Overexpression of Q-rich prion-like proteins suppresses polyQ cytotoxicity and alters the polyQ interactome

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 51, 2014, Pages 18219-18224

  Ripaud, Leslie ^a   Chumakova, Victoria ^a   Antonin, Matthias ^a   Hastie, Alex R ^a   Pinkert, Stefan ^a   Körner, Roman ^a   Ruff, Kiersten M ^b   Pappu, Rohit V ^b   Hornburg, Daniel ^a   Mann, Matthias ^a   Hartl, F Ulrich ^a   Hipp, Mark S ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

Neurodegeneration; Polyglutamine proteins; Prion; Protein aggregation; Protein misfolding

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 40; HUNTINGTIN; MINICHROMOSOME MAINTENANCE PROTEIN 1; POLYGLUTAMINE; PRION PROTEIN; Q RICH PRION LIKE PROTEIN; RNA BINDING PROTEIN; SERINE; SYNAPSIN I; UNCLASSIFIED DRUG; PEPTIDE; PRION; PROTEIN BINDING;

ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; GENE DELETION; GENE OVEREXPRESSION; MINICHROMOSOME; NONHUMAN; PROMOTER REGION; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; STOICHIOMETRY; ZINC FINGER MOTIF; GENETICS; METABOLISM; PRION;

PEPTIDES; PRIONS; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE;

EID: 84919904527     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421313111     Document Type: Article

References (63)

