: Global Health Estimates 2017.
[17]
Bandelow, B.; Sher, L.; Bunevicius, R.; Hollander, E.; Kasper, S.; Zohar, J.; Möller, H.J.; Care, W.T.F.M.D.P. Guidelines for the pharmacological treatment of anxiety disorders, obsessive-compulsive disorder and posttraumatic stress disorder in primary care. Int. J. Psychiatry Clin. Pract., 2012, 16(2), 77-84.
[http://dx.doi.org/10.3109/13651501.2012.667114] [PMID: 22540422]
[18]
Bandelow, B.; Michaelis, S.; Wedekind, D. Treatment of anxiety disorders., Dialogues Clin. Neurosci., 2017, 19(2), 93-107.
[PMID: 28867934]
[19]
Sung, S.C.; Wisniewski, S.R.; Balasubramani, G.K.; Zisook, S.; Kurian, B.; Warden, D.; Trivedi, M.H.; Rush, A.J. Does early-onset chronic or recurrent major depression impact outcomes with antidepressant medications? A CO-MED trial report. Psychol. Med., 2013, 43(5), 945-960.
[http://dx.doi.org/10.1017/S0033291712001742] [PMID: 23228340]
[20]
Gelenberg, A.J. Optimizing depression treatment to increase the likelihood of remission. J. Clin. Psychiatry, 2010, 71(9)e22
[http://dx.doi.org/10.4088/JCP.9078tx2c] [PMID: 20923615]
[21]
Gelenberg, A.J. A review of the current guidelines for depression treatment. J. Clin. Psychiatry, 2010, 71(7)e15
[http://dx.doi.org/10.4088/JCP.9078tx1c] [PMID: 20667285]
[22]
Zuckerbrot, R.A.; Cheung, A.; Jensen, P.S.; Stein, R.E.K.; Laraque, D.; Glad-Pc Steering, G. Guidelines for Adolescent Depression in Primary Care (GLAD-PC): Part I. Practice preparation, identification, assessment, and initial management. Pediatrics, 2018, 141(3)e20174081
[http://dx.doi.org/10.1542/peds.2017-4081] [PMID: 29483200]
[23]
Thorlund, K.; Druyts, E.; Wu, P.; Balijepalli, C.; Keohane, D.; Mills, E. Comparative efficacy and safety of selective serotonin reuptake inhibitors and serotonin-norepinephrine reuptake inhibitors in older adults: a network meta-analysis. J. Am. Geriatr. Soc., 2015, 63(5), 1002-1009.
[http://dx.doi.org/10.1111/jgs.13395] [PMID: 25945410]
[24]
Ornoy, A.; Koren, G. SSRIs and SNRIs (SRI) in pregnancy: Effects on the course of pregnancy and the offspring: How far are we from having all the answers? Int. J. Mol. Sci., 2019, 20(10)E2370
[http://dx.doi.org/10.3390/ijms20102370] [PMID: 31091646]
[25]
Almeida-Santos, A.F.; Kangussu, L.M.; Campagnole-Santos, M.J. The renin-angiotensin system and the neurodegenerative diseases: A brief review. Protein Pept. Lett., 2017, 24(9), 841-853.
[http://dx.doi.org/10.2174/0929866524666170822120258] [PMID: 28828974]
[26]
Farag, E.; Sessler, D.I.; Ebrahim, Z.; Kurz, A.; Morgan, J.; Ahuja, S.; Maheshwari, K.; John Doyle, D. The renin angiotensin system and the brain: New developments. J. Clin. Neurosci., 2017, 46, 1-8.
[27]
Nishimura, H. Renin-angiotensin system in vertebrates: phylogenetic view of structure and function. Anat. Sci. Int., 2017, 92(2), 215-247.
[http://dx.doi.org/10.1007/s12565-016-0372-8] [PMID: 27718210]
[28]
Ren, L.; Lu, X.; Danser, A.H.J. Revisiting the brain renin-angiotensin system-focus on novel therapies. Curr. Hypertens. Rep., 2019, 21(4), 28.
