Cited by 273Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms
Sex differences in β-amyloid accumulation in 3xTg-AD mice: Role of neonatal sex steroid hormone exposure
Open accessCarroll, Jenna C., Rosario, Emily R., Kreimer, Sara, Villamagna, Angela, Gentzschein, Elisabet, Stanczyk, Frank Z., Pike, Christian J.·2010·Brain Research
Abstract
The risk of Alzheimer's disease (AD) is higher in women than in men, a sex difference that likely results from the effects of sex steroid hormones. To investigate this relationship, we first compared progression of β-amyloid (Aβ) pathology in male and female triple transgenic (3xTg-AD) mice. We found that female 3xTg-AD mice exhibit significantly greater Aβ burden and larger behavioral deficits than age-matched males. Next, we evaluated how the organizational effects of sex steroid hormones during postnatal development may affect adult vulnerability to Aβ pathology. We observed that male 3xTg-AD mice demasculinized during early development exhibit significantly increased Aβ accumulation in adulthood. In contrast, female mice defeminized during early development exhibit a more male-like pattern of Aβ pathology in adulthood. Taken together, these results demonstrate significant sex differences in pathology in 3xTg-AD mice and suggest that these differences may be mediated by organizational actions of sex steroid hormones during development.
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Only female mice were used because AD pathology development is far less pronounced and more variable in male 3xTg-AD mice.
“Only female mice were used in this study since the development of AD pathology is far less pronounced and more variable in male 3xTg-AD mice [18,19].”
From Brain microstructure abnormalities in the 3xTg-AD mouse – A diffusion MRI and morphology correlation study (2022) · cites this paper as [19]
The Results section ('Female 3xTg-AD mice display higher levels of Aβ immunoreactivity than males'; page unavailable) reports greater Aβ loads and more plaques in females than in age-matched males. This supports less pronounced amyloid pathology in males, but the paper does not establish that pathology development in males is more variable. 'Only female mice were used' describes the citing study, not this source. (LLM, conf=0.86)
Experimental — accuracy not yet measuredMale 3xTg-AD mice no longer consistently exhibit plaque and tangle pathology.
“Since the initial generation of the model, it has been described by multiple groups and confirmed by the donating investigator that male 3xTg-AD mice no longer consistently exhibit plaque and tangle pathology [23–25].”
From Age, sex and Alzheimer’s disease: a longitudinal study of 3xTg-AD mice reveals sex-specific disease trajectories and inflammatory responses mirrored in postmortem brains from Alzheimer’s patients (2024) · cites this paper as [23]
The Results (page unavailable) report fewer plaques in 12–14-month-old males than females, supporting a sex difference in plaque burden. They do not establish that males have ceased to exhibit plaques consistently. The Discussion (page unavailable) says tau pathology was not evaluated, and the paper does not document a loss of plaque-and-tangle pathology since the model’s initial generation. (LLM, conf=0.82)
Experimental — accuracy not yet measuredThe present study's focus on male 3×Tg-AD mice at 9 months of age may limit the generalizability of our findings to the broader patient population.
“One limitation of the present study is its focus on male 3×Tg-AD mice at 9 months of age, which may limit the generalizability of our findings to the broader patient population (Carroll et al., 2010).”
From Multimodal MRI combined with RNA sequencing reveals pathological signatures in the 9-month-old 3×Tg-AD mouse brain (2026) · cites this paper as Carroll et al., 2010
These results align with published literature and reinforce the translatability of the 3xTg-AD model.
“Together, these results align with published literature [20, 21, 23, 24, 26, 27] and reinforce the translatability of the 3xTg-AD model.”
