A yeast model for polyalanine-expansion aggregation and toxicity

Molecular Biology of the Cell

Volumn 22, Issue 12, 2011, Pages 1971-1984

  Konopka, Catherine A ^a   Locke, Melissa N ^a   Gallagher, Pamela S ^a   Pham, Ngan ^a   Hart, Michael P ^b   Walker, Claire J ^a   Gitler, Aaron D ^b   Gardner, Richard G ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; BINDING PROTEIN; FUNGAL PROTEIN; MESSENGER RNA; PROTEOME;

ARTICLE; CELL LEVEL; CYTOPLASM; CYTOTOXICITY; EUKARYOTE; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; RNA BINDING; TOXICITY; YEAST;

AMINO ACID SEQUENCE; CELL AGGREGATION; DNA REPEAT EXPANSION; DNA-BINDING PROTEINS; EXODEOXYRIBONUCLEASES; MUTATION; PEPTIDES; PHOSPHOPROTEINS; POLY(A)-BINDING PROTEIN I; PROTEOME; RNA POLYMERASE II; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 79959270550     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-01-0037     Document Type: Article

References (74)

1. Abu-Baker A, Messaed C, Laganiere J, Gaspar C, Brais B, Rouleau GA (2003). Involvement of the ubiquitin-proteasome pathway and molecular chaperones in oculopharyngeal muscular dystrophy. Hum Mol Genet 12, 2609-2623.
2. Albrecht A, Mundlos S (2005). The other trinucleotide repeat: polyalanine expansion disorders. Curr Opin Genet Dev 15, 285-293. (Pubitemid 40726052)
3. Albrecht AN, Kornak U, Boddrich A, Suring K, Robinson PN, Stiege AC, Lurz R, Stricker S, Wanker EE, Mundlos S (2004). A molecular pathogenesis for transcription factor associated poly-alanine tract expansions. Hum Mol Genet 13, 2351-2359. (Pubitemid 39377839)
4. Amiel J, Trochet D, Clement-Ziza M, Munnich A, Lyonnet S (2004). Polyalanine expansions in human. Hum Mol Genet 13 Spec No 2, R235-R243. (Pubitemid 39359908)
5. Amrani N, Minet M, Le Gouar M, Lacroute F, Wyers F (1997). Yeast Pab1 interacts with Rna15 and participates in the control of the poly(A) tail length in vitro. Mol Cell Biol 17, 3694-3701. (Pubitemid 27281844)
6. Berciano MT, Villagra NT, Ojeda JL, Navascues J, Gomes A, Lafarga M, Carmo-Fonseca M (2004). Oculopharyngeal muscular dystrophy-like nuclear inclusions are present in normal magnocellular neurosecretory neurons of the hypothalamus. Hum Mol Genet 13, 829-838. (Pubitemid 38515212)
7. Bond U (2006). Stressed out! Effects of environmental stress on mRNA metabolism. FEMS Yeast Res 6, 160-170.
8. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132. (Pubitemid 28062863)
9. Brais B (2003). Oculopharyngeal muscular dystrophy: a late-onset polyalanine disease. Cytogenet Genome Res 100, 252-260.
10. Brais B et al. (1998). Short GCG expansions in the PABP2 gene cause oculopharyngeal muscular dystrophy. Nat Genet 18, 164-167. (Pubitemid 28082465)
11. Brune C, Munchel SE, Fischer N, Podtelejnikov AV, Weis K (2005). Yeast poly(A)-binding protein Pab1 shuttles between the nucleus and the cytoplasm and functions in mRNA export. RNA 11, 517-531. (Pubitemid 40397185)
12. Buchan JR, Muhlrad D, Parker R (2008). P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol 183, 441-455.
13. Burd CG, Matunis EL, Dreyfuss G (1991). The multiple RNA-binding domains of the mRNA poly(A)-binding protein have different RNA-binding activities. Mol Cell Biol 11, 3419-3424. (Pubitemid 21895728)
14. Caburet S, Demarez A, Moumne L, Fellous M, De Baere E, Veitia RA (2004). A recurrent polyalanine expansion in the transcription factor FOXL2 induces extensive nuclear and cytoplasmic protein aggregation. J Med Genet 41, 932-936. (Pubitemid 40007254)
