Brain angiotensin type-1 and type-2 receptors: cellular locations under normal and hypertensive conditions.
Blood pressure
Neurogenic hypertension
Renin-angiotensin system
Transgenic reporter mice
Journal
Hypertension research : official journal of the Japanese Society of Hypertension
ISSN: 1348-4214
Titre abrégé: Hypertens Res
Pays: England
ID NLM: 9307690
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
24
06
2019
accepted:
02
11
2019
revised:
25
10
2019
pubmed:
20
12
2019
medline:
5
6
2021
entrez:
20
12
2019
Statut:
ppublish
Résumé
Brain angiotensin-II (Ang-II) type-1 receptors (AT1Rs), which exert profound effects on normal cardiovascular, fluid, and metabolic homeostasis, are overactivated in and contribute to chronic sympathoexcitation and hypertension. Accumulating evidence indicates that the activation of Ang-II type-2 receptors (AT2Rs) in the brain exerts effects that are opposite to those of AT1Rs, lowering blood pressure, and reducing hypertension. Thus, it would be interesting to understand the relative cellular localization of AT1R and AT2R in the brain under normal conditions and whether this localization changes during hypertension. Here, we developed a novel AT1aR-tdTomato reporter mouse strain in which the location of brain AT1aR was largely consistent with that determined in the previous studies. This AT1aR-tdTomato reporter mouse strain was crossed with our previously described AT2R-eGFP reporter mouse strain to yield a novel dual AT1aR/AT2R reporter mouse strain, which allowed us to determine that AT1aR and AT2R are primarily localized to different populations of neurons in brain regions controlling cardiovascular, fluid, and metabolic homeostasis. Using the individual AT1aR-tdTomato reporter mice, we also demonstrated that during hypertension induced by the administration of deoxycorticosterone acetate-salt, there was no shift in the expression of AT1aR from neurons to microglia or astrocytes in the paraventricular nucleus, a brain area important for sympathetic regulation. Using AT2R-eGFP reporter mice under similar hypertensive conditions, we demonstrated that the same was true of AT2R expression in the nucleus of the solitary tract (NTS), an area critical for baroreflex control. Collectively, these findings provided a novel means to assess the colocalization of AT1R and AT2R in the brain and a novel view of their cellular localization in hypertension.
Identifiants
pubmed: 31853042
doi: 10.1038/s41440-019-0374-8
pii: 10.1038/s41440-019-0374-8
pmc: PMC7538702
mid: NIHMS1627791
doi:
Substances chimiques
Receptor, Angiotensin, Type 1
0
Receptor, Angiotensin, Type 2
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
281-295Subventions
Organisme : NHLBI NIH HHS
ID : R01 HL139868
Pays : United States
Organisme : NHLBI NIH HHS
ID : R35 HL150750
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL136595
Pays : United States
Organisme : NHLBI NIH HHS
ID : K99 HL125805
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL093186
Pays : United States
Organisme : NHLBI NIH HHS
ID : R00 HL125805
Pays : United States
Organisme : NHLBI NIH HHS
ID : K99 HL096830
Pays : United States
Organisme : NHLBI NIH HHS
ID : R00 HL096830
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL122494
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL145028
Pays : United States
Commentaires et corrections
Type : CommentIn
Références
Hollenberg NK. The renin-angiotensin system and sodium homeostasis. J Cardiovasc Pharm. 1984;6 Suppl :S176–183.
Dzau VJ. Circulating versus local renin-angiotensin system in cardiovascular homeostasis. Circulation. 1988;77:I4–13.
pubmed: 3286045
Fitzsimons JT. Angiotensin, thirst, and sodium appetite. Physiol Rev. 1998;78:583–686.
pubmed: 9674690
Ferguson AV. Angiotensinergic regulation of autonomic and neuroendocrine outputs: critical roles for the subfornical organ and paraventricular nucleus. Neuroendocrinology. 2009;89:370–6.
pubmed: 19342823
McKinley MJ, Allen AM, Mathai ML, May C, McAllen RM, Oldfield BJ, et al. Brain angiotensin and body fluid homeostasis. Jpn J Physiol. 2001;51:281–9.
pubmed: 11492952
Miller AJ, Arnold AC. The renin-angiotensin system in cardiovascular autonomic control: recent developments and clinical implications. Clin Auton Res. 2019;29:231–43.
