ACE2/angiotensin-(1–7)/mas receptor axis in the central nervous system

Carregando...
Imagem de Miniatura
Citações na Scopus
1
Tipo de produção
bookPart
Data de publicação
2023
Título da Revista
ISSN da Revista
Título do Volume
Editora
ELSEVIER
Autores
ROCHA, N. P.
RACHID, M. A.
TEIXEIRA, A. L.
MIRANDA, A. S. de
Citação
Brito-Toscano, E. C.; Rocha, N. P.; Rachid, M. A.; Teixeira, A. L.; de Miranda, A. S.. ACE2/angiotensin-(1–7)/mas receptor axis in the central nervous system. In: . Angiotensin: From the Kidney to Coronavirus: ELSEVIER, 2023. p.545-565.
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
The renin–angiotensin system (RAS) is classically conceived as a circulating hormonal system involved in cardiovascular and renal homeostasis. The discovery that RAS components are locally expressed in the brain tissue pointed out to a role for this system in the pathophysiology of neuropsychiatric diseases, including mood disorders and neurodegenerative and cerebrovascular illnesses. The RAS counterregulatory axis composed by the angiotensin-converting enzyme 2 (ACE2), angiotensin-(1–7) (Ang-(1–7)), and Mas receptor mediates, among others, antiinflammatory, antioxidant, and antiapoptotic processes, frequently opposing the classical RAS arm (ACE/Ang II/AT1 receptor) actions. Accumulating evidence has supported protective roles of the ACE2/Ang-(1–7)/Mas receptor axis in the brain. Herein, we will discuss emerging evidence regarding the role of RAS, mainly focusing in the ACE2-Ang-(1–7)-Mas receptor arm, in brain physiology and pathophysiology. We will also report current experimental and clinical evidence in relation to ACE2 stimulation and Mas receptor agonists as potential therapeutic targets for neuropsychiatric diseases. © 2023 Elsevier Inc. All rights reserved.
Palavras-chave
Angiotensin-(1–7), Angiotensin-converting enzyme, Brain, Cerebrovascular diseases, Mas receptor, Mood disorders, Neurodegenerative diseases, Renin–angiotensin system
Referências
  1. Paul M., Poyan Mehr A., Kreutz R., Physiology of local renin-angiotensin systems, Physiol Rev, 86, 3, pp. 747-803, (2006)
  2. Fyhrquist F., Saijonmaa O., Renin-angiotensin system revisited, J Intern Med, 264, 3, pp. 224-236, (2008)
  3. Santos R.A., Ferreira A.J., Simoes e Silva A.C., Recent advances in the angiotensin-converting enzyme 2–angiotensin (1–7)–Mas axis, Exp Physiol, 93, 5, pp. 519-527, (2008)
  4. Tipnis S.R., Hooper N.M., Hyde R., Karran E., Christie G., Turner A.J., A human homolog of angiotensin-converting enzyme: cloning and functional expression as a captopril-insensitive carboxypeptidase, J Biol Chem, 275, 43, pp. 33238-33243, (2000)
  5. Santos R.A., e Silva A.C.S., Maric C., Silva D.M., Machado R.P., de Buhr I., Et al., Angiotensin-(1–7) is an endogenous ligand for the G protein-coupled receptor Mas, Proc Natl Acad Sci USA, 100, 14, pp. 8258-8263, (2003)
  6. Simoes e Silva A.C., Flynn J.T., The renin–angiotensin–aldosterone system in 2011: role in hypertension and chronic kidney disease, Pediatr Nephrol, 27, 10, pp. 1835-1845, (2012)
  7. Rodrigues Prestes T.R., Rocha N.P., Miranda A.S., Teixeira A.L., Simoes-e-Silva A.C., The anti-inflammatory potential of ACE2/angiotensin-(1–7)/mas receptor axis: evidence from basic and clinical research, Curr Drug Targets, 18, 11, pp. 1301-1313, (2017)
  8. Kamo T., Akazawa H., Komuro I., Pleiotropic effects of angiotensin II receptor signaling in cardiovascular homeostasis and aging, Int Heart J, 56, 3, pp. 249-254, (2015)
