A protein polymerization cascade mediates toxicity of non-pathological human huntingtin in yeast

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Serpionov, Genrikh V ^a   Alexandrov, Alexander I ^a   Antonenko, Yuri N ^b   Ter Avanesyan, Michael D ^a  

^a BACH INSTITUTE OF BIOCHEMISTRY   (Russian Federation)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; GREEN FLUORESCENT PROTEIN; HTT PROTEIN, HUMAN; HUNTINGTIN; PEPTIDE; POLYGLUTAMINE; PRION PROTEIN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

CHEMISTRY; FLUORESCENCE MICROSCOPY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; HUNTINGTON CHOREA; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERIZATION; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE; SPECTROFLUOROMETRY; TRINUCLEOTIDE REPEAT;

AMYLOID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GREEN FLUORESCENT PROTEINS; HUMANS; HUNTINGTIN PROTEIN; HUNTINGTON DISEASE; MICROSCOPY, FLUORESCENCE; PEPTIDES; POLYMERIZATION; PRION PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECTROMETRY, FLUORESCENCE; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84950327520     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep18407     Document Type: Article

References (61)

1. The Huntington's disease collaborative research group. A novel gene containing a trinucleotide repeats that is expanded and unstable on Huntington's disease chromosomes. Cell 72, 971-983 (1993).
2. Bates, G. Huntingtin aggregation and toxicity in Huntington's disease. Lancet 361, 1642-1644 (2003).
3. Ross, C. A. & Tabrizi, S. J. Huntington's disease: From molecular pathogenesis to clinical treatment. Lancet Neurol 10, 83-98 (2011).
4. Roizin, L., Stellar, S. & Liu, J. C. Neuronal nuclear-cytoplasmic changes in Huntington's chorea: Electron microscope investigations. Adv Neurol 23, 95-122 (1979).
5. DiFiglia, M. et al. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277, 1990-1993 (1997).
6. Davies, S. W. et al. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90, 537-548 (1997).
7. Takahashi, T., Katada, S. & Onodera O. Polyglutamine Diseases: Where does toxicity come from? What is toxicity? Where are we going? J Mol Cell Biol 2, 180-191 (2010).
8. Meriin, A. B. et al. Huntingtin toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J Cell Biol 157, 997-1004 (2002).
9. Faber, P. W., Voisine, C., King, D. C., Bates, E. A. & Hart, A. C. Glutamine/proline-rich PQE-1 proteins protect Caenorhabditis elegans neurons from huntingtin polyglutamine neurotoxicity. Proc Natl Acad Sci USA 99, 17131-17136 (2002).
10. Weiss, K. R., Kimura, Y., Lee, W. C. & Littleton, J. T. Huntingtin aggregation kinetics and their pathological role in a Drosophila Huntington's disease model. Genetics 190, 581-600 (2012).
11. Davies, S. W. et al. Detection of polyglutamine aggregation in mouse models. Methods Enzymol 309, 687-701 (1999).
12. Landles, C. et al. Proteolysis of mutant huntingtin produces an exon 1 fragment that accumulates as an aggregated protein in neuronal nuclei in Huntington disease. J Biol Chem 285, 8808-8823 (2010).
13. Hughes, R. E. et al. Altered transcription in yeast expressing expanded polyglutamine. Proc Natl Acad Sci USA 98, 13201-13206 (2001).
14. Duennwald, M. L., Jagadish, S., Muchowski, P. L. & Lindquist, S. Flanking sequences profoundly alter polyglutamine toxicity in yeast. Proc Natl Acad Sci USA 103, 11045-11050 (2006).
15. Giorgini, F., Guidetti, P., Nguyen, Q., Bennett, S. C. & Muchowski, P. J. A genomic screen in yeast implicates kynurenine 3-monooxygenase as a therapeutic target for Huntington disease. Nat Genet 37, 526-531 (2005).
16. Duennwald, M. L., Jagadish, S., Giogini, F., Muchowski, P. L. & Lindquist, S. A network of protein interactions determines polyglutamine toxicity. Proc Natl Acad Sci USA 103, 11051-11056 (2006).