pubmed: 30413906
Leenen FH. Actions of circulating angiotensin II and aldosterone in the brain contributing to hypertension. Am J Hypertens. 2014;27:1024–32.
pubmed: 24742639
Marc Y, Llorens-Cortes C. The role of the brain renin-angiotensin system in hypertension: implications for new treatment. Prog Neurobiol. 2011;95:89–103.
pubmed: 21763394
Young CN, Davisson RL. Angiotensin-ii, the brain, and hypertension: an update. Hypertension. 2015;66:920–6.
pubmed: 26324508
pmcid: 4600031
Lenkei Z, Palkovits M, Corvol P, Llorens-Cortès C. Expression of angiotensin type-1 (at1) and type-2 (at2) receptor mrnas in the adult rat brain: a functional neuroanatomical review. Front Neuroendocrinol. 1997;18:383.
pubmed: 9344632
Millan MA, Jacobowitz DM, Aguilera G, Catt KJ. Differential distribution of at1 and at2 angiotensin II receptor subtypes in the rat brain during development. Proc Natl Acad Sci USA. 1991;88:11440–4.
pubmed: 1763058
Tsutsumi K, Saavedra JM. Characterization and development of angiotensin II receptor subtypes (at1 and at2) in rat brain. Am J Physiol. 1991;261:R209-216.
Carter DA, Choong YT, Connelly AA, Bassi JK, Hunter NO, Thongsepee N, et al. Functional and neurochemical characterization of angiotensin type 1a receptor-expressing neurons in the nucleus of the solitary tract of the mouse. Am J Physiol Regul. 2017;313:R438–49.
Chen D, Jancovski N, Bassi JK, Nguyen-Huu TP, Choong YT, Palma-Rigo K, et al. Angiotensin type 1a receptors in c1 neurons of the rostral ventrolateral medulla modulate the pressor response to aversive stress. J Neurosci. 2012;32:2051–61.
pubmed: 22323719
pmcid: 6621685
Gonzalez AD, Wang G, Waters EM, Gonzales KL, Speth RC, Van Kempen TA, et al. Distribution of angiotensin type 1a receptor-containing cells in the brains of bacterial artificial chromosome transgenic mice. Neuroscience. 2012;226:489–509.
pubmed: 22922351
pmcid: 3505886
de Kloet AD, Wang L, Ludin JA, Smith JA, Pioquinto DJ, Hiller H, et al. Reporter mouse strain provides a novel look at angiotensin type-2 receptor distribution in the central nervous system. Brain Struct Funct. 2016;221:891–912.
pubmed: 25427952
Brouwers S, Smolders I, Wainford RD, Dupont AG. Hypotensive and sympathoinhibitory responses to selective central at2 receptor stimulation in spontaneously hypertensive rats. Clin Sci. 2015;129:81–92.
pubmed: 25655919
pmcid: 4430196
Dai SY, Peng W, Zhang YP, Li JD, Shen Y, Sun XF. Brain endogenous angiotensin II receptor type 2 (at2-r) protects against doca/salt-induced hypertension in female rats. J Neuroinflammation. 2015;12:47.
pubmed: 25885968
pmcid: 4355980
de Kloet AD, Steckelings UM, Sumners C. Protective angiotensin type 2 receptors in the brain and hypertension. Curr Hypertens Rep. 2017;19:46.
pubmed: 28488048
pmcid: 5600899
Gao J, Zhang H, Le KD, Chao J, Gao L. Activation of central angiotensin type 2 receptors suppresses norepinephrine excretion and blood pressure in conscious rats. Am J Hypertens. 2011;24:724–30.
pubmed: 21394088
pmcid: 3286515
Gao L, Wang W, Li H, Sumners C, Zucker IH. Effects of angiotensin type 2 receptor overexpression in the rostral ventrolateral medulla on blood pressure and urine excretion in normal rats. Hypertension. 2008;51:521–7.
pubmed: 18086951
Dai SY, Zhang YP, Peng W, Shen Y, He JJ. Central infusion of angiotensin II type 2 receptor agonist compound 21 attenuates doca/nacl-induced hypertension in female rats. Oxid Med Cell Longev. 2016;2016:3981790.
pubmed: 26783414
Blanch GT, Freiria-Oliveira AH, Speretta GF, Carrera EJ, Li H, Speth RC, et al. Increased expression of angiotensin II type 2 receptors in the solitary-vagal complex blunts renovascular hypertension. Hypertension. 2014;64:777–83.
