Prion-promoted phosphorylation of heterologous amyloid is coupled with ubiquitin-proteasome system inhibition and toxicity

Molecular Microbiology

Volumn 93, Issue 5, 2014, Pages 1043-1056

  Yang, Zi ^a   Stone, David E ^a   Liebman, Susan W ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF NEVADA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; CHAPERONE; PEPTIDES AND PROTEINS; PRION PROTEIN; PROTEASOME; PROTEIN; PROTEIN PIN4C; PROTEIN RNQ1; PROTEIN SIS1; UBIQUITIN; UNCLASSIFIED DRUG; PIN4 PROTEIN, S CEREVISIAE; PRION; RAD52 PROTEIN; RNQ1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SUP35 PROTEIN, S CEREVISIAE; TRANSLATION TERMINATION FACTOR;

ARTICLE; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; G2 PHASE CELL CYCLE CHECKPOINT; NONHUMAN; PRION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN UNFOLDING; YEAST; ENZYMOLOGY; GENETICS; METABOLISM; SACCHAROMYCES CEREVISIAE;

AMYLOID; PEPTIDE TERMINATION FACTORS; PRIONS; PROTEASOME ENDOPEPTIDASE COMPLEX; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN;

EID: 84906938792     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12716     Document Type: Article

References (52)

