DNA-induced partial unfolding of prion protein leads to its polymerisation to amyloid

Journal of Molecular Biology

Volumn 322, Issue 1, 2002, Pages 153-161

  Nandi, P K ^a   Leclerc, E ^b   Nicole, J C ^c   Takahashi, M ^d  

^a CEMAGREF   (France)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c I N la R A P de la R des M D   (France)

^d INSTITUT CURIE   (France)

Author keywords

Amyloid; Nucleic acid interaction; Polymerisation; Prion protein; Protein conformation

Indexed keywords

AMINO ACID; AMYLOID; CONGO RED; DNA; DYE; NUCLEIC ACID; PRION PROTEIN; RECOMBINANT PROTEIN; THIOFLAVINE;

ALPHA HELIX; ARTICLE; BETA SHEET; BIREFRINGENCE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; DENATURATION; ELECTRON MICROSCOPY; FIBER; FLUORESCENCE; IN VIVO STUDY; INCUBATION TIME; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STRUCTURE;

EID: 0036970469     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)00750-7     Document Type: Article

References (43)

1. Prusiner, S. B. (1998). Prions. Proc. Natl Acad. Sci. USA, 95, 13363-13383.
2. Horwich, A. L. & Weissmann, J. S. (1997). Deadly conformations - protein misfolding in prion disease. Cell, 89, 499-510.
3. Wadsworth, J. D., Jackson, G. S., Hill, A. F. & Collinge, J. (1999). Molecular biology of prion propagation. Curr. Opin. Genet. Dev. 9, 338-345.
4. Lansbury, P. T. & Caughey, B. (1996). The double life of prion protein. Curr. Biol. 6, 914-916.
5. Harper, J. D. & Lansbury, P. T., Jr (1997). Model of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequence of the time dependent solubility of amyloid proteins. Annu. Rev. Biochem. 66, 385-407.
6. Goldberg, M. S. & Lansbury, P. T., Jr (2000). Is there a cause-and-effect relationship between a-synuclein fibrillization and Parkinson's disease? Nature Cell Biol. 2, 115-119.
7. Nandi, P. K. & Leclerc, E. (1999). Polymerization of murine recombinant prion protein in nucleic acid solution. Arch. Virol. 144, 1751-1763.
8. Nandi, P. K. & Sizaret, P.-Y. (2001). Murine recombinant prion protein induces ordered aggregation of linear nucleic acids to condensed globular structure. Arch. Virol. 146, 327-345.
9. Sikorav, J. L., Church, G. M. (1991). Complementary recognotion in condensed DNA: accelerated DNA renaturation. J. Mol. Biol. 222, 1085-1089.
10. Le Cam, E., Coulaud, D., Delain, E., Petitjean, P., Roques, B. P., Gerard, D. et al. (1998). Properties and growth mechanism of the ordered aggregation of a model RNA by the HIV-1 nucleocapsid protein: an electron microscopy investigation. Biopolymers, 45, 217-229.
11. Gabuus, C., Auxilien, S., Péchoux, C., Dormont, D., Swietnicki, W., Morillas, M. et al. (2001). The prion protein has DNA strand transfer properties similar to retroviral nuclecapsid protein. J. Mol. Biol. 307, 1011-1021.
12. Derrington, E., Gabus, C., Leblanc, P., Chnaidermann, J., Grave, L., Dormont, D. et al. (2002). PrPC has nucleic acid chaperoning properties similar to the nucleocapsid protein of HIV-1. C. R. Acad. Sci. III, 325, 17-23.
13. Corderio, Y., Machado, F., Neto, L. J., Juliano, M. A., Brentani, R. R., Foguel, D. & Silva, J. L. (2001). DNA converts cellular prion protein into the β-sheet conformation and inhibits prion peptide aggregation. J. Biol. Chem. 276, 49400-49409.
14. Prusiner, S. B., Scott, M. R., DeArmond, S. J. & Cohen, F. E. (1998). Prion protein biology. Cell, 93, 337-348.
15. Riek, R., Hornemann, S., Wider, G., Glockshuber, R. & Wuthrich, K. (1997). NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Letters, 413, 282-288.
16. Reik, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R. & Wuthrich, K. (1996). NMR structure of the mouse prion protein domain PrP(121-321). Nature, 382, 180-182.
17. Hornemann, S. & Glockshuber, R. (1998). A scrapie-like unfolded intermediate of the prion protein domain PrP(121-231) induced by acid pH. Proc. Natl Acad. Sci. USA, 95, 6010-6014.
18. Liberski, P. P., Brown, P., Xiao, S.-Y. & Gajdusek, D. C. (1991). The ultrastructural diversity of scrapie-associated fibrils isolated from experimental scrapie and Creutzfeldt-Jakob disease. J. Comp. Pathol. 105, 377-386.
19. Villemeur, T., Fournier, J. G., Robain, O., Escaig-Haye, F. & Brown, P. (1995). Electronmicroscopic detection of prion protein positive fibers in brain from iatrogenic Creutzfeldt-Jakob disease. Lancet, 345, 861-862.
