884
Views
1
CrossRef citations to date
0
Altmetric
Reviews

Interactions between estradiol, diabetes, and brain aging and the risk for cognitive impairment

ORCID Icon, ORCID Icon & ORCID Icon
Pages 359-365 | Received 29 Jul 2020, Accepted 04 Jan 2021, Published online: 15 Feb 2021

References

  • Shumaker SA, Legault C, Kuller L, et al. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: women’s Health Initiative Memory Study. JAMA 2004;291:2947–58
  • Shumaker SA, Legault C, Rapp SR, et al. Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women’s Health Initiative Memory Study: a randomized controlled trial. JAMA 2003;289:2651–62
  • Espeland MA, Tindle HA, Bushnell CA, et al. Brain volumes, cognitive impairment, and conjugated equine estrogens. J Gerontol A Biol Sci Med Sci 2009;64:1243–50
  • Zhang T, Casanova R, Resnick SM, et al. Effects of hormone therapy on brain volumes changes of postmenopausal women revealed by optimally-discriminative voxel-based morphometry. PLoS One 2016;11:e0150834
  • Espeland MA, Rapp SR, Manson JE, et al. Long-term effects on cognitive trajectories of postmenopausal hormone therapy in two age groups. J Gerontol A Biol Sci Med Sci 2017;72:838–45
  • Rocca WA, Grossardt BR, Shuster LT. Oophorectomy, menopause, estrogen treatment, and cognitive aging: clinical evidence for a window of opportunity. Brain Res 2011;1379:188–98
  • Espeland MA, Shumaker SA, Leng I, et al. Long-term effects on cognitive function of postmenopausal hormone therapy prescribed to women aged 50 to 55 years. JAMA Intern Med 2013;173:1429–36
  • Gleason CE, Dowling NM, Wharton W, et al. Effects of hormone therapy on cognition and mood in recently postmenopausal women: findings from the randomized, controlled KEEPS-Cognitive and Affective Study. PLoS Med 2015;12:e1001833
  • Henderson VW, St John JA, Hodis HN, et al. Cognitive effects of estradiol after menopause: a randomized trial of the timing hypothesis. Neurology 2016;87:699–708
  • Carcaillon L, Brailly-Tabard S, Ancelin M-L, et al. High plasma estradiol interacts with diabetes on risk of dementia in older postmenopausal women. Neurology 2014;82:504–11
  • Espeland MA, Brinton RD, Hugenschmidt C, et al. Impact of type 2 diabetes and postmenopausal hormone therapy on incidence of cognitive impairment in older women. Diabetes Care 2015;38:2316–24
  • Espeland MA, Brinton RD, Manson JE, et al. Postmenopausal hormone therapy, type 2 diabetes mellitus, and brain volumes. Neurology 2015;85:1131–8
  • Lee SR, Cho MK, Cho YJ, et al. The 2020 menopausal hormone therapy guidelines. J Menopausal Med 2020;26:69–98
  • Johnson RR, Sweeney ME. Debate: the potential role of estrogen in the prevention of heart disease in women after menopause. Curr Control Trials Cardiovasc Med 2000;1:139–42
  • Barrett-Connor E, Wenger NK, Grady D, et al. Hormone and nonhormone therapy for the maintenance of postmenopausal health: the need for randomized controlled trials of estrogen and raloxifene. J Womens Health 1998;7:839–47
  • Alexander LaRosa JH, Bader H, et al. New Dimensions in Women’s Health. Burlington, MA: Jones & Bartlett Publishers; 2016
  • Stefanick ML. Estrogens and progestins: background and history, trends in use, and guidelines and regimens approved by the US Food and Drug Administration. Am J Med 2005;118:64–73
  • Singh M, Meyer EM, Millard WJ, et al. Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res 1994;644:305–12
  • Yaffe K, Barnes D, Lindquist K, et al. Endogenous sex hormone levels and risk of cognitive decline in an older biracial cohort. Neurobiol Aging 2007;28:171–8
  • Yaffe K, Sawaya G, Lieberburg I, et al. Estrogen therapy in postmenopausal women: effects on cognitive function and dementia. JAMA 1998;279:688–95
  • Packard MG, Teather LA. Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. Neuroreport 1997;8:3009–13
  • Hara Y, Waters EM, McEwen BS, et al. Estrogen effects on cognitive and synaptic health over the lifecourse. Physiol Rev 2015;95:785–807
  • Boulware MI, Heisler JD, Frick KM. The memory-enhancing effects of hippocampal estrogen receptor activation involve metabotropic glutamate receptor signaling. J Neurosci 2013;33:15184–94
  • Mehta JM, Chester RC, Kling JM. The timing hypothesis: hormone therapy for treating symptomatic women during menopause and its relationship to cardiovascular disease. J Women’s Health 2019;28:705–11
