Emerging roles of spliceosome in cancer and immunity
Hui Yang, Bruce Beutler, Duanwu Zhang
Emerging roles of spliceosome in cancer and immunity
Precursor messenger RNA (pre-mRNA) splicing is catalyzed by an intricate ribonucleoprotein complex called the spliceosome. Although the spliceosome is considered to be general cell “housekeeping” machinery, mutations in core components of the spliceosome frequently correlate with cellor tissue-specific phenotypes and diseases. In this review, we expound the links between spliceosome mutations, aberrant splicing, and human cancers. Remarkably, spliceosome-targeted therapies (STTs) have become efficient anti-cancer strategies for cancer patients with splicing defects. We also highlight the links between spliceosome and immune signaling. Recent studies have shown that some spliceosome gene mutations can result in immune dysregulation and notable phenotypes due to missplicing of immune-related genes. Furthermore, several core spliceosome components harbor splicing-independent immune functions within the cell, expanding the functional repertoire of these diverse proteins.
spliceosome / splicing / cancer / innate immunity / immune dysregulation
[1] |
Adler AS , McCleland ML, Yee S, Yaylaoglu M, Hussain S, Cosino E, Quinones G, Modrusan Z, Seshagiri S, Torres E
CrossRef
Google scholar
|
[2] |
Albers CA, Paul DS, Schulze H, Freson K, Stephens JC, Smethurst PA, Jolley JD, Cvejic A, Kostadima M, Bertone P
CrossRef
Google scholar
|
[3] |
Alsafadi S, Houy A, Battistella A, Popova T, Wassef M, Henry E, Tirode F, Constantinou A, Piperno-Neumann S, Roman-Roman S
CrossRef
Google scholar
|
[4] |
Anczukow O, Krainer AR ( 2016) Splicing-factor alterations in cancers . RNA 22: 1285– 1301
CrossRef
Google scholar
|
[5] |
Argente J, Flores R, Gutierrez-Arumi A, Verma B, Martos-Moreno GA, Cusco I, Oghabian A, Chowen JA, Frilander MJ, Perez-Jurado LA ( 2014) Defective minor spliceosome mRNA processing results in isolated familial growth hormone deficiency . EMBO Mol Med 6: 299– 306
CrossRef
Google scholar
|
[6] |
Bacrot S, Doyard M, Huber C, Alibeu O, Feldhahn N, Lehalle D, Lacombe D, Marlin S, Nitschke P, Petit F
CrossRef
Google scholar
|
[7] |
Bailey P, Chang DK, Nones K, Johns AL, Patch AM, Gingras MC, Miller DK, Christ AN, Bruxner TJ, Quinn MC
CrossRef
Google scholar
|
[8] |
Baldridge MT, King KY, Goodell MA ( 2011) Inflammatory signals regulate hematopoietic stem cells . Trends Immunol 32: 57– 65
CrossRef
Google scholar
|
[9] |
Bejar R, Stevenson KE, Caughey BA, Abdel-Wahab O, Steensma DP, Galili N, Raza A, Kantarjian H, Levine RL, Neuberg D
CrossRef
Google scholar
|
[10] |
Bernier FP, Caluseriu O, Ng S, Schwartzentruber J, Buckingham KJ, Innes AM, Jabs EW, Innis JW, Schuette JL, Gorski JL
CrossRef
Google scholar
|
[11] |
Bersanelli M, Travaglino E, Meggendorfer M, Matteuzzi T, Sala C, Mosca E, Chiereghin C, Di Nanni N, Gnocchi M, Zampini M
CrossRef
Google scholar
|
[12] |
Blaustein M, Pelisch F, Tanos T, Munoz MJ, Wengier D, Quadrana L, Sanford JR, Muschietti JP, Kornblihtt AR, Caceres JF
CrossRef
Google scholar
|
[13] |
Boguslawska J, Sokol E, Rybicka B, Czubaty A, Rodzik K, Piekielko-Witkowska A ( 2016) microRNAs target SRSF7 splicing factor to modulate the expression of osteopontin splice variants in renal cancer cells . Gene 595: 142– 149
CrossRef
Google scholar
|
[14] |
Bonnal SC, Lopez-Oreja I, Valcarcel J ( 2020) Roles and mecha-nisms of alternative splicing in cancer- implications for care . Nat Rev Clin Oncol 17: 457– 474
CrossRef
Google scholar
|
[15] |
Bowling EA, Wang JH, Gong F, Wu W, Neill NJ, Kim IS, Tyagi S, Orellana M, Kurley SJ, Dominguez-Vidana R
CrossRef
Google scholar
|
[16] |
Brooks AN, Choi PS, de Waal L, Sharifnia T, Imielinski M, Saksena G, Pedamallu CS, Sivachenko A, Rosenberg M, Chmielecki J
CrossRef
Google scholar
|
[17] |
Burge CB, Padgett RA, Sharp PA ( 1998) Evolutionary fates and origins of U12-type introns . Mol Cell 2: 773– 785
CrossRef
Google scholar
|
[18] |
Chakarova CF, Hims MM, Bolz H, Abu-Safieh L, Patel RJ, Papaioannou MG, Inglehearn CF, Keen TJ, Willis C, Moore AT
CrossRef
Google scholar
|
[19] |
Chen X, Liu Y, Sheng X, Tam PO, Zhao K, Chen X, Rong W, Liu Y, Liu X, Pan X
CrossRef
Google scholar
|
[20] |
Corbett MA, Dudding-Byth T, Crock PA, Botta E, Christie LM, Nardo T, Caligiuri G, Hobson L, Boyle J, Mansour A
CrossRef
