Paraquat Modulates Alternative Pre-mRNA Splicing by Modifying the Intracellular Distribution of SRPK2

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Vivarelli, Silvia ^a,c   Lenzken, Silvia C ^a   Ruepp, Marc David ^b   Ranzini, Francesco ^a   Maffioletti, Andrea ^a,d   Alvarez, Reinaldo ^a   Mühlemann, Oliver ^b   Barabino, Silvia M L ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d Department of Cell Biology Sciences III ^*  (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MESSENGER RNA; PARAQUAT; PROTEIN KINASE; SERINE ARGININE PROTEIN SPECIFIC KINASE 2; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; BIOACCUMULATION; CELL NUCLEUS; CONTROLLED STUDY; DNA DAMAGE; E1A GENE; ENZYME PHOSPHORYLATION; GENETIC REGULATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REPORTER GENE; SITE DIRECTED MUTAGENESIS;

HUMANS; MUTAGENESIS, SITE-DIRECTED; PARAQUAT; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA PRECURSORS; RNA SPLICING;

EID: 84876161743     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061980     Document Type: Article

References (38)

1. Cocheme HM, Murphy MP, (2008) Complex I is the major site of mitochondrial superoxide production by paraquat. J Biol Chem 283: 1786-1798.
2. Lenzken SC, Romeo V, Zolezzi F, Cordero F, Lamorte G, et al. (2011) Mutant SOD1 and mitochondrial damage alter expression and splicing of genes controlling neuritogenesis in models of neurodegeneration. Hum Mutat 32: 168-182.
3. Schwerk C, Schulze-Osthoff K, (2005) Regulation of apoptosis by alternative pre-mRNA splicing. Mol Cell 19: 1-13.
4. Shin C, Manley JL, (2004) Cell signalling and the control of pre-mRNA splicing. Nat Rev Mol Cell Biol 5: 727-738.
5. Cooper TA, Wan L, Dreyfuss G, (2009) RNA and disease. Cell 136: 777-793.
6. Heyd F, Lynch KW, (2011) Degrade, move, regroup: signaling control of splicing proteins. Trends Biochem Sci 36: 397-404.
7. Long JC, Caceres JF, (2009) The SR protein family of splicing factors: master regulators of gene expression. Biochem J 417: 15-27.
8. Wang HY, Lin W, Dyck JA, Yeakley JM, Songyang Z, et al. (1998) SRPK2: a differentially expressed SR protein-specific kinase involved in mediating the interaction and localization of pre-mRNA splicing factors in mammalian cells. J Cell Biol 140: 737-750.
9. Lai MC, Lin RI, Tarn WY, (2001) Transportin-SR2 mediates nuclear import of phosphorylated SR proteins. Proc Natl Acad Sci U S A 98: 10154-10159.
10. Ding JH, Zhong XY, Hagopian JC, Cruz MM, Ghosh G, et al. (2006) Regulated cellular partitioning of SR protein-specific kinases in mammalian cells. Mol Biol Cell 17: 876-885.
11. Zhou Z, Qiu J, Liu W, Zhou Y, Plocinik RM, et al. (2012) The Akt-SRPK-SR axis constitutes a major pathway in transducing EGF signaling to regulate alternative splicing in the nucleus. Mol Cell 47: 422-433.
12. van der Houven van Oordt W, Diaz-Meco MT, Lozano J, Krainer AR, Moscat J, et al. (2000) The MKK(3/6)-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J Cell Biol 149: 307-316.
13. Guil S, Long JC, Caceres JF, (2006) hnRNP A1 relocalization to the stress granules reflects a role in the stress response. Mol Cell Biol 26: 5744-5758.
14. Lai MC, Kuo HW, Chang WC, Tarn WY, (2003) A novel splicing regulator shares a nuclear import pathway with SR proteins. Embo J 22: 1359-1369.
15. 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.
16. Neugebauer KM, Roth MB, (1997) Distribution of pre-mRNA splicing factors at sites of RNA polymerase II transcription. Genes Dev 11: 1148-1159.
