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.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Sharp PA (2005) Trends Biochem Sci 30:279
Lee Y, Rio DC (2015) Annu Rev Biochem 84:291
Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Nature 456:470
Merkin J, Russell C, Chen P, Burge CB (2012) Science 338:1593
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 338:1587
Reyes A, Anders S, Weatheritt RJ, Gibson TJ, Steinmetz LM, Huber W (2013) Proc Natl Acad Sci U S A 110:15377
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 348:660
Tress ML, Abascal F, Valencia A (2017) Trends Biochem Sci 42:98
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 28:2949
Cascino I, Fiucci G, Papoff G, Ruberti G (1995) J Immunol 154:2706
Medina MW, Gao F, Naidoo D, Rudel LL, Temel RE, McDaniel AL, Marshall SM, Krauss RM (2011) PLoS One 6(4):e19420
Lareau LF, Brenner SE (2015) Mol Biol Evol 32:1072
van Roon-Mom WMC, Aartsma-Rus A (2012) Methods Mol Biol 867:79
Havens MA, Duelli DM, Hastings ML (2013) WIREs RNA 4:247
Eteplirsen NDA #206466. www.fda.gov
Nusinersen NDA #209531. www.fda.gov
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 80:155
Lorson CL, Hahnen E, Androphy J, Wirth B (1999) Proc Natl Acad Sci U S A 96:6307
Cho S, Dreyfuss G (2010) Genes Dev 24:438
Burnett BG, Muñoz E, Tandon A, Kwon DY, Sumner CJ, Fischbeck KH (2009) Mol Cell Biol 29:1107
Baughan TD, Dickson A, Osman EY, Lorson CL (2009) Hum Mol Genet 18:1600
Hua Y, Vickers TA, Baker BF, Bennett CF, Krainer AR (2007) PLoS Biol 5:729
Hua Y, Vickers TA, Okunola HL, Bennett CF, Krainer AR (2008) Am J Hum Genet 82:834
Singh NK, Singh NN, Androphy EJ, Singh RN (2006) Mol Cell Biol 26:1333
Lim SR, Hertel KJ (2001) J Biol Chem 276:45476
Madocsai C, Lim SR, Geib T, Lam BJ, Hertel KJ (2005) Mol Ther 12:1013
Dickson A, Osman E, Lorson CL (2008) Hum Gene Ther 19:1307
Odermatt P, Trüb J, Furrer L, Fricker R, Marti A, Schümperli D (2016) Mol Ther 24:1797
Williams JH, Schray RC, Patterson CA, Ayitey SO, Tallent MK, Lutz GJ (2009) J Neurosci 29:7633
Hua Y, Sahashi K, Rigo F, Hung G, Horev G, Bennett CF, Krainer AR (2011) Nature 478:123
Porensky PN, Mitrpant C, McGovern VL, Bevan AK, Foust KD, Kaspar BK, Wilton SD, Burghes AHM (2012) Hum Mol Genet 21:1625
Zhou H, Janghra N, Mitrpant C, Dickinson RL, Anthony K, Price L, Eperon IC, Wilton SD, Morgan J, Muntoni F (2013) Hum Gene Ther 24:331
Hsieh-Li HM, Chang JG, Jong YJ, Wu MH, Wang NM, Tsai CH, Li H (2000) Nat Genet 24:66
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 3:72ra18
Mitrpant C, Porensky P, Zhou H, Price L, Muntoni F, Fletcher S, Wilton SD, Burghes AHM (2013) PLoS One 8:e62114
Dervan PB, Edelson BS (2003) Curr Opin Struct Biol 13:284
Thomas JR, Hergenrother PJ (2008) Chem Rev 108:1171
Guan L, Disney MD (2012) ACS Chem Biol 7:73
Rzuczek SG, Colgan LA, Nakai Y, Cameron MD, Furling D, Yasuda R, Disney MD (2017) Nat Chem Biol 13:188
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 59:6070
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 345:688
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 59:6086
SMN2 splicing modifier RG7800 increases SMN protein in first study in SMA patients. In: World Muscle Society Congress, Brighton, UK, 30 Sept–4 Oct 2015
