Towards Understanding RNA-Mediated Neurological Disorders

Journal of Genetics and Genomics

Volumn 41, Issue 9, 2014, Pages 473-484

  Duan, Ranhui ^a   Sharma, Sumeet ^b   Xia, Qiuping ^a   Garber, Kathryn ^b   Jin, Peng ^b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Neurodegeneration; R loop; RAN translation; Repeat expansion; RNA toxicity

Indexed keywords

HUNTINGTON DISEASE LIKE 2; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; AUTOSOMAL DOMINANT INHERITANCE; DEGENERATIVE DISEASE; DNA RNA HYBRIDIZATION; FRAGILE X ASSOCIATED TREMOR ATAXIA SYNDROME; FRAGILE X SYNDROME; FRIEDREICH ATAXIA; FRONTOTEMPORAL DEGENERATION; GENE MUTATION; HUMAN; NEUROLOGIC DISEASE; NONHUMAN; REVIEW; RNA PROCESSING; RNA TRANSLATION; SPINOCEREBELLAR ATAXIA TYPE 7; SPINOCEREBELLAR ATAXIA TYPE 8; SPINOCEREBELLAR DEGENERATION; ANIMAL; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NERVOUS SYSTEM DISEASES; NUCLEOTIDE SEQUENCE; PROTEIN SYNTHESIS;

ANIMALS; BASE SEQUENCE; HUMANS; NERVOUS SYSTEM DISEASES; PROTEIN BIOSYNTHESIS; RNA; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84908463807     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2014.08.003     Document Type: Review

References (116)

1. Aguilera A., Garcia-Muse T. R loops: from transcription byproducts to threats to genome stability. Mol. Cell 2012, 46:115-124.
2. Amack J.D., Paguio A.P., Mahadevan M.S. Cis and trans effects of the myotonic dystrophy (DM) mutation in a cell culture model. Hum. Mol. Genet. 1999, 8:1975-1984.
3. Amato A.A. Muscular dystrophies and other muscle diseases. Harrison's Principles of Internal Medicine 2012, The McGraw-Hill Companies, New York. R.H. B. (Ed.).
4. Arocena D.G., Iwahashi C.K., Won N., Beilina A., Ludwig A.L., Tassone F., Schwartz P.H., Hagerman P.J. Induction of inclusion formation and disruption of lamin A/C structure by premutation CGG-repeat RNA in human cultured neural cells. Hum. Mol. Genet. 2005, 14:3661-3671.
5. Ash P.E., Bieniek K.F., Gendron T.F., Caulfield T., Lin W.L., Dejesus-Hernandez M., van Blitterswijk M.M., Jansen-West K., Paul J.W., Rademakers R., Boylan K.B., Dickson D.W., Petrucelli L. Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron 2013, 77:639-646.
6. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
7. Batista P.J., Chang H.Y. Long noncoding RNAs: cellular address codes in development and disease. Cell 2013, 152:1298-1307.
8. Brook J.D., McCurrach M.E., Harley H.G., Buckler A.J., Church D., Aburatani H., Hunter K., Stanton V.P., Thirion J.P., Hudson T., Sohn R., Zemelman B., Snell R.G., Rundle S.A., Crow S., Davies J., Shelbourne P., Buxton J., Jones C., Juvonen V., Johnson K., Harper P.S., Shaw D.J., Housman D.E. 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 1992, 68:799-808.
9. Charlet B.N., Savkur R.S., Singh G., Philips A.V., Grice E.A., Cooper T.A. Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol. Cell 2002, 10:45-53.
10. Colak D., Zaninovic N., Cohen M.S., Rosenwaks Z., Yang W.Y., Gerhardt J., Disney M.D., Jaffrey S.R. Promoter-bound trinucleotide repeat mRNA drives epigenetic silencing in fragile X syndrome. Science 2014, 343:1002-1005.
11. Dansithong W., Paul S., Comai L., Reddy S. MBNL1 is the primary determinant of focus formation and aberrant insulin receptor splicing in DM1. J. Biol. Chem. 2005, 280:5773-5780.
12. David G., Abbas N., Stevanin G., Durr A., Yvert G., Cancel G., Weber C., Imbert G., Saudou F., Antoniou E., Drabkin H., Gemmill R., Giunti P., Benomar A., Wood N., Ruberg M., Agid Y., Mandel J.L., Brice A. Cloning of the SCA7 gene reveals a highly unstable CAG repeat expansion. Nat. Genet. 1997, 17:65-70.
