Muscleblind participates in RNA toxicity of expanded CAG and CUG repeats in Caenorhabditis elegans

Cellular and Molecular Life Sciences

Volumn 68, Issue 7, 2011, Pages 1255-1267

  Wang, Li Chun ^a   Chen, Kuan Yu ^b   Pan, Huichin ^a,c   Wu, Chia Chieh ^d   Chen, Po Hsuan ^d   Liao, Yuan Ting ^d   Li, Chin ^d   Huang, Min Lang ^d   Hsiao, Kuang Ming ^d  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL CHUNG CHENG UNIVERSITY   (Taiwan)

Author keywords

C. elegans; CAG and CUG repeats; Muscleblind; RNA toxicity; Sequestration

Indexed keywords

MUSCLEBLIND PROTEIN; REGULATOR PROTEIN; RNA; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CAG REPEAT; CONTROLLED STUDY; CUG REPEAT; DNA STRUCTURE; LIFESPAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UNTRANSLATED REGION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; HUMANS; PHENOTYPE; RNA; RNA INTERFERENCE; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC; TRINUCLEOTIDE REPEAT EXPANSION;

CAENORHABDITIS ELEGANS;

EID: 79953716235     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0522-4     Document Type: Article

References (60)

1. ML Moseley T Zu Y Ikeda W Gao AK Mosemiller RS Daughters G Chen MR Weatherspoon HB Clark TJ Ebner JW Day LP Ranum 2006 Bidirectional expression of CUG and CAG expansion transcripts and intranuclear polyglutamine inclusions in spinocerebellar ataxia type 8 Nat Genet 38 758 769 16804541 10.1038/ng1827 1:CAS:528:DC%2BD28XmtFyru7Y%3D (Pubitemid 43980596)
2. SE Holmes EE O'Hearn MG McInnis DA Gorelick-Feldman JJ Kleiderlein C Callahan NG Kwak RG Ingersoll-Ashworth M Sherr AJ Sumner AH Sharp U Ananth WK Seltzer MA Boss AM Vieria-Saecker JT Epplen O Riess CA Ross RL Margolis 1999 Expansion of a novel CAG trinucleotide repeat in the 5′ region of PPP2R2B is associated with SCA12 Nat Genet 23 391 392 10581021 10.1038/70493 1:STN:280:DC%2BD3c%2FkslOlsQ%3D%3D
3. SE Holmes E O'Hearn A Rosenblatt C Callahan HS Hwang RG Ingersoll-Ashworth A Fleisher G Stevanin A Brice NT Potter CA Ross RL Margolis 2001 A repeat expansion in the gene encoding junctophilin-3 is associated with Huntington disease-like 2 Nat Genet 29 377 378 11694876 10.1038/ng760 1:CAS:528:DC%2BD3MXovFalurc%3D (Pubitemid 34326684)
4. LP Ranum JW Day 2004 Pathogenic RNA repeats: an expanding role in genetic disease Trends Genet 20 506 512 15363905 10.1016/j.tig.2004.08.004 1:CAS:528:DC%2BD2cXnsFGntro%3D (Pubitemid 39201071)
5. RJ Osborne CA Thornton 2006 RNA-dominant diseases Hum Mol Genet 15 Spec No 2 R162 R169 16987879 10.1093/hmg/ddl181 1:CAS:528:DC%2BD28XpvFGls7o%3D (Pubitemid 44446789)
6. TM Wheeler CA Thornton 2007 Myotonic dystrophy: RNA-mediated muscle disease Curr Opin Neurol 20 572 576 17885447 10.1097/WCO.0b013e3282ef6064 1:CAS:528:DC%2BD2sXht1Kku7vO (Pubitemid 47462288)
7. G Michlewski WJ Krzyzosiak 2005 Pathogenesis of spinocerebellar ataxias viewed from the RNA perspective Cerebellum 4 19 24 15895554 10.1080/ 14734220510007905 1:CAS:528:DC%2BD2MXkvVemtbg%3D (Pubitemid 40592804)
8. LP Ranum TA Cooper 2006 RNA-mediated neuromuscular disorders Annu Rev Neurosci 29 259 277 16776586 10.1146/annurev.neuro.29.051605.113014 1:CAS:528:DC%2BD28XosVeitr0%3D (Pubitemid 44476846)