  9. Rabie M.A., Abd El Fattah M.A., Nassar N.N., Abdallah D.M., El-Abhar H.S., Correlation between angiotensin 1–7-mediated Mas receptor expression with motor improvement, activated STAT3/SOCS3 cascade, and suppressed HMGB-1/RAGE/NF-kappaB signaling in 6-hydroxydopamine hemiparkinsonian rats, Biochem Pharmacol, 171, (2020)
  10. Rocha N.P., Simoes e Silva A.C., Prestes T.R., Feracin V., Machado C.A., Ferreira R.N., Et al., RAS in the central nervous system: potential role in neuropsychiatric disorders, Curr Med Chem, 25, 28, pp. 3333-3352, (2018)
  11. Meira-Lima I.V., Pereira A.C., Mota G.F., Krieger J.E., Vallada H., Angiotensinogen and angiotensin converting enzyme gene polymorphisms and the risk of bipolar affective disorder in humans, Neurosci Lett, 293, 2, pp. 103-106, (2000)
  12. Murray C.J., Lopez A.D., Measuring the global burden of disease, N Engl J Med, 369, 5, pp. 448-457, (2013)
  13. Roth G.A., Johnson C.O., Nguyen G., Naghavi M., Feigin V.L., Murray C.J., Et al., Methods for estimating the global burden of cerebrovascular diseases, Neuroepidemiology, 45, 3, pp. 146-151, (2015)
  14. Thone-Reineke C., Steckelings U.M., Unger T., Angiotensin receptor blockers and cerebral protection in stroke, J Hypertens, 24, pp. S115-S121, (2006)
  15. Nishimura Y., Ito T., Saavedra J.M., Angiotensin II AT1 blockade normalizes cerebrovascular autoregulation and reduces cerebral ischemia in spontaneously hypertensive rats, Stroke
  16. a journal of cerebral circulation, 31, 10, pp. 2478-2486, (2000)
  17. Regenhardt R.W., Bennion D.M., Sumners C., Cerebroprotective action of angiotensin peptides in stroke, Clin Sci, 126, 3, pp. 195-205, (2014)
  18. Kangussu L.M., Marzano L.A., Souza C.F., Dantas C.C., Miranda A.S., Simoes e Silva A.C., The renin-angiotensin system and the cerebrovascular diseases: experimental and clinical evidence, Protein Pept Lett, 27, 6, pp. 463-475, (2020)
  19. Jackson L., Eldahshan W., Fagan S.C., Ergul A., Within the brain: the renin angiotensin system, Int J Mol Sci, 19, 3, (2018)
  20. Lu J., Jiang T., Wu L., Gao L., Wang Y., Zhou F., Et al., The expression of angiotensin-converting enzyme 2–angiotensin-(1–7)–Mas receptor axis are upregulated after acute cerebral ischemic stroke in rats, Neuropeptides, 47, 5, pp. 289-295, (2013)
  21. Bennion D.M., Haltigan E.A., Irwin A.J., Donnangelo L.L., Regenhardt R.W., Pioquinto D.J., Et al., Activation of the neuroprotective angiotensin-converting enzyme 2 in rat ischemic stroke, Hypertension, 66, 1, pp. 141-148, (2015)
  22. Bennion D.M., Rosado C.A., Haltigan E.A., Regenhardt R.W., Sumners C., Waters M.F., Serum activity of angiotensin converting enzyme 2 is decreased in patients with acute ischemic stroke, J Renin-Angiotensin-Aldosterone Syst JRAAS, 17, 3, (2016)
  23. Mecca A.P., Regenhardt R.W., O'Connor T.E., Joseph J.P., Raizada M.K., Katovich M.J., Et al., Cerebroprotection by angiotensin-(1–7) in endothelin-1-induced ischaemic stroke, Exp Physiol, 96, 10, pp. 1084-1096, (2011)
  24. Bennion D.M., Jones C.H., Donnangelo L.L., Graham J.T., Isenberg J.D., Dang A.N., Et al., Neuroprotection by post-stroke administration of an oral formulation of angiotensin-(1–7) in ischaemic stroke, Exp Physiol, 103, 6, pp. 916-923, (2018)
  25. Chen J., Zhao Y., Chen S., Wang J., Xiao X., Ma X., Et al., Neuronal over-expression of ACE2 protects brain from ischemia-induced damage, Neuropharmacology, 79, pp. 550-558, (2014)