  • Hodis HN, Mack WJ, Shoupe D, et al. Methods and baseline cardiovascular data from the Early versus Late Intervention Trial with Estradiol testing the menopausal hormone timing hypothesis. Menopause 2015;22:391–401
  • Miller VM, Naftolin F, Asthana S, et al. The Kronos Early Estrogen Prevention Study (KEEPS): what have we learned? Menopause 2019;26:1071–84
  • Wharton W, Gleason CE, Dowling NM, et al. The KEEPS-Cognitive and Affective Study: baseline associations between vascular risk factors and cognition. J Alzheimers Dis 2014;40:331–41
  • Sherwin BB. Estrogen therapy: is time of initiation critical for neuroprotection? Nat Rev Endocrinol 2009;5:620–7
  • Sherwin BB. Estrogen and cognitive functioning in women: lessons we have learned. Behav Neurosci 2012;126:123–7
  • Maki PM. Critical window hypothesis of hormone therapy and cognition: a scientific update on clinical studies. Menopause 2013;20:695–709
  • Maki PM, Girard LM, Manson JE. Menopausal hormone therapy and cognition. BMJ 2019;364:l877
  • Brinton RD. The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci 2008;31:529–37
  • Rettberg JR, Yao J, Brinton RD. Estrogen: a master regulator of bioenergetic systems in the brain and body. Front Neuroendocrinol 2014;35:8–30
  • Talbot K, Wang HY, Kazi H, et al. Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest 2012;122:1316–38
  • Arnold SE, Arvanitakis Z, Macauley-Rambach SL, et al. Brain insulin resistance in type 2 diabetes and Alzheimer disease: concepts and conundrums. Nat Rev Neurol 2018;14:168–81
  • Cunnane SC, Trushina E, Morland C, et al. Brain energy rescue: an emerging therapeutic concept for neurodegenerative disorders of ageing. Nat Rev Drug Discov 2020;19:609–33
  • Mauvais-Jarvis F, Clegg DJ, Hevener AL. The role of estrogens in control of energy balance and glucose homeostasis. Endocr Rev 2013;34:309–38
  • Mauvais-Jarvis F, Manson JE, Stevenson JC, et al. Menopausal hormone therapy and type 2 diabetes prevention: evidence, mechanisms, and clinical implications. Endocr Rev 2017;38:173–88
  • Pereira RI, Casey BA, Swibas TA, et al. Timing of estradiol treatment after menopause may determine benefit or harm to insulin action. J Clin Endocrinol Metab 2015;100:4456–62
  • Barros RP, Gustafsson JA. Estrogen receptors and the metabolic network. Cell Metab 2011;14:289–99
  • Lopez M, Tena-Sempere M. Estrogens and the control of energy homeostasis: a brain perspective. Trends Endocrinol Metab 2015;26:411–21
  • Frank A, Brown LM, Clegg DJ. The role of hypothalamic estrogen receptors in metabolic regulation. Front Neuroendocrinol 2014;35:550–7
  • Bacon ER, Mishra A, Wang Y, et al. Neuroendocrine aging precedes perimenopause and is regulated by DNA methylation. Neurobiol Aging 2019;74:213–24
  • Inigo MR, Amorese AJ, Tarpey MD, et al. Estrogen receptor-α in female skeletal muscle is not required for regulation of muscle insulin sensitivity and mitochondrial regulation. Mol Metab 2020;34:1–15
  • Shi J, Simpkins JW. 17 beta-Estradiol modulation of glucose transporter 1 expression in blood-brain barrier. Am J Physiol 1997;272:E1016–22
  • Foryst-Ludwig A, Kintscher U. Metabolic impact of estrogen signalling through ERalpha and ERbeta. J Steroid Biochem Mol Biol 2010;122:74–81
  • Kim CK, Torcaso A, Asimes A, et al. Structural and functional characteristics of oestrogen receptor beta splice variants: implications for the ageing brain. J Neuroendocrinol 2018;30:e12488
  • Bean LA, Kumar A, Rani A, et al. Re-opening the critical window for estrogen therapy. J Neurosci 2015;35:16077–93
  • Wu TW, Chen S, Brinton RD. Membrane estrogen receptors mediate calcium signaling and MAP kinase activation in individual hippocampal neurons. Brain Res 2011;1379:34–43
  • Wu TW, Wang JM, Chen S, et al. 17Beta-estradiol induced Ca2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 2005;135:59–72
  • Arevalo MA, Azcoitia I, Garcia-Segura LM. The neuroprotective actions of oestradiol and oestrogen receptors. Nat Rev Neurosci 2015;16:17–29
  • Yao J, Hamilton RT, Cadenas E, et al. Decline in mitochondrial bioenergetics and shift to ketogenic profile in brain during reproductive senescence. Biochim Biophys Acta 2010;1800:1121–6
  • Yao J, Irwin R, Chen S, et al. Ovarian hormone loss induces bioenergetic deficits and mitochondrial β-amyloid. Neurobiol Aging 2012;33:1507–21
