Estrogen receptor involvement in vascular cognitive impairment and vascular dementia pathogenesis and treatment

Erkinjuntti T, Roman G, Gauthier S, Feldman H, Rockwood K. Emerging therapies for vascular dementia and vascular cognitive impairment. Stroke. 2004;35(4):1010–7. https://doi.org/10.1161/01.STR.0000120731.88236.33. Roman GC, Sachdev P, Royall DR, Bullock RA, Orgogozo JM, Lopez-Pousa S, et al. Vascular cognitive disorder: a new diagnostic category updating vascular cognitive impairment and vascular dementia. J Neurol Sci. 2004;226(1–2):81–7. https://doi.org/10.1016/j.jns.2004.09.016. Dichgans M, Leys D. Vascular cognitive impairment. Circ Res. 2017;120(3):573–91. https://doi.org/10.1161/CIRCRESAHA.116.308426. van der Flier WM, Skoog I, Schneider JA, Pantoni L, Mok V, Chen CLH, et al. Vascular cognitive impairment. Nat Rev Dis Primers. 2018;4:18003. https://doi.org/10.1038/nrdp.2018.3. Appelman Y, van Rijn BB, Ten Haaf ME, Boersma E, Peters SA. Sex differences in cardiovascular risk factors and disease prevention. Atherosclerosis. 2015;241(1):211–8. https://doi.org/10.1016/j.atherosclerosis.2015.01.027. Regitz-Zagrosek V, Kararigas G. Mechanistic pathways of sex differences in cardiovascular disease. Physiol Rev. 2017;97(1):1–37. https://doi.org/10.1152/physrev.00021.2015. Barnes LL, Wilson RS, Bienias JL, Schneider JA, Evans DA, Bennett DA. Sex differences in the clinical manifestations of Alzheimer disease pathology. Arch Gen Psychiatry. 2005;62(6):685–91. https://doi.org/10.1001/archpsyc.62.6.685. Laws KR, Irvine K, Gale TM. Sex differences in cognitive impairment in Alzheimer’s disease. World J Psychiatry. 2016;6(1):54–65. https://doi.org/10.5498/wjp.v6.i1.54. Li R, Singh M. Sex differences in cognitive impairment and Alzheimer’s disease. Front Neuroendocrinol. 2014;35(3):385–403. https://doi.org/10.1016/j.yfrne.2014.01.002. Mazure CM, Swendsen J. Sex differences in Alzheimer’s disease and other dementias. Lancet Neurol. 2016;15(5):451–2. https://doi.org/10.1016/S1474-4422(16)00067-3. Wilson RS, Weir DR, Leurgans SE, Evans DA, Hebert LE, Langa KM, et al. Sources of variability in estimates of the prevalence of Alzheimer’s disease in the United States. Alzheimers Dement. 2011;7(1):74–9. https://doi.org/10.1016/j.jalz.2010.11.006. Mielke MM, Vemuri P, Rocca WA. Clinical epidemiology of Alzheimer’s disease: assessing sex and gender differences. Clin Epidemiol. 2014;6:37–48. https://doi.org/10.2147/CLEP.S37929. Ji Y, Urakami K, Wada-Isoe K, Adachi Y, Nakashima K. Estrogen receptor gene polymorphisms in patients with Alzheimer’s disease, vascular dementia and alcohol-associated dementia. Dement Geriatr Cogn Disord. 2000;11(3):119–22. https://doi.org/10.1159/000017224. Xin J, Zhang J, Gao Y, Xiong L. Association of estrogen receptor beta gene polymorphisms with vascular dementia in women. Neurol Sci. 2012;33(5):1029–35. https://doi.org/10.1007/s10072-011-0885-9. Dresner-Pollak R, Kinnar T, Friedlander Y, Sharon N, Rosenmann H, Pollak A. Estrogen receptor beta gene variant is associated with vascular dementia in elderly women. Genet Test Mol Biomarkers. 2009;13(3):339–42. https://doi.org/10.1089/gtmb.2008.0129. Smith EE. Clinical presentations and epidemiology of vascular dementia. Clin Sci (Lond). 2017;131(11):1059–68. https://doi.org/10.1042/CS20160607. Iadecola C, Duering M, Hachinski V, Joutel A, Pendlebury ST, Schneider JA, et al. Vascular cognitive impairment and dementia: JACC scientific expert panel. J Am Coll Cardiol. 2019;73(25):3326–44. https://doi.org/10.1016/j.jacc.2019.04.034. Hebert R, Brayne C. Epidemiology of vascular dementia. Neuroepidemiology. 