Effects of sex hormones on Alzheimer's disease-associated β-amyloid oligomer formation in vitro

Experimental Neurology

Volumn 228, Issue 2, 2011, Pages 298-302

  Morinaga, Akiyoshi ^a,b   Ono, Kenjiro ^a   Takasaki, Junichi ^a   Ikeda, Tokuhei ^a   Hirohata, Mie ^a,b   Yamada, Masahito ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

^b National Hospital Organization Iou National Hospital   (Japan)

Author keywords

Alzheimer's disease; Amyloid protein; Central nervous systems; Electron microscopy; Estrogen; Oligomer; Photo induced cross linking of unmodified proteins; Sex hormones

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; ANDROSTENEDIONE; ESTRADIOL; ESTRIOL; ESTRONE; TESTOSTERONE;

ALZHEIMER DISEASE; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; IN VITRO STUDY; OLIGOMERIZATION; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; FEMALE; GONADAL STEROID HORMONES; HUMANS; PLAQUE, AMYLOID; POSTMENOPAUSE; PROTEIN MULTIMERIZATION;

EID: 79952697850     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.01.011     Document Type: Article

References (48)

1. Andersen K., Launer L.J., Dewey M.E., Letenneur L., Ott A., Copeland J.R., Dartigues J.F., Kragh-Sorensen P., Baldereschi M., Brayne C., Lobo A., Martinez-Lage J.M., Stijnen T., Hofman A. Gender differences in the incidence of AD and vascular dementia: the EURODEM Studies. EURODEM Incidence Research Group. Neurology 1999, 53:1992-1997.
2. Bitan G., Lomakin A., Teplow D.B. Amyloid β-protein oligomerization: prenucleation interactions revealed by photo-induced cross-linking of unmodified proteins. J. Biol. Chem. 2001, 276:35176-35184.
3. Bitan G., Kirkitadze M.D., Lomakin A., Vollers S.S., Benedek G.B., Teplow D.B. Amyloid β-protein (Aβ) assembly: Aβ 40 and Aβ 42 oligomerize through distinct pathways. Proc. Natl Acad. Sci. U. S. A. 2003, 100:330-335.
4. Bitan G., Fradinger E.A., Spring S.M., Teplow D.B. Neurotoxic protein oligomers-what you see is not always what you get. Amyloid 2005, 12:88-95.
5. Bitan G. Structural study of metastable amyloidogenic protein oligomers by photo-induced cross-linking of unmodified proteins. Methods Enzymol. 2006, 413:217-236.
6. Canadian Study of Health and Aging Working Group Canadian study of health and aging: study methods and prevalence of dementia. Can. Med. Assoc. J. 1994, 150:899-913.
7. Coffey C.E., Lucke J.F., Saxton J.A., Ratcliff G., Unitas L.J., Billing B., Bryan R.N. Sex differences in brain aging: a quantitative magnetic resonance imaging study. Arch. Neurol. 1998, 55:169-179.
8. Dahlgren K.N., Menelli A.M., Stine W.B., Baker L.K., Krefft G.A., LaDu M.J. Oligomeric and fibrillar species of amyloid-β peptides differentially affect neuronal viability. J. Biol. Chem. 2002, 277:32046-32053.
9. Englund D.E., Elamsson K.B., Johansson E.D.B. Bioavailability of oestriol. Acta Endorinol. 1982, 99:136-140.
10. Espeland M.A., Rapp S.R., Shumaker S.A., Brunner R., Manson J.E., Sherwin B.B., Hsia J., Margolis K.L., Hogan P.E., Wallace R., Dailey M., Freeman R., Hays J. Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004, 291:2959-2968. Women's Health Initiative Memory Study.
11. Fancy D.A., Kodadek T. Chemistry for the analysis of protein-protein interactions: rapid and efficient cross-linking triggered by long wavelength light. Proc. Natl Acad. Sci. USA 1999, 96:6020-6024.
12. Haass C., Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid-β-peptide. Nat. Rev. Mol. Cell Biol. 2007, 8:101-112.