Google scholar
|
[21] |
Corbo C, Orru S, Gemei M, Noto RD, Mirabelli P, Imperlini E, Ruoppolo M, Vecchio LD, Salvatore F ( 2012) Protein cross-talk in CD133+ colon cancer cells indicates activation of the Wnt pathway and upregulation of SRp20 that is potentially involved in tumorigenicity . Proteomics 12: 2045– 2059
CrossRef
Google scholar
|
[22] |
Cvitkovic I, Jurica MS ( 2013) Spliceosome database: a tool for tracking components of the spliceosome . Nucleic Acids Res 41: D132– 141
CrossRef
Google scholar
|
[23] |
Damm F, Kosmider O, Gelsi-Boyer V, Renneville A, Carbuccia N, Hidalgo-Curtis C, Della Valle V Couronne L, Scourzic L, Chesnais V,
CrossRef
Google scholar
|
[24] |
Darman RB, Seiler M, Agrawal AA, Lim KH, Peng S, Aird D, Bailey SL, Bhavsar EB, Chan B, Colla S
CrossRef
Google scholar
|
[25] |
Dauber A, Golzio C, Guenot C, Jodelka FM, Kibaek M, Kjaergaard S, Leheup B, Martinet D, Nowaczyk MJ, Rosenfeld JA
CrossRef
Google scholar
|
[26] |
De Arras L, Alper S ( 2013) Limiting of the innate immune response by SF3A-dependent control of MyD88 alternative mRNA splicing . PLoS Genet 9: e1003855
CrossRef
Google scholar
|
[27] |
De Arras L, Laws R, Leach SM, Pontis K, Freedman JH, Schwartz DA, Alper S ( 2014) Comparative genomics RNAi screen identifies Eftud2 as a novel regulator of innate immunity . Genetics 197: 485– 496
CrossRef
Google scholar
|
[28] |
Deery EC, Vithana EN, Newbold RJ, Gallon VA, Bhattacharya SS, Warren MJ, Hunt DM, Wilkie SE ( 2002) Disease mechanism for retinitis pigmentosa (RP11) caused by mutations in the splicing factor gene PRPF31 . Hum Mol Genet 11: 3209– 3219
CrossRef
Google scholar
|
[29] |
Desai P, Mencia-Trinchant N, Savenkov O, Simon MS, Cheang G, Lee S, Samuel M, Ritchie EK, Guzman ML, Ballman KV
CrossRef
Google scholar
|
[30] |
Devotta A, Juraver-Geslin H, Gonzalez JA, Hong CS, Saint-Jeannet JP ( 2016) Sf3b4-depleted Xenopus embryos: A model to study the pathogenesis of craniofacial defects in Nager syndrome . Dev Biol 415: 371– 382
CrossRef
Google scholar
|
[31] |
Dominski Z, Kole R ( 1993) Restoration of correct splicing in thalassemic pre-mRNA by antisense oligonucleotides . Proc Natl Acad Sci U S A 90: 8673– 8677
CrossRef
Google scholar
|
[32] |
Dvinge H, Kim E, Abdel-Wahab O, Bradley RK ( 2016) RNA splicing factors as oncoproteins and tumour suppressors . Nat Rev Cancer 16: 413– 430
CrossRef
Google scholar
|
[33] |
Edery P, Marcaillou C, Sahbatou M, Labalme A, Chastang J, Touraine R, Tubacher E, Senni F, Bober MB, Nampoothiri S
CrossRef
Google scholar
|
[34] |
Elsaid MF, Chalhoub N, Ben-Omran T, Kumar P, Kamel H, Ibrahim K, Mohamoud Y, Al-Dous E, Al-Azwani I, Malek JA
CrossRef
Google scholar
|
[35] |
Eymin B ( 2021) Targeting the spliceosome machinery: A new therapeutic axis in cancer? Biochem Pharmacol 189: 114039
CrossRef
Google scholar
|
[36] |
Fabrizio P, Dannenberg J, Dube P, Kastner B, Stark H, Urlaub H, Luhrmann R ( 2009) The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome . Mol Cell 36: 593– 608
CrossRef
Google scholar
|
[37] |
Fallini C, Donlin-Asp PG, Rouanet JP, Bassell GJ, Rossoll W ( 2016) Deficiency of the survival of motor neuron protein impairs mrna localization and local translation in the growth cone of motor neurons . J Neurosci 36: 3811– 3820
CrossRef
Google scholar
|
[38] |
Favaro FP, Alvizi L, Zechi-Ceide RM, Bertola D, Felix TM, de Souza J, Raskin S, Twigg SR, Weiner AM, Armas P
CrossRef
Google scholar
|
[39] |
Folco EG, Coil KE, Reed R ( 2011) The anti-tumor drug E7107 reveals an essential role for SF3b in remodeling U2 snRNP to expose the branch point-binding region . Genes Dev 25: 440– 444
CrossRef
Google scholar
|
[40] |
Freund C, Kuhne R, Yang H, Park S, Reinherz EL, Wagner G ( 2002) Dynamic interaction of CD2 with the GYF and the SH3 domain of compartmentalized effector molecules . EMBO J 21: 5985– 5995
CrossRef
Google scholar
|
[41] |
Furney SJ, Pedersen M, Gentien D, Dumont AG, Rapinat A, Desjardins L, Turajlic S, Piperno-Neumann S, de la Grange P, Roman-Roman S
CrossRef
Google scholar
|
[42] |
Goncalves V, Matos P, Jordan P ( 2008) The beta-catenin/TCF4 pathway modifies alternative splicing through modulation of SRp20 expression . RNA 14: 2538– 2549
CrossRef
Google scholar
|
[43] |
Graubert TA, Shen D, Ding L, Okeyo-Owuor T, Lunn CL, Shao J, Krysiak K, Harris CC, Koboldt DC, Larson DE
CrossRef
Google scholar
|
[44] |
