Nonpolar substitution at the C-terminus of the prion protein, a mimic of the glycosylphosphatidylinositol anchor, partially impairs amyloid fibril formation

Biochemistry

Volumn 46, Issue 3, 2007, Pages 852-861

  Breydo, Leonid ^a   Sun, Ying ^a   Makarava, Natallia ^a   Lee, Cheng I ^a   Novitskaia, Vera ^a,c   Bocharova, Olga ^a,d   Kao, Joseph P Y ^a,b   Baskakov, Ilia V ^a,b  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; CONFORMATIONS; MOLECULAR DYNAMICS; MOLECULAR STRUCTURE; SUBSTITUTION REACTIONS;

AMYLOID CONFORMATION; AMYLOID FIBRIL FORMATION; FIBRILLAR STRUCTURE; NONPOLAR SUBSTITUTION;

PROTEINS;

AMYLOID; GLYCOSYLPHOSPHATIDYLINOSITOL; PRION PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; HUMAN; HUMAN CELL; MEMBRANE BINDING; MYRISTYLATION; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROCESSING;

AMYLOID; BIOMIMETICS; CELL MEMBRANE; EPITOPES; ETHYLMALEIMIDE; GLUTATHIONE; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; HYDROPHOBICITY; MYRISTIC ACID; PRIONS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 33846338233     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061923v     Document Type: Article

References (37)