13. Davis B.M., McCurrach M.E., Taneja K.L., Singer R.H., Housman D.E. Expansion of a CUG trinucleotide repeat in the 3' untranslated region of myotonic dystrophy protein kinase transcripts results in nuclear retention of transcripts. Proc. Natl. Acad. Sci. USA 1997, 94:7388-7393.
14. Day J.W., Schut L.J., Moseley M.L., Durand A.C., Ranum L.P. Spinocerebellar ataxia type 8: clinical features in a large family. Neurology 2000, 55:649-657.
15. de Haro M., Al-Ramahi I., De Gouyon B., Ukani L., Rosa A., Faustino N.A., Ashizawa T., Cooper T.A., Botas J. MBNL1 and CUGBP1 modify expanded CUG-induced toxicity in a Drosophila model of myotonic dystrophy type 1. Hum. Mol. Genet. 2006, 15:2138-2145.
16. DeJesus-Hernandez M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., Nicholson A.M., Finch N.A., Flynn H., Adamson J., Kouri N., Wojtas A., Sengdy P., Hsiung G.Y., Karydas A., Seeley W.W., Josephs K.A., Coppola G., Geschwind D.H., Wszolek Z.K., Feldman H., Knopman D.S., Petersen R.C., Miller B.L., Dickson D.W., Boylan K.B., Graff-Radford N.R., Rademakers R. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
17. Donnelly C.J., Zhang P.W., Pham J.T., Haeusler A.R., Mistry N.A., Vidensky S., Daley E.L., Poth E.M., Hoover B., Fines D.M., Maragakis N., Tienari P.J., Petrucelli L., Traynor B.J., Wang J., Rigo F., Bennett C.F., Blackshaw S., Sattler R., Rothstein J.D. RNA toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention. Neuron 2013, 80:415-428.
18. Encode Project Consortium An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74.
19. Erdmann V.A., Barciszewska M.Z., Hochberg A., de Groot N., Barciszewski J. Regulatory RNAs. Cell. Mol. Life Sci. 2001, 58:960-977.
20. Faghihi M.A., Wahlestedt C. Regulatory roles of natural antisense transcripts. Nat. Rev. Mol. Cell Biol. 2009, 10:637-643.
21. Fardaei M., Larkin K., Brook J.D., Hamshere M.G. Invivo co-localisation of MBNL protein with DMPK expanded-repeat transcripts. Nucleic Acids Res. 2001, 29:2766-2771.
22. Fardaei M., Rogers M.T., Thorpe H.M., Larkin K., Hamshere M.G., Harper P.S., Brook J.D. Three proteins, MBNL, MBLL and MBXL, co-localize invivo with nuclear foci of expanded-repeat transcripts in DM1 and DM2 cells. Hum. Mol. Genet. 2002, 11:805-814.
23. Fatica A., Bozzoni I. Long non-coding RNAs: new players in cell differentiation and development. Nat. Rev. Genet. 2014, 15:7-21.
24. Filipowicz W., Bhattacharyya S.N., Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat. Rev. Genet. 2008, 9:102-114.
25. Fu Y.H., Pizzuti A., Fenwick R.G., King J., Rajnarayan S., Dunne P.W., Dubel J., Nasser G.A., Ashizawa T., de Jong P., Wieringa B., Korneluk R., Perryman M.B., Epstein H.F., Caskey T.C. An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 1992, 255:1256-1258.
26. Gendron T.F., Belzil V.V., Zhang Y.J., Petrucelli L. Mechanisms of toxicity in C9FTLD/ALS. Acta Neuropathol. 2014, 127:359-376.
27. Gendron T.F., Bieniek K.F., Zhang Y.J., Jansen-West K., Ash P.E., Caulfield T., Daughrity L., Dunmore J.H., Castanedes-Casey M., Chew J., Cosio D.M., van Blitterswijk M., Lee W.C., Rademakers R., Boylan K.B., Dickson D.W., Petrucelli L. Antisense transcripts of the expanded C9ORF72 hexanucleotide repeat form nuclear RNA foci and undergo repeat-associated non-ATG translation in c9FTD/ALS. Acta Neuropathol. 2013, 126:829-844.
28. Giordana M.T., Ferrero P., Grifoni S., Pellerino A., Naldi A., Montuschi A. Dementia and cognitive impairment in amyotrophic lateral sclerosis: a review. Neurol. Sci. 2011, 32:9-16.
29. Grammatikakis I., Goo Y.H., Echeverria G.V., Cooper T.A. Identification of MBNL1 and MBNL3 domains required for splicing activation and repression. Nucleic Acids Res. 2011, 39:2769-2780.