1. Aguzzi, A., and Rajendran, L. (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64: 783-790.
2. Arai, T., Hasegawa, M., Akiyama, H., Ikeda, K., Nonaka, T., Mori, H., etal. (2006) TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 351: 602-611.
3. Aron, R., Higurashi, T., Sahi, C., and Craig, E.A. (2007) J-protein co-chaperone Sis1 required for generation of [RNQ+] seeds necessary for prion propagation. EMBO J 26: 3794-3803.
4. Bagriantsev, S.N., Kushnirov, V.V., and Liebman, S.W. (2006) Analysis of amyloid aggregates using agarose gel electrophoresis. Methods Enzymol 412: 33-48.
5. Bagriantsev, S.N., Gracheva, E.O., Richmond, J.E., and Liebman, S.W. (2008) Variant-specific [PSI+] infection is transmitted by Sup35 polymers within [PSI+] aggregates with heterogeneous protein composition. Mol Biol Cell 19: 2433-2443.
6. Behrends, C., Langer, C.A., Boteva, R., Bottcher, U.M., Stemp, M.J., Schaffar, G., etal. (2006) Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers. Mol Cell 23: 887-897.
7. Binder, L.I., Guillozet-Bongaarts, A.L., Garcia-Sierra, F., and Berry, R.W. (2005) Tau, tangles, and Alzheimer's disease. Biochim Biophys Acta 1739: 216-223.
8. Bradley, M.E., and Liebman, S.W. (2003) Destabilizing interactions among [PSI(+)] and [PIN(+)] yeast prion variants. Genetics 165: 1675-1685.
9. Bradley, M.E., Edskes, H.K., Hong, J.Y., Wickner, R.B., and Liebman, S.W. (2002) Interactions among prions and prion 'strains' in yeast. Proc Natl Acad Sci USA 99 (Suppl. 4): 16392-16399.
10. Chernoff, Y.O., Derkach, I.L., and Inge-Vechtomov, S.G. (1993) Multicopy SUP35 gene induces de-novo appearance of psi-like factors in the yeast Saccharomyces cerevisiae. Curr Genet 24: 268-270.
11. Cooper, A.A., Gitler, A.D., Cashikar, A., Haynes, C.M., Hill, K.J., Bhullar, B., etal. (2006) Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 313: 324-328.
12. 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 USA 94: 9773-9778.
13. Dagkesamanskaya, A.R., and Ter-Avanesyan, M.D. (1991) Interaction of the yeast omnipotent suppressors SUP1(SUP45) and SUP2(SUP35) with non-mendelian factors. Genetics 128: 513-520.
14. Derkatch, I.L., Chernoff, Y.O., Kushnirov, V.V., Inge-Vechtomov, S.G., and Liebman, S.W. (1996) Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 144: 1375-1386.
15. Derkatch, I.L., Bradley, M.E., Zhou, P., Chernoff, Y.O., and Liebman, S.W. (1997) Genetic and environmental factors affecting the de novo appearance of the [PSI+] prion in Saccharomyces cerevisiae. Genetics 147: 507-519.
16. Derkatch, I.L., Bradley, M.E., Masse, S.V., Zadorsky, S.P., Polozkov, G.V., Inge-Vechtomov, S.G., and Liebman, S.W. (2000) Dependence and independence of [PSI(+)] and [PIN(+)]: a two-prion system in yeast? EMBO J 19: 1942-1952.
17. Derkatch, I.L., Bradley, M.E., Hong, J.Y., and Liebman, S.W. (2001) Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 106: 171-182.
18. Douglas, P.M., Treusch, S., Ren, H.Y., Halfmann, R., Duennwald, M.L., Lindquist, S., and Cyr, D.M. (2008) Chaperone-dependent amyloid assembly protects cells from prion toxicity. Proc Natl Acad Sci USA 105: 7206-7211.
19. Douglas, P.M., Summers, D.W., Ren, H.Y., and Cyr, D.M. (2009) Reciprocal efficiency of RNQ1 and polyglutamine detoxification in the cytosol and nucleus. Mol Biol Cell 20: 4162-4173.
20. Duennwald, M.L., and Lindquist, S. (2008) Impaired ERAD and ER stress are early and specific events in polyglutamine toxicity. Genes Dev 22: 3308-3319.
21. Erhart, E., and Hollenberg, C.P. (1983) The presence of a defective LEU2 gene on 2 mu DNA recombinant plasmids of Saccharomyces cerevisiae is responsible for curing and high copy number. J Bacteriol 156: 625-635.
22. Glabe, C.G. (2006) Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol Aging 27: 570-575.
23. Gong, H., Romanova, N.V., Allen, K.D., Chandramowlishwaran, P., Gokhale, K., Newnam, G.P., etal. (2012) Polyglutamine toxicity is controlled by prion composition and gene dosage in yeast. PLoS Genet 8: e1002634.
24. Higurashi, T., Hines, J.K., Sahi, C., Aron, R., and Craig, E.A. (2008) Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc Natl Acad Sci USA 105: 16596-16601.
25. Huh, W.K., Falvo, J.V., Gerke, L.C., Carroll, A.S., Howson, R.W., Weissman, J.S., and O'Shea, E.K. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691.
26. Jiang, H., Poirier, M.A., Liang, Y., Pei, Z., Weiskittel, C.E., Smith, W.W., etal. (2006) Depletion of CBP is directly linked with cellular toxicity caused by mutant huntingtin. Neurobiol Dis 23: 543-551.