15. Calado A, Tome FM, Brais B, Rouleau GA, Kuhn U, Wahle E, Carmo- Fonseca M (2000). Nuclear inclusions in oculopharyngeal muscular dystrophy consist of poly(A) binding protein 2 aggregates which sequester poly(A) RNA. Hum Mol Genet 9, 2321-2328.
16. Carmichael J, Chatellier J, Woolfson A, Milstein C, Fersht AR, Rubinsztein DC (2000). Bacterial and yeast chaperones reduce both aggregate formation and cell death in mammalian cell models of Huntington's disease. Proc Natl Acad Sci USA 97, 9701-9705. (Pubitemid 30650839)
17. Chartier A, Benoit B, Simonelig M (2006). A Drosophila model of oculopharyngeal muscular dystrophy reveals intrinsic toxicity of PABPN1. EMBO J 25, 2253-2262.
18. Chen-Plotkin AS, Lee VM, Trojanowski JQ (2010). TAR DNA-binding protein 43 in neurodegenerative disease. Nat Rev Neurol 6, 211-220.
19. Collins SR, Schuldiner M, Krogan NJ, Weissman JS (2006). A strategy for extracting and analyzing large-scale quantitative epistatic interaction data. Genome Biol 7, R63.
20. Cooper AA et al. (2006). Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 313, 324-328. (Pubitemid 44480951)
21. Deardorff JA, Sachs AB (1997). Differential effects of aromatic and charged residue substitutions in the RNA binding domains of the yeast poly(A)-binding protein. J Mol Biol 269, 67-81. (Pubitemid 27243622)
22. Decker CJ, Teixeira D, Parker R (2007). Edc3p and a glutamine/ asparaginerich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J Cell Biol 179, 437-449. (Pubitemid 350074789)
23. Douglas PM, Treusch S, Ren HY, Halfmann R, Duennwald ML, Lindquist S, Cyr DM (2008). Chaperone-dependent amyloid assembly protects cells from prion toxicity. Proc Natl Acad Sci USA 105, 7206-7211. (Pubitemid 351754456)
24. Duennwald ML, Jagadish S, Giorgini F, Muchowski PJ, Lindquist S (2006a). A network of protein interactions determines polyglutamine toxicity. Proc Natl Acad Sci USA 103, 11051-11056. (Pubitemid 44148416)
25. Duennwald ML, Jagadish S, Muchowski PJ, Lindquist S (2006b). Flanking sequences profoundly alter polyglutamine toxicity in yeast. Proc Natl Acad Sci USA 103, 11045-11050. (Pubitemid 44148415)
26. Duennwald ML, Lindquist S (2008). Impaired ERAD and ER stress are early and specific events in polyglutamine toxicity. Genes Dev 22, 3308-3319.
27. Elden AC et al. (2010). Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 466, 1069-1075.
28. Fan X, Dion P, Laganiere J, Brais B, Rouleau GA (2001). Oligomerization of polyalanine expanded PABPN1 facilitates nuclear protein aggregation that is associated with cell death. Hum Mol Genet 10, 2341-2351. (Pubitemid 33069540)
29. Fares H, Goetsch L, Pringle JR (1996). Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae. J Cell Biol 132, 399-411. (Pubitemid 26052573)
30. Fasken MB, Stewart M, Corbett AH (2008). Functional significance of the interaction between the mRNA-binding protein, Nab2, and the nuclear pore-associated protein, Mlp1, in mRNA export. J Biol Chem 283, 27130-27143.
31. Faux NG, Bottomley SP, Lesk AM, Irving JA, Morrison JR, de la Banda MG, Whisstock JC (2005). Functional insights from the distribution and role of homopeptide repeat-containing proteins. Genome Res 15, 537-551. (Pubitemid 41057816)
32. Fischer T, Strasser K, Racz A, Rodriguez-Navarro S, Oppizzi M, Ihrig P, Lechner J, Hurt E (2002). The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J 21, 5843-5852.