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 11:511
Anderson SL, Coli R, Daly IW, Kichula EA, Rork MJ, Volpi SA, Ekstein J, Rubin BY (2001) Am J Hum Genet 68:753
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 68:598
Ibrahim EC, Hims MM, Shomron N, Burge CB, Slaugenhaupt SA, Reed R (2007) Hum Mutat 28:41
Slaugenhaupt SA, Mull J, Leyne M, Cuajungco MP, Gill SP, Hims MM, Quintero F, Axelrod FB, Gusella JF (2004) Hum Mol Genet 13:429
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 72:749
Anderson SL, Qiu J, Rubin BY (2003) Biochem Biophys Res Commun 310:627
Keren H, Donyo M, Zeevi D, Maayan C, Pupko T, Ast G (2010) PLoS One 5:e15884
Liu B, Anderson SL, Qiu J, Rubin BY (2013) FEBS J 280:3632
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 85:149
Hims MM, Shetty RS, Pickel J, Mull J, Leyne M, Liu L, Gusella JF, Slaugenhaupt SA (2007) Genomics 90:389
Shetty RS, Gallagher CS, Chen YT, Hims MM, Mull J, Leyne M, Pickel J, Kwok D, Slaugenhaupt SA (2011) Hum Mol Genet 20:4093
Axelrod FB, Liebes L, Gold-Von Simson G, Mendoza S, Mull J, Leyne M, Norcliffe-Kaufmann L, Kaufmann H, Slaugenhaupt SA (2011) Pediatr Res 70:480
Slaugenhaupt SA, Johnson G, Paquette WD, Zhang W, Marugan J (2016) WO 2016115434 A1
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 112:2764
Monaco AP, Neve RL, Colletti-Feener C, Bertelson CJ, Kurnit DM, Kunkel LM (1986) Nature 323:646
Monaco AP, Bertelson CJ, Liechti-Gallati S, Moser H, Kunkel KL (1988) Genomics 2:90
Aartsma-Rus A, Fokkema I, Verschuuren J, Ginjaar I, van Deutekom J, van Ommen GJ, den Dunnen JT (2009) Hum Mutat 30:293
Nicholson LV, Davison K, Johnson MA, Slater CR, Young C, Bhattacharya S, Gardner-Medwin D, Harris JB (1989) J Neurol Sci 94:137
Fanin M, Danieli GA, Vitiello L, Senter L, Angelini C (1992) Neuromuscul Disord 2:41
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 20:295
Pigozzo SR, Da Re L, Romualdi C, Mazzara PG, Galletta E, Fletcher S, Wilton SD, Vitiello L (2013) PLoS One 28:e72147
Bulfield G, Siller WG, Wight PA, Moore KJ (1984) Proc Natl Acad Sci U S A 81:1189
Lu QL, Morris GE, Wilton SD, Ly T, Artem’yeva OV, Strong P, Partridge TA (2000) J Cell Biol 148:985
Wilton SD, Dye DE, Laing NG (1997) Muscle Nerve 20:728
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 36:395
Matsuo M, Masumura T, Nishio H, Nakajima T, Kitoh Y, Takumi T, Koga J, Nakamura H (1991) J Clin Invest 87:2127
Takeshima Y, Nishio H, Sakamoto H, Nakamura H, Matsuo M (1995) J Clin Invest 95:515
Pramono ZA, Takeshima Y, Alimsardjono H, Ishii A, Takeda S, Matsuo M (1996) Biochem Biophys Res Commun 226:445
Takeshima Y, Wada H, Yagi M, Ishikawa Y, Ishikawa Y, Minami R, Nakamura H, Matsuo M (2001) Brain Dev 23:788
Takeshima Y, Yagi M, Wada H, Matsuo M (2005) Brain Dev 27:488
Takeshima Y, Yagi M, Wada H, Ishibashi K, Nishiyama A, Kakumoto M, Sakaeda T, Saura R, Okumura K, Matsuo M (2006) Pediatr Res 59:690
Klein CJ, Coovert DD, Bulman DE, Ray PN, Mendell JR, Burghes AH (1992) Am J Hum Genet 50:950
Wallgren-Pettersson C, Jasani B, Rosser LG, Lazarou LP, Nicholson LVB, Clarke A (1993) J Neurol Sci 118:56
Wilton SD, Lloyd F, Carville K, Fletcher S, Honeyman K, Agrawal S (1999) Neuromuscul Disord 9:330