1. Carrell, R. W., and Lomas, D. A. (1997) Conformational disease, Lancet 350, 134-138.
2. Prusiner, S. B. (2001) Shattuck Lecture-Neurodegenerative diseases and prions, N. Engl. J. Med. 344, 1516-1526.
3. Endo, T., Groth, D., Prusiner, S. B., and Kobata, A. (1989) Diversity of oligosaccharide structures linked to asparagines of the scrapie prion protein, Biochemistry 28, 8380-8388.
4. Stahl, N., Borchelt, D. R., Hsiao, K., and Prusiner, S. B. (1987) Scrapie prion protein contains a phosphatidylinositol glycolipid, Cell 51, 229-240.
5. Prusiner, S. B., McKinley, M. P., Bowman, K. A., Bolton, D. C., Bendheim, P. E., Groth, D. F., and Glenner, G. G. (1983) Scrapie prions aggregate to form amyloid-like birefringent rods, Cell 35, 349-358.
6. Somerville, R. A., Ritchie, L. A., and Gibson, P. H. (1989) Structural and biochemical evidence that scrapie-associated fibrils assemble in vivo, J. Gen. Virol. 70, 25-35.
7. Liberski, P. P., Brown, P., Xiao, S.-Y., and 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.
8. Lewis, P. A., Properzi, F., Prodromidou, K., Clarke, A. R., Collinge, J., and Jackson, G. S. (2006) Removal of the glycosylphosphatidylinositol anchor from PrPSc by cathepsin-D does not reduce prion infectivity, Biochem. J. 395, 443-448.
9. Legname, G., Baskakov, I. V., Nguyen, H.-O. B., Riesner, D., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (2004) Synthetic mammalian prions, Science 305, 673-676.
10. Baskakov, I. V., Legname, G., Baldwin, M. A., Prusiner, S. B., and Cohen, F. E. (2002) Pathway complexity of prion protein assembly into amyloid, J. Biol. Chem. 277, 21140-21148.
11. Bocharova, O. V., Breydo, L., Parfenov, A. S., Salnikov, V. V., and Baskakov, I. V. (2005) In vitro conversion of full length mammalian prion protein produces amyloid form with physical property of PrPSc, J. Mol. Biol. 346, 645-659.
12. Breydo, L., Bocharova, O. V., Makarava, N., Salnikov, V. V., Anderson, M., and Baskakov, I. V. (2005) Methionine oxidation interferes with conversion of the prion protein into the fibrillar proteinase K-resistant conformation, Biochemistry 44, 15534-15543.
13. Breydo, L., Bocharova, O. V., and Baskakov, I. V. (2005) Semiautomated cell-free conversion of prion protein: Applications for high-throughput screening of potential antiprion drugs, Anal. Biochem. 339, 165-173.
14. Bocharova, O. V., Makarava, N., Breydo, L., Anderson, M., Salnikov, V. V., and Baskakov, I. V. (2006) Annealing PrP amyloid firbils at high temperature results in extension of a proteinase K resistant core, J. Biol. Chem. 281, 2373-2379.
15. Novitskaya, V., Makarava, N., Bellon, A., Bocharova, O. V., Bronstein, I. B., Williamson, R. A., and Baskakov, I. V. (2006) Probing the conformation of the prion protein within a single amyloid fibril using a novel immunoconformational assay, J. Biol. Chem. 281, 15536-15545.
16. Sc, Protein Sci. 14, 1222-1232.
17. Scozzafava, A., Casini, A., and Supuran, C. T. (2002) Targeting cysteine residues of biomolecules: new approaches for the design of antiviral and anticancer drugs, Curr. Med. Chem. 9, 1167-1185.
18. Carne, A. F. (2003) Chemical modifications of proteins as an aid to sequence analysis, Methods Mol. Biol. 211, 333-354.
19. Borchelt, D. R., Rogers, M., Stahl, N., Telling, G., and Prusiner, S. B. (1993) Release of the cellular prion protein from cultured cells after loss of its glycoinositol phospholipid anchor, Glycobiology 3, 319-329.
20. Stahl, N., Borchelt, D. R., and Prusiner, S. B. (1990) Differential release of cellular and scrapie prion proteins from cellular membranes by phosphatidylinositol-specific phospholipase C, Biochemistry 29, 5405-5412.
21. Caughey, B., Neary, K., Butler, R., Ernst, D., Perry, L., Chesebro, B., and Race, R. E. (1990) Normal and scrapie-associated forms of prion protein differ in their sensitivities to phospholipase and proteases in intact neuroblastoma cells, J. Virol. 64, 1093-1101.
22. Peitzsch, R. M., and McLaughlin, S. (1993) Binding of acylated peptides and fatty acids to phospholipid vesicles pertinence to myristoylated proteins, Biochemistry 32, 10436-10443.
23. Eberl, H., Tittman, P., and Glockshuber, R. (2004) Characterization of recombinant, membrane-attached full-length prion protein, J. Biol. Chem. 279, 25058-25065.
24. Hicks, M. R., Gill, A. C., Bath, I. K., Rullay, A. K., Sylvester, I. D., Crout, D. H., and Pinheiro, T. J. (2006) Synthesis and structural characterization of a mimetic membrane-anchored prion protein, FEBS J. 273, 1285-1299.
25. Anderson, M., Bocharova, O. V., Makarava, N., Breydo, L., Salnikov, V. V., and Baskakov, I. V. (2006) Polymorphism and ultrastructural organization of prion protein amyloid fibrils: An insight from high resolution atomic force microscopy, J. Mol. Biol. 358, 580-596.
26. Hayashi, N., Nakagawa, C., Ito, Y., Takasaki, A., Jinbo, Y., Yamakava, Y., Titani, K., Hashimoto, K., Izumi, Y., and Matsushima, N. (2004) Myristoylation-regulated direct interaction between calcium-bound calmodulin and N-terminal region of pp60v-src, J. Mol. Biol. 338, 169-180.
27. Chow, M., Newman, J. F. E., Filman, D., Hogle, J. M., Rowlands, D. J., and Brown, F. (1987) Myristylation of picornavirus capsid protein VP4 and its structural significance, Nature 327, 482-486.
28. Vey, M., Pilkuhn, S., Wille, H., Nixon, R., DeArmond, S. J., Smart, E. J., Anderson, R. G., Taraboulos, A., and Prusiner, S. B. (1996) Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains, Proc. Natl. Acad. Sci. U.S.A. 93, 14945-14949.
29. Taraboulos, A., Scott, M., Semenov, A., Avrahami, D., Laszlo, L., and Prusiner, S. B. (1995) Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibits formation of the scrapie isoform, J. Cell Biol. 129, 121-132.
30. Naslavsky, N., Stein, R., Yanai, A., Friedlander, G., and Taraboulos, A. (1997) Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform, J. Biol. Chem. 272, 6324-6331.
31. Baron, G. S., Wehrly, K., Dorward, D. W., Chesebro, B., and Caughey, B. (2002) Conversion of raf associated prion protein to the protease-resistant state requires insertion of PrP-res(PrP(Sc)) into contiguous membrane, EMBO J. 21, 1031-1040.
32. Harris, D. A. (1999) Cellular biology of prion diseases, Clin. Microbiol. Rev. 12, 429-444.
33. Ball, H. L., King, D. S., Cohen, F. E., Prusiner, S. B., and Baldwin, M. A. (2001) Engineering the prion protein using chemical synthesis, J. Pept. Res. 58, 357-374.
34. Baron, G. S., and Caughey, B. (2003) Effect of glycosylphosphatidylinositol anchor-dependent and -independent prion protein associated with model raft membranes on conversion to the protease-resistant isoform, J. Biol. Chem. 278, 14883-14892.
35. Leffer, K. -W., Wille, H., Stohr, J., Junger, E., Prusiner, S.B., and Riesner, D. (2005) Assembly of natural and recombinant prion protein into fibrils, Biol. Chem. 386, 569-580.
36. Makarava, N., Bocharova, O. V., Salnikov, V. V., Breydo, L., Anderson, M., and Baskakov, I. V. (2006) Dichotomous versus palm-type mechanisms of lateral assembly of amyloid fibrils, Protein Sci. 15, 1334-1341.
37. Chesebro, B., Trifilo, M., Race, M., Meade-White, K., Teng, C., LaCasse, R., Raymond, L., Favara, C., Baron, G., Priola, S., Caughey, B., Masliah, E., and Oldstone, M. (2005) Anchorless prion protein result in infectious amyloid disease without clinical scrapie, Science 308, 1435-1439.