Menopause, Estrogen, and Gonadotropins in Alzheimer's Disease

Advances in Clinical Chemistry

Volumn 45, Issue SUPPL.: COMPLETE, 2008, Pages 139-153

  Casadesus, Gemma ^a,e   Rolston, Raj K ^a,e   Webber, Kate M ^a   Atwood, Craig S ^b   Bowen, Richard L ^c,e   Perry, George ^a,d   Smith, Mark A ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c Voyager Pharmaceutical Corporation   (United States)

^d University of San Antonio   (United States)

^e NONE

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; GONADOTROPIN;

ALZHEIMER DISEASE; FEMALE; HUMAN; MALE; MENOPAUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SEX DIFFERENCE;

ALZHEIMER DISEASE; ESTROGENS; FEMALE; GONADOTROPINS; HUMANS; MALE; MENOPAUSE; SEX FACTORS;

EID: 38749107639     PISSN: 00652423     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-2423(07)00006-6     Document Type: Review

References (109)

1. Bird T., and Miller B. Alzheimer's disease and other dementias. In: Kasper D., Braunwald E., Fauci A., Hauser S., Longo D., and Jameson J. (Eds). Harrison's Principles of Internal Medicine (2004), McGraw-Hill Professional, New York 2393-2401
2. Smith M. Alzheimer disease. Int Rev Neurobiol 42 (1998) 1-54
3. Hebert L., Scherr P., Bienias J., Bennett D., and Evans D. Alzheimer disease in the US population: Prevalence estimates using the 2000 census. Arch Neurol 60 (2003) 1119-1122
4. Katzman R. Alzheimer's disease. N Engl J Med 314 (1986) 964-973
5. McDowd J., and Craik F. Effects of aging and task difficulty on divided attention performance. J Exp Psychol Hum Percept Perform 14 (1988) 267-280
6. Lindeboom J., and Weinstein H. Neuropsychology of cognitive ageing, minimal cognitive impairment, Alzheimer's disease, and vascular cognitive impairment. Eur J Pharmacol 490 (2004) 83-86
7. Weber R., Brown L., and Weldon J. Cognitive maps of environmental knowledge and preference in nursing home patients. Exp Aging Res 4 (1978) 157-174
8. Selkoe D. Alzheimer's disease: Genotypes, phenotypes, and treatments. Science 275 (1997) 630-631
9. Irizarry M., Soriano F., McNamara M., Page K., Schenk D., Games D., et al. Abeta deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein V717F (PDAPP) transgenic mouse. J Neurosci 17 (1997) 7053-7059
10. Perry G., Nunomura A., Raina A., and Smith M. Amyloid-beta junkies. Lancet 355 (2000) 757
11. Obrenovich M., Joseph J., Atwood C., Perry G., and Smith M. Amyloid-beta: A (life) preserver for the brain. Neurobiol Aging 23 (2002) 1097-1099
12. Rottkamp C., Atwood C., Joseph J., Nunomura A., Perry G., and Smith M. The state versus amyloid-beta: The trial of the most wanted criminal in Alzheimer disease. Peptides 23 (2002) 1333-1341
13. Lee H., Casadesus G., Zhu X., Takeda A., Perry G., and Smith M. Challenging the amyloid cascade hypothesis: Senile plaques and amyloid-beta as protective adaptations to Alzheimer disease. Ann N Y Acad Sci 1019 (2004) 1-4
14. Trojanowski J., Clark C., Arai H., and Lee V. Elevated levels of tau in cerebrospinal fluid: Implications for the antemortem diagnosis of Alzheimer's disease. J Alzheimers Dis 1 (1999) 297-305
15. Avila J. Tau aggregation into fibrillar polymers: Taupathies. FEBS Lett 476 (2000) 89-92
16. Zhu X., Lee H., Raina A., Perry G., and Smith M. The role of mitogen-activated protein kinase pathways in Alzheimer's disease. Neurosignals 11 (2002) 270-281
17. Perry G., Castellani R., Hirai K., and Smith M. Reactive oxygen species mediate cellular damage in Alzheimer disease. J Alzheimers Dis 1 (1998) 45-55
18. Perry G., Sayre L., Atwood C., Castellani R., Cash A., Rottkamp C., et al. The role of iron and copper in the aetiology of neurodegenerative disorders: Therapeutic implications. CNS Drugs 16 (2002) 339-352