9. A Mankodi E Logigian L Callahan C McClain R White D Henderson M Krym CA Thornton 2000 Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat Science 289 1769 1773 10976074 10.1126/science.289.5485.1769 1:CAS:528:DC%2BD3cXmsV2rsLs%3D
10. H Seznec O Agbulut N Sergeant C Savouret A Ghestem N Tabti JC Willer L Ourth C Duros E Brisson C Fouquet G Butler-Browne A Delacourte C Junien G Gourdon 2001 Mice transgenic for the human myotonic dystrophy region with expanded CTG repeats display muscular and brain abnormalities Hum Mol Genet 10 2717 2726 11726559 10.1093/hmg/10.23.2717 1:CAS:528:DC%2BD3MXptFGhurY%3D (Pubitemid 33133413)
11. LT Timchenko JW Miller NA Timchenko DR DeVore KV Datar L Lin R Roberts CT Caskey MS Swanson 1996 Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy Nucleic Acids Res 24 4407 4414 8948631 10.1093/nar/24.22.4407 1:CAS:528:DyaK28Xnt12ktbc%3D (Pubitemid 26388627)
12. JW Miller CR Urbinati P Teng-Umnuay MG Stenberg BJ Byrne CA Thornton MS Swanson 2000 Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy EMBO J 19 4439 4448 10970838 10.1093/emboj/19.17.4439 1:CAS:528:DC%2BD3cXmslGktbk%3D
13. AV Philips LT Timchenko TA Cooper 1998 Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy Science 280 737 741 9563950 10.1126/science.280.5364.737 1:CAS:528:DyaK1cXjtVOktLk%3D (Pubitemid 28243348)
14. RN Kanadia KA Johnstone A Mankodi C Lungu CA Thornton D Esson AM Timmers WW Hauswirth MS Swanson 2003 A muscleblind knockout model for myotonic dystrophy Science 302 1978 1980 14671308 10.1126/science.1088583 1:CAS:528: DC%2BD3sXps1amsLo%3D (Pubitemid 37523508)
15. TH Ho BN Charlet MG Poulos G Singh MS Swanson TA Cooper 2004 Muscleblind proteins regulate alternative splicing EMBO J 23 3103 3112 15257297 10.1038/sj.emboj.7600300 1:CAS:528:DC%2BD2cXmt1Wqu7w%3D (Pubitemid 39093604)
16. NA Timchenko ZJ Cai AL Welm S Reddy T Ashizawa LT Timchenko 2001 RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1 J Biol Chem 276 7820 7826 11124939 10.1074/jbc.M005960200 1:CAS:528: DC%2BD3MXitFKhtbg%3D
17. NM Kuyumcu-Martinez GS Wang TA Cooper 2007 Increased steady-state levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mediated hyperphosphorylation Mol Cell 28 68 78 17936705 10.1016/j.molcel.2007.07.027 1:CAS:528: DC%2BD2sXht1Kmsr%2FF (Pubitemid 47531966)
18. TH Ho D Bundman DL Armstrong TA Cooper 2005 Transgenic mice expressing CUG-BP1 reproduce splicing mis-regulation observed in myotonic dystrophy Hum Mol Genet 14 1539 1547 15843400 10.1093/hmg/ddi162 1:CAS:528:DC%2BD2MXktlKqt7g%3D (Pubitemid 40823462)
19. G Begemann N Paricio R Artero I Kiss M Perez-Alonso M Mlodzik 1997 Muscleblind, a gene required for photoreceptor differentiation in Drosophila, encodes novel nuclear Cys3His-type zinc-finger-containing proteins Development 124 4321 4331 9334280 1:CAS:528:DyaK2sXnsFWmt7w%3D (Pubitemid 27496867)
20. R Artero A Prokop N Paricio G Begemann I Pueyo M Mlodzik M Perez-Alonso MK Baylies 1998 The muscleblind gene participates in the organization of Z-bands and epidermal attachments of Drosophila muscles and is regulated by Dmef2 Dev Biol 195 131 143 9520330 10.1006/dbio.1997.8833 1:CAS:528:DyaK1cXit1egs7c%3D (Pubitemid 28152874)
