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Drugging Pre-mRNA Splicing

  • Matthew G. WollEmail author
  • Nikolai A. Naryshkin
  • Gary M. Karp
Chapter
  • 2k Downloads
Part of the Topics in Medicinal Chemistry book series (TMC, volume 27)

Abstract

The splicing of precursor messenger RNA (pre-mRNA) requires the precise cleavage and formation of multiple phosphodiester bonds in nascent pre-mRNA polymers in order to produce a protein coding message that can be properly translated by the ribosome. Despite the precision of this process, the spliceosome maintains considerable flexibility to include, or not include, defined segments in the final message, thus allowing for the production of diverse transcripts with distinct functions from a single gene sequence. The combination of control and flexibility displayed by the spliceosome, in conjunction with input from cis-acting sequences and trans factors, presents a unique opportunity for molecular intervention during gene expression. Various chemical agents have the capacity to alter the natural process of pre-mRNA splicing, thereby producing levels of splicing products different than those found under natural conditions. This approach has powerful therapeutic utility where mutation has caused certain splice variants to be under- or over-represented. The following chapter highlights the exceptional advances that have been achieved recently in splicing modulation with splice switching oligonucleotides (SSOs) and small molecules, the two leading therapeutic modalities in this field.

Keywords

Alternative splicing Duchenne muscular dystrophy Exon skipping Familial dysautonomia Pre-mRNA splicing Spinal muscular atrophy Splice switching oligonucleotides Spliceosome 

References

  1. 1.
    Sharp PA (2005) Trends Biochem Sci 30:279CrossRefGoogle Scholar
  2. 2.
    Lee Y, Rio DC (2015) Annu Rev Biochem 84:291CrossRefGoogle Scholar
  3. 3.
    Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Nature 456:470CrossRefGoogle Scholar
  4. 4.
    Merkin J, Russell C, Chen P, Burge CB (2012) Science 338:1593CrossRefGoogle Scholar
  5. 5.
    Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, Lee LJ, Slobodeniuc V, Kutter C, Watt S, Colak R, Kim T, Misquitta-Ali CM, Wilson MD, Kim PM, Odom DT, Frey BJ, Blencowe BJ (2012) Science 338:1587CrossRefGoogle Scholar
  6. 6.
    Reyes A, Anders S, Weatheritt RJ, Gibson TJ, Steinmetz LM, Huber W (2013) Proc Natl Acad Sci U S A 110:15377CrossRefGoogle Scholar
  7. 7.
    Melé M, Ferreira PG, Reverter F, DeLuca DS, Monlong J, Sammeth M, Young TR, Goldmann JM, Pervouchine DD, Sullivan TJ, Johnson R, Segrè AV, Djebali S, Niarchou A, The GTEx Consortium, Wright FA, Lappalainen T, Calvo M, Getz G, Dermitzakis ET, Ardlie KG, Guigó R (2015) Science 348:660CrossRefGoogle Scholar
  8. 8.
    Tress ML, Abascal F, Valencia A (2017) Trends Biochem Sci 42:98CrossRefGoogle Scholar
  9. 9.
    Mudge JM, Frankish A, Fernandez-Banet J, Alioto T, Derrien T, Howald C, Reymond A, Guigó R, Hubbard T, Harrow J (2011) Mol Biol Evol 28:2949CrossRefGoogle Scholar
  10. 10.
    Cascino I, Fiucci G, Papoff G, Ruberti G (1995) J Immunol 154:2706Google Scholar
  11. 11.
    Medina MW, Gao F, Naidoo D, Rudel LL, Temel RE, McDaniel AL, Marshall SM, Krauss RM (2011) PLoS One 6(4):e19420CrossRefGoogle Scholar
  12. 12.
    Lareau LF, Brenner SE (2015) Mol Biol Evol 32:1072CrossRefGoogle Scholar
  13. 13.
    van Roon-Mom WMC, Aartsma-Rus A (2012) Methods Mol Biol 867:79CrossRefGoogle Scholar
  14. 14.
    Havens MA, Duelli DM, Hastings ML (2013) WIREs RNA 4:247CrossRefGoogle Scholar
  15. 15.
    Eteplirsen NDA #206466. www.fda.gov
  16. 16.
    Nusinersen NDA #209531. www.fda.gov
  17. 17.
    Lefebvre S, Bürglen L, Reboullet S, Clermont O, Burlet P, Viollet L, Benichou B, Cruaud C, Millasseau P, Zeviani M, Paslier DL, Frézal J, Cohen D, Weissenbach J, Munnich A, Melki J (1995) Cell 80:155CrossRefGoogle Scholar
  18. 18.
    Lorson CL, Hahnen E, Androphy J, Wirth B (1999) Proc Natl Acad Sci U S A 96:6307CrossRefGoogle Scholar
  19. 19.
