L-ILF3 and L-NF90 traffic to the nucleolus granular component: Alternatively-spliced exon 3 encodes a nucleolar localization motif

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Viranaicken, Wildriss ^a,b,d   Gasmi, Laila ^a,b,e   Chaumet, Alexandre ^a,b,f   Durieux, Christiane ^c,g   Georget, Virginie ^a,h   Denoulet, Philippe ^a,b   Larcher, Jean Christophe ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS and Université Pierre et Marie Curie   (France)

^c INSTITUT JACQUES MONOD   (France)

^d UNIVERSITÉ DE LA RÉUNION   (France)

^e INSTITUT DU FER À MOULIN   (France)

^f INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^g INSERM   (France)

^h Centre National de la Recherche Scientifique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; HISTIDINE; INTERLEUKIN ENHANCER BINDING FACTOR 3; ISOPROTEIN; RECOMBINANT PROTEIN; 5,6 DICHLOROBENZIMIDAZOLE RIBOSIDE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; ILF3 PROTEIN, HUMAN; RNA ISOFORM; SIGNAL PEPTIDE;

ALTERNATIVE RNA SPLICING; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL GRANULE; CONTROLLED STUDY; EXON; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MOUSE; NONHUMAN; NUCLEOLAR LOCALIZATION SIGNAL; NUCLEOLUS; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN TARGETING; PROTEIN TRANSPORT; AMINO ACID SEQUENCE; CELL FRACTIONATION; CHEMISTRY; DRUG EFFECT; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE DELETION; GENETICS; HELA CELL; METABOLISM; MOLECULAR GENETICS;

ALTERNATIVE SPLICING; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL NUCLEOLUS; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; EXONS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR FACTOR 90 PROTEINS; PROTEIN ISOFORMS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; RNA ISOFORMS; SEQUENCE DELETION; SUBCELLULAR FRACTIONS;

EID: 79960445464     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022296     Document Type: Article

References (47)

