Stimulation of angiotensin II receptor 2 preserves cognitive function and is associated with an enhanced cerebral vascular density after stroke

Persky, 2010, Stroke in women: disparities and outcomes, Curr. Cardiol. Rep., 12, 6, 10.1007/s11886-009-0080-2 Reeves, 2008, Sex differences in stroke: epidemiology, clinical presentation, medical care, and outcomes, Lancet Neurol., 7, 915, 10.1016/S1474-4422(08)70193-5 Leys, 2005, Poststroke dementia, Lancet Neurol., 4, 752, 10.1016/S1474-4422(05)70221-0 Association As, 2019, 2019 Alzheimer’s disease facts and figures, Alzheimers Dement., 15, 321, 10.1016/j.jalz.2019.01.010 Buckley, 2019, To what extent does age at death account for sex differences in rates of mortality from Alzheimer disease?, Am. J. Epidemiol., 188, 1213, 10.1093/aje/kwz048 Justin, 2013, Heart disease as a risk factor for dementia, Clin Epidemiol., 5, 135 Ahmad, 2017, Hypertension in women: recent advances and lingering questions, Hypertension., 70, 19, 10.1161/HYPERTENSIONAHA.117.08317 Elias, 1993, Untreated blood pressure level is inversely related to cognitive functioning: the Framingham study, Am. J. Epidemiol., 138, 353, 10.1093/oxfordjournals.aje.a116868 Bove, 2014, Age at surgical menopause influences cognitive decline and Alzheimer pathology in older women, Neurology., 82, 222, 10.1212/WNL.0000000000000033 Jackson, 2018, Within the brain: the renin angiotensin system, Int. J. Mol. Sci., 19, 10.3390/ijms19030876 Alhusban, 2015, Compound 21 is pro-angiogenic in the brain and results in sustained recovery after ischemic stroke, J. Hypertens., 33, 170, 10.1097/HJH.0000000000000364 McCarthy, 2014, Direct angiotensin AT2 receptor stimulation using a novel AT2 receptor agonist, compound 21, evokes neuroprotection in conscious hypertensive rats, PLoS One, 9, 10.1371/journal.pone.0095762 Bennion, 2018, Protective effects of the angiotensin II AT2 receptor agonist compound 21 in ischemic stroke: a nose-to-brain delivery approach, Clin. Sci. (Lond.), 132, 581, 10.1042/CS20180100 Ahmed, 2019, Angiotensin receptor (AT2R) agonist C21 prevents cognitive decline after permanent stroke in aged animals-a randomized double- blind pre-clinical study, Behav. Brain Res., 359, 560, 10.1016/j.bbr.2018.10.010 Ahmed, 2018, RAS modulation prevents progressive cognitive impairment after experimental stroke: a randomized, blinded preclinical trial, J. Neuroinflammation, 15, 229, 10.1186/s12974-018-1262-x Ishrat, 2019, Dose-response, therapeutic time-window and tPA-combinatorial efficacy of compound 21: a randomized, blinded preclinical trial in a rat model of thromboembolic stroke, J. Cereb. Blood Flow Metab., 39, 1635, 10.1177/0271678X18764773 Jackson, 2019, Diabetic stroke promotes a sexually dimorphic expansion of T cells, NeuroMolecular Med., 21, 445, 10.1007/s12017-019-08554-6 Khan, 2018, Chronic remote ischemic conditioning is Cerebroprotective and induces vascular remodeling in a VCID model, Transl. Stroke Res., 9, 51, 10.1007/s12975-017-0555-1 Wan, 2004, Design, synthesis, and biological evaluation of the first selective nonpeptide AT2 receptor agonist, J. Med. Chem., 47, 5995, 10.1021/jm049715t Guan, 2011, Vascular protection by angiotensin receptor antagonism involves differential VEGF expression in both hemispheres after experimental stroke, PLoS One, 6, 10.1371/journal.pone.0024551 Sullivan, 2010, Angiotensin (1-7) receptor antagonism equalizes angiotensin II-induced