1995;14(5):240–57. https://doi.org/10.1159/000109800. Rockwood K. Vascular cognitive impairment and vascular dementia. J Neurol Sci. 2002;203–204:23–7. https://doi.org/10.1016/s0022-510x(02)00255-1. Plassman BL, Langa KM, Fisher GG, Heeringa SG, Weir DR, Ofstedal MB, et al. Prevalence of dementia in the United States: the aging, demographics, and memory study. Neuroepidemiology. 2007;29(1–2):125–32. https://doi.org/10.1159/000109998. Gorelick PB, Counts SE, Nyenhuis D. Vascular cognitive impairment and dementia. Biochim Biophys Acta. 2016;1862(5):860–8. https://doi.org/10.1016/j.bbadis.2015.12.015. O’Brien JT, Thomas A. Vascular dementia. Lancet. 2015;386(10004):1698–706. https://doi.org/10.1016/S0140-6736(15)00463-8. Sundboll J, Horvath-Puho E, Adelborg K, Schmidt M, Pedersen L, Botker HE, et al. Higher risk of vascular dementia in myocardial infarction survivors. Circulation. 2018;137(6):567–77. https://doi.org/10.1161/CIRCULATIONAHA.117.029127. Javanshiri K, Waldo ML, Friberg N, Sjovall F, Wickerstrom K, Haglund M, et al. Atherosclerosis, hypertension, and diabetes in Alzheimer’s disease, vascular dementia, and mixed dementia: prevalence and presentation. J Alzheimers Dis. 2018;65(4):1247–58. https://doi.org/10.3233/JAD-180644. Gannon OJ, Robison LS, Custozzo AJ, Zuloaga KL. Sex differences in risk factors for vascular contributions to cognitive impairment & dementia. Neurochem Int. 2019;127:38–55. https://doi.org/10.1016/j.neuint.2018.11.014. Du SQ, Wang XR, Xiao LY, Tu JF, Zhu W, He T, et al. Molecular mechanisms of vascular dementia: what can be learned from animal models of chronic cerebral hypoperfusion? Mol Neurobiol. 2017;54(5):3670–82. https://doi.org/10.1007/s12035-016-9915-1. Kalaria RN. The pathology and pathophysiology of vascular dementia. Neuropharmacology. 2018;134(Pt B):226–39. https://doi.org/10.1016/j.neuropharm.2017.12.030. Venkat P, Chopp M, Chen J. Models and mechanisms of vascular dementia. Exp Neurol. 2015;272:97–108. https://doi.org/10.1016/j.expneurol.2015.05.006. Bowler JV, Eliasziw M, Steenhuis R, Munoz DG, Fry R, Merskey H, et al. Comparative evolution of Alzheimer disease, vascular dementia, and mixed dementia. Arch Neurol. 1997;54(6):697–703. https://doi.org/10.1001/archneur.1997.00550180021007. Rasquin SM, Lodder J, Verhey FR. Predictors of reversible mild cognitive impairment after stroke: a 2-year follow-up study. J Neurol Sci. 2005;229–230:21–5. https://doi.org/10.1016/j.jns.2004.11.015. Langa KM, Foster NL, Larson EB. Mixed dementia: emerging concepts and therapeutic implications. JAMA. 2004;292(23):2901–8. https://doi.org/10.1001/jama.292.23.2901. Cui J, Shen Y, Li R. Estrogen synthesis and signaling pathways during aging: from periphery to brain. Trends Mol Med. 2013;19(3):197–209. https://doi.org/10.1016/j.molmed.2012.12.007. Prossnitz ER, Barton M. The G-protein-coupled estrogen receptor GPER in health and disease. Nat Rev Endocrinol. 2011;7(12):715–26. https://doi.org/10.1038/nrendo.2011.122. Deroo BJ, Korach KS. Estrogen receptors and human disease. J Clin Invest. 2006;116(3):561–70. https://doi.org/10.1172/JCI27987. Burns KA, Korach KS. Estrogen receptors and human disease: an update. Arch Toxicol. 2012;86(10):1491–504. https://doi.org/10.1007/s00204-012-0868-5. Bean LA, Ianov L, Foster TC. Estrogen receptors, the hippocampus, and memory. Neuroscientist. 2014;20(5):534–45. https://doi.org/10.1177/1073858413519865. Garcia-Segura LM, Diz-Chaves Y, Perez-Martin M, Darnaudery M. Estradiol, insulin-like growth factor-I and brain aging. Psychoneuroendocrinology. 2007;32(Suppl 1):S57–61. https://doi.org/10.1016/j.psyneuen.2007.03.001. Foster TC. Role of estrogen receptor alpha and beta expression and signaling on cognitive function during aging. Hippocampus. 