Grignano E, Jachiet V, Fenaux P, Ades L, Fain O, Mekinian A ( 2018) Autoimmune manifestations associated with myelodysplastic syndromes . Ann Hematol 97: 2015– 2023
CrossRef
Google scholar
|
[45] |
Haferlach T, Nagata Y, Grossmann V, Okuno Y, Bacher U, Nagae G, Schnittger S, Sanada M, Kon A, Alpermann T
CrossRef
Google scholar
|
[46] |
Harbour JW, Roberson ED, Anbunathan H, Onken MD, Worley LA, Bowcock AM ( 2013) Recurrent mutations at codon 625 of the splicing factor SF3B1 in uveal melanoma . Nat Genet 45: 133– 135
CrossRef
Google scholar
|
[47] |
Havens MA, Hastings ML ( 2016) Splice-switching antisense oligonu-cleotides as therapeutic drugs . Nucleic Acids Res 44: 6549– 6563
CrossRef
Google scholar
|
[48] |
He H, Liyanarachchi S, Akagi K, Nagy R, Li J, Dietrich RC, Li W, Sebastian N, Wen B, Xin B
CrossRef
Google scholar
|
[49] |
Heaney ML, Golde DW ( 1999) Myelodysplasia . N Engl J Med 340: 1649– 1660
CrossRef
Google scholar
|
[50] |
Heinze M, Kofler M, Freund C ( 2007) Investigating the functional role of CD2BP2 in T cells . Int Immunol 19: 1313– 1318
CrossRef
Google scholar
|
[51] |
Ilagan JO, Ramakrishnan A, Hayes B, Murphy ME, Zebari AS, Bradley P, Bradley RK ( 2015) U2AF1 mutations alter splice site recognition in hematological malignancies . Genome Res 25: 14– 26
CrossRef
Google scholar
|
[52] |
Imielinski M, Berger AH, Hammerman PS, Hernandez B, Pugh TJ, Hodis E, Cho J, Suh J, Capelletti M, Sivachenko A
CrossRef
Google scholar
|
[53] |
Inoue D, Bradley RK, Abdel-Wahab O ( 2016) Spliceosomal gene mutations in myelodysplasia: molecular links to clonal abnormalities of hematopoiesis . Genes Dev 30: 989– 1001
CrossRef
Google scholar
|
[54] |
Inoue D, Polaski JT, Taylor J, Castel P, Chen S, Kobayashi S, Hogg SJ, Hayashi Y, Pineda JMB, El Marabti E
CrossRef
Google scholar
|
[55] |
Ishak CA, Loo Yau H, De Carvalho DD ( 2021) Spliceosome-targeted therapies induce dsRNA responses . Immunity 54: 11– 13
CrossRef
Google scholar
|
[56] |
Ishihara T, Ariizumi Y, Shiga A, Kato T, Tan CF, Sato T, Miki Y, Yokoo M, Fujino T, Koyama A
CrossRef
Google scholar
|
[57] |
Johnston JJ, Teer JK, Cherukuri PF, Hansen NF, Loftus SK, Center NIHIS, Chong K, Mullikin JC, Biesecker LG ( 2010) Massively parallel sequencing of exons on the X chromosome identifies RBM10 as the gene that causes a syndromic form of cleft palate . Am J Hum Genet 86: 743– 748
CrossRef
Google scholar
|
[58] |
Jumaa H, Nielsen PJ ( 1997) The splicing factor SRp20 modifies splicing of its own mRNA and ASF/SF2 antagonizes this regulation . EMBO J 16: 5077– 5085
CrossRef
Google scholar
|
[59] |
Jurica MS, Moore MJ ( 2003) Pre-mRNA splicing: awash in a sea of proteins . Mol Cell 12: 5– 14
CrossRef
Google scholar
|
[60] |
Kaida D, Motoyoshi H, Tashiro E, Nojima T, Hagiwara M, Ishigami K, Watanabe H, Kitahara T, Yoshida T, Nakajima H
CrossRef
Google scholar
|
[61] |
Kalscheuer VM, Freude K, Musante L, Jensen LR, Yntema HG, Gecz J, Sefiani A, Hoffmann K, Moser B, Haas S
CrossRef
Google scholar
|
[62] |
Katsuyama T, Li H, Krishfield SM, Kyttaris VC, Moulton VR ( 2021) Splicing factor SRSF1 limits IFN-gamma production via RhoH and ameliorates experimental nephritis . Rheumatology (oxford) 60: 420– 429
CrossRef
Google scholar
|
[63] |
Kim E, Ilagan JO, Liang Y, Daubner GM, Lee SC, Ramakrishnan A, Li Y, Chung YR, Micol JB, Murphy ME
CrossRef
Google scholar
|
[64] |
Kim HJ, Kim NC, Wang YD, Scarborough EA, Moore J, Diaz Z, MacLea KS, Freibaum B, Li S, Molliex A
CrossRef
Google scholar
|
[65] |
Kofler M, Heuer K, Zech T, Freund C ( 2004) Recognition sequences for the GYF domain reveal a possible spliceosomal function of CD2BP2 . J Biol Chem 279: 28292– 28297
CrossRef
Google scholar
|
[66] |
Koh CM, Bezzi M, Low DH, Ang WX, Teo SX, Gay FP, Al-Haddawi M, Tan SY, Osato M, Sabo A
CrossRef
Google scholar
|
[67] |
Koizumi J, Okamoto Y, Onogi H, Mayeda A, Krainer AR, Hagiwara M ( 1999) The subcellular localization of SF2/ASF is regulated by direct interaction with SR protein kinases (SRPKs) . J Biol Chem 274: 11125– 11131
CrossRef
Google scholar
|
[68] |
Komeno Y, Huang YJ, Qiu J, Lin L, Xu Y, Zhou Y, Chen L, Monterroza DD, Li H, DeKelver RC
CrossRef
Google scholar
|
[69] |
Kong J, Sun W, Li C, Wan L, Wang S, Wu Y, Xu E, Zhang H, Lai M ( 2016) Long non-coding RNA LINC01133 inhibits epithelial-mesenchymal transition and metastasis in colorectal cancer by interacting with SRSF6 . Cancer Lett 380: 476– 484
