857
Views
5
CrossRef citations to date
0
Altmetric
Extra Views

Wild type huntingtin toxicity in yeast: Implications for the role of amyloid cross-seeding in polyQ diseases

, , &
Pages 221-227 | Received 11 Mar 2016, Accepted 05 Apr 2016, Published online: 24 May 2016

REFERENCES

  • Chiti F, Dobson CM. Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 2006; 75:333-66; PMID:16756495; http://dx.doi.org/10.1146/annurev.biochem.75.101304.123901
  • Knowles TPJ, Vendruscolo M, Dobson CM. The amyloid state and its association with protein misfolding diseases. Nat Rev Mol Cell Biol 2014; 15:384-96; PMID:24854788; http://dx.doi.org/10.1038/nrm3810
  • Nizhnikov AA, Antonets KS, Inge-Vechtomov SG. Amyloids: from pathogenesis to function. Biochem 2015; 80:1127-44
  • MacDonald ME, Ambrose CM, Duyao MP, Myers RH, Lin C, Srinidhi L, Barnes G, Taylor SA, James M, Groot N, et al. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 1993; 72:971-83; PMID:8458085; http://dx.doi.org/10.1016/0092-8674(93)90585-E
  • Bates G. Huntingtin aggregation and toxicity in Huntington's disease. Lancet 2003; 361:1642-4; PMID:12747895; http://dx.doi.org/10.1016/S0140-6736(03)13304-1
  • Ross CA, Tabrizi SJ. Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol 2011; 10:83-98; PMID:21163446; http://dx.doi.org/10.1016/S1474-4422(10)70245-3
  • Roizin L, Stellar S, Liu JC. Neuronal nuclear-cytoplasmic changes in Huntington's chorea: electron microscope investigations. Adv Neurol 1979; 23:95-122; PMID:506869
  • DiFiglia M. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997; 277:1990-3; PMID:9302293; http://dx.doi.org/10.1126/science.277.5334.1990
  • Davies SW, Turmaine M, Cozens BA, DiFiglia M, Sharp AH, Ross CA, Scherzinger E, Wanker EE, Mangiarini L, Bates GP. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 1997; 90:537-48; PMID:9267033; http://dx.doi.org/10.1016/S0092-8674(00)80513-9
  • Takahashi T, Katada S, Onodera O. Polyglutamine diseases: where does toxicity come from? what is toxicity? where are we going? J Mol Cell Biol 2010; 2:180-91; PMID:20410236; http://dx.doi.org/10.1093/jmcb/mjq005
  • Davies SW, Sathasivam K, Hobbs C, Doherty P, Mangiarini L, Scherzinger E, Wanker EE, Bates GP. Detection of polyglutamine aggregation in mouse models. Methods Enzym 1999; 309:687-701; http://dx.doi.org/10.1016/S0076-6879(99)09045-X
  • Marsh JL, Pallos J, Thompson LM. Fly models of Huntington's disease. Hum Mol Genet 2003; 12:R187-93; PMID:12925571; http://dx.doi.org/10.1093/hmg/ddg271
  • Faber PW, Voisine C, King DC, Bates EA, Hart AC. Glutamine/proline-rich PQE-1 proteins protect Caenorhabditis elegans neurons from huntingtin polyglutamine neurotoxicity. Proc Natl Acad Sci USA 2002; 99:17131-6; PMID:12486229; http://dx.doi.org/10.1073/pnas.262544899
  • Meriin AB, Zhang X, He X, Newnam GP, Chernoff YO, Sherman MY. Huntington toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J Cell Biol 2002; 157:997-1004; PMID:12058016; http://dx.doi.org/10.1083/jcb.200112104
