Structural Characterization of the Fibrillar Form of the Yeast Saccharomyces cerevisiae Prion Ure2p

Biochemistry

Volumn 43, Issue 17, 2004, Pages 5022-5032

  Bousset, Luc ^a,c   Redeker, Virginie ^a   Decottignies, Paulette ^b   Dubois, Steven ^a   Le Maréchal, Pierre ^b   Melki, Ronald ^a  

^a CNRS   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ASSAYS; BIREFRINGENCE; LIGHT POLARIZATION; MASS SPECTROMETRY; PROTEINS; SEDIMENTATION; YEAST;

DOMAINS PROTRUDE; INTRAMOLECULAR INTERACTION; MICROSEQUENCING; PROTEOLYSIS;

BIOCHEMISTRY;

FUNGAL PROTEIN; PRION PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; BIREFRINGENCE; BLOTTING, WESTERN; CHYMOTRYPSIN; COLORING AGENTS; CONGO RED; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; FACTOR XA; HYDROLYSIS; KINETICS; MASS SPECTROMETRY; PRIONS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, PROTEIN; SOLUBILITY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRYPSIN; VARIATION (GENETICS);

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 2142762962     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049828e     Document Type: Article

References (48)

1. Prusiner, S. B. (1998) Prions, Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383.
2. Wickner, R. B. (1994) [URE3] as an altered URE2 protein: evidence for a prion analogue in Saccharomyces cerevisiae, Science 264, 566-569.
3. Coustou, V., Deleu, C., Saupe, S., and Begueret, J. (1997) The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog, Proc. Natl. Acad. Sci. U.S.A. 94, 9773-9778.
4. Cohen, F. E., Pan, K. M., Huang, Z., Baldwin, M., Fletterick, R. J., and Prusiner, S. B. (1994) Structural clues to prion replication, Science 264, 530-531.
5. Sipe, J. D., and Cohen, A. S. (2000) History of amyloid fibril, J. Struct. Biol. 130, 88-98.
6. Koo, E. H., Lansbury, P. T., Jr., and Kelly, J. W. (1999) Amyloid diseases: abnormal protein aggregation in neurodegeneration, Proc. Natl. Acad. Sci. U.S.A. 96, 9989-9990.
7. Taylor, J. P., Hardy, J., and Fischbeck (2002) Toxic proteins in neurodegenerative disease, Science 296, 1991-1995.
8. Lacroute, F. (1971) Non-Mendelian mutation allowing ureidosuccinic acid uptake in yeast, J. Bacteriol. 106, 519-522.
9. Magasanik, B. (1992) in The Molecular and Cellular Biology of the Yeast Saccharomyces cerevisiae (Jones, E. W., Pringle, J. R., and Broach, J. R., Eds.) Vol. 2, pp 283-317, Cold Spring Harbor Laboratory Press, Plainview, NY.
10. Masison, D. C., and Wickner, R. B. (1995) Prion-inducing region of yeast Ure2p and protease resistance of Ure2p in prion-containing cells, Science 270, 93-95.
11. Coschigano, P. W., and Magasanik, B. (1991) The URE2 gene product of Saccharomyces cerevisiae plays an important role in the cellular response to the nitrogen source and has homology to glutathione S-transferases, Mol. Cell. Biol. 11, 822-832.
12. Thual, C., Komar, A. A., Bousset, L., Femandez-Bellot, E., Cullin, C., and Melki, R. (1999) Structural Characterization of Saccharomyces cerevisiae Prion-like Protein Ure2, J. Biol. Chem. 274, 13666-13674.
13. Bousset, L., Belrhali, H., Janin, J., Melki, R., and Morera, S. (2001) Structure of the Globular Region of the Prion Protein Ure2 from the Yeast Saccharomyces cerevisiae, Structure 9, 39-46.
14. Umland, T., Taylor, K. L., Rhee, S., Wickner, R. B., and Davies, D. R. (2001) The crystal structure of the nitrogen regulation fragment of the yeast prion protein Ure2p, Proc. Natl. Acad. Sci. U.S.A. 98, 1459-1464.
15. Masison, D. C., Maddelein, M. L., and Wickner, R. B. (1997) The prion model for [URE3] of yeast: spontaneous generation and requirements for propagation, Proc. Natl. Acad. Sci. U.S.A. 94, 12503-12508.
16. Bousset, L., Thomson, N. H., Radford, S. E., and Melki, R. (2002) The yeast prion Ure2p retains its native alpha-helical conformation upon assembly into protein fibrils in vitro, EMBO J. 21, 2903-2911.
17. Taylor, K. L., Cheng, N., Williams, R. W., Steven, A. C., and Wickner, R. B. (1999) Prion domain initiation of amyloid formation in vitro from native Ure2p, Science 283, 1339-1343.
18. Holmes, K. C., Popp, D., Gebhard, W., and Kabsch, W. (1990) Atomic model of the actin filament, Nature 347, 44-49.
19. Nogales, E., Whittaker, M., Milligan, R. A., and Downing, K. H. (1999) High-resolution model of the microtubule, Cell 96, 79-88.
20. Huntington, J. A., Pannu, N. S., Hazes, B., Read, R. J., Lomas, D. A., and Carrell, R. W. (1999) A 2.6 Å structure of a serpin polymer and implications for conformational disease, J. Mol. Biol. 293, 449-455.
21. Liu, Y., Gotte, G., Libonati, M., and Eisenberg, D. (2001) A domain-swapped RNase A dimer with implications for amyloid formation, Nat. Struct. Biol. 8, 211-214.