33. Flescher EG, Madden K, Snyder M (1993). Components required for cytokinesis are important for bud site selection in yeast. J Cell Biol 122, 373-386. (Pubitemid 23210464)
34. 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, 526-531. (Pubitemid 40617282)
35. Giri K, Ghosh U, Bhattacharyya NP, Basak S (2003). Caspase 8 mediated apoptotic cell death induced by beta-sheet forming polyalanine peptides. FEBS Lett 555, 380-384. (Pubitemid 37486060)
36. Gitler AD et al. (2009). Alpha-synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nat Genet 41, 308-315.
37. Gokhale KC, Newnam GP, Sherman MY, Chernoff YO (2005). Modulation of prion-dependent polyglutamine aggregation and toxicity by chaperone proteins in the yeast model. J Biol Chem 280, 22809-22818. (Pubitemid 40853187)
38. Guthrie C, Fink GR (1991). Guide to yeast genetics and molecular biology. Methods Enzymol 194, 1-863.
39. Halfmann R, Lindquist S (2008). Screening for amyloid aggregation by semi-denaturing detergent-agarose gel electrophoresis. J Vis Exp 17, pii: 838.
40. Jana NR, Nukina N (2003). Recent advances in understanding the pathogenesis of polyglutamine diseases: involvement of molecular chaperones and ubiquitin-proteasome pathway. J Chem Neuroanat 26, 95-101. (Pubitemid 37346281)
41. Johnson BS, McCaffery JM, Lindquist S, Gitler AD (2008). A yeast TDP- 43 proteinopathy model: Exploring the molecular determinants of TDP-43 aggregation and cellular toxicity. Proc Natl Acad Sci USA 105, 6439-6444. (Pubitemid 351758364)
42. Johnson BS, Snead D, Lee JJ, McCaffery JM, Shorter J, Gitler AD (2009). TDP-43 is intrinsically aggregation-prone, and amyotrophic lateral sclerosis-linked mutations accelerate aggregation and increase toxicity. J Biol Chem 284, 20329-20339.
43. Kaganovich D, Kopito R, Frydman J (2008). Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088-1095.
44. Kim YJ, Noguchi S, Hayashi YK, Tsukahara T, Shimizu T, Arahata K (2001). The product of an oculopharyngeal muscular dystrophy gene, poly(A)- binding protein 2, interacts with SKIP and stimulates muscle-specific gene expression. Hum Mol Genet 10, 1129-1139. (Pubitemid 32487536)
45. Klein AF, Ebihara M, Alexander C, Dicaire MJ, Sasseville AM, Langelier Y, Rouleau GA, Brais B (2008). PABPN1 polyalanine tract deletion and long expansions modify its aggregation pattern and expression. Exp Cell Res 314, 1652-1666.
46. Kohler A, Hurt E (2007). Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol 8, 761-773. (Pubitemid 47462133)
47. 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, 1589-1594. (Pubitemid 30118486)
48. Lennon JC 3rd, Wind M, Saunders L, Hock MB, Reines D (1998). Mutations in RNA polymerase II and elongation factor SII severely reduce mRNA levels in Saccharomyces cerevisiae. Mol Cell Biol 18, 5771-5779. (Pubitemid 28450528)
49. Lucking CB, Brice A (2000). Alpha-synuclein and Parkinson's disease. Cell Mol Life Sci 57, 1894-1908. (Pubitemid 32102585)
50. Mangus DA, Amrani N, Jacobson A (1998). Pbp1p, a factor interacting with Saccharomyces cerevisiae poly(A)-binding protein, regulates polyadenylation. Mol Cell Biol 18, 7383-7396. (Pubitemid 28533058)
51. Maris C, Dominguez C, Allain FH (2005). The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272, 2118-2131. (Pubitemid 40655326)
52. Meriin AB, Zhang X, Alexandrov IM, Salnikova AB, Ter-Avanesian MD, Chernoff YO, Sherman MY (2007). Endocytosis machinery is involved in aggregation of proteins with expanded polyglutamine domains. FASEB J 21, 1915-1925. (Pubitemid 46855636)