2012;22(4):656–69. https://doi.org/10.1002/hipo.20935. Wilson ME, Rosewell KL, Kashon ML, Shughrue PJ, Merchenthaler I, Wise PM. Age differentially influences estrogen receptor-alpha (ERalpha) and estrogen receptor-beta (ERbeta) gene expression in specific regions of the rat brain. Mech Ageing Dev. 2002;123(6):593–601. https://doi.org/10.1016/s0047-6374(01)00406-7. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, Milner TA, et al. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci. 2002;22(9):3608–14. Stirone C, Duckles SP, Krause DN. Multiple forms of estrogen receptor-alpha in cerebral blood vessels: regulation by estrogen. Am J Physiol Endocrinol Metab. 2003;284(1):E184–92. https://doi.org/10.1152/ajpendo.00165.2002. Aenlle KK, Foster TC. Aging alters the expression of genes for neuroprotection and synaptic function following acute estradiol treatment. Hippocampus. 2010;20(9):1047–60. https://doi.org/10.1002/hipo.20703. Reslan OM, Yin Z, do Nascimento GR, Khalil RA. Subtype-specific estrogen receptor-mediated vasodilator activity in the cephalic, thoracic, and abdominal vasculature of female rat. J Cardiovasc Pharmacol. 2013;62(1):26–40. https://doi.org/10.1097/FJC.0b013e31828bc88a. Khalil RA. Estrogen, vascular estrogen receptor and hormone therapy in postmenopausal vascular disease. Biochem Pharmacol. 2013;86(12):1627–42. https://doi.org/10.1016/j.bcp.2013.09.024. Yaffe K, Lui LY, Grady D, Stone K, Morin P. Estrogen receptor 1 polymorphisms and risk of cognitive impairment in older women. Biol Psychiatry. 2002;51(8):677–82. https://doi.org/10.1016/s0006-3223(01)01289-6. Olsen L, Rasmussen HB, Hansen T, Bagger YZ, Tanko LB, Qin G, et al. Estrogen receptor alpha and risk for cognitive impairment in postmenopausal women. Psychiatr Genet. 2006;16(2):85–8. https://doi.org/10.1097/01.ypg.0000194445.27555.71. Yaffe K, Lindquist K, Sen S, Cauley J, Ferrell R, Penninx B, et al. Estrogen receptor genotype and risk of cognitive impairment in elders: findings from the Health ABC study. Neurobiol Aging. 2009;30(4):607–14. https://doi.org/10.1016/j.neurobiolaging.2007.08.003. Iorga A, Cunningham CM, Moazeni S, Ruffenach G, Umar S, Eghbali M. The protective role of estrogen and estrogen receptors in cardiovascular disease and the controversial use of estrogen therapy. Biol Sex Differ. 2017;8(1):33. https://doi.org/10.1186/s13293-017-0152-8. Maekawa H, Tada Y, Yagi K, Miyamoto T, Kitazato KT, Korai M, et al. Bazedoxifene, a selective estrogen receptor modulator, reduces cerebral aneurysm rupture in Ovariectomized rats. J Neuroinflammation. 2017;14(1):197. https://doi.org/10.1186/s12974-017-0966-7. Zhu Y, Zhang Q, Zhang W, Li N, Dai Y, Tu J, et al. Protective effect of 17beta-estradiol upon hippocampal spine density and cognitive function in an animal model of vascular dementia. Sci Rep. 2017;7:42660. https://doi.org/10.1038/srep42660. Lu CL, Herndon C. New roles for neuronal estrogen receptors. Neurogastroenterol Motil. 2017;29(7). https://doi.org/10.1111/nmo.13121. Tang H, Zhang Q, Yang L, Dong Y, Khan M, Yang F, et al. GPR30 mediates estrogen rapid signaling and neuroprotection. Mol Cell Endocrinol. 2014;387(1–2):52–8. https://doi.org/10.1016/j.mce.2014.01.024. Wang ZF, Pan ZY, Xu CS, Li ZQ. Activation of G-protein coupled estrogen receptor 1 improves early-onset cognitive impairment via PI3K/Akt pathway in rats with traumatic brain injury. Biochem Biophys Res Commun. 2017;482(4):948–53. https://doi.org/10.1016/j.bbrc.2016.11.138. Zhao TZ, Ding Q, Hu J, He SM, Shi F, Ma LT. GPER expressed on microglia mediates the anti-inflammatory effect of estradiol in ischemic stroke. Brain Behav. 2016;6(4):e00449. https://doi.org/10.1002/brb3.449.