21. M Fardaei MT Rogers HM Thorpe K Larkin MG Hamshere PS Harper JD Brook 2002 Three proteins, MBNL, MBLL and MBXL, co-localize in vivo with nuclear foci of expanded-repeat transcripts in DM1 and DM2 cells Hum Mol Genet 11 805 814 11929853 10.1093/hmg/11.7.805 1:CAS:528:DC%2BD38Xjt1GrsbY%3D (Pubitemid 34428648)
22. RM Squillace DM Chenault EH Wang 2002 Inhibition of muscle differentiation by the novel muscleblind-related protein CHCR Dev Biol 250 218 230 12297108 10.1006/dbio.2002.0798 1:CAS:528:DC%2BD38XntVymsLo%3D
23. Y Adereth V Dammai N Kose R Li T Hsu 2005 RNA-dependent integrin alpha3 protein localization regulated by the Muscleblind-like protein MLP1 Nat Cell Biol 7 1240 1247 16273094 10.1038/ncb1335 (Pubitemid 41741737)
24. KS Lee K Smith PS Amieux EH Wang 2008 MBNL3/CHCR prevents myogenic differentiation by inhibiting MyoD-dependent gene transcription Differentiation 76 299 309 17697127 10.1111/j.1432-0436.2007.00209.x 1:CAS:528: DC%2BD1cXktVCjuro%3D (Pubitemid 351322682)
25. RN Kanadia J Shin Y Yuan SG Beattie TM Wheeler CA Thornton MS Swanson 2006 Reversal of RNA missplicing and myotonia after muscleblind overexpression in a mouse poly(CUG) model for myotonic dystrophy Proc Natl Acad Sci USA 103 11748 11753 16864772 10.1073/pnas.0604970103 1:CAS:528:DC%2BD28XotFagt7o%3D (Pubitemid 44182522)
26. CL Liquori K Ricker ML Moseley JF Jacobsen W Kress SL Naylor JW Day LP Ranum 2001 Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9 Science 293 864 867 11486088 10.1126/science.1062125 1:CAS:528: DC%2BD3MXlvVKktbc%3D (Pubitemid 32743976)
27. A Mankodi CR Urbinati QP Yuan RT Moxley V Sansone M Krym D Henderson M Schalling MS Swanson CA Thornton 2001 Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2 Hum Mol Genet 10 2165 2170 11590133 10.1093/hmg/10.19.2165 1:CAS:528:DC%2BD3MXnsl2ktbg%3D (Pubitemid 32998828)
28. RS Savkur AV Philips TA Cooper JC Dalton ML Moseley LP Ranum JW Day 2004 Insulin receptor splicing alteration in myotonic dystrophy type 2 Am J Hum Genet 74 1309 1313 15114529 10.1086/421528 1:CAS:528:DC%2BD2cXks1Cqs7s%3D (Pubitemid 38669332)
29. K Sobczak M de Mezer G Michlewski J Krol WJ Krzyzosiak 2003 RNA structure of trinucleotide repeats associated with human neurological diseases Nucleic Acids Res 31 5469 5482 14500809 10.1093/nar/gkg766 1:CAS:528: DC%2BD3sXns1Cntb8%3D (Pubitemid 37441917)
30. TH Ho RS Savkur MG Poulos MA Mancini MS Swanson TA Cooper 2005 Colocalization of muscleblind with RNA foci is separable from mis-regulation of alternative splicing in myotonic dystrophy J Cell Sci 118 2923 2933 15961406 10.1242/jcs.02404 1:CAS:528:DC%2BD2MXnsVCjt70%3D (Pubitemid 41136369)
31. Y Kino D Mori Y Oma Y Takeshita N Sasagawa S Ishiura 2004 Muscleblind protein, MBNL1/EXP, binds specifically to CHHG repeats Hum Mol Genet 13 495 507 14722159 10.1093/hmg/ddh056 1:CAS:528:DC%2BD2cXht1Klu7g%3D (Pubitemid 38313209)
32. Y Yuan SA Compton K Sobczak MG Stenberg CA Thornton JD Griffith MS Swanson 2007 Muscleblind-like 1 interacts with RNA hairpins in splicing target and pathogenic RNAs Nucleic Acids Res 35 5474 5486 17702765 10.1093/nar/gkm601 1:CAS:528:DC%2BD2sXht1ygtb%2FO (Pubitemid 47423921)
33. CJ McLeod LV O'Keefe RI Richards 2005 The pathogenic agent in Drosophila models of 'polyglutamine' diseases Hum Mol Genet 14 1041 1048 15757976 10.1093/hmg/ddi096 1:CAS:528:DC%2BD2MXjtlensro%3D (Pubitemid 40575879)