CrossRef
Google scholar
|
[70] |
Kotake Y, Sagane K, Owa T, Mimori-Kiyosue Y, Shimizu H, Uesugi M, Ishihama Y, Iwata M, Mizui Y ( 2007) Splicing factor SF3b as a target of the antitumor natural product pladienolide . Nat Chem Biol 3: 570– 575
CrossRef
Google scholar
|
[71] |
Kurtovic-Kozaric A, Przychodzen B, Singh J, Konarska MM, Clemente MJ, Otrock ZK, Nakashima M, Hsi ED, Yoshida K, Shiraishi Y
CrossRef
Google scholar
|
[72] |
Laggerbauer B, Liu S, Makarov E, Vornlocher HP, Makarova O, Ingelfinger D, Achsel T, Luhrmann R ( 2005) The human U5 snRNP 52K protein (CD2BP2) interacts with U5–102K (hPrp6), a U4/U6.U5 tri-snRNP bridging protein, but dissociates upon tri-snRNP formation . RNA 11: 598– 608
CrossRef
Google scholar
|
[73] |
Lai MC, Lin RI, Huang SY, Tsai CW, Tarn WY ( 2000) A human importin-beta family protein, transportin-SR2, interacts with the phosphorylated RS domain of SR proteins . J Biol Chem 275: 7950– 7957
CrossRef
Google scholar
|
[74] |
Lee SC, Abdel-Wahab O ( 2016) Therapeutic targeting of splicing in cancer . Nat Med 22: 976– 986
CrossRef
Google scholar
|
[75] |
Lee SC, North K, Kim E, Jang E, Obeng E, Lu SX, Liu B, Inoue D, Yoshimi A, Ki M
CrossRef
Google scholar
|
[76] |
Li DK, Tisdale S, Lotti F, Pellizzoni L ( 2014) SMN control of RNP assembly: from post-transcriptional gene regulation to motor neuron disease . Semin Cell Dev Biol 32: 22– 29
CrossRef
Google scholar
|
[77] |
Li YI, van de Geijn B, Raj A, Knowles DA, Petti AA, Golan D, Gilad Y, Pritchard JK ( 2016) RNA splicing is a primary link between genetic variation and disease . Science 352: 600– 604
CrossRef
Google scholar
|
[78] |
Lindsley RC, Mar BG, Mazzola E, Grauman PV, Shareef S, Allen SL, Pigneux A, Wetzler M, Stuart RK, Erba HP
CrossRef
Google scholar
|
[79] |
Lines MA, Huang L, Schwartzentruber J, Douglas SL, Lynch DC, Beaulieu C, Guion-Almeida ML, Zechi-Ceide RM, Gener B, Gillessen-Kaesbach G
CrossRef
Google scholar
|
[80] |
Liu S, Cai X, Wu J, Cong Q, Chen X, Li T, Du F, Ren J, Wu YT, Grishin NV
CrossRef
Google scholar
|
[81] |
Liu T, Jin X, Zhang X, Yuan H, Cheng J, Lee J, Zhang B, Zhang M, Wu J, Wang L
CrossRef
Google scholar
|
[82] |
Low KJ, Ansari M, Abou Jamra R, Clarke A, El Chehadeh S FitzPatrick DR, Greenslade M, Henderson A, Hurst J, Keller K,
CrossRef
Google scholar
|
[83] |
Lv Z, Wang Z, Luo L, Chen Y, Han G, Wang R, Xiao H, Li X, Hou C, Feng J
CrossRef
Google scholar
|
[84] |
Lynch DC, Revil T, Schwartzentruber J, Bhoj EJ, Innes AM, Lamont RE, Lemire EG, Chodirker BN, Taylor JP, Zackai EH
CrossRef
Google scholar
|
[85] |
Madan V, Kanojia D, Li J, Okamoto R, Sato-Otsubo A, Kohlmann A, Sanada M, Grossmann V, Sundaresan J, Shiraishi Y
CrossRef
Google scholar
|
[86] |
Maguire SL, Leonidou A, Wai P, Marchio C, Ng CK, Sapino A, Salomon AV, Reis-Filho JS, Weigelt B, Natrajan RC ( 2015) SF3B1 mutations constitute a novel therapeutic target in breast cancer . J Pathol 235: 571– 580
CrossRef
Google scholar
|
[87] |
Malcovati L, Karimi M, Papaemmanuil E, Ambaglio I, Jadersten M, Jansson M, Elena C, Galli A, Walldin G, Della Porta MG
CrossRef
Google scholar
|
[88] |
Malcovati L, Papaemmanuil E, Bowen DT, Boultwood J, Della Porta MG, Pascutto C, Travaglino E, Groves MJ, Godfrey AL, Ambaglio I
CrossRef
Google scholar
|
[89] |
Marques F, Tenney J, Duran I, Martin J, Nevarez L, Pogue R, Krakow D, Cohn DH, Li B ( 2016) Altered mRNA splicing, chondrocyte gene expression and abnormal skeletal development due to SF3B4 mutations in rodriguez acrofacial dysostosis . PLoS Genet 12: 1006307
CrossRef
Google scholar
|
[90] |
Martin M, Masshofer L, Temming P, Rahmann S, Metz C, Bornfeld N, van de Nes J, Klein-Hitpass L , Hinnebusch AG, Horsthemke B
CrossRef
Google scholar
|
[91] |
Matlin AJ, Moore MJ ( 2007) Spliceosome assembly and composi-tion . Adv Exp Med Biol 623: 14– 35
CrossRef
Google scholar
|
[92] |
Maubaret CG, Vaclavik V, Mukhopadhyay R, Waseem NH, Churchill A, Holder GE, Moore AT, Bhattacharya SS, Webster AR ( 2011) Autosomal dominant retinitis pigmentosa with intrafamilial variability and incomplete penetrance in two families carrying mutations in PRPF8 . Invest Ophthalmol vis Sci 52: 9304– 9309
CrossRef
Google scholar
|
[93] |
McKie AB, McHale JC, Keen TJ, Tarttelin EE, Goliath R, van Lith-Verhoeven JJ, Greenberg J, Ramesar RS, Hoyng CB, Cremers FP
CrossRef
