Menopause and Parkinson’s disease. Interaction between estrogens and brain renin-angiotensin system in dopaminergic degeneration

Al Sweidi, 2012, Oestrogen receptors and signalling pathways: implications for neuroprotective effects of sex steroids in Parkinson’s disease, J. Neuroendocrinol., 24, 48, 10.1111/j.1365-2826.2011.02193.x Alberici, 2009, Mitochondrial ATP-sensitive K(+) channels as redox signals to liver mitochondria in response to hypertriglyceridemia, Free Radic. Biol. Med., 47, 1432, 10.1016/j.freeradbiomed.2009.08.013 Allen, 1992, Angiotensin II receptor binding associated with nigrostriatal dopaminergic neurons in human basal ganglia, Ann. Neurol., 32, 339, 10.1002/ana.410320306 Andersen, 2004, Oxidative stress in neurodegeneration: cause or consequence?, Nat. Med., 10, S18, 10.1038/nrn1434 Antonicelli, 2008, Prevention of cardiovascular events in early menopause: a possible role for hormone replacement therapy, Int. J. Cardiol., 130, 140, 10.1016/j.ijcard.2008.03.051 Armando, 2002, Estrogen upregulates renal angiotensin II AT(2) receptors, Am. J. Physiol. Renal Physiol., 283, F934, 10.1152/ajprenal.00145.2002 Azcoitia, 2011, Estradiol synthesis within the human brain, Neuroscience, 191, 139, 10.1016/j.neuroscience.2011.02.012 Babior, 2004, NADPH oxidase, Curr. Opin. Immunol., 16, 42, 10.1016/j.coi.2003.12.001 Baiardi, 2005, Estrogen upregulates renal angiotensin II AT1 and AT2 receptors in the rat, Regul. Pept., 124, 7, 10.1016/j.regpep.2004.06.021 Bains, 2007, Neuroprotection by estrogen against MPP+-induced dopamine neuron death is mediated by ERalpha in primary cultures of mouse mesencephalon, Exp. Neurol., 204, 767, 10.1016/j.expneurol.2007.01.020 Baker, 2004, Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor beta, Endocrinology, 145, 5021, 10.1210/en.2004-0619 Baldereschi, 2000, Parkinson’s disease and parkinsonism in a longitudinal study: two-fold higher incidence in men. ILSA Working Group. Italian Longitudinal Study on Aging, Neurology, 55, 1358, 10.1212/WNL.55.9.1358 Balthazart, 2006, Is brain estradiol a hormone or a neurotransmitter?, Trends Neurosci., 29, 241, 10.1016/j.tins.2006.03.004 Benedetti, 2001, Hysterectomy, menopause, and estrogen use preceding Parkinson’s disease: an exploratory case-control study, Mov. Disord., 16, 830, 10.1002/mds.1170 Berg, 2004, Redox imbalance, Cell Tissue Res., 318, 201, 10.1007/s00441-004-0976-5 Bernhart, 2010, Lysophosphatidic acid receptor activation affects the C13NJ microglia cell line proteome leading to alterations in glycolysis, motility, and cytoskeletal architecture, Proteomics, 10, 141, 10.1002/pmic.200900195 Blasko, 2009, Beneficial role of the GPR30 agonist G-1 in an animal model of multiple sclerosis, J. Neuroimmunol., 214, 67, 10.1016/j.jneuroim.2009.06.023 Block, 2007, Microglia-mediated neurotoxicity: uncovering the molecular mechanisms, Nat. Rev. Neurosci., 8, 57, 10.1038/nrn2038 Borrajo, 2014, Microglial TNF-alpha mediates enhancement of dopaminergic degeneration by brain angiotensin, Glia, 62, 145, 10.1002/glia.22595 Borrajo, 2014, Inhibition of the microglial response is essential for the neuroprotective effects of Rho-kinase inhibitors on MPTP-induced dopaminergic cell death, Neuropharmacology, 85, 1, 10.1016/j.neuropharm.2014.05.021 Bourque, 2013, Implication of GPER1 in neuroprotection in a mouse model of Parkinson’s disease, Neurobiol. Aging, 34, 887, 10.1016/j.neurobiolaging.2012.05.022 Bourque, 2014, Raloxifene activates G protein-coupled estrogen receptor 1/Akt signaling to protect dopamine neurons in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mice, Neurobiol. Aging, 35, 2347, 10.1016/j.neurobiolaging.2014.03.017 Brendel, 2013, Differential regulation of apoptosis-associated genes by estrogen receptor alpha in human neuroblastoma cells, Restor. Neurol. Neurosci., 31, 199 Brichta, 2014, Molecular determinants of selective dopaminergic vulnerability in Parkinson’s disease: an update, Front. Neuroanat., 8, 152, 10.3389/fnana.2014.00152 Brinton, 2008, The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications, Trends Neurosci., 31, 529, 10.1016/j.tins.2008.07.003 Brinton, 2009, Reproductive aging of females: neural systems, 2199 Brinton, 2015, Perimenopause as a neurological transition state, Nat. Rev. Endocrinol., 11, 393, 10.1038/nrendo.2015.82 Cai, 2005, NAD(P)H oxidase-dependent self-propagation of hydrogen peroxide and vascular disease, Circ. Res., 96, 818, 10.1161/01.RES.0000163631.07205.fb Callier, 2002, Evaluation of the protective effect of oestradiol against toxicity induced by 6-hydroxydopamine and 1-methyl-4-phenylpyridinium ion (MPP+) towards dopaminergic mesencephalic neurones in primary culture, J. Neurochem., 