    Cho S, Dreyfuss G (2010) Genes Dev 24:438CrossRefGoogle Scholar
  20. 20.
    Burnett BG, Muñoz E, Tandon A, Kwon DY, Sumner CJ, Fischbeck KH (2009) Mol Cell Biol 29:1107CrossRefGoogle Scholar
  21. 21.
    Baughan TD, Dickson A, Osman EY, Lorson CL (2009) Hum Mol Genet 18:1600CrossRefGoogle Scholar
  22. 22.
    Hua Y, Vickers TA, Baker BF, Bennett CF, Krainer AR (2007) PLoS Biol 5:729CrossRefGoogle Scholar
  23. 23.
    Hua Y, Vickers TA, Okunola HL, Bennett CF, Krainer AR (2008) Am J Hum Genet 82:834CrossRefGoogle Scholar
  24. 24.
    Singh NK, Singh NN, Androphy EJ, Singh RN (2006) Mol Cell Biol 26:1333CrossRefGoogle Scholar
  25. 25.
    Lim SR, Hertel KJ (2001) J Biol Chem 276:45476CrossRefGoogle Scholar
  26. 26.
    Madocsai C, Lim SR, Geib T, Lam BJ, Hertel KJ (2005) Mol Ther 12:1013CrossRefGoogle Scholar
  27. 27.
    Dickson A, Osman E, Lorson CL (2008) Hum Gene Ther 19:1307CrossRefGoogle Scholar
  28. 28.
    Odermatt P, Trüb J, Furrer L, Fricker R, Marti A, Schümperli D (2016) Mol Ther 24:1797CrossRefGoogle Scholar
  29. 29.
    Williams JH, Schray RC, Patterson CA, Ayitey SO, Tallent MK, Lutz GJ (2009) J Neurosci 29:7633CrossRefGoogle Scholar
  30. 30.
    Hua Y, Sahashi K, Rigo F, Hung G, Horev G, Bennett CF, Krainer AR (2011) Nature 478:123CrossRefGoogle Scholar
  31. 31.
    Porensky PN, Mitrpant C, McGovern VL, Bevan AK, Foust KD, Kaspar BK, Wilton SD, Burghes AHM (2012) Hum Mol Genet 21:1625CrossRefGoogle Scholar
  32. 32.
    Zhou H, Janghra N, Mitrpant C, Dickinson RL, Anthony K, Price L, Eperon IC, Wilton SD, Morgan J, Muntoni F (2013) Hum Gene Ther 24:331CrossRefGoogle Scholar
  33. 33.
    Hsieh-Li HM, Chang JG, Jong YJ, Wu MH, Wang NM, Tsai CH, Li H (2000) Nat Genet 24:66CrossRefGoogle Scholar
  34. 34.
    Passini MA, Bu J, Richards AM, Kinnecom C, Sardi SP, Stanek LM, Hua Y, Rigo F, Matson J, Hung G, Kaye EM, Shihabuddin LS, Krainer AR, Bennett CF, Cheng SH (2011) Sci Transl Med 3:72ra18CrossRefGoogle Scholar
  35. 35.
    Mitrpant C, Porensky P, Zhou H, Price L, Muntoni F, Fletcher S, Wilton SD, Burghes AHM (2013) PLoS One 8:e62114CrossRefGoogle Scholar
  36. 36.
    Dervan PB, Edelson BS (2003) Curr Opin Struct Biol 13:284CrossRefGoogle Scholar
  37. 37.
    Thomas JR, Hergenrother PJ (2008) Chem Rev 108:1171CrossRefGoogle Scholar
  38. 38.
    Guan L, Disney MD (2012) ACS Chem Biol 7:73CrossRefGoogle Scholar
  39. 39.
    Rzuczek SG, Colgan LA, Nakai Y, Cameron MD, Furling D, Yasuda R, Disney MD (2017) Nat Chem Biol 13:188CrossRefGoogle Scholar
  40. 40.
    Woll MG, Qi H, Turpoff A, Zhang N, Zhang X, Chen G, Li C, Huang S, Yang T, Moon Y-C, Lee C-S, Choi S, Almstead NG, Naryshkin NA, Dakka A, Narasimhan J, Gabbeta V, Welch E, Zhao X, Risher N, Sheedy J, Weetall M, Karp GM (2016) J Med Chem 59:6070CrossRefGoogle Scholar
  41. 41.
