RAN translation and frameshifting as translational challenges at simple repeats of human neurodegenerative disorders

Nucleic Acids Research

Volumn 42, Issue 19, 2014, Pages 11849-11864

  Wojciechowska, Marzena ^a   Olejniczak, Marta ^a   Galka Marciniak, Paulina ^a   Jazurek, Magdalena ^a   Krzyzosiak, Wlodzimierz J ^a  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 1; INITIATION FACTOR 3; INITIATION FACTOR 4A; REPETITIVE DNA;

ATAXIA; CAG REPEAT; DEGENERATIVE DISEASE; FRAGILE X SYNDROME; GENE EXPRESSION; GENE LOCATION; GENE LOCUS; GENE STRUCTURE; GENETIC CODE; GENETIC TRANSCRIPTION; HUMAN; HUNTINGTON CHOREA; MYOTONIC DYSTROPHY; NONHUMAN; NUCLEIC ACID PROBE; NUCLEOTIDE REPEAT; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; RAN TRANSLATION; REVIEW; RIBOSOMAL FRAMESHIFTING; RNA STRUCTURE; SPINOCEREBELLAR DEGENERATION; TRANSCRIPTION ELONGATION; TRANSLATION INITIATION; DEMYELINATING DISEASE; GENETICS; MACHADO JOSEPH DISEASE; RNA TRANSLATION;

DNA REPEAT EXPANSION; FRAMESHIFTING, RIBOSOMAL; HEREDODEGENERATIVE DISORDERS, NERVOUS SYSTEM; HUMANS; HUNTINGTON DISEASE; MACHADO-JOSEPH DISEASE; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PEPTIDE CHAIN INITIATION, TRANSLATIONAL;

EID: 84925284100     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku794     Document Type: Review

References (115)

1. Lopez Castel, A., Cleary, J.D. and Pearson, C.E. (2010) Repeat instability as the basis for human diseases and as a potential target for therapy. Nat. Rev. Mol. Cell Biol., 11, 165-170.
2. Ranum, L.P. and Day, J.W. (2002) Dominantly inherited, non-coding microsatellite expansion disorders. Curr. Opin. Genet. Dev., 12, 266-271.
3. Orr, H.T. and Zoghbi, H.Y. (2007) Trinucleotide repeat disorders. Annu. Rev. Neurosci., 30, 575-621.
4. Hsu, R.J., Hsiao, K.M., Lin, M.J., Li, C.Y., Wang, L.C., Chen, L.K. and Pan, H. (2011) Long tract of untranslated CAG repeats is deleterious in transgenic mice. PLoS One, 6, e16417.
5. Ho, T.H., Savkur, R.S., Poulos, M.G., Mancini, M.A., Swanson, M.S. and Cooper, T.A. (2005) Colocalization of muscleblind with RNA foci is separable from mis-regulation of alternative splicing in myotonic dystrophy. J. Cell Sci., 118, 2923-2933.
6. Li, L.B., Yu, Z., Teng, X. and Bonini, N.M. (2008) RNA toxicity is a component of ataxin-3 degeneration in Drosophila. Nature, 453, 1107-1111.
7. Wang, L.C., Chen, K.Y., Pan, H., Wu, C.C., Chen, P.H., Liao, Y.T., Li, C., Huang, M.L. and Hsiao, K.M. (2011) Muscleblind participates in RNA toxicity of expanded CAG and CUG repeats in Caenorhabditis elegans. Cell. Mol. Life Sci., 68, 1255-1267.
8. Mykowska, A., Sobczak, K., Wojciechowska, M., Kozlowski, P. and Krzyzosiak, W.J. (2011) CAG repeats mimic CUG repeats in the misregulation of alternative splicing. Nucleic Acids Res., 39, 8938-8951.
9. Wojciechowska, M. and Krzyzosiak, W.J. (2011) Cellular toxicity of expanded RNA repeats: focus on RNA foci. Hum. Mol.Genet., 20, 3811-3821.
10. Galka-Marciniak, P., Urbanek, M.O. and Krzyzosiak, W.J. (2012) Triplet repeats in transcripts: structural insights into RNA toxicity. Biol. Chem., 393, 1299-1315.
11. Gendron, T.F., Belzil, V.V., Zhang, Y.J. and Petrucelli, L. (2014) Mechanisms of toxicity in C9FTLD/ALS. Acta Neuropathol., 127, 359-376.