22. Bousset, L., Briki, F., Doucet, J., and Melki, R. (2003) The native-like conformation of Ure2p in fibrils assembled under physiologically relevant conditions switches to an amyloid-like conformation upon heat-treatment of the fibrils, J. Struct. Biol. 141, 132-142.
23. Speransky, V. V., Taylor, K. L., Edskes, H. K., Wickner, R. B., and Steven, A. C. (2001) Prion filament networks in [URE3] cells of Saccharomyces cerevisiae, J. Cell Biol. 153, 1327-1336.
24. Baxa, U., Taylor, K. L., Wall, J. S., Simon, M. N., Cheng, N., Wickner, R. B., and Steven, A. C. (2003) Architecture of Ure2p prion filaments: The N-terminal domains form a central core fiber, J. Biol. Chem. 278, 43717-43727.
25. Thual, C., Bousset, L., Komar, A. A., Walter, S., Buchner, J., Cullin, C., and Melki, R. (2001) Stability, Folding, Dimerization, and Assembly Properties of the Yeast Prion Ure2p, Biochemistry 40, 1764-1773.
26. Spudich, J. A., and Watt, S. (1971) The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin, J. Biol. Chem. 246, 4866-4871.
27. Eisenberg, E., and Kielley, W. W. (1974) Troponin-tropomyosin complex. Column chromatographic separation and activity of the three, active troponin components with and without tropomyosin present, J. Biol. Chem. 249, 4742-4748.
28. Melki, R., Fievez, S., and Carlier, M. F. (1996) Continuous monitoring of Pi release following nucleotide hydrolysis in actin or tubulin assembly using 2-amino-6-mercapto-7-methylpurine ribonucleoside and purine-nucleoside phosphorylase as an enzyme-linked assay, Biochemistry 35, 12038-12045.
29. MacLean-Fletcher, S., and Pollard, T. D. (1980) Identification of a factor in conventional muscle actin preparations which inhibits actin filament self-association, Biochem. Biophys. Res. Commun. 96, 18-27.
30. Shelanski, M. L., Gaskin, F., and Cantor, C. R. (1973) Microtubule assembly in the absence of added nucleotides, Proc. Natl. Acad. Sci. U.S.A. 70, 765-768.
31. Weingarten, M. D., Lockwood, A. H., Hwo, S. Y., and Kirschner, M. W. (1975) A protein factor essential for microtubule assembly, Proc. Natl. Acad. Sci. U.S.A. 72, 1858-1862.
32. McParland, V. J., Kad, N. M., Kalverda, A. P., Brown, A., Kirwin-Jones, P., Hunter, M. G., Sunde, M., and Radford, S. E. (2000) Partially unfolded states of b2-microglobulin and amyloid formation in vitro, Biochemistry 39, 8735-8746.
33. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
34. Morrissey, J. H. (1981) Silver stain for proteins in polyacrylamide gels: A modified procedure with enhanced uniform sensitivity, Anal. Biochem. 117, 307-310.
35. Khurana, R., Uversky, V. N., Nielsen, L., and Fink, A. L. (2001) Is Congo red an amyloid-specific dye?, J. Biol. Chem. 276, 22715-22721.
36. Elghetany, M. T., Saleem, A., and Barr, K. (1989) The congo red stain revisited, Ann. Clin. Lab. Sci. 19, 190-195.
37. Zurdo, J., Guijarro, J. I., and Dobson, C. M. (2001) Preparation and characterization of purified amyloid fibrils, J. Am. Chem. Soc. 123, 8141-8142.
38. Sunde, M., Serpell, L. C., Bartlam, M., Fraser, P. E., Pepys, M. B., and Blake, C. C. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction, J. Mol. Biol. 273, 729-739.
39. Perrett, S., Freeman, S. J., Butler, P. J., and Fersht, A. R. (1999) Equilibrium folding properties of the yeast prion protein determinant Ure2, J. Mol. Biol. 290, 331-345.
40. Baxa, U., Speransky, V., Steven, A. C., and Wickner, R. B. (2002) Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein, Proc. Natl. Acad. ScL U.S.A. 99, 5253-5260.
41. Amos, L. A. (1985) Structure of muscle filaments studied by electron microscopy, Annu. Rev. Biophys. Biophys. Chem. 14, 291-313.
42. Van Loock, M. S., Yu, X., Yang, S., Lai, A. L., Low, C., Campbell, M. J., and Egelman, E. H. (2003) ATP-mediated conformational changes in the RecA filament, Structure (Cambridge) 11, 187-196.
43. 2+-induced FtsZ sheets, EMBO J. 18, 2364-2371.
44. Gregoire, C., Marco, S., Thimonier, J., Duplan, L., Laurine, E., Chauvin, J. P., Michel, B., Peyrot, V., and Verdier, J. M. (2001) Three-dimensional structure of the lithostathine protofibril, a protein involved in Alzheimer's disease, EMBO J. 20, 3313-3321.
45. Lomas, D. A., and Carrell, R. W. (2002) Serpinopathies and the conformational dementias, Nat. Rev. Genet. 3, 759-768.
46. Westermark, P., Benson, M. D., Buxbaum, J. N., Cohen, A. S., Frangione, B., Ikeda, S., Masters, C. L., Merlini, G., Saraiva, M. J., and Sipe, J. D. (2002) Amyloid fibril protein nomenclature-2002, Amyloid 9, 197-200.
47. Fernandez-Bellot, E., Guillemet, E., and Cullin, C. (2000) The yeast prion [URE3] can be greatly induced by a functional mutated URE2 allele, EMBO J. 19, 3215-3222.
48. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: multiple sequence alignments in postcript, Bioinformatics 15, 305-308.