Novel polyglutamine model uncouples proteotoxicity from aging

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Christie, Nakeirah T M ^a   Lee, Amy L ^a   Fay, Hannah G ^a   Gray, Amelia A ^a   Kikis, Elise A ^a  

^a UNIVERSITY OF THE SOUTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 3; POLYGLUTAMINE; ATXN3 PROTEIN, HUMAN; NERVE PROTEIN; NUCLEAR PROTEIN; PEPTIDE; PEPTIDE FRAGMENT; REPRESSOR PROTEIN;

AGING; ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CONTROLLED STUDY; MACHADO JOSEPH DISEASE; MOLECULAR MODEL; MUSCLE CELL; NEUROPATHOLOGY; NONHUMAN; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SPINOCEREBELLAR DEGENERATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CYTOLOGY; GENETICS; HEAT SHOCK RESPONSE; HUMAN; METABOLISM; MOLECULAR GENETICS; MUSCLE; PHYSIOLOGY; PROTEIN FOLDING; PROTEINOSIS;

AGING; AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; HEAT-SHOCK RESPONSE; HUMANS; MOLECULAR SEQUENCE DATA; MUSCLES; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEPTIDE FRAGMENTS; PEPTIDES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN FOLDING; REPRESSOR PROTEINS;

EID: 84901236353     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096835     Document Type: Article

References (44)