53. Meriin AB, Zhang X, He X, Newnam GP, Chernoff YO, Sherman MY (2002). Huntington toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J Cell Biol 157, 997-1004. (Pubitemid 34839774)
54. Muchowski PJ, Schaffar G, Sittler A, Wanker EE, Hayer-Hartl MK, Hartl FU (2000). Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc Natl Acad Sci USA 97, 7841-7846. (Pubitemid 30460735)
55. Parker R, Sheth U (2007). P bodies and the control of mRNA translation and degradation. Mol Cell 25, 635-646. (Pubitemid 46341926)
56. Rankin J, Wyttenbach A, Rubinsztein DC (2000). Intracellular green fluorescent protein-polyalanine aggregates are associated with cell death. Biochem J 348 Pt 1, 15-19. (Pubitemid 30312125)
57. Riley BE, Orr HT (2006). Polyglutamine neurodegenerative diseases and regulation of transcription: assembling the puzzle. Genes Dev 20, 2183-2192.
58. Ross CA (2002). Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron 35, 819-822.
59. Sachs AB, Bond MW, Kornberg RD (1986). A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell 45, 827-835.
60. Shinchuk LM, Sharma D, Blondelle SE, Reixach N, Inouye H, Kirschner DA (2005). Poly-(L-alanine) expansions form core beta-sheets that nucleate amyloid assembly. Proteins 61, 579-589. (Pubitemid 41547414)
61. Strasser K et al. (2002). TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417, 304-308.
62. Sun Z, Zamia D, Xiaodon F, Hart MP, Chesi A, Shorter J, Gitler AD (2011). Molecular determinants and genetic modifiers of aggregation and toxicity for the ALS disease protein FUS/TLS. PLoS Biol 9, e1000614.
63. Takahashi T, Katada S, Onodera O (2010). Polyglutamine diseases: where does toxicity come from? What is toxicity? Where are we going? J Mol Cell Biol 2, 180-191.
64. Tam S, Geller R, Spiess C, Frydman J (2006). The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunit-specific interactions. Nat Cell Biol 8, 1155-1162. (Pubitemid 44473612)
65. Tarun SZ Jr, Sachs AB (1996). Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J 15, 7168-7177.
66. Tavanez JP, Calado P, Braga J, Lafarga M, Carmo-Fonseca M (2005). In vivo aggregation properties of the nuclear poly(A)-binding protein PABPN1. RNA 11, 752-762.
67. Tong AH et al. (2001). Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368. (Pubitemid 33140562)
68. Tong AH et al. (2004). Global mapping of the yeast genetic interaction network. Science 303, 808-813. (Pubitemid 38174652)
69. Tong XS, Xu S, Zheng S, Pivnichny JV, Martin J, Dufresne C (2006). High throughput metabolic stability screen for lead optimization in drug discovery. J Chromatogr B Analyt Technol Biomed Life Sci 833, 165-173.
70. van Ham TJ, Breitling R, Swertz MA, Nollen EA (2009). Neurodegenerative diseases: lessons from genome-wide screens in small model organisms. EMBO Mol Med 1, 360-370.
71. Voigt A, Herholz D, Fiesel FC, Kaur K, Muller D, Karsten P, Weber SS, Kahle PJ, Marquardt T, Schulz JB (2010). TDP-43-mediated neuron loss in vivo requires RNA-binding activity. PLoS One 5, e12247.
72. 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, 1769-1772. (Pubitemid 37505741)
73. Yao G, Chiang YC, Zhang C, Lee DJ, Laue TM, Denis CL (2007). PAB1 selfassociation precludes its binding to poly(A), thereby accelerating CCR4 deadenylation in vivo. Mol Cell Biol 27, 6243-6253. (Pubitemid 47326710)
74. Zoghbi HY, Orr HT (2000). Glutamine repeats and neurodegeneration. Annu Rev Neurosci 23, 217-247. (Pubitemid 30350043)