12. 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. 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.
13. Batra, R., Charizanis, K. and Swanson, M.S. (2010) Partners in crime: bidirectional transcription in unstable microsatellite disease. Hum. Mol. Genet., 19, R77-R82.
14. 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. et al. (2011) Non-ATG-initiated translation directed by microsatellite expansions. Proc. Natl. Acad. Sci. U.S.A., 108, 260-265.
15. 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. et al. (2013) RAN proteins and RNA foci from antisense transcripts in C9ORF72 ALS and frontotemporal dementia. Proc. Natl. Acad. Sci. U.S.A., 110, E4968-E4977.
16. 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. et al. (2013) CGG repeat-associated translation mediates neurodegeneration in fragile X tremor ataxia syndrome. Neuron, 78, 440-455.
17. 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. et al. (2013) Antisense transcripts of the expanded C9ORF72 hexanucleotide repeat form nuclear RNA foci and undergo repeat-associated non-ATG translation in c9FTD/ALS. Acta Neuropathol., 126, 829-844.
18. 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. 3rd, Rademakers, R. et al. (2013) Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron, 77, 639-646.
19. Mori, K., Weng, S.M., Arzberger, T., May, S., Rentzsch, K., Kremmer, E., Schmid, B., Kretzschmar, H.A., Cruts, M., Van Broeckhoven, C. et al. (2013) The C9orf72 GGGGCC repeat is translated into aggregating dipeptide-repeat proteins in FTLD/ALS. Science, 339, 1335-1338.
20. Donnelly, C.J., Zhang, P.W., Pham, J.T., Heusler, A.R., Mistry, N.A., Vidensky, S., Daley, E.L., Poth, E.M., Hoover, B., Fines, D.M. et al. (2013) RNA toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention. Neuron, 80, 415-428.
21. Almeida, S., Gascon, E., Tran, H., Chou, H.J., Gendron, T.F., Degroot, S., Tapper, A.R., Sellier, C., Charlet-Berguerand, N., Karydas, A. et al. (2013) Modeling key pathological features of frontotemporal dementia with C9ORF72 repeat expansion in iPSC-derived human neurons. Acta Neuropathol., 126, 385-399.
22. 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. et al. (2013) Bidirectional transcripts of the expanded C9orf72 hexanucleotide repeat are translated into aggregating dipeptide repeat proteins. Acta Neuropathol., 126, 881-893.
23. Jackson, R.J., Hellen, C.U. and Pestova, T.V. (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol, 11, 113-127.
24. Sonenberg, N. and Hinnebusch, A.G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell, 136, 731-745.
25. Firth, A.E. and Brierley, I. (2012) Non-canonical translation in RNA viruses. J. Gen. Virol., 93, 1385-1409.
26. Toulouse, A., Au-Yeung, F., Gaspar, C., Roussel, J., Dion, P. and Rouleau, G.A. (2005) Ribosomal frameshifting on MJD-1 transcripts with long CAG tracts. Hum. Mol. Genet., 14, 2649-2660.
27. Gaspar, C., Jannatipour, M., Dion, P., Laganiere, J., Sequeiros, J., Brais, B. and Rouleau, G.A. (2000) CAG tract of MJD-1 may be prone to frameshifts causing polyalanine accumulation. Hum. Mol. Genet., 9, 1957-1966.
28. Stochmanski, S.J., Therrien, M., Laganiere, J., Rochefort, D., Laurent, S., Karemera, L., Gaudet, R., Vyboh, K., Van Meyel, D.J., Di Cristo, G. et al. (2012) Expanded ATXN3 frameshifting events are toxic in Drosophila and mammalian neuron models. Hum. Mol. Genet., 21, 2211-2218.
29. Davies, J.E. and Rubinsztein, D.C. (2006) Polyalanine and polyserine frameshift products in Huntington's disease. J. Med. Genet., 43, 893-896.
30. Girstmair, H., Saffert, P., Rode, S., Czech, A., Holland, G., Bannert, N. and Ignatova, Z. (2013) Depletion of cognate charged transfer RNA causes translational frameshifting within the expanded CAG stretch in huntingtin. Cell Rep., 3, 148-159.
31. Mann, D.M., Rollinson, S., Robinson, A., Bennion Callister, J., Thompson, J.C., Snowden, J.S., Gendron, T., Petrucelli, L., Masuda-Suzukake, M., Hasegawa, M. et al. (2013) Dipeptide repeat proteins are present in the p62 positive inclusions in patients with frontotemporal lobar degeneration and motor neurone disease associated with expansions in C9ORF72. Acta Neuropathol. Commun., 1, 68.
