Anti-aggregation and fibril-destabilizing effects of sex hormones on α-synuclein fibrils in vitro

Experimental Neurology

Volumn 217, Issue 2, 2009, Pages 434-439

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

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

^b National Hospital Organization Iou National Hospital   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Synuclein fibrils; Anti aggregation effects; Effective concentrations (EC50); Electron microscopy; Estrogen; Lewy body diseases; Multiple system atrophy; Parkinson's disease; Sex hormone; Thioflavin S

Indexed keywords

ALPHA SYNUCLEIN; ANDROSTENEDIONE; ESTRADIOL; ESTRIOL; ESTRONE; TESTOSTERONE; THIOFLAVINE;

ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; ELECTRON MICROSCOPY; FLUORESCENCE SPECTROSCOPY; HORMONE STRUCTURE; HUMAN; IN VITRO STUDY; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; TEMPERATURE;

ALPHA-SYNUCLEIN; ESTRADIOL; ESTRIOL; GONADAL STEROID HORMONES; HUMANS; LEWY BODIES; LEWY BODY DISEASE; MICROSCOPY, ELECTRON; MOLECULAR STRUCTURE; NEUROFIBRILS; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE; SPECTROMETRY, FLUORESCENCE; TESTOSTERONE; THIAZOLES;

EID: 67349162100     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.03.003     Document Type: Article

References (45)