80, 307, 10.1046/j.0022-3042.2001.00693.x Campos, 2012, GDNF contributes to oestrogen-mediated protection of midbrain dopaminergic neurones, J. Neuroendocrinol., 24, 1386, 10.1111/j.1365-2826.2012.02348.x Carlsson, 1962, Cellular localization of brain monoamines, Acta Physiol. Scand. Suppl., 56, 1 Cerciat, 2010, Selective estrogen receptor modulators decrease the production of interleukin-6 and interferon-gamma-inducible protein-10 by astrocytes exposed to inflammatory challenge in vitro, Glia, 58, 93, 10.1002/glia.20904 Chabrashvili, 2003, 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, R117, 10.1152/ajpregu.00476.2002 Chai, 1987, Angiotensin converting enzyme in rat brain visualized by quantitative in vitro autoradiography, Neuroscience, 20, 615, 10.1016/0306-4522(87)90114-X Chakrabarty, 2008, Estrogen elicits dorsal root ganglion axon sprouting via a renin-angiotensin system, Endocrinology, 149, 3452, 10.1210/en.2008-0061 Chen, 2008, Estrogen prevents intestinal inflammation after trauma-hemorrhage via downregulation of angiotensin II and angiotensin II subtype I receptor, Am. J. Physiol. Gastrointest. Liver Physiol., 295, G1131, 10.1152/ajpgi.90443.2008 Chlebowski, 2010, Estrogen plus progestin and breast cancer incidence and mortality in postmenopausal women, JAMA, 304, 1684, 10.1001/jama.2010.1500 Choi, 2010, Aging enhances the neuroinflammatory response and alpha-synuclein nitration in rats, Neurobiol. Aging, 31, 1649, 10.1016/j.neurobiolaging.2008.09.010 Clark, 2008, Angiotensin II induces proliferation of cultured rat astrocytes through c-Jun N-terminal kinase, Brain Res. Bull., 75, 101, 10.1016/j.brainresbull.2007.07.028 Clarkson, 2007, Estrogen effects on arteries vary with stage of reproductive life and extent of subclinical atherosclerosis progression, Menopause, 14, 373, 10.1097/GME.0b013e31803c764d Clarkson, 2009, Coronary heart disease of females: lessons learned from nonhuman primates, Am. J. Primatol., 71, 785, 10.1002/ajp.20693 Cruz-Muros, 2007, Aging of the rat mesostriatal system: differences between the nigrostriatal and the mesolimbic compartments, Exp. Neurol., 204, 147, 10.1016/j.expneurol.2006.10.004 Cruz-Muros, 2009, Aging effects on the dopamine transporter expression and compensatory mechanisms, Neurobiol. Aging, 30, 973, 10.1016/j.neurobiolaging.2007.09.009 Csiszar, 2003, Aging-induced proinflammatory shift in cytokine expression profile in coronary arteries, FASEB J., 17, 1183, 10.1096/fj.02-1049fje Cuadra, 2010, A current view of brain renin-angiotensin system: is the (pro)renin receptor the missing link?, Pharmacol. Ther., 125, 27, 10.1016/j.pharmthera.2009.07.007 Currie, 2004, Postmenopausal estrogen use affects risk for Parkinson disease, Arch. Neurol., 61, 886, 10.1001/archneur.61.6.886 Daniel, 2013, Estrogens, estrogen receptors, and female cognitive aging: the impact of timing, Horm. Behav., 63, 231, 10.1016/j.yhbeh.2012.05.003 Das, 2011, Estrogen receptor agonists and estrogen attenuate TNF-alpha-induced apoptosis in VSC4.1 motoneurons, J. Endocrinol., 208, 171, 10.1677/JOE-10-0338 Dauer, 2003, Parkinson’s disease: mechanisms and models, Neuron, 39, 889, 10.1016/S0896-6273(03)00568-3 De Marinis, 2013, 17beta-Oestradiol anti-inflammatory effects in primary astrocytes require oestrogen receptor beta-mediated neuroglobin up-regulation, J. Neuroendocrinol., 25, 260, 10.1111/jne.12007 de Villiers, 2013, Global consensus statement on menopausal hormone therapy, Climacteric, 16, 203, 10.3109/13697137.2013.771520 Dean, 2005, 17beta-Estradiol downregulates tissue angiotensin-converting enzyme and ANG II type 1 receptor in female rats, Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R759, 10.1152/ajpregu.00595.2004 Diaz-Ruiz, 2015, Reciprocal regulation between sirtuin-1 and angiotensin-II in the substantia nigra: implications for aging and neurodegeneration, Oncotarget, 6, 26675, 10.18632/oncotarget.5596 Dluzen, 1997, Estrogen decreases corpus striatal neurotoxicity in response to 6-hydroxydopamine, Brain Res., 767, 340, 10.1016/S0006-8993(97)00630-6 Dominguez-Meijide, 2014, Effect of chronic treatment with angiotensin type 1 receptor antagonists on striatal dopamine levels in normal rats and in a rat model of Parkinson’s disease treated with L-DOPA, Neuropharmacology, 76, 156, 10.1016/j.neuropharm.2013.07.016 Doughan, 2008, Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction, Circ. Res., 102, 488, 10.1161/CIRCRESAHA.107.162800 Dubal, 2006, Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERalpha in estradiol-mediated protection against delayed cell death, Endocrinology, 147, 3076, 10.1210/en.2005-1177 Elbaz, 2002, Risk tables for parkinsonism and Parkinson’s disease, J. Clin. Epidemiol., 