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References 119 · Cited by 273
Research works printed but not linked: 101
- Akhmadeev AV Kalimullina LB 2005 [Neonatal androgenization of female rats during sex differentiation of the brain modifies neuronal organization of the amygdala complex] Ontogenez 36 64 7 15807439
- Akhondzadeh S Rezaei F Larijani B Nejatisafa AA Kashani L Abbasi SH 2006 Correlation between testosterone, gonadotropins and prolactin and severity of negative symptoms in male patients with chronic schizophrenia Schizophr Res 84 405 10 16545544
- Alkayed NJ Murphy SJ Traystman RJ Hurn PD Miller VM 2000 Neuroprotective effects of female gonadal steroids in reproductively senescent female rats Stroke 31 161 8 10625733
- Anahara R Toyama Y Mori C 2004 Flutamide induces ultrastructural changes in spermatids and the ectoplasmic specialization between the Sertoli cell and spermatids in mouse testes Reprod Toxicol 18 589 96 15135853
- Anderson LI Leipheimer RE Dluzen DE 2005 Effects of neonatal and prepubertal hormonal manipulations upon estrogen neuroprotection of the nigrostriatal dopaminergic system within female and male mice Neuroscience 130 369 82 15664693
- Arato M Frecska E Beck C An M Kiss H 2004 Digit length pattern in schizophrenia suggests disturbed prenatal hemispheric lateralization Prog Neuropsychopharmacol Biol Psychiatry 28 191 4 14687873
- Bachman DL Wolf PA Linn R Knoefel JE Cobb J Belanger A D’Agostino RB White LR 1992 Prevalence of dementia and probable senile dementia of the Alzheimer type in the Framingham Study Neurology 42 115 9 1734291
- Bakker J Baum MJ 2008 Role for estradiol in female-typical brain and behavioral sexual differentiation Front Neuroendocrinol 29 1 16 17720235 PMC2373265
- Barnes LL Wilson RS Bienias JL Schneider JA Evans DA Bennett DA 2005 Sex differences in the clinical manifestations of Alzheimer disease pathology Arch Gen Psychiatry 62 685 91 15939846
- Barron AM Verdile G Martins RN 2006 The role of gonadotropins in Alzheimer’s disease: potential neurodegenerative mechanisms Endocrine 29 257 69 16785601
- Becu-Villalobos D Gonzalez Iglesias A Diaz-Torga G Hockl P Libertun C 1997 Brain sexual differentiation and gonadotropins secretion in the rat Cell Mol Neurobiol 17 699 715 9442354 PMC11560204
- Bergemann N Mundt C Parzer P Jannakos I Nagl I Salbach B Klinga K Runnebaum B Resch F 2005 Plasma concentrations of estradiol in women suffering from schizophrenia treated with conventional versus atypical antipsychotics Schizophr Res 73 357 66 15653282
- Breedlove SM 1997 Neonatal androgen and estrogen treatments masculinize the size of motoneurons in the rat spinal nucleus of the bulbocavernosus Cell Mol Neurobiol 17 687 97 9442353 PMC11560189
- Cahill L 2006 Why sex matters for neuroscience Nat Rev Neurosci 7 477 84 16688123
- Canli T Desmond JE Zhao Z Gabrieli JD 2002 Sex differences in the neural basis of emotional memories Proc Natl Acad Sci U S A 99 10789 94 12145327 PMC125046
- Carroll JC Rosario ER Chang L Stanczyk FZ Oddo S LaFerla FM Pike CJ 2007 Progesterone and estrogen regulate Alzheimer-like neuropathology in female 3xTg-AD mice J Neurosci 27 13357 65 18045930 PMC6673397
- Carroll JC Pike CJ 2008 Selective estrogen receptor modulators differentially regulate Alzheimer-like changes in female 3xTg-AD mice Endocrinology 149 2607 11 18276750 PMC2329277