17. Wolfe, K. J., Ren, H. Y., Trepte, P. & Cyr, D. M. Polyglutamine-rich suppressors of huntingtin toxicity act upstream of Hsp70 and Sti1 in spatial quality control of amyloid-like proteins. PLoS One 9, e95914 (2014).
18. Kayatekin, C. et al. Prion-like proteins sequester and suppress the toxicity of huntingtin exon 1. Proc Natl Acad Sci USA 111, 12085-12090 (2014).
19. Meriin, A. B. et al. Aggregation of expanded polyglutamine domain in yeast leads to defects in endocytosis. Mol Cell Biol 23, 7554-7565 (2003).
20. Kochneva-Pervukhova, N. V., Alexandrov, A. I. & Ter-Avanesyan, M. D. Amyloid-mediated sequestration of essential proteins contributes to mutant huntingtin toxicity in yeast. PLoS One 7, e29832 (2012).
21. Duennwald, M. L. & Lindquist, S., Impaired ERAD and ER stress are early and specific events in polyglutamine toxicity. Genes Dev 22, 3308-3319 (2008).
22. Bocharova, N. A., Sokolov, S. S., Knorre, D. A., Skulachev, V. P. & Severin, F. F. Unexpected link between anaphase promoting complex and the toxicity of expanded polyglutamines expressed in yeast. Cell Cycle 7, 3943-2946 (2008).
23. Gong, H. et al. Polyglutamine toxicity is controlled by prion composition and gene dosage in yeast. PLoS Genet 8, e1002634 (2012).
24. Zhao, X. et al. Sequestration of Sup35 by aggregates of huntingtin fragments causes toxicity of [PSI+] yeast. J Biol Chem 287, 23346-23355 (2012).
25. Djoussé, L. et al. Interaction of normal and expanded CAG repeat sizes influences age at onset of Huntington disease. Am J Med Genet A 119A 279-282 (2003).
26. Aziz, N. A. et al. Normal and mutant HTT interact to affect clinical severity and progression in Huntington disease. Neurology 73, 1280-1285 (2009).
27. Busch, A. et al. Mutant huntingtin promotes the fibrillogenesis of wild-type huntingtin: A potential mechanism for loss of huntingtin function in Huntington's disease. J Biol Chem 278, 41452-41461 (2003).
28. Alexandrov, A. I., Polyanskaya, A. B., Serpionov, G. V., Ter-Avanesyan, M. D. & Kushnirov, V. V. The effects of amino acid composition of glutamine-rich domains on amyloid formation and fragmentation. PLoS One 7, e46458 (2012).
29. Kryndushkin, D. S., Alexandrov, I. M., Ter-Avanesyan, M. D. & Kushnirov, V. V. Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J Biol Chem 278, 49636-49643 (2003).
30. Mitsui, K., Doi, H. & Nukina, N. Proteomics of polyglutamine aggregates. Methods Enzymol 412, 63-76 (2006).
31. Mitkevich, O. V. et al. DNA aptamers detecting generic amyloid epitopes. Prion 6, 400-406 (2012).
32. Perez, M. K. et al. Recruitment and the role of nuclear localization in polyglutamine-mediated aggregation. J Cell Biol 143, 1457-1470 (1998).
33. 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 USA 96, 11404-11409 (1999).
34. Steffan, J. S. et al. The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci USA 97, 6763-6768 (2000).
35. Shimohata, T. et al. Expanded polyglutamine stretches interact with TAFII130, interfering with CREB-dependent transcription. Nature Genet 26, 29-36 (2000).
36. Nucifora, F. C. Jr. et al. Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291, 2423-2428 (2001).
37. Alexandrov, I. M., Vishnevskaya, A. B., Ter-Avanesyan, M. D. & Kushnirov, V. V. Appearance and propagation of polyglutamine-based amyloids in yeast: Tyrosine residues enable polymer fragmentation. J Biol Chem 283, 15185-15192 (2008).
38. Elson, E. L. Fluorescence correlation spectroscopy: Past, present, future. Biophys J 101, 2855-2870 (2011).
39. Kawai-Noma, S. et al. In vivo evidence for the fibrillar structures of Sup35 prions in yeast cells. J Cell Biol 190, 223-231 (2010).