1. Larcher JC, Gasmi L, Viranaicken W, Eddé B, Bernard R, et al. (2004) Ilf3 and NF90 associates with the axonal targeting element of Tau mRNA. FASEB J 18: 1761-1763.
2. St Johnston D, Brown NH, Gall GJ, Jantsch M, (1992) A conserved double-stranded RNA-binding domain. Proc Natl Acad Sci U S A 89: 10979-10983.
3. Duchange N, Pidoux J, Camus E, Sauvaget D, (2000) Alternative splicing in the human interleukin enhancer binding factor 3 (ILF3) gene. Gene 261: 345-353.
4. Saunders LR, Perkins DJ, Balachandran S, Michaels R, Ford R, et al. (2001) Characterization of two evolutionarily conserved, alternatively spliced nuclear phosphoproteins, N-FAR-1 and-2, that function in mRNA processing and interact with the double-stranded-RNA-dependent protein kinase, PKR. J Biol Chem 276: 32300-32312.
5. Viranaicken W, Gasmi L, Chauvin C, Denoulet P, Larcher JC, (2006) Identification of a newly spliced exon in the mouse Ilf3 gene generating two long and short isoforms of Ilf3 and NF90. Genomics88: 622-632.
6. Tang J, Kao PN, Herschman HR, (2000) Protein-arginine methyltransferase I, the predominant protein-arginine methyltransferase in cells, interacts with and is regulated by interleukin enhancer-binding factor 3. J Biol Chem 275: 19866-19876.
7. Patel RC, Vestal DJ, Xu Z, Bandyopadhyay S, Guo W, et al. (1999) DRBP76, a double-stranded RNA-binding nuclear protein, is phosphorylated by the interferon-induced protein kinase, PKR. J Biol Chem 274: 20432-20437.
8. Parker LM, Fierro-Monti I, Mathews MB, (2001) Nuclear factor 90 is a substrate and a regulator of the eukaryotic initiation factor 2 kinase double-stranded RNA-activated protein kinase. J Biol Chem 276/ 32522-32530.
9. Ting NS, Kao PN, Chan DW, Lintott LG, Lees-Miller SP, (1998) DNA-dependent protein kinase interacts with antigen receptor response element binding proteins NF90 and NF45. J Biol Chem 273: 2136-2145.
10. Pei Y, Zhu P, Dang Y, Wu J, Yang X, et al. (2008) Nuclear export of NF90 to stabilize IL-2 mRNA is mediated by AKT-dependent phosphorylation at Ser467 in reponse to CD28 costimulation. J Immunol 180: 222-229.
11. Corthesy B, Kao PN, (2000) Purification by DNA affinity chromatography of two polypeptides that contact the NF-AT DNA binding site in the interleukin 2 promoter. J Biol Chem 269: 20682-20690.
12. Reichman TW, Muñiz LC, Mathews MB, (2002) The RNA binding protein nuclear factor 90 functions as both a positive and negative regulator of gene expression in mammalian cells. Mol Cell Biol 22/ 343-356.
13. Reichman TW, Mathews MB, (2003) RNA binding and intramolecular interactions modulate the regulation of gene expression by nuclear factor 110. RNA 9: 543-554.
14. Reichman TW, Parrott AM, Fierro-Monti I, Caron DJ, Kao PN, et al. (2003) Selective regulation of gene expression by nuclear factor 110, a member of the NF90 family of double-stranded RNA-binding proteins. J Mol Biol 332: 85-98.
15. Liao HJ, Kobayashi R, Mathews MB, (1998) Activities of adenovirus virus-associated RNAs: purification and characterization of RNA binding proteins. Proc Natl Acad Sci U S A 95: 8514-8519.
16. Buaas FW, Lee K, Edelhoff S, Disteche C, Braun RE, (1999) Cloning and characterization of the mouse interleukin enhancer binding factor 3 (Ilf3) homolog in a screen for RNA binding proteins. Mammal Genome 10: 451-456.
17. Shim J, Lim H, Yates JR III, Karin M, (2002) Nuclear export of NF90 is required for interleukin-2 mRNA stabilization. Mol Cell 10: 1331-1344.
18. Isken O, Grassmann CW, Sarisky RT, Kann M, Zhang S, et al. (2003) Members of the NF90/NFAR protein group are involved in the life cycle of a positive-strand RNA virus. EMBO J 22: 5655-5665.
19. Shi L, Zhao G, Qiu D, Godfrey WR, Vogel H, et al. (2005) NF90 regulates cell cycle exit and terminal myogenic differentiation by direct binding of the 3′-untranslated region of MyoD and p21WAF1/CIP1 mRNAs. J Biol Chem 280: 18981-18989.
20. Parrott AM, Mathews MB, (2007) Novel rapidly evolving hominid RNAs bind nuclear factor 90 and display tissue-restricted distribution. Nucleic Acid Res 35: 6249-6258.
21. Xu YH, Grabowski GA, (1999) Molecular cloning and characterization of a translational inhibitory protein that binds to coding sequences of human acid beta-glucosidase and other mRNAs. Mol Genet Metab 68: 441-454.
22. Xu YH, Busald C, Grabowski GA, (2000) Reconstitution of TCP80/NF90 translation inhibition activity in insect cells. Mol Genet Metab 70: 106-115.