- Carroll JC Rosario ER Villamagna A Pike CJ 2010 Continuous and cyclic progesterone differentially interact with estradiol in the regulation of Alzheimer-like pathology in female 3xTransgenic-Alzheimer’s disease mice Endocrinology 151 2713 22 20410196 PMC2875823
- Casadesus G Atwood CS Zhu X Hartzler AW Webber KM Perry G Bowen RL Smith MA 2005 Evidence for the role of gonadotropin hormones in the development of Alzheimer disease Cell Mol Life Sci 62 293 8 15723165 PMC11924470
- Conrad CD Galea LA Kuroda Y McEwen BS 1996 Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment Behav Neurosci 110 1321 34 8986335
- Cooke BM Woolley CS 2005 Sexually dimorphic synaptic organization of the medial amygdala J Neurosci 25 10759 67 16291949 PMC6725860
- Corder EH Ghebremedhin E Taylor MG Thal DR Ohm TG Braak H 2004 The biphasic relationship between regional brain senile plaque and neurofibrillary tangle distributions: modification by age, sex, and APOE polymorphism Ann N Y Acad Sci 1019 24 8 15246987
- Cosgrove KP Mazure CM Staley JK 2007 Evolving knowledge of sex differences in brain structure, function, and chemistry Biol Psychiatry 62 847 55 17544382 PMC2711771
- Dominguez-Salazar E Portillo W Baum MJ Bakker J Paredes RG 2002 Effect of prenatal androgen receptor antagonist or aromatase inhibitor on sexual behavior, partner preference and neuronal Fos responses to estrous female odors in the rat accessory olfactory system Physiol Behav 75 337 46 11897260
- Duff SJ Hampson E 2001 A sex difference on a novel spatial working memory task in humans Brain Cogn 47 470 93 11748902
- Espeland MA Rapp SR Shumaker SA Brunner R Manson JE Sherwin BB Hsia J Margolis KL Hogan PE Wallace R Dailey M Freeman R Hays J 2004 Conjugated equine estrogens and global cognitive function in postmenopausal women: Women’s Health Initiative Memory Study Jama 291 2959 68 15213207
- Felicio LS Nelson JF Finch CE 1984 Longitudinal studies of estrous cyclicity in aging C57BL/6J mice: II. Cessation of cyclicity and the duration of persistent vaginal cornification Biol Reprod 31 446 53 6541508
- Franklin KBJ Paxinos G 1997 The Mouse Brain in Stereotaxic Coordinates Academic Press San Diego
- Fratiglioni L Small BJ Winblad B Bäckman L Iqbal K Sisodia S Winblad B 2001 The transition from normal functioning to dementia in the ageing population Alzheimer’s Disease: Advances in Etiology, Pathogenesis and Therapeutics John Wiley & Sons, Ltd Chichester 3 10
- Gillett MJ Martins RN Clarnette RM Chubb SA Bruce DG Yeap BB 2003 Relationship between testosterone, sex hormone binding globulin and plasma amyloid beta peptide 40 in older men with subjective memory loss or dementia J Alzheimers Dis 5 267 9 14624021
- Goldstein JM Seidman LJ Horton NJ Makris N Kennedy DN Caviness VS Jr Faraone SV Tsuang MT 2001 Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging Cereb Cortex 11 490 7 11375910
- Gore AC 2008 Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems Front Neuroendocrinol 29 358 74 18394690 PMC2702520
- Hamann S 2005 Sex differences in the responses of the human amygdala Neuroscientist 11 288 93 16061516
- Henderson VW Paganini-Hill A Emanuel CK Dunn ME Buckwalter JG 1994 Estrogen replacement therapy in older women. Comparisons between Alzheimer’s disease cases and nondemented control subjects Arch Neurol 51 896 900 8080389