1. Orr HT, Zoghbi HY (2007) Trinucleotide repeat disorders. Annu Rev Neurosci 30: 575-621.
2. Duyao M, et al. (1993) Trinucleotide repeat length instability and age of onset in Huntington's disease. Nat Genet 4(4):387-392.
3. Gusella JF, MacDonald ME (2000) Molecular genetics: Unmasking polyglutamine triggers in neurodegenerative disease. Nat Rev Neurosci 1(2):109-115.
4. Stefani M, Dobson CM (2003) Protein aggregation and aggregate toxicity: New insights into protein folding, misfolding diseases and biological evolution. J Mol Med (Berl) 81(11):678-699.
5. Winklhofer KF, Tatzelt J, Haass C (2008) The two faces of protein misfolding: Gain- and loss-of-function in neurodegenerative diseases. EMBO J 27(2):336-349.
6. Ross CA, Poirier MA (2005) Opinion: What is the role of protein aggregation in neurodegeneration? Nat Rev Mol Cell Biol 6(11):891-898.
7. Perez MK, et al. (1998) Recruitment and the role of nuclear localization in polyglutamine-mediated aggregation. J Cell Biol 143(6):1457-1470.
8. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366.
9. Olzscha H, et al. (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144(1):67-78.
10. Hipp MS, Park SH, Hartl FU (2014) Proteostasis impairment in protein-misfolding and -aggregation diseases. Trends Cell Biol 24(9):506-514.
11. Gidalevitz T, Kikis EA, Morimoto RI (2010) A cellular perspective on conformational disease: The role of genetic background and proteostasis networks. Curr Opin Struct Biol 20(1):23-32.
12. Powers ET, Morimoto RI, Dillin A, Kelly JW, Balch WE (2009) Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 78:959-991.
13. Holmes WM, Klaips CL, Serio TR (2014) Defining the limits: Protein aggregation and toxicity in vivo. Crit Rev Biochem Mol Biol 49(4):294-303.
14. Krobitsch S, Lindquist S (2000) Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins. Proc Natl Acad Sci USA 97(4):1589-1594.
15. Muchowski PJ, et al. (2000) Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc Natl Acad Sci USA 97(14):7841-7846.
16. Duennwald ML, Jagadish S, Muchowski PJ, Lindquist S (2006) Flanking sequences profoundly alter polyglutamine toxicity in yeast. Proc Natl Acad Sci USA 103(29):11045-11050.
17. Wickner RB (1994) [URE3] as an altered URE2 protein: Evidence for a prion analog in Saccharomyces cerevisiae. Science 264(5158):566-569.
18. Duennwald ML, Jagadish S, Giorgini F, Muchowski PJ, Lindquist S (2006) A network of protein interactions determines polyglutamine toxicity. Proc Natl Acad Sci USA 103(29):11051-11056.
19. Meriin AB, et al. (2002) Huntington toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J Cell Biol 157(6):997-1004.
20. Michelitsch MD, Weissman JS (2000) A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions. Proc Natl Acad Sci USA 97(22):11910-11915.
21. Alberti S, Halfmann R, King O, Kapila A, Lindquist S (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137(1):146-158.
22. Nasmyth KA, Tatchell K (1980) The structure of transposable yeast mating type loci. Cell 19(3):753-764.
23. Nasmyth KA, Reed SI (1980) Isolation of genes by complementation in yeast: molecular cloning of a cell-cycle gene. Proc Natl Acad Sci USA 77(4):2119-2123.
24. Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350:87-96.
25. Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26(12):1367-1372.
26. Cox J, et al. (2014) Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics 13(9):2513-2526.
27. Willingham S, Outeiro TF, DeVit MJ, Lindquist SL, Muchowski PJ (2003) Yeast genes that enhance the toxicity of a mutant huntingtin fragment or alpha-synuclein. Science 302(5651):1769-1772.
28. Giorgini F, Guidetti P, Nguyen Q, Bennett SC, Muchowski PJ (2005) A genomic screen in yeast implicates kynurenine 3-monooxygenase as a therapeutic target for Huntington disease. Nat Genet 37(5):526-531.
29. Mason RP, et al. (2013) Glutathione peroxidase activity is neuroprotective in models of Huntington's disease. Nat Genet 45(10):1249-1254.
30. Kayatekin C, et al. (2014) Prion-like proteins sequester and suppress the toxicity of huntingtin exon 1. Proc Natl Acad Sci USA 111(33):12085-12090.
31. Douglas PM, Summers DW, Ren HY, Cyr DM (2009) Reciprocal efficiency of RNQ1 and polyglutamine detoxification in the cytosol and nucleus. Mol Biol Cell 20(19):4162-4173.
32. Park SH, et al. (2013) PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone. Cell 154(1):134-145.
33. Ward MP, Garrett S (1994) Suppression of a yeast cyclic AMP-dependent protein kinase defect by overexpression of SOK1, a yeast gene exhibiting sequence similarity to a developmentally regulated mouse gene. Mol Cell Biol 14(9):5619-5627.
34. Trumbly RJ (1992) Glucose repression in the yeast Saccharomyces cerevisiae. Mol Microbiol 6(1):15-21.
