Binding of methylene blue to a surface cleft inhibits the oligomerization and fibrillization of prion protein

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 1, 2013, Pages 20-28

  Cavaliere, Paola ^a,b,e   Torrent, Joan ^c   Prigent, Stephanie ^c   Granata, Vincenzo ^b   Pauwels, Kris ^d,f   Pastore, Annalisa ^d   Rezaei, Human ^c   Zagari, Adriana ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^c INRA Institut National de la Recherche Agronomique   (France)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^e INSTITUT PASTEUR   (France)

^f VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

Amyloidogenic protein; Anti prion agent; Neurodegenerative disease; PrP fiber; PrP oligomer

Indexed keywords

METHYLENE BLUE; PRION PROTEIN;

ARTICLE; DEPOLYMERIZATION; ESCHERICHIA COLI; GEL PERMEATION CHROMATOGRAPHY; HUMAN; IN VITRO STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OLIGOMERIZATION; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; HUMANS; KINETICS; METHYLENE BLUE; MICE; MOLECULAR SEQUENCE DATA; PRIONS; PROTEIN CONFORMATION; SHEEP;

MURINAE; OVIS;

EID: 84868537186     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.09.005     Document Type: Article

References (38)

1. DeArmond S.J. Alzheimer's disease and Creutzfeldt-Jakob disease: overlap of pathogenic mechanisms. Curr. Opin. Neurol. 1993, 6:872-881.
2. Prusiner S.B. Shattuck lecture-neurodegenerative diseases and prions. N. Engl. J. Med. 2001, 344:1516-1526.
3. Aguzzi A., Haass C. Games played by rogue proteins in prion disorders and Alzheimer's disease. Science 2003, 302:814-818.
4. Winklhofer K.F., Tatzelt J., Haass C. The two faces of protein misfolding: gain- and loss-offunction in neurodegenerative diseases. EMBO J. 2008, 27:336-349.
5. Prusiner S.B. Prions. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13363-13383.
6. Caughey B., Lansbury P.T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 2003, 26:267-298.
7. Rezaei H. Prion protein oligomerization. Curr. Alzheimer Res. 2008, 5:572-578.
8. Kelly J.W. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr. Opin. Struct. Biol. 1998, 8:101-106.
9. Schirmer R.H., Adler H., Pickhardt M., Mandelkow E. Lest we forget you-methylene blue . .. Neurobiol. Aging 2011, 32:2325.e7-2325.e16.
10. Oz M., Lorke D.E., Petroianu G.A. Methylene blue and Alzheimer's disease. Biochem. Pharmacol. 2009, 78:927-932.
11. O'Leary J.L., Petty J., Harris A.B., Inukai J. Supravital staining of mammalian brain with intraarterial methylene blue followed by pressurized oxygen. Stain Technol. 1968, 43:197-201.
12. Peter C., Hongwan D., Kupfer A., Lauterburg B.H. Pharmacokinetics and organ distribution of intravenous and oral methylene blue. Eur. J. Clin. Pharmacol. 2000, 56:247-250.
13. Necula M., Breydo L., Milton S., Kayed R., van der Veer W.E., Tone P., Glabe C.G. Methylene blue inhibits amyloid Aβ oligomerization by promoting fibrillization. Biochemistry 2007, 46:8850-8860.
14. Taniguchi S., Suzuki N., Masuda M., Hisanaga S., Iwatsubo T., Goedert M., Hasegawa M. Inhibition of heparin-induced tau filament formation by phenothiazines, polyphenols, and porphyrins. J. Biol. Chem. 2005, 280:7614-7623.
15. Wang A.M., Morishima Y., Clapp K.M., Peng H.M., Pratt W.B., Gestwicki J.E., Osawa Y., Lieberman A.P. Inhibition of hsp70 by methylene blue affects signaling protein function and ubiquitination and modulates polyglutamine protein degradation. J. Biol. Chem. 2010, 285:15714-15723.
16. Yamashita M., Nonaka T., Arai T., Kametani F., Buchman V.L., Ninkina N., Bachurin S.O., Akiyama H., Goedert M., Hasegawa M. Methylene blue and dimebon inhibit aggregation of TDP-43 in cellular models. FEBS Lett. 2009, 14:2419-2424.
17. Korth C., May B.C., Cohen F.E., Prusiner S.B. Acridine and phenothiazine derivatives as pharmacotherapeutics for prion disease. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8936-8941.
18. Hornsey V.S., Casey C., McColl K., Young H., Drummond O., McMillan L., Morrison A., Prowse C.V. Characteristics of prion-filtered red cells suspended in pathogen-inactivated plasma (MB treated or solvent-detergent treated) for neonatal exchange transfusion. Vox Sang. 2010, 101:28-34.