  26. Zhang Y., Lu J., Shi J., Lin X., Dong J., Zhang S., Et al., Central administration of angiotensin-(1–7) stimulates nitric oxide release and upregulates the endothelial nitric oxide synthase expression following focal cerebral ischemia/reperfusion in rats, Neuropeptides, 42, 5-6, pp. 593-600, (2008)
  27. Jiang M.H., Kaku T., Hada J., Hayashi Y., Different effects of eNOS and nNOS inhibition on transient forebrain ischemia, Brain Res, 946, 1, pp. 139-147, (2002)
  28. Moro M.A., Cardenas A., Hurtado O., Leza J., Lizasoain I., Role of nitric oxide after brain ischaemia, Cell Calcium, 36, 3-4, pp. 265-275, (2004)
  29. Jiang T., Yu J.T., Zhu X.C., Zhang Q.Q., Tan M.S., Cao L., Et al., Angiotensin-(1–7) induces cerebral ischaemic tolerance by promoting brain angiogenesis in a M as/eNOS-dependent pathway, Br J Pharmacol, 171, 18, pp. 4222-4232, (2014)
  30. Jiang T., Gao L., Guo J., Lu J., Wang Y., Zhang Y., Suppressing inflammation by inhibiting the NF-κB pathway contributes to the neuroprotective effect of angiotensin-(1-7) in rats with permanent cerebral ischaemia, Br J Pharmacol, 167, 7, pp. 1520-1532, (2012)
  31. Regenhardt R.W., Desland F., Mecca A.P., Pioquinto D.J., Afzal A., Mocco J., Et al., Anti-inflammatory effects of angiotensin-(1–7) in ischemic stroke, Neuropharmacology, 71, pp. 154-163, (2013)
  32. Zheng J.L., Li G.Z., Chen S.Z., Wang J.J., Olson J.E., Xia H.J., Et al., Angiotensin converting enzyme 2/Ang-(1–7)/mas Axis protects brain from ischemic injury with a tendency of age-dependence, CNS Neurosci Ther, 20, 5, pp. 452-459, (2014)
  33. Inci S., Spetzler R.F., Intracranial aneurysms and arterial hypertension: a review and hypothesis, Surg Neurol, 53, 6, pp. 530-542, (2000)
  34. Silva R.A.P., Chu Y., Miller J.D., Mitchell I.J., Penninger J.M., Faraci F.M., Et al., Impact of ACE2 deficiency and oxidative stress on cerebrovascular function with aging, Stroke
  35. a journal of cerebral circulation, 43, 12, pp. 3358-3363, (2012)
  36. Kissela B.M., Sauerbeck L., Woo D., Khoury J., Carrozzella J., Pancioli A., Et al., Subarachnoid hemorrhage: a preventable disease with a heritable component, Stroke
  37. a journal of cerebral circulation, 33, 5, pp. 1321-1326, (2002)
  38. Takenaka K., Yamakawa H., Sakai H., Yoshimura S., Murase S., Okumura A., Et al., Angiotensin I-converting enzyme gene polymorphism in intracranial saccular aneurysm individuals, Neurol Res, 20, 7, pp. 607-611, (1998)
  39. Keramatipour M., McConnell R.S., Kirkpatrick P., Tebbs S., Furlong R.A., Rubinsztein D.C., The ACE I allele is associated with increased risk for ruptured intracranial aneurysms, J Med Genet, 37, 7, pp. 498-500, (2000)
  40. Slowik A., Borratynska A., Pera J., Betlej M., Dziedzic T., Krzyszkowski T., Et al., II genotype of the angiotensin-converting enzyme gene increases the risk for subarachnoid hemorrhage from ruptured aneurysm, Stroke
  41. a journal of cerebral circulation, 35, 7, pp. 1594-1597, (2004)
  42. Regenhardt R.W., Mecca A.P., Desland F., Ritucci-Chinni P.F., Ludin J.A., Greenstein D., Et al., Centrally administered angiotensin-(1–7) increases the survival of stroke-prone spontaneously hypertensive rats, Exp Physiol, 99, 2, pp. 442-453, (2014)
  43. Wu G.B., Du H.B., Zhai J.Y., Sun S., Cui J.L., Zhang Y., Et al., Controlled hemorrhage sensitizes angiotensin II-elicited hypertension through activation of the brain renin-angiotensin system independently of endoplasmic reticulum stress, Oxid Med Cell Longev, 2022, (2022)
  44. Voigt J.-P., Hortnagl H., Rex A., van Hove L., Bader M., Fink H., Brain angiotensin and anxiety-related behavior: the transgenic rat TGR (ASrAOGEN) 680, Brain Res, 1046, 1-2, pp. 145-156, (2005)