pubmed: 24958505
pmcid: 4162765
Gao J, Zucker IH, Gao L. Activation of central angiotensin type 2 receptors by compound 21 improves arterial baroreflex sensitivity in rats with heart failure. Am J Hypertens. 2014;27:1248–56.
pubmed: 24687998
pmcid: 4229732
Gao L, Zucker IH. At2 receptor signaling and sympathetic regulation. Curr Opin Pharmacol. 2011;11:124–30.
pubmed: 21159555
Legat L, Smolders I, Dupont AG. Gabaergic signaling mediates central cardiovascular angiotensin II type 2 receptor effects. Trends Endocrinol Metab. 2018;29:605–6.
pubmed: 29739704
Ruchaya PJ, Speretta GF, Blanch GT, Li H, Sumners C, Menani JV, et al. Overexpression of at2r in the solitary-vagal complex improves baroreflex in the spontaneously hypertensive rat. Neuropeptides. 2016;60:29–36.
pubmed: 27469059
Speretta GF, Ruchaya PJ, Delbin MA, Melo MR, Li H, Menani JV, et al. Importance of at1 and at2 receptors in the nucleus of the solitary tract in cardiovascular responses induced by a high-fat diet. Hypertens Res. 2019;42:439–49.
pubmed: 30631157
Steckelings UM, Kloet A, Sumners C. Centrally mediated cardiovascular actions of the angiotensin II type 2 receptor. Trends Endocrinol Metab. 2017;28:684–93.
pubmed: 28733135
pmcid: 5563271
Han C, Rice MW, Cai D. Neuroinflammatory and autonomic mechanisms in diabetes and hypertension. Am J Physiol Endocrinol Metab. 2016;311:E32–41.
pubmed: 27166279
pmcid: 4967151
Montaniel KR, Harrison DG. Is hypertension a bone marrow disease? Circulation. 2016;134:1369–72.
pubmed: 27678263
pmcid: 5117669
Santisteban MM, Zubcevic J, Baekey DM, Raizada MK. Dysfunctional brain-bone marrow communication: a paradigm shift in the pathophysiology of hypertension. Curr Hypertens Rep. 2013;15:377–89.
pubmed: 23715920
pmcid: 3714364
Farina C, Aloisi F, Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol. 2007;28:138–45.
pubmed: 17276138
Norris GT, Kipnis J. Immune cells and cns physiology: microglia and beyond. J Exp Med. 2019;216:60–70.
pubmed: 30504438
pmcid: 6314530
de Kloet AD, Pitra S, Wang L, Hiller H, Pioquinto DJ, Smith JA, et al. Angiotensin type-2 receptors influence the activity of vasopressin neurons in the paraventricular nucleus of the hypothalamus in male mice. Endocrinology. 2016;157:3167–80.
pubmed: 27267713
pmcid: 4967126
de Kloet AD, Wang L, Pitra S, Hiller H, Smith JA, Tan Y, et al. A unique "angiotensin-sensitive" neuronal population coordinates neuroendocrine, cardiovascular, and behavioral responses to stress. J Neurosci. 2017;37:3478–90.
pubmed: 28219987
pmcid: 5373130
Grobe JL, Buehrer BA, Hilzendeger AM, Liu X, Davis DR, Xu D, et al. Angiotensinergic signaling in the brain mediates metabolic effects of deoxycorticosterone (doca)-salt in c57 mice. Hypertension. 2011;57:600–7.
pubmed: 21263123
pmcid: 3144490
Hilzendeger AM, Cassell MD, Davis DR, Stauss HM, Mark AL, Grobe JL, et al. Angiotensin type 1a receptors in the subfornical organ are required for deoxycorticosterone acetate-salt hypertension. Hypertension. 2013;61:716–22.
pubmed: 23266541
Jessberger S, Toni N, Clemenson GD Jr., Ray J, Gage FH. Directed differentiation of hippocampal stem/progenitor cells in the adult brain. Nat Neurosci. 2008;11:888–93.
pubmed: 18587391
pmcid: 2795354
Krause EG, de Kloet AD, Scott KA, Flak JN, Jones K, Smeltzer MD, et al. Blood-borne angiotensin II acts in the brain to influence behavioral and endocrine responses to psychogenic stress. J Neurosci. 2011;31:15009–15.
pubmed: 22016534
pmcid: 3214963
de Kloet AD, Pioquinto DJ, Nguyen D, Wang L, Smith JA, Hiller H, et al. Obesity induces neuroinflammation mediated by altered expression of the renin-angiotensin system in mouse forebrain nuclei. Physiol Behav. 2014;136:31–8.