1. Masino L, Musi V, Menon RP, Fusi P, Kelly G, et al. (2003) Domain architecture of the polyglutamine protein ataxin-3: a globular domain followed by a flexible tail. FEBS Lett 549: 21-25. (Pubitemid 36959836)
2. Ellisdon AM, Thomas B, Bottomley SP (2006) The two-stage pathway of ataxin-3 fibrillogenesis involves a polyglutamine-independent step. J Biol Chem 281: 16888-16896.
3. Chow MK, Ellisdon AM, Cabrita LD, Bottomley SP (2004) Polyglutamine expansion in ataxin-3 does not affect protein stability: implications for misfolding and disease. J Biol Chem 279: 47643-47651. (Pubitemid 39540910)
4. Paulson HL, Perez MK, Trottier Y, Trojanowski JQ, Subramony SH, et al. (1997) Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron 19: 333-344. (Pubitemid 27374232)
5. McLeod CJ, O'Keefe LV, Richards RI (2005) The pathogenic agent in Drosophila models of 'polyglutamine' diseases. Hum Mol Genet 14: 1041-1048. (Pubitemid 40575879)
6. 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.
7. Mohri-Shiomi A, Garsin DA (2008) Insulin signaling and the heat shock response modulate protein homeostasis in the Caenorhabditis elegans intestine during infection. J Biol Chem 283: 194-201.
8. Brignull HR, Moore FE, Tang SJ, Morimoto RI (2006) Polyglutamine proteins at the pathogenic threshold display neuron-specific aggregation in a panneuronal Caenorhabditis elegans model. J Neurosci 26: 7597-7606. (Pubitemid 44315179)
9. Nollen EA, Garcia SM, van Haaften G, Kim S, Chavez A, et al. (2004) Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc Natl Acad Sci U S A 101: 6403-6408. (Pubitemid 38585986)
10. 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.
11. Mitsui K, Nakayama H, Akagi T, Nekooki M, Ohtawa K, et al. (2002) Purification of polyglutamine aggregates and identification of elongation factor-1alpha and heat shock protein 84 as aggregate-interacting proteins. J Neurosci 22: 9267-9277. (Pubitemid 35356170)
12. Kim S, Nollen EA, Kitagawa K, Bindokas VP, Morimoto RI (2002) Polyglutamine protein aggregates are dynamic. Nat Cell Biol 4: 826-831.
13. 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. (Pubitemid 37064935)
14. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A (2006) Opposing activities protect against age-onset proteotoxicity. Science 313: 1604-1610. (Pubitemid 44414028)
15. Kim MW, Chelliah Y, Kim SW, Otwinowski Z, Bezprozvanny I (2009) Secondary structure of Huntingtin amino-terminal region. Structure 17: 1205-1212.
16. Kawaguchi Y, Okamoto T, Taniwaki M, Aizawa M, Inoue M, et al. (1994) CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat Genet 8: 221-228. (Pubitemid 24338732)
17. Kuhlbrodt K, Janiesch PC, Kevei E, Segref A, Barikbin R, et al. The Machado-Joseph disease deubiquitylase ATX-3 couples longevity and proteostasis. Nat Cell Biol 13: 273-281.
18. Teixeira-Castro A, Ailion M, Jalles A, Brignull HR, Vilaca JL, et al. (2011) Neuron-specific proteotoxicity of mutant ataxin-3 in C. elegans: rescue by the DAF-16 and HSF-1 pathways. Hum Mol Genet 20: 2996-3009.
19. Brignull HR, Morley JF, Garcia SM, Morimoto RI (2006) Modeling polyglutamine pathogenesis in C. elegans. Methods Enzymol 412: 256-282. (Pubitemid 44548585)
20. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
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 106: 14914-14919.
22. Prahlad V, Cornelius T, Morimoto RI (2008) Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320: 811-814. (Pubitemid 351929633)
23. Gidalevitz T, Krupinski T, Garcia S, Morimoto RI (2009) Destabilizing protein polymorphisms in the genetic background direct phenotypic expression of mutant SOD1 toxicity. PLoS Genet 5: e1000399.
24. Goti D, Katzen SM, Mez J, Kurtis N, Kiluk J, et al. (2004) A mutant ataxin-3 putative-cleavage fragment in brains of Machado-Joseph disease patients and transgenic mice is cytotoxic above a critical concentration. J Neurosci 24: 10266-10279. (Pubitemid 39492054)
25. Berke SJ, Schmied FA, Brunt ER, Ellerby LM, Paulson HL (2004) Caspase-mediated proteolysis of the polyglutamine disease protein ataxin-3. J Neurochem 89: 908-918. (Pubitemid 38684738)
26. Colomer Gould VF, Goti D, Pearce D, Gonzalez GA, Gao H, et al. (2007) A mutant ataxin-3 fragment results from processing at a site N-terminal to amino acid 190 in brain of Machado-Joseph disease-like transgenic mice. Neurobiol Dis 27: 362-369. (Pubitemid 47337189)
27. Haacke A, Hartl FU, Breuer P (2007) Calpain inhibition is sufficient to suppress aggregation of polyglutamine-expanded ataxin-3. J Biol Chem 282: 18851-18856. (Pubitemid 47100145)
28. Guisbert E, Czyz DM, Richter K, McMullen PD, Morimoto RI (2013) Identification of a tissue-selective heat shock response regulatory network. PLoS Genet 9: e1003466.
29. Kikis EA, Gidalevitz T, Morimoto RI (2010) Protein homeostasis in models of aging and age-related conformational disease. Adv Exp Med Biol 694: 138-159.
30. 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: 23-32.
31. Gidalevitz T, Ben-Zvi A, Ho KH, Brignull HR, Morimoto RI (2006) Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 311: 1471-1474. (Pubitemid 43376703)
32. David DC, Ollikainen N, Trinidad JC, Cary MP, Burlingame AL, et al. (2010) Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol 8: e1000450.
33. Duyao M, Ambrose C, Myers R, Novelletto A, Persichetti F, et al. (1993) Trinucleotide repeat length instability and age of onset in Huntington's disease. Nat Genet 4: 387-392. (Pubitemid 23231488)
34. 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. (Pubitemid 23231489)
35. 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. (Pubitemid 23231490)
36. Horwich AL, Weissman JS (1997) Deadly conformations-protein misfolding in prion disease. Cell 89: 499-510. (Pubitemid 27511761)
37. Kopito RR, Ron D (2000) Conformational disease. Nat Cell Biol 2: E207-209.
38. Takahashi T, Kikuchi S, Katada S, Nagai Y, Nishizawa M, et al. (2008) Soluble polyglutamine oligomers formed prior to inclusion body formation are cytotoxic. Hum Mol Genet 17: 345-356.
39. Koch P, Breuer P, Peitz M, Jungverdorben J, Kesavan J, et al. (2011) Excitation-induced ataxin-3 aggregation in neurons from patients with Machado-Joseph disease. Nature 480: 543-546.
40. Hands SL, Wyttenbach A (2010) Neurotoxic protein oligomerisation associated with polyglutamine diseases. Acta Neuropathol 120: 419-437.
41. Walters RH, Murphy RM (2009) Examining polyglutamine peptide length: a connection between collapsed conformations and increased aggregation. J Mol Biol 393: 978-992.
42. Nagai Y, Popiel HA (2008) Conformational changes and aggregation of expanded polyglutamine proteins as therapeutic targets of the polyglutamine diseases: exposed beta-sheet hypothesis. Curr Pharm Des 14: 3267-3279.
43. Carrell RW, Lomas DA (1997) Conformational disease. Lancet 350: 134-138. (Pubitemid 27313650)
44. van Oosten-Hawle P, Porter RS, Morimoto RI (2013) Regulation of organismal proteostasis by transcellular chaperone signaling. Cell 153: 1366-1378.