  45. Nwachuku E.L., Puccio A.M., Adeboye A., Chang Y.-F., Kim J., Okonkwo D.O., Time course of cerebrospinal fluid inflammatory biomarkers and relationship to 6-month neurologic outcome in adult severe traumatic brain injury, Clin Neurol Neurosurg, 149, pp. 1-5, (2016)
  46. de Freitas Cardoso M.G., Faleiro R.M., De Paula J.J., Kummer A., Caramelli P., Teixeira A.L., Et al., Cognitive impairment following acute mild traumatic brain injury, Front Neurol, 10, (2019)
  47. Kumar A., Loane D.J., Neuroinflammation after traumatic brain injury: opportunities for therapeutic intervention, Brain Behav Immun, 26, 8, pp. 1191-1201, (2012)
  48. Woodcock T., Morganti-Kossmann C., The role of markers of inflammation in traumatic brain injury, Front Neurol, 4, (2013)
  49. Khellaf A., Khan D.Z., Helmy A., Recent advances in traumatic brain injury, J Neurol, 266, 11, pp. 2878-2889, (2019)
  50. Janatpour Z.C., Korotcov A., Bosomtwi A., Dardzinski B.J., Symes A.J., Subcutaneous administration of angiotensin-(1–7) improves recovery after traumatic brain injury in mice, J Neurotrauma, 36, 22, pp. 3115-3131, (2019)
  51. Li T., Huang H.Y., Wang H.D., Gao C.C., Liang H., Deng C.L., Et al., Restoration of brain angiotensin-converting enzyme 2 Alleviates neurological deficits after severe traumatic brain injury via mitigation of pyroptosis and apoptosis, J Neurotrauma, (2022)
  52. de Barros J., Cardoso M.G., Machado C.A., Vieira E L.M., Faleiro R.M., Pedroso V.S.P., Et al., The potential role of renin-angiotensin system in mild traumatic brain injury, Neurol Sci, 43, 5, pp. 3353-3359, (2022)
  53. Kehoe A., Eleftheriou K., Heron M., Coats T., Montgomery H., Angiotensin-converting enzyme genotype may predict survival following major trauma, Emerg Med J, 25, 11, pp. 759-761, (2008)
  54. Schunkert H., Ingelfinger J.R., Hirsch A.T., Pinto Y., Remme W.J., Jacob H., Et al., Feedback regulation of angiotensin converting enzyme activity and mRNA levels by angiotensin II, Circ Res, 72, 2, pp. 312-318, (1993)
  55. Kangussu L.M., Almeida-Santos A.F., Bader M., Alenina N., Fontes M.A.P., Santos R.A., Et al., Angiotensin-(1–7) attenuates the anxiety and depression-like behaviors in transgenic rats with low brain angiotensinogen, Behav Brain Res, 257, pp. 25-30, (2013)
  56. Deshotels M.R., Xia H., Sriramula S., Lazartigues E., Filipeanu C.M., Angiotensin II mediates angiotensin converting enzyme type 2 internalization and degradation through an angiotensin ii type i receptor-dependent mechanism, Hypertension, 64, 6, pp. 1368-1375, (2014)
  57. Machado-Silva A., Passos-Silva D., Santos R.A., Sinisterra R.D., Therapeutic uses for angiotensin-(1-7), Expert Opin Ther Pat, 26, 6, pp. 669-678, (2016)
  58. Sanches M., Colpo G.D., Cuellar V.A., Bockmann T., Rogith D., Soares J.C., Et al., Decreased plasma levels of angiotensin-converting enzyme among patients with bipolar disorder, Front Neurosci, (2021)
  59. Gong X., Hu H., Qiao Y., Xu P., Yang M., Dang R., Et al., The involvement of renin-angiotensin system in lipopolysaccharide-induced behavioral changes, neuroinflammation, and disturbed insulin signaling, Front Pharmacol, 10, (2019)
  60. de Souza Gomes J.A., de Souza G.C., Berk M., Cavalcante L.M., de Sousa F.C.F., Budni J., Et al., Antimanic-like activity of candesartan in mice: possible involvement of antioxidant, anti-inflammatory and neurotrophic mechanisms, Eur Neuropsychopharmacol, 25, 11, pp. 2086-2097, (2015)
