Neuroprotective and nootropic drug noopept rescues α-synuclein amyloid cytotoxicity

Journal of Molecular Biology

Volumn 414, Issue 5, 2011, Pages 699-712

  Jia, Xueen ^a   Gharibyan, Anna L ^a   Öhman, Anders ^a   Liu, Yonggang ^a,b   Olofsson, Anders ^a   Morozova Roche, Ludmilla A ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

amyloid; cytotoxicity; noopept; Parkinson's disease; synuclein

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; NOOPEPT; NOOTROPIC AGENT; THIOFLAVINE; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL VIABILITY; CIRCULAR DICHROISM; CONTROLLED STUDY; CYTOTOXICITY; DRUG BINDING; DRUG EFFECT; FLUORESCENCE ANALYSIS; HETERONUCLEAR MULTIPLE BOND CORRELATION; HETERONUCLEAR NUCLEAR MAGNETIC RESONANCE; HUMAN; HUMAN CELL; HYDROPHOBICITY; NEUROBLASTOMA CELL; NEUROPROTECTION; OLIGOMERIZATION; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL;

EID: 82555186980     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.09.044     Document Type: Article

References (53)

1. Simuni T., and Hurtig H.I. Parkinson's disease: the clinical picture C.M. Clark, J.Q. Trojanowski, Neurodegenerative Dementias 2000 McGraw-Hill New York, NY 193 203
2. Gelb D.J., Oliver E., and Gilman S. Diagnostic criteria for Parkinson disease Arch. Neurol. 56 1999 33 39 (Pubitemid 29046907)
3. Pakkenberg B., Moller A., Gundersen H.J., Mouritzen Dam A., and Pakkenberg H. The absolute number of nerve cells in substantia nigra in normal subjects and in patients with Parkinson's disease estimated with an unbiased stereological method J. Neurol., Neurosurg. Psychiatry 54 1991 30 33
4. Damier P., Hirsch E.C., Agid Y., and Graybiel A.M. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease Brain 122 1999 1437 1448 (Pubitemid 29374122)
5. Uversky V.N. Alpha-synuclein misfolding and neurodegenerative diseases Curr. Protein Pept. Sci. 9 2008 507 540
6. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., and Kosel S. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease Nat. Genet. 18 1998 106 108
7. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., and Lansbury Jr.P.T. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy Proc. Natl Acad. Sci. USA 97 2000 571 576 (Pubitemid 30070350)
8. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., and Kachergus J. Alpha-synuclein locus triplication causes Parkinson's disease Science 302 2003 841 (Pubitemid 37339619)
9. Maraganore D.M., Wilkes K., Lesnick T.G., Strain K.J., de Andrade M., and Rocca W.A. A limited role for DJ1 in Parkinson disease susceptibility Neurology 63 2004 550 553 (Pubitemid 39031392)
10. Singleton A., Gwinn-Hardy K., Sharabi Y., Li S.T., Holmes C., and Dendi R. Association between cardiac denervation and parkinsonism caused by alpha-synuclein gene triplication Brain 127 2004 768 772 (Pubitemid 38478521)
11. Conway K.A., Harper J.D., and Lansbury P.T. Jr Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid Biochemistry 39 2000 2552 2563 (Pubitemid 30148907)
12. Li J., Uversky V.N., and Fink A.L. Effect of familial Parkinson's disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human alpha-synuclein Biochemistry 40 2001 11604 11613 (Pubitemid 32911305)
13. Fredenburg R.A., Rospigliosi C., Meray R.K., Kessler J.C., Lashuel H.A., Eliezer D., and Lansbury Jr.P.T. The impact of the E46K mutation on the properties of alpha-synuclein in its monomeric and oligomeric states Biochemistry 46 2007 7107 7118 (Pubitemid 46973985)
14. Brown D.R. Oligomeric alpha-synuclein and its role in neuronal death IUBMB Life 62 2010 334 339
15. 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 (Pubitemid 26363912)
16. Totterdell S., Hanger D., and Meredith G.E. The ultrastructural distribution of alpha-synuclein-like protein in normal mouse brain Brain Res. 1004 2004 61 72 (Pubitemid 38368062)