- Hirata-Fukae C Li HF Hoe HS Gray AJ Minami SS Hamada K Niikura T Hua F Tsukagoshi-Nagai H Horikoshi-Sakuraba Y Mughal M Rebeck GW LaFerla FM Mattson MP Iwata N Saido TC Klein WL Duff KE Aisen PS Matsuoka Y 2008 Females exhibit more extensive amyloid, but not tau, pathology in an Alzheimer transgenic model Brain Res 1216 92 103 18486110
- Hogervorst E Williams J Biudge M Barnetson L Combrinck M Smith AD 2001 Serum total testosterone is lower in men with Alzheimer’s disease Neuro Endocrinol Lett 22 163 168 11449190
- Holcomb L Gordon MN McGowan E Yu X Benkovic S Jantzen P Wright K Saad I Mueller R Morgan D Sanders S Zehr C O’Campo K Hardy J Prada CM Eckman C Younkin S Hsiao K Duff K 1998 Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes Nat Med 4 97 100 9427614
- Houtsmuller EJ Brand T de Jonge FH Joosten RN van de Poll NE Slob AK 1994 SDN-POA volume, sexual behavior, and partner preference of male rats affected by perinatal treatment with ATD Physiol Behav 56 535 41 7972405
- Hsiao K Chapman P Nilsen S Eckman C Harigaya Y Younkin S Yang F Cole G 1996 Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice Science 274 99 102 8810256
- Hurd PL Bailey AA Gongal PA Yan RH Greer JJ Pagliardini S 2008 Intrauterine position effects on anogenital distance and digit ratio in male and female mice Arch Sex Behav 37 9 18 18080736
- Husmann DA McPhaul MJ 1991 Time-specific androgen blockade with flutamide inhibits testicular descent in the rat Endocrinology 129 1409 16 1678699
- Hutter HS Gibson MJ 1988 Effect of neonatal androgenization on positive feedback in female mice Biol Reprod 38 636 8 3378076
- Iguchi T Takasugi N 1981 Occurrence of permanent anovulation in mouse ovaries and permanent changes in the vaginal and uterine epithelia following neonatal treatment with large doses of 5 alpha-dihydrotestosterone Endocrinol Jpn 28 207 13 7198030
- Isgor C Sengelaub DR 1998 Prenatal gonadal steroids affect adult spatial behavior, CA1 and CA3 pyramidal cell morphology in rats Horm Behav 34 183 98 9799628
- Isgor C Sengelaub DR 2003 Effects of neonatal gonadal steroids on adult CA3 pyramidal neuron dendritic morphology and spatial memory in rats J Neurobiol 55 179 90 12672016
- Jezierski MK Sohrabji F 2001 Neurotrophin expression in the reproductively senescent forebrain is refractory to estrogen stimulation Neurobiol Aging 22 309 319 11182481
- Jorm AF Korten AE Henderson AS 1987 The prevalence of dementia: a quantitative integration of the literature Acta Psychiatr Scand 76 465 79 3324647
- Jorm AF Jolley D 1998 The incidence of dementia: a meta-analysis Neurology 51 728 33 9748017
- Kawas C Resnick S Morrison A Brookmeyer R Corrada M Zonderman A Bacal C Lingle DD Metter E 1997 A prospective study of estrogen replacement therapy and the risk of developing Alzheimer’s disease: the Baltimore Longitudinal Study of Aging Neurology 48 1517 21 9191758
- King DL Arendash GW Crawford F Sterk T Menendez J Mullan MJ 1999 Progressive and gender-dependent cognitive impairment in the APP(SW) transgenic mouse model for Alzheimer’s disease Behav Brain Res 103 145 62 10513583
- King DL Arendash GW 2002 Behavioral characterization of the Tg2576 transgenic model of Alzheimer’s disease through 19 months Physiol Behav 75 627 42 12020728
- Krohmer RW Baum MJ 1989 Effect of sex, intrauterine position and androgen manipulation on the development of brain aromatase activity in fetal ferrets J Neuroendocrinol 1 265 71 19210439