  61. Firouzabadi N., Farshadfar P., Haghnegahdar M., Alavi-Shoushtari A., Ghanbarinejad V., Impact of ACE2 genetic variant on antidepressant efficacy of SSRIs, Acta Neuropsychiatr, 34, 1, pp. 30-36, (2022)
  62. Schiavone M.T., Santos R., Brosnihan K.B., Khosla M.C., Ferrario C.M., Release of vasopressin from the rat hypothalamo-neurohypophysial system by angiotensin-(1–7) heptapeptide, Proc Natl Acad Sci USA, 85, 11, pp. 4095-4098, (1988)
  63. Block C., Santos R., Brosnihan K., Ferrario C., Immunocytochemical localization of angiotensin-(1–7) in the rat forebrain, Peptides, 9, 6, pp. 1395-1401, (1988)
  64. Campagnole-Santos M.J., Diz D.I., Santos R., Khosla M.C., Brosnihan K.B., Ferrario C.M., Cardiovascular effects of angiotensin-(1–7) injected into the dorsal medulla of rats, Am J Physiol Heart Circ Physiol, 257, 1, pp. H324-H329, (1989)
  65. Campagnole-Santos M.J., Heringer S.B., Batista E.N., Khosla M.C., Santos R., Differential baroreceptor reflex modulation by centrally infused angiotensin peptides, Am J Physiol Regul Integr Comp Physiol, 263, 1, pp. R89-R94, (1992)
  66. SAAVEDRA J.M., Ando H., Armando I., Baiardi G., Bregonzio C., Jezova M., Et al., Brain angiotensin II, an important stress hormone: regulatory sites and therapeutic opportunities, Ann N Y Acad Sci, 1018, 1, pp. 76-84, (2004)
  67. Braga V., Medeiros I., Ribeiro T., Franca-Silva M., Botelho-Ono M., Guimaraes D., Angiotensin-II-induced reactive oxygen species along the SFO-PVN-RVLM pathway: implications in neurogenic hypertension, Braz J Med Biol Res, 44, pp. 871-876, (2011)
  68. Chaves G.Z., Caligiorne S.M., Santos R.A., Khosla M.C., Campagnole-Santos M.J., Modulation of the baroreflex control of heart rate by angiotensin-(1–7) at the nucleus tractus solitarii of normotensive and spontaneously hypertensive rats, J Hypertens, 18, 12, pp. 1841-1848, (2000)
  69. Heringer-Walther S., Batista E.N., Walther T., Khosla M.C., Santos R.A., Campagnole-Santos M.J., Baroreflex improvement in SHR after ACE inhibition involves angiotensin-(1–7), Hypertension, 37, 5, pp. 1309-1314, (2001)
  70. Yamazato M., Ferreira A.J., Yamazato Y., Diez-Freire C., Yuan L., Gillies R., Et al., Gene transfer of angiotensin-converting enzyme 2 in the nucleus tractus solitarius improves baroreceptor heart rate reflex in spontaneously hypertensive rats, J Renin-Angiotensin-Aldosterone Syst JRAAS, 12, 4, pp. 456-461, (2011)
  71. Xu P., Sriramula S., Lazartigues E., ACE2/ANG-(1–7)/Mas pathway in the brain: the axis of good, Am J Physiol Regul Integr Comp Physiol, 300, 4, pp. R804-R817, (2011)
  72. Jiang T., Gao L., Shi J., Lu J., Wang Y., Zhang Y., Angiotensin-(1–7) modulates renin–angiotensin system associated with reducing oxidative stress and attenuating neuronal apoptosis in the brain of hypertensive rats, Pharmacol Res, 67, 1, pp. 84-93, (2013)
  73. Zheng J., Li G., Chen S., Bihl J., Buck J., Zhu Y., Et al., Activation of the ACE2/Ang-(1–7)/Mas pathway reduces oxygen–glucose deprivation-induced tissue swelling, ROS production, and cell death in mouse brain with angiotensin II overproduction, Neuroscience, 273, pp. 39-51, (2014)
  74. Ren L., Lu X., Danser A., Revisiting the brain renin-angiotensin system—focus on novel therapies, Curr Hypertens Rep, 21, 4, pp. 1-7, (2019)
  75. Jiang T., Gao L., Zhu X.C., Yu J.T., Shi J.Q., Tan M.S., Et al., Angiotensin-(1–7) inhibits autophagy in the brain of spontaneously hypertensive rats, Pharmacol Res, 71, pp. 61-68, (2013)