30. Greco C.M., Berman R.F., Martin R.M., Tassone F., Schwartz P.H., Chang A., Trapp B.D., Iwahashi C., Brunberg J., Grigsby J., Hessl D., Becker E.J., Papazian J., Leehey M.A., Hagerman R.J., Hagerman P.J. Neuropathology of fragile X-associated tremor/ataxia syndrome (FXTAS). Brain 2006, 129:243-255.
31. Greco C.M., Hagerman R.J., Tassone F., Chudley A.E., Del Bigio M.R., Jacquemont S., Leehey M., Hagerman P.J. Neuronal intranuclear inclusions in a new cerebellar tremor/ataxia syndrome among fragile X carriers. Brain 2002, 125:1760-1771.
32. Greenstein P.E., Vonsattel J.P., Margolis R.L., Joseph J.T. Huntington's disease like-2 neuropathology. Mov. Disord. 2007, 22:1416-1423.
33. Groh M., Lufino M.M., Wade-Martins R., Gromak N. R-loops associated with triplet repeat expansions promote gene silencing in Friedreich ataxia and fragile X syndrome. PLoS Genet. 2014, 10:e1004318.
34. Haeusler A.R., Donnelly C.J., Periz G., Simko E.A., Shaw P.G., Kim M.S., Maragakis N.J., Troncoso J.C., Pandey A., Sattler R., Rothstein J.D., Wang J. C9orf72 nucleotide repeat structures initiate molecular cascades of disease. Nature 2014, 507:195-200.
35. Hagerman P.J., Hagerman R.J. The fragile-X premutation: a maturing perspective. Am. J. Hum. Genet. 2004, 74:805-816.
36. Hagerman R.J., Hagerman P.J. The fragile X premutation: into the phenotypic fold. Curr. Opin. Genet. Dev. 2002, 12:278-283.
37. Hann S.R., King M.W., Bentley D.L., Anderson C.W., Eisenman R.N. A non-AUG translational initiation in c-myc exon 1 generates an N-terminally distinct protein whose synthesis is disrupted in Burkitt's lymphomas. Cell 1988, 52:185-195.
38. Hastings M.L., Ingle H.A., Lazar M.A., Munroe S.H. Post-transcriptional regulation of thyroid hormone receptor expression by cis-acting sequences and a naturally occurring antisense RNA. J. Biol. Chem. 2000, 275:11507-11513.
39. He Y., Vogelstein B., Velculescu V.E., Papadopoulos N., Kinzler K.W. The antisense transcriptomes of human cells. Science 2008, 322:1855-1857.
40. Ho T.H., Bundman D., Armstrong D.L., Cooper T.A. Transgenic mice expressing CUG-BP1 reproduce splicing mis-regulation observed in myotonic dystrophy. Hum. Mol. Genet. 2005, 14:1539-1547.
41. Ho T.H., Charlet B.N., Poulos M.G., Singh G., Swanson M.S., Cooper T.A. Muscleblind proteins regulate alternative splicing. EMBO J. 2004, 23:3103-3112.
42. Holmes S.E., O'Hearn E., Rosenblatt A., Callahan C., Hwang H.S., Ingersoll-Ashworth R.G., Fleisher A., Stevanin G., Brice A., Potter N.T., Ross C.A., Margolis R.L. A repeat expansion in the gene encoding junctophilin-3 is associated with Huntington disease-like 2. Nat. Genet. 2001, 29:377-378.
43. Iwahashi C.K., Yasui D.H., An H.J., Greco C.M., Tassone F., Nannen K., Babineau B., Lebrilla C.B., Hagerman R.J., Hagerman P.J. Protein composition of the intranuclear inclusions of FXTAS. Brain 2006, 129:256-271.
44. Jacquemont S., Hagerman R.J., Leehey M., Grigsby J., Zhang L., Brunberg J.A., Greco C., Des Portes V., Jardini T., Levine R., Berry-Kravis E., Brown W.T., Schaeffer S., Kissel J., Tassone F., Hagerman P.J. Fragile X premutation tremor/ataxia syndrome: molecular, clinical, and neuroimaging correlates. Am. J. Hum. Genet. 2003, 72:869-878.
45. Jiang H., Mankodi A., Swanson M.S., Moxley R.T., Thornton C.A. Myotonic dystrophy type 1 is associated with nuclear foci of mutant RNA, sequestration of muscleblind proteins and deregulated alternative splicing in neurons. Hum. Mol. Genet. 2004, 13:3079-3088.