32. Mackenzie, I.R., Arzberger, T., Kremmer, E., Troost, D., Lorenzl, S., Mori, K., Weng, S.M., Haass, C., Kretzschmar, H.A., Edbauer, D. et al. (2013) Dipeptide repeat protein pathology in C9ORF72 mutation cases: clinico-pathological correlations. Acta Neuropathol., 126, 859-879.
33. Cooper-Knock, J., Walsh, M.J., Higginbottom, A., Robin Highley, J., Dickman, M.J., Edbauer, D., Ince, P.G., Wharton, S.B., Wilson, S.A., Kirby, J. et al. (2014) Sequestration of multiple RNA recognition motif-containing proteins by C9orf72 repeat expansions. Brain, 137, 2040-2051.
34. Murray, M.E., Bieniek, K.F., Banks Greenberg, M., DeJesus-Hernandez, M., Rutherford, N.J., van Blitterswijk, M., Niemantsverdriet, E., Ash, P.E., Gendron, T.F., Kouri, N. et al. (2013) Progressive amnestic dementia, hippocampal sclerosis, and mutation in C9ORF72. Acta Neuropathol., 126, 545-554.
35. Pletnikova, O., Sloane, K.L., Renton, A.E., Traynor, B.J., Crain, B.J., Reid, T., Zu, T., Ranum, L.P., Troncoso, J.C., Rabins, P.V. et al. (2014) Hippocampal sclerosis dementia with the C9ORF72 hexanucleotide repeat expansion. Neurobiol. Aging, 35, 2419.e17-2419.e21.
36. Proudfoot, M., Gutowski, N.J., Edbauer, D., Hilton, D.A., Stephens, M., Rankin, J. and Mackenzie, I.R. (2014) Early dipeptide repeat pathology in a frontotemporal dementia kindred with C9ORF72 mutation and intellectual disability. Acta Neuropathol., 127, 451-458.
37. Liu, E.Y., Russ, J., Wu, K., Neal, D., Suh, E., McNally, A.G., Irwin, D.J., Van Deerlin, V.M. and Lee, E.B. (2014) C9orf72 hypermethylation protects against repeat expansion-associated pathology in ALS/FTD. Acta Neuropathol., doi:10.1007/s00401-014-1286-y.
38. Sareen, D., O'Rourke, J.G., Meera, P., Muhammad, A.K., Grant, S., Simpkinson, M., Bell, S., Carmona, S., Ornelas, L., Sahabian, A. et al. (2013) Targeting RNA foci in iPSC-derived motor neurons from ALS patients with a C9ORF72 repeat expansion. Sci. Transl. Med., 5, 208ra149.
39. Kwon, I., Xiang, S., Kato, M., Wu, L., Theodoropoulos, P., Wang, T., Kim, J., Yun, J., Xie, Y. and McKnight, S.L. (2014) Poly-dipeptides encoded by the C9ORF72 repeats bind nucleoli, impede RNA biogenesis, and kill cells. Science, pii:1254917.
40. Landles, C., Sathasivam, K., Weiss, A., Woodman, B., Moffitt, H., Finkbeiner, S., Sun, B., Gafni, J., Ellerby, L.M., Trottier, Y. et al. (2010) 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.
41. Ross, C.A. and Tabrizi, S.J. (2011) Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol., 10, 83-98.
42. Arrasate, M., Mitra, S., Schweitzer, E.S., Segal, M.R. and Finkbeiner, S. (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature, 431, 805-810.
43. Wolfe, K.J. and Cyr, D.M. (2011) Amyloid in neurodegenerative diseases: friend or foe? Semin. Cell Dev. Biol., 22, 476-481.
44. Napierala, M., Michalowski, D., de Mezer, M. and Krzyzosiak, W.J. (2005) Facile FMR1 mRNA structure regulation by interruptions in CGG repeats. Nucleic Acids Res., 33, 451-463.
45. Schaeffer, C., Bardoni, B., Mandel, J.L., Ehresmann, B., Ehresmann, C. and Moine, H. (2001) The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. Embo J., 20, 4803-4813.