  76. Mendelsohn F.A., Jenkins T.A., Berkovic S.F., Effects of angiotensin II on dopamine and serotonin turnover in the striatum of conscious rats, Brain Res, 613, 2, pp. 221-229, (1993)
  77. Brown D.C., Steward L.J., Ge J., Barnes N.M., Ability of angiotensin II to modulate striatal dopamine release via the AT1 receptor in vitro and in vivo, Br J Pharmacol, 118, 2, pp. 414-420, (1996)
  78. Jenkins T.A., Mendelsohn F.A., Chai S.Y., Angiotensin-converting enzyme modulates dopamine turnover in the striatum, J Neurochem, 68, 3, pp. 1304-1311, (1997)
  79. Griendling K.K., Sorescu D., Ushio-Fukai M., NAD(P)H oxidase: role in cardiovascular biology and disease, Circ Res, 86, 5, pp. 494-501, (2000)
  80. Chabrashvili T., Kitiyakara C., Blau J., Karber A., Aslam S., Welch W.J., Et al., Effects of ANG II type 1 and 2 receptors on oxidative stress, renal NADPH oxidase, and SOD expression, Am J Physiol Regul Integr Comp Physiol, 285, 1, pp. R117-R124, (2003)
  81. Rodriguez-Pallares J., Rey P., Parga J.A., Munoz A., Guerra M.J., Labandeira-Garcia J.L., Brain angiotensin enhances dopaminergic cell death via microglial activation and NADPH-derived ROS, Neurobiol Dis, 31, 1, pp. 58-73, (2008)
  82. Labandeira-Garcia J.L., Garrido-Gil P., Rodriguez-Pallares J., Valenzuela R., Borrajo A., Rodriguez-Perez A.I., Brain renin-angiotensin system and dopaminergic cell vulnerability, Front Neuroanat, 8, (2014)
  83. Grammatopoulos T.N., Jones S.M., Ahmadi F.A., Hoover B.R., Snell L.D., Skoch J., Et al., Angiotensin type 1 receptor antagonist losartan, reduces MPTP-induced degeneration of dopaminergic neurons in substantia nigra, Mol Neurodegener, 2, (2007)
  84. Rey P., Lopez-Real A., Sanchez-Iglesias S., Munoz A., Soto-Otero R., Labandeira-Garcia J.L., Angiotensin type-1–receptor antagonists reduce 6-hydroxydopamine toxicity for dopaminergic neurons, Neurobiol Aging, 28, 4, pp. 555-567, (2007)
  85. Munoz A., Garrido-Gil P., Dominguez-Meijide A., Labandeira-Garcia J.L., Angiotensin type 1 receptor blockage reduces l-dopa-induced dyskinesia in the 6-OHDA model of Parkinson's disease. Involvement of vascular endothelial growth factor and interleukin-1beta, Exp Neurol, 261, pp. 720-732, (2014)
  86. Jenkins T.A., Wong J.Y., Howells D.W., Mendelsohn F.A., Chai S.Y., Effect of chronic angiotensin-converting enzyme inhibition on striatal dopamine content in the MPTP-treated mouse, J Neurochem, 73, 1, pp. 214-219, (1999)
  87. Kurosaki R., Muramatsu Y., Kato H., Watanabe Y., Imai Y., Itoyama Y., Et al., Effect of angiotensin-converting enzyme inhibitor perindopril on interneurons in MPTP-treated mice, Eur Neuropsychopharmacol, 15, 1, pp. 57-67, (2005)
  88. Munoz A., Rey P., Guerra M.J., Mendez-Alvarez E., Soto-Otero R., Labandeira-Garcia J.L., Reduction of dopaminergic degeneration and oxidative stress by inhibition of angiotensin converting enzyme in a MPTP model of parkinsonism, Neuropharmacology, 51, 1, pp. 112-120, (2006)
  89. Lopez-Real A., Rey P., Soto-Otero R., Mendez-Alvarez E., Labandeira-Garcia J.L., Angiotensin-converting enzyme inhibition reduces oxidative stress and protects dopaminergic neurons in a 6-hydroxydopamine rat model of Parkinsonism, J Neurosci Res, 81, 6, pp. 865-873, (2005)
  90. Grammatopoulos T.N., Outeiro T.F., Hyman B.T., Standaert D.G., Angiotensin II protects against alpha-synuclein toxicity and reduces protein aggregation in vitro, Biochem Biophys Res Commun, 363, 3, pp. 846-851, (2007)
