Globular and pre-fibrillar prion aggregates are toxic to neuronal cells and perturb their electrophysiology

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1784, Issue 6, 2008, Pages 873-881

  Sanghera, Narinder ^a   Wall, Mark ^a   Vénien Bryan, Catherine ^b   Pinheiro, Teresa J T ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Amyloid globular aggregate; Fibrillisation; Membrane potential; Prion; Toxic molecule

Indexed keywords

AMYLOID; ISOPROTEIN; OLIGOMER; PRION PROTEIN; RECOMBINANT PROTEIN;

ALPHA HELIX; ANIMAL CELL; ARTICLE; AUTOPSY; BETA SHEET; CELL LOSS; CYTOPLASM; DISULFIDE BOND; ELECTROPHYSIOLOGY; HUMAN; INTERNALIZATION; MOUSE; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN STRUCTURE;

ANIMALS; CELL LINE; CELL SURVIVAL; CIRCULAR DICHROISM; CRICETINAE; ELECTROPHYSIOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; MEMBRANE POTENTIALS; MICE; MICROSCOPY, ELECTRON; NEURONS; PRIONS; PROTEIN FOLDING; SPECTROPHOTOMETRY, INFRARED; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

ANIMALIA;

EID: 43649097136     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2008.02.017     Document Type: Article

References (55)