[http://dx.doi.org/10.1007/s11906-019-0937-8] [PMID: 30949864]
[29]
Paul, M.; Poyan Mehr, A.; Kreutz, R. Physiology of local renin-angiotensin systems. Physiol. Rev., 2006, 86(3), 747-803.
[http://dx.doi.org/10.1152/physrev.00036.2005] [PMID: 16816138]
[30]
Patel, S.; Rauf, A.; Khan, H.; Abu-Izneid, T. Renin-angiotensin-aldosterone (RAAS): The ubiquitous system for homeostasis and pathologies. Biomed. Pharmacother., 2017, 94, 317-325.
[http://dx.doi.org/10.1016/j.biopha.2017.07.091] [PMID: 28772209]
[31]
Nunes-Silva, A.; Rocha, G.C.; Magalhaes, D.M.; Vaz, L.N.; Salviano de Faria, M.H.; Simoes E Silva, A.C. Physical exercise and ACE2-Angiotensin-(1-7)-Mas receptor axis of the renin angiotensin system. Protein Pept. Lett., 2017, 24(9), 809-816.
[PMID: 28758593]
[32]
Wang, L.; de Kloet, A.D.; Pati, D.; Hiller, H.; Smith, J.A.; Pioquinto, D.J.; Ludin, J.A.; Oh, S.P.; Katovich, M.J.; Frazier, C.J.; Raizada, M.K.; Krause, E.G. Increasing brain angiotensin converting enzyme 2 activity decreases anxiety-like behavior in male mice by activating central Mas receptors. Neuropharmacology, 2016, 105, 114-123.
[http://dx.doi.org/10.1016/j.neuropharm.2015.12.026] [PMID: 26767952]
[33]
Gard, P.R. Angiotensin as a target for the treatment of Alzheimer’s disease, anxiety and depression. Expert Opin. Ther. Targets, 2004, 8(1), 7-14.
[http://dx.doi.org/10.1517/14728222.8.1.7] [PMID: 14996614]
[34]
de Kloet, A.D.; Wang, L.; Pitra, S.; Hiller, H.; Smith, J.A.; Tan, Y.; Nguyen, D.; Cahill, K.M.; Sumners, C.; Stern, J.E.; Krause, E.G. A unique “Angiotensin-Sensitive” neuronal population coordinates neuroendocrine, cardiovascular, and behavioral responses to Stress. J. Neurosci., 2017, 37(13), 3478-3490.
[http://dx.doi.org/10.1523/JNEUROSCI.3674-16.2017] [PMID: 28219987]
[35]
Bali, A.; Jaggi, A.S. Angiotensin as stress mediator: role of its receptor and interrelationships among other stress mediators and receptors. Pharmacol. Res., 2013, 76, 49-57.
[http://dx.doi.org/10.1016/j.phrs.2013.07.004] [PMID: 23892268]
[36]
Schleifenbaum, J. Alamandine and its receptor MrgD pair up to join the protective arm of the renin-angiotensin system. Front. Med. (Lausanne), 2019, 6, 107.
[http://dx.doi.org/10.3389/fmed.2019.00107] [PMID: 31245374]
[37]
Lautner, R.Q.; Villela, D.C.; Fraga-Silva, R.A.; Silva, N.; Verano-Braga, T.; Costa-Fraga, F.; Jankowski, J.; Jankowski, V.; Sousa, F.; Alzamora, A.; Soares, E.; Barbosa, C.; Kjeldsen, F.; Oliveira, A.; Braga, J.; Savergnini, S.; Maia, G.; Peluso, A.B.; Passos-Silva, D.; Ferreira, A.; Alves, F.; Martins, A.; Raizada, M.; Paula, R.; Motta-Santos, D.; Klempin, F.; Pimenta, A.; Alenina, N.; Sinisterra, R.; Bader, M.; Campagnole-Santos, M.J.; Santos, R.A. Discovery and characterization of alamandine: a novel component of the renin-angiotensin system. Circ. Res., 2013, 112(8), 1104-1111.