1. Amantea D., Russo R., Bagetta G., and Corasaniti M.T. From clinical evidence to molecular mechanisms underlying neuroprotection afforded by estrogens. Pharmacol. Res. 52 (2005) 119-132
2. Behl C., Skutella T., Lezoualch F., Post A., Widmann M., Newton C.J., and Holsboer F. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol. Pharmacol. 51 (1997) 535-541
3. Braak H., Del Tredici K., Rüb U., de Vos R.A., Jansen Steur E.N., and Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 24 (2003) 197-211
4. Currie L.J., Harrison M.B., Trugman J.M., Bennett J.P., and Wooten G.F. Postmenopausal estrogen use affects risk for Parkinson disease. Arch. Neurol. 61 (2004) 886-888
5. Disshon K.A., and Dluzen D.E. Estrogen as a neuromodulator of MPTP-induced neurotoxicity: effects upon striatal dopamine release. Brain Res. 764 (1997) 9-16
6. Ehrnhoefer D.E., Bieschke J., Boeddrich A., Herbst M., Masino L., Lurz R., Engemann S., Pastore A., and Wanker E.E. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Mol. Biol. 15 (2008) 558-566
7. Eliezer D., Kutluay E., Bussell Jr. R., and Browne G. Conformational properties of α-synuclein in its free and lipid-associated states. J. Mol. Biol. 307 (2001) 1061-1073
8. Fink A.L. Natively unfolded proteins. Curr. Opin. Struct. Biol. 15 (2005) 35-41
9. Goedert M. α-Synuclein and neurodegenerative diseases. Nat. Rev. Neurosci. 2 (2001) 492-501
10. Hirohata M., Ono K., Naiki H., and Yamada M. Non-steroidal anti-inflammatory drugs have potent anti-fibrillogenic and fibril-destabilizating effects for α-synuclein fibrils in vitro. Neuropharmacology 54 (2008) 620-627
11. Hofman A., Collette H.J., and Bartelds A.I. Incidence and risk factors of Parkinson's disease in The Netherlands. Neuroepidemiology 8 (1989) 296-299
12. Irizarry M.C., Kim T.W., McNamara M., Tanzi R.E., George J.M., Clayton D.F., and Hyman B.T. Characterization of the precursor protein of the non-Aβ component of senile plaques (NACP) in the human central nervous system. J. Neuropathol. Exp. Neurol. 55 (1996) 889-895
13. Iwai A., Masliah E., Yoshimoto M., Ge N., Flanagan L., de Silva H.A., Kittel A., and Saitoh T. The precursor protein of non-Aβ component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14 (1995) 467-475
14. Lashuel H.A., Petre B.M., Wall J., Simon M., Nowak R.J., Walz T., and Lansbury Jr. P.T. α-Synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J. Mol. Biol. 322 (2002) 1089-1102
15. Liu B., and Dluzen D.E. Oestrogen and nigrostriatal dopaminergic neurodegeneration: animal models and clinical reports of Parkinson's disease. Clin. Exp. Pharmacol. Physiol. 34 (2007) 555-565
16. Lobo R.A., Brenner P., and Mishell D.R. Metabolic parameters and steroid levels in postmenopausal women receiving lower doses of natural estrogen replacement. Obstet. Gynecol. 62 (1983) 94-98
17. Longcope C. Methods and results of aromatization studies in vivo. Cancer Res. 42 (1982) 3307s-3311s
18. Lücking C.B., and Brice A. Alpha-synuclein and Parkinson's disease. Cell Mol. Life Sci. 57 (2000) 1894-1908
19. Marchetti B., Serra P.A., L, 'Episcopo F., Tirolo C., Caniglia S., Testa N., Cioni S., Gennuso F., Rocchitta G., Desole M.S., Mazzarino M.C., Miele E., and Morale M.C. Hormones are key actors in gene × environment interactions programming the vulnerability to Parkinson's disease: glia as a common final pathway. Ann. N.Y. Acad. Sci. 1057 (2005) 296-318
20. Marder K., Tang M.X., Alfaro B., Mejia H., Cote L., Jacobs D., Stern Y., Sano M., and Mayeux R. Postmenopausal estrogen use and Parkinson's disease with and without dementia. Neurology 50 (1998) 1141-1143
21. Mayeux R., Marder K., Cote L.J., Denaro J., Hemenegildo N., Mejia H., Tang M.X., Lantigua R., Wilder D., Gurland B., and Hauser A. The frequency of idiopathic Parkinson's disease by age, ethnic group, and sex in northern Manhattan, 1988-1993. Am. J. Epidemiol. 142 (1995) 820-827
22. Molnar G., and Kassai-Bazsa Z. Gonadotropin, ACTH, prolactin, sexual steroid and cortisol levels in postmenopausal women's cerebrospinal fluid (CSF). Arch. Gerontol. Geriatr. 24 (1997) 269-280
23. Morinaga A., Hirohata M., Ono K., and Yamada M. Estrogen has anti-amyloidogenic effects on Alzheimer's β-amyloid fibrils in vitro. Biochem. Biophys. Res. Commun. 359 (2007) 697-702