- Lansing SW Lonstein JS 2006 Tyrosine hydroxylase-synthesizing cells in the hypothalamus of prairie voles (Microtus ochrogaster): sex differences in the anteroventral periventricular preoptic area and effects of adult gonadectomy or neonatal gonadal hormones J Neurobiol 66 197 204 16329116
- Lee JY Cole TB Palmiter RD Suh SW Koh JY 2002 Contribution by synaptic zinc to the gender-disparate plaque formation in human Swedish mutant APP transgenic mice Proc Natl Acad Sci U S A 99 7705 10 12032347 PMC124328
- Levin-Allerhand JA Lominska CE Wang J Smith JD 2002 17Alpha-estradiol and 17beta-estradiol treatments are effective in lowering cerebral amyloid-beta levels in AbetaPPSWE transgenic mice J Alzheimers Dis 4 449 57 12515896
- Li L Rasul I Liu J Zhao B Tang R Premont RT Suo WZ 2009 Augmented axonal defects and synaptic degenerative changes in female GRK5 deficient mice Brain Res Bull 78 145 51 18955119
- Lutchmaya S Baron-Cohen S Raggatt P Knickmeyer R Manning JT 2004 2nd to 4th digit ratios, fetal testosterone and estradiol Early Hum Dev 77 23 8 15113628
- Madeira MD Lieberman AR 1995 Sexual dimorphism in the mammalian limbic system Prog Neurobiol 45 275 333 7624480
- McAllister C Long J Bowers A Walker A Cao P Honda S Harada N Staufenbiel M Shen Y Li R 2010 Genetic targeting aromatase in male amyloid precursor protein transgenic mice down-regulates beta-secretase (BACE1) and prevents Alzheimer-like pathology and cognitive impairment J Neurosci 30 7326 34 20505099 PMC3506430
- McCarthy MM Schwarz JM Wright CL Dean SL 2008 Mechanisms mediating oestradiol modulation of the developing brain J Neuroendocrinol 20 777 83 18601700 PMC2570052
- McCormick CM Furey BF Child M Sawyer MJ Donohue SM 1998 Neonatal sex hormones have ‘organizational’ effects on the hypothalamic-pituitary-adrenal axis of male rats Brain Res Dev Brain Res 105 295 307 9541747
- McCormick CM Mahoney E 1999 Persistent effects of prenatal, neonatal, or adult treatment with flutamide on the hypothalamic-pituitary-adrenal stress response of adult male rats Horm Behav 35 90 101 10049607
- Meek LR Schulz KM Keith CA 2006 Effects of prenatal stress on sexual partner preference in mice Physiol Behav 89 133 8 16844154
- Meethal SV Smith MA Bowen RL Atwood CS 2005 The gonadotropin connection in Alzheimer’s disease Endocrine 26 317 26 16034187
- Mendrek A 2007 Reversal of normal cerebral sexual dimorphism in schizophrenia: evidence and speculations Med Hypotheses 69 896 902 17379422
- Miyata K Yabushita S Sano M Miyashita K Okuno Y Matsuo M 2003 Effects of perinatal exposure to flutamide on sex hormone responsiveness in F1 male rats J Toxicol Sci 28 149 63 12974607
- Moffat SD Zonderman AB Metter EJ Kawas C Blackman MR Harman SM Resnick SM 2004 Free testosterone and risk for Alzheimer disease in older men Neurology 62 188 93 14745052
- Morris JA Jordan CL Breedlove SM 2004 Sexual differentiation of the vertebrate nervous system Nat Neurosci 7 1034 9 15452574
- Negri-Cesi P Poletti A Celotti F 1996 Metabolism of steroids in the brain: a new insight into the role of 5alpha-reductase and aromatase in brain differentiation and functions J Steroid Biochem Mol Biol 58 455 66 8918971
- Nordell VL Scarborough MM Buchanan AK Sohrabji F 2003 Differential effects of estrogen in the injured forebrain of young adult and reproductive senescent animals Neurobiol Aging 24 733 743 12885581