[http://dx.doi.org/10.1161/CIRCRESAHA.113.301077] [PMID: 23446738]
[38]
Santos, R.A.; Brosnihan, K.B.; Chappell, M.C.; Pesquero, J.; Chernicky, C.L.; Greene, L.J.; Ferrario, C.M. Converting enzyme activity and angiotensin metabolism in the dog brainstem. Hypertension, 1988, 11(2 Pt 2), I153-I157.
[http://dx.doi.org/10.1161/01.HYP.11.2_Pt_2.I153] [PMID: 2831145]
[39]
Ferrario, C.M.; Santos, R.A.; Brosnihan, K.B.; Block, C.H.; Schiavone, M.T.; Khosla, M.C.; Greene, L.J. A hypothesis regarding the function of angiotensin peptides in the brain. Clin. Exp. Hypertens. A, 1988, 10(Suppl. 1), 107-121.
[http://dx.doi.org/10.3109/10641968809075966] [PMID: 3072120]
[40]
Chappell, M.C.; Brosnihan, K.B.; Diz, D.I.; Ferrario, C.M. Identification of angiotensin-(1-7) in rat brain. Evidence for differential processing of angiotensin peptides. J. Biol. Chem., 1989, 264(28), 16518-16523.
[PMID: 2777795]
[41]
Kalra, J.; Prakash, A.; Kumar, P.; Majeed, A.B. Cerebroprotective effects of RAS inhibitors: Beyond their cardio-renal actions. J. Renin Angiotensin Aldosterone Syst., 2015, 16(3), 459-468.
[http://dx.doi.org/10.1177/1470320315583582] [PMID: 25944853]
[42]
Mertens, B.; Vanderheyden, P.; Michotte, Y.; Sarre, S. The role of the central renin-angiotensin system in Parkinson’s disease. J. Renin Angiotensin Aldosterone Syst., 2010, 11(1), 49-56.
[http://dx.doi.org/10.1177/1470320309347789] [PMID: 19861346]
[43]
Savaskan, E.; Hock, C.; Olivieri, G.; Bruttel, S.; Rosenberg, C.; Hulette, C.; Müller-Spahn, F. Cortical alterations of angiotensin converting enzyme, angiotensin II and AT1 receptor in Alzheimer’s dementia. Neurobiol. Aging, 2001, 22(4), 541-546.
[http://dx.doi.org/10.1016/S0197-4580(00)00259-1] [PMID: 11445253]
[44]
Braszko, J.J. Valsartan abolishes most of the memory-improving effects of intracerebroventricular angiotensin II in rats. Clin. Exp. Hypertens., 2005, 27(8), 635-649.
[http://dx.doi.org/10.1080/10641960500298723] [PMID: 16303640]
[45]
Lovrecić, L.; Ristić, S.; Starcević-Cizmarević, N.; Jazbec, S.S.; Sepcić, J.; Kapović, M.; Peterlin, B. Angiotensin-converting enzyme I/D gene polymorphism and risk of multiple sclerosis. Acta Neurol. Scand., 2006, 114(6), 374-377.
[http://dx.doi.org/10.1111/j.1600-0404.2006.00711.x] [PMID: 17083336]
[46]
Kawajiri, M.; Mogi, M.; Higaki, N.; Matsuoka, T.; Ohyagi, Y.; Tsukuda, K.; Kohara, K.; Horiuchi, M.; Miki, T.; Kira, J.I. Angiotensin-converting enzyme (ACE) and ACE2 levels in the cerebrospinal fluid of patients with multiple sclerosis. Mult. Scler., 2009, 15(2), 262-265.