Langlet F, Mullier A, Bouret SG, Prevot V, Dehouck B. Tanycyte-like cells form a blood–cerebrospinal fluid barrier in the circumventricular organs of the mouse brain. J Comp Neurol. 2013;521:3389–405.
pubmed: 23649873
pmcid: 3973970
Kádár A, Sánchez E, Wittmann G, Singru PS, Füzesi T, Marsili A, et al. Distribution of hypophysiotropic thyrotropin-releasing hormone (trh)-synthesizing neurons in the hypothalamic paraventricular nucleus of the mouse. J Comp Neurol. 2010;518:3948–61.
pubmed: 20737594
pmcid: 2932658
Gautron L, Rutkowski JM, Burton MD, Wei W, Wan Y, Elmquist JK. Neuronal and nonneuronal cholinergic structures in the mouse gastrointestinal tract and spleen. J Comp Neurol. 2013;521:3741–67.
pubmed: 23749724
pmcid: 4081472
Mousa SA, Shaqura M, Schäper J, Treskatsch S, Habazettl H, Schäfer M, et al. Developmental expression of δ-opioid receptors during maturation of the parasympathetic, sympathetic, and sensory innervations of the neonatal heart: early targets for opioid regulation of autonomic control. J Comp Neurol. 2011;519:957–71.
pubmed: 21280046
Liu M, Shi P, Sumners C. Direct anti-inflammatory effects of angiotensin-(1-7) on microglia. J Neurochem. 2016;136:163–71.
pubmed: 26448556
Mecca AP, Regenhardt RW, O'Connor TE, Joseph JP, Raizada MK, Katovich MJ, et al. Cerebroprotection by angiotensin-(1-7) in endothelin-1-induced ischaemic stroke. Exp Physiol. 2011;96:1084–96.
pubmed: 21685445
pmcid: 3210510
Regenhardt RW, Mecca AP, Desland F, Ritucci-Chinni PF, Ludin JA, Greenstein D, et al. Centrally administered angiotensin-(1-7) increases the survival of stroke-prone spontaneously hypertensive rats. Exp Physiol. 2014;99:442–53.
pubmed: 24142453
de Kloet AD, Wang L, Pitra S, Hiller H, Smith JA, Tan Y, et al. A unique ‘angiotensin sensitive' neuronal population coordinates neuroendocrine, cardiovascular and behavioral responses to stress. J Neurosci. 2017;37:3478–90.
Franklin KBJ, Paxinos G. The mouse brain: in stereotaxic coordinates. New York, NY: Elsevier; 2008.
Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 7th Edition, Academic Press, San Diego, CA: Elsevier Life Sciences; 2013.
Karnik SS, Unal H, Kemp JR, Tirupula KC, Eguchi S, Vanderheyden PM, et al. International union of basic and clinical pharmacology. Xcix. Angiotensin receptors: interpreters of pathophysiological angiotensinergic stimuli [corrected]. Pharmacol Rev. 2015;67:754–819.
pubmed: 26315714
pmcid: 4630565
Shi P, Diez-Freire C, Jun JY, Qi Y, Katovich MJ, Li Q, et al. Brain microglial cytokines in neurogenic hypertension. Hypertension. 2010;56:297–303.
pubmed: 20547972
pmcid: 2929640
Coote JH, Yang Z, Pyner S, Deering J. Control of sympathetic outflows by the hypothalamic paraventricular nucleus. Clin Exp Pharmacol Physiol. 1998;25:461–3.
pubmed: 9673825
Ciriello J, Kline RL, Zhang TX, Caverson MM. Lesions of the paraventricular nucleus alter the development of spontaneous hypertension in the rat. Brain Res. 1984;310:355–9.
pubmed: 6488025
Nakata T, Takeda K, Itho H, Hirata M, Kawasaki S, Hayashi J, et al. Paraventricular nucleus lesions attenuate the development of hypertension in doca/salt-treated rats. Am J Hypertens. 1989;2:625–30.
pubmed: 2570597
Gutkind JS, Kurihara M, Castren E, Saavedra JM. Increased concentration of angiotensin II binding sites in selected brain areas of spontaneously hypertensive rats. J hypertens. 1988;6:79–84.