34. LB Li Z Yu X Teng NM Bonini 2008 RNA toxicity is a component of ataxin-3 degeneration in Drosophila Nature 453 1107 1111 18449188 10.1038/nature06909 1:CAS:528:DC%2BD1cXntlGjtLw%3D (Pubitemid 351871727)
35. PW Faber JR Alter ME MacDonald AC Hart 1999 Polyglutamine-mediated dysfunction and apoptotic death of a Caenorhabditis elegans sensory neuron Proc Natl Acad Sci USA 96 179 184 9874792 10.1073/pnas.96.1.179 1:CAS:528: DyaK1MXjvV2hsg%3D%3D (Pubitemid 29036073)
36. JA Parker JB Connolly C Wellington M Hayden J Dausset C Neri 2001 Expanded polyglutamines in Caenorhabditis elegans cause axonal abnormalities and severe dysfunction of PLM mechanosensory neurons without cell death Proc Natl Acad Sci USA 98 13318 13323 11687635 10.1073/pnas.231476398 1:CAS:528: DC%2BD3MXosFygtLo%3D (Pubitemid 33051360)
37. JF Morley HR Brignull JJ Weyers RI Morimoto 2002 The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans Proc Natl Acad Sci USA 99 10417 10422 12122205 10.1073/pnas.152161099
38. KY Chen H Pan MJ Lin YY Li LC Wang YC Wu KM Hsiao 2007 Length-dependent toxicity of untranslated CUG repeats on Caenorhabditis elegans Biochem Biophys Res Commun 352 774 779 17150182 10.1016/j.bbrc.2006.11.102 1:CAS:528: DC%2BD28Xhtleis7rI (Pubitemid 44880322)
39. LC Wang WT Hung H Pan KY Chen YC Wu YF Liu KM Hsiao 2008 Growth-dependent effect of muscleblind knockdown on Caenorhabditis elegans Biochem Biophys Res Commun 366 705 709 18082131 10.1016/j.bbrc.2007.12.024 1:CAS:528: DC%2BD1cXivVentQ%3D%3D
40. C Mello A Fire 1995 DNA transformation Methods Cell Biol 48 451 482 8531738 10.1016/S0091-679X(08)61399-0 1:CAS:528:DyaK2MXps1Cmu74%3D
41. S Brenner 1974 The genetics of Caenorhabditis elegans Genetics 77 71 94 4366476 1:STN:280:DyaE2c3ntFWlsw%3D%3D
42. JA Lewis JT Fleming 1995 Basic culture methods Methods Cell Biol 48 3 29 8531730 10.1016/S0091-679X(08)61381-3 1:CAS:528:DyaK2MXps1Cmtbc%3D
43. RH Waterston D Hirsh TR Lane 1984 Dominant mutations affecting muscle structure in Caenorhabditis elegans that map near the actin gene cluster J Mol Biol 180 473 496 6527380 10.1016/0022-2836(84)90023-8 1:CAS:528: DyaL2MXptVOlug%3D%3D (Pubitemid 16223398)
44. Hall DH (1995) Electron microscopy and 3D image reconstruction. In: Epstein HF, Shakes DC (eds) C. elegans: modern biological analysis of an organism. Methods in cell biology, vol. 48. Academic Press, New York, 395-436
45. ML Nonet JE Staunton MP Kilgard T Fergestad E Hartwieg HR Horvitz EM Jorgensen BJ Meyer 1997 Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles J Neurosci 17 8061 8073 9334382 1:CAS:528:DyaK2sXntVyjsbg%3D (Pubitemid 27461031)
46. DG Albertson RM Fishpool PS Birchall 1995 Fluorescence in situ hybridization for the detection of DNA and RNA Methods Cell Biol 48 339 364 8531734 10.1016/S0091-679X(08)61395-3 1:CAS:528:DyaK2MXps1Cmurk%3D
47. FD Fakhari DP Dittmer 2002 Charting latency transcripts in Kaposi's sarcoma-associated herpesvirus by whole-genome real-time quantitative PCR J Virol 76 6213 6223 12021355 10.1128/JVI.76.12.6213-6223.2002 1:CAS:528:DC%2BD38XktlSqsLs%3D (Pubitemid 34556317)
48. DP Dittmer 2003 Transcription profile of Kaposi's sarcoma-associated herpesvirus in primary Kaposi's sarcoma lesions as determined by real-time PCR arrays Cancer Res 63 2010 2015 12727810 1:CAS:528:DC%2BD3sXjtlGmsL8%3D (Pubitemid 36538598)