    Naryshkin NA, Weetall M, Dakka A, Narasimhan J, Zhao X, Feng Z, Ling KKY, Karp GM, Qi H, Woll MG, Chen G, Zhang N, Gabbeta V, Vazirani P, Bhattacharyya A, Furia B, Risher N, Sheedy J, Kong R, Ma J, Turpoff A, Lee CS, Zhang X, Moon Y-C, Trifillis P, Welch EM, Colacino JM, Babiak J, Almstead NG, Peltz SW, Eng LA, Chen KS, Mull JL, Lynes MS, Rubin LL, Fontoura P, Santarelli L, Haehnke D, McCarthy KD, Schmucki R, Ebeling M, Sivaramakrishnan M, Ko C-P, Paushkin SV, Ratni H, Gerlach I, Ghosh A, Metzger F (2014) Science 345:688CrossRefGoogle Scholar
  42. 42.
    Ratni H, Karp GM, Weetall M, Naryshkin NA, Paushkin SV, Chen KS, McCarthy KD, Qi H, Turpoff A, Woll MG, Zhang X, Zhang N, Yang T, Dakka A, Vazirani P, Zhao X, Pinard E, Green L, David-Pierson P, Tuerck D, Poirier A, Muster W, Kirchner S, Mueller L, Gerlach I, Metzger F (2016) J Med Chem 59:6086CrossRefGoogle Scholar
  43. 43.
    SMN2 splicing modifier RG7800 increases SMN protein in first study in SMA patients. In: World Muscle Society Congress, Brighton, UK, 30 Sept–4 Oct 2015Google Scholar
  44. 44.
    Palacino J, Swalley SE, Song C, Cheung AK, Shu L, Zhang X, Van Hoosear M, Shin Y, Chin DN, Keller CG, Beibel M, Renaud NA, Smith TA, Salcius M, Shi X, Hild M, Servais R, Jain M, Deng L, Bullock C, McLellan M, Schuierer S, Murphy L, Blommers MJJ, Blaustein C, Berenshteyn F, Lacoste A, Thomas JR, Roma G, Michaud GA, Tseng BS, Porter JA, Myer VE, Tallarico JA, Hamann LG, Curtis D, Fishman MC, Dietrich WF, Dales NA, Sivasankaran R (2015) Nat Chem Biol 11:511CrossRefGoogle Scholar
  45. 46.
    Anderson SL, Coli R, Daly IW, Kichula EA, Rork MJ, Volpi SA, Ekstein J, Rubin BY (2001) Am J Hum Genet 68:753CrossRefGoogle Scholar
  46. 47.
    Slaugenhaupt SA, Blumenfeld A, Gill SP, Leyne M, Mull J, Cuajungco MP, Liebert CB, Chadwick B, Idelson M, Reznik L, Robbins CM, Makalowska I, Brownstein MJ, Krappmann D, Scheidereit C, Maayan C, Axelrod FB, Gusella JF (2001) Am J Hum Genet 68:598CrossRefGoogle Scholar
  47. 48.
    Ibrahim EC, Hims MM, Shomron N, Burge CB, Slaugenhaupt SA, Reed R (2007) Hum Mutat 28:41CrossRefGoogle Scholar
  48. 49.
    Slaugenhaupt SA, Mull J, Leyne M, Cuajungco MP, Gill SP, Hims MM, Quintero F, Axelrod FB, Gusella JF (2004) Hum Mol Genet 13:429CrossRefGoogle Scholar
  49. 50.
    Cuajungco MP, Leyne M, Mull J, Gill SP, Lu W, Zagzag D, Axelrod FB, Maayan C, Gusella JF, Slaugenhaupt SA (2003) Am J Hum Genet 72:749CrossRefGoogle Scholar
  50. 51.
    Anderson SL, Qiu J, Rubin BY (2003) Biochem Biophys Res Commun 310:627CrossRefGoogle Scholar
  51. 52.
    Keren H, Donyo M, Zeevi D, Maayan C, Pupko T, Ast G (2010) PLoS One 5:e15884CrossRefGoogle Scholar
  52. 53.
    Liu B, Anderson SL, Qiu J, Rubin BY (2013) FEBS J 280:3632CrossRefGoogle Scholar
  53. 54.
    Hims MM, Ibrahim EC, Leyne M, Mull J, Liu L, Lazaro C, Shetty RS, Gill S, Gusella JF, Reed R, Slaugenhaupt SA (2007) J Mol Med 85:149CrossRefGoogle Scholar
  54. 55.
    Hims MM, Shetty RS, Pickel J, Mull J, Leyne M, Liu L, Gusella JF, Slaugenhaupt SA (2007) Genomics 90:389CrossRefGoogle Scholar
  55. 56.
    Shetty RS, Gallagher CS, Chen YT, Hims MM, Mull J, Leyne M, Pickel J, Kwok D, Slaugenhaupt SA (2011) Hum Mol Genet 20:4093CrossRefGoogle Scholar
  56. 57.