55, 25, 10.1016/S0895-4356(01)00425-5 Fahn, 1992, The oxidant stress hypothesis in Parkinson’s disease: evidence supporting it, Ann. Neurol., 32, 804, 10.1002/ana.410320616 Farber, 2005, Dopamine and noradrenaline control distinct functions in rodent microglial cells, Mol. Cell. Neurosci., 29, 128, 10.1016/j.mcn.2005.01.003 Fischer, 2002, Renin angiotensin system and gender differences in the cardiovascular system, Cardiovasc. Res., 53, 672, 10.1016/S0008-6363(01)00479-5 Fisher, 2001, Adrenal response to angiotensin II in black hypertension: lack of sexual dimorphism, Hypertension, 38, 373, 10.1161/01.HYP.38.3.373 Fogle, 2007, Ovarian androgen production in postmenopausal women, J. Clin. Endocrinol. Metab., 92, 3040, 10.1210/jc.2007-0581 Funakoshi, 2006, G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane, Biochem. Biophys. Res. Commun., 346, 904, 10.1016/j.bbrc.2006.05.191 Ganong, 1994, Origin of the angiotensin II secreted by cells, Proc. Soc. Exp. Biol. Med., 205, 213, 10.3181/00379727-205-43699A Garrido-Gil, 2012, Involvement of PPAR-gamma in the neuroprotective and anti-inflammatory effects of angiotensin type 1 receptor inhibition: effects of the receptor antagonist telmisartan and receptor deletion in a mouse MPTP model of Parkinson’s disease, J. Neuroinflammation, 9, 38, 10.1186/1742-2094-9-38 Garrido-Gil, 2013, Brain angiotensin regulates iron homeostasis in dopaminergic neurons and microglial cells, Exp. Neurol., 250, 384, 10.1016/j.expneurol.2013.10.013 Garrido-Gil, 2013, Expression of angiotensinogen and receptors for angiotensin and prorenin in the monkey and human substantia nigra: an intracellular renin-angiotensin system in the nigra, Brain Struct. Funct., 218, 373, 10.1007/s00429-012-0402-9 Garrido, 2009, NADPH oxidases and angiotensin II receptor signaling, Mol. Cell. Endocrinol., 302, 148, 10.1016/j.mce.2008.11.003 Gerhard, 2006, In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson’s disease, Neurobiol. Dis., 21, 404, 10.1016/j.nbd.2005.08.002 Gildea, 2009, Dopamine and angiotensin as renal counterregulatory systems controlling sodium balance, Curr. Opin. Nephrol. Hypertens., 18, 28, 10.1097/MNH.0b013e32831a9e0b Gillies, 2014, Sex differences in Parkinson’s disease, Front. Neuroendocrinol., 35, 370, 10.1016/j.yfrne.2014.02.002 Gold, 2013, Factors related to age at natural menopause: longitudinal analyses from SWAN, Am. J. Epidemiol., 178, 70, 10.1093/aje/kws421 Gómez-Tortosa, 2001, Cortical neurons expressing calcium binding proteins are spared in dementia with Lewy bodies, Acta Neuropathol., 101, 36, 10.1007/s004010000270 Grammatopoulos, 2007, Angiotensin type 1 receptor antagonist losartan, reduces MPTP-induced degeneration of dopaminergic neurons in substantia nigra, Mol. Neurodegener., 2, 1, 10.1186/1750-1326-2-1 Greenamyre, 2004, Biomedicine. Parkinson’s–divergent causes, convergent mechanisms, Science, 304, 1120, 10.1126/science.1098966 Greenwood, 2003, Lovastatin inhibits brain endothelial cell Rho-mediated lymphocyte migration and attenuates experimental autoimmune encephalomyelitis, FASEB J., 17, 905, 10.1096/fj.02-1014fje Griendling, 2000, NAD(P)H oxidase: role in cardiovascular biology and disease, Circ. Res., 86, 494, 10.1161/01.RES.86.5.494 Guidozzi, 2014, South African Menopause Society revised consensus position statement on menopausal hormone therapy, 2014, S. Afr. Med. J., 104, 537, 10.7196/SAMJ.8423 Harding, 1988, Inability of [125I]Sar1, Ile8-angiotensin II to move between the blood and cerebrospinal fluid compartments, J. Neurochem., 50, 554, 10.1111/j.1471-4159.1988.tb02946.x Harlow, 2011, Menstruation and the menopausal transition, Obstet. Gynecol. Clin. North Am., 38, 595, 10.1016/j.ogc.2011.05.010 Harman, 2005, Is the estrogen controversy over? Deconstructing the Women’s Health Initiative study: a critical evaluation of the evidence, Ann. N. Y. Acad. Sci., 1052, 43, 10.1196/annals.1347.004 Henriques, 2008, Androgen increases AT1a receptor expression in abdominal aortas to promote angiotensin II-induced AAAs in apolipoprotein E-deficient mice, Arterioscler. Thromb. Vasc. Biol., 28, 1251, 10.1161/ATVBAHA.107.160382 Henze, 2005, Proliferation of microglial cells induced by 1-methyl-4-phenylpyridinium in mesencephalic cultures results from an astrocyte-dependent mechanism: role of granulocyte macrophage colony-stimulating factor, J. Neurochem., 95, 1069, 10.1111/j.1471-4159.2005.03416.x Hirsch, 2012, Neuroinflammation in Parkinson’s disease, Parkinsonism Relat. Disord., 18, S210, 10.1016/S1353-8020(11)70065-7 Hoban, 2013, Further characterisation of the LPS model of Parkinson’s disease: a comparison of intra-nigral and intra-striatal lipopolysaccharide administration on