pubmed: 3351297
Lenkei Z, Corvol P, Llorens-Cortes C. Comparative expression of vasopressin and angiotensin type-1 receptor mrna in rat hypothalamic nuclei: a double in situ hybridization study. brain Res Mol brain Res. 1995;34:135–42.
pubmed: 8750869
Santisteban MM, Ahmari N, Carvajal JM, Zingler MB, Qi Y, Kim S, et al. Involvement of bone marrow cells and neuroinflammation in hypertension. Circ Res. 2015;117:178–91.
pubmed: 25963715
pmcid: 4490954
de Kloet AD, Pati D, Wang L, Hiller H, Sumners C, Frazier CJ, et al. Angiotensin type 1a receptors in the paraventricular nucleus of the hypothalamus protect against diet-induced obesity. J Neurosci. 2013;33:4825–33.
pubmed: 23486953
pmcid: 3638262
Obermuller N, Unger T, Culman J, Gohlke P, de Gasparo M, Bottari SP. Distribution of angiotensin II receptor subtypes in rat brain nuclei. Neurosci Lett. 1991;132:11–15.
pubmed: 1787912
Daniels D. Diverse roles of angiotensin receptor intracellular signaling pathways in the control of water and salt intake. In: De Luca LA, Jr., Menani JV, Johnson AK, editors. Neurobiology of body fluid homeostasis: transduction and integration. Boca Raton, FL: CRC Press/Taylor & Francis; 2014.
Ferguson AV, Bains JS. Actions of angiotensin in the subfornical organ and area postrema: implications for long term control of autonomic output. Clin Exp Pharmacol Physiol. 1997;24:96–101.
pubmed: 9043813
McKinley MJ, McAllen RM, Pennington GL, Smardencas A, Weisinger RS, Oldfield BJ. Physiological actions of angiotensin II mediated by at1 and at2 receptors in the brain. Clin Exp Pharm Physiol Suppl. 1996;3:S99–104.
Vieira AA, Nahey DB, Collister JP. Role of the organum vasculosum of the lamina terminalis for the chronic cardiovascular effects produced by endogenous and exogenous ang ii in conscious rats. Am J Physiol Regul. 2010;299:R1564–71.
Aguilera G, Young WS, Kiss A, Bathia A. Direct regulation of hypothalamic corticotropin-releasing-hormone neurons by angiotensin-ii. Neuroendocrinology. 1995;61:437–44.
pubmed: 7783857
Bains JS, Ferguson AV. Paraventricular nucleus neurons projecting to the spinal cord receive excitatory input from the subfornical organ. Am J Physiol. 1995;268:R625–33.
pubmed: 7900904
Zhu GQ, Patel KP, Zucker IH, Wang W. Microinjection of ang ii into paraventricular nucleus enhances cardiac sympathetic afferent reflex in rats. Am J Physiol Heart Circ Physiol. 2002;282:H2039–2045.
pubmed: 12003809
Cunningham JT, Beltz T, Johnson RF, Johnson AK. The effects of ibotenate lesions of the median preoptic nucleus on experimentally-induced and circadian drinking behavior in rats. Brain Res. 1992;580:325–30.
pubmed: 1504809
McKinley MJ, Yao ST, Uschakov A, McAllen RM, Rundgren M, Martelli D. The median preoptic nucleus: front and centre for the regulation of body fluid, sodium, temperature, sleep and cardiovascular homeostasis. Acta Physiol. 2015;214:8–32.
Abegaz B, Davern PJ, Jackson KL, Nguyen-Huu TP, Bassi JK, Connelly A, et al. Cardiovascular role of angiotensin type 1a receptors in the nucleus of the solitary tract of mice. Cardiovascular Res. 2013;100:181–91.