  91. Simoes E.S.A.C., Teixeira M.M., ACE inhibition, ACE2 and angiotensin-(1–7) axis in kidney and cardiac inflammation and fibrosis, Pharmacol Res, 107, pp. 154-162, (2016)
  92. Rabie M.A., Abd El Fattah M.A., Nassar N.N., El-Abhar H.S., Abdallah D.M., Angiotensin 1–7 ameliorates 6-hydroxydopamine lesions in hemiparkinsonian rats through activation of MAS receptor/PI3K/Akt/BDNF pathway and inhibition of angiotensin II type-1 receptor/NF-kappaB axis, Biochem Pharmacol, 151, pp. 126-134, (2018)
  93. Gao Q., Chen R., Wu L., Huang Q., Wang X.X., Tian Y.Y., Et al., Angiotensin-(1–7) reduces alpha-synuclein aggregation by enhancing autophagic activity in Parkinson's disease, Neural Regen Res, 17, 5, pp. 1138-1145, (2022)
  94. Ge J., Barnes N.M., Alterations in angiotensin AT1 and AT2 receptor subtype levels in brain regions from patients with neurodegenerative disorders, Eur J Pharmacol, 297, 3, pp. 299-306, (1996)
  95. Konings C.H., Kuiper M.A., Bergmans P.L., Grijpma A.M., van Kamp G.J., Wolters E.C., Increased angiotensin-converting enzyme activity in cerebrospinal fluid of treated patients with Parkinson's disease, Clin Chim Acta, 231, 1, pp. 101-106, (1994)
  96. Rocha N.P., Scalzo P.L., Barbosa I.G., de Campos-Carli S.M., Tavares L.D., de Souza M.S., Et al., Peripheral levels of angiotensins are associated with depressive symptoms in Parkinson's disease, J Neurol Sci, 368, pp. 235-239, (2016)
  97. Li N.C., Lee A., Whitmer R.A., Kivipelto M., Lawler E., Kazis L.E., Et al., Use of angiotensin receptor blockers and risk of dementia in a predominantly male population: prospective cohort analysis, BMJ, 340, (2010)
  98. Kume K., Hanyu H., Sakurai H., Takada Y., Onuma T., Iwamoto T., Effects of telmisartan on cognition and regional cerebral blood flow in hypertensive patients with Alzheimer's disease, Geriatr Gerontol Int, 12, 2, pp. 207-214, (2012)
  99. Zhuang S., Wang H.F., Wang X., Li J., Xing C.M., The association of renin-angiotensin system blockade use with the risks of cognitive impairment of aging and Alzheimer's disease: a meta-analysis, J Clin Neurosci, 33, pp. 32-38, (2016)
  100. Braszko J.J., Wincewicz D., Jakubow P., Candesartan prevents impairment of recall caused by repeated stress in rats, Psychopharmacology, 225, 2, pp. 421-428, (2013)
  101. Wincewicz D., Braszko J.J., Telmisartan attenuates cognitive impairment caused by chronic stress in rats, Pharmacol Rep, 66, 3, pp. 436-441, (2014)
  102. Wincewicz D., Braszko J.J., Angiotensin II AT1 receptor blockade by telmisartan reduces impairment of spatial maze performance induced by both acute and chronic stress, J Renin-Angiotensin-Aldosterone Syst JRAAS, 16, 3, pp. 495-505, (2015)
  103. Wincewicz D., Juchniewicz A., Waszkiewicz N., Braszko J.J., Angiotensin II type 1 receptor blockade by telmisartan prevents stress-induced impairment of memory via HPA axis deactivation and up-regulation of brain-derived neurotrophic factor gene expression, Pharmacol Biochem Behav, 148, pp. 108-118, (2016)
  104. Kurata T., Lukic V., Kozuki M., Wada D., Miyazaki K., Morimoto N., Et al., Long-term effect of telmisartan on Alzheimer's amyloid genesis in SHR-SR after tMCAO, Transl Stroke Res, 6, 2, pp. 107-115, (2015)
  105. Saavedra J.M., Evidence to consider angiotensin II receptor blockers for the treatment of early Alzheimer's disease, Cell Mol Neurobiol, 36, 2, pp. 259-279, (2016)
  106. Rocha N.P., Toledo A., Corgosinho L.T.S., de Souza L.C., Guimaraes H.C., Resende E.P.F., Et al., Cerebrospinal fluid levels of angiotensin-converting enzyme are associated with amyloid-beta42 burden in Alzheimer's disease, J Alzheimers Dis, 64, 4, pp. 1085-1090, (2018)
