Triplet repeat-derived siRNAs enhance RNA-mediated toxicity in a drosophila model for myotonic dystrophy

PLoS Genetics

Volumn 7, Issue 3, 2011, Pages

  Yu, Zhenming ^a   Teng, Xiuyin ^a   Bonini, Nancy M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; CELL CYCLE PROTEIN; PROTEIN DCR2; RNA; SMALL INTERFERING RNA; TATA BINDING PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAG REPEAT; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE TARGETING; MYOTONIC DYSTROPHY; NEUROPATHOLOGY; NONHUMAN; TOXICITY TESTING; TRINUCLEOTIDE REPEAT; ANIMAL; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; MALE; METABOLISM; MUTATION; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION; MALE; MUTATION; MYOTONIC DYSTROPHY; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; TRINUCLEOTIDE REPEAT EXPANSION; TRINUCLEOTIDE REPEATS;

EID: 79953762028     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001340     Document Type: Article

References (56)

1. Ranum LP, Cooper TA, (2006) RNA-mediated neuromuscular disorders. Annu Rev Neurosci 29: 259-277.
2. Orr HT, Zoghbi HY, (2007) Trinucleotide Repeat Disorders. Annu Rev Neurosci.
3. Li LB, Bonini NM, (2010) Roles of trinucleotide-repeat RNA in neurological disease and degeneration. Trends Neurosci 33: 292-298.
4. Brook JD, McCurrach ME, Harley HG, Buckler AJ, Church D, et al. (1992) Molecular basis of myotonic dystrophy: Expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell 68: 799-808.
5. Fu YH, Pizzuti A, Fenwick RG, King J, Rajnarayan S, et al. (1992) An unstable triplet repeat in a gene related to myotonic muscular-dystrophy. Science 255: 1256-1258.
6. Philips AV, Timchenko LT, Cooper TA, (1998) Disruption of Splicing Regulated by a CUG-Binding Protein in Myotonic Dystrophy. Science 280: 737-741.
7. Savkur RS, Philips AV, Cooper TA, (2001) Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat Genet 29: 40-47.
8. Mankodi A, Takahashi MP, Jiang H, Beck CL, Bowers WJ, et al. (2002) Expanded CUG repeats trigger aberrant splicing of ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol Cell 10: 35-44.
9. Rudnicki DD, Holmes SE, Lin MW, Thornton CA, Ross CA, et al. (2007) Huntington's disease-like 2 is associated with CUG repeat-containing RNA foci. Ann Neurol 61: 272-282.
10. Daughters RS, Tuttle DL, Gao W, Ikeda Y, Moseley ML, et al. (2009) RNA gain-of-function in spinocerebellar ataxia type 8. PLoS Genet 5: e1000600 doi:10.1371/journal.pgen.1000600.
11. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, et al. (2005) Antisense transcription in the mammalian transcriptome. Science 309: 1564-1566.
12. Batra R, Charizanis K, Swanson MS, (2010) Partners in crime: bidirectional transcription in unstable microsatellite disease. Hum Mol Genet 19: R77-82.
13. Ladd PD, Smith LE, Rabaia NA, Moore JM, Georges SA, et al. (2007) An antisense transcript spanning the CGG repeat region of FMR1 is upregulated in premutation carriers but silenced in full mutation individuals. Hum Mol Genet 16: 3174-3187.
14. Moseley ML, Zu T, Ikeda Y, Gao W, Mosemiller AK, et al. (2006) Bidirectional expression of CUG and CAG expansion transcripts and intranuclear polyglutamine inclusions in spinocerebellar ataxia type 8. Nat Genet 38: 758-769.
15. Cho DH, Thienes CP, Mahoney SE, Analau E, Filippova GN, et al. (2005) Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol Cell 20: 483-489.
16. Dion V, Wilson JH, (2009) Instability and chromatin structure of expanded trinucleotide repeats. Trends Genet 25: 288-297.
17. Ge X, Wu Q, Jung Y-C, Chen J, Wang SM, (2006) A large quantity of novel human antisense transcripts detected by LongSAGE. Bioinformatics 22: 2475-2479.
18. He Y, Vogelstein B, Velculescu VE, Papadopoulos N, Kinzler KW, (2008) The antisense transcriptomes of human cells. Science 322: 1855-1857.
19. Zoghbi HY, Botas J, (2002) Mouse and fly models of neurodegeneration. Trends Genet 18: 463-471.
20. Marsh JL, Thompson LM, (2006) Drosophila in the study of neurodegenerative disease. Neuron 52: 169-178.
21. Cauchi RJ, van den Heuvel M, (2006) The fly as a model for neurodegenerative diseases: is it worth the jump? Neurodegener Dis 3: 338-356.
22. Bilen J, Bonini NM, (2005) Drosophila as a model for human neurodegenerative disease. Annu Rev Genet 39: 153-171.
23. Houseley JM, Wang Z, Brock GJR, Soloway J, Artero R, et al. (2005) Myotonic dystrophy associated expanded CUG repeat muscleblind positive ribonuclear foci are not toxic to Drosophila. Human Molecular Genetics 14: 873-883.
24. de Haro M, Al-Ramahi I, De Gouyon B, Ukani L, Rosa A, et al. (2006) MBNL1 and CUGBP1 modify expanded CUG-induced toxicity in a Drosophila model of myotonic dystrophy type 1. Human Molecular Genetics 15: 2138-2145.
25. Garcia-Lopez A, Monferrer L, Garcia-Alcover I, Vicente-Crespo M, Alvarez-Abril MC, et al. (2008) Genetic and chemical modifiers of a CUG toxicity model in Drosophila. PLoS ONE 3: e1595 doi:10.1371/journal.pone.0001595.