46. Jin P., Duan R., Qurashi A., Qin Y., Tian D., Rosser T.C., Liu H., Feng Y., Warren S.T. Pur alpha binds to rCGG repeats and modulates repeat-mediated neurodegeneration in a Drosophila model of fragile X tremor/ataxia syndrome. Neuron 2007, 55:556-564.
47. Jin P., Zarnescu D.C., Zhang F., Pearson C.E., Lucchesi J.C., Moses K., Warren S.T. RNA-mediated neurodegeneration caused by the fragile X premutation rCGG repeats in Drosophila. Neuron 2003, 39:739-747.
48. Kalsotra A., Xiao X., Ward A.J., Castle J.C., Johnson J.M., Burge C.B., Cooper T.A. A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc. Natl. Acad. Sci. USA 2008, 105:20333-20338.
49. Kanadia R.N., Johnstone K.A., Mankodi A., Lungu C., Thornton C.A., Esson D., Timmers A.M., Hauswirth W.W., Swanson M.S. A muscleblind knockout model for myotonic dystrophy. Science 2003, 302:1978-1980.
50. Kanadia R.N., Shin J., Yuan Y., Beattie S.G., Wheeler T.M., Thornton C.A., Swanson M.S. Reversal of RNA missplicing and myotonia after muscleblind overexpression in a mouse poly(CUG) model for myotonic dystrophy. Proc. Natl. Acad. Sci. USA 2006, 103:11748-11753.
51. Kenneson A., Zhang F., Hagedorn C.H., Warren S.T. Reduced FMRP and increased FMR1 transcription is proportionally associated with CGG repeat number in intermediate-length and premutation carriers. Hum. Mol. Genet. 2001, 10:1449-1454.
52. Khalil A.M., Faghihi M.A., Modarresi F., Brothers S.P., Wahlestedt C. A novel RNA transcript with antiapoptotic function is silenced in fragile X syndrome. PLoS ONE 2008, 3:e1486.
53. Knee R., Murphy P.R. Regulation of gene expression by natural antisense RNA transcripts. Neurochem. Int. 1997, 31:379-392.
54. Koob M.D., Moseley M.L., Schut L.J., Benzow K.A., Bird T.D., Day J.W., Ranum L.P. An untranslated CTG expansion causes a novel form of spinocerebellar ataxia (SCA8). Nat. Genet. 1999, 21:379-384.
55. Kozak M. Context effects and inefficient initiation at non-AUG codons in eukaryotic cell-free translation systems. Mol. Cell Biol. 1989, 9:5073-5080.
56. Kremer E.J., Pritchard M., Lynch M., Yu S., Holman K., Baker E., Warren S.T., Schlessinger D., Sutherland G.R., Richards R.I. Mapping of DNA instability at the fragile X to a trinucleotide repeat sequence p(CCG)n. Science 1991, 252:1711-1714.
57. Krol J., Loedige I., Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 2010, 11:597-610.
58. Kuyumcu-Martinez N.M., Wang G.S., Cooper T.A. Increased steady-state levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mediated hyperphosphorylation. Mol. Cell 2007, 28:68-78.
59. La Spada A.R., Fu Y.H., Sopher B.L., Libby R.T., Wang X., Li L.Y., Einum D.D., Huang J., Possin D.E., Smith A.C., Martinez R.A., Koszdin K.L., Treuting P.M., Ware C.B., Hurley J.B., Ptacek L.J., Chen S. Polyglutamine-expanded ataxin-7 antagonizes CRX function and induces cone-rod dystrophy in a mouse model of SCA7. Neuron 2001, 31:913-927.
60. Ladd P.D., Smith L.E., Rabaia N.A., Moore J.M., Georges S.A., Hansen R.S., Hagerman R.J., Tassone F., Tapscott S.J., Filippova G.N. An antisense transcript spanning the CGG repeat region of FMR1 is upregulated in premutation carriers but silenced in full mutation individuals. Hum. Mol. Genet. 2007, 16:3174-3187.
61. Lagier-Tourenne C., Baughn M., Rigo F., Sun S., Liu P., Li H.R., Jiang J., Watt A.T., Chun S., Katz M., Qiu J., Sun Y., Ling S.C., Zhu Q., Polymenidou M., Drenner K., Artates J.W., McAlonis-Downes M., Markmiller S., Hutt K.R., Pizzo D.P., Cady J., Harms M.B., Baloh R.H., Vandenberg S.R., Yeo G.W., Fu X.D., Bennett C.F., Cleveland D.W., Ravits J. Targeted degradation of sense and antisense C9orf72 RNA foci as therapy for ALS and frontotemporal degeneration. Proc. Natl. Acad. Sci. USA 2013, 110:E4530-E4539.