  • Hughes RE, Lo RS, Davis C, Strand AD, Neal CL, Olson JM, Fields S. Altered transcription in yeast expressing expanded polyglutamine. Proc Natl Acad Sci USA 2001; 98:13201-6; PMID:11687606; http://dx.doi.org/10.1073/pnas.191498198
  • Kryndushkin DS, Alexandrov IM, Ter-Avanesyan MD, Kushnirov VV. Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J Biol Chem 2003; 278:49636-43; PMID:14507919; http://dx.doi.org/10.1074/jbc.M307996200
  • Mitkevich OV, Kochneva-Pervukhova NV, Surina ER, Benevolensky SV, Kushnirov VV, Ter-Avanesyan MD. DNA aptamers detecting generic amyloid epitopes. Prion 2012; 6:400-6; PMID:22874671; http://dx.doi.org/10.4161/pri.20678
  • Gokhale KC, Newnam GP, Sherman MY, Chernoff YO. Modulation of prion-dependent polyglutamine aggregation and toxicity by chaperone proteins in the yeast model. J Biol Chem 2005; 280:22809-18; PMID:15824100; http://dx.doi.org/10.1074/jbc.M500390200
  • O'Nuallain B, Williams AD, Westermark P, Wetzel R. Seeding specificity in amyloid growth induced by heterologous fibrils. J Biol Chem 2004; 279:17490-9; http://dx.doi.org/10.1074/jbc.M311300200
  • Krebs MRH, Morozova-Roche LA, Daniel K, Robinson CV. Dobson CM. Observation of sequence specificity in the seeding of protein amyloid fibrils. Protein Sci 2004; 13:1933-8; PMID:15215533; http://dx.doi.org/10.1110/ps.04707004
  • Urakov VN, Vishnevskaya AB, Alexandrov IM, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD. Interdependence of amyloid formation in yeast: implications for polyglutamine disorders and biological functions. Prion 2010; 4:45-52; PMID:20118659; http://dx.doi.org/10.4161/pri.4.1.11074
  • Tauber E, Miller-Fleming L, Mason RP, Kwan W, Clapp J, Butler NJ, Outeiro TF, Muchowski PJ, Giorgini F. Functional gene expression profiling in yeast implicates translational dysfunction in mutant huntingtin toxicity. J Biol Chem 2011; 286:410-9; PMID:21044956; http://dx.doi.org/10.1074/jbc.M110.101527
  • Meriin AB, Zhang X, Alexandrov IM, Salnikova AB, Ter-Avanesian MD, Chernoff YO, Sherman MY. Endocytosis machinery is involved in aggregation of proteins with expanded polyglutamine domains. FASEB J 2007; 21:1915-25; PMID:17341688; http://dx.doi.org/10.1096/fj.06-6878com
  • Duennwald ML, Lindquist S. Impaired ERAD and ER stress are early and specific events in polyglutamine toxicity. Genes Dev 2008; 22:3308-19; PMID:19015277; http://dx.doi.org/10.1101/gad.1673408
  • Bocharova NA, Sokolov SS, Knorre DA, Skulachev VP, Severin FF. Unexpected link between anaphase promoting complex and the toxicity of expanded polyglutamines expressed in yeast. Cell Cycle 2008; 7:3943-6; PMID:19066445; http://dx.doi.org/10.4161/cc.7.24.7398
  • Kochneva-Pervukhova NV, Alexandrov AI, Ter-Avanesyan MD. Amyloid-mediated sequestration of essential proteins contributes to mutant huntingtin toxicity in yeast. PLoS One 2012; 7:e29832; PMID:22253794; http://dx.doi.org/10.1371/journal.pone.0029832
  • Papsdorf K, Kaiser CJO, Drazic A, Grötzinger SW, Haeßner C, Eisenreich W, Richter K. Polyglutamine toxicity in yeast induces metabolic alterations and mitochondrial defects. BMC Genomics 2015; 16:662; PMID:26335097; http://dx.doi.org/10.1186/s12864-015-1831-7