Google scholar
|
[94] |
Meggendorfer M, Roller A, Haferlach T, Eder C, Dicker F, Grossmann V, Kohlmann A, Alpermann T, Yoshida K, Ogawa S
CrossRef
Google scholar
|
[95] |
Merico D, Roifman M, Braunschweig U, Yuen RK, Alexandrova R, Bates A, Reid B, Nalpathamkalam T, Wang Z, Thiruvahindrapuram B
CrossRef
Google scholar
|
[96] |
Meseguer S, Mudduluru G, Escamilla JM, Allgayer H, Barettino D ( 2011) MicroRNAs-10a and-10b contribute to retinoic acidinduced differentiation of neuroblastoma cells and target the alternative splicing regulatory factor SFRS1 (SF2/ASF) . J Biol Chem 286: 4150– 4164
CrossRef
Google scholar
|
[97] |
Moore MJ, Query CC, Sharp PA ( 1993) Splicing of precursors to mRNA by the spliceosome. In RNA World, Gesteland RF, Atkins JF, eds . (Cold Spring Harbor, New York, Cold Spring Harbor Labratory Press), pp. 303– 357
|
[98] |
Nguyen HD, Leong WY, Li W, Reddy PNG, Sullivan JD, Walter MJ, Zou L, Graubert TA ( 2018) Spliceosome mutations induce R Loop-associated sensitivity to ATR inhibition in myelodysplastic syndromes . Cancer Res 78: 5363– 5374
CrossRef
Google scholar
|
[99] |
Nik-Zainal S, Davies H, Staaf J, Ramakrishna M, Glodzik D, Zou X, Martincorena I, Alexandrov LB, Martin S, Wedge DC
CrossRef
Google scholar
|
[100] |
Nilsen TW, Graveley BR ( 2010) Expansion of the eukaryotic proteome by alternative splicing . Nature 463: 457– 463
CrossRef
Google scholar
|
[101] |
Nishanian TG, Waldman T ( 2004) Interaction of the BMPR-IA tumor suppressor with a developmentally relevant splicing factor . Biochem Biophys Res Commun 323: 91– 97
CrossRef
Google scholar
|
[102] |
Nishizawa K, Freund C, Li J, Wagner G, Reinherz EL ( 1998) Identification of a proline-binding motif regulating CD2-triggered T lymphocyte activation . Proc Natl Acad Sci U S A 95: 14897– 14902
CrossRef
Google scholar
|
[103] |
Novoyatleva T, Tang Y, Rafalska I, Stamm S ( 2006) Pre-mRNA missplicing as a cause of human disease . Prog Mol Subcell Biol 44: 27– 46
CrossRef
Google scholar
|
[104] |
O’Connor BP, Danhorn T, De Arras L, Flatley BR, Marcus RA, Farias-Hesson E, Leach SM, Alper S ( 2015) Regulation of tolllike receptor signaling by the SF3a mRNA splicing complex . PLoS Genet 11: 1004932
CrossRef
Google scholar
|
[105] |
Okeyo-Owuor T, White BS, Chatrikhi R, Mohan DR, Kim S, Griffith M, Ding L, Ketkar-Kulkarni S, Hundal J, Laird KM
CrossRef
Google scholar
|
[106] |
Pagano L, Caira M ( 2012) Risks for infection in patients with myelodysplasia and acute leukemia . Curr Opin Infect Dis 25: 612– 618
CrossRef
Google scholar
|
[107] |
Paine I, Posey JE, Grochowski CM, Jhangiani SN, Rosenheck S, Kleyner R, Marmorale T, Yoon M, Wang K, Robison R
CrossRef
Google scholar
|
[108] |
Papaemmanuil E, Cazzola M, Boultwood J, Malcovati L, Vyas P, Bowen D, Pellagatti A, Wainscoat JS, Hellstrom-Lindberg E, Gambacorti-Passerini C
CrossRef
Google scholar
|
[109] |
Papaemmanuil E, Gerstung M, Bullinger L, Gaidzik VI, Paschka P, Roberts ND, Potter NE, Heuser M, Thol F, Bolli N
CrossRef
Google scholar
|
[110] |
Papaemmanuil E, Gerstung M, Malcovati L, Tauro S, Gundem G, Van Loo P Yoon CJ, Ellis P, Wedge DC, Pellagatti A,
CrossRef
Google scholar
|
[111] |
Pasternack SM, Refke M, Paknia E, Hennies HC, Franz T, Schafer N, Fryer A, van Steensel M Sweeney E, Just M,
CrossRef
Google scholar
|
[112] |
Patel AA, Steitz JA ( 2003) Splicing double: insights from the second spliceosome . Nat Rev Mol Cell Biol 4: 960– 970
CrossRef
Google scholar
|
[113] |
Paz S, Ritchie A, Mauer C, Caputi M ( 2021) The RNA binding protein SRSF1 is a master switch of gene expression and regulation in the immune system . Cytokine Growth Factor Rev 57: 19– 26
CrossRef
Google scholar
|
[114] |
Pellagatti A, Boultwood J ( 2015) The molecular pathogenesis of the myelodysplastic syndromes . Eur J Haematol 95: 3– 15
CrossRef
Google scholar
|
[115] |
Petit F, Escande F, Jourdain AS, Porchet N, Amiel J, Doray B, Delrue MA, Flori E, Kim CA, Marlin S
CrossRef
Google scholar
|
[116] |
Pollyea DA, Harris C, Rabe JL, Hedin BR, De Arras L, Katz S, Wheeler E, Bejar R, Walter MJ, Jordan CT
CrossRef
Google scholar
|
[117] |
Polprasert C, Schulze I, Sekeres MA, Makishima H, Przychodzen B, Hosono N, Singh J, Padgett RA, Gu X, Phillips JG
CrossRef
Google scholar
|
[118] |
Qi Z, Wang F, Yu G, Wang D, Yao Y, You M, Liu J, Liu J, Sun Z, Ji C
CrossRef
Google scholar
|
[119] |
