Amyloid-associated activity contributes to the severity and toxicity of a prion phenotype

Nature Communications

Volumn 5, Issue , 2014, Pages

  Pezza, John A ^a,c   Villali, Janice ^a,d   Sindi, Suzanne S ^b   Serio, Tricia R ^a,e  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NEW ENGLAND BIOLABS   (United States)

^d BRANDEIS UNIVERSITY   (United States)

^e University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; PRION PROTEIN; PRION; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE OVEREXPRESSION; NONHUMAN; PHENOTYPE; PROTEIN CONFORMATION; RIBOSOME; SACCHAROMYCES CEREVISIAE; STOP CODON; CHEMISTRY; METABOLISM; PRION; PROTEIN FOLDING;

AMYLOID; PRIONS; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84904497710     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5384     Document Type: Article

References (68)

1. Tuite, M. F. & Serio, T. R. The prion hypothesis: From biological anomaly to basic regulatory mechanism. Nat. Rev. Mol. Cell Biol. 11, 823-833 (2010).
2. Chiti, F. & Dobson, C. M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366 (2006).
3. Fowler, D. M., Koulov, A. V., Balch, W. E. & Kelly, J. W. Functional amyloidfrom bacteria to humans. Trends Biochem. Sci. 32, 217-224 (2007).
4. Blanco, L. P., Evans, M. L., Smith, D. R., Badtke, M. P. & Chapman, M. R. Diversity, biogenesis and function of microbial amyloids. Trends Microbiol. 20, 66-73 (2012).
5. Si, K., Choi, Y. B., White-Grindley, E., Majumdar, A. & Kandel, E. R. Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 140, 421-435 (2010).
6. Klement, I. A. et al. Ataxin-1 nuclear localization and aggregation: Role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 95, 41-53 (1998).
7. Saudou, F., Finkbeiner, S., Devys, D. & Greenberg, M. E. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95, 55-66 (1998).
8. Nicoll, A. J. & Collinge, J. Preventing prion pathogenicity by targeting the cellular prion protein. Infect. Disord. Drug Targets. 9, 48-57 (2009).
9. Radford, H. E. & Mallucci, G. R. The role of GPI-anchored PrP(C) in mediating the neurotoxic effect of scrapie prions in neurons. Curr. Issues Mol. Biol. 12, 119-128 (2009).
10. Bueler, H. et al. High prion and PrPSc levels but delayed onset of disease in scrapie-inoculated mice heterozygous for a disrupted PrP gene. Mol. Med. 1, 19-30 (1994).
11. Warrick, J. M. et al. Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat. Genet. 23, 425-428 (1999).
12. Kazemi-Esfarjani, P. & Benzer, S. Genetic suppression of polyglutamine toxicity in Drosophila. Science 287, 1837-1840 (2000).
13. Arrasate, M., Mitra, S., Schweitzer, E. S., Segal, M. R. & Finkbeiner, S. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431, 805-810 (2004).
14. Cohen, E., Bieschke, J., Perciavalle, R. M., Kelly, J. W. & Dillin, A. Opposing activities protect against age-onset proteotoxicity. Science 313, 1604-1610 (2006).
15. Collinge, J. & Clarke, A. R. A general model of prion strains and their pathogenicity. Science 318, 930-936 (2007).
16. Cox, B. [PSI], a cytoplasmic suppressor of super-suppression in yeast. Heredity 20, 505-521 (1965).
17. Wickner, R. B. [URE3] as an altered URE2 protein: Evidence for a prion analog in Saccharomyces cerevisiae. Science 264, 566-569 (1994).
18. Chernoff, Y. O., Lindquist, S. L., Ono, B., Inge-Vechtomov, S. G. & Liebman, S. W. Role of the chaperone protein Hsp104 in propagation of the yeast prionlike factor [PSI]. Science 268, 880-884 (1995).
19. Patino, M. M., Liu, J. J., Glover, J. R. & Lindquist, S. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273, 622-626 (1996).
20. Paushkin, S. V., Kushnirov, V. V., Smirnov, V. N. & Ter-Avanesyan, M. D. Propagation of the yeast prion-like [PSI] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J. 15, 3127-3134 (1996).
21. Tanaka, M., Collins, S. R., Toyama, B. H. & Weissman, J. S. The physical basis of how prion conformations determine strain phenotypes. Nature 442, 585-589 (2006).