13. Henderson V.W., Paganini-Hill A., Emanual C.K., Dunn M.E., Buckwalter J.G. Estrogen replacement therapy in older women. Comparisons between Alzheimer's disease cases and nondemented control subjects. Arch. Neurol. 1994, 51:896-900.
14. Hogervorst E., Williams J., Budge M., Riedel W., Jolles J. The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis. Neuroscience 2000, 101:485-512.
15. Hy L.X., Keller D.M. Prevalence of AD among whites: a summary by levels of severity. Neurology 2000, 55:198-204.
16. Jaffe A.B., Toran-Allerand C.D., Greengard P., Gandy S.E. Estrogen regulates metabolism of Alzheimer amyloid β precursor protein. J. Biol. Chem. 1994, 269:13065-13068.
17. Jorm A.F., Korten A.E., Henderson A.S. The prevalence of dementia: a quantitative integration of the literature. Acta Psychiatr. Scand. 1987, 76:465-479.
18. Kawas C., Resnick S., Morrison A., Brookmeyer R., Corrada M., Zonderman A., Bacal C., Lingle D.D., Metter E. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: the Baltimore Longitudinal Study of Aging. Neurology 1997, 48:1517-1521.
19. Launer L.J., Andersen K., Dewey M.E., Letenneur L., Ott A., Amaducci L.A., Brayne C., Copeland J.R., Dartigues J.F., Kragh-Sorensen P., Lobo A., Martinez-Lage J.M., Stijnen T., Hofman A. Rates and risk factors for dementia and Alzheimer's disease: results from EURODEM pooled analyses EURODEM Incidence Research Group and Work Groups. European Studies of Dementia. Neurology 1999, 52:78-84.
20. LeBlanc E.S., Janowsky J., Chan B.K., Nelson H.D. Hormone replacement therapy and cognition: systemic review and meta-analysis. JAMA 2001, 285:1489-1499.
21. Li R., Shen Y., Yang L.B., Leu L.F., Finch C., Rogers J. Estrogen enhances uptake of amyloid β-protein by microglia derived from the human cortex. J. Neurochem. 2000, 75:1447-1454.
22. Lobo R.A., Brenner P., Mishell D.R. Metabolic parameters and steroid levels in postmenopausal women receiving lower doses of natural estrogen replacement. Obstet. Gynecol. 1983, 62:94-98.
23. Longcope C. Methods and results of aromatization studies in vivo. Cancer Res. 1982, 42:3307s-3311s.
24. Manly J.J., Merchant C.A., Jacobs D.M., Small S.A., Bell K., Ferin M., Mayeux R. Endogenous estrogen levels and Alzheimer's disease among postmenopausal women. Neurology 2000, 54:833-837.
25. Molnar G., Kassai-Bazsa Z. Gonadotoropin, ACTH, prolactin, sexual steroid and cortisol levels in postmenopausal women's cerebrospinal fluid (CSF). Arch. Gerontol. Geriatr. 1997, 24:269-280.
26. Morinaga A., Hirohata M., Ono K., Yamada M. Estrogen has anti-amyloidogenic effects on Alzheimer's β-amyloid fibrils in vitro. Biochem. Biophys. Res. Commun. 2007, 359:697-702.
27. Necula M., Kayed R., Milton S., Glabe C.G. Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J. Biol. Chem. 2007, 282:10311-11034.
28. Nitz M., Fenili D., Darabie A.A., Wu L., Cousins J.E., McLaurin J. Modulation of amyloid-β aggregation and toxicity by inosose stereoisomers. FEBS J. 2008, 275:1663-1674.
29. Ono K., Hasegawa K., Yoshiike Y., Takashima A., Yamada M., Naiki H. Nordihydroguaiaretic acid potently breaks down pre-formed Alzheimer's β-amyloid fibrils in vitro. J. Neurochem. 2002, 81:434-440.
30. Ono K., Hamaguchi T., Naiki H., Yamada M. Anti-amyloidogenic effects of antioxidants: implications for the prevention and therapeutics of Alzheimer's disease. Biochim. Biophys. Acta 2006, 1762:575-586.