23. Xu YH, Grabowski GA, (2005) Translation modulation of acid ß-glucosidase in HepG2 cells: participation of the PKC pathway. Mol Genet Metab 84: 252-264.
24. Kuwano Y, Pullmann R Jr, Masara BS, Abdelmohsen K, Lee EK, et al. (2010) NF90 selectively represses the translation of target mRNAs bearing an AU-rich signature motif. Nucleic Acid Res 38: 225-238.
25. Xu YH, Leonova T, Grabowski GA, (2003) Cell cycle dependent intracellular distribution of two spliced isoforms of TCP/ILF3 proteins. Mol Genet Metab 80: 426-436.
26. Parrott AM, Walsh MR, Reichman TW, Mathews MB, (2005) RNA binding and phosphorylation determine the intracellular distribution of nuclear factors 90 and 110. J. Mol Biol 348: 281-293.
27. Brownawell AM, Macara IG, (2002) Exportin-5, a novel karyopherin, mediates nuclear export of double-stranded RNA binding proteins. J Cell Biol 156: 53-64.
28. Weber JD, Kuo ML, Bothner B, DiGiammarino EL, Kriwacki RW, et al. (2000) Cooperative signals governing ARF-Mdm2 interaction and nucleolar localization of the complex. Mol Cell Biol 20: 2517-2528.
29. Horke S, Reumann K, Schweizer M, Will H, Heise T, (2004) Nuclear trafficking of La protein depends on a newly identified nucleolar localization signal and the ability to bind RNA. J Biol Chem 279: 26563-26570.
30. Song Z, Wu M, (2005) Identification of a novel nucleolar localization signal and a degradation signal in Survivin-deltaEx3: a potential link between nucleolus and protein degradation. Oncogene 24: 2723-2734.
31. Louvet E, Junéra HR, Le Panse S, Hernandez-Verdun D, (2005) Dynamics and compartimentation of the nucleolar processing machinery. Exp Cell Res 304: 457-470.
32. Louvet E, Junéra HR, Berthuy I, Hernandez-Verdun D, (2006) Compartmentation of the nucleolar processing proteins in the granular component is a CK2-driven process. Mol Biol Cell 17: 2537-2546.
33. Negi SS, Olson MO, (2006) Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. J Cell Sci 119: 3676-3685.
34. Hatanaka M, (1990) Discovery of the nucleolar targeting signal. Bioessays 12: 143-148.
35. Scott SS, Boisvert F-M, McDowall MD, Lamond AI, Barton GJ, (2010) Characterization and prediction of protein nucleolar localization sequences. Nucleic Acid Res 38: 7388-7399.
36. Macchi P, Brownawell AM, Grunewald B, DesGroseillers L, Macara IG, et al. (2004) The brain-specific double-stranded RNA-binding protein Staufen2- Nucleolar accumulation and isoform-specific exportin-5 dependent export. J Biol Chem 279: 31440-31444.
37. Sansam CL, Wells KS, Emeson RB, (2003) Modulation of RNA editing by functional nucleolar sequestration of ADAR2. Proc Natl Acad Sci U S A 100: 14018-14023.
38. Kiebler MA, Jansen RP, Dahm R, Macchi P, (2005) A putative nuclear function for mammalian Staufen. Trends Biochem Sci 30: 228-231.
39. Nie Y, Ding L, Kao PN, Braun R, Yang JH, (2005) ADAR1 interacts with NF90 through double-stranded RNA and regulates NF90-mediated gene expression independently of RNA editing. Mol Cell Biol 25: 6956-6963.
40. Leung AK, Gerlich D, Miller G, Lyon C, Lam YW, et al. (2006) Quantitative kinetic analysis of nucleolar breakdown and reassembly during mitosis in live human cells. J Cell Biol 166: 787-800.
41. Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, et al. (2005) Nucleolar proteome dynamics. Nature 433: 77-83.
42. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
43. O'Farell PA, Goodman HM, O'Farell P, (1977) High resolution two-dimensionnal electrophoresis of basic as well as acidic proteins. Cell 12: 1133-1142.
44. Larcher JC, Boucher D, Ginzburg I, Gros F, Denoulet P, (1992) Heterogeneity of Tau proteins during mouse brain development and differentiation of cultured neurons. Develop Biol 154: 195-204.
45. Towbin H, Staehelin T, Gordon J, (1979) Electrophoretic transfert of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci U S A 76: 4350-4354.
46. Chauvin C, Salhi S, Le Goff C, Viranaicken W, Diop D, et al. (2005) Involvement of human eukaryotic release factors 3a and 3b in translation termination. Mol Cell Biol 25: 5801-5811.
47. Rabut G, Ellenberg J, (2005) Photobleaching techniques to study mobility and molecular dynamics of proteins in live cells: FRAP, iFRAP, and FLIP. In: Goldman RD, Spector DL, editors. Live Cell Imaging: A Laboratory Manual Cold Spring Harbor Laboratory Press, Cold Spring Harbor: 101-127.