hypertension in male and female spontaneously hypertensive rats, Hypertension., 56, 658, 10.1161/HYPERTENSIONAHA.110.153668 Hafez, 2015, Comparative analysis of different methods of ischemia/reperfusion in hyperglycemic stroke outcomes: interaction with tPA, Transl. Stroke Res., 6, 171, 10.1007/s12975-015-0391-0 Ennaceur, 1997, Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix, Exp. Brain Res., 113, 509, 10.1007/PL00005603 Frye, 2007, Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task, Neurobiol. Learn. Mem., 88, 208, 10.1016/j.nlm.2007.04.003 Gomes Junior, 2018, Anxiolytic effect of anacardic acids from cashew (Anacardium occidentale) nut shell in mice, IUBMB Life, 70, 420, 10.1002/iub.1738 Ahmed, 2018, Role of angiotensin system modulation on progression of cognitive impairment and brain MRI changes in aged hypertensive animals - a randomized double- blind pre-clinical study, Behav. Brain Res., 346, 29, 10.1016/j.bbr.2017.12.007 Eldahshan, 2019, Angiotensin II type 2 receptor stimulation with compound 21 improves neurological function after stroke in female rats: a pilot study, Am. J. Physiol. Heart Circ. Physiol., 316, H1192, 10.1152/ajpheart.00446.2018 Sanz, 2017, drLumi: An open-source package to manage data, calibrate, and conduct quality control of multiplex bead-based immunoassays data analysis, PLoS One, 12, 10.1371/journal.pone.0187901 Winter, 2005, Anxious and hyperactive phenotype following brief ischemic episodes in mice, Biol. Psychiatry, 57, 1166, 10.1016/j.biopsych.2005.02.010 Tuscher, 2015, Regulation of object recognition and object placement by ovarian sex steroid hormones, Behav. Brain Res., 285, 140, 10.1016/j.bbr.2014.08.001 Iadecola, 2016, Impact of hypertension on cognitive function: a scientific statement from the American Heart Association, Hypertension., 68, e67, 10.1161/HYP.0000000000000053 Jackson, 2020, Delayed Administration of Angiotensin II type 2 receptor (AT2R) agonist compound 21 prevents the development of post-stroke cognitive impairment in diabetes through the modulation of microglia polarization, Transl. Stroke Res., 11, 762, 10.1007/s12975-019-00752-5 Robinson, 1979, Differential behavioral and biochemical effects of right and left hemispheric cerebral infarction in the rat, Science., 205, 707, 10.1126/science.462179 Menlove, 2015, Predictors of anxiety after stroke: a systematic review of observational studies, J. Stroke Cerebrovasc. Dis., 24, 1107, 10.1016/j.jstrokecerebrovasdis.2014.12.036 Campbell Burton, 2013, Frequency of anxiety after stroke: a systematic review and meta-analysis of observational studies, Int. J. Stroke, 8, 545, 10.1111/j.1747-4949.2012.00906.x Ranjbar, 2018, Angiotensin II type 1 receptor blocker losartan attenuates locomotor, anxiety-like behavior, and passive avoidance learning deficits in a sub-chronic stress model, Iran J. Basic Med. Sci., 21, 856 Tashev, 2018, Involvement of hippocampal angiotensin 1 receptors in anxiety-like behaviour of olfactory bulbectomized rats, Pharmacol. Rep., 70, 847, 10.1016/j.pharep.2018.03.001 Yang, 2015, Chronic oleoylethanolamide treatment improves spatial cognitive deficits through enhancing hippocampal neurogenesis after transient focal cerebral ischemia, Biochem. Pharmacol., 94, 270, 10.1016/j.bcp.2015.02.012 Yu, 2018, Hydroxysafflor yellow a (HSYA) improves learning and memory in cerebral ischemia reperfusion-injured rats via recovering synaptic plasticity