35. Wolfe KJ, Ren HY, Trepte P, Cyr DM (2014) Polyglutamine-rich suppressors of huntingtin toxicity act upstream of Hsp70 and Sti1 in spatial quality control of amyloid-like proteins. PLoS ONE 9(5):e95914.
36. Conrad NK, et al. (2000) A yeast heterogeneous nuclear ribonucleoprotein complex associated with RNA polymerase II. Genetics 154(2):557-571.
37. Elble R, Tye BK (1991) Both activation and repression of a-mating-type-specific genes in yeast require transcription factor Mcm1. Proc Natl Acad Sci USA 88(23):10966-10970.
38. Espinet C, de la Torre MA, Aldea M, Herrero E (1995) An efficient method to isolate yeast genes causing overexpression-mediated growth arrest. Yeast 11(1):25-32.
39. Yaguchi S, Mitsui K, Kawabata K, Xu Z, Tsurugi K (1996) The pleiotropic effect of the GTS1 gene product on heat tolerance, sporulation and the life span of Saccharomyces cerevisiae. Biochem Biophys Res Commun 218(1):234-237.
40. Bossier P, Goethals P, Rodrigues-Pousada C (1997) Constitutive flocculation in Saccharomyces cerevisiae through overexpression of the GTS1 gene, coding for a 'Glo'-type Zn-finger-containing protein. Yeast 13(8):717-725.
41. Yaguchi S, Tsurugi K (2003) Gts1p activates SNF1-dependent derepression of HSP104 and TPS1 in the stationary phase of yeast growth. J Biol Chem 278(32):29760-29768.
42. Sondheimer N, Lindquist S (2000) Rnq1: An epigenetic modifier of protein function in yeast. Mol Cell 5(1):163-172.
43. Warrick JM, et al. (1999) Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat Genet 23(4):425-428.
44. Wanker EE, et al. (1999) Membrane filter assay for detection of amyloid-like polyglutamine-containing protein aggregates. Methods Enzymol 309:375-386.
45. Vitalis A, Pappu RV (2009) ABSINTH: A new continuum solvation model for simulations of polypeptides in aqueous solutions. J Comput Chem 30(5):673-699.
46. Vitalis A, Wang X, Pappu RV (2008) Atomistic simulations of the effects of polyglutamine chain length and solvent quality on conformational equilibria and spontaneous homodimerization. J Mol Biol 384(1):279-297.
47. Vitalis A, Lyle N, Pappu RV (2009) Thermodynamics of beta-sheet formation in polyglutamine. Biophys J 97(1):303-311.
48. Williamson TE, Vitalis A, Crick SL, Pappu RV (2010) Modulation of polyglutamine conformations and dimer formation by the N-terminus of huntingtin. J Mol Biol 396(5):1295-1309.
49. Crick SL, Ruff KM, Garai K, Frieden C, Pappu RV (2013) Unmasking the roles of N- and C-terminal flanking sequences from exon 1 of huntingtin as modulators of polyglutamine aggregation. Proc Natl Acad Sci USA 110(50):20075-20080.
50. Schaffar G, et al. (2004) Cellular toxicity of polyglutamine expansion proteins: Mechanism of transcription factor deactivation. Mol Cell 15(1):95-105.
51. Meriin AB, et al. (2003) Aggregation of expanded polyglutamine domain in yeast leads to defects in endocytosis. Mol Cell Biol 23(21):7554-7565.
52. Meriin AB, et al. (2007) Endocytosis machinery is involved in aggregation of proteins with expanded polyglutamine domains. FASEB J 21(8):1915-1925.
53. Jana NR, Zemskov EA, Wang Gh, Nukina N (2001) Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum Mol Genet 10(10):1049-1059.
54. Yamanaka T, et al. (2008) Mutant Huntingtin reduces HSP70 expression through the sequestration of NF-Y transcription factor. EMBO J 27(6):827-839.
55. Zhao X, et al. (2012) Sequestration of Sup35 by aggregates of huntingtin fragments causes toxicity of [PSI+] yeast. J Biol Chem 287(28):23346-23355.
56. Steffan JS, et al. (2000) The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci USA 97(12):6763-6768.
57. Gong H, et al. (2012) Polyglutamine toxicity is controlled by prion composition and gene dosage in yeast. PLoS Genet 8(4):e1002634.
58. Kochneva-Pervukhova NV, Alexandrov AI, Ter-Avanesyan MD (2012) Amyloid-mediated sequestration of essential proteins contributes to mutant huntingtin toxicity in yeast. PLoS ONE 7(1):e29832.
59. DiSalvo S, Derdowski A, Pezza JA, Serio TR (2011) Dominant prion mutants induce curing through pathways that promote chaperone-mediated disaggregation. Nat Struct Mol Biol 18(4):486-492.
60. Holbert S, et al. (2001) The Gln-Ala repeat transcriptional activator CA150 interacts with huntingtin: Neuropathologic and genetic evidence for a role in Huntington's disease pathogenesis. Proc Natl Acad Sci USA 98(4):1811-1816.
61. Arango M, et al. (2006) CA150 expression delays striatal cell death in overexpression and knock-in conditions for mutant huntingtin neurotoxicity. J Neurosci 26(17):4649-4659.
62. Sanada M, Kuroda K, Ueda M (2011) GTS1 induction causes derepression of Tup1-Cyc8-repressing genes and chromatin remodeling through the interaction of Gts1p with Cyc8p. Biosci Biotechnol Biochem 75(4):740-747.
63. Patel BK, Gavin-Smyth J, Liebman SW (2009) The yeast global transcriptional co-repressor protein Cyc8 can propagate as a prion. Nat Cell Biol 11(3):344-349.