62. Lee Y.B., Chen H.J., Peres J.N., Gomez-Deza J., Attig J., Stalekar M., Troakes C., Nishimura A.L., Scotter E.L., Vance C., Adachi Y., Sardone V., Miller J.W., Smith B.N., Gallo J.M., Ule J., Hirth F., Rogelj B., Houart C., Shaw C.E. Hexanucleotide repeats in ALS/FTD form length-dependent RNA foci, sequester RNA binding proteins, and are neurotoxic. Cell Rep. 2013, 5:1178-1186.
63. Li A.W., Murphy P.R. Expression of alternatively spliced FGF-2 antisense RNA transcripts in the central nervous system: regulation of FGF-2 mRNA translation. Mol. Cell. Endocrinol. 2000, 170:233-242.
64. Li Y., Jin P. RNA-mediated neurodegeneration in fragile X-associated tremor/ataxia syndrome. Brain Res. 2012, 1462:112-117.
65. Lin X., Miller J.W., Mankodi A., Kanadia R.N., Yuan Y., Moxley R.T., Swanson M.S., Thornton C.A. Failure of MBNL1-dependent post-natal splicing transitions in myotonic dystrophy. Hum. Mol. Genet. 2006, 15:2087-2097.
66. Liquori C.L., Ricker K., Moseley M.L., Jacobsen J.F., Kress W., Naylor S.L., Day J.W., Ranum L.P. Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9. Science 2001, 293:864-867.
67. Loomis E.W., Sanz L.A., Chedin F., Hagerman P.J. Transcription-associated R-loop formation across the human FMR1 CGG-repeat region. PLoS Genet. 2014, 10:e1004294.
68. Mankodi A., Lin X., Blaxall B.C., Swanson M.S., Thornton C.A. Nuclear RNA foci in the heart in myotonic dystrophy. Circ. Res. 2005, 97:1152-1155.
69. Mankodi A., Logigian E., Callahan L., McClain C., White R., Henderson D., Krym M., Thornton C.A. Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science 2000, 289:1769-1773.
70. Mankodi A., Takahashi M.P., Jiang H., Beck C.L., Bowers W.J., Moxley R.T., Cannon S.C., Thornton C.A. Expanded CUG repeats trigger aberrant splicing of ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol. Cell 2002, 10:35-44.
71. Mankodi A., Urbinati C.R., Yuan Q.P., Moxley R.T., Sansone V., Krym M., Henderson D., Schalling M., Swanson M.S., Thornton C.A. Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2. Hum. Mol. Genet. 2001, 10:2165-2170.
72. Margolis R.L., Holmes S.E., Rosenblatt A., Gourley L., O'Hearn E., Ross C.A., Seltzer W.K., Walker R.H., Ashizawa T., Rasmussen A., Hayden M., Almqvist E.W., Harris J., Fahn S., MacDonald M.E., Mysore J., Shimohata T., Tsuji S., Potter N., Nakaso K., Adachi Y., Nakashima K., Bird T., Krause A., Greenstein P. Huntington's Disease-like 2 (HDL2) in North America and Japan. Ann. Neurol. 2004, 56:670-674.
73. Margolis R.L., O'Hearn E., Rosenblatt A., Willour V., Holmes S.E., Franz M.L., Callahan C., Hwang H.S., Troncoso J.C., Ross C.A. A disorder similar to Huntington's disease is associated with a novel CAG repeat expansion. Ann. Neurol. 2001, 50:373-380.
74. Marsh J.L., Walker H., Theisen H., Zhu Y.Z., Fielder T., Purcell J., Thompson L.M. Expanded polyglutamine peptides alone are intrinsically cytotoxic and cause neurodegeneration in Drosophila. Hum. Mol. Genet. 2000, 9:13-25.
75. Miller J.W., Urbinati C.R., Teng-Umnuay P., Stenberg M.G., Byrne B.J., Thornton C.A., Swanson M.S. Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J. 2000, 19:4439-4448.
76. Mizielinska S., Lashley T., Norona F.E., Clayton E.L., Ridler C.E., Fratta P., Isaacs A.M. C9orf72 frontotemporal lobar degeneration is characterised by frequent neuronal sense and antisense RNA foci. Acta Neuropathol. 2013, 126:845-857.