19. De Simone A., Zagari A., Derreumauxz P. Structural and hydration properties of the partially unfolded states of the prion protein. Biophys. J. 2007, 93:1284-1292.
20. Rezaei H., Marc D., Choiset Y., Takahashi M., Hui Bon Hoa G., Haertlé T., Grosclaude J., Debey P. High yield purification and physico-chemical properties of full-length recombinant allelic variants of sheep prion protein linked to scrapie susceptibility. Eur. J. Biochem. 2000, 267:2833-2839.
21. Sanchez-Ruiz J.M. Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry. Biophys. J. 1992, 61:921-935.
22. Chakroun N., Prigent S., Dreiss C.A., Noinville S., Chapuis C., Fraternali F., Rezaei H. The oligomerization properties of prion protein are restricted to the H2H3 domain. FASEB J. 2010, 24:1-10.
23. Eghiaian F., Daubenfeld T., Quenet Y., van Audenhaege M., Bouin A.P., van der Rest G., Grosclaude J., Rezaei H. Diversity in prion protein oligomerization pathways results from domain expansion as revealed by hydrogen/deuterium exchange and disulfide linkage. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:7414-7419.
24. Prigent S., Rezaei H. PrP assemblies: spotting the responsible regions in prion propagation. Prion 2011, 5:69-75.
25. Rezaei H., Choiset Y., Eghiaian F., Treguer E., Mentre P., Debey P., Grosclaude J., Haertle T. Amyloidogenic unfolding intermediates differentiate sheep prion protein variants. J. Mol. Biol. 2002, 322:799-814.
26. Rezaei H., Eghiaian F., Perez J., Doublet B., Choiset Y., Haertle T., Grosclaude J. Sequential generation of two structurally distinct ovine prion protein soluble oligomers displaying different biochemical reactivities. J. Mol. Biol. 2005, 347:665-679.
27. Kocisko D.A., Baron G.S., Rubenstein R., Chen J., Kuizon S., Caughey B. New inhibitors of scrapie-associated prion protein formation in a library of 2000 drugs and natural products. J. Virol. 2003, 77:10288-10294.
28. Perrier V., Wallace A.C., Kaneko K., Safar J., Prusiner S.B., Cohen F.E. Mimicking dominant negative inhibition of prion replication through structure-based drug design. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:6073-6078.
29. Roberts B.E., Duennwald M.L., Wang H., Chung C., Lopreiato N.P., Sweeny E.A., Knight M.N., Shorter J. A synergistic small-molecule combination directly eradicates diverse prion strain structures. Nat. Chem. Biol. 2009, 5:936-946.
30. Ladiwala A.R., Dordick J.S., Tessier P.M. Aromatic small molecules remodel toxic soluble oligomers of amyloid beta through three independent pathways. J. Biol. Mol. 2011, 286:3209-3218.
31. Wischik C.M., Edwards P.C., Lai R.Y., Roth M., Harrington C.R. Selective inhibition of Alzheimer disease-like tau aggregation by phenothiazines. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11213-11218.
32. Caughey B., Race R.E. Potent inhibition of scrapie-associated PrP accumulation by congo red. J. Neurochem. 1992, 59:768-771.
33. Kuwata K., Nishida N., Matsumoto T., Kamatari Y.O., Hosokawa-Muto J., Kodama K., Nakamura H.K., Kimura K., Kawasaki M., Takakura Y., Shirabe S., Takata J., Kataoka Y., Katamine S. Hot spots in prion protein for pathogenic conversion. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11921-11926.
34. Nicoll A.J., Trevitt C.R., Tattum M.H., Risse E., Quarterman E., Ibarra A.A., Wright C., Jackson G.S., Sessions R.B., Farrow M., Waltho J.P., Clarke A.R., Colling J. Pharmacological chaperone for the structured domain of human prion protein. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17610-17615.
35. Caspi S., Halimi M., Yanai A., Sasson S.B., Taraboulos A., Gabizon R. The anti-prion activity of Congo red. Putative mechanism. J. Biol. Chem. 1998, 273:3484-3489.
36. Lee Y.J., Savtchenko R., Ostapchenko V.G., Makarava N., Baskakov I. Molecular structure of amyloid fibrils controls the relationship between fibrillar size and toxicity. PLoS One 2011, 6:e20244.
37. Stefani M., Dobson C.M. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. (Berl.) 2003, 81:678-699.
38. Legname G., Baskakov I.V., Nguyen H.O., Riesner D., Cohen F.E., DeArmond S.J., Prusiner S.B. Synthetic mammalian prions. Science 2004, 305.