- Nwagwu MO Baines H Kerr JB Ebling FJ 2005 Neonatal androgenization of hypogonadal (hpg) male mice does not abolish estradiol-induced FSH production and spermatogenesis Reprod Biol Endocrinol 3 48 16176578 PMC1249589
- Paganini-Hill A Henderson VW 1996 Estrogen replacement therapy and risk of Alzheimer disease Arch Intern Med 156 2213 7 8885820
- Petanceska SS Nagy V Frail D Gandy S 2000 Ovariectomy and 17beta-estradiol modulate the levels of Alzheimer’s amyloid beta peptides in brain Exp Gerontol 35 1317 25 11113610
- Pike CJ 1999 Estrogen modulates neuronal Bcl-xL expression and beta-amyloid-induced apoptosis: relevance to Alzheimer’s disease J Neurochem 72 1552 63 10098861
- Pike CJ Carroll JC Rosario ER Barron AM 2009 Protective actions of sex steroid hormones in Alzheimer’s disease Front Neuroendocrinol 30 239 58 19427328 PMC2728624
- Pistell PJ Zhu M Ingram DK 2008 Acquisition of conditioned taste aversion is impaired in the amyloid precursor protein/presenilin 1 mouse model of Alzheimer’s disease Neuroscience 152 594 600 18304749 PMC2390908
- Raber J Bongers G LeFevour A Buttini M Mucke L 2002 Androgens protect against apolipoprotein E4-induced cognitive deficits J Neurosci 22 5204 9 12077215 PMC6757715
- Rapp SR Espeland MA Shumaker SA Henderson VW Brunner RL Manson JE Gass ML Stefanick ML Lane DS Hays J Johnson KC Coker LH Dailey M Bowen D 2003 Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women’s Health Initiative Memory Study: a randomized controlled trial Jama 289 2663 72 12771113
- Rocca WA Amaducci LA Schoenberg BS 1986 Epidemiology of clinically diagnosed Alzheimer’s disease Ann Neurol 19 415 24 3717905
- Rosario ER Carroll JC Oddo S LaFerla FM Pike CJ 2006 Androgens regulate the development of neuropathology in a triple transgenic mouse model of Alzheimer’s disease J Neurosci 26 13384 9 17182789 PMC6674990
- Rosario ER Chang L Stanczyk FZ Pike CJ 2004 Age-related testosterone depletion and the development of Alzheimer disease Jama 292 1431 2 15383512
- Ruitenberg A Ott A van Swieten JC Hofman A Breteler MMB 2001 Incidence of dementia: does gender make a difference? Neurobiology of Aging 22 575 580 11445258
- Schafer S Wirths O Multhaup G Bayer TA 2007 Gender dependent APP processing in a transgenic mouse model of Alzheimer’s disease J Neural Transm 114 387 94 17075721
- Seale JV Wood SA Atkinson HC Harbuz MS Lightman SL 2005 Postnatal masculinization alters the HPA axis phenotype in the adult female rat J Physiol 563 265 74 15611026 PMC1665574
- Slater CC Zhang C Hodis HN Mack WJ Boostanfar R Shoupe D Paulson RJ Stanczyk FZ 2001 Comparison of estrogen and androgen levels after oral estrogen replacement therapy J Reprod Med 46 1052 6 11789085
- Slob AK Ooms MP Vreeburg JT 1980 Prenatal and early postnatal sex differences in plasma and gonadal testosterone and plasma luteinizing hormone in female and male rats J Endocrinol 87 81 7 7430918
- Speck O Ernst T Braun J Koch C Miller E Chang L 2000 Gender differences in the functional organization of the brain for working memory Neuroreport 11 2581 5 10943726
- Sturchler-Pierrat C Staufenbiel M 2000 Pathogenic mechanisms of Alzheimer’s disease analyzed in the APP23 transgenic mouse model Ann N Y Acad Sci 920 134 9 11193142
- Swaab DF Chung WC Kruijver FP Hofman MA Ishunina TA 2001 Structural and functional sex differences in the human hypothalamus Horm Behav 40 93 8 11534968