Dunckley MG, Manoharan M, Villiet P, Eperon IC, Dickson G (1998) Hum Mol Genet 7:1083
van Deutekom JC, Bremmer-Bout M, Janson AA, Ginjaar IB, Baas F, den Dunnen JT, van Ommen GJ (2001) Hum Mol Genet 10:1547
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 10:232
Aartsma-Rus A, De Winter CL, Janson AA, Kaman WE, Van Ommen GJ, Den Dunnen JT, Van Deutekom JC (2005) Oligonucleotides 15:284
Wilton SD, Fall AM, Harding PL, McClorey G, Coleman C, Fletcher S (2007) Mol Ther 15:1288
Adkin CF, Meloni PL, Fletcher S, Adams AM, Muntoni F, Wong B, Wilton SD (2012) Neuromuscul Disord 22:297
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 74:83
Mitrpant C, Fletcher S, Wilton SD (2009) Curr Mol Pharmacol 2:110
Jarver P, O’Donovan L, Gait MJ (2014) Nucleic Acids Ther 24:37
Aartsma-Rus A, Kaman WE, Bremmer-Bout M, Janson AA, den Dunnen JT, van Ommen GJ, van Deutekom JC (2004) Gene Ther 11:1391
Arzumanov A, Walsh AP, Rajwanshi VK, Kumar R, Wengel J, Gait MJ (2001) Biochemistry 40:14645
Saleh AF, Arzumanov AA, Gait MJ (2012) Methods Mol Biol 867:365
Fletcher S, Honeyman K, Fall AM, Harding PL, Johnsen RD, Wilton SD (2006) J Gene Med 8:207
Yin H, Betts C, Saleh AF, Ivanova GD, Lee H, Seow Y, Kim D, Gait MJ, Wood MJ (2010) Mol Ther 18:819
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 21:270
Summerton J, Weller D (1997) Antisense Nucleic Acid Drug Dev 7:187
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 20:102
Aartsma-Rus A (2010) RNA Biol 7:453
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 11:257
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 5:44
Alter J, Lou F, Rabinowitz A, Yin H, Rosenfeld J, Wilton SD, Partridge TA, Lu QL (2006) Nat Med 12:175
Yokota T, Lu QL, Partridge T, Kobayashi M, Nakamura A, Takeda S, Hoffman E (2009) Ann Neurol 65:667
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 109:13763
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:e225
Echigoya Y, Yokota T (2014) Nucleic Acid Ther 24:57
Lebleu B, Moulton HM, Abes R, Ivanova GD, Abes S, Stein DA, Iversen PL, Arzumanov AA, Gait MJ (2008) Adv Drug Deliv Rev 60:517
Boisguérin P, Deshayes S, Gait MJ, O’Donovan L, Godfrey C, Betts CA, Wood MJ, Lebleu B (2015) Adv Drug Deliv Rev 87:52
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 24:25
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 113:10962
Fletcher S, Honeyman K, Fall AM, Harding PL, Johnsen RD, Steinhaus JP, Moulton HM, Iversen PL, Wilton SD (2007) Mol Ther 15:1587
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 105:14814
Moulton HM, Moulton JD (2010) Biochim Biophys Acta 1798:2296
van Westering TL, Betts CA, Wood MJ (2015) Molecules 20:8823
Amantana A, Moulton HM, Cate ML, Reddy MT, Whitehead T, Hassinger JN, Youngblood DS, Iversen PL (2007) Bioconjug Chem 18:1325
Incitti T, De Angelis FG, Cazzella V, Sthandier O, Pinnarò C, Legnini I, Bozzoni I (2010) Mol Ther 18:1675
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 20:2134
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 99:9456
Martone J, De Angelis FG, Bozzoni I (2012) Methods Mol Biol 867:239
Goyenvalle A, Vulin A, Fougerousse F, Leturcq F, Kaplan JC, Garcia L, Danos O (2004) Science 306:1796