22. Zhou, P. et al. The yeast non-Mendelian factor [ETA] is a variant of [PSI], a prion-like form of release factor eRF3. EMBO J. 18, 1182-1191 (1999).
23. Serio, T. R. & Lindquist, S. L. [PSI]: an epigenetic modulator of translation termination efficiency. Annu. Rev. Cell Dev. Biol. 15, 661-703 (1999).
24. Baxa, U., Keller, P. W., Cheng, N., Wall, J. S. & Steven, A. C. In Sup35p filaments (the [PSI] prion), the globular C-terminal domains are widely offset from the amyloid fibril backbone. Mol. Microbiol. 79, 523-532 (2011).
25. Glover, J. R. et al. Self-seeded fibers formed by Sup35, the protein determinant of [PSI], a heritable prion-like factor of S. cerevisiae. Cell 89, 811-819 (1997).
26. Krzewska, J., Tanaka, M., Burston, S. G. & Melki, R. Biochemical and functional analysis of the assembly of full-length Sup35p and its prion-forming domain. J. Biol. Chem. 282, 1679-1686 (2007).
27. Dever, T. E. & Green, R. The elongation, termination, and recycling phases of translation in eukaryotes. Cold Spring Harb. Perspect. Biol. 4, a013706 (2012).
28. Czaplinski, K. et al. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12, 1665-1677 (1998).
29. Paushkin, S. V., Kushnirov, V. V., Smirnov, V. N. & Ter-Avanesyan, M. D. Interaction between yeast Sup45p (eRF1) and Sup35p (eRF3) polypeptide chain release factors: implications for prion-dependent regulation. Mol. Cell Biol. 17, 2798-2805 (1997).
30. Eaglestone, S. S., Cox, B. S. & Tuite, M. F. Translation termination efficiency can be regulated in Saccharomyces cerevisiae by environmental stress through a prion-mediated mechanism. EMBO J. 18, 1974-1981 (1999).
31. Vishveshwara, N., Bradley, M. E. & Liebman, S. W. Sequestration of essential proteins causes prion associated toxicity in yeast. Mol. Microbiol. 73, 1101-1114 (2009).
32. Ter-Avanesyan, M. D. et al. Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two non-overlapping functional regions in the encoded protein. Mol. Microbiol. 7, 683-692 (1993).
33. Didichenko, S. A., Ter-Avanesyan, M. D. & Smirnov, V. N. Ribosome-bound EF-1 alpha-like protein of yeast Saccharomyces cerevisiae. Eur. J. Biochem. 198, 705-711 (1991).
34. Wang, M. et al. PaxDb, a database of protein abundance averages across all three domains of life. Mol. Cell Proteomics. 11, 492-500 (2012).
35. Satpute-Krishnan, P. & Serio, T. R. Prion protein remodelling confers an immediate phenotypic switch. Nature 437, 262-265 (2005).
36. Kawai-Noma, S., Pack, C. G., Tsuji, T., Kinjo, M. & Taguchi, H. Single mother-daughter pair analysis to clarify the diffusion properties of yeast prion Sup35 in guanidine-HCl-treated [PSI] cells. Genes Cells 14, 1045-1054 (2009).
37. Satpute-Krishnan, P., Langseth, S. X. & Serio, T. R. Hsp104-dependent remodeling of prion complexes mediates protein-only inheritance. PLoS Biol. 5, e24 (2007).
38. Jung, G., Jones, G. & Masison, D. C. Amino acid residue 184 of yeast Hsp104 chaperone is critical for prion-curing by guanidine, prion propagation, and thermotolerance. Proc. Natl Acad. Sci. USA 99, 9936-9941 (2002).
39. McGlinchey, R. P., Kryndushkin, D. & Wickner, R. B. Suicidal [PSI] is a lethal yeast prion. Proc. Natl Acad. Sci. USA 108, 5337-5341 (2011).
40. Halfmann, R., Alberti, S. & Lindquist, S. Prions, protein homeostasis, and phenotypic diversity. Trends Cell. Biol. 20, 125-133 (2010).
41. Chernoff, Y. O., Derkach, I. L. & Inge-Vechtomov, S. G. Multicopy SUP35 gene induces de-novo appearance of psi-like factors in the yeast Saccharomyces cerevisiae. Curr. Genet. 24, 268-270 (1993).
42. Chernoff, Y. O. et al. Dosage-dependent translational suppression in yeast Saccharomyces cerevisiae. Yeast 8, 489-499 (1992).
43. Dagkesamanskaya, A. R. & Ter-Avanesyan, M. D. Interaction of the yeast omnipotent suppressors SUP1(SUP45) and SUP2(SUP35) with non-mendelian factors. Genetics 128, 513-520 (1991).
44. Derdowski, A., Sindi, S. S., Klaips, C. L., DiSalvo, S. & Serio, T. R. A size threshold limits prion transmission and establishes phenotypic diversity. Science 330, 680-683 (2010).