Quemener AM, Bachelot L, Forestier A, Donnou-Fournet E, Gilot D, Galibert MD ( 2020) The powerful world of antisense oligonu-cleotides: From bench to bedside . Wiley Interdiscip Rev RNA 11: 1594
CrossRef
Google scholar
|
[120] |
Quesada V, Conde L, Villamor N, Ordonez GR, Jares P, Bas-saganyas L, Ramsay AJ, Bea S, Pinyol M, Martinez-Trillos A
CrossRef
Google scholar
|
[121] |
Rahman MA, Krainer AR, Abdel-Wahab O ( 2020) SnapShot: Splicing Alterations in Cancer . Cell 180: 208– 208
CrossRef
Google scholar
|
[122] |
Reber S, Stettler J, Filosa G, Colombo M, Jutzi D, Lenzken SC, Schweingruber C, Bruggmann R, Bachi A, Barabino SM
CrossRef
Google scholar
|
[123] |
Rivolta C, McGee TL, Rio Frio T, Jensen RV, Berson EL, Dryja TP ( 2006) Variation in retinitis pigmentosa-11 (PRPF31 or RP11) gene expression between symptomatic and asymptomatic patients with dominant RP11 mutations . Hum Mutat 27: 644– 653
CrossRef
Google scholar
|
[124] |
Rossbach O, Hung LH, Schreiner S, Grishina I, Heiner M, Hui J, Bindereif A ( 2009) Auto- and cross-regulation of the hnRNP L proteins by alternative splicing . Mol Cell Biol 29: 1442– 1451
CrossRef
Google scholar
|
[125] |
Rossi D, Bruscaggin A, Spina V, Rasi S, Khiabanian H, Messina M, Fangazio M, Vaisitti T, Monti S, Chiaretti S
CrossRef
Google scholar
|
[126] |
Ruzickova S, Stanek D ( 2017) Mutations in spliceosomal proteins and retina degeneration . RNA Biol 14: 544– 552
CrossRef
Google scholar
|
[127] |
Scott LM, Rebel VI ( 2013) Acquired mutations that affect pre-mRNA splicing in hematologic malignancies and solid tumors . J Natl Cancer Inst 105: 1540– 1549
CrossRef
Google scholar
|
[128] |
Scotti MM, Swanson MS ( 2016) RNA mis-splicing in disease . Nat Rev Genet 17: 19– 32
CrossRef
Google scholar
|
[129] |
Sebestyen E, Singh B, Minana B, Pages A, Mateo F, Pujana MA, Valcarcel J, Eyras E ( 2016) Large-scale analysis of genome and transcriptome alterations in multiple tumors unveils novel cancer-relevant splicing networks . Genome Res 26: 732– 744
CrossRef
Google scholar
|
[130] |
Shannon JL, Murphy MS, Kantheti U, Burnett JM, Hahn MG, Dorrity TJ, Bacas CJ, Mattice EB, Corpuz KD, Barker BR ( 2018) Polyglutamine binding protein 1 (PQBP1) inhibits innate immune responses to cytosolic DNA . Mol Immunol 99: 182– 190
CrossRef
Google scholar
|
[131] |
Shi Y ( 2017a) Mechanistic insights into precursor messenger RNA splicing by the spliceosome . Nat Rev Mol Cell Biol 18: 655– 670
CrossRef
Google scholar
|
[132] |
Shi Y ( 2017b) The spliceosome: a protein-directed metalloribozyme . J Mol Biol 429: 2640– 2653
CrossRef
Google scholar
|
[133] |
Shirai CL, Ley JN, White BS, Kim S, Tibbitts J, Shao J, Ndonwi M, Wadugu B, Duncavage EJ, Okeyo-Owuor T
CrossRef
Google scholar
|
[134] |
Shostak K, Jiang Z, Charloteaux B, Mayer A, Habraken Y, Tharun L, Klein S, Xu X, Duong HQ, Vislovukh A
CrossRef
Google scholar
|
[135] |
Sidhar SK, Clark J, Gill S, Hamoudi R, Crew AJ, Gwilliam R, Ross M, Linehan WM, Birdsall S, Shipley J
CrossRef
Google scholar
|
[136] |
Singh R, Gupta SC, Peng WX, Zhou N, Pochampally R, Atfi A, Watabe K, Lu Z, Mo YY ( 2016) Regulation of alternative splicing of Bcl-x by BC200 contributes to breast cancer pathogenesis . Cell Death Dis 7: e2262
CrossRef
Google scholar
|
[137] |
Singh RK, Cooper TA ( 2012) Pre-mRNA splicing in disease and therapeutics . Trends Mol Med 18: 472– 482
CrossRef
Google scholar
|
[138] |
Smith MA, Choudhary GS, Pellagatti A, Choi K, Bolanos LC, Bhagat TD, Gordon-Mitchell S, Von Ahrens D Pradhan K, Steeples V,
CrossRef
Google scholar
|
[139] |
Spitali P, Aartsma-Rus A ( 2012) Splice modulating therapies for human disease . Cell 148: 1085– 1088
CrossRef
Google scholar
|
[140] |
Staley JP, Woolford JL Jr ( 2009) Assembly of ribosomes and spliceosomes: complex ribonucleoprotein machines . Curr Opin Cell Biol 21: 109– 118
CrossRef
Google scholar
|
[141] |
Starczynowski DT, Karsan A ( 2010a) Deregulation of innate immune signaling in myelodysplastic syndromes is associated with deletion of chromosome-arm 5q . Cell Cycle 9: 855– 856
CrossRef
Google scholar
|
[142] |
Starczynowski DT, Karsan A ( 2010b) Innate immune signaling in the myelodysplastic syndromes . Hematol Oncol Clin North Am 24: 343– 359
CrossRef
Google scholar
|
[143] |
Sureau A, Gattoni R, Dooghe Y, Stevenin J, Soret J ( 2001) SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs . EMBO J 20: 1785– 1796