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 20:2120
Goyenvalle A (2012) Methods Mol Biol 867:259
Sharma M, McFarlane C, Kambadur R, Kukreti H, Bonala S, Srinivasan S (2015) IUBMB Life 67:589
Kang JK, Malerba A, Popplewell L, Foster K, Dickson G (2011) Mol Ther 19:159
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 4:36
Lu-Nguyen NB, Jarmin SA, Saleh AF, Popplewell L, Gait MJ, Dickson G (2015) Mol Ther 23:1341
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 104:1835
Koo T, Wood MJ (2013) Hum Gene Ther 24:479
Shimizu-Motohashi Y, Miyatake S, Komaki H, Takeda S, Aoki Y (2016) Am J Transl Res 8:2471
Havens MA, Hastings ML (2016) Nucleic Acids Res 44:6549
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 357:2677
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 8:918
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 279:24246
Nishida A, Kataoka N, Takeshima Y, Yagi M, Awano H, Ota M, Itoh K, Hagiwara M, Matsuo M (2011) Nat Commun 2:308
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 4:164
Hu Y, Wu B, Zillmer A, Lu P, Benrashid E, Wang M, Doran T, Shaban M, Wu X, Lu QL (2010) Mol Ther 18:812
Verhaart IE, Aartsma-Rus A (2012) PLoS Curr 4
Bonnal S, Vigevani L, Valcárcel J (2012) Nat Rev Drug Discov 11:847
Salton M, Misteli T (2016) Trends Mol Med 22:28
Nakajima H, Hori Y, Terano H, Okuhara M, Manda T, Matsumoto S, Shimomura K (1996) J Antibiot (Tokyo) 49:1204
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 3:576
Mizui Y, Sakai T, Iwata M, Uenaka T, Okamoto K, Shimizu H, Yamori T, Yoshimatsu K, Asada M (2004) J Antibiot (Tokyo) 57:188
Kotake Y, Sagane K, Owa T, Mimori-Kiyosue Y, Shimizu H, Uesugi M, Ishihama Y, Iwata M, Mizui Y (2007) Nat Chem Biol 3:570
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 8:2308
Fan L, Lagisetti C, Edwards CC, Webb TR, Potter PM (2011) ACS Chem Biol 6:582
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 6:229
Effenberger KA, Urabe VK, Prichard BE, Ghosh AK, Jurica MS (2016) RNA 22:350
Roybal GA, Jurica MS (2010) Nucleic Acids Res 38:6664
Corrionero A, Miñana B, Valcárcel J (2011) Genes Dev 25:445
Effenberger KA, Urabe VK, Jurica MS (2016) WIREs RNA 8:e1381. doi:10.1002/wrna.1381
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 45:691
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 32:436
O’Brien K, Matlin AJ, Lowell AM, Moore MJ (2008) J Biol Chem 283:33147
Yoon SO, Shin S, Lee HJ, Chun HK, Chung AS (2006) Mol Cancer Ther 5:2666
Samatov TR, Wolf A, Odenwälder P, Bessonov S, Deraeve C, Bon RS, Waldmann H, Lührmann R (2012) Chembiochem 13:640
Pawellek A, McElroy S, Samatov T, Mitchell L, Woodland A, Ryder U, Gray D, Lührmann R, Lamond AI (2014) J Biol Chem 289:34683
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Woll, M.G., Naryshkin, N.A., Karp, G.M. (2017). Drugging Pre-mRNA Splicing. In: Garner, A. (eds) RNA Therapeutics. Topics in Medicinal Chemistry, vol 27. Springer, Cham. https://doi.org/10.1007/7355_2017_12
Download citation
DOI: https://doi.org/10.1007/7355_2017_12
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-68090-3
Online ISBN: 978-3-319-68091-0
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)