77. Mori K., Arzberger T., Grasser F.A., Gijselinck I., May S., Rentzsch K., Weng S.M., Schludi M.H., van der Zee J., Cruts M., Van Broeckhoven C., Kremmer E., Kretzschmar H.A., Haass C., Edbauer D. Bidirectional transcripts of the expanded C9orf72 hexanucleotide repeat are translated into aggregating dipeptide repeat proteins. Acta Neuropathol. 2013, 126:881-893.
78. Mori K., Lammich S., Mackenzie I.R., Forne I., Zilow S., Kretzschmar H., Edbauer D., Janssens J., Kleinberger G., Cruts M., Herms J., Neumann M., Van Broeckhoven C., Arzberger T., Haass C. hnRNP A3 binds to GGGGCC repeats and is a constituent of p62-positive/TDP43-negative inclusions in the hippocampus of patients with C9orf72 mutations. Acta Neuropathol. 2013, 125:413-423.
79. Mori K., Weng S.M., Arzberger T., May S., Rentzsch K., Kremmer E., Schmid B., Kretzschmar H.A., Cruts M., Van Broeckhoven C., Haass C., Edbauer D. The C9orf72 GGGGCC repeat is translated into aggregating dipeptide-repeat proteins in FTLD/ALS. Science 2013, 339:1335-1338.
80. Moseley M.L., Zu T., Ikeda Y., Gao W., Mosemiller A.K., Daughters R.S., Chen G., Weatherspoon M.R., Clark H.B., Ebner T.J., Day J.W., Ranum L.P. Bidirectional expression of CUG and CAG expansion transcripts and intranuclear polyglutamine inclusions in spinocerebellar ataxia type 8. Nat. Genet. 2006, 38:758-769.
81. Mutsuddi M., Marshall C.M., Benzow K.A., Koob M.D., Rebay I. The spinocerebellar ataxia 8 noncoding RNA causes neurodegeneration and associates with staufen in Drosophila. Curr. Biol. 2004, 14:302-308.
82. Nelson D.L., Orr H.T., Warren S.T. The unstable repeats-three evolving faces of neurological disease. Neuron 2013, 77:825-843.
83. Oberle I., Rousseau F., Heitz D., Kretz C., Devys D., Hanauer A., Boue J., Bertheas M.F., Mandel J.L. Instability of a 550-base pair DNA segment and abnormal methylation in fragile X syndrome. Science 1991, 252:1097-1102.
84. Orengo J.P., Chambon P., Metzger D., Mosier D.R., Snipes G.J., Cooper T.A. Expanded CTG repeats within the DMPK 3' UTR causes severe skeletal muscle wasting in an inducible mouse model for myotonic dystrophy. Proc. Natl. Acad. Sci. USA 2008, 105:2646-2651.
85. Peabody D.S. Translation initiation at non-AUG triplets in mammalian cells. J. Biol. Chem. 1989, 264:5031-5035.
86. Pearson C.E. Repeat associated non-ATG translation initiation: one DNA, two transcripts, seven reading frames, potentially nine toxic entities!. PLoS Genet. 2011, 7:e1002018.
87. Pieretti M., Zhang F.P., Fu Y.H., Warren S.T., Oostra B.A., Caskey C.T., Nelson D.L. Absence of expression of the FMR-1 gene in fragile X syndrome. Cell 1991, 66:817-822.
88. Rademakers R., Neumann M., Mackenzie I.R. Advances in understanding the molecular basis of frontotemporal dementia. Nat. Rev. Neurol. 2012, 8:423-434.
89. Renton A.E., Majounie E., Waite A., Simon-Sanchez J., Rollinson S., Gibbs J.R., Schymick J.C., Laaksovirta H., van Swieten J.C., Myllykangas L., Kalimo H., Paetau A., Abramzon Y., Remes A.M., Kaganovich A., Scholz S.W., Duckworth J., Ding J., Harmer D.W., Hernandez D.G., Johnson J.O., Mok K., Ryten M., Trabzuni D., Guerreiro R.J., Orrell R.W., Neal J., Murray A., Pearson J., Jansen I.E., Sondervan D., Seelaar H., Blake D., Young K., Halliwell N., Callister J.B., Toulson G., Richardson A., Gerhard A., Snowden J., Mann D., Neary D., Nalls M.A., Peuralinna T., Jansson L., Isoviita V.M., Kaivorinne A.L., Holtta-Vuori M., Ikonen E., Sulkava R., Benatar M., Wuu J., Chio A., Restagno G., Borghero G., Sabatelli M., Heckerman D., Rogaeva E., Zinman L., Rothstein J.D., Sendtner M., Drepper C., Eichler E.E., Alkan C., Abdullaev Z., Pack S.D., Dutra A., Pak E., Hardy J., Singleton A., Williams N.M., Heutink P., Pickering-Brown S., Morris H.R., Tienari P.J., Traynor B.J. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