    Axelrod FB, Liebes L, Gold-Von Simson G, Mendoza S, Mull J, Leyne M, Norcliffe-Kaufmann L, Kaufmann H, Slaugenhaupt SA (2011) Pediatr Res 70:480CrossRefGoogle Scholar
  57. 58.
    Slaugenhaupt SA, Johnson G, Paquette WD, Zhang W, Marugan J (2016) WO 2016115434 A1Google Scholar
  58. 59.
    Yoshida M, Kataoka N, Miyauchi K, Ohe K, Iida K, Yoshida S, Nojima T, Okuno Y, Onogi H, Usui T, Takeuchi A, Hosoya T, Suzuki T, Hagiwara M (2015) Proc Natl Acad Sci U S A 112:2764CrossRefGoogle Scholar
  59. 60.
    Monaco AP, Neve RL, Colletti-Feener C, Bertelson CJ, Kurnit DM, Kunkel LM (1986) Nature 323:646CrossRefGoogle Scholar
  60. 61.
    Monaco AP, Bertelson CJ, Liechti-Gallati S, Moser H, Kunkel KL (1988) Genomics 2:90CrossRefGoogle Scholar
  61. 62.
    Aartsma-Rus A, Fokkema I, Verschuuren J, Ginjaar I, van Deutekom J, van Ommen GJ, den Dunnen JT (2009) Hum Mutat 30:293CrossRefGoogle Scholar
  62. 63.
    Nicholson LV, Davison K, Johnson MA, Slater CR, Young C, Bhattacharya S, Gardner-Medwin D, Harris JB (1989) J Neurol Sci 94:137CrossRefGoogle Scholar
  63. 64.
    Fanin M, Danieli GA, Vitiello L, Senter L, Angelini C (1992) Neuromuscul Disord 2:41CrossRefGoogle Scholar
  64. 65.
    Arechavala-Gomeza V, Kinali M, Feng L, Guglieri M, Edge G, Main M, Hunt D, Lehovsky J, Straub V, Bushby K, Sewry CA, Morgan JE, Muntoni F (2010) Neuromuscul Disord 20:295CrossRefGoogle Scholar
  65. 66.
    Pigozzo SR, Da Re L, Romualdi C, Mazzara PG, Galletta E, Fletcher S, Wilton SD, Vitiello L (2013) PLoS One 28:e72147CrossRefGoogle Scholar
  66. 67.
    Bulfield G, Siller WG, Wight PA, Moore KJ (1984) Proc Natl Acad Sci U S A 81:1189CrossRefGoogle Scholar
  67. 68.
    Lu QL, Morris GE, Wilton SD, Ly T, Artem’yeva OV, Strong P, Partridge TA (2000) J Cell Biol 148:985CrossRefGoogle Scholar
  68. 69.
    Wilton SD, Dye DE, Laing NG (1997) Muscle Nerve 20:728CrossRefGoogle Scholar
  69. 70.
    Bladen CL, Salgado D, Monges S, Foncuberta ME, Kekou K, Kosma K, Dawkins H, Lamont L, Roy AJ, Chamova T, Guergueltcheva V, Chan S, Korngut L, Campbell C, Dai Y, Wang J, Barišić N, Brabec P, Lahdetie J, Walter MC, Schreiber-Katz O, Karcagi V, Garami M, Viswanathan V, Bayat F, Buccella F, Kimura E, Koeks Z, van den Bergen JC, Rodrigues M, Roxburgh R, Lusakowska A, Kostera-Pruszczyk A, Zimowski J, Santos R, Neagu E, Artemieva S, Rasic VM, Vojinovic D, Posada M, Bloetzer C, Jeannet PY, Joncourt F, Díaz-Manera J, Gallardo E, Karaduman AA, Topaloğlu H, El Sherif R, Stringer A, Shatillo AV, Martin AS, Peay HL, Bellgard MI, Kirschner J, Flanigan KM, Straub V, Bushby K, Verschuuren J, Aartsma-Rus A, Béroud C, Lochmüller H (2015) Hum Mutat 36:395CrossRefGoogle Scholar
  70. 71.
    Matsuo M, Masumura T, Nishio H, Nakajima T, Kitoh Y, Takumi T, Koga J, Nakamura H (1991) J Clin Invest 87:2127CrossRefGoogle Scholar
  71. 72.
    Takeshima Y, Nishio H, Sakamoto H, Nakamura H, Matsuo M (1995) J Clin Invest 95:515CrossRefGoogle Scholar
  72. 73.
    Pramono ZA, Takeshima Y, Alimsardjono H, Ishii A, Takeda S, Matsuo M (1996) Biochem Biophys Res Commun 226:445CrossRefGoogle Scholar
  73. 74.