[http://dx.doi.org/10.1177/1352458508097923] [PMID: 19136547]
[47]
Lee, D.H.; Heidecke, H.; Schröder, A.; Paul, F.; Wachter, R.; Hoffmann, R.; Ellrichmann, G.; Dragun, D.; Waschbisch, A.; Stegbauer, J.; Klotz, P.; Gold, R.; Dechend, R.; Müller, D.N.; Saft, C.; Linker, R.A. Increase of angiotensin II type 1 receptor auto-antibodies in Huntington’s disease. Mol. Neurodegener., 2014, 9, 49.
[http://dx.doi.org/10.1186/1750-1326-9-49] [PMID: 25398321]
[48]
Lazaroni, T.L.; Bastos, C.P.; Moraes, M.F.; Santos, R.S.; Pereira, G.S. Angiotensin-(1-7)/Mas axis modulates fear memory and extinction in mice. Neurobiol. Learn. Mem., 2016, 127, 27-33.
[http://dx.doi.org/10.1016/j.nlm.2015.11.012] [PMID: 26642920]
[49]
Kangussu, L.M.; Almeida-Santos, A.F.; Moreira, F.A.; Fontes, M.A.P.; Santos, R.A.S.; Aguiar, D.C.; Campagnole-Santos, M.J. Reduced anxiety-like behavior in transgenic rats with chronically overproduction of angiotensin-(1-7): Role of the Mas receptor. Behav. Brain Res., 2017, 331, 193-198.
[http://dx.doi.org/10.1016/j.bbr.2017.05.026] [PMID: 28502733]
[50]
Almeida-Santos, A.F.; Kangussu, L.M.; Moreira, F.A.; Santos, R.A.; Aguiar, D.C.; Campagnole-Santos, M.J. Anxiolytic- and antidepressant-like effects of angiotensin-(1-7) in hypertensive transgenic (mRen2)27 rats. Clin. Sci. (Lond.), 2016, 130(14), 1247-1255.
[http://dx.doi.org/10.1042/CS20160116] [PMID: 27129185]
[51]
Moura Santos, D.; Ribeiro Marins, F.; Limborço-Filho, M.; de Oliveira, M.L.; Hamamoto, D.; Xavier, C.H.; Moreira, F.A.; Santos, R.A.; Campagnole-Santos, M.J.; Peliky Fontes, M.A. Chronic overexpression of angiotensin-(1-7) in rats reduces cardiac reactivity to acute stress and dampens anxious behavior. Stress, 2017, 20(2), 189-196.
[http://dx.doi.org/10.1080/10253890.2017.1296949] [PMID: 28288545]
[52]
Saab, Y.B.; Gard, P.R.; Yeoman, M.S.; Mfarrej, B.; El-Moalem, H.; Ingram, M.J. Renin-angiotensin-system gene polymorphisms and depression. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2007, 31(5), 1113-1118.
[http://dx.doi.org/10.1016/j.pnpbp.2007.04.002] [PMID: 17499413]
[53]
Gard, P.R.; Mandy, A.; Sutcliffe, M.A. Evidence of a possible role of altered angiotensin function in the treatment, but not etiology, of depression. Biol. Psychiatry, 1999, 45(8), 1030-1034.
[http://dx.doi.org/10.1016/S0006-3223(98)00101-2] [PMID: 10386186]
[54]
Gard, P.R.; Mandy, A.; Whiting, J.M.; Nickels, D.P.; Meakin, A.J. Reduction of responses to angiotensin II by antidepressant drugs. Eur. J. Pharmacol., 1994, 264(3), 295-300.
[http://dx.doi.org/10.1016/0014-2999(94)00481-1] [PMID: 7698168]
[55]
Deicken, R.F. Captopril treatment of depression. Biol. Psychiatry, 1986, 21(14), 1425-1428.
[http://dx.doi.org/10.1016/0006-3223(86)90334-3] [PMID: 3539210]
[56]
Germain, L.; Chouinard, G. Treatment of recurrent unipolar major depression with captopril. Biol. Psychiatry, 1988, 23(6), 637-641.