- Swanson HE van der WTBJ 1963 Sex differences in growth of rats, and their modification by a single injection of testosterone propionate shortly after birth J Endocrinol 26 197 207 13979629
- Tang MX Jacobs D Stern Y Marder K Schofield P Gurland B Andrews H Mayeux R 1996 Effect of oestrogen during menopause on risk and age at onset of Alzheimer’s disease Lancet 348 429 32 8709781
- Tarttelin MF Shryne JE Gorski RA 1975 Patterns of body weight change in rats following neonatal hormone manipulation: a “critical period” for androgen-induced growth increases Acta Endocrinol (Copenh) 79 177 91 1173305
- Vagnerova K Koerner IP Hurn PD 2008 Gender and the injured brain Anesth Analg 107 201 14 18635489 PMC2651745
- vom Saal FS 1989 Sexual differentiation in litter-bearing mammals: influence of sex of adjacent fetuses in utero J Anim Sci 67 1824 40 2670873
- Wang J Tanila H Puolivali J Kadish I van Groen T 2003 Gender differences in the amount and deposition of amyloidbeta in APPswe and PS1 double transgenic mice Neurobiol Dis 14 318 27 14678749
- Wang PY Protheroe A Clarkson AN Imhoff F Koishi K McLennan IS 2009 Mullerian inhibiting substance contributes to sex-linked biases in the brain and behavior Proc Natl Acad Sci U S A PMC2678437 19359476
- Weisz J Ward IL 1980 Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring Endocrinology 106 306 16 7349961
- Wise PM 2002 Estrogens and neuroprotection Trends Endocrinol Metab 13 229 30 12128278
- Yang SL Chen YY Hsieh YL Jin SH Hsu HK Hsu C 2004 Perinatal androgenization prevents age-related neuron loss in the sexually dimorphic nucleus of the preoptic area in female rats Dev Neurosci 26 54 60 15509899
- Zandi PP Carlson MC Plassman BL Welsh-Bohmer KA Mayer LS Steffens DC Breitner JC 2002 Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County Study Jama 288 2123 9 12413371
- Zheng H Xu H Uljon SN Gross R Hardy K Gaynor J Lafrancois J Simpkins J Refolo LM Petanceska S Wang R Duff K 2002 Modulation of A(beta) peptides by estrogen in mouse models J Neurochem 80 191 6 11796757
- Authors
- Carroll, J. C., Rosario, E. R., Kreimer, S., Villamagna, A., Gentzschein, E., Stanczyk, F. Z., & Pike, C. J.
- Affiliations
- University of Southern California (US)
- Corresponding author
- Pike, Christian J.
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 2010-12
- Volume
- 1366
- Pages
- 233-245
- ISSN
- 0006-8993 (ISSN-L)
- PMC
- PMC2993873
- OpenAlex
- W2072193814
- Cited by
- 273
- References
- 119
- Citations by year
- 2026: 11 · 2025: 26 · 2024: 31 · 2023: 15 · 2022: 25 · 2021: 27 · 2020: 33 · 2019: 24 · 2018: 27 · 2017: 13 · 2016: 12 · 2015: 11 · 2014: 5 · 2013: 4 · 2012: 7
- FWCI
- 2.82
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (AG23739, AG026572, F31NS059174, NS52143)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- sex differences, amyloid-beta deposition, Alzheimer's disease, 3xTg-AD mice, sex hormones, organizational effects, neonatal hormone exposure, demasculinization, defeminization, postnatal development, amyloid pathology, behavioral deficits
- MeSH terms
- Age Factors, Analysis of Variance, Androgen Antagonists, Androgens, Animals, Animals, Newborn, Brain, Exploratory Behavior, Female, Flutamide, Humans, Male, Mice, Transgenic, Mutation, Orchiectomy, Ovariectomy, Sexual Behavior, Animal, Sex Characteristics, Testosterone, Amyloid beta-Peptides, Amyloid beta-Protein Precursor, tau Proteins, Maze Learning, Mice, Presenilin-1
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