    Takeshima Y, Wada H, Yagi M, Ishikawa Y, Ishikawa Y, Minami R, Nakamura H, Matsuo M (2001) Brain Dev 23:788CrossRefGoogle Scholar
  74. 75.
    Takeshima Y, Yagi M, Wada H, Matsuo M (2005) Brain Dev 27:488CrossRefGoogle Scholar
  75. 76.
    Takeshima Y, Yagi M, Wada H, Ishibashi K, Nishiyama A, Kakumoto M, Sakaeda T, Saura R, Okumura K, Matsuo M (2006) Pediatr Res 59:690CrossRefGoogle Scholar
  76. 77.
    Klein CJ, Coovert DD, Bulman DE, Ray PN, Mendell JR, Burghes AH (1992) Am J Hum Genet 50:950Google Scholar
  77. 78.
    Wallgren-Pettersson C, Jasani B, Rosser LG, Lazarou LP, Nicholson LVB, Clarke A (1993) J Neurol Sci 118:56CrossRefGoogle Scholar
  78. 79.
    Wilton SD, Lloyd F, Carville K, Fletcher S, Honeyman K, Agrawal S (1999) Neuromuscul Disord 9:330CrossRefGoogle Scholar
  79. 80.
    Dunckley MG, Manoharan M, Villiet P, Eperon IC, Dickson G (1998) Hum Mol Genet 7:1083CrossRefGoogle Scholar
  80. 81.
    van Deutekom JC, Bremmer-Bout M, Janson AA, Ginjaar IB, Baas F, den Dunnen JT, van Ommen GJ (2001) Hum Mol Genet 10:1547CrossRefGoogle Scholar
  81. 82.
    Bremmer-Bout M, Aartsma-Rus A, De Meijer EJ, Kaman WE, Janson AAM, Vossen RHAM, Van Ommen G-JB, Den Dunnen JT, Van Deutekom JCT (2004) Mol Ther 10:232CrossRefGoogle Scholar
  82. 83.
    Aartsma-Rus A, De Winter CL, Janson AA, Kaman WE, Van Ommen GJ, Den Dunnen JT, Van Deutekom JC (2005) Oligonucleotides 15:284CrossRefGoogle Scholar
  83. 84.
    Wilton SD, Fall AM, Harding PL, McClorey G, Coleman C, Fletcher S (2007) Mol Ther 15:1288CrossRefGoogle Scholar
  84. 85.
    Adkin CF, Meloni PL, Fletcher S, Adams AM, Muntoni F, Wong B, Wilton SD (2012) Neuromuscul Disord 22:297CrossRefGoogle Scholar
  85. 86.
    Aartsma-Rus A, Janson AAM, Kaman WE, Bremmer-Bout M, van Ommen G-JB, den Dunnen JT, van Deutekom JCT (2004) Am J Hum Genet 74:83CrossRefGoogle Scholar
  86. 87.
    Mitrpant C, Fletcher S, Wilton SD (2009) Curr Mol Pharmacol 2:110CrossRefGoogle Scholar
  87. 88.
    Jarver P, O’Donovan L, Gait MJ (2014) Nucleic Acids Ther 24:37CrossRefGoogle Scholar
  88. 89.
    Aartsma-Rus A, Kaman WE, Bremmer-Bout M, Janson AA, den Dunnen JT, van Ommen GJ, van Deutekom JC (2004) Gene Ther 11:1391CrossRefGoogle Scholar
  89. 90.
    Arzumanov A, Walsh AP, Rajwanshi VK, Kumar R, Wengel J, Gait MJ (2001) Biochemistry 40:14645CrossRefGoogle Scholar
  90. 91.
    Saleh AF, Arzumanov AA, Gait MJ (2012) Methods Mol Biol 867:365CrossRefGoogle Scholar
  91. 92.
    Fletcher S, Honeyman K, Fall AM, Harding PL, Johnsen RD, Wilton SD (2006) J Gene Med 8:207CrossRefGoogle Scholar
  92. 93.
    Yin H, Betts C, Saleh AF, Ivanova GD, Lee H, Seow Y, Kim D, Gait MJ, Wood MJ (2010) Mol Ther 18:819CrossRefGoogle Scholar
  93. 94.
    Goyenvalle A, Griffith G, Babbs A, El Andaloussi S, Ezzat K, Avril A, Dugovic B, Chaussenot R, Ferry A, Voit T, Amthor H, Bühr C, Schürch S, Wood MJ, Davies KE, Vaillend C, Leumann C, Garcia L (2015) Nat Med 21:270Google Scholar
  94. 95.
    Summerton J, Weller D (1997) Antisense Nucleic Acid Drug Dev 7:187CrossRefGoogle Scholar
  95. 96.