motor function, microgliosis and nigrostriatal neurodegeneration in the rat, Brain Behav. Immun., 27, 91, 10.1016/j.bbi.2012.10.001 Honing, 2004, RhoA activation promotes transendothelial migration of monocytes via ROCK, J. Leukoc. Biol., 75, 523, 10.1189/jlb.0203054 Hoogwerf, 2010, Renin-angiotensin system blockade and cardiovascular and renal protection, Am. J. Cardiol., 105, 30A, 10.1016/j.amjcard.2009.10.009 Hoshi-Fukushima, 2008, Estrogen and angiotensin II interactions determine cardio-renal damage in Dahl salt-sensitive rats with heart failure, Am. J. Nephrol., 28, 413, 10.1159/000112806 Imanishi, 2005, Estrogen reduces angiotensin II-induced acceleration of senescence in endothelial progenitor cells, Hypertens. Res., 28, 263, 10.1291/hypres.28.263 Irwin, 2012, Selective oestrogen receptor modulators differentially potentiate brain mitochondrial function, J. Neuroendocrinol., 24, 236, 10.1111/j.1365-2826.2011.02251.x Ito, 2006, Ovariectomy augments hypertension through rho-kinase activation in the brain stem in female spontaneously hypertensive rats, Hypertension, 48, 651, 10.1161/01.HYP.0000238125.21656.9e Iwanami, 2010, Low dose of telmisartan prevents ischemic brain damage with peroxisome proliferator-activated receptor-gamma activation in diabetic mice, J. Hypertens., 28, 1730, 10.1097/HJH.0b013e32833a551a Joglar, 2009, The inflammatory response in the MPTP model of Parkinson’s disease is mediated by brain angiotensin: relevance to progression of the disease, J. Neurochem., 109, 656, 10.1111/j.1471-4159.2009.05999.x Jones, 2008, AT2 receptors: functional relevance in cardiovascular disease, Pharmacol. Ther., 120, 292, 10.1016/j.pharmthera.2008.08.009 Kehoe, 2007, Is inhibition of the renin-angiotensin system a new treatment option for Alzheimer’s disease?, Lancet Neurol., 6, 373, 10.1016/S1474-4422(07)70077-7 Khan, 2008, Negative reciprocity between angiotensin II type 1 and dopamine D1 receptors in rat renal proximal tubule cells, Am. J. Physiol. Renal Physiol., 295, F1110, 10.1152/ajprenal.90336.2008 Koprich, 2008, Neuroinflammation mediated by IL-1beta increases susceptibility of dopamine neurons to degeneration in an animal model of Parkinson’s disease, J. Neuroinflammation, 5, 8, 10.1186/1742-2094-5-8 Korse, 2009, Estradiol and testosterone levels are lower after oophorectomy than after natural menopause, Tumour Biol., 30, 37, 10.1159/000199449 Kumar, 1988, Angiotensinogen gene expression in neuronal and glial cells in primary cultures of rat brain, J. Neurosci. Res., 19, 287, 10.1002/jnr.490190302 Kumar, 2007, The intracellular renin-angiotensin system: a new paradigm, Trends Endocrinol. Metab., 18, 208, 10.1016/j.tem.2007.05.001 Labandeira-Garcia, 2015, Rho kinase and dopaminergic degeneration: a promising therapeutic target for Parkinson’s disease, Neuroscientist, 21, 616, 10.1177/1073858414554954 Lanz, 2010, Angiotensin II sustains brain inflammation in mice via TGF-beta, J. Clin. Invest., 120, 2782, 10.1172/JCI41709 Lebouvier, 2009, The second brain and Parkinson’s disease, Eur. J. Neurosci., 30, 735, 10.1111/j.1460-9568.2009.06873.x Leranth, 2000, Estrogen is essential for maintaining nigrostriatal dopamine neurons in primates: implications for Parkinson’s disease and memory, J. Neurosci., 20, 8604, 10.1523/JNEUROSCI.20-23-08604.2000 Levin, 2014, Extranuclear estrogen receptor’s roles in physiology: lessons from mouse models, Am. J. Physiol. Endocrinol. Metab., 307, E133, 10.1152/ajpendo.00626.2013 Lindqvist, 2013, Cerebrospinal fluid inflammatory markers in Parkinson’s disease–associations with depression, fatigue, and cognitive impairment, Brain Behav. Immun., 33, 183, 10.1016/j.bbi.2013.07.007 Liu, 2007, Oestrogen and nigrostriatal dopaminergic neurodegeneration: animal models and clinical reports of Parkinson’s disease, Clin. Exp. Pharmacol. Physiol., 34, 555, 10.1111/j.1440-1681.2007.04616.x Liu, 2002, Effect of estrogen and AT1 receptor blocker on neointima formation, Hypertension, 40, 451, 10.1161/01.HYP.0000033466.05496.89 Liu, 2010, Sex differences in renal angiotensin converting enzyme 2 (ACE2) activity are 17beta-oestradiol-dependent and sex chromosome-independent, Biol. Sex Differ., 1, 6, 10.1186/2042-6410-1-6 Liu, 2014, Female reproductive factors, menopausal hormone use, and Parkinson’s disease, Mov. Disord., 29, 889, 10.1002/mds.25771 Lopez-Martin, 1999, Striatal dopaminergic afferents concentrate in GDNF-positive patches during development and in developing intrastriatal striatal grafts, J. Comp. Neurol., 406, 199, 10.1002/(SICI)1096-9861(19990405)406:2<199::AID-CNE5>3.0.CO;2-Z Lopez-Real, 2005, Angiotensin-converting enzyme inhibition reduces oxidative stress and protects dopaminergic neurons