1. Dobson C.M. Protein folding and misfolding. Nature 426 (2003) 884-890
2. Sipe J.D., and Cohen A.S. Review: history of the amyloid fibril. J. Struc. Biol. 130 (2000) 88-98
3. 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
4. Bèueler H., Aguzzi A., Sailer A., Greiner R.A., Autenried P., Aguet M., and Weissmann C. Mice devoid of PrP are resistant to scrapie. Cell 73 (1993) 1339-1347
5. Sailer A., Bèueler H., Fischer M., Aguzzi A., and Weissmann C. No propagation of prions in mice devoid of PrP. Cell 77 (1994) 967-968
6. Lloyd S.E., Thompson S.R., Beck J.A., Linehan J.M., Wadsworth J.D., Brandner S., Collinge J., and Fisher E.M. Identification and characterization of a novel mouse prion gene allele. Mamm. Genome 15 (2004) 383-389
7. Mallucci G., Dickinson A., Linehan J., Klèohn P.C., Brandner S., and Collinge J. Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302 (2003) 871-874
8. Caughey B. Prion protein conversions: insight into mechanisms, TSE transmission barriers and strains. Br. Med. Bull. 66 (2003) 109-120
9. Stefani M., and Dobson C.M. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81 (2003) 678-699
10. Hill A.F., Joiner S., Linehan J., Desbruslais M., Lantos P.L., and Collinge J. Species-barrier-independent prion replication in apparently resistant species. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 10248-10253
11. El-Agnaf O.M., Jakes R., Curran M.D., Middleton D., Ingenito R., Bianchi E., Pessi A., Neill D., and Wallace A. Aggregates from mutant and wild-type alpha-synuclein proteins and NAC peptide induce apoptotic cell death in human neuroblastoma cells by formation of beta-sheet and amyloid-like filaments. FEBS Lett. 440 (1998) 71-75
12. Kayed R., Sokolov Y., Edmonds B., McIntire T.M., Milton S.C., Hall J.E., and Glabe C.G. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J. Biol. Chem. 279 (2004) 46363-46366
13. Kazlauskaite J., Young A., Gardner C.E., Macpherson J.V., Venien-Bryan C., and Pinheiro T.J. An unusual soluble beta-turn-rich conformation of prion is involved in fibril formation and toxic to neuronal cells. Biochem. Biophys. Res. Commun. 328 (2005) 292-305
14. Novitskaya V., Bocharova O.V., Bronstein I., and Baskakov I.V. Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons. J. Biol. Chem. 281 (2006) 13828-13836
15. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., Taddei N., Ramponi G., Dobson C.M., and Stefani M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
16. Baglioni S., Casamenti F., Bucciantini M., Luheshi L.M., Taddei N., Chiti F., Dobson C.M., and Stefani M. Prefibrillar amyloid aggregates could be generic toxins in higher organisms. J. Neurosci. 26 (2006) 8160-8167
17. Bondareff W., Mountjoy C.Q., Roth M., and Hauser D.L. Neurofibrillary degeneration and neuronal loss in Alzheimer's disease. Neurobiol. Aging 10 (1989) 709-715
18. Forno L.S. Neuropathology of Parkinson's disease. J. Neuropathol. Exp. Neurol. 55 (1996) 259-272
19. Chiesa R., and Harris D.A. Prion diseases: what is the neurotoxic molecule?. Neurobiol. Dis. 8 (2001) 743-763
20. Klement I.A., Skinner P.J., Kaytor M.D., Yi H., Hersch S.M., Clark H.B., Zoghbi H.Y., and Orr H.T. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 95 (1998) 41-53
21. Moechars D., Dewachter I., Lorent K., Reversâe D., Baekelandt V., Naidu A., Tesseur I., Spittaels K., Haute C.V., Checler F., Godaux E., Cordell B., and Van Leuven F. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J. Biol. Chem. 274 (1999) 6483-6492
22. Jeffrey M., Halliday W.G., Bell J., Johnston A.R., MacLeod N.K., Ingham C., Sayers A.R., Brown D.A., and Fraser J.R. Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus. Neuropathol. App. Neurobiol. 26 (2000) 41-54
23. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., and Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416 (2002) 535-539
24. Whalen B.M., Selkoe D.J., and Hartley D.M. Small non-fibrillar assemblies of amyloid beta-protein bearing the Arctic mutation induce rapid neuritic degeneration. Neurobiol. Dis. 20 (2005) 254-266
25. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., and Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300 (2003) 486-489
26. Demaimay R., Harper J., Gordon H., Weaver D., Chesebro B., and Caughey B. Structural aspects of Congo red as an inhibitor of protease-resistant prion protein formation. J. Neurochem. 71 (1998) 2534-2541
27. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., and Klein W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 6448-6453
28. Volles M.J., Lee S.J., Rochet J.C., Shtilerman M.D., Ding T.T., Kessler J.C., and Lansbury Jr. P.T. Vesicle permeabilization by protofibrillar alpha-synuclein: implications for the pathogenesis and treatment of Parkinson's disease. Biochemistry 40 (2001) 7812-7819
29. Baskakov I.V., Legname G., Prusiner S.B., and Cohen F.E. Folding of prion protein to its native alpha-helical conformation is under kinetic control. J. Biol. Chem. 276 (2001) 19687-19690