17. Labourier E, Rossi F, Gallouzi IE, Allemand E, Divita G, et al. (1998) Interaction between the N-terminal domain of human DNA topoisomerase I and the arginine-serine domain of its substrate determines phosphorylation of SF2/ASF splicing factor. Nucleic Acids Res 26: 2955-2962.
18. Kuroyanagi N, Onogi H, Wakabayashi T, Hagiwara M, (1998) Novel SR-protein-specific kinase, SRPK2, disassembles nuclear speckles. Biochem Biophys Res Commun 242: 357-364.
19. Gui J, Lane W, Fu X, (1994) A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 369: 678-682.
20. Nakagawa O, Arnold M, Nakagawa M, Hamada H, Shelton JM, et al. (2005) Centronuclear myopathy in mice lacking a novel muscle-specific protein kinase transcriptionally regulated by MEF2. Genes Dev 19: 2066-2077.
21. Colwill K, Pawson T, Andrews B, Prasad J, Manley JL, et al. (1996) The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. Embo J 15: 265-275.
22. Obenauer JC, Cantley LC, Yaffe MB, (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31: 3635-3641.
23. Barreau C, Paillard L, Mereau A, Osborne HB, (2006) Mammalian CELF/Bruno-like RNA-binding proteins: molecular characteristics and biological functions. Biochimie 88: 515-525.
24. Caceres JF, Stamm S, Helfman DM, Krainer AR, (1994) Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265: 1706-1709.
25. Popielarz M, Gattoni R, Stevenin J, (1993) Contrasted cis-acting effects of downstream 5′ splice sites on the splicing of a retained intron: the adenoviral E1A pre-mRNA model. Nucleic Acids Res 21: 5144-5151.
26. McCormack AL, Atienza JG, Johnston LC, Andersen JK, Vu S, et al. (2005) Role of oxidative stress in paraquat-induced dopaminergic cell degeneration. J Neurochem 93: 1030-1037.
27. Mah LJ, El-Osta A, Karagiannis TC, gammaH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia 24: 679-686.
28. Wohlbold L, Fisher RP, (2009) Behind the wheel and under the hood: functions of cyclin-dependent kinases in response to DNA damage. DNA Repair (Amst) 8: 1018-1024.
29. Cerqueira A, Santamaria D, Martinez-Pastor B, Cuadrado M, Fernandez-Capetillo O, et al. (2009) Overall Cdk activity modulates the DNA damage response in mammalian cells. J Cell Biol 187: 773-780.
30. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, et al. (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8: 37-45.
31. Yu X, Chen J, (2004) DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol Cell Biol 24: 9478-9486.
32. Murray-Zmijewski F, Lane DP, Bourdon JC, (2006) p53/p63/p73 isoforms: an orchestra of isoforms to harmonise cell differentiation and response to stress. Cell Death Differ 13: 962-972.
33. Stamm S, (2008) Regulation of alternative splicing by reversible protein phosphorylation. J Biol Chem 283: 1223-1227.
34. Shi Y, Reddy B, Manley JL, (2006) PP1/PP2A phosphatases are required for the second step of Pre-mRNA splicing and target specific snRNP proteins. Mol Cell 23: 819-829.
35. Paillusson A, Hirschi N, Vallan C, Azzalin CM, Muhlemann O, (2005) A GFP-based reporter system to monitor nonsense-mediated mRNA decay. Nucleic Acids Res 33: e54.
36. Brummelkamp TR, Bernards R, Agami R, (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553.
37. Wiznerowicz M, Trono D, (2003) Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J Virol 77: 8957-8961.
38. Jenny A, Minvielle-Sebastia L, Preker PJ, Keller W, (1996) Sequence similarity between the 73 kDa protein of mammalian CPSF and a subunit of yeast Polyadenylation Factor I. Science 274: 1514-1517.