    Popplewell LJ, Adkin C, Arechavala-Gomeza V, Aartsma-Rus A, de Winter CL, Wilton SD, Morgan JE, Muntoni F, Graham IR, Dickson G (2010) Neuromuscul Disord 20:102CrossRefGoogle Scholar
  96. 97.
    Aartsma-Rus A (2010) RNA Biol 7:453CrossRefGoogle Scholar
  97. 98.
    Heemskerk HA, de Winter CL, de Kimpe SJ, van Kuik-Romeijn P, Heuvelmans N, Platenburg GJ, van Ommen GJ, van Deutekom JC, Aartsma-Rus A (2009) J Gene Med 11:257CrossRefGoogle Scholar
  98. 99.
    Vila MC, Klimek MB, Novak JS, Rayavarapu S, Uaesoontrachoon K, Boehler JF, Fiorillo AA, Hogarth MW, Zhang A, Shaughnessy C, Gordish-Dressman H, Burki U, Straub V, Lu QL, Partridge TA, Brown KJ, Hathout Y, van den Anker J, Hoffman EP, Nagaraju K (2015) Skelet Muscle 5:44CrossRefGoogle Scholar
  99. 100.
    Alter J, Lou F, Rabinowitz A, Yin H, Rosenfeld J, Wilton SD, Partridge TA, Lu QL (2006) Nat Med 12:175CrossRefGoogle Scholar
  100. 101.
    Yokota T, Lu QL, Partridge T, Kobayashi M, Nakamura A, Takeda S, Hoffman E (2009) Ann Neurol 65:667CrossRefGoogle Scholar
  101. 102.
    Aoki Y, Yokota T, Nagata T, Nakamura A, Tanihata J, Saito T, Duguez SM, Nagaraju K, Hoffman EP, Partridge T, Takeda S (2012) Proc Natl Acad Sci U S A 109:13763CrossRefGoogle Scholar
  102. 103.
    Echigoya Y, Aoki Y, Miskew B, Panesar D, Touznik A, Nagata T, Tanihata J, Nakamura A, Nagaraju K, Yokota T (2015) Mol Ther Nucleic Acids 4:e225CrossRefGoogle Scholar
  103. 104.
    Echigoya Y, Yokota T (2014) Nucleic Acid Ther 24:57CrossRefGoogle Scholar
  104. 105.
    Lebleu B, Moulton HM, Abes R, Ivanova GD, Abes S, Stein DA, Iversen PL, Arzumanov AA, Gait MJ (2008) Adv Drug Deliv Rev 60:517CrossRefGoogle Scholar
  105. 106.
    Boisguérin P, Deshayes S, Gait MJ, O’Donovan L, Godfrey C, Betts CA, Wood MJ, Lebleu B (2015) Adv Drug Deliv Rev 87:52CrossRefGoogle Scholar
  106. 107.
    Jirka SM, Heemskerk H, Tanganyika-de Winter CL, Muilwijk D, Pang KH, de Visser PC, Janson A, Karnaoukh TG, Vermue R, ’t Hoen PA, van Deutekom JC, Aguilera B, Aartsma-Rus A (2014) Nucleic Acid Ther 24:25CrossRefGoogle Scholar
  107. 108.
    Hammond SM, Hazell G, Shabanpoor F, Saleh AF, Bowerman M, Sleigh JN, Meijboom KE, Zhou H, Muntoni F, Talbot K, Gait MJ, Wood MJ (2016) Proc Natl Acad Sci U S A 113:10962CrossRefGoogle Scholar
  108. 109.
    Fletcher S, Honeyman K, Fall AM, Harding PL, Johnsen RD, Steinhaus JP, Moulton HM, Iversen PL, Wilton SD (2007) Mol Ther 15:1587CrossRefGoogle Scholar
  109. 110.
    Wu B, Moulton HM, Iverson PL, Jiang J, Li J, Li J, Spurney CF, Sali A, Guerron AD, Nagaraju K, Doran T, Lu P, Xiao X, Lu QL (2008) PNAS 105:14814CrossRefGoogle Scholar
  110. 111.
    Moulton HM, Moulton JD (2010) Biochim Biophys Acta 1798:2296CrossRefGoogle Scholar
  111. 112.
    van Westering TL, Betts CA, Wood MJ (2015) Molecules 20:8823CrossRefGoogle Scholar
  112. 113.
    Amantana A, Moulton HM, Cate ML, Reddy MT, Whitehead T, Hassinger JN, Youngblood DS, Iversen PL (2007) Bioconjug Chem 18:1325CrossRefGoogle Scholar
  113. 114.
    Incitti T, De Angelis FG, Cazzella V, Sthandier O, Pinnarò C, Legnini I, Bozzoni I (2010) Mol Ther 18:1675CrossRefGoogle Scholar
  114. 115.