  • Kryndushkin D, Pripuzova N, Burnett BG, Shewmaker F. Non-targeted identification of prions and amyloid-forming proteins from yeast and mammalian cells. J Biol Chem 2013; 288:27100-11; PMID:23926098; http://dx.doi.org/10.1074/jbc.M113.485359
  • Nizhnikov AA, Alexandrov AI, Ryzhova TA, Mitkevich OV, Dergalev AA, Ter-Avanesyan MD, Galkin AP. Proteomic screening for amyloid proteins. PLoS One 2014; 9:e116003; PMID:25549323; http://dx.doi.org/10.1371/journal.pone.0116003
  • Zhao X, Park Y-N, Todor H, Moomau C, Masison D, Eisenberg E, Greene LE. Sequestration of Sup35 by aggregates of huntingtin fragments causes toxicity of [PSI+] yeast. J Biol Chem 2012; 287:23346-55; PMID:22573320; http://dx.doi.org/10.1074/jbc.M111.287748
  • Perez MK, Paulson HL, Pendse SJ, Saionz SJ, Bonini NM, Pittman RN. Recruitment and the role of nuclear localization in polyglutamine-mediated aggregation. J Cell Biol 1998; 143:1457-70; PMID:9852144; http://dx.doi.org/10.1083/jcb.143.6.1457
  • Kazantsev A, Preisinger E, Dranovsky A, Goldgaber D, Housman D. Insoluble detergent-resistant aggregates form between pathological and nonpathological lengths of polyglutamine in mammalian cells. Proc Natl Acad Sci U S A 1999; 96:11404-9; PMID:10500189; http://dx.doi.org/10.1073/pnas.96.20.11404
  • Nucifora FC, Sasaki M, Peters MF, Huang H, Cooper JK, Yamada M, Takahashi H, Tsuji S, Troncoso J, Dawson VL, et al. Interference by huntingtin and atrophin-1 with CBP-mediated transcription leading to cellular toxicity. Science 2001; 291:2423-8; PMID:11264541; http://dx.doi.org/10.1126/science.1056784
  • Duennwald ML, Jagadish S, Giorgini F, Muchowski PJ, Lindquist S. A network of protein interactions determines polyglutamine toxicity. Proc Natl Acad Sci U S A 2006; 103:11051-6; PMID:16832049; http://dx.doi.org/10.1073/pnas.0604548103
  • Busch A, Engemann S, Lurz R, Okazawa H, Lehrach H, Wanker EE. Mutant huntingtin promotes the fibrillogenesis of wild-type huntingtin: a potential mechanism for loss of huntingtin function in Huntington's disease. J Biol Chem 2003; 278:41452-61; PMID:12888569; http://dx.doi.org/10.1074/jbc.M303354200
  • Serpionov GV, Alexandrov AI, Antonenko YN, Ter-Avanesyan MD. A protein polymerization cascade mediates toxicity of non-pathological human huntingtin in yeast. Sci Rep 2015; 5:18407; PMID:26673834; http://dx.doi.org/10.1038/srep18407
  • Yamanaka T, Miyazaki H, Oyama F, Kurosawa M, Washizu C, Doi H, Nukina N. Mutant Huntingtin reduces HSP70 expression through the sequestration of NF-Y transcription factor. EMBO J 2008; 27:827-39; PMID:18288205; http://dx.doi.org/10.1038/emboj.2008.23
  • Mitsui K, Doi H, Nukina N. Proteomics of polyglutamine aggregates. Methods Enzymol 2006; 412:63-76; PMID:17046652; http://dx.doi.org/10.1016/S0076-6879(06)12005-4
  • Wear MP, Kryndushkin D, O'Meally R, Sonnenberg JL, Cole RN, Shewmaker FP. Proteins with intrinsically disordered domains are preferentially recruited to polyglutamine aggregates. PLoS One 2015; 10:e0136362; PMID:26317359; http://dx.doi.org/10.1371/journal.pone.0136362