19. Atwood C., Huang X., Moir R., Smith M., Tanzi R., Roher A., et al. Neuroinflammatory responses in the Alzheimer's disease brain promote the oxidative post-translation modification of amyloid deposits. In: Iqbal K., Sisodia S., and Winblad B. (Eds). Alzheimer's Disease: Advances in Etiology, Pathogenesis and Therapeutics (2001), John Wiley & Sons, Ltd., Chichester, UK 341-361
20. Smith M., Sayre L., Monnier V., and Perry G. Radical AGEing in Alzheimer's disease. Trends Neurosci 18 (1995) 172-176
21. Smith M., Perry G., Richey P., Sayre L., Anderson V., Beal M., et al. Oxidative damage in Alzheimer's. Nature 382 (1996) 120-121
22. Smith M., Harris P., Sayre L., and Perry G. Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc Natl Acad Sci USA 94 (1997) 9866-9868
23. Sayre L., Perry G., Harris P., Liu Y., Schubert K., and Smith M. In situ oxidative catalysis by neurofibrillary tangles and senile plaques in Alzheimer's disease: A central role for bound transition metals. J Neurochem 74 (2000) 270-279
24. Zhu X., Raina A., Perry G., and Smith M. Alzheimer's disease: The two-hit hypothesis. Lancet Neurol 3 (2004) 219-226
25. Fratiglioni L., Viitanen M., von Strauss E., Tontodonati V., Herlitz A., and Winblad B. Very old women at highest risk of dementia and Alzheimer's disease: Incidence data from the Kungsholmen Project, Stockholm. Neurology 48 (1997) 132-138
26. Letenneur L., Commenges D., Dartigues J., and Barberger-Gateau P. Incidence of dementia and Alzheimer's disease in elderly community residents of south-western France. Int J Epidemiol 23 (1994) 1256-1261
27. Jorm A., Korten A., and Henderson A. The prevalence of dementia: A quantitative integration of the literature. Acta Psychiatr Scand 76 (1987) 465-479
28. Breitner J., Silverman J., Mohs R., and Davis K. Familial aggregation in Alzheimer's disease: Comparison of risk among relatives of early- and late-onset cases, and among male and female relatives in successive generations. Neurology 38 (1988) 207-212
29. Rocca W., Hofman A., Brayne C., Breteler M., Clarke M., Copeland J., et al. Frequency and distribution of Alzheimer's disease in Europe: A collaborative study of 1980-1990 prevalence findings. The EURODEM-Prevalence Research Group. Ann Neurol 30 (1991) 381-390
30. McGonigal G., Thomas B., McQuade C., Starr J., MacLennan W., and Whalley L. Epidemiology of Alzheimer's presenile dementia in Scotland, 1974-88. BMJ 306 (1993) 680-683
31. Jorm A., and Jolley D. The incidence of dementia: A meta-analysis. Neurology 51 (1998) 728-733
32. Stam F., Wigboldus J., and Smeulders A. Age incidence of senile brain amyloidosis. Pathol Res Pract 181 (1986) 558-562
33. Sherwin B. Estrogen and cognitive functioning in women. Proc Soc Exp Biol Med 217 (1998) 17-22
34. Birge S., McEwen B., and Wise P. Effects of estrogen deficiency on brain function. Implications for the treatment of postmenopausal women. Postgrad Med Spec No (2001) 11-16
35. Genazzani A., Spinetti A., Gallo R., and Bernardi F. Menopause and the central nervous system: Intervention options. Maturitas 31 (1999) 103-110
36. Manly J., Merchant C., Jacobs D., Small S., Bell K., Ferin M., et al. Endogenous estrogen levels and Alzheimer's disease among postmenopausal women. Neurology 54 (2000) 833-837
37. Brookmeyer R., Gray S., and Kawas C. Projections of Alzheimer's disease in the United States and the public health impact of delaying disease onset. Am J Public Health 88 (1998) 1337-1342
38. Henderson V., Paganini-Hill A., Emanuel C., Dunn M., and Buckwalter J. Estrogen replacement therapy in older women. Comparisons between Alzheimer's disease cases and nondemented control subjects. Arch Neurol 51 (1994) 896-900
39. Tang M., Jacobs D., Stern Y., Marder K., Schofield P., Gurland B., et al. Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 348 (1996) 429-432