20. Morozova-Roche, L. A., Zurdo, J., Spencer, A., Noppe, W., Receveur, V., Archer, D. V. et al. (2000). Amyloid fibril formation and seeding by wild-type human lysozyme and its disease related mutants. J. Struct. Biol. 130, 339-351.
21. Goldfarb, L. G., Brown, P., Haltia, M., Ghiso, J., Frangione, B., Gajdusek, D. C. et al. (1993). Synthetic peptides corresponding to different mutated regions of the amyloid gene in familial Creutzfeldt-Jakob disease show enhanced in vitro formation of morphologically different amyloid fibrils. Proc. Natl Acad. Sci. USA, 90, 4451-4454.
22. Safar, J., Roller, P. P., Gajdusek, D. C. & Gibbs, C. J., Jr (1993). Conformational transitions, dissociation, and unfolding of scrapie amyloid (prion) protein. J. Biol. Chem. 268, 20276-20284.
23. Wildegger, G., Liemann, S. & Glockshuber, R. (1999). Extremely rapid folding of the C-terminal domain of the prion protein without kinetic intermediates. Nature Struct. Biol. 6, 550-553.
24. Nandi, P. K. (1998). Evidence of molten globule like structure(s) of interferon gamma in acidic and sodium perchlorate solutions. Int. J. Biol. Macromol. 22, 23-31.
25. Nandi, P. K. (1998). Polymerization of human prion peptide HuPrP 106-126 to amyloid in nucleic acid solution. Arch. Virol. 143, 1251-1263.
26. Safar, J., Roller, P. P., Gajdusek, D. C. & Gibbs, C. J. (1994). Scrapie amyloid (Prion) protein has the conformational characteristics of an aggregated molten globule folding intermediate. Biochemistry, 33, 8375-8383.
27. Spolar, R. S. & Record, R. T., Jr (1994). Coupling of local folding to site-specific binding of proteins to DNA. Science, 263, 777-784.
28. Chang, K.-Y. & Varani, G. (1997). Nucleic acid structure and recognition. Nature Struct. Biol., 854-858.
29. Frankel, A. D. & Smith, C. A. (1998). Induced folding in RNA-protein recognition: more than a simple molecular hand shake. Cell, 92, 149-151.
30. Morrissey, M. P. & Shakhnovich, E. I. (1999). Evidence for the role of PrP(C) helix 1 in the hydrophilic seeding of prion aggregates. Proc. Natl Acad. Sci. USA, 96, 11293-11298.
31. Ciubotaru, M., Bright, F. V., Ingersoll, C. M. & Koudelka, G. B. (1999). DNA-induced conformational changes in bacteriophage 434 repressor. J. Mol. Biol. 294, 859-873.
32. Morillas, M., Swietnicki, W., Gambetti, P. & Surewicz, W. K. (1999). Membrane environment alters the conformational structure of the recombinant human prion protein. J. Biol. Chem. 274, 36859-36865.
33. Chiti, F., Webster, P., Taddei, N., Clark, A., Stefani, M., Ramponi, G. & Dobson, C. M. (1999). Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc. Natl Acad. Sci. USA, 96, 3590-3594.
34. Jarret, J. T. & Lansbury, P. T., Jr (1993). Seeding one-dimensional crystallization of amyloid: a pathogenic mechanism mechanism in Alzheimer's disease and scrapie? Cell, 73, 1055-1058.
35. Weissmann, C. (1999). Molecular genetics of transmissible spongifirm Encephalopathies. J. Biol. Chem. 274, 3-6.
36. Booth, D. R., Sunde, M., Bellotti, V., Robinson, C. V., Hutchinson, W. L., Fraser, P. E. et al. (1997). Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillo-genesis. Nature, 385, 787-793.
37. Newman, M., Strzelecka, T., Donner, L. F., Schildkraut, I. & Aggarwal, A. K. (1995). Structure of Bam HI endonuclease bound to DNA: partial folding and unfolding on DNA binding. Science, 269, 656-663.
38. Hegde, R. S., Mastrianni, J. A., Scott, M. R., DeFea, K., Trembly, P., Torchia, M. et al. (1998). A transmembrane form of prion protein in neurodegenerative disease. Science, 279, 827-834.
39. Muro-Pasteur, A. M., Ostrovsky, P. & Mayloi, S. J. (1997). Regulation of gene expression by repressor localization; biochemical evidence that membrane and DNA binding by putA protein are mutually exclusive. J. Bacteriol. 179, 2788-2791.
40. Jeffery, C. J. (1999). Moon lighting proteins. Trends Biochem. Sci. 27, 8-11.
41. Weissmann, C. (1991). A unified theory of prion propagation. Nature, 352, 679-683.
42. Lansbury, P. T., Jr (1999). Evolution of amyloid: what normal protein folding may tell us about fibrillogenesis and disease. Proc. Natl Acad. Sci. USA, 96, 3334-3342.
43. Carra, J. H. & Privalov, P. L. (1997). Energetics of folding and DNA binding of the MAT alpha 2 homeodomain. Biochemistry, 36, 526-535.