Aggregation of PolyQ Proteins Is Increased upon Yeast Aging and Affected by Sir2 and Hsf1: Novel Quantitative Biochemical and Microscopic Assays

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Cohen, Aviv ^a   Ross, Liron ^a   Nachman, Iftach ^a   Bar Nun, Shoshana ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; HUNTINGTIN; POLYGLUTAMINE; POLYQ PROTEIN; PROTEIN; SILENT INFORMATION REGULATOR PROTEIN 2; UNCLASSIFIED DRUG;

AGING; ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; CYTOTOXICITY; ENVIRONMENT; FUNGAL STRAIN; GENE; MICROSCOPY; NONHUMAN; PROTEIN AGGREGATION; QUANTITATIVE ASSAY; SACCHAROMYCES CEREVISIAE; YEAST; YEAST CELL;

BLOTTING, WESTERN; DNA-BINDING PROTEINS; HEAT-SHOCK PROTEINS; MICROSCOPY, FLUORESCENCE; PEPTIDES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; SIRTUIN 2; TRANSCRIPTION FACTORS;

SACCHAROMYCES CEREVISIAE;

EID: 84866131380     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044785     Document Type: Article

References (86)

1. Harper PS (1991) Aspects of Huntington's Disease. In: Harper PS (ed) Huntington Disese Major Problems in Neurology. W.B. Sanders Co., London, 281-315.
2. Myers RH, MacDonald ME, Koroshetz WJ, Duyao MP, Ambrose CM, et al. (1993) De novo expansion of a (CAG)n repeat in sporadic Huntington's disease. Nat Genet 5: 168-173.
3. Hedreen JC, Folstein SE, (1995) Early loss of neostriatal striosome neurons in Huntington's disease. J Neuropathol Exp Neurol 54: 105-120.
4. Vonsattel JP, DiFiglia M, (1998) Huntington disease. J Neuropathol Exp Neurol 57: 369-384.
5. Wexler NS, Lorimer J, Porter J, Gomez F, Moskowitz C, et al. (2004) Venezuelan kindreds reveal that genetic and environmental factors modulate Huntington's disease age of onset. Proc Natl Acad Sci U S A 101: 3498-3503.
6. Novak MJ, Tabrizi SJ, (2010) Huntington's disease. BMJ 340: c3109.
7. The Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72: 971-983.
8. Cattaneo E, Zuccato C, Tartari M, (2005) Normal huntingtin function: an alternative approach to Huntington's disease. Nat Rev Neurosci 6: 919-930.
9. Suopanki J, Gotz C, Lutsch G, Schiller J, Harjes P, et al. (2006) Interaction of huntingtin fragments with brain membranes - clues to early dysfunction in Huntington's disease. J Neurochem 96: 870-884.
10. Davies SW, Turmaine M, Cozens BA, DiFiglia M, Sharp AH, et al. (1997) Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90: 537-548.
11. Wojciechowska M, Krzyzosiak WJ, (2011) Cellular toxicity of expanded RNA repeats: focus on RNA foci. Hum Mol Genet 20: 3811-3821.
12. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, et al. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277: 1990-1993.
13. Scherzinger E, Lurz R, Turmaine M, Mangiarini L, Hollenbach B, et al. (1997) Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90: 549-558.
14. Saunders HM, Gilis D, Rooman M, Dehouck Y, Robertson AL, et al. (2011) Flanking domain stability modulates the aggregation kinetics of a polyglutamine disease protein. Protein Sci 20: 1675-1681.
15. Zoghbi HY, Orr HT, (1999) Polyglutamine diseases: protein cleavage and aggregation. Curr Opin Neurobiol 9: 566-570.
16. Fischbeck KH, (2001) Polyglutamine expansion neurodegenerative disease. Brain Res Bull 56: 161-163.
17. Ross CA, Poirier MA, Wanker EE, Amzel M, (2003) Polyglutamine fibrillogenesis: the pathway unfolds. Proc Natl Acad Sci U S A 100: 1-3.
18. Landles C, Bates GP, (2004) Huntingtin and the molecular pathogenesis of Huntington's disease. Fourth in molecular medicine review series. EMBO Rep 5: 958-963.
19. Morley JF, Brignull HR, Weyers JJ, Morimoto RI, (2002) The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc Natl Acad Sci U S A 99: 10417-10422.
20. Morimoto RI, (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 22: 1427-1438.
21. Ben Zvi A, Miller EA, Morimoto RI (2009) Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc Natl Acad Sci U S A.
22. Gusella JF, MacDonald ME, (2009) Huntington's disease: the case for genetic modifiers. Genome Med 1: 80.
23. Telenius H, Kremer HP, Theilmann J, Andrew SE, Almqvist E, et al. (1993) Molecular analysis of juvenile Huntington disease: the major influence on (CAG)n repeat length is the sex of the affected parent. Hum Mol Genet 2: 1535-1540.
24. Andrew SE, Goldberg YP, Kremer B, Telenius H, Theilmann J, et al. (1993) The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington's disease. Nat Genet 4: 398-403.
25. Snell RG, MacMillan JC, Cheadle JP, Fenton I, Lazarou LP, et al. (1993) Relationship between trinucleotide repeat expansion and phenotypic variation in Huntington's disease. Nat Genet 4: 393-397.