46. Khateb, S., Weisman-Shomer, P., Hershco-Shani, I., Ludwig, A.L. and Fry, M. (2007) The tetraplex (CGG)n destabilizing proteins hnRNP A2 and CBF-A enhance the in vivo translation of fragile X premutation mRNA. Nucleic Acids Res., 35, 5775-5788.
47. Reddy, K., Zamiri, B., Stanley, S.Y., Macgregor, R.B. Jr. and Pearson, C.E. (2013) The disease-associated r(GGGGCC)n repeat from the C9orf72 gene forms tract length-dependent uni- and multimolecular RNA G-quadruplex structures. J. Biol. Chem., 288, 9860-9866.
48. Chiang, P.W., Carpenter, L.E. and Hagerman, P.J. (2001) The 5'-untranslated region of the FMR1 message facilitates translation by internal ribosome entry. J. Biol. Chem., 276, 37916-37921.
49. Kieft, J.S. (2008) Viral IRES RNA structures and ribosome interactions. Trends Biochem. Sci., 33, 274-283.
50. Filbin, M.E. and Kieft, J.S. (2009) Toward a structural understanding of IRES RNA function. Curr. Opin. Struct. Biol., 19, 267-276.
51. Krzyzosiak, W.J., Sobczak, K., Wojciechowska, M., Fiszer, A., Mykowska, A. and Kozlowski, P. (2012) Triplet repeat RNA structure and its role as pathogenic agent and therapeutic target. Nucleic Acids Res., 40, 11-26.
52. Sobczak, K., Michlewski, G., de Mezer, M., Kierzek, E., Krol, J., Olejniczak, M., Kierzek, R. and Krzyzosiak, W.J. (2010) Structural diversity of triplet repeat RNAs. J. Biol. Chem., 285, 12755-12764.
53. Kiliszek, A., Kierzek, R., Krzyzosiak, W.J. and Rypniewski, W. (2009) Structural insights into CUG repeats containing the 'stretched U-U wobble': implications for myotonic dystrophy. Nucleic Acids Res., 37, 4149-4156.
54. Kiliszek, A., Kierzek, R., Krzyzosiak, W.J. and Rypniewski, W. (2010) Atomic resolution structure of CAG RNA repeats: structural insights and implications for the trinucleotide repeat expansion diseases. Nucleic Acids Res., 38, 8370-8376.
55. Kiliszek, A., Kierzek, R., Krzyzosiak, W.J. and Rypniewski, W. (2011) Crystal structures of CGG RNA repeats with implications for fragile X-associated tremor ataxia syndrome. Nucleic Acids Res., 39, 7308-7315.
56. Jasinska, A., Michlewski, G., de Mezer, M., Sobczak, K., Kozlowski, P., Napierala, M. and Krzyzosiak, W.J. (2003) Structures of trinucleotide repeats in human transcripts and their functional implications. Nucleic Acids Res., 31, 5463-5468.
57. Sobczak, K. and Krzyzosiak, W.J. (2005) CAG repeats containing CAA interruptions form branched hairpin structures in spinocerebellar ataxia type 2 transcripts. J. Biol. Chem., 280, 3898-3910.
58. Payet, L. and Huppert, J.L. (2012) Stability and structure of long intramolecular G-quadruplexes. Biochemistry, 51, 3154-3161.
59. Wong, H.M. and Huppert, J.L. (2009) Stable G-quadruplexes are found outside nucleosome-bound regions. Mol. Biosyst., 5, 1713-1719.
60. Bugaut, A. and Balasubramanian, S. (2012) 5'-UTR RNA G-quadruplexes: translation regulation and targeting. Nucleic Acids Res., 40, 4727-4741.
61. Peabody, D.S. (1989) Translation initiation at non-AUG triplets in mammalian cells. J. Biol. Chem., 264, 5031-5035.
62. Martinez-Salas, E., Lozano, G., Fernandez-Chamorro, J., Francisco-Velilla, R., Galan, A. and Diaz, R. (2013) RNA-binding proteins impacting on internal initiation of translation. Int. J. Mol. Sci., 14, 21705-21726.
63. Pestova, T.V., de Breyne, S., Pisarev, A.V., Abaeva, I.S. and Hellen, C.U. (2008) eIF2-dependent and eIF2-independent modes of initiation on the CSFV IRES: a common role of domain II. Embo J., 27, 1060-1072.
64. Terenin, I.M., Dmitriev, S.E., Andreev, D.E. and Shatsky, I.N. (2008) Eukaryotic translation initiation machinery can operate in a bacterial-like mode without eIF2. Nat. Struct. Mol. Biol., 15, 836-841.