CrossRef
Google scholar
|
[144] |
Suzuki H, Kumar SA, Shuai S, Diaz-Navarro A, Gutierrez-Fernandez A, De Antonellis P Cavalli FMG, Juraschka K, Farooq H, Shibahara I,
CrossRef
Google scholar
|
[145] |
Tanackovic G, Ransijn A, Ayuso C, Harper S, Berson EL, Rivolta C ( 2011a) A missense mutation in PRPF6 causes impairment of pre-mRNA splicing and autosomal-dominant retinitis pigmentosa . Am J Hum Genet 88: 643– 649
CrossRef
Google scholar
|
[146] |
Tanackovic G, Ransijn A, Thibault P, Abou Elela S, Klinck R, Berson EL, Chabot B, Rivolta C ( 2011b) PRPF mutations are associated with generalized defects in spliceosome formation and pre-mRNA splicing in patients with retinitis pigmentosa . Hum Mol Genet 20: 2116– 2130
CrossRef
Google scholar
|
[147] |
Taylor J, Lee SC ( 2019) Mutations in spliceosome genes and therapeutic opportunities in myeloid malignancies . Genes Chro-mosomes Cancer 58: 889– 902
CrossRef
Google scholar
|
[148] |
Tisdale S, Lotti F, Saieva L, Van Meerbeke JP, Crawford TO, Sumner CJ, Mentis GZ, Pellizzoni L ( 2013) SMN is essential for the biogenesis of U7 small nuclear ribonucleoprotein and 3’-end formation of histone mRNAs . Cell Rep 5: 1187– 1195
CrossRef
Google scholar
|
[149] |
Tooley M, Lynch D, Bernier F, Parboosingh J, Bhoj E, Zackai E, Calder A, Itasaki N, Wakeling E, Scott R
CrossRef
Google scholar
|
[150] |
Towns KV, Kipioti A, Long V, McKibbin M, Maubaret C, Vaclavik V, Ehsani P, Springell K, Kamal M, Ramesar RS
CrossRef
Google scholar
|
[151] |
Tremblay N, Baril M, Chatel-Chaix L, Es-Saad S, Park AY, Koenekoop RK, Lamarre D ( 2016) Spliceosome SNRNP200 promotes viral RNA sensing and IRF3 activation of antiviral response . PLoS Pathog 12: e1005772
CrossRef
Google scholar
|
[152] |
Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA
CrossRef
Google scholar
|
[153] |
Turunen JJ, Niemela EH, Verma B, Frilander MJ ( 2013) The significant other: splicing by the minor spliceosome . Wiley Interdiscip Rev RNA 4: 61– 76
CrossRef
Google scholar
|
[154] |
Turunen JJ, Will CL, Grote M, Luhrmann R, Frilander MJ ( 2008) The U11–48K protein contacts the 5’ splice site of U12-type introns and the U11–59K protein . Mol Cell Biol 28: 3548– 3560
CrossRef
Google scholar
|
[155] |
Ueno T, Taga Y, Yoshimoto R, Mayeda A, Hattori S, Ogawa-Goto K ( 2019) Component of splicing factor SF3b plays a key role in translational control of polyribosomes on the endoplasmic retic-ulum . Proc Natl Acad Sci U S A 116: 9340– 9349
CrossRef
Google scholar
|
[156] |
Urbanski LM, Leclair N, Anczukow O ( 2018) Alternative-splicing defects in cancer: Splicing regulators and their downstream targets, guiding the way to novel cancer therapeutics . Wiley Interdiscip Rev RNA 9: 1476
CrossRef
Google scholar
|
[157] |
Venables JP, Brosseau JP, Gadea G, Klinck R, Prinos P, Beaulieu JF, Lapointe E, Durand M, Thibault P, Tremblay K
CrossRef
Google scholar
|
[158] |
Verduci L, Simili M, Rizzo M, Mercatanti A, Evangelista M, Mariani L, Rainaldi G, Pitto L( 2010) MicroRNA (miRNA)-mediated interact-tion between leukemia/lymphoma-related factor (LRF) and alternative splicing factor/splicing factor 2 (ASF/SF2) affects mouse embryonic fibroblast senescence and apoptosis . J Biol Chem 285: 39551– 39563
CrossRef
Google scholar
|
[159] |
Verkerk A, Zeidler S, Breedveld G, Overbeek L, Huigh D, Koster L, van der Linde H, de Esch C, Severijnen LA, de Vries BBA
CrossRef
Google scholar
|
[160] |
Verma B, Akinyi MV, Norppa AJ, Frilander MJ ( 2018) Minor spliceosome and disease . Semin Cell Dev Biol 79: 103– 112
CrossRef
Google scholar
|
[161] |
Visconte V, Makishima H, Jankowska A, Szpurka H, Traina F, Jerez A, O’Keefe C, Rogers HJ, Sekeres MA, Maciejewski JP
CrossRef
Google scholar
|
[162] |
Visconte V, Rogers HJ, Singh J, Barnard J, Bupathi M, Traina F, McMahon J, Makishima H, Szpurka H, Jankowska A
CrossRef
Google scholar
|
[163] |
Vithana EN, Abu-Safieh L, Allen MJ, Carey A, Papaioannou M, Chakarova C, Al-Maghtheh M, Ebenezer ND, Willis C, Moore AT
CrossRef
Google scholar
|
[164] |
Wahl MC, Will CL, Luhrmann R ( 2009) The spliceosome: design principles of a dynamic RNP machine . Cell 136: 701– 718
CrossRef
Google scholar
|
[165] |
Wang GS, Cooper TA ( 2007) Splicing in disease: disruption of the splicing code and the decoding machinery . Nat Rev Genet 8: 749– 761
CrossRef
Google scholar
|
[166] |