  • Paradisi I, Hernández A, Arias S. Huntington disease mutation in Venezuela: age of onset, haplotype analyses and geographic aggregation. J Hum Genet 2008; 53:127-35; PMID:18157708; http://dx.doi.org/10.1007/s10038-007-0227-1
  • The U.S.-Venezuela Collaborative Research Project, Wexler NS, Lorimer J, Porter J, Gomez F, Moskowitz C, Shackell E, Marder K, Penchaszadeh G, Roberts SA, et al. Venezuelan kindreds reveal that genetic and environmental factors modulate Huntington's disease age of onset. Proc Natl Acad Sci USA 2004; 101:3498-503; PMID:14993615; http://dx.doi.org/10.1073/pnas.0308679101
  • Djoussé L, Knowlton B, Hayden M, Almqvist EW, Brinkman R, Ross C, Margolis R, Rosenblatt A, Durr A, Dode C, et al. Interaction of normal and expanded CAG repeat sizes influences age at onset of Huntington disease. Am J Med Genet A 2003; 119A:279-82; http://dx.doi.org/10.1002/ajmg.a.20190
  • Aziz NA, Jurgens CK, Landwehrmeyer GB, van Roon-Mom WMC, van Ommen GJB, Stijnen T, Roos RAC. Normal and mutant HTT interact to affect clinical severity and progression in Huntington disease. Neurology 2009; 73:1280-5; PMID:19776381; http://dx.doi.org/10.1212/WNL.0b013e3181bd1121
  • França MC, Emmel VE, D'Abreu A, Maurer-Morelli CV. Secolin R, Bonadia LC, da Silva MS, Nucci A, Jardim LB, Saraiva-Pereira ML, et al. Normal ATXN3 allele but not CHIP polymorphisms modulates age at onset in Machado–Joseph disease. Front Neurol 2012; 3:164.
  • Slepko N, Bhattacharyya AM, Jackson GR, Steffan JS, Marsh JL, Thompson LM, Wetzel R. Normal-repeat-length polyglutamine peptides accelerate aggregation nucleation and cytotoxicity of expanded polyglutamine proteins. Proc Natl Acad Sci USA 2006; 103:14367-72; PMID:16980414; http://dx.doi.org/10.1073/pnas.0602348103
  • Saleh AA, Bhadra AK, Roy I. Cytotoxicity of mutant huntingtin fragment in yeast can be modulated by the expression level of wild type huntingtin fragment. ACS Chem Neurosci 2014; 5:205-15; PMID:24377263; http://dx.doi.org/10.1021/cn400171d
  • Jardim L, Silveira I, Pereira ML, do Ceu Moreira M, Mendonca P, Sequeiros J, Giugliani R. Searching for modulating effects of SCA2, SCA6 and DRPLA CAG tracts on the Machado-Joseph disease (SCA3) phenotype. Acta Neurol Scand 2003; 107:211-4; PMID:12614315; http://dx.doi.org/10.1034/j.1600-0404.2003.00046.x
  • Pulst S-M, Santos N, Wang D, Yang H, Huynh D, Velazquez L, Figueroa KP. Spinocerebellar ataxia type 2: polyQ repeat variation in the CACNA1A calcium channel modifies age of onset. Brain 2005; 128:2297-303; PMID:16000334; http://dx.doi.org/10.1093/brain/awh586
  • de Castilhos RM, Furtado GV, Gheno TC, Schaeffer P, Russo A, Barsottini O, Pedroso JL, Salarini DZ, Vargas FR, de Lima MADFD, et al. Spinocerebellar ataxias in Brazil–frequencies and modulating effects of related genes. Cerebellum 2014; 13:17-28; PMID:23943520; http://dx.doi.org/10.1007/s12311-013-0510-y
  • Du Montcel ST, Durr A, Bauer P, Figueroa KP, Ichikawa Y, Brussino A, Forlani S, Rakowicz M, Schöls L, Mariotti C, et al. Modulation of the age at onset in spinocerebellar ataxia by CAG tracts in various genes. Brain 2014; 137:2444-55; PMID:24972706; http://dx.doi.org/10.1093/brain/awu174