31. Ono K., Condron M.M., Ho L., Wang J., Zhao W., Pasinetti G.M., Teplow D.B. Effects of grape seed-derived polyphenols on amyloid β-protein self-assembly and cytotoxicity. J. Biol. Chem. 2008, 283:32176-32187.
32. Ono K., Condron M.M., Teplow D.B. Structure-neurotoxicity relationships of amyloid β-protein oligomers. Proc. Natl Acad. Sci. U. S. A. 2009, 106:14745-14750.
33. Ono K., Condron M.M., Teplow D.B. Effect of the English (H6R) and Tottori (D7N) familial Alzheimer disease mutations on amyloid β protein assembly and toxicity. J Biol Chem 2010, 285:23186-23197.
34. Paganini-Hill A., Henderson V.W. Estrogen replacement therapy and risk of Alzheimer disease. Arch. Intern. Med. 1996, 156:2213-2217.
35. Petanceska S.S., Nagy V., Frail D., Gandy S. Ovariectomy and 17β-estradiol modulate the levels of Alzheimer's amyloid β peptides in brain. Neurology 2000, 54:2212-2217.
36. Pinkerton J.V., Henderson V.W. Estrogen and cognition, with a focus on Alzheimer's disease. Semin. Reprod. Med. 2005, 23:172-179.
37. Roychaudhuri R., Yang M., Hoshi M.M., Teplow D.B. Amyloid β-protein assembly and Alzheimer disease. J. Biol. Chem. 2009, 284:4749-4753.
38. Schönknecht P., Pantel J., Klinga K., Jensen M., Hartmann T., Salbach B., Schroder J. Reduced cerebrospinal fluid estradiol levels are associated with increased β-amyloid levels in female patients with Alzheimer's disease. Neurosci. Lett. 2001, 307:122-124.
39. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., Brett F.M., Farrell M.A., Rowan M.J., Lemere C.A., Regan C.M., Walsh D.M., Sabatini B.L., Selkoe D.J. Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 2008, 14:837-842.
40. Sherwin, B.B., Chertkow, H., Schipper, H., Nasreddine, Z., A randomized controlled trial of estrogen treatment in men with mild cognitive impairment. Neurobiol Aging. In press.
41. Shumaker S.A., Legault C., Rapp S.R., Thal L., Wallance R.B., Ockene J.K., Hendrix S.L., Jones B.N., Assaf A.R., Jackson R.D., Kotchen J.M., Wassertheil-Smoller S., Wactawski-Wende J., WHIMS Investigators 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, 289:2651-2662.
42. Teplow D.B. Structural and kinetic features of amyloid β-protein fibrillogenesis. Amyloid 1998, 5:121-142.
43. Tomiyama T., Shoji A., Kataoka K., Suwa Y., Asano S., Kaneko H., Endo N. Inhibition of amyloid β protein aggregation and neurotoxicity by rifampicin. Its possible function as a hydroxyl radical scavenger. J. Biol. Chem. 1996, 271:6839-6844.
44. Wright J.V., Schliesman B., Robinson L. Comparative measurement of serum estriol, estradiol, and estrone in non-pregnant, premenopausal women: a preliminary investigation. Altern. Med. Rev. 1999, 4:266-270.
45. Yaffe K., Sawaya G., Lieberburg I., Grady D. Estrogen therapy in postmenopausal women. Effects on cognitive function and dementia. JAMA 1998, 279:688-695.
46. Yamin G., Ono K., Inayathullah M., Teplow D.B. Amyloid β-protein assembly as a therapeutic target of Alzheimer's disease. Curr. Pharm. Des. 2008, 14:3231-3246.
47. Yue X., Lu M., Lancaster T., Cao P., Honda S., Staufenbiel M., Harada N., Zhong Z., Shen Y., Li R. Brain estrogen deficiency accelerates Aβ plaque formation in an Alzheimer's disease animal model. Proc. Natl Acad. Sci. USA 2005, 102:19198-19203.
48. Zandi P.P., Carlson M.C., Plassman B.L., Welsh-Bohmer K.A., Mayer L.S., Steffens D.C., Breitner J.C., Cache County Memory Study Investigators Hormone replacement therapy and incidence of Alzheimer's disease in older women. The Cache County Study. JAMA 2002, 288:2123-2129.