in a 6-hydroxydopamine rat model of Parkinsonism, J. Neurosci. Res., 81, 865, 10.1002/jnr.20598 Luhder, 2009, Small but powerful: short peptide hormones and their role in autoimmune inflammation, J. Neuroimmunol., 217, 1, 10.1016/j.jneuroim.2009.08.008 Lundin, 2014, Formulations of hormone therapy and risk of Parkinson’s disease, Mov. Disord., 29, 1631, 10.1002/mds.26037 Lyons, 1998, Gender differences in Parkinson’s disease, Clin. Neuropharmacol., 21, 118 Maki, 2006, Hormone therapy and cognitive function: is there a critical period for benefit?, Neuroscience, 138, 1027, 10.1016/j.neuroscience.2006.01.001 Marras, 2014, The complexities of hormonal influences and risk of Parkinson’s disease, Mov. Disord., 29, 845, 10.1002/mds.25891 McCormack, 2004, Aging of the nigrostriatal system in the squirrel monkey, J. Comp. Neurol., 471, 387, 10.1002/cne.20036 McGuire, 2007, Gender differences in the renin-angiotensin and nitric oxide systems: relevance in the normal and diseased kidney, Kidney Blood Press. Res., 30, 67, 10.1159/000099150 Milsted, 1990, Astrocyte cultures derived from human brain tissue express angiotensinogen mRNA, Proc. Natl. Acad. Sci. USA, 87, 5720, 10.1073/pnas.87.15.5720 Miller, 2009, Using basic science to design a clinical trial: baseline characteristics of women enrolled in the Kronos Early Estrogen Prevention Study (KEEPS), J. Cardiovasc. Transl. Res., 2, 228, 10.1007/s12265-009-9104-y Miller, 2005, Women, hormones, and clinical trials: a beginning, not an end, J. Appl. Physiol. (1985), 9, 381, 10.1152/japplphysiol.00248.2005 Mintziori, 2015, EMAS position statement: non-hormonal management of menopausal vasomotor symptoms, Maturitas, 81, 410, 10.1016/j.maturitas.2015.04.009 Miyazaki, 2004, Direct evidence for expression of dopamine receptors in astrocytes from basal ganglia, Brain Res., 1029, 120, 10.1016/j.brainres.2004.09.014 Mogi, 2009, Effects of angiotensin II receptor blockers on dementia, Hypertens. Res., 32, 738, 10.1038/hr.2009.110 Morale, 2006, Estrogen, neuroinflammation and neuroprotection in Parkinson’s disease: glia dictates resistance versus vulnerability to neurodegeneration, Neuroscience, 138, 869, 10.1016/j.neuroscience.2005.07.060 Munoz, 2006, Reduction of dopaminergic degeneration and oxidative stress by inhibition of angiotensin converting enzyme in a MPTP model of parkinsonism, Neuropharmacology, 51, 112, 10.1016/j.neuropharm.2006.03.004 Munzel, 2001, Are ACE inhibitors a “magic bullet” against oxidative stress?, Circulation, 104, 1571, 10.1161/hc3801.095585 Nickenig, 1998, Estrogen modulates AT1 receptor gene expression in vitro and in vivo, Circulation, 97, 2197, 10.1161/01.CIR.97.22.2197 Nilsson, 2011, Development of subtype-selective oestrogen receptor-based therapeutics, Nat. Rev. Drug Discov., 10, 778, 10.1038/nrd3551 Nwachukwu, 2014, Resveratrol modulates the inflammatory response via an estrogen receptor-signal integration network, Elife, 3, e02057, 10.7554/eLife.02057 O’Callaghan, 2011, Regulation of angiotensinogen by angiotensin II in mouse primary astrocyte cultures, J. Neurochem., 119, 18, 10.1111/j.1471-4159.2011.07406.x Ohtani, 2001, Chronic estrogen treatment replaces striatal dopaminergic function in ovariectomized rats, Brain Res., 900, 163, 10.1016/S0006-8993(01)02276-4 Ojeda, 2010, Enhanced sensitivity to acute angiotensin II is testosterone dependent in adult male growth-restricted offspring, Am. J. Physiol. Regul. Integr. Comp. Physiol., 298, R1421, 10.1152/ajpregu.00096.2010 Okumura, 2005, Sex difference in vascular injury and the vasoprotective effect of valsartan are related to differential AT2 receptor expression, Hypertension, 46, 577, 10.1161/01.HYP.0000178564.14464.80 Olanow, 1990, Oxidation reactions in Parkinson’s disease, Neurology, 40, 32 Olanow, 2007, The pathogenesis of cell death in Parkinson’s disease–2007, Mov. Disord., 22, S335, 10.1002/mds.21675 Oro, 2007, Type 1 angiotensin receptor pharmacology: signaling beyond G proteins, Pharmacol. Ther., 113, 210, 10.1016/j.pharmthera.2006.10.001 Ouchi, 2005, Microglial activation and dopamine terminal loss in early Parkinson’s disease, Ann. Neurol., 57, 168, 10.1002/ana.20338 Pacelli, 2015, Elevated mitochondrial bioenergetics and axonal arborization size are key contributors to the vulnerability of dopamine neurons, Curr. Biol., 25, 2349, 10.1016/j.cub.2015.07.050 Padia, 2012, Mechanisms of dopamine D(1) and angiotensin type 2 receptor interaction in natriuresis, Hypertension, 59, 437, 10.1161/HYPERTENSIONAHA.111.184788 Panay, 2014, The ’window of opportunity’–should we be taking it?, Climacteric, 17, 211, 10.3109/13697137.2014.917393 Parkinson Study Group, 1996, Impact of deprenyl and tocopherol treatment on