    Cazzella V, Martone J, Pinnarò C, Santini T, Twayana SS, Sthandier O, D’Amico A, Ricotti V, Bertini E, Muntoni F, Bozzoni I (2012) Mol Ther 20:2134CrossRefGoogle Scholar
  115. 116.
    De Angelis FG, Sthandier O, Berarducci B, Toso S, Galluzzi G, Ricci E, Cossu G, Bozzoni I (2002) Proc Natl Acad Sci U S A 99:9456CrossRefGoogle Scholar
  116. 117.
    Martone J, De Angelis FG, Bozzoni I (2012) Methods Mol Biol 867:239CrossRefGoogle Scholar
  117. 118.
    Goyenvalle A, Vulin A, Fougerousse F, Leturcq F, Kaplan JC, Garcia L, Danos O (2004) Science 306:1796CrossRefGoogle Scholar
  118. 119.
    Vulin A, Barthélémy I, Goyenvalle A, Thibaud JL, Beley C, Griffith G, Benchaouir R, le Hir M, Unterfinger Y, Lorain S, Dreyfus P, Voit T, Carlier P, Blot S, Garcia L (2012) Mol Ther 20:2120CrossRefGoogle Scholar
  119. 120.
    Goyenvalle A (2012) Methods Mol Biol 867:259CrossRefGoogle Scholar
  120. 121.
    Sharma M, McFarlane C, Kambadur R, Kukreti H, Bonala S, Srinivasan S (2015) IUBMB Life 67:589CrossRefGoogle Scholar
  121. 122.
    Kang JK, Malerba A, Popplewell L, Foster K, Dickson G (2011) Mol Ther 19:159CrossRefGoogle Scholar
  122. 123.
    Kemaladewi DU, Hoogaars WM, van Heiningen SH, Terlouw S, de Gorter DJ, den Dunnen JT, van Ommen GJ, Aartsma-Rus A, ten Dijke P, ’t Hoen PA (2011) BMC Med Genomics 4:36CrossRefGoogle Scholar
  123. 124.
    Lu-Nguyen NB, Jarmin SA, Saleh AF, Popplewell L, Gait MJ, Dickson G (2015) Mol Ther 23:1341CrossRefGoogle Scholar
  124. 125.
    Amthor H, Macharia R, Navarrete R, Schuelke M, Brown SB, Otto A, Voit T, Muntoni F, Vrbova G, Partridge T, Zammit P, Bunger L, Patel K (2007) Proc Natl Acad Sci U S A 104:1835CrossRefGoogle Scholar
  125. 126.
    Koo T, Wood MJ (2013) Hum Gene Ther 24:479CrossRefGoogle Scholar
  126. 127.
    Shimizu-Motohashi Y, Miyatake S, Komaki H, Takeda S, Aoki Y (2016) Am J Transl Res 8:2471Google Scholar
  127. 128.
    Havens MA, Hastings ML (2016) Nucleic Acids Res 44:6549CrossRefGoogle Scholar
  128. 129.
    van Deutekom JC, Janson AA, Ginjaar IB, Frankhuizen WS, Aartsma-Rus A, Bremmer-Bout M, den Dunnen JT, Koop K, van der Kooi AJ, Goemans NM, de Kimpe SJ, Ekhart PF, Venneker EH, Platenburg GJ, Verschuuren JJ, van Ommen GJ (2007) N Engl J Med 357:2677CrossRefGoogle Scholar
  129. 130.
    Kinali M, Arechavala-Gomeza V, Feng L, Cirak S, Hunt D, Adkin C, Guglieri M, Ashton E, Abbs S, Nihoyannopoulos P, Garralda ME, Rutherford M, McCulley C, Popplewell L, Graham IR, Dickson G, Wood MJ, Wells DJ, Wilton SD, Kole R, Straub V, Bushby K, Sewry C, Morgan JE, Muntoni F (2009) Lancet Neurol 8:918CrossRefGoogle Scholar
  130. 131.
    Muraki M, Ohkawara B, Hosoya T, Onogi H, Koizumi J, Koizumi T, Sumi K, Yomoda J, Murray MV, Kimura H, Furuichi K, Shibuya H, Krainer AR, Suzuki M, Hagiwara M (2004) J Biol Chem 279:24246CrossRefGoogle Scholar
  131. 132.
    Nishida A, Kataoka N, Takeshima Y, Yagi M, Awano H, Ota M, Itoh K, Hagiwara M, Matsuo M (2011) Nat Commun 2:308CrossRefGoogle Scholar
  132. 133.
    Kendall GC, Mokhonova EI, Moran M, Sejbuk NE, Wang DW, Silva O, Wang RT, Martinez L, Lu QL, Damoiseaux R, Spencer MJ, Nelson SF, Miceli MC (2012) Sci Transl Med 4:164CrossRefGoogle Scholar
  133. 134.