Colombari E, Colombari DS. Nts at 1a receptor on long-term arterial pressure regulation: putative mechanism. Cardiovasc Res. 2013;100:173–4.
pubmed: 24048944
Hasser EM, Cunningham JT, Sullivan MJ, Curtis KS, Blaine EH, Hay M. Area postrema and sympathetic nervous system effects of vasopressin and angiotensin ii. Clin Exp Pharmacol Physiol. 2000;27:432–6.
pubmed: 10831249
Nahey DB, Collister JP. Ang ii-induced hypertension and the role of the area postrema during normal and increased dietary salt. Am J Physiol Heart Circ Physiol. 2007;292:H694–700.
pubmed: 16980346
Oldfield BJ, Davern PJ, Giles ME, Allen AM, Badoer E, McKinley MJ. Efferent neural projections of angiotensin receptor (at1) expressing neurones in the hypothalamic paraventricular nucleus of the rat. J Neuroendocrinol. 2001;13:139–46.
pubmed: 11168839
Rowe BP, Saylor DL, Speth RC. Analysis of angiotensin II receptor subtypes in individual rat brain nuclei. Neuroendocrinology. 1992;55:563–73.
pubmed: 1584339
MacGregor DP, Murone C, Song K, Allen AM, Paxinos G, Mendelsohn FA. Angiotensin II receptor subtypes in the human central nervous system. Brain Res. 1995;675:231–40.
pubmed: 7796134
Song K, Allen AM, Paxinos G, Mendelsohn FA. Mapping of angiotensin II receptor subtype heterogeneity in rat brain. J Comp Neurol. 1992;316:467–84.
pubmed: 1577995
Guimond MO, Gallo-Payet N. The angiotensin II type 2 receptor in brain functions: an update. Int J Hypertens. 2012;2012:351758.
pubmed: 23320146
pmcid: 3540774
Lenkei Z, Palkovits M, Corvol P, Llorens-Cortes C. Distribution of angiotensin II type-2 receptor (at2) mrna expression in the adult rat brain. J Comp Neurol. 1996;373:322–39.
pubmed: 8889931
Haspula D, Clark MA. Neuroinflammation and sympathetic overactivity: mechanisms and implications in hypertension. Auton Neurosci. 2018;210:10–17.
pubmed: 29361405
Santisteban MM, Kim S, Pepine CJ, Raizada MK. Brain-gut-bone marrow axis: implications for hypertension and related therapeutics. Circ Res. 2016;118:1327–36.
pubmed: 27081113
pmcid: 4834860
Biancardi VC, Stranahan AM, Krause EG, de Kloet AD, Stern JE. Cross talk between at1 receptors and toll-like receptor 4 in microglia contributes to angiotensin ii-derived ros production in the hypothalamic paraventricular nucleus. Am J Physiol Heart Circ Physiol. 2016;310:H404–415.
pubmed: 26637556
Stern JE, Son S, Biancardi VC, Zheng H, Sharma N, Patel KP. Astrocytes contribute to angiotensin II stimulation of hypothalamic neuronal activity and sympathetic outflow. Hypertension. 2016;68:1483–93.
pubmed: 27698069
pmcid: 5159229
Joglar B, Rodriguez-Pallares J, Rodriguez-Perez AI, Rey P, Guerra MJ, Labandeira-Garcia JL. The inflammatory response in the mptp model of parkinson's disease is mediated by brain angiotensin: relevance to progression of the disease. J Neurochem. 2009;109:656–69.
pubmed: 19245663
Lanz TV, Ding Z, Ho PP, Luo J, Agrawal AN, Srinagesh H, et al. Angiotensin II sustains brain inflammation in mice via tgf-beta. J Clin Investig. 2010;120:2782–94.
pubmed: 20628203
Negussie S, Lymperopoulos A, Clark MA. Role of betaarrestin1 in at1 r-mediated mitogen-activated protein kinase activation in wistar and shr brainstem astrocytes. J Neurochem. 2019;148:46–62.
pubmed: 30347436
Sumners C, Tang W, Zelezna B, Raizada MK. Angiotensin II receptor subtypes are coupled with distinct signal-transduction mechanisms in neurons and astrocytes from rat brain. Proc Natl Acad Sci USA. 1991;88:7567–71.
pubmed: 1881896
Tallant EA, Higson JT. Angiotensin II activates distinct signal transduction pathways in astrocytes isolated from neonatal rat brain. Glia. 1997;19:333–42.
pubmed: 9097077
Wu CY, Zha H, Xia QQ, Yuan Y, Liang XY, Li JH, et al. Expression of angiotensin II and its receptors in activated microglia in experimentally induced cerebral ischemia in the adult rats. Mol Cell Biochem. 2013;382:47–58.
pubmed: 23754618
O'Callaghan EL, Bassi JK, Porrello ER, Delbridge LM, Thomas WG, Allen AM. Regulation of angiotensinogen by angiotensin II in mouse primary astrocyte cultures. J Neurochem. 2011;119:18–26.
pubmed: 21797869