90. Robberecht W., Philips T. The changing scene of amyotrophic lateral sclerosis. Nat. Rev. Neurosci. 2013, 14:248-264.
91. Rudnicki D.D., Holmes S.E., Lin M.W., Thornton C.A., Ross C.A., Margolis R.L. Huntington's disease-like 2 is associated with CUG repeat-containing RNA foci. Ann. Neurol. 2007, 61:272-282.
92. Rudnicki D.D., Pletnikova O., Vonsattel J.P., Ross C.A., Margolis R.L. A comparison of huntington disease and huntington disease-like 2 neuropathology. J. Neuropathol. Exp. Neurol. 2008, 67:366-374.
93. Rutherford N.J., Heckman M.G., Dejesus-Hernandez M., Baker M.C., Soto-Ortolaza A.I., Rayaprolu S., Stewart H., Finger E., Volkening K., Seeley W.W., Hatanpaa K.J., Lomen-Hoerth C., Kertesz A., Bigio E.H., Lippa C., Knopman D.S., Kretzschmar H.A., Neumann M., Caselli R.J., White C.L., Mackenzie I.R., Petersen R.C., Strong M.J., Miller B.L., Boeve B.F., Uitti R.J., Boylan K.B., Wszolek Z.K., Graff-Radford N.R., Dickson D.W., Ross O.A., Rademakers R. Length of normal alleles of C9ORF72 GGGGCC repeat do not influence disease phenotype. Neurbiol. Aging 2012, 33(2950):e2955-2957.
94. Savkur R.S., Philips A.V., Cooper T.A. Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat. Genet. 2001, 29:40-47.
95. Sellier C., Rau F., Liu Y., Tassone F., Hukema R.K., Gattoni R., Schneider A., Richard S., Willemsen R., Elliott D.J., Hagerman P.J., Charlet-Berguerand N. Sam68 sequestration and partial loss of function are associated with splicing alterations in FXTAS patients. EMBO J. 2010, 29:1248-1261.
96. Sen S., Talukdar I., Liu Y., Tam J., Reddy S., Webster N.J. Muscleblind-like 1 (Mbnl1) promotes insulin receptor exon 11 inclusion via binding to a downstream evolutionarily conserved intronic enhancer. J. Biol. Chem. 2010, 285:25426-25437.
97. Seznec H., Agbulut O., Sergeant N., Savouret C., Ghestem A., Tabti N., Willer J.C., Ourth L., Duros C., Brisson E., Fouquet C., Butler-Browne G., Delacourte A., Junien C., Gourdon G. Mice transgenic for the human myotonic dystrophy region with expanded CTG repeats display muscular and brain abnormalities. Hum. Mol. Genet. 2001, 10:2717-2726.
98. Sofola O.A., Jin P., Qin Y., Duan R., Liu H., de Haro M., Nelson D.L., Botas J. RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron 2007, 55:565-571.
99. Stepto A., Gallo J.M., Shaw C.E., Hirth F. Modelling C9ORF72 hexanucleotide repeat expansion in amyotrophic lateral sclerosis and frontotemporal dementia. Acta Neuropathol. 2014, 127:377-389.
100. Tan H., Poidevin M., Li H., Chen D., Jin P. MicroRNA-277 modulates the neurodegeneration caused by Fragile X premutation rCGG repeats. PLoS Genet. 2012, 8:e1002681.
101. Taneja K.L., McCurrach M., Schalling M., Housman D., Singer R.H. Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues. J. Cell Biol. 1995, 128:995-1002.
102. Tassone F., Beilina A., Carosi C., Albertosi S., Bagni C., Li L., Glover K., Bentley D., Hagerman P.J. Elevated FMR1 mRNA in premutation carriers is due to increased transcription. RNA 2007, 13:555-562.
103. Tassone F., Hagerman R.J., Taylor A.K., Gane L.W., Godfrey T.E., Hagerman P.J. Elevated levels of FMR1 mRNA in carrier males: a new mechanism of involvement in the fragile-X syndrome. Am. J. Hum. Genet. 2000, 66:6-15.