24. Ono K., Hirohata M., and Yamada M. α-Synuclein assembly as a therapeutic target of Parkinson's disease and related disorders. Curr. Pharm. Des. 14 (2008) 3247-3266
25. Ono K., Hirohata M., and Yamada M. Anti-fibrillogenic and fibril-destabilizing activities of anti-Parkinsonian agents for α-synuclein fibrils in vitro. J. Neurosci. Res. 85 (2007) 1547-1557
26. Ono K., Hirohata M., and Yamada M. Anti-fibrillogenic and fibril-destabilizing activity of nicotine in vitro: implications for the prevention and therapeutics of Lewy body diseases. Exp. Neurol. 205 (2007) 414-424
27. Ono K., Noguchi M., Matsumoto Y., Yanase D., Iwasa K., Naiki H., and Yamada M. Cerebrospinal fluid of Alzheimer patients promotes β-amyloid fibril formation in vitro. Neurobiol. Dis. 20 (2005) 233-240
28. Ono K., Noguchi-Shinohara M., Yoshita M., Naiki H., and Yamada M. Cerebrospinal fluid of Alzheimer's disease and dementia with Lewy bodies patients enhances α-synuclein fibril formation in vitro. Exp. Neurol. 203 (2007) 579-583
29. Ono K., and Yamada M. Antioxidant compounds have potent antifibrillogenic and fibril-destabilizing effects for α-synuclein fibrils in vitro. J. Neurochem. 97 (2006) 105-115
30. Popat R.A., Van Den Eeden S.K., Tanner C.M., McGuire V., Bernstein A.L., Bloch D.A., Leimpeter A., and Nelson L.M. Effect of reproductive factors and postmenopausal hormone use on the risk of Parkinson disease. Neurology 65 (2005) 383-390
31. Ragonese P., D, 'Amelio M., Salemi G., Aridon P., Gammino M., Epifanio A., Morgante L., and Savettieri G. Risk of Parkinson disease in women: effect of reproductive characteristics. Neurology 62 (2004) 2010-2014
32. Ragonese P., D, 'Amelio M., and Savettieri G. Implications for estrogens in Parkinson's disease: an epidemiological approach. Ann. N. Y. Acad. Sci. 1089 (2006) 373-382
33. Saunders-Pullman R., Gordon-Elliott J., Parides M., Fahn S., Saunders H.R., and Bressman S. The effect of estrogen replacement on early Parkinson's disease. Neurology 52 (1999) 1417-1421
34. Schönknecht P., Pantel J., Klinga K., Jensen M., Hartmann T., Salbach B., and Schröder J. Reduced cerebrospinal fluid estradiol levels are associated with increased β-amyloid levels in female patients with Alzheimer's disease. Neurosci. Lett. 307 (2001) 122-124
35. Serpell L.C., Berriman J., Jakes R., Goedert M., and Crowther R.A. Fiber diffraction of synthetic α-synuclein filaments shows amyloid-like cross-β conformation. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 4897-4902
36. Trojanowski J.Q., and Lee V.M. Parkinson's disease and related α-synucleinopathies are brain amyloidoses. Ann. N. Y. Acad. Sci. 991 (2003) 107-110
37. Uversky V.N., Lee H.J., Li J., Fink A.L., and Lee S.J. Stabilization of partially folded conformation during α-synuclein oligomerization in both purified and cytosolic preparations. J. Biol. Chem. 276 (2001) 43495-43498
38. Uversky V.N., Li J., and Fink A.L. Evidence for a partially folded intermediate in α-synuclein fibril formation. J. Biol. Chem. 276 (2001) 10737-10744
39. Uversky V.N. Neuropathology, biochemistry, and biophysics of α-synuclein aggregation. J. Neurochem. 103 (2007) 17-37
40. Van Den Eeden S.K., Tanner C.M., Bernstein A.L., Fross R.D., Leimpeter A., Bloch D.A., and Nelson L.M. Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity. Am. J. Epidemiol. 157 (2003) 1015-1022
41. Volles M.J., and Lansbury Jr. P.T. Zeroing in on the pathogenic form of α-synuclein and its mechanism of neurotoxicity in Parkinson's disease. Biochemistry 42 (2003) 7871-7878
42. Weinreb P.H., Zhen W., Poon A.W., Conway K.A., and Lansbury Jr. P.T. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 35 (1996) 13709-13715
43. Wood S.J., Wypych J., Steavenson S., Louis J.C., Citron M., and Biere A.L. α-Synuclein fibrillogenesis is nucleation dependent. Implications for the pathogenesis of Parkinson's disease. J. Biol. Chem. 274 (1999) 19509-19512
44. Wright J.V., Schliesman B., and Robinson L. Comparative measurement of serum estriol, estradiol, and estrone in non-pregnant, premenopausal women: a preliminary investigation. Altern. Med. Rev. 4 (1999) 266-270
45. Zhu M., Rajamani S., Kaylor J., Han S., Zhou F., and Fink A.L. The flavonoid baicalein inhibits fibrillation of α-synuclein and disaggregates existing fibrils. J. Biol. Chem. 279 (2004) 26846-26857