[http://dx.doi.org/10.1016/0006-3223(88)90010-8] [PMID: 3281718]
[57]
Zubenko, G.S.; Nixon, R.A. Mood-elevating effect of captopril in depressed patients. Am. J. Psychiatry, 1984, 141(1), 110-111.
[http://dx.doi.org/10.1176/ajp.141.1.110] [PMID: 6318579]
[58]
Walther, T.; Balschun, D.; Voigt, J.P.; Fink, H.; Zuschratter, W.; Birchmeier, C.; Ganten, D.; Bader, M. Sustained long term potentiation and anxiety in mice lacking the Mas protooncogene. J. Biol. Chem., 1998, 273(19), 11867-11873.
[http://dx.doi.org/10.1074/jbc.273.19.11867] [PMID: 9565612]
[59]
Kangussu, L.M.; Almeida-Santos, A.F.; Bader, M.; Alenina, N.; Fontes, M.A.; Santos, R.A.; Aguiar, D.C.; Campagnole-Santos, M.J. Angiotensin-(1-7) attenuates the anxiety and depression-like behaviors in transgenic rats with low brain angiotensinogen. Behav. Brain Res., 2013, 257, 25-30.
[http://dx.doi.org/10.1016/j.bbr.2013.09.003]
[60]
Cryan, J.F.; Markou, A.; Lucki, I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol. Sci., 2002, 23(5), 238-245.
[PMID: 12008002]
[61]
Porsolt, R.D.; Le Pichon, M.; Jalfre, M. Depression: a new animal model sensitive to antidepressant treatments. Nature, 1977, 266(5604), 730-732.
[http://dx.doi.org/10.1038/266730a0] [PMID: 559941]
[62]
Handley, S.L.; Mithani, S. Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of ‘fear’-motivated behaviour. Naunyn Schmiedebergs Arch. Pharmacol., 1984, 327(1), 1-5.
[http://dx.doi.org/10.1007/BF00504983] [PMID: 6149466]
[63]
Martin, P.; Massol, J.; Puech, A.J. Captopril as an antidepressant? Effects on the learned helplessness paradigm in rats. Biol. Psychiatry, 1990, 27(9), 968-974.
[http://dx.doi.org/10.1016/0006-3223(90)90034-Y] [PMID: 2185850]
[64]
Belcheva, I.; Chobanova, M.; Georgiev, V. Differential behavioral effects of angiotensin II microinjected unilaterally into the CA1 hippocampal area. Regul. Pept., 1998, 74(2-3), 67-71.
[http://dx.doi.org/10.1016/S0167-0115(98)00015-9] [PMID: 9712165]
[65]
Voigt, J.P.; Hörtnagl, H.; Rex, A.; van Hove, L.; Bader, M.; Fink, H. Brain angiotensin and anxiety-related behavior: the transgenic rat TGR(ASrAOGEN)680. Brain Res., 2005, 1046(1-2), 145-156.
[http://dx.doi.org/10.1016/j.brainres.2005.03.048] [PMID: 15869747]
[66]
P.R., Gard The role of angiotensin II in cognition and behaviour. Eur. J. Pharmacol., 2002, 438(1-2), 1-14.
[PMID: 11906704]
[67]
Vian, J.; Pereira, C.; Chavarria, V.; Köhler, C.; Stubbs, B.; Quevedo, J.; Kim, S.W.; Carvalho, A.F.; Berk, M.; Fernandes, B.S. The renin-angiotensin system: a possible new target for depression. BMC Med., 2017, 15(1), 144.
[http://dx.doi.org/10.1186/s12916-017-0916-3] [PMID: 28760142]
[68]
Fontes, M.A.; Martins Lima, A.; Santos, R.A. Brain angiotensin-(1-7)/Mas axis: A new target to reduce the cardiovascular risk to emotional stress. Neuropeptides, 2016, 56, 9-17.