40. Kawas C., Resnick S., Morrison A., Brookmeyer R., Corrada M., Zonderman A., et al. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: The Baltimore Longitudinal Study of Aging. Neurology 48 (1997) 1517-1521
41. Sherwin B. Can estrogen keep you smart? Evidence from clinical studies. J Psychiatry Neurosci 24 (1999) 315-321
42. Sherwin B. Estrogen and cognitive aging in women. Trends Pharmacol Sci 23 (2002) 527-534
43. Sherwin B. Surgical menopause, estrogen, and cognitive function in women: What do the findings tell us?. Ann N Y Acad Sci 1052 (2005) 3-10
44. Sherwin B. Estrogen and cognitive aging in women. Neuroscience 138 (2006) 1021-1026
45. Resnick S., and Henderson V. Hormone therapy and risk of Alzheimer disease: A critical time. JAMA 288 (2002) 2170-2172
46. Shumaker S., Legault C., Rapp S., Thal L., Wallace R., Ockene J., 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 289 (2003) 2651-2662
47. Sherwin B. Estrogen and cognitive functioning in women. Endocr Rev 24 (2003) 133-151
48. Petanceska S., Nagy V., Frail D., and Gandy S. Ovariectomy and 17beta-estradiol modulate the levels of Alzheimer's amyloid beta peptides in brain. Neurology 54 (2000) 2212-2217
49. Goodman Y., Bruce A., Cheng B., and Mattson M. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J Neurochem 66 (1996) 1836-1844
50. McEwen B., Alves S., Bulloch K., and Weiland N. Ovarian steroids and the brain: Implications for cognition and aging. Neurology 48 (1997) S8-S15
51. Bi R., Foy M., Vouimba R., Thompson R., and Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc Natl Acad Sci USA 98 (2001) 13391-13395
52. Choi J., Romeo R., Brake W., Bethea C., Rosenwaks Z., and McEwen B. Estradiol increases pre- and post-synaptic proteins in the CA1 region of the hippocampus in female rhesus macaques (Macaca mulatta). Endocrinology 144 (2003) 4734-4738
53. Pinkerton J., and Henderson V. Estrogen and cognition, with a focus on Alzheimer's disease. Semin Reprod Med 23 (2005) 172-179
54. Conrad C., Lupien S., and McEwen B. Support for a bimodal role for type II adrenal steroid receptors in spatial memory. Neurobiol Learn Mem 72 (1999) 39-46
55. McEwen B. Plasticity of the hippocampus: Adaptation to chronic stress and allostatic load. Ann N Y Acad Sci 933 (2001) 265-277
56. McEwen B. Stress and hippocampal plasticity. Annu Rev Neurosci 22 (1999) 105-122
57. Jellinck P., Lee S., and McEwen B. Metabolism of dehydroepiandrosterone by rat hippocampal cells in culture: Possible role of aromatization and 7-hydroxylation in neuroprotection. J Steroid Biochem Mol Biol 78 (2001) 313-317
58. Sherwin B. Steroid hormones and cognitive functioning in aging men: A mini-review. J Mol Neurosci 20 (2003) 385-393
59. Carlson L., and Sherwin B. Higher levels of plasma estradiol and testosterone in healthy elderly men compared with age-matched women may protect aspects of explicit memory. Menopause 7 (2000) 168-177
60. Seftel A. Memory loss as reported symptom of andropause. J Urol 168 (2002) 862
61. Mulligan T., and Godschalk M. Male menopause. Drugs Today (Barc) 34 (1998) 455-461
62. Maki P., and Hogervorst E. The menopause and HRT. HRT and cognitive decline. Best Pract Res Clin Endocrinol Metab 17 (2003) 105-122
63. Schupf N., Kapell D., Nightingale B., Rodriguez A., Tycko B., and Mayeux R. Earlier onset of Alzheimer's disease in men with Down syndrome. Neurology 50 (1998) 991-995
64. Espeland M., Rapp S., Shumaker S., Brunner R., Manson J., Sherwin B., et al. Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291 (2004) 2959-2968
65. Rapp S., Espeland M., Shumaker S., Henderson V., Brunner R., Manson J., et al. 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 (2003) 2663-2672
66. Mulnard R. Estrogen as a treatment for Alzheimer disease. JAMA 284 (2000) 307-308
67. Mulnard R., Cotman C., Kawas C., van Dyck C., Sano M., Doody R., et al. Estrogen replacement therapy for treatment of mild to moderate Alzheimer disease: A randomized controlled trial. Alzheimer's Disease Cooperative Study. JAMA 283 (2000) 1007-1015