Wang L, Lawrence MS, Wan Y, Stojanov P, Sougnez C, Stevenson K, Werner L, Sivachenko A, DeLuca DS, Zhang L
CrossRef
Google scholar
|
[167] |
Wassarman DA, Steitz JA ( 1992) Interactions of small nuclear RNA’s with precursor messenger RNA during in vitro splicing . Science 257: 1918– 1925
CrossRef
Google scholar
|
[168] |
Watanabe H, Shionyu M, Kimura T, Kimata K, Watanabe H ( 2007) Splicing factor 3b subunit 4 binds BMPR-IA and inhibits osteo-chondral cell differentiation . J Biol Chem 282: 20728– 20738
CrossRef
Google scholar
|
[169] |
Waterfall JJ, Arons E, Walker RL, Pineda M, Roth L, Killian JK, Abaan OD, Davis SR, Kreitman RJ, Meltzer PS ( 2014) High prevalence of MAP2K1 mutations in variant and IGHV4-34- expressing hairy-cell leukemias . Nat Genet 46: 8– 10
CrossRef
Google scholar
|
[170] |
Wieczorek D, Gener B, Gonzalez MJ, Seland S, Fischer S, Hehr U, Kuechler A, Hoefsloot LH, de Leeuw N, Gillessen-Kaesbach G
CrossRef
Google scholar
|
[171] |
Wieczorek D, Newman WG, Wieland T, Berulava T, Kaffe M, Falkenstein D, Beetz C, Graf E, Schwarzmayr T, Douzgou S
CrossRef
Google scholar
|
[172] |
Will CL, Luhrmann R ( 2011) Spliceosome structure and function . Cold Spring Harb Perspect Biol 3: a003707
CrossRef
Google scholar
|
[173] |
Will CL, Luhrmann R ( 2006) Spliceosome structure and function. In The RNA World, Gesteland RF et al, eds. (Cold Spring Harbor, New York, Cold Spring Harbor Laboratory Press), pp. 369– 400
|
[174] |
Wu S, Romfo CM, Nilsen TW, Green MR ( 1999) Functional recognition of the 3’ splice site AG by the splicing factor U2AF35 . Nature 402: 832– 835
CrossRef
Google scholar
|
[175] |
Xiong F, Liu HH, Duan CY, Zhang BK, Wei G, Zhang Y, Li S ( 2019) Arabidopsis JANUS Regulates Embryonic Pattern Formation through Pol II-Mediated Transcription of WOX2 and PIN7 . iScience 19: 1179– 1188
CrossRef
Google scholar
|
[176] |
Xu M, Xie YA, Abouzeid H, Gordon CT, Fiorentino A, Sun Z, Lehman A, Osman IS, Dharmat R, Riveiro-Alvarez R
CrossRef
Google scholar
|
[177] |
Yip BH, Dolatshad H, Roy S, Pellagatti A, Boultwood J ( 2016) Impact of splicing factor mutations on pre-mrna splicing in the myelodysplastic syndromes . Curr Pharm Des 22: 2333– 2344
CrossRef
Google scholar
|
[178] |
Yoh SM, Schneider M, Seifried J, Soonthornvacharin S, Akleh RE, Olivieri KC, De Jesus PD Ruan C, de Castro E, Ruiz PA,
CrossRef
Google scholar
|
[179] |
Yoshida K, Ogawa S ( 2014) Splicing factor mutations and cancer . Wiley Interdiscip Rev RNA 5: 445– 459
CrossRef
Google scholar
|
[180] |
Yoshida K, Sanada M, Shiraishi Y, Nowak D, Nagata Y, Yamamoto R, Sato Y, Sato-Otsubo A, Kon A, Nagasaki M
CrossRef
Google scholar
|
[181] |
Yoshida T, Kim JH, Carver K, Su Y, Weremowicz S, Mulvey L, Yamamoto S, Brennan C, Mei S, Long H
CrossRef
Google scholar
|
[182] |
Zhang D, Hu Q, Liu X, Ji Y, Chao HP, Liu Y, Tracz A, Kirk J, Buonamici S, Zhu P
CrossRef
Google scholar
|
[183] |
Zhang D, Yue T, Choi JH, Nair-Gill E, Zhong X, Wang KW, Zhan X, Li X, Choi M, Tang M
CrossRef
Google scholar
|
[184] |
Zhang J, Lieu YK, Ali AM, Penson A, Reggio KS, Rabadan R, Raza A, Mukherjee S, Manley JL ( 2015) Disease-associated mutation in SRSF2 misregulates splicing by altering RNA-binding affinities . Proc Natl Acad Sci U S A 112: E4726– 4734
CrossRef
Google scholar
|
[185] |
Zhang J, Manley JL ( 2013) Misregulation of pre-mRNA alternative splicing in cancer . Cancer Discov 3: 1228– 1237
CrossRef
Google scholar
|
[186] |
Zhang S, Wei JS, Li SQ, Badgett TC, Song YK, Agarwal S, Coarfa C, Tolman C, Hurd L, Liao H
CrossRef
Google scholar
|
[187] |
Zhang SJ, Rampal R, Manshouri T, Patel J, Mensah N, Kayserian A, Hricik T, Heguy A, Hedvat C, Gonen M
CrossRef
Google scholar
|
[188] |
Zhang Z, Zhou N, Huang J, Ho TT, Zhu Z, Qiu Z, Zhou X, Bai C, Wu F, Xu M
CrossRef
Google scholar
|
[189] |
Zhao C, Lu S, Zhou X, Zhang X, Zhao K, Larsson C ( 2006) A novel locus (RP33) for autosomal dominant retinitis pigmentosa mapping to chromosomal region 2cen-q12.1 . Hum Genet 119: 617– 623
CrossRef
Google scholar
|
[190] |
Zhong XY, Ding JH, Adams JA, Ghosh G, Fu XD ( 2009) Regulation of SR protein phosphorylation and alternative splicing by modulating kinetic interactions of SRPK1 with molecular chaperones . Genes Dev 23: 482– 495
CrossRef
Google scholar
|
[191] |
Zhou Z, Qiu J, Liu W, Zhou Y, Plocinik RM, Li H, Hu Q, Ghosh G, Adams JA, Rosenfeld MG
CrossRef
Google scholar
|
/
〈 | 〉 |