[http://dx.doi.org/10.1016/j.npep.2015.10.003] [PMID: 26584971]
[69]
Pereira, V.H.; Cerqueira, J.J.; Palha, J.A.; Sousa, N. Stressed brain, diseased heart: a review on the pathophysiologic mechanisms of neurocardiology. Int. J. Cardiol., 2013, 166(1), 30-37.
[http://dx.doi.org/10.1016/j.ijcard.2012.03.165] [PMID: 22521375]
[70]
Song, H.; Fang, F.; Arnberg, F.K.; Mataix-Cols, D.; Fernández de la Cruz, L.; Almqvist, C.; Fall, K.; Lichtenstein, P.; Thorgeirsson, G.; Valdimarsdóttir, U.A. Stress related disorders and risk of cardiovascular disease: population based, sibling controlled cohort study. BMJ, 2019, 365, l1255.
[http://dx.doi.org/10.1136/bmj.l1255] [PMID: 30971390]
[71]
Yu, X.J.; Miao, Y.W.; Li, H.B.; Su, Q.; Liu, K.L.; Fu, L.Y.; Hou, Y.K.; Shi, X.L.; Li, Y.; Mu, J.J.; Chen, W.S.; Cui, W.; Zhu, G.Q.; Ebenezer, P.J.; Francis, J.; Kang, Y.M. Blockade of endogenous angiotensin-(1-7) in hypothalamic paraventricular nucleus attenuates high salt-induced sympathoexcitation and hypertension. Neurosci. Bull., 2019, 35(1), 47-56.
[http://dx.doi.org/10.1007/s12264-018-0297-4] [PMID: 30328008]
[72]
Ren, X.; Zhang, F.; Zhao, M.; Zhao, Z.; Sun, S.; Fraidenburg, D.R.; Tang, H.; Han, Y. Angiotensin-(1-7) in paraventricular nucleus contributes to the enhanced cardiac sympathetic afferent reflex and sympathetic activity in chronic heart failure rats. Cell. Physiol. Biochem., 2017, 42(6), 2523-2539.
[http://dx.doi.org/10.1159/000480214] [PMID: 28848201]
[73]
A.J., Miller; A.C., Arnold The renin-angiotensin system in cardiovascular autonomic control: Recent developments and clinical implications. Clin. Auton. Res., 2019, 29(2), 231-243.
[PMID: 30413906]
[74]
de Morais, S.D.B.; Shanks, J.; Zucker, I.H. Integrative physiological aspects of brain RAS in hypertension. Curr. Hypertens. Rep., 2018, 20(2), 10.
[http://dx.doi.org/10.1007/s11906-018-0810-1] [PMID: 29480460]
[75]
Dartora, D.R.; Irigoyen, M.C.; Casali, K.R.; Moraes-Silva, I.C.; Bertagnolli, M.; Bader, M.; Santos, R.A.S. Improved cardiovascular autonomic modulation in transgenic rats expressing an Ang-(1-7)-producing fusion protein. Can. J. Physiol. Pharmacol., 2017, 95(9), 993-998.
[http://dx.doi.org/10.1139/cjpp-2016-0557] [PMID: 28459154]
[76]
Santos, R.A.; Haibara, A.S.; Campagnole-Santos, M.J.; Simões e Silva, A.C.; Paula, R.D.; Pinheiro, S.V.; Leite, M.F.; Lemos, V.S.; Silva, D.M.; Guerra, M.T.; Khosla, M.C. Characterization of a new selective antagonist for angiotensin-(1-7), D-pro7-angiotensin-(1-7). Hypertension, 2003, 41(3 Pt 2), 737-743.
[http://dx.doi.org/10.1161/01.HYP.0000052947.60363.24] [PMID: 12623989]
[77]
Park, B.M.; Phuong, H.T.A.; Yu, L.; Kim, S.H. Alamandine protects the heart against reperfusion injury via the MrgD receptor. Circ. J., 2018, 82(10), 2584-2593.
[http://dx.doi.org/10.1253/circj.CJ-17-1381] [PMID: 29998915]

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