45. Kryndushkin, D. S., Alexandrov, I. M., Ter-Avanesyan, M. D. & Kushnirov, V. V. Yeast [PSI] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J. Biol. Chem. 278, 49636-49643 (2003).
46. Derkatch, I. L., Chernoff, Y. O., Kushnirov, V. V., Inge-Vechtomov, S. G. & Liebman, S. W. Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 144, 1375-1386 (1996).
47. Holmes, W. M., Manakee, B., Gutenkunst, R. & Serio, T. R. Loss of N-terminal acetylation creates a unique phenotype by modulating global protein folding. Nat. Commun. 5, 4383 (2014).
48. Pezza, J. A. et al. The NatA acetyltransferase couples Sup35 prion complexes to the [PSI] phenotype. Mol. Biol. Cell 20, 1068-1080 (2009).
49. Baxa, U., Speransky, V., Steven, A. C. & Wickner, R. B. Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein. Proc. Natl Acad. Sci. USA 99, 5253-5260 (2002).
50. Bai, M., Zhou, J. M. & Perrett, S. The yeast prion protein Ure2 shows glutathione peroxidase activity in both native and fibrillar forms. J. Biol. Chem. 279, 50025-50030 (2004).
51. Serio, T. R. et al. Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289, 1317-1321 (2000).
52. Gokhale, K. C., Newnam, G. P., Sherman, M. Y. & Chernoff, Y. O. Modulation of prion-dependent polyglutamine aggregation and toxicity by chaperone proteins in the yeast model. J. Biol. Chem. 280, 22809-22818 (2005).
53. Caughey, B. & Lansbury, P. T. Protofibrils, pores, fibrils, and neurodegeneration: Separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298 (2003).
54. Douglas, P. M. et al. Chaperone-dependent amyloid assembly protects cells from prion toxicity. Proc. Natl Acad. Sci. USA 105, 7206-7211 (2008).
55. Urbanc, B. et al. Neurotoxic effects of thioflavin S-positive amyloid deposits in transgenic mice and Alzheimer's disease. Proc. Natl Acad. Sci. USA 99, 13990-13995 (2002).
56. Williams, A. J. & Paulson, H. L. Polyglutamine neurodegeneration: Protein misfolding revisited. Trends Neurosci. 31, 521-528 (2008).
57. Plakoutsi, G. et al. Evidence for a mechanism of amyloid formation involving molecular reorganisation within native-like precursor aggregates. J. Mol. Biol. 351, 910-922 (2005).
58. Chien, P., Weissman, J. S. & DePace, A. H. Emerging principles of conformation-based prion inheritance. Annu. Rev. Biochem. 73, 617-656 (2004).
59. Frost, B. & Diamond, M. I. Prion-like mechanisms in neurodegenerative diseases. Nat. Rev. Neurosci. 11, 155-159 (2010).
60. Silveira, J. R. et al. The most infectious prion protein particles. Nature 437, 257-261 (2005).
61. Caughey, B. Interactions between prion protein isoforms: the kiss of death? Trends Biochem. Sci. 26, 235-242 (2001).
62. DePace, A. H., Santoso, A., Hillner, P. & Weissman, J. S. A critical role for amino-terminal glutamine/asparagine repeats in the formation and propagation of a yeast prion. Cell 93, 1241-1252 (1998).
63. Sikorski, R. S. & Hieter, P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27 (1989).
64. Longtine, M. S. et al. Additional modules for versatile and economical PCRbased gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961 (1998).
65. Belli, G., Gari, E., Aldea, M. & Herrero, E. Functional analysis of yeast essential genes using a promoter-substitution cassette and the tetracycline-regulatable dual expression system. Yeast 14, 1127-1138 (1998).
66. DiSalvo, S., Derdowski, A., Pezza, J. A. & Serio, T. R. Dominant prion mutants induce curing through pathways that promote chaperone-mediated disaggregation. Nat. Struct. Mol. Biol. 18, 486-492 (2011).
67. Bagriantsev, S. N., Gracheva, E. O., Richmond, J. E. & Liebman, S. W. Variantspecific [PSI] infection is transmitted by Sup35 polymers within [PSI] aggregates with heterogeneous protein composition. Mol. Biol. Cell (2008).
68. Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Interference: A Practical Information-Theoretic Approach (Springer-Verlag, 2002).