17. Walsh D.M., and Selkoe D.J. Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration Protein Pept. Lett. 11 2004 213 228 (Pubitemid 38689025)
18. Caughey B., and Lansbury P.T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders Annu. Rev. Neurosci. 26 2003 267 298 (Pubitemid 37064935)
19. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., and Liosatos M. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins Proc. Natl. Acad. Sci. USA 95 1998 6448 6453
20. Burke W.J., Kumar V.B., Pandey N., Panneton W.M., Gan Q., and Franko M.W. Aggregation of alpha-synuclein by DOPAL, the monoamine oxidase metabolite of dopamine Acta Neuropathol. 115 2008 193 203
21. Rekas A., Knott R.B., Sokolova A., Barnham K.J., Perez K.A., and Masters C.L. The structure of dopamine induced alpha-synuclein oligomers Eur. Biophys. J. 39 2010 1407 1419
22. Mazzulli J.R., Mishizen A.J., Giasson B.I., Lynch D.R., Thomas S.A., and Nakashima A. Cytosolic catechols inhibit alpha-synuclein aggregation and facilitate the formation of intracellular soluble oligomeric intermediates J. Neurosci. 26 2006 10068 10078 (Pubitemid 44477168)
23. Leong S.L., Cappai R., Barnham K.J., and Pham C.L. Modulation of alpha-synuclein aggregation by dopamine: a review Neurochem. Res. 34 2009 1838 1846
24. Pham C.L., Leong S.L., Ali F.E., Kenche V.B., Hill A.F., and Gras S.L. Dopamine and the dopamine oxidation product 5,6-dihydroxylindole promote distinct on-pathway and off-pathway aggregation of alpha-synuclein in a pH-dependent manner J. Mol. Biol. 387 2009 771 785
25. Yang D.S., Yip C.M., Huang T.H., Chakrabartty A., and Fraser P.E. Manipulating the amyloid-beta aggregation pathway with chemical chaperones J. Biol. Chem. 274 1999 32970 32974 (Pubitemid 129535336)
26. Wang M.S., Boddapati S., Emadi S., and Sierks M.R. Curcumin reduces alpha-synuclein induced cytotoxicity in Parkinson's disease cell model BMC Neurosci. 11 2010 57
27. Bieschke J., Russ J., Friedrich R.P., Ehrnhoefer D.E., Wobst H., Neugebauer K., and Wanker E.E. EGCG remodels mature alpha-synuclein and amyloid-beta fibrils and reduces cellular toxicity Proc. Natl Acad. Sci. USA 107 2010 7710 7715
28. Necula M., Breydo L., Milton S., Kayed R., van der Veer W.E., Tone P., and Glabe C.G. Methylene blue inhibits amyloid Abeta oligomerization by promoting fibrillization Biochemistry 46 2007 8850 8860 (Pubitemid 47208418)
29. Gudasheva T.A., Voronina T.A., Ostrovskaya R.U., Rozantsev G.G., Vasilevich N.I., and Trofimov S.S. Synthesis and antiamnestic activity of a series of N-acylprolyl-containing dipeptides Eur. J. Med Chem. 31 1996 151 157 (Pubitemid 26081881)
30. Pelsman A., Hoyo-Vadillo C., Gudasheva T.A., Seredenin S.B., Ostrovskaya R.U., and Busciglio J. GVS-111 prevents oxidative damage and apoptosis in normal and Down's syndrome human cortical neurons Int. J. Dev. Neurosci. 21 2003 117 124 (Pubitemid 36444536)
31. Bukanova J.V., Solntseva E.I., and Skrebitsky V.G. Selective suppression of the slow-inactivating potassium currents by nootropics in molluscan neurons Int. J. Neuropsychopharmacol. 5 2002 229 237
32. Ostrovskaya R.U., Gruden M.A., Bobkova N.A., Sewell R.D., Gudasheva T.A., and Samokhin A.N. The nootropic and neuroprotective proline-containing dipeptide noopept restores spatial memory and increases immunoreactivity to amyloid in an Alzheimer's disease model J. Psychopharmacol. 21 2007 611 619 (Pubitemid 47472723)
33. Ostrovskaia R.U., Gudasheva T.A., Voronina T.A., and Seredenin S.B. [The original novel nootropic and neuroprotective agent noopept] Eksp. Klin. Farmakol. 65 2002 66 72
34. Vorobyov V., Kaptsov V., Kovalev G., and Sengpiel F. Effects of nootropics on the EEG in conscious rats and their modification by glutamatergic inhibitors Brain Res. Bull. 85 2011 123 132