30. Baskakov I.V., Legname G., Baldwin M.A., Prusiner S.B., and Cohen F.E. Pathway complexity of prion protein assembly into amyloid. J. Biol. Chem. 277 (2002) 21140-21148
31. Giaccone G., Verga L., Bugiani O., Frangione B., Serban D., Prusiner S.B., Farlow M.R., Ghetti B., and Tagliavini F. Prion protein preamyloid and amyloid deposits in Gerstmann-Strèaussler-Scheinker disease, Indiana kindred. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 9349-9353
32. Lue L.F., Kuo Y.M., Roher A.E., Brachova L., Shen Y., Sue L., Beach T., Kurth J.H., Rydel R.E., and Rogers J. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155 (1999) 853-862
33. Mehlhorn I., Groth D., Stèockel J., Moffat B., Reilly D., Yansura D., Willett W.S., Baldwin M., Fletterick R., Cohen F.E., Vandlen R., Henner D., and Prusiner S.B. High-level expression and characterization of a purified 142-residue polypeptide of the prion protein. Biochemistry 35 (1996) 5528-5537
34. Sanghera N., and Pinheiro T.J. Binding of prion protein to lipid membranes and implications for prion conversion. J. Mol. Biol. 315 (2002) 1241-1256
35. Hoyer W., Antony T., Cherny D., Heim G., Jovin T.M., and Subramaniam V. Dependence of alpha-synuclein aggregate morphology on solution conditions. J. Mol. Biol. 322 (2002) 383-393
36. Goormaghtigh E., Cabiaux V., and Ruysschaert J.M. Secondary structure and dosage of soluble and membrane proteins by attenuated total reflection Fourier-transform infrared spectroscopy on hydrated films. Eur. J. Biochem. 193 (1990) 409-420
37. Monnet C., Marthiens V., Enslen H., Frobert Y., Sobel A., and Máege R.M. Heterogeneity and regulation of cellular prion protein glycoforms in neuronal cell lines. Eur. J. Neurosci. 18 (2003) 542-548
38. Jackson M., and Mantsch H.H. Beware of proteins in DMSO. Biochim. Biophys. Acta 1078 (1991) 231-235
39. Barth A. The infrared absorption of amino acid side chains. Prog. Biophys. Mol. Biol. 74 (2000) 141-173
40. Bocharova O.V., Breydo L., Parfenov A.S., Salnikov V.V., and Baskakov I.V. In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrP(Sc). J. Mol. Biol. 346 (2005) 645-659
41. Lashuel H.A., Petre B.M., Wall J., Simon M., Nowak R.J., Walz T., and Lansbury Jr. P.T. Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J. Mol. Biol. 322 (2002) 1089-1102
42. Tattum M.H., Cohen-Krausz S., Khalili-Shirazi A., Jackson G.S., Orlova E.V., Collinge J., Clarke A.R., and Saibil H.R. Elongated oligomers assemble into mammalian PrP amyloid fibrils. J. Mol. Biol. 357 (2006) 975-985
43. Backus K.H., Pflimlin P., and Trube G. Action of diazepam on the voltage-dependent Na+ current. Comparison with the effects of phenytoin, carbamazepine, lidocaine and flumazenil. Brain Res. 548 (1991) 41-49
44. Costantin J.L., and Charles A.C. Spontaneous action potentials initiate rhythmic intercellular calcium waves in immortalized hypothalamic (GT1-1) neurons. J. Neurophysiol. 82 (1999) 429-435
45. James T.L., Liu H., Ulyanov N.B., Farr-Jones S., Zhang H., Donne D.G., Kaneko K., Groth D., Mehlhorn I., Prusiner S.B., and Cohen F.E. Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10086-10091
46. Abe K., and Saito H. Amyloid beta protein inhibits cellular MTT reduction not by suppression of mitochondrial succinate dehydrogenase but by acceleration of MTT formazan exocytosis in cultured rat cortical astrocytes. Neurosci. Res. 31 (1998) 295-305
47. Brown D.R., Schmidt B., and Kretzschmar H.A. Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 380 (1996) 345-347
48. Ettaiche M., Pichot R., Vincent J.P., and Chabry J. In vivo cytotoxicity of the prion protein fragment 106-126. J. Biol. Chem. 275 (2000) 36487-36490
49. Thellung S., Florio T., Villa V., Corsaro A., Arena S., Amico C., Robello M., Salmona M., Forloni G., Bugiani O., Tagliavini F., and Schettini G. Apoptotic cell death and impairment of L-type voltage-sensitive calcium channel activity in rat cerebellar granule cells treated with the prion protein fragment 106-126. Neurobiol. Dis. 7 (2000) 299-309
50. Walsh D.M., Lomakin A., Benedek G.B., Condron M.M., and Teplow D.B. Amyloid beta-protein fibrillogenesis. Detection of a protofibrillar intermediate. J. Biol. Chem. 272 (1997) 22364-22372
51. Fournier J.G., Escaig-Haye F., and Grigoriev V. Ultrastructural localization of prion proteins: physiological and pathological implications. Microsc. Res. Tech. 50 (2000) 76-88
52. Pan K.M., Baldwin M., Nguyen J., Gasset M., Serban A., Groth D., Mehlhorn I., Huang Z., Fletterick R.J., Cohen F.E., et al. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 10962-10966
53. Gonzalez L., Martin S., and Jeffrey M. Distinct profiles of PrP(d) immunoreactivity in the brain of scrapie- and BSE-infected sheep: implications for differential cell targeting and PrP processing. J. Gen. Virol. 84 (2003) 1339-1350
54. Demuro A., Mina E., Kayed R., Milton S.C., Parker I., and Glabe C.G. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 280 (2005) 17294-17300
55. Kazlauskaite J., Sanghera N., Sylvester I., Venien-Bryan C., and Pinheiro T.J. Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization. Biochemistry 42 (2003) 3295-3304