65. Dmitriev, S.E., Terenin, I.M., Andreev, D.E., Ivanov, P.A., Dunaevsky, J.E., Merrick, W.C. and Shatsky, I.N. (2010) GTP-independent tRNA delivery to the ribosomal P-site by a novel eukaryotic translation factor. J. Biol. Chem., 285, 26779-26787.
66. Skabkin, M.A., Skabkina, O.V., Dhote, V., Komar, A.A., Hellen, C.U. and Pestova, T.V. (2010) Activities of Ligatin and MCT-1/DENR in eukaryotic translation initiation and ribosomal recycling. Genes Dev., 24, 1787-1801.
67. Komar, A.A. and Hatzoglou, M. (2011) Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle, 10, 229-240.
68. Miller, J.W., Urbinati, C.R., Teng-Umnuay, P., Stenberg, M.G., Byrne, B.J., Thornton, C.A. and Swanson, M.S. (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. Embo J., 19, 4439-4448.
69. Houseley, J.M., Wang, Z., Brock, G.J., Soloway, J., Artero, R., Perez-Alonso, M., O'Dell, K.M. and Monckton, D.G. (2005) Myotonic dystrophy associated expanded CUG repeat muscleblind positive ribonuclear foci are not toxic to Drosophila. Hum. Mol. Genet., 14, 873-883.
70. Fardaei, M., Larkin, K., Brook, J.D. and Hamshere, M.G. (2001) In vivo co-localisation ofMBNL protein with DMPK expanded-repeat transcripts. Nucleic Acids Res., 29, 2766-2771.
71. Huichalaf, C., Sakai, K., Jin, B., Jones, K., Wang, G.L., Schoser, B., Schneider-Gold, C., Sarkar, P., Pereira-Smith, O.M., Timchenko, N. et al. (2010) Expansion of CUG RNA repeats causes stress and inhibition of translation in myotonic dystrophy 1 (DM1) cells. Faseb J., 24, 3706-3719.
72. Huichalaf, C., Schoser, B., Schneider-Gold, C., Jin, B., Sarkar, P. and Timchenko, L. (2009) Reduction of the rate of protein translation in patients with myotonic dystrophy 2. J. Neurosci., 29, 9042-9049.
73. Botta, A., Malena, A., Loro, E., Del Moro, G., Suman, M., Pantic, B., Szabadkai, G. and Vergani, L. (2013) Altered Ca2+ homeostasis and endoplasmic reticulum stress in myotonic dystrophy type 1 muscle cells. Genes (Basel), 4, 275-292.
74. Ikezoe, K., Nakamori, M., Furuya, H., Arahata, H., Kanemoto, S., Kimura, T., Imaizumi, K., Takahashi, M.P., Sakoda, S., Fujii, N. et al. (2007) Endoplasmic reticulum stress in myotonic dystrophy type 1 muscle. Acta Neuropathol., 114, 527-535.
75. Reineke, L.C., Cao, Y., Baus, D., Hossain, N.M. and Merrick, W.C. (2011) Insights into the role of yeast eIF2A in IRES-mediated translation. PLoS One, 6, e24492.
76. Tsoi, H. and Chan, H.Y. (2013) Expression of expanded CAG transcripts triggers nucleolar stress in Huntington's disease. Cerebellum, 12, 310-312.
77. Tsoi, H., Lau, T.C., Tsang, S.Y., Lau, K.F. and Chan, H.Y. (2012) CAG expansion induces nucleolar stress in polyglutamine diseases. Proc. Natl. Acad. Sci. U.S.A., 109, 13428-13433.
78. 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. et al. (2014) C9orf72 nucleotide repeat structures initiate molecular cascades of disease. Nature, 507, 195-200.
79. Berger, Z., Davies, J.E., Luo, S., Pasco, M.Y., Majoul, I., O'Kane, C.J. and Rubinsztein, D.C. (2006) Deleterious and protective properties of an aggregate-prone protein with a polyalanine expansion. Hum. Mol. Genet., 15, 453-465.
80. Gonitel, R., Moffitt, H., Sathasivam, K., Woodman, B., Detloff, P.J., Faull, R.L. and Bates, G.P. (2008) DNA instability in postmitotic neurons. Proc. Natl. Acad. Sci. U.S.A., 105, 3467-3472.