49. G Le Mee N Ezzeddine M Capri O Ait-Ahmed 2008 Repeat length and RNA expression level are not primary determinants in CUG expansion toxicity in Drosophila models PLoS ONE 3 e1466 18213375 10.1371/journal.pone.0001466 (Pubitemid 351796325)
50. R Galvao L Mendes-Soares J Camara I Jaco M Carmo-Fonseca 2001 Triplet repeats, RNA secondary structure and toxic gain-of-function models for pathogenesis Brain Res Bull 56 191 201 11719250 10.1016/S0361-9230(01)00651-7 1:CAS:528:DC%2BD3MXosFKqu7o%3D (Pubitemid 33062342)
51. YP Goldberg MA Kalchman M Metzler J Nasir J Zeisler R Graham HB Koide J O'Kusky AH Sharp CA Ross F Jirik MR Hayden 1996 Absence of disease phenotype and intergenerational stability of the CAG repeat in transgenic mice expressing the human Huntington disease transcript Hum Mol Genet 5 177 185 8824873 10.1093/hmg/5.2.177 1:CAS:528:DyaK28XptVCmsg%3D%3D (Pubitemid 26036913)
52. AL Peel RV Rao BA Cottrell MR Hayden LM Ellerby DE Bredesen 2001 Double-stranded RNA-dependent protein kinase, PKR, binds preferentially to Huntington's disease (HD) transcripts and is activated in HD tissue Hum Mol Genet 10 1531 1538 11468270 10.1093/hmg/10.15.1531 1:CAS:528: DC%2BD3MXlvFOitb0%3D (Pubitemid 32734304)
53. GH Klinkerfuss 1967 An electron microscopic study of myotonic dystrophy Arch Neurol 16 181 193 6018048 1:STN:280:DyaF2s%2FptV2jsQ%3D%3D
54. RM Ludatscher H Kerner S Amikam B Gellei 1978 Myotonia dystrophica with heart involvement: an electron microscopic study of skeletal, cardiac, and smooth muscle J Clin Pathol 31 1057 1064 739051 10.1136/jcp.31.11.1057 1:STN:280:DyaE1M7gvF2ntA%3D%3D (Pubitemid 9068632)
55. B Tian RJ White T Xia S Welle DH Turner MB Mathews CA Thornton 2000 Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR RNA 6 79 87 10668800 10.1017/S1355838200991544 1:CAS:528:DC%2BD3cXosF2guw%3D%3D (Pubitemid 30069038)
56. A Ebralidze Y Wang V Petkova K Ebralidse RP Junghans 2004 RNA leaching of transcription factors disrupts transcription in myotonic dystrophy Science 303 383 387 14657503 10.1126/science.1088679 1:CAS:528:DC%2BD2cXjtFGmtQ%3D%3D (Pubitemid 38095780)
57. RJ Osborne X Lin S Welle K Sobczak JR O'Rourke MS Swanson CA Thornton 2009 Transcriptional and post-transcriptional impact of toxic RNA in myotonic dystrophy Hum Mol Genet 18 1471 1481 19223393 10.1093/hmg/ddp058 1:CAS:528:DC%2BD1MXktV2hurg%3D
58. CA Milne J Hodgkin 1999 ETR-1, a homologue of a protein linked to myotonic dystrophy, is essential for muscle development in Caenorhabditis elegans Curr Biol 9 1243 1246 10556089 10.1016/S0960-9822(99)80504-1 1:CAS:528:DyaK1MXnt1yqu7s%3D (Pubitemid 29527149)
59. P Fernandez-Funez ML Nino-Rosales B de Gouyon WC She JM Luchak P Martinez E Turiegano J Benito M Capovilla PJ Skinner A McCall I Canal HT Orr HY Zoghbi J Botas 2000 Identification of genes that modify ataxin-1-induced neurodegeneration Nature 408 101 106 11081516 10.1038/35040584 1:CAS:528:DC%2BD3cXotVaksLk%3D
60. H Siomi G Dreyfuss 1997 RNA-binding proteins as regulators of gene expression Curr Opin Genet Dev 7 345 353 9229110 10.1016/S0959-437X(97)80148-7 1:CAS:528:DyaK2sXksVyntrY%3D (Pubitemid 27292286)