68. Gleason C., Cholerton B., Carlsson C., Johnson S., and Asthana S. Neuroprotective effects of female sex steroids in humans: Current controversies and future directions. Cell Mol Life Sci 62 (2005) 299-312
69. Baum L. Sex, hormones, and Alzheimer's disease. J Gerontol A Biol Sci Med Sci 60 (2005) 736-743
70. Yaffe K. Hormone therapy and the brain: Déjà vu all over again?. JAMA 289 (2003) 2717-2719
71. Snowdon D., Greiner L., Mortimer J., Riley K., Greiner P., and Markesbery W. Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA 277 (1997) 813-817
72. Burger H. The endocrinology of the menopause. Maturitas 23 (1996) 129-136
73. Henderson V. Hormone therapy and Alzheimer's disease: Benefit or harm. Expert Opin Pharmacother 5 (2004) 389-406
74. Zandi P., Carlson M., Plassman B., Welsh-Bohmer K., Mayer L., Steffens D., et al. Hormone replacement therapy and incidence of Alzheimer disease in older women: The Cache County Study. JAMA 288 (2002) 2123-2129
75. Genazzani A., Gastaldi M., Bidzinska B., Mercuri N., Genazzani A., Nappi R., et al. The brain as a target organ of gonadal steroids. Psychoneuroendocrinology 17 (1992) 385-390
76. Couzinet B., and Schaison G. The control of gonadotrophin secretion by ovarian steroids. Hum Reprod 8 Suppl. 2 (1993) 97-101
77. Chakravarti S., Collins W., Forecast J., Newton J., Oram D., and Studd J. Hormonal profiles after the menopause. Br Med J 2 (1976) 784-787
78. Neaves W., Johnson L., Porter J., Parker Jr. C., and Petty C. Leydig cell numbers, daily sperm production, and serum gonadotropin levels in aging men. J Clin Endocrinol Metab 59 (1984) 756-763
79. Lukacs H., Hiatt E., Lei Z., and Rao C. Peripheral and intracerebroventricular administration of human chorionic gonadotropin alters several hippocampus-associated behaviors in cycling female rats. Horm Behav 29 (1995) 42-58
80. Lei Z., Rao C., Kornyei J., Licht P., and Hiatt E. Novel expression of human chorionic gonadotropin/luteinizing hormone receptor gene in brain. Endocrinology 132 (1993) 2262-2270
81. Apaja P., Harju K., Aatsinki J., Petaja-Repo U., and Rajaniemi H. Identification and structural characterization of the neuronal luteinizing hormone receptor associated with sensory systems. J Biol Chem 279 (2004) 1899-1906
82. Hamalainen T., Poutanen M., and Huhtaniemi I. Age- and sex-specific promoter function of a 2-kilobase 5′-flanking sequence of the murine luteinizing hormone receptor gene in transgenic mice. Endocrinology 140 (1999) 5322-5329
83. Bowen R., Smith M., Harris P., Kubat Z., Martins R., Castellani R., et al. Elevated luteinizing hormone expression colocalizes with neurons vulnerable to Alzheimer's disease pathology. J Neurosci Res 70 (2002) 514-518
84. Temeli E., Oprescu M., Coculescu M., and Alessandrescu D. LH and FSH levels in serum and cerebrospinal fluid (CSF) of human fetus. Endocrinologie 23 (1985) 55-59
85. Lei Z., and Rao C. Neural actions of luteinizing hormone and human chorionic gonadotropin. Semin Reprod Med 19 (2001) 103-109
86. Webber K., Stocco D., Casadesus G., Bowen R., Atwood C., Previll L., et al. Steroidogenic Acute Regulatory Protein (StAR): Evidence of gonadotropin-induced steroidogenesis in Alzheimer disease. Mol Neurodegener 1 (2006) 14
87. Smith M., Perry G., Atwood C., and Bowen R. Estrogen replacement and risk of Alzheimer disease. JAMA 289 (2003) 1100 [author reply 1101-1102]
88. Hsiang Y., Berkovitz G., Bland G., Migeon C., and Warren A. Gonadal function in patients with Down syndrome. Am J Med Genet 27 (1987) 449-458
89. Barron A., Verdile G., and Martins R. The role of gonadotropins in Alzheimer's disease: Potential neurodegenerative mechanisms. Endocrine 29 (2006) 257-269