27. Kaganovich, D., Kopito, R., and Frydman, J. (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454: 1088-1095.
28. Kanaan, N.M., Morfini, G.A., LaPointe, N.E., Pigino, G.F., Patterson, K.R., Song, Y., etal. (2011) Pathogenic forms of tau inhibit kinesin-dependent axonal transport through a mechanism involving activation of axonal phosphotransferases. J Neurosci 31: 9858-9868.
29. Kucsera, J., Yarita, K., and Takeo, K. (2000) Simple detection method for distinguishing dead and living yeast colonies. J Microbiol Methods 41: 19-21.
30. Mathur, V., Hong, J.Y., and Liebman, S.W. (2009) Ssa1 overexpression and [PIN(+)] variants cure [PSI(+)] by dilution of aggregates. J Mol Biol 390: 155-167.
31. Mathur, V., Seuring, C., Riek, R., Saupe, S.J., and Liebman, S.W. (2012) Localization of HET-S to the cell periphery, not to [Het-s] aggregates, is associated with [Het-s]-HET-S toxicity. Mol Cell Biol 32: 139-153.
32. Meriin, A.B., Zhang, X., He, X., Newnam, G.P., Chernoff, Y.O., and Sherman, M.Y. (2002) Huntington toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J Cell Biol 157: 997-1004.
33. Meriin, A.B., Zhang, X., Alexandrov, I.M., Salnikova, A.B., Ter-Avanesian, M.D., Chernoff, Y.O., and Sherman, M.Y. (2007) Endocytosis machinery is involved in aggregation of proteins with expanded polyglutamine domains. FASEB J 21: 1915-1925.
34. Morfini, G., Szebenyi, G., Richards, B., and Brady, S.T. (2001) Regulation of kinesin: implications for neuronal development. Dev Neurosci 23: 364-376.
35. Neumann, M., Sampathu, D.M., Kwong, L.K., Truax, A.C., Micsenyi, M.C., Chou, T.T., etal. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314: 130-133.
36. Nucifora, F.C., Jr, Sasaki, M., Peters, M.F., Huang, H., Cooper, J.K., Yamada, M., etal. (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291: 2423-2428.
37. Park, S.H., Kukushkin, Y., Gupta, R., Chen, T., Konagai, A., Hipp, M.S., etal. (2013) PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone. Cell 154: 134-145.
38. Pike, B.L., Yongkiettrakul, S., Tsai, M.D., and Heierhorst, J. (2004) Mdt1, a novel Rad53 FHA1 domain-interacting protein, modulates DNA damage tolerance and G(2)/M cell cycle progression in Saccharomyces cerevisiae. Mol Cell Biol 24: 2779-2788.
39. Prusiner, S.B. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216: 136-144.
40. Seuring, C., Greenwald, J., Wasmer, C., Wepf, R., Saupe, S.J., Meier, B.H., and Riek, R. (2013) The mechanism of toxicity in HET-S/HET-s prion incompatibility. PLoS Biol 10: e1001451.
41. Sondheimer, N., and Lindquist, S. (2000) Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 5: 163-172.
42. Sondheimer, N., Lopez, N., Craig, E.A., and Lindquist, S. (2001) The role of Sis1 in the maintenance of the [RNQ+] prion. EMBO J 20: 2435-2442.
43. Specht, S., Miller, S.B., Mogk, A., and Bukau, B. (2011) Hsp42 is required for sequestration of protein aggregates into deposition sites in Saccharomyces cerevisiae. J Cell Biol 195: 617-629.
44. Stein, K.C., and True, H.L. (2011) The [RNQ+] prion: a model of both functional and pathological amyloid. Prion 5: 291-298.
45. Treusch, S., and Lindquist, S. (2012) An intrinsically disordered yeast prion arrests the cell cycle by sequestering a spindle pole body component. J Cell Biol 197: 369-379.
46. Vishveshwara, N., Bradley, M.E., and Liebman, S.W. (2009) Sequestration of essential proteins causes prion associated toxicity in yeast. Mol Microbiol 73: 1101-1114.
47. Wang, Y., Meriin, A.B., Costello, C.E., and Sherman, M.Y. (2007) Characterization of proteins associated with polyglutamine aggregates: a novel approach towards isolation of aggregates from protein conformation disorders. Prion 1: 128-135.
48. Wickner, R.B. (1994) [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264: 566-569.
49. Wickner, R.B., Masison, D.C., and Edskes, H.K. (1995) [PSI] and [URE3] as yeast prions. Yeast 11: 1671-1685.
50. Wu, J., Lin, F., and Qin, Z. (2007) Sequestration of glyceraldehyde-3-phosphate dehydrogenase to aggregates formed by mutant huntingtin. Acta Biochim Biophys Sin (Shanghai) 39: 885-890.
51. Yang, W., Yang, H., and Tien, P. (2006) In vitro self-propagation of recombinant PrPSc-like conformation generated in the yeast cytoplasm. FEBS Lett 580: 4231-4235.
52. Yang, Z., Hong, J.Y., Derkatch, I.L., and Liebman, S.W. (2013) Heterologous gln/asn-rich proteins impede the propagation of yeast prions by altering chaperone availability. PLoS Genet 9: e1003236.