in the Hippocampus, Front. Cell. Neurosci., 12, 371, 10.3389/fncel.2018.00371 Izquierdo, 2002, Molecular pharmacological dissection of short- and long-term memory, Cell. Mol. Neurobiol., 22, 269, 10.1023/A:1020715800956 Orduna, 2017, Impulsivity in spontaneously hypertensive rats: within-subjects comparison of sensitivity to delay and to amount of reinforcement, Behav. Brain Res., 328, 178, 10.1016/j.bbr.2017.04.033 Sanabria, 2008, Evidence for impulsivity in the spontaneously hypertensive rat drawn from complementary response-withholding tasks, Behav. Brain Funct., 4, 7, 10.1186/1744-9081-4-7 Adriani, 2003, The spontaneously hypertensive-rat as an animal model of ADHD: evidence for impulsive and non-impulsive subpopulations, Neurosci. Biobehav. Rev., 27, 639, 10.1016/j.neubiorev.2003.08.007 Tanaka, 2014, Cortical representations are reinstated by the hippocampus during memory retrieval, Neuron., 84, 347, 10.1016/j.neuron.2014.09.037 Myskiw, 2012, Posterior parietal cortex and long-term memory: some data from laboratory animals, Front. Integr. Neurosci., 6, 8, 10.3389/fnint.2012.00008 Ghosh, 2015, Neuronal encoding of the switch from specific to generalized fear, Nat. Neurosci., 18, 112, 10.1038/nn.3888 Cammarota, 2007, Studies of short-term avoidance memory Giovannini, 2015, The integrated role of ACh, ERK and mTOR in the mechanisms of hippocampal inhibitory avoidance memory, Neurobiol. Learn. Mem., 119, 18, 10.1016/j.nlm.2014.12.014 Tota, 2012, Central angiotensin converting enzyme facilitates memory impairment in intracerebroventricular streptozotocin treated rats, Behav. Brain Res., 226, 317, 10.1016/j.bbr.2011.07.047 Zhang, 2012, The neuroprotective effect of losartan through inhibiting AT1/ASK1/MKK4/JNK3 pathway following cerebral I/R in rat hippocampal CA1 region, CNS Neurosci Ther., 18, 981, 10.1111/cns.12015 Barnes, 1990, Angiotensin II inhibits cortical cholinergic function: implications for cognition, J. Cardiovasc. Pharmacol., 16, 234, 10.1097/00005344-199008000-00009 McGaugh, 1989, Involvement of hormonal and neuromodulatory systems in the regulation of memory storage, Annu. Rev. Neurosci., 12, 255, 10.1146/annurev.ne.12.030189.001351 Ennaceur, 1988, A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data, Behav. Brain Res., 31, 47, 10.1016/0166-4328(88)90157-X Iwanami, 2015, Direct angiotensin II type 2 receptor stimulation by compound 21 prevents vascular dementia, J. Am. Soc. Hypertens., 9, 250, 10.1016/j.jash.2015.01.010 Hayashi, 2003, Temporal profile of angiogenesis and expression of related genes in the brain after ischemia, J. Cereb. Blood Flow Metab., 23, 166, 10.1097/01.WCB.0000041283.53351.CB Alhusban, 2016, ARBs improve stroke outcome through an AT2-dependent, BDNF-induced proangiogenic and prorecovery response, Neural Regen. Res., 11, 912, 10.4103/1673-5374.184484 Alhusban, 2017, Mechanisms of acute neurovascular protection with AT1 blockade after stroke: effect of prestroke hypertension, PLoS One, 12, 10.1371/journal.pone.0178867 Fouda, 2017, Brain-derived neurotrophic factor knockdown blocks the Angiogenic and protective effects of angiotensin modulation after experimental stroke, Mol. Neurobiol., 54, 661, 10.1007/s12035-015-9675-3 Tipton, 2014, Female spontaneously hypertensive rats have a compensatory increase in renal regulatory T cells in response to elevations in blood pressure, Hypertension., 64, 557, 10.1161/HYPERTENSIONAHA.114.03512