  • Ding F, Yao J, Rettberg JR, et al. Early decline in glucose transport and metabolism precedes shift to ketogenic system in female aging and Alzheimer’s mouse brain: implication for bioenergetic intervention. PLoS One 2013;8:e79977
  • Ding F, Yao J, Zhao L, et al. Ovariectomy induces a shift in fuel availability and metabolism in the hippocampus of the female transgenic model of familial Alzheimer’s. PLoS One 2013;8:e59825
  • Eberling JL, Reed BR, Coleman JE, et al. Effect of estrogen on cerebral glucose metabolism in postmenopausal women. Neurology 2000;55:875–7
  • Schonknecht P, Henze M, Hunt A, et al. Hippocampal glucose metabolism is associated with cerebrospinal fluid estrogen levels in postmenopausal women with Alzheimer’s disease. Psychiatry Res 2003;124:125–7
  • Maki PM, Resnick SM. Longitudinal effects of estrogen replacement therapy on PET cerebral blood flow and cognition. Neurobiol Aging 2000;21:373–83
  • Rasgon NL, Silverman D, Siddarth P, et al. Estrogen use and brain metabolic change in postmenopausal women. Neurobiol Aging 2005;26:229–35
  • Rasgon NL, Small GW, Siddarth P, et al. Estrogen use and brain metabolic change in older adults. A preliminary report. Psychiatry Res 2001;107:11–18
  • Mosconi L, Rahman A, Diaz I, et al. Increased Alzheimer’s risk during the menopause transition: a 3-year longitudinal brain imaging study. PLoS One 2018;13:e0207885
  • Mosconi L, Berti V, Quinn C, et al. Perimenopause and emergence of an Alzheimer’s bioenergetic phenotype in brain and periphery. PLoS One 2017;12:e0185926
  • Mosconi L, Tsui WH, Herholz K, et al. Multicenter standardized 18F-FDG PET diagnosis of mild cognitive impairment, Alzheimer’s disease, and other dementias. J Nucl Med 2008;49:390–8
  • Ishibashi K, Onishi A, Fujiwara Y, et al. Plasma glucose levels affect cerebral 18F-FDG distribution in cognitively normal subjects with diabetes. Clin Nucl Med 2016;41:e274–80
  • Roberts RO, Knopman DS, Cha RH, et al. Diabetes and elevated hemoglobin A1c levels are associated with brain hypometabolism but not amyloid accumulation. J Nucl Med 2014;55:759–64
  • Li W, Risacher SL, Huang E, et al. Type 2 diabetes mellitus is associated with brain atrophy and hypometabolism in the ADNI cohort. Neurology 2016;87:595–600
  • Baker LD, Cross DJ, Minoshima S, et al. Insulin resistance and Alzheimer-like reductions in regional cerebral glucose metabolism for cognitively normal adults with prediabetes or early type 2 diabetes. Arch Neurol 2011;68:51–7
  • Garris DR. Obese (ob/ob) and diabetes (db/db) mutations: two factors modulating brain and peripheral tissue accumulation of estradiol in C57BL/KsJ mice. Brain Res 1987;432:153–7
  • Garris DR. Estrogenic stimulation of hypothalamic-limbic system metabolism in ageing diabetic C57BL/KsJ mice. Neuroendocrinology 1999;69:424–9
  • Tang SS, Ren Y, Ren XQ, et al. ERα and/or ERβ activation ameliorates cognitive impairment, neurogenesis and apoptosis in type 2 diabetes mellitus mice. Exp Neurol 2019;311:33–43
  • Santizo RA, Xu H-L, Ye S, et al. Loss of benefit from estrogen replacement therapy in diabetic ovariectomized female rats subjected to transient forebrain ischemia. Brain Res 2002;956:86–95
  • Shen B, Vetri F, Mao L, et al. Aldose reductase inhibition ameliorates the detrimental effect of estrogen replacement therapy on neuropathology in diabetic rats subjected to transient forebrain ischemia. Brain Res 2010;1342:118–26
  • Pratchayasakul W, Chattipakorn N, Chattipakorn SC. Estrogen restores brain insulin sensitivity in ovariectomized non-obese rats, but not in ovariectomized obese rats. Metabolism 2014;63:851–9
  • Rasgon NL, Kenna HA, Wroolie TE, et al. Insulin resistance and medial prefrontal gyrus metabolism in women receiving hormone therapy. Psychiatry Res 2014;223:28–36
  • Davey DA. Menopausal hormone therapy: a better and safer future. Climacteric 2018;21:454–61
  • Yassine HN, Anderson A, Brinton R, et al. Do menopausal status and APOE4 genotype alter the long-term effects of intensive lifestyle intervention on cognitive function in women with type 2 diabetes mellitus? Neurobiol Aging 2020;92:61–72
  • Lopez-Otin C, Blasco MA, Partridge L, et al. The hallmarks of aging. Cell 2013;153:1194–217

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.