The cardiotonic steroid digitoxin regulates alternative splicing through depletion of the splicing factors SRSF3 and TRA2B

RNA

Volumn 18, Issue 5, 2012, Pages 1041-1049

  Anderson, Erik S ^a   Lin, Chia H O ^a   Xiao, Xinshu ^a   Stoilov, Peter ^b   Burge, Christopher B ^c   Black, Douglas L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Alternative splicing; Cardiotonic steroid; SRp20; Tra2

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CELL PROTEIN; DIGITOXIN; PROTEIN SRP20; PROTEIN TRA2 BETA; RNA BINDING PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING SITE; CONTROLLED STUDY; EXON; HEART FAILURE; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION;

ALTERNATIVE SPLICING; BINDING SITES; CARDIOTONIC AGENTS; CELL LINE; DIGITOXIN; EXONS; GENE EXPRESSION; HUMANS; NERVE TISSUE PROTEINS; PROTEIN STABILITY; RNA-BINDING PROTEINS;

EID: 84859971554     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.032912.112     Document Type: Article

References (43)

1. Black DL. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72: 291-336. (Pubitemid 36930448)
2. Blaustein M, Pelisch F, Tanos T, Munoz MJ, Wengier D, Quadrana L, Sanford JR, Muschietti JP, Kornblihtt AR, Caceres JF, et al. 2005. Concerted regulation of nuclear and cytoplasmic activities of SR proteins by AKT. Nat Struct Mol Biol 12: 1037-1044. (Pubitemid 41746773)
3. Buratti E, Stuani C, De Prato G, Baralle FE. 2007. SR protein-mediated inhibition of CFTR exon 9 inclusion: molecular characterization of the intronic splicing silencer. Nucleic Acids Res 35: 4359-4368. (Pubitemid 47244589)
4. Caffrey TM, Wade-Martins R. 2007. Functional MAPT haplotypes: bridging the gap between genotype and neuropathology. Neurobiol Dis 27: 1-10. (Pubitemid 46921479)
5. Cartegni L, Wang J, Zhu Z, Zhang MQ, Krainer AR. 2003. ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res 31: 3568-3571. (Pubitemid 37442199)
6. Cavaloc Y, Bourgeois CF, Kister L, Stevenin J. 1999. The splicing factors 9G8 and SRp20 transactivate splicing through different and specific enhancers. RNA 5: 468-483. (Pubitemid 29125005)
7. Dawson HN, Cantillana V, Chen L, Vitek MP. 2007. The tau N279K exon 10 splicing mutation recapitulates frontotemporal dementia and parkinsonism linked to chromosome 17 tauopathy in a mouse model. J Neurosci 27: 9155-9168. (Pubitemid 47312069)
8. Gao L, Wang J, Wang Y, Andreadis A. 2007. SR protein 9G8 modulates splicing of tau exon 10 via its proximal downstream intron, a clustering region for frontotemporal dementia mutations. Mol Cell Neurosci 34: 48-58. (Pubitemid 46026933)
9. Hofmann Y, Lorson CL, Stamm S, Androphy EJ, Wirth B. 2000. Htra2-β1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proc Natl Acad Sci 97: 9618-9623. (Pubitemid 30650825)
10. Kaida D, Motoyoshi H, Tashiro E, Nojima T, Hagiwara M, Ishigami K, Watanabe H, Kitahara T, Yoshida T, Nakajima H, et al. 2007. Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nat Chem Biol 3: 576-583. (Pubitemid 47294395)
11. Kanopka A, Muhlemann O, Akusjarvi G. 1996. Inhibition by SR proteins of splicing of a regulated adenovirus pre-mRNA. Nature 381: 535-538. (Pubitemid 26170934)
12. Katzenberger RJ, Marengo MS, Wassarman DA. 2009. Control of alternative splicing by signal-dependent degradation of splicing-regulatory proteins. J Biol Chem 284: 10737-10746.
13. 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. (Pubitemid 47294394)
14. Liu HX, Zhang M, Krainer AR. 1998. Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins. Genes Dev 12: 1998-2012. (Pubitemid 28323874)
15. Long JC, Caceres JF. 2009. The SR protein family of splicing factors: master regulators of gene expression. Biochem J 417: 15-27.
16. Lorson CL, Androphy EJ. 2000. An exonic enhancer is required for inclusion of an essential exon in the SMA-determining gene SMN. Hum Mol Genet 9: 259-265.
17. Lynch KW. 2007. Regulation of alternative splicing by signal transduction pathways. Adv Exp Med Biol 623: 161-174.
18. O'Brien K, Matlin AJ, Lowell AM, Moore MJ. 2008. The biflavonoid isoginkgetin is a general inhibitor of pre-mRNA splicing. J Biol Chem 283: 33147-33154.
19. Patel NA, Kaneko S, Apostolatos HS, Bae SS, Watson JE, Davidowitz K, Chappell DS, Birnbaum MJ, Cheng JQ, Cooper DR. 2005. Molecular and genetic studies imply Akt-mediated signaling promotes protein kinase CbII alternative splicing via phosphorylation of serine/arginine-rich splicing factor SRp40. J Biol Chem 280: 14302-14309. (Pubitemid 40517333)