26. Stine OC, Pleasant N, Franz ML, Abbott MH, Folstein SE, et al. (1993) Correlation between the onset age of Huntington's disease and length of the trinucleotide repeat in IT-15. Hum Mol Genet 2: 1547-1549.
27. Kremer B, Goldberg P, Andrew SE, Theilmann J, Telenius H, et al. (1994) A worldwide study of the Huntington's disease mutation. The sensitivity and specificity of measuring CAG repeats. N Engl J Med 330: 1401-1406.
28. Langbehn DR, Hayden MR, Paulsen JS, (2010) CAG-repeat length and the age of onset in Huntington disease (HD): a review and validation study of statistical approaches. Am J Med Genet B Neuropsychiatr Genet 153B: 397-408.
29. Langbehn DR, Brinkman RR, Falush D, Paulsen JS, Hayden MR, (2004) A new model for prediction of the age of onset and penetrance for Huntington's disease based on CAG length. Clin Genet 65: 267-277.
30. Sohal RS, Mockett RJ, Orr WC, (2002) Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Radic Biol Med 33: 575-586.
31. Taylor RC, Dillin A (2011) Aging as an event of proteostasis collapse. Cold Spring Harb Perspect Biol 3:.
32. Fontana L, Partridge L, Longo VD, (2010) Extending healthy life span - from yeast to humans. Science 328: 321-326.
33. Parrella E, Longo VD, (2008) The chronological life span of Saccharomyces cerevisiae to study mitochondrial dysfunction and disease. Methods 46: 256-262.
34. Fabrizio P, Hoon S, Shamalnasab M, Galbani A, Wei M, et al. (2010) Genome-wide screen in Saccharomyces cerevisiae identifies vacuolar protein sorting, autophagy, biosynthetic, and tRNA methylation genes involved in life span regulation. PLoS Genet 6: e1001024.
35. Chen Q, Ding Q, Keller JN, (2005) The stationary phase model of aging in yeast for the study of oxidative stress and age-related neurodegeneration. Biogerontology 6: 1-13.
36. Haigis MC, Guarente LP, (2006) Mammalian sirtuins - emerging roles in physiology, aging, and calorie restriction. Genes Dev 20: 2913-2921.
37. Frye RA, (2000) Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun 273: 793-798.
38. Schwer B, Verdin E, (2008) Conserved metabolic regulatory functions of sirtuins. Cell Metab 7: 104-112.
39. Kaeberlein M, McVey M, Guarente L, (1999) The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev 13: 2570-2580.
40. Fabrizio P, Gattazzo C, Battistella L, Wei M, Cheng C, et al. (2005) Sir2 blocks extreme life-span extension. Cell 123: 655-667.
41. Hsu AL, Murphy CT, Kenyon C, (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300: 1142-1145.
42. Garigan D, Hsu AL, Fraser AG, Kamath RS, Ahringer J, et al. (2002) Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161: 1101-1112.
43. Steinkraus KA, Smith ED, Davis C, Carr D, Pendergrass WR, et al. (2008) Dietary restriction suppresses proteotoxicity and enhances longevity by an hsf-1-dependent mechanism in Caenorhabditis elegans. Aging Cell 7: 394-404.
44. Ohtsuka H, Azuma K, Murakami H, Aiba H, (2011) hsf1 (+) extends chronological lifespan through Ecl1 family genes in fission yeast. Mol Genet Genomics 285: 67-77.
45. Sorger PK, (1991) Heat shock factor and the heat shock response. Cell 65: 363-366.
46. Yamamoto A, Mizukami Y, Sakurai H, (2005) Identification of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae. J Biol Chem 280: 11911-11919.
47. Akerfelt M, Morimoto RI, Sistonen L, (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11: 545-555.
48. Sorger PK, Pelham HR, (1988) Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54: 855-864.
49. Hahn JS, Hu Z, Thiele DJ, Iyer VR, (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24: 5249-5256.
50. Eastmond DL, Nelson HC, (2006) Genome-wide analysis reveals new roles for the activation domains of the Saccharomyces cerevisiae heat shock transcription factor (Hsf1) during the transient heat shock response. J Biol Chem 281: 32909-32921.
51. Westerheide SD, Anckar J, Stevens SM Jr, Sistonen L, Morimoto RI, (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323: 1063-1066.
52. Gidalevitz T, Prahlad V, Morimoto RI (2011) The stress of protein misfolding: from single cells to multicellular organisms. Cold Spring Harb Perspect Biol 3:.
53. Monteiro JP, Cano MI, (2011) SIRT1 deacetylase activity and the maintenance of protein homeostasis in response to stress: an overview. Protein Pept Lett 18: 167-173.
54. Swinnen E, Buttner S, Outeiro TF, Galas MC, Madeo F, et al. (2011) Aggresome formation and segregation of inclusions influence toxicity of alpha-synuclein and synphilin-1 in yeast. Biochem Soc Trans 39: 1476-1481.