104. Tassone F., Iwahashi C., Hagerman P.J. FMR1 RNA within the intranuclear inclusions of fragile X-associated tremor/ataxia syndrome (FXTAS). RNA Biol. 2004, 1:103-105.
105. Timchenko L.T., Miller J.W., Timchenko N.A., DeVore D.R., Datar K.V., Lin L., Roberts R., Caskey C.T., Swanson M.S. Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucleic Acids Res. 1996, 24:4407-4414.
106. Timchenko N.A., Cai Z.J., Welm A.L., Reddy S., Ashizawa T., Timchenko L.T. RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1. J. Biol. Chem. 2001, 276:7820-7826.
107. Todd P.K., Oh S.Y., Krans A., He F., Sellier C., Frazer M., Renoux A.J., Chen K.C., Scaglione K.M., Basrur V., Elenitoba-Johnson K., Vonsattel J.P., Louis E.D., Sutton M.A., Taylor J.P., Mills R.E., Charlet-Berguerand N., Paulson H.L. CGG repeat-associated translation mediates neurodegeneration in fragile X tremor ataxia syndrome. Neuron 2013, 78:440-455.
108. Udd B., Krahe R. The myotonic dystrophies: molecular, clinical, and therapeutic challenges. Lancet Neurol. 2012, 11:891-905.
109. Verkerk A.J., Pieretti M., Sutcliffe J.S., Fu Y.H., Kuhl D.P., Pizzuti A., Reiner O., Richards S., Victoria M.F., Zhang F.P., et al. Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 1991, 65:905-914.
110. Wang G.S., Kuyumcu-Martinez M.N., Sarma S., Mathur N., Wehrens X.H., Cooper T.A. PKC inhibition ameliorates the cardiac phenotype in a mouse model of myotonic dystrophy type 1. J. Clin. Invest. 2009, 119:3797-3806.
111. Wilburn B., Rudnicki D.D., Zhao J., Weitz T.M., Cheng Y., Gu X., Greiner E., Park C.S., Wang N., Sopher B.L., La Spada A.R., Osmand A., Margolis R.L., Sun Y.E., Yang X.W. An antisense CAG repeat transcript at JPH3 locus mediates expanded polyglutamine protein toxicity in Huntington's disease-like 2 mice. Neuron 2011, 70:427-440.
112. Willemsen R., Hoogeveen-Westerveld M., Reis S., Holstege J., Severijnen L.A., Nieuwenhuizen I.M., Schrier M., van Unen L., Tassone F., Hoogeveen A.T., Hagerman P.J., Mientjes E.J., Oostra B.A. The FMR1 CGG repeat mouse displays ubiquitin-positive intranuclear neuronal inclusions; implications for the cerebellar tremor/ataxia syndrome. Hum. Mol. Genet. 2003, 12:949-959.
113. Xu Z., Poidevin M., Li X., Li Y., Shu L., Nelson D.L., Li H., Hales C.M., Gearing M., Wingo T.S., Jin P. Expanded GGGGCC repeat RNA associated with amyotrophic lateral sclerosis and frontotemporal dementia causes neurodegeneration. Proc. Natl. Acad. Sci. USA 2013, 110:7778-7783.
114. Yelin R., Dahary D., Sorek R., Levanon E.Y., Goldstein O., Shoshan A., Diber A., Biton S., Tamir Y., Khosravi R., Nemzer S., Pinner E., Walach S., Bernstein J., Savitsky K., Rotman G. Widespread occurrence of antisense transcription in the human genome. Nat. Biotechnol. 2003, 21:379-386.
115. Zu T., Gibbens B., Doty N.S., Gomes-Pereira M., Huguet A., Stone M.D., Margolis J., Peterson M., Markowski T.W., Ingram M.A., Nan Z., Forster C., Low W.C., Schoser B., Somia N.V., Clark H.B., Schmechel S., Bitterman P.B., Gourdon G., Swanson M.S., Moseley M., Ranum L.P. Non-ATG-initiated translation directed by microsatellite expansions. Proc. Natl. Acad. Sci. USA 2011, 108:260-265.
116. Zu T., Liu Y., Banez-Coronel M., Reid T., Pletnikova O., Lewis J., Miller T.M., Harms M.B., Falchook A.E., Subramony S.H., Ostrow L.W., Rothstein J.D., Troncoso J.C., Ranum L.P. RAN proteins and RNA foci from antisense transcripts in C9ORF72 ALS and frontotemporal dementia. Proc. Natl. Acad. Sci. USA 2013, 110:E4968-E4977.