Parkinson’s disease in DATATOP patients requiring levodopa, Ann. Neurol., 39, 37, 10.1002/ana.410390107 Pavon, 2010, Parkinson’s disease in women: a call for improved clinical studies and for comparative effectiveness research, Maturitas, 65, 352, 10.1016/j.maturitas.2010.01.001 Phillips, 2008, Brain renin angiotensin in disease, J. Mol. Med., 86, 715, 10.1007/s00109-008-0331-5 Platten, 2009, Blocking angiotensin-converting enzyme induces potent regulatory T cells and modulates TH1- and TH17-mediated autoimmunity, Proc. Natl. Acad. Sci. USA, 106, 14948, 10.1073/pnas.0903958106 Post, 2011, Progression and prognostic factors of motor impairment, disability and quality of life in newly diagnosed Parkinson’s disease, Mov. Disord., 26, 449, 10.1002/mds.23467 Prossnitz, 2011, The G-protein-coupled estrogen receptor GPER in health and disease, Nat. Rev. Endocrinol., 7, 715, 10.1038/nrendo.2011.122 Prossnitz, 2009, Mechanisms of estrogen signaling and gene expression via GPR30, Mol. Cell. Endocrinol., 308, 32, 10.1016/j.mce.2009.03.026 Qin, 2004, NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia, J. Biol. Chem., 279, 1415, 10.1074/jbc.M307657200 Ragonese, 2006, Age at menopause predicts age at onset of Parkinson’s disease, Mov. Disord., 21, 2211, 10.1002/mds.21127 Ragonese, 2004, Risk of Parkinson disease in women: effect of reproductive characteristics, Neurology, 62, 2010, 10.1212/WNL.62.11.2010 Ragonese, 2006, Implications for estrogens in Parkinson’s disease: an epidemiological approach, Ann. N. Y. Acad. Sci., 1089, 373, 10.1196/annals.1386.004 Re, 2004, Tissue renin angiotensin systems, Med. Clin. North Am., 88, 19, 10.1016/S0025-7125(03)00124-X Re, 2015, Studies of intracellular angiotensin II, Methods Mol. Biol., 1234, 1, 10.1007/978-1-4939-1755-6_1 Rettberg, 2014, Estrogen: a master regulator of bioenergetic systems in the brain and body, Front. Neuroendocrinol., 35, 8, 10.1016/j.yfrne.2013.08.001 Rey, 2007, Angiotensin type-1-receptor antagonists reduce 6-hydroxydopamine toxicity for dopaminergic neurons, Neurobiol. Aging, 28, 555, 10.1016/j.neurobiolaging.2006.02.018 Rocca, 2008, Increased risk of parkinsonism in women who underwent oophorectomy before menopause, Neurology, 70, 200, 10.1212/01.wnl.0000280573.30975.6a Rodriguez-Pallares, 2009, The mitochondrial ATP-sensitive potassium channel blocker 5-hydroxydecanoate inhibits toxicity of 6-hydroxydopamine on dopaminergic neurons, Neurotox. Res., 15, 82, 10.1007/s12640-009-9010-8 Rodriguez-Pallares, 2012, Mitochondrial ATP-sensitive potassium channels enhance angiotensin-induced oxidative damage and dopaminergic neuron degeneration. Relevance for aging-associated susceptibility to Parkinson’s disease, Age (Dordr), 34, 863, 10.1007/s11357-011-9284-7 Rodriguez-Pallares, 2007, Mechanism of 6-hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamine-induced degeneration of dopaminergic neurons, J. Neurochem., 103, 145 Rodriguez-Pallares, 2004, Angiotensin II increases differentiation of dopaminergic neurons from mesencephalic precursors via angiotensin type 2 receptors, Eur. J. Neurosci., 20, 1489, 10.1111/j.1460-9568.2004.03621.x Rodriguez-Pallares, 2008, Brain angiotensin enhances dopaminergic cell death via microglial activation and NADPH-derived ROS, Neurobiol. Dis., 31, 58, 10.1016/j.nbd.2008.03.003 Rodriguez-Perez, 2016, Crosstalk between insulin-like growth factor-1 and angiotensin-II in dopaminergic neurons and glial cells: role in neuroinflammation and aging, Oncotarget, 7, 30049, 10.18632/oncotarget.9174 Rodriguez-Perez, 2015, Interaction between NADPH-oxidase and Rho-kinase in angiotensin II-induced microglial activation, Glia, 63, 466, 10.1002/glia.22765 Rodriguez-Perez, 2015, Critical period for dopaminergic neuroprotection by hormonal replacement in menopausal rats, Neurobiol. Aging, 36, 1194, 10.1016/j.neurobiolaging.2014.10.028 Rodriguez-Perez, 2013, Inhibition of Rho kinase mediates the neuroprotective effects of estrogen in the MPTP model of Parkinson’s disease, Neurobiol. Dis., 58, 209, 10.1016/j.nbd.2013.06.004 Rodriguez-Perez, 2011, Renin angiotensin system and gender differences in dopaminergic degeneration, Mol. Neurodegener., 6, 58, 10.1186/1750-1326-6-58 Rodriguez-Perez, 2012, Dopaminergic neuroprotection of hormonal replacement therapy in young and aged menopausal rats: role of the brain angiotensin system, Brain, 135, 124, 10.1093/brain/awr320 Rodriguez-Perez, 2010, Estrogen and angiotensin interaction in the substantia nigra. Relevance to postmenopausal Parkinson’s disease, Exp. Neurol., 224, 517, 10.1016/j.expneurol.2010.05.015 Rossouw, 2002, Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women’s Health Initiative randomized controlled