81. Kennedy, L., Evans, E., Chen, C.M., Craven, L., Detloff, P.J., Ennis, M. and Shelbourne, P.F. (2003) Dramatic tissue-specific mutation length increases are an early molecular event in Huntington disease pathogenesis. Hum. Mol. Genet., 12, 3359-3367.
82. Clark, M.B., Janicke, M., Gottesbuhren, U., Kleffmann, T., Legge, M., Poole, E.S. and Tate, W.P. (2007) Mammalian gene PEG10 expresses two reading frames by high efficiency -1 frameshifting in embryonic-associated tissues. J. Biol. Chem., 282, 37359-37369.
83. Manktelow, E., Shigemoto, K. and Brierley, I. (2005) Characterization of the frameshift signal of Edr, a mammalian example of programmed -1 ribosomal frameshifting. Nucleic Acids Res., 33, 1553-1563.
84. Brierley, I., Jenner, A.J. and Inglis, S.C. (1992) Mutational analysis of the "slippery-sequence" component of a coronavirus ribosomal frameshifting signal. J. Mol. Biol., 227, 463-479.
85. Namy, O., Moran, S.J., Stuart, D.I., Gilbert, R.J. and Brierley, I. (2006) A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting. Nature, 441, 244-247.
86. Baril, M., Dulude, D., Steinberg, S.V. and Brakier-Gingras, L. (2003) The frameshift stimulatory signal of human immunodeficiency virus type 1 group O is a pseudoknot. J. Mol. Biol., 331, 571-583.
87. Yu, C.H., Noteborn, M.H., Pleij, C.W. and Olsthoorn, R.C. (2011) Stem-loop structures can effectively substitute for an RNA pseudoknot in -1 ribosomal frameshifting. Nucleic Acids Res., 39, 8952-8959.
88. Yu, C.H., Teulade-Fichou, M.P. and Olsthoorn, R.C. (2014) Stimulation of ribosomal frameshifting by RNA G-quadruplex structures. Nucleic Acids Res., 42, 1887-1892.
89. Endoh, T., Kawasaki, Y. and Sugimoto, N. (2013) Suppression of gene expression by G-quadruplexes in open reading frames depends on G-quadruplex stability. Angew. Chem. Int. Ed. Engl., 52, 5522-5526.
90. Howard, M.T., Gesteland, R.F. and Atkins, J.F. (2004) Efficient stimulation of site-specific ribosome frameshifting by antisense oligonucleotides. RNA, 10, 1653-1661.
91. Jacks, T. and Varmus, H.E. (1985) Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science, 230, 1237-1242.
92. Harger, J.W., Meskauskas, A. and Dinman, J.D. (2002) An "integrated model" of programmed ribosomal frameshifting. Trends Biochem. Sci., 27, 448-454.
93. Leger, M., Dulude, D., Steinberg, S.V. and Brakier-Gingras, L. (2007) The three transfer RNAs occupying the A, P and E sites on the ribosome are involved in viral programmed -1 ribosomal frameshift. Nucleic Acids Res., 35, 5581-5592.
94. Liao, P.Y., Choi, Y.S., Dinman, J.D. and Lee, K.H. (2011) The many paths to frameshifting: kinetic modelling and analysis of the effects of different elongation steps on programmed -1 ribosomal frameshifting. Nucleic Acids Res., 39, 300-312.
95. Mouzakis, K.D., Lang, A.L., Vander Meulen, K.A., Easterday, P.D. and Butcher, S.E. (2013) HIV-1 frameshift efficiency is primarily determined by the stability of base pairs positioned at the mRNA entrance channel of the ribosome. Nucleic Acids Res., 41, 1901-1913.
96. Plant, E.P., Jacobs, K.L., Harger, J.W., Meskauskas, A., Jacobs, J.L., Baxter, J.L., Petrov, A.N. and Dinman, J.D. (2003) The 9-A solution: how mRNA pseudoknots promote efficient programmed -1 ribosomal frameshifting. RNA, 9, 168-174.
97. Weiss, R.B., Dunn, D.M., Shuh, M., Atkins, J.F. and Gesteland, R.F. (1989) E. coli ribosomes re-phase on retroviral frameshift signals at rates ranging from 2 to 50 percent. New Biol., 1, 159-169.
98. Busan, S. and Weeks, K.M. (2013) Role of context in RNA structure: flanking sequences reconfigure CAG motif folding in huntingtin exon 1 transcripts. Biochemistry, 52, 8219-8225.