55. 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 U S A 97: 1589-1594.
56. Meriin AB, Zhang X, He X, Newnam GP, Chernoff YO, et al. (2002) Huntington toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J Cell Biol 157: 997-1004.
57. Duennwald ML, Jagadish S, Giorgini F, Muchowski PJ, Lindquist S, (2006) A network of protein interactions determines polyglutamine toxicity. Proc Natl Acad Sci U S A 103: 11051-11056.
58. Kaeberlein M, Burtner CR, Kennedy BK, (2007) Recent developments in yeast aging. PLoS Genet 3: e84.
59. Sherman MY, Muchowski PJ, (2003) Making yeast tremble: yeast models as tools to study neurodegenerative disorders. Neuromolecular Med 4: 133-146.
60. 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.
61. Outeiro TF, Muchowski PJ, (2004) Molecular genetics approaches in yeast to study amyloid diseases. J Mol Neurosci 23: 49-60.
62. 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.
63. Giorgini F, Muchowski PJ, (2006) Screening for genetic modifiers of amyloid toxicity in yeast. Methods Enzymol 412: 201-222.
64. Duennwald ML, Jagadish S, Muchowski PJ, Lindquist S, (2006) Flanking sequences profoundly alter polyglutamine toxicity in yeast. Proc Natl Acad Sci U S A 103: 11045-11050.
65. Ehrnhoefer DE, Duennwald M, Markovic P, Wacker JL, Engemann S, et al. (2006) Green tea (-)-epigallocatechin-gallate modulates early events in huntingtin misfolding and reduces toxicity in Huntington's disease models. Hum Mol Genet 15: 2743-2751.
66. Duennwald ML, Lindquist S, (2008) Impaired ERAD and ER stress are early and specific events in polyglutamine toxicity. Genes Dev 22: 3308-3319.
67. Giorgini F, Muchowski PJ, (2009) Exploiting yeast genetics to inform therapeutic strategies for Huntington's disease. Methods Mol Biol 548: 161-174.
68. Beam M, Silva MC, Morimoto RI (2012) Dynamic imaging by fluorescence correlation spectroscopy identifies diverse populations of polyglutamine oligomers formed in vivo. J Biol Chem.
69. Imai S, Armstrong CM, Kaeberlein M, Guarente L, (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403: 795-800.
70. Voisine C, Pedersen JS, Morimoto RI, (2010) Chaperone networks: tipping the balance in protein folding diseases. Neurobiol Dis 40: 12-20.
71. Yokoyama K, Fukumoto K, Murakami T, Harada S, Hosono R, et al. (2002) Extended longevity of Caenorhabditis elegans by knocking in extra copies of hsp70F, a homolog of mot-2 (mortalin)/mthsp70/Grp75. FEBS Lett 516: 53-57.
72. Tatar M, Khazaeli AA, Curtsinger JW, (1997) Chaperoning extended life. Nature 390: 30.
73. Calamini B, Silva MC, Madoux F, Hutt DM, Khanna S, et al. (2012) Small-molecule proteostasis regulators for protein conformational diseases. Nat Chem Biol 8: 185-196.
74. 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.
75. Muller I, Zimmermann M, Becker D, Flomer M, (1980) Calendar life span versus budding life span of Saccharomyces cerevisiae. Mech Ageing Dev 12: 47-52.
76. Erjavec N, Larsson L, Grantham J, Nystrom T, (2007) Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes Dev 21: 2410-2421.
77. Liu B, Larsson L, Caballero A, Hao X, Oling D, et al. (2010) The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140: 257-267.
78. Silva MC, Fox S, Beam M, Thakkar H, Amaral MD, et al. (2011) A genetic screening strategy identifies novel regulators of the proteostasis network. PLoS Genet 7: e1002438.
79. Weiss A, Klein C, Woodman B, Sathasivam K, Bibel M, et al. (2008) Sensitive biochemical aggregate detection reveals aggregation onset before symptom development in cellular and murine models of Huntington's disease. J Neurochem 104: 846-858.
80. Arrasate M, Mitra S, Schweitzer ES, Segal MR, Finkbeiner S, (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431: 805-810.
81. Nagai Y, Inui T, Popiel HA, Fujikake N, Hasegawa K, et al. (2007) A toxic monomeric conformer of the polyglutamine protein. Nat Struct Mol Biol 14: 332-340.
82. Caughey B, Lansbury PT, (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci 26: 267-298.
83. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A, (2006) Opposing activities protect against age-onset proteotoxicity. Science 313: 1604-1610.
84. Wang CL, Landry J, Sternglanz R, (2008) A yeast sir2 mutant temperature sensitive for silencing. Genetics 180: 1955-1962.
85. Nachman I, Regev A, Ramanathan S, (2007) Dissecting timing variability in yeast meiosis. Cell 131: 544-556.
86. Wanker EE, Scherzinger E, Heiser V, Sittler A, Eickhoff H, et al. (1999) Membrane filter assay for detection of amyloid-like polyglutamine-containing protein aggregates. Methods Enzymol 309: 375-386.