trial, JAMA, 288, 321, 10.1001/jama.288.3.321 Rugbjerg, 2013, Exposure to estrogen and women’s risk for Parkinson’s disease: a prospective cohort study in Denmark, Parkinsonism Relat. Disord., 19, 457, 10.1016/j.parkreldis.2013.01.008 Ruiz-Ortega, 2001, Proinflammatory actions of angiotensins, Curr. Opin. Nephrol. Hypertens., 10, 321, 10.1097/00041552-200105000-00005 Sakata, 2009, Sex-different effect of angiotensin II type 2 receptor on ischemic brain injury and cognitive function, Brain Res., 1300, 14, 10.1016/j.brainres.2009.08.068 Sanchez-Iglesias, 2007, Time-course of brain oxidative damage caused by intrastriatal administration of 6-hydroxydopamine in a rat model of Parkinson’s disease, Neurochem. Res., 32, 99, 10.1007/s11064-006-9232-6 Sandberg, 2003, Sex and the renin angiotensin system: implications for gender differences in the progression of kidney disease, Adv. Ren. Replace. Ther., 10, 15, 10.1053/jarr.2003.50006 Saunders-Pullman, 2011, Gender differences in the risk of familial parkinsonism: beyond LRRK2?, Neurosci. Lett., 496, 125, 10.1016/j.neulet.2011.03.098 Savica, 2013, Risk factors for Parkinson’s disease may differ in men and women: an exploratory study, Horm. Behav., 63, 308, 10.1016/j.yhbeh.2012.05.013 Scott, 2014, Premature menopause and risk of neurological disease: basic mechanisms and clinical implications, Mol. Cell. Endocrinol., 389, 2, 10.1016/j.mce.2014.01.013 Selvamani, 2010, The neurotoxic effects of estrogen on ischemic stroke in older female rats is associated with age-dependent loss of insulin-like growth factor-1, J. Neurosci., 30, 6852, 10.1523/JNEUROSCI.0761-10.2010 Shen, 2014, SIRT1 functions as an important regulator of estrogen-mediated cardiomyocyte protection in angiotensin II-induced heart hypertrophy, Oxid. Med. Cell Longev., 2014, 713894, 10.1155/2014/713894 Sherwin, 2009, Estrogen therapy: is time of initiation critical for neuroprotection?, Nat. Rev. Endocrinol., 5, 620, 10.1038/nrendo.2009.193 Simpkins, 2010, Mitochondrial mechanisms of estrogen neuroprotection, Biochim. Biophys. Acta, 1800, 1113, 10.1016/j.bbagen.2009.11.013 Smith, 2014, Sex differences in Parkinson’s disease and other movement disorders, Exp. Neurol., 259, 44, 10.1016/j.expneurol.2014.03.010 Sohn, 2000, Differential role of angiotensin II receptor subtypes on endothelial superoxide formation, Br. J. Pharmacol., 131, 667, 10.1038/sj.bjp.0703566 Sohrabji, 2013, Stroke neuroprotection: oestrogen and insulin-like growth factor-1 interactions and the role of microglia, J. Neuroendocrinol., 25, 1173, 10.1111/jne.12059 Sonsalla, 2013, The angiotensin converting enzyme inhibitor captopril protects nigrostriatal dopamine neurons in animal models of parkinsonism, Exp. Neurol., 250, 376, 10.1016/j.expneurol.2013.10.014 Spence, 2013, Estrogen mediates neuroprotection and anti-inflammatory effects during EAE through ERalpha signaling on astrocytes but not through ERbeta signaling on astrocytes or neurons, J. Neurosci., 33, 10924, 10.1523/JNEUROSCI.0886-13.2013 Stegbauer, 2009, Role of the renin-angiotensin system in autoimmune inflammation of the central nervous system, Proc. Natl. Acad. Sci. USA, 106, 14942, 10.1073/pnas.0903602106 Stornetta, 1988, Astrocytes synthesize angiotensinogen in brain, Science, 242, 1444, 10.1126/science.3201232 Suarez, 2004, Upregulation of angiotensin II type 2 receptor expression in estrogen-induced pituitary hyperplasia, Am. J. Physiol. Endocrinol. Metab., 286, E786, 10.1152/ajpendo.00477.2003 Sullivan, 2008, Sex and the renin-angiotensin system: inequality between the sexes in response to RAS stimulation and inhibition, Am. J. Physiol. Regul. Integr. Comp. Physiol., 294, R1220, 10.1152/ajpregu.00864.2007 Suzuki, 2007, Timing of estrogen therapy after ovariectomy dictates the efficacy of its neuroprotective and antiinflammatory actions, Proc. Natl. Acad. Sci. USA, 104, 6013, 10.1073/pnas.0610394104 Suzuki, 2003, Inflammation and angiotensin II, Int. J. Biochem. Cell Biol., 35, 881, 10.1016/S1357-2725(02)00271-6 Thomas, 1992, Angiotensinogen is secreted by pure rat neuronal cell cultures, Brain Res., 588, 191, 10.1016/0006-8993(92)91575-Y Touyz, 2004, Reactive oxygen species and angiotensin II signaling in vascular cells – implications in cardiovascular disease, Braz. J. Med. Biol. Res., 37, 1263, 10.1590/S0100-879X2004000800018 Tripanichkul, 2006, Estrogen down-regulates glial activation in male mice following 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine intoxication, Brain Res., 1084, 28, 10.1016/j.brainres.2006.02.029 Tsuda, 2005, Inhibitory effects of AT1 receptor blocker, olmesartan, and estrogen on atherosclerosis via anti-oxidative stress, Hypertension, 45, 545, 10.1161/01.HYP.0000157409.88971.fc