  107. Kehoe P.G., Wong S., Al Mulhim N., Palmer L.E., Miners J.S., Angiotensin-converting enzyme 2 is reduced in Alzheimer's disease in association with increasing amyloid-beta and tau pathology, Alzheimer's Res Ther, 8, 1, (2016)
  108. Jiang T., Tan L., Gao Q., Lu H., Zhu X.C., Zhou J.S., Et al., Plasma angiotensin-(1–7) is a potential biomarker for Alzheimer's disease, Curr Neurovascular Res, 13, 2, pp. 96-99, (2016)
  109. Ribeiro V.T., Cordeiro T.M.E., Filha R.D.S., Perez L.G., Caramelli P., Teixeira A.L., Et al., Circulating angiotensin-(1–7) is reduced in Alzheimer's disease patients and correlates with white matter Abnormalities: results from a pilot study, Front Neurosci, 15, (2021)
  110. Jiang T., Zhang Y.D., Zhou J.S., Zhu X.C., Tian Y.Y., Zhao H.D., Et al., Angiotensin-(1–7) is reduced and inversely correlates with tau hyperphosphorylation in animal models of Alzheimer's disease, Mol Neurobiol, 53, 4, pp. 2489-2497, (2016)
  111. Uekawa K., Hasegawa Y., Senju S., Nakagata N., Ma M., Nakagawa T., Et al., Intracerebroventricular infusion of angiotensin-(1–7) ameliorates cognitive impairment and memory dysfunction in a mouse model of Alzheimer's disease, J Alzheimers Dis, 53, 1, pp. 127-133, (2016)
  112. Chen J.L., Zhang D.L., Sun Y., Zhao Y.X., Zhao K.X., Pu D., Et al., Angiotensin-(1–7) administration attenuates Alzheimer's disease-like neuropathology in rats with streptozotocin-induced diabetes via Mas receptor activation, Neuroscience, 346, pp. 267-277, (2017)
  113. Varshney V., Garabadu D., Ang (1–7)/Mas receptor-axis activation promotes amyloid beta-induced altered mitochondrial bioenergetics in discrete brain regions of Alzheimer's disease-like rats, Neuropeptides, 86, (2021)
  114. Duan R., Wang S.Y., Wei B., Deng Y., Fu X.X., Gong P.Y., Et al., Angiotensin-(1–7) analogue AVE0991 modulates astrocyte-mediated neuroinflammation via lncRNA SNHG14/miR-223-3p/NLRP3 pathway and offers neuroprotection in a transgenic mouse model of Alzheimer's disease, J Inflamm Res, 14, pp. 7007-7019, (2021)
  115. Evans C.E., Miners J.S., Piva G., Willis C.L., Heard D.M., Kidd E.J., Et al., ACE2 activation protects against cognitive decline and reduces amyloid pathology in the Tg2576 mouse model of Alzheimer's disease, Acta Neuropathol, 139, 3, pp. 485-502, (2020)
  116. James S.L., Abate D., Abate K.H., Abay S.M., Abbafati C., Abbasi N., Et al., Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017, Lancet, 392, 10159, pp. 1789-1858, (2018)
  117. Villarroel M.A., Terlizzi E.P., Symptoms of Depression Among Adults: United States, 2019: US Department of Health and Human Services, Centers for Disease Control and …, (2020)
  118. Datta S., Suryadevara U., Cheong J., Mood disorders, Continuum: Lifelong Learning in Neurology, 27, 6, pp. 1712-1737, (2021)
  119. 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, 130, 14, pp. 1247-1255, (2016)
  120. Sanches M., Teixeira A.L., The renin-angiotensin system, mood, and suicide: are there associations?, World J Psychiatr, 11, 9, pp. 581-588, (2021)
  121. de Miranda A.S., Andreatini R., Teixeira A.L., Chapter 43 - animal models of mania: essential tools to better understand bipolar disorder, Animal Models for the Study of Human Disease, pp. 1131-1143, (2017)
  122. Chandra A., Stone C.R., Li W.A., Geng X., Ding Y., The cerebral circulation and cerebrovascular disease II: pathogenesis of cerebrovascular disease, Brain Circ, 3, 2, pp. 57-65, (2017)