35. Avedisova A.S., and Yastrebov D.B. Comparative efficiency of noopept and piracetam in therapy of astenic disorder of organic genesis Neurology 15 2007 435 438
36. Malisauskas M., Ostman J., Darinskas A., Zamotin V., Liutkevicius E., Lundgren E., and Morozova-Roche L.A. Does the cytotoxic effect of transient amyloid oligomers from common equine lysozyme in vitro imply innate amyloid toxicity J. Biol. Chem. 280 2005 6269 6275 (Pubitemid 40341172)
37. Zamotin V., Gharibyan A., Gibanova N.V., Lavrikova M.A., Dolgikh D.A., and Kirpichnikov M.P. Cytotoxicity of albebetin oligomers depends on cross-beta-sheet formation FEBS Lett. 580 2006 2451 2457
38. Winblad B. Piracetam: a review of pharmacological properties and clinical uses CNS Drug Rev. 11 2005 169 182 (Pubitemid 41278980)
39. Neznamov G.G., and Teleshova E.S. Comparative studies of Noopept and piracetam in the treatment of patients with mild cognitive disorders in organic brain diseases of vascular and traumatic origin Neurosci. Behav. Physiol. 39 2009 311 321
40. Gudasheva T.A., Konstantinopol'skii M.A., Ostrovskaya R.U., and Seredenin S.B. Anxiolytic activity of endogenous nootropic dipeptide cycloprolylglycine in elevated plus-maze test Bull. Exp. Biol. Med. 131 2001 464 466 (Pubitemid 33149862)
41. Kondratenko R.V., Derevyagin V.I., and Skrebitsky V.G. Novel nootropic dipeptide Noopept increases inhibitory synaptic transmission in CA1 pyramidal cells Neurosci. Lett. 476 2010 70 73
42. Ostrovskaia R.U., Vakhitova Iu V., Salimgareeva M., Iamidanov R.S., Sadovnikov S.V., Kapitsa I.G., and Seredenin S.B. [On the mechanism of noopept action: decrease in activity of stress-induced kinases and increase in expression of neutrophines] Eksp. Klin. Farmakol. 73 2010 2 5
43. Ehrnhoefer D.E., Bieschke J., Boeddrich A., Herbst M., Masino L., and Lurz R. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers Nat. Struct. Mol. Biol. 15 2008 558 566 (Pubitemid 351799141)
44. Gazit E. A possible role for pi-stacking in the self-assembly of amyloid fibrils FASEB J. 16 2002 77 83 (Pubitemid 34027953)
45. Azriel R., and Gazit E. Analysis of the minimal amyloid-forming fragment of the islet amyloid polypeptide. An experimental support for the key role of the phenylalanine residue in amyloid formation J. Biol. Chem. 276 2001 34156 34161
46. Gharibyan A.L., Zamotin V., Yanamandra K., Moskaleva O.S., Margulis B.A., Kostanyan I.A., and Morozova-Roche L.A. Lysozyme amyloid oligomers and fibrils induce cellular death via different apoptotic/necrotic pathways J. Mol. Biol. 365 2007 1337 1349 (Pubitemid 46048842)
47. Xue W.F., Hellewell A.L., Hewitt E.W., and Radford S.E. Fibril fragmentation in amyloid assembly and cytotoxicity: when size matters Prion 4 2010 20 25
48. Seredenin, S. B., Voronina, T. A., Gudasheva, T. A., Ostrovskaya, R. U., Rozantsev, G. G., Skoldinov, A. P. et al. (1995). Biologically active N-acylprolyldipeptides having antiamnestic, antihypoxic effects. US Patent No. 5,439,930.
49. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
50. Johnson B.A., and Blevins R.A. NMRView: a computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
51. Eliezer D., Kutluay E., Bussell R. Jr., and Browne G. Conformational properties of alpha-synuclein in its free and lipid-associated states J. Mol. Biol. 307 2001 1061 1073 (Pubitemid 33029953)
52. Rao J.N., Kim Y.E., Park L.S., and Ulmer T.S. Effect of pseudorepeat rearrangement on alpha-synuclein misfolding, vesicle binding, and micelle binding J. Mol. Biol. 390 2009 516 529
53. Molina-Jimenez M.F., Sanchez-Reus M.I., Andres D., Cascales M., and Benedi J. Neuroprotective effect of fraxetin and myricetin against rotenone-induced apoptosis in neuroblastoma cells Brain Res. 1009 2004 9 16 (Pubitemid 38553843)