Turgeon, 2006, Complex actions of sex steroids in adipose tissue, the cardiovascular system, and brain: insights from basic science and clinical studies, Endocr. Rev., 27, 575, 10.1210/er.2005-0020 Turgeon, 2004, Hormone therapy: physiological complexity belies therapeutic simplicity, Science, 304, 1269, 10.1126/science.1096725 Unger, 1996, Angiotensin receptors, J. Hypertens. Suppl., 14, S95 Ungvari, 2004, Vascular inflammation in aging, Herz, 29, 733, 10.1007/s00059-004-2625-x Valenzuela, 2010, Location of prorenin receptors in primate substantia nigra: effects on dopaminergic cell death, J. Neuropathol. Exp. Neurol., 69, 1130, 10.1097/NEN.0b013e3181fa0308 Van Den Eeden, 2003, Incidence of Parkinson’s disease: variation by age, gender, and race/ethnicity, Am. J. Epidemiol., 157, 1015, 10.1093/aje/kwg068 Vegeto, 2006, The endogenous estrogen status regulates microglia reactivity in animal models of neuroinflammation, Endocrinology, 147, 2263, 10.1210/en.2005-1330 Vegeto, 2008, Estrogen anti-inflammatory activity in brain: a therapeutic opportunity for menopause and neurodegenerative diseases, Front. Neuroendocrinol., 29, 507, 10.1016/j.yfrne.2008.04.001 Verstraeten, 2015, Progress in unraveling the genetic etiology of Parkinson disease in a genomic era, Trends Genet., 31, 140, 10.1016/j.tig.2015.01.004 Vilchez, 2014, The role of protein clearance mechanisms in organismal ageing and age-related diseases, Nat. Commun., 5, 5659, 10.1038/ncomms6659 Villar-Cheda, 2012, Involvement of microglial RhoA/Rho-kinase pathway activation in the dopaminergic neuron death. Role of angiotensin via angiotensin type 1 receptors, Neurobiol. Dis., 47, 268, 10.1016/j.nbd.2012.04.010 Villar-Cheda, 2014, Aging-related dysregulation of dopamine and angiotensin receptor interaction, Neurobiol. Aging, 35, 1726, 10.1016/j.neurobiolaging.2014.01.017 Villar-Cheda, 2010, Nigral and striatal regulation of angiotensin receptor expression by dopamine and angiotensin in rodents: implications for progression of Parkinson’s disease, Eur. J. Neurosci., 32, 1695, 10.1111/j.1460-9568.2010.07448.x Villar-Cheda, 2012, Aging-related changes in the nigral angiotensin system enhances proinflammatory and pro-oxidative markers and 6-OHDA-induced dopaminergic degeneration, Neurobiol. Aging, 33, e201 Wang, 2012, A dominant negative ERbeta splice variant determines the effectiveness of early or late estrogen therapy after ovariectomy in rats, PLoS ONE, 7, e33493, 10.1371/journal.pone.0033493 Wosniak, 2009, Cross-talk between mitochondria and NADPH oxidase: effects of mild mitochondrial dysfunction on angiotensin II-mediated increase in Nox isoform expression and activity in vascular smooth muscle cells, Antioxid. Redox Signal., 11, 1265, 10.1089/ars.2009.2392 Wright, 2013, The brain renin-angiotensin system: a diversity of functions and implications for CNS diseases, Pflugers Arch., 465, 133, 10.1007/s00424-012-1102-2 Wu, 2013, Targeting estrogen receptor beta in microglia and T cells to treat experimental autoimmune encephalomyelitis, Proc. Natl. Acad. Sci. USA, 110, 3543, 10.1073/pnas.1300313110 Xue, 2007, Sex differences in angiotensin II- induced hypertension, Braz. J. Med. Biol. Res., 40, 727, 10.1590/S0100-879X2007000500018 Xue, 2007, Estrogen receptor-alpha mediates estrogen protection from angiotensin II-induced hypertension in conscious female mice, Am. J. Physiol. Heart Circ. Physiol., 292, H1770, 10.1152/ajpheart.01011.2005 Xue, 2008, Central estrogen inhibition of angiotensin II-induced hypertension in male mice and the role of reactive oxygen species, Am. J. Physiol. Heart Circ. Physiol., 295, H1025, 10.1152/ajpheart.00021.2008 Yager, 2007, Mitochondrial estrogen receptors–new insights into specific functions, Trends Endocrinol. Metab., 18, 89, 10.1016/j.tem.2007.02.006 Yan, 2012, Nogo-66 inhibits adhesion and migration of microglia via GTPase Rho pathway in vitro, J. Neurochem., 120, 721, 10.1111/j.1471-4159.2011.07619.x Zalba, 2001, Oxidative stress in arterial hypertension: role of NAD(P)H oxidase, Hypertension, 38, 1395, 10.1161/hy1201.099611 Zawada, 2011, Generation of reactive oxygen species in 1-methyl-4-phenylpyridinium (MPP+) treated dopaminergic neurons occurs as an NADPH oxidase-dependent two-wave cascade, J. Neuroinflammation, 8, 129, 10.1186/1742-2094-8-129 Zhang, 2007, Role of mitochondria in angiotensin II-induced reactive oxygen species and mitogen-activated protein kinase activation, Cardiovasc. Res., 76, 204, 10.1016/j.cardiores.2007.07.014 Zhang, 2009, Estrogen attenuates ischemic oxidative damage via an estrogen receptor alpha-mediated inhibition of NADPH oxidase activation, J. Neurosci., 29, 13823, 10.1523/JNEUROSCI.3574-09.2009