20. Prassas I, Diamandis EP. 2008. Novel therapeutic applications of cardiac glycosides. Nat Rev Drug Discov 7: 926-935.
21. Roybal GA, Jurica MS. 2010. Spliceostatin A inhibits spliceosome assembly subsequent to prespliceosome formation. Nucleic Acids Res 38: 6664-6672.
22. Schaal TD, Maniatis T. 1999. Multiple distinct splicing enhancers in the protein-coding sequences of a constitutively spliced pre-mRNA. Mol Cell Biol 19: 261-273. (Pubitemid 29018428)
23. Schoner W, Scheiner-Bobis G. 2007a. Endogenous and exogenous cardiac glycosides and their mechanisms of action. Am J Cardiovasc Drugs 7: 173-189. (Pubitemid 47049626)
24. Schoner W, Scheiner-Bobis G. 2007b. Endogenous and exogenous cardiac glycosides: their roles in hypertension, salt metabolism, and cell growth. Am J Physiol Cell Physiol 293: C509-C536. (Pubitemid 47235171)
25. Shen S, Warzecha CC, Carstens RP, Xing Y. 2010. MADS+: discovery of differential splicing events from Affymetrix exon junction array data. Bioinformatics 26: 268-269.
26. Shepard PJ, Hertel KJ. 2009. The SR protein family. Genome Biol 10: 242. doi: 10.1186/gb-2009-10-10-242.
27. Shin C, Manley JL. 2004. Cell signalling and the control of pre-mRNA splicing. Nat Rev Mol Cell Biol 5: 727-738. (Pubitemid 39208182)
28. Shin C, Feng Y, Manley JL. 2004. Dephosphorylated SRp38 acts as a splicing repressor in response to heat shock. Nature 427: 553-558. (Pubitemid 38209114)
29. Soret J, Bakkour N, Maire S, Durand S, Zekri L, Gabut M, Fic W, Divita G, Rivalle C, Dauzonne D, et al. 2005. Selective modification of alternative splicing by indole derivatives that target serinearginine- rich protein splicing factors. Proc Natl Acad Sci 102: 8764-8769. (Pubitemid 40862809)
30. Spellman R, Smith CW. 2006. Novel modes of splicing repression by PTB. Trends Biochem Sci 31: 73-76. (Pubitemid 43221838)
31. Stamm S. 2008. Regulation of alternative splicing by reversible protein phosphorylation. J Biol Chem 283: 1223-1227.
32. Stoilov P, Daoud R, Nayler O, Stamm S. 2004. Human tra2-b1 autoregulates its protein concentration by influencing alternative splicing of its pre-mRNA. Hum Mol Genet 13: 509-524. (Pubitemid 38313210)
33. Stoilov P, Lin CH, Damoiseaux R, Nikolic J, Black DL. 2008. A highthroughput screening strategy identifies cardiotonic steroids as alternative splicing modulators. Proc Natl Acad Sci 105: 11218-11223.
34. Sugnet CW, Srinivasan K, Clark TA, O'Brien G, Cline MS, Wang H, Williams A, Kulp D, Blume JE, Haussler D, et al. 2006. Unusual intron conservation near tissue-regulated exons found by splicing microarrays. PLoS Comput Biol 2: e4. doi: 10.1371/journal.pcbi. 0020004.
35. Tacke R, Manley JL. 1995. The human splicing factors ASF/SF2 and SC35 possess distinct, functionally significant RNA binding specificities. EMBO J 14: 3540-3551.
36. Tacke R, Tohyama M, Ogawa S, Manley JL. 1998. Human Tra2 proteins are sequence-specific activators of pre-mRNA splicing. Cell 93: 139-148. (Pubitemid 28173559)
37. Wang GS, Cooper TA. 2007. Splicing in disease: disruption of the splicing code and the decoding machinery. Nat Rev Genet 8: 749-761. (Pubitemid 47429207)
38. Wang Y, Wang J, Gao L, Lafyatis R, Stamm S, Andreadis A. 2005. Tau exons 2 and 10, which are misregulated in neurodegenerative diseases, are partly regulated by silencers which bind a SRp30c. SRp55 complex that either recruits or antagonizes htra2b1. J Biol Chem 280: 14230-14239. (Pubitemid 40517325)
39. Weg-Remers S, Ponta H, Herrlich P, Konig H. 2001. Regulation of alternative pre-mRNA splicing by the ERK MAP-kinase pathway. EMBO J 20: 4194-4203. (Pubitemid 32751835)
40. Yamamoto ML, Clark TA, Gee SL, Kang JA, Schweitzer AC, Wickrema A, Conboy JG. 2009. Alternative pre-mRNA splicing switches modulate gene expression in late erythropoiesis. Blood 113: 3363-3370.
41. Young PJ, DiDonato CJ, Hu D, Kothary R, Androphy EJ, Lorson CL. 2002. SRp30c-dependent stimulation of survival motor neuron (SMN) exon 7 inclusion is facilitated by a direct interaction with hTra2 β1. Hum Mol Genet 11: 577-587. (Pubitemid 34257494)
42. Younis I, Berg M, Kaida D, Dittmar K, Wang C, Dreyfuss G. 2010. Rapid-response splicing reporter screens identify differential regulators of constitutive and alternative splicing. Mol Cell Biol 30: 1718-1728.
43. Yu Q, Guo J, Zhou J. 2004. A minimal length between tau exon 10 and 11 is required for correct splicing of exon 10. J Neurochem 90: 164-172. (Pubitemid 38879171)