    Hu Y, Wu B, Zillmer A, Lu P, Benrashid E, Wang M, Doran T, Shaban M, Wu X, Lu QL (2010) Mol Ther 18:812CrossRefGoogle Scholar
  134. 135.
    Verhaart IE, Aartsma-Rus A (2012) PLoS Curr 4Google Scholar
  135. 136.
    Bonnal S, Vigevani L, Valcárcel J (2012) Nat Rev Drug Discov 11:847CrossRefGoogle Scholar
  136. 137.
    Salton M, Misteli T (2016) Trends Mol Med 22:28CrossRefGoogle Scholar
  137. 138.
    Nakajima H, Hori Y, Terano H, Okuhara M, Manda T, Matsumoto S, Shimomura K (1996) J Antibiot (Tokyo) 49:1204CrossRefGoogle Scholar
  138. 139.
    Kaida D, Motoyoshi H, Tashiro E, Nojima T, Hagiwara M, Ishigami K, Watanabe H, Kitahara T, Yoshida T, Nakajima H, Tani T, Horinouchi S, Yoshida M (2007) Nat Chem Biol 3:576CrossRefGoogle Scholar
  139. 140.
    Mizui Y, Sakai T, Iwata M, Uenaka T, Okamoto K, Shimizu H, Yamori T, Yoshimatsu K, Asada M (2004) J Antibiot (Tokyo) 57:188CrossRefGoogle Scholar
  140. 141.
    Kotake Y, Sagane K, Owa T, Mimori-Kiyosue Y, Shimizu H, Uesugi M, Ishihama Y, Iwata M, Mizui Y (2007) Nat Chem Biol 3:570CrossRefGoogle Scholar
  141. 142.
    Albert BJ, McPherson PA, O’Brien K, Czaicki NL, Destefino V, Osman S, Li M, Day BW, Grabowski PJ, Moore MJ, Vogt A, Koide K (2009) Mol Cancer Ther 8:2308CrossRefGoogle Scholar
  142. 143.
    Fan L, Lagisetti C, Edwards CC, Webb TR, Potter PM (2011) ACS Chem Biol 6:582CrossRefGoogle Scholar
  143. 144.
    Hasegawa M, Miura T, Kuzuya K, Inoue A, Won Ki S, Horinouchi S, Yoshida T, Kunoh T, Koseki K, Mino K, Sasaki R, Yoshida M, Mizukami T (2011) ACS Chem Biol 6:229CrossRefGoogle Scholar
  144. 145.
    Effenberger KA, Urabe VK, Prichard BE, Ghosh AK, Jurica MS (2016) RNA 22:350CrossRefGoogle Scholar
  145. 146.
    Roybal GA, Jurica MS (2010) Nucleic Acids Res 38:6664CrossRefGoogle Scholar
  146. 147.
    Corrionero A, Miñana B, Valcárcel J (2011) Genes Dev 25:445CrossRefGoogle Scholar
  147. 148.
    Effenberger KA, Urabe VK, Jurica MS (2016) WIREs RNA 8:e1381. doi: 10.1002/wrna.1381 CrossRefGoogle Scholar
  148. 149.
    Iwata M, Ozawa Y, Uenaka T, Shimizu H, Niijima J, Kanada RM, Fukuda Y, Nagai M, Kotake Y, Yoshida M, Tsuchida T, Mizui Y, Yoshimatsu K, Asada M (2004) Proc Am Assoc Cancer Res 45:691Google Scholar
  149. 150.
    Hong DS, Kurzrock R, Naing A, Wheler JJ, Falchook GS, Schiffman JS, Faulkner N, Pilat MJ, O’Brien J, LoRusso P (2014) Invest New Drugs 32:436CrossRefGoogle Scholar
  150. 151.
    O’Brien K, Matlin AJ, Lowell AM, Moore MJ (2008) J Biol Chem 283:33147CrossRefGoogle Scholar
  151. 152.
    Yoon SO, Shin S, Lee HJ, Chun HK, Chung AS (2006) Mol Cancer Ther 5:2666CrossRefGoogle Scholar
  152. 153.
    Samatov TR, Wolf A, Odenwälder P, Bessonov S, Deraeve C, Bon RS, Waldmann H, Lührmann R (2012) Chembiochem 13:640CrossRefGoogle Scholar
  153. 154.
    Pawellek A, McElroy S, Samatov T, Mitchell L, Woodland A, Ryder U, Gray D, Lührmann R, Lamond AI (2014) J Biol Chem 289:34683CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Matthew G. Woll
    • 1
    Email author
  • Nikolai A. Naryshkin
    • 1
  • Gary M. Karp
    • 1
  1. 1.PTC TherapeuticsSouth PlainfieldUSA

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