40. Kawai-Noma, S. et al. Dynamics of yeast prion aggregates in single living cells. Genes Cells 11, 1085-1096 (2006).
41. Urakov, V. N. et al. Interdependence of amyloid formation in yeast: Implications for polyglutamine disorders and biological functions. Prion 4, 45-52 (2010).
42. Gokhale, K. C., Newnam, G. P., Sherman, M. Y. & Chernoff, Y. O. Modulation of prion-dependent polyglutamine aggregation and toxicity by chaperone proteins in the yeast model. J Biol Chem 280, 22809-22818 (2005).
43. McGlinchey, R. P., Kryndushkin, D. & Wickner, R. B. Suicidal [PSI+] is a lethal yeast prion. Proc Natl Acad Sci USA 108, 5337-5341 (2011).
44. Derkatch, I. L. et al. Effects of Q/N-rich, polyQ, and non-polyQ amyloids on the de novo formation of the [PSI+] prion in yeast and aggregation of Sup35 in vitro. Proc Natl Acad Sci USA 101, 12934-12939 (2004).
45. Nizhnikov, A. A. et al. Proteomic screening for amyloid proteins. PLoS One 9, e116003 (2014).
46. Wear, M. P. et al. Proteins with intrinsically disordered domains are preferentially recruited to polyglutamine aggregates. PLoS One 10, e0136362 (2015).
47. Wolfe, K. J., Ren, H. Y., Trepte, P. & Cyr, D. M. Polyglutamine-rich suppressors of huntingtin toxicity act upstream of Hsp70 and Sti1 in spatial quality control of amyloid-like proteins. PLoS One 9, e95914 (2014).
48. Kayatekin, C. et al. Prion-like proteins sequester and suppress the toxicity of huntingtin exon 1. Proc Natl Acad Sci USA, 111, 12085-90 (2014).
49. Salnikova, A. B., Kryndushkin, D. S., Smirnov, V. N., Kushnirov, V. V. & Ter-Avanesyan, M. D. Nonsense suppression in yeast cells overproducing Sup35 (eRF3) is caused by its non-heritable amyloids. J Biol Chem 280, 8808-8812 (2005).
50. Gietz, R. D. & Woods, R. A. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350, 87-96 (2002).
51. Urakov, V. N. et al. N-terminal region of Saccharomyces cerevisiae eRF3 is essential for the functioning of the eRF1/eRF3 complex beyond translation termination. BMC Mol Biol 7, 34 (2006).
52. Valouev, I. A., Urakov, V. N., Kochneva-Pervukhova, N. V., Smirnov, V. N. & Ter-Avanesyan, M. D. Translation termination factors function outside of translation: Yeast eRF1 interacts with myosin light chain, Mlc1p, to effect cytokinesis. Mol Microbiol 53, 687-696 (2004).
53. Chernoff, Y. O., Lindquist, S. L., Ono, B., Inge-Vechtomov, S. G. & Liebman, S. W. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 12, 268, 880-884 (1995).
54. Thomas, B. J. & Rothstein, R. Elevated recombination rates in transcriptionally active DNA. Cell 56, 619-630 (1989).
55. Kushnirov, V. V., Alexandrov, I. M., Mitkevich, O. V., Shkundina, I. S. & Ter-Avanesyan, M. D. Purification and analysis of prion and amyloid aggregates. Methods 39, 50-55 (2006).
56. Perevoshchikova, I. V., Zorov, D. B. & Antonenko, Y. N. Peak intensity analysis as a method for estimation of fluorescent probe binding to artificial and natural nanoparticles: Tetramethylrhodamine uptake by isolated mitochondria. Biochim Biophys Acta-Biomembranes 1778, 2182-2190 (2008).
57. Hess, S. T., Huang, S., Heikal, A. A. & Webb, W. W. Biological and chemical applications of fluorescence correlation spectroscopy: A review. Biochemistry 41, 697-705 (2002).
58. Haupts, U., Maiti, S., Schwille, P. & Webb, W. W. Dynamics of fluorescence fluctuations in green fluorescent protein observed by fluorescence correlation spectroscopy. Proc Natl Acad Sci USA 95, 13573-13578 (1998).
59. Agaphonov, M. & Alexandrov, A. Self-excising integrative yeast plasmid vectors containing an intronated recombinase gene. FEMS Yeast Res 14, 1048-1054 (2014).
60. Gietz, R. D. & Sugino, A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534 (1988).
61. Sikorski, R. S. & Hieter, P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27 (1989).