26. Li LB, Yu Z, Teng X, Bonini NM, (2008) RNA toxicity is a component of ataxin-3 degeneration in Drosophila. Nature 453: 1107-1111.
27. Lee YS, Nakahara K, Pham JW, Kim K, He Z, et al. (2004) Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117: 69-81.
28. Horwich MD, Li C, Matranga C, Vagin V, Farley G, et al. (2007) The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr Biol 17: 1265-1272.
29. Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, et al. (2008) An endogenous small interfering RNA pathway in Drosophila. Nature 453: 798-802.
30. Mutsuddi M, Marshall CM, Benzow KA, Koob MD, Rebay I, (2004) The spinocerebellar ataxia 8 noncoding RNA causes neurodegeneration and associates with staufen in Drosophila. Curr Biol 14: 302-308.
31. Sofola OA, Jin P, Botas J, Nelson DL, (2007) Argonaute-2-dependent rescue of a Drosophila model of FXTAS by FRAXE premutation repeat. Hum Mol Genet 16: 2326-2332.
32. Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, et al. (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115: 199-208.
33. Khvorova A, Reynolds A, Jayasena SD, (2003) Functional siRNAs and miRNAs exhibit strand bias. Cell 115: 209-216.
34. Hutvagner G, (2005) Small RNA asymmetry in RNAi: function in RISC assembly and gene regulation. FEBS Lett 579: 5850-5857.
35. Pei Y, Tuschl T, (2006) On the art of identifying effective and specific siRNAs. Nat Methods 3: 670-676.
36. Miller JW, Urbinati CR, Teng-Umnuay P, Stenberg MG, Byrne BJ, et al. (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. Embo J 19: 4439-4448.
37. Timchenko LT, Miller JW, Timchenko NA, DeVore DR, Datar KV, et al. (1996) Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucleic Acids Res 24: 4407-4414.
38. Tian B, White RJ, Xia T, Welle S, Turner DH, et al. (2000) Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR. Rna 6: 79-87.
39. Ho TH, Savkur RS, Poulos MG, Mancini MA, Swanson MS, et al. (2005) Colocalization of muscleblind with RNA foci is separable from mis-regulation of alternative splicing in myotonic dystrophy. J Cell Sci 118: 2923-2933.
40. Jasinska A, Michlewski G, de Mezer M, Sobczak K, Kozlowski P, et al. (2003) Structures of trinucleotide repeats in human transcripts and their functional implications. Nucleic Acids Res 31: 5463-5468.
41. Ma Y, Creanga A, Lum L, Beachy PA, (2006) Prevalence of off-target effects in Drosophila RNA interference screens. Nature 443: 359-363.
42. Lim J, Crespo-Barreto J, Jafar-Nejad P, Bowman AB, Richman R, et al. (2008) Opposing effects of polyglutamine expansion on native protein complexes contribute to SCA1. Nature 452: 713-718.
43. Thomas PS Jr, Fraley GS, Damian V, Woodke LB, Zapata F, et al. (2006) Loss of endogenous androgen receptor protein accelerates motor neuron degeneration and accentuates androgen insensitivity in a mouse model of X-linked spinal and bulbar muscular atrophy. Hum Mol Genet 15: 2225-2238.
44. Kawaji H, Nakamura M, Takahashi Y, Sandelin A, Katayama S, et al. (2008) Hidden layers of human small RNAs. BMC Genomics 9: 157.
45. Yang N, Kazazian HH Jr, (2006) L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 13: 763-771.
46. Ui-Tei K, Zenno S, Miyata Y, Saigo K, (2000) Sensitive assay of RNA interference in Drosophila and Chinese hamster cultured cells using firefly luciferase gene as target. FEBS Lett 479: 79-82.
47. Caplen NJ, Fleenor J, Fire A, Morgan RA, (2000) dsRNA-mediated gene silencing in cultured Drosophila cells: a tissue culture model for the analysis of RNA interference. Gene 252: 95-105.
48. Nakamura K, Jeong SY, Uchihara T, Anno M, Nagashima K, et al. (2001) SCA17, a novel autosomal dominant cerebellar ataxia caused by an expanded polyglutamine in TATA-binding protein. Hum Mol Genet 10: 1441-1448.
49. Freiman RN, Tjian R, (2002) Neurodegeneration. A glutamine-rich trail leads to transcription factors. Science 296: 2149-2150.
50. Riley BE, Orr HT, (2006) Polyglutamine neurodegenerative diseases and regulation of transcription: assembling the puzzle. Genes Dev 20: 2183-2192.
51. Krol J, Fiszer A, Mykowska A, Sobczak K, de Mezer M, et al. (2007) Ribonuclease dicer cleaves triplet repeat hairpins into shorter repeats that silence specific targets. Mol Cell 25: 575-586.
52. Okamura K, Ishizuka A, Siomi H, Siomi MC, (2004) Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev 18: 1655-1666.
53. Saito K, Sakaguchi Y, Suzuki T, Suzuki T, Siomi H, et al. (2007) Pimet, the Drosophila homolog of HEN1, mediates 2′-O-methylation of Piwi- interacting RNAs at their 3′ ends. Genes Dev 21: 1603-1608.
54. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
55. Cooper TA, (2005) Use of minigene systems to dissect alternative splicing elements. Methods 37: 331-340.
56. Koob MD, Moseley ML, Schut LJ, Benzow KA, Bird TD, et al. (1999) An untranslated CTG expansion causes a novel form of spinocerebellar ataxia (SCA8). Nature Genetics 21: 379-384.