99. de Mezer, M., Wojciechowska, M., Napierala, M., Sobczak, K. and Krzyzosiaka, W.J. (2011) Mutant CAG repeats of Huntingtin transcript fold into hairpins, form nuclear foci and are targets for RNA interference. Nucleic Acids Res., 39, 3852-3863.
100. Michlewski, G. and Krzyzosiak, W.J. (2004) Molecular architecture of CAG repeats in human disease related transcripts. J. Mol. Biol., 340, 665-679.
101. Dulude, D., Baril, M. and Brakier-Gingras, L. (2002) Characterization of the frameshift stimulatory signal controlling a programmed -1 ribosomal frameshift in the human immunodeficiency virus type 1. Nucleic Acids Res., 30, 5094-5102.
102. Gaudin, C., Mazauric, M.H., Traikia, M., Guittet, E., Yoshizawa, S. and Fourmy, D. (2005) Structure of the RNA signal essential for translational frameshifting in HIV-1. J. Mol. Biol., 349, 1024-1035.
103. Wills, N.M. and Atkins, J.F. (2006) The potential role of ribosomal frameshifting in generating aberrant proteins implicated in neurodegenerative diseases. RNA, 12, 1149-1153.
104. Kollmus, H., Hentze, M.W. and Hauser, H. (1996) Regulated ribosomal frameshifting by an RNA-protein interaction. RNA, 2, 316-323.
105. Landwehrmeyer, G.B., McNeil, S.M., Dure, L.S.t., Ge, P., Aizawa, H., Huang, Q., Ambrose, C.M., Duyao, M.P., Bird, E.D., Bonilla, E. et al. (1995) Huntington's disease gene: regional and cellular expression in brain of normal and affected individuals. Ann. Neurol., 37, 218-230.
106. Craigen, W.J. and Caskey, C.T. (1986) Expression of peptide chain release factor 2 requires high-efficiency frameshift. Nature, 322, 273-275.
107. Belcourt, M.F. and Farabaugh, P.J. (1990) Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell, 62, 339-352.
108. Morris, D.K. and Lundblad, V. (1997) Programmed translational frameshifting in a gene required for yeast telomere replication. Curr. Biol., 7, 969-976.
109. Kawakami, K., Pande, S., Faiola, B., Moore, D.P., Boeke, J.D., Farabaugh, P.J., Strathern, J.N., Nakamura, Y. and Garfinkel, D.J. (1993) A rare tRNA-Arg(CCU) that regulates Ty1 element ribosomal frameshifting is essential for Ty1 retrotransposition in Saccharomyces cerevisiae. Genetics, 135, 309-320.
110. Lindsley, D. and Gallant, J. (1993) On the directional specificity of ribosome frameshifting at a "hungry" codon. Proc. Natl. Acad. Sci. U.S.A., 90, 5469-5473.
111. Slavoff, S.A., Mitchell, A.J., Schwaid, A.G., Cabili, M.N., Ma, J., Levin, J.Z., Karger, A.D., Budnik, B.A., Rinn, J.L. and Saghatelian, A. (2013) Peptidomic discovery of short open reading frame-encoded peptides in human cells. Nat. Chem. Biol., 9, 59-64.
112. Ma, J., Ward, C.C., Jungreis, I., Slavoff, S.A., Schwaid, A.G., Neveu, J., Budnik, B.A., Kellis, M. and Saghatelian, A. (2014) Discovery of human sORF-encoded polypeptides (SEPs) in cell lines and tissue. J. Proteome Res., 13, 1757-1765.
113. Somers, J., Poyry, T. and Willis, A.E. (2013) A perspective on mammalian upstream open reading frame function. Int. J. Biochem. Cell Biol., 45, 1690-1700.
114. Apcher, S., Daskalogianni, C., Lejeune, F., Manoury, B., Imhoos, G., Heslop, L. and Fahraeus, R. (2011) Major source of antigenic peptides for the MHC class I pathway is produced during the pioneer round of mRNA translation. Proc. Natl. Acad. Sci. U.S.A., 108, 11572-11577.
115. Starck, S.R., Ow, Y., Jiang, V., Tokuyama, M., Rivera, M., Qi, X., Roberts, R.W. and Shastri, N. (2008) A distinct translation initiation mechanism generates cryptic peptides for immune surveillance. PLoS One, 3, e3460.