90. Bowen R., Isley J., and Atkinson R. An association of elevated serum gonadotropin concentrations and Alzheimer disease?. J Neuroendocrinol 12 (2000) 351-354
91. Short R., Bowen R., O'Brien P., and Graff-Radford N. Elevated gonadotropin levels in patients with Alzheimer disease. Mayo Clin Proc 76 (2001) 906-909
92. Ogawa O., Lee H., Zhu X., Raina A., Harris P., Castellani R., et al. Increased p27, an essential component of cell cycle control, in Alzheimer's disease. Aging Cell 2 (2003) 105-110
93. Nunomura A., Perry G., Aliev G., Hirai K., Takeda A., Balraj E., et al. Oxidative damage is the earliest event in Alzheimer disease. J Neuropathol Exp Neurol 60 (2001) 759-767
94. Raina A., Zhu X., Rottkamp C., Monteiro M., Takeda A., and Smith M. Cyclin toward dementia: Cell cycle abnormalities and abortive oncogenesis in Alzheimer disease. J Neurosci Res 61 (2000) 128-133
95. Bowser R., and Smith M. Cell cycle proteins in Alzheimer's disease: Plenty of wheels but no cycle. J Alzheimer's Dis 4 (2002) 249-254
96. Obrenovich M., Raina A., Ogawa O., Atwood C., and Smith M. Alzheimer disease-A new beginning, or a final exit?. In: Copani A., and Nicoletti F. (Eds). The Cell Cycle and Neuronal Cell Death (2005), Landes Bioscience, Georgestown, Texas 79-93
97. McShea A., Harris P., Webster K., Wahl A., and Smith M. Abnormal expression of the cell cycle regulators P16 and CDK4 in Alzheimer's disease. Am J Pathol 150 (1997) 1933-1939
98. Hirai K., Aliev G., Nunomura A., Fujioka H., Russell R., Atwood C., et al. Mitochondrial abnormalities in Alzheimers disease. J Neurosci 21 (2001) 3017-3023
99. Zhu X., Rottkamp C., Boux H., Takeda A., Perry G., and Smith M. Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer disease. J Neuropathol Exp Neurol 59 (2000) 880-888
100. Perry G., Roder H., Nunomura A., Takeda A., Friedlich A., Zhu X., et al. Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal phosphorylation. Neuroreport 10 (1999) 2411-2415
101. Zhu X., Castellani R., Takeda A., Nunomura A., Atwood C., Perry G., et al. Differential activation of neuronal ERK, JNK/SAPK and p38 in Alzheimer disease: The 'two hit' hypothesis. Mech Ageing Dev 123 (2001) 39-46
102. Harris D., Bonfil D., Chuderland D., Kraus S., Seger R., and Naor Z. Activation of MAPK cascades by GnRH: ERK and Jun N-terminal kinase are involved in basal and GnRH-stimulated activity of the glycoprotein hormone LHbeta-subunit promoter. Endocrinology 143 (2002) 1018-1025
103. Vincent I., Zheng J., Dickson D., Kress Y., and Davies P. Mitotic phosphoepitopes precede paired helical filaments in Alzheimer's disease. Neurobiol Aging 19 (1998) 287-296
104. Bowen R., Verdile G., Liu T., Parlow A., Perry G., Smith M., et al. Luteinizing hormone, a reproductive regulator that modulates the processing of amyloid-beta precursor protein and amyloid-beta deposition. J Biol Chem 279 (2004) 20539-20545
105. Schally A., and Nagy A. Targeted cytotoxic analogs of luteinizing hormone-releasing hormone: A reply. Eur J Endocrinol 144 (2001) 559
106. Casadesus G., Webber K., Atwood C., Pappolla M., Perry G., Bowen R., et al. Luteinizing hormone modulates cognition and amyloid-beta deposition in Alzheimer APP transgenic mice. Biochim Biophys Acta 1762 (2006) 447-452
107. Casadesus G., Milliken E., Webber K., Bowen R., Lei Z., Rao C., et al. Increases in luteinizing hormone are associated with declines in cognitive performance. Mol Cell Endocrinol 269 (2007) 107-111
108. Reynolds B., Smith M., and Gregory C. Luteinizing hormone: A unifying hypothesis for Alzheimer disease etiology, pathogenesis and treatment. Alzheimer's Dementia 2 Suppl. 1 (2006) S621
109. LaPlante B., Powers C., Gault J., Reynolds B., and Gregory C. Stabilization of cognitive decline in Alzheimer's disease following treatment with leuprolide acetate. Alzheimer's Dementia 2 Suppl (2006) S620-S621