  • Lessing D, Bonini NM. Polyglutamine genes interact to modulate the severity and progression of neurodegeneration in drosophila. PLoS Biol 2008; 6:e29; PMID:18271626; http://dx.doi.org/10.1371/journal.pbio.0060029
  • Uchihara T, Fujigasaki H, Koyano S, Nakamura A, Yagishita S, Iwabuchi K. Non-expanded polyglutamine proteins in intranuclear inclusions of hereditary ataxias–triple-labeling immunofluorescence study. Acta Neuropathol 2001; 102:149-52; PMID:11563629
  • Elden AC, Kim H-J, Hart MP, Chen-Plotkin AS, Johnson BS, Fang X, Armakola M, Geser F, Greene R, Lu MM, et al. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 2010; 466:1069-75; PMID:20740007; http://dx.doi.org/10.1038/nature09320
  • Bonini NM, Gitler AD. Model organisms reveal insight into human neurodegenerative disease: ataxin-2 intermediate-length polyglutamine expansions are a risk factor for ALS. J Mol Neurosci 2011; 45:676-83; PMID:21660502; http://dx.doi.org/10.1007/s12031-011-9548-9
  • Farg MA, Soo KY, Warraich ST, Sundaramoorthy V, Blair IP, Atkin JD. Ataxin-2 interacts with FUS and intermediate-length polyglutamine expansions enhance FUS-related pathology in amyotrophic lateral sclerosis. Hum Mol Genet 2013; 22:717-28; PMID:23172909; http://dx.doi.org/10.1093/hmg/dds479
  • Kayatekin C, Matlack KES, Hesse WR, Guan Y, Chakrabortee S, Russ J, Wanker EE, Shah J V, Lindquist S. Prion-like proteins sequester and suppress the toxicity of huntingtin exon 1. Proc Natl Acad Sci U S A 2014; 111:12085-90; PMID:25092318; http://dx.doi.org/10.1073/pnas.1412504111
  • Kim J-M, Hong S, Kim GP, Choi YJ, Kim YK, Park SS, Kim SE, Jeon BS. Importance of low-Range CAG expansion and CAA interruption in SCA2 Parkinsonism. Arch Neurol 2007; 64:1510; PMID:17923635; http://dx.doi.org/10.1001/archneur.64.10.1510
  • Yamashita C, Tomiyama H, Funayama M, Inamizu S, Ando M, Li Y, Yoshino H, Araki T, Ichikawa T, Ehara Y, et al. The evaluation of polyglutamine repeats in autosomal dominant Parkinson's disease. Neurobiol Aging 2014; 35:1779.e17-1779.e21; PMID:24534762; http://dx.doi.org/10.1016/j.neurobiolaging.2014.01.022
  • Gratuze M, Cisbani G, Cicchetti F, Planel E. Is Huntington's disease a tauopathy? Brain 2016; 139:1014-25; PMID:26969684; http://dx.doi.org/10.1093/brain/aww021
  • Jellinger KA. Interaction between pathogenic proteins in neurodegenerative disorders. J Cell Mol Med 2012; 16:1166-83; PMID:22176890; http://dx.doi.org/10.1111/j.1582-4934.2011.01507.x
  • Gotz J. Formation of neurofibrillary tangles in p301l Tau transgenic mice induced by Abeta 42 fibrils. Science 2001; 293:1491-5; PMID:11520988; http://dx.doi.org/10.1126/science.1062097
  • Arslan F, Hong JY, Kanneganti V, Park S-K, Liebman SW. Heterologous aggregates promote de novo prion appearance via more than one mechanism. PLoS Genet 2015; 11:e1004814; PMID:25568955; http://dx.doi.org/10.1371/journal.pgen.1004814

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.