Identification of a Binding Site for ASF/SF2 on an RNA Fragment Derived from the Hepatitis delta Virus Genome

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Sikora, Dorota ^a   Zhang, Dajiang ^a   Bojic, Teodora ^a   Beeharry, Yasnee ^a   Tanara, Ali ^a   Pelchat, Martin ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN ASF; SERINE ARGININE RICH PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; HEPATITIS DELTA VIRUS; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN RNA BINDING; RNA BINDING; RNA FOLDING; RNA REPLICATION; SITE DIRECTED MUTAGENESIS; VIRUS GENOME; VIRUS REPLICATION;

BINDING SITES; GENOME, VIRAL; HEK293 CELLS; HEPATITIS DELTA VIRUS; HUMANS; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA; RNA POLYMERASE II; RNA-BINDING PROTEINS; VIRUS REPLICATION;

HEPATITIS DELTA VIRUS;

EID: 84872539627     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054832     Document Type: Article

References (69)

1. Taylor JM, (2009) Chapter 3. Replication of the hepatitis delta virus RNA genome. Adv Virus Res 74: 103-121.
2. Casey JL, (2012) Control of ADAR1 editing of hepatitis delta virus RNAs. Curr Top Microbiol Immunol 353: 123-143.
3. Kuo MY, Chao M, Taylor J, (1989) Initiation of replication of the human hepatitis delta virus genome from cloned DNA: role of delta antigen. J Virol 63: 1945-1950.
4. Yamaguchi Y, Filipovska J, Yano K, Furuya A, Inukai N, et al. (2001) Stimulation of RNA polymerase II elongation by hepatitis delta antigen. Science 293: 124-127.
5. Chao M, Hsieh SY, Taylor J, (1990) Role of two forms of hepatitis delta virus antigen: evidence for a mechanism of self-limiting genome replication. J Virol 64: 5066-5069.
6. Chang FL, Chen PJ, Tu SJ, Wang CJ, Chen DS, (1991) The large form of hepatitis delta antigen is crucial for assembly of hepatitis delta virus. Proc Natl Acad Sci USA 88: 8490-8494.
7. Ryu WS, Bayer M, Taylor J, (1992) Assembly of hepatitis delta virus particles. J Virol 66: 2310-2315.
8. Sureau C, Moriarty AM, Thornton GB, Lanford RE, (1992) Production of infectious hepatitis delta virus in vitro and neutralization with antibodies directed against hepatitis B virus pre-S antigens. J Virol 66: 1241-1245.
9. Lee CZ, Chen PJ, Chen DS, (1995) Large hepatitis delta antigen in packaging and replication inhibition: role of the carboxyl-terminal 19 amino acids and amino-terminal sequences. J Virol 69: 5332-5336.
10. Rizzetto M, Canese MG, Arico S, Crivelli O, Trepo C, et al. (1977) Immunofluorescence detection of new antigen-antibody system (delta/anti-delta) associated to hepatitis B virus in liver and in serum of HBsAg carriers. Gut 18: 997-1003.
11. Abrahem A, Pelchat M, (2008) Formation of an RNA polymerase II preinitiation complex on an RNA promoter derived from the hepatitis delta virus RNA genome. Nucleic Acids Res 36: 5201-5211.
12. Filipovska J, Konarska MM, (2000) Specific HDV RNA-templated transcription by pol II in vitro. RNA 6: 41-54.
13. Greco-Stewart VS, Miron P, Abrahem A, Pelchat M, (2007) The human RNA polymerase II interacts with the terminal stem-loop regions of the hepatitis delta virus RNA genome. Virology 357: 68-78.
14. Gudima S, Wu SY, Chiang CM, Moraleda G, Taylor J, (2000) Origin of hepatitis delta virus mRNA. J Virol 74: 7204-7210.
15. Moraleda G, Taylor J, (2001) Host RNA polymerase requirements for transcription of the human hepatitis delta virus genome. J Virol 75: 10161-10169.
16. Fu TB, Taylor J, (1993) The RNAs of hepatitis delta virus are copied by RNA polymerase II in nuclear homogenates. J Virol 67: 6965-6972.
17. Chang J, Nie X, Chang HE, Han Z, Taylor J, (2008) Transcription of hepatitis delta virus RNA by RNA polymerase II. J Virol 82: 1118-1127.
18. Beard MR, MacNaughton TB, Gowans EJ, (1996) Identification and characterization of a hepatitis delta virus RNA transcriptional promoter. J Virol 70: 4986-4995.
19. Gudima S, Dingle K, Wu TT, Moraleda G, Taylor J, (1999) Characterization of the 5′ ends for polyadenylated RNAs synthesized during the replication of hepatitis delta virus. J Virol 73: 6533-6539.
20. Wu TT, Netter HJ, Lazinski DW, Taylor JM, (1997) Effects of nucleotide changes on the ability of hepatitis delta virus to transcribe, process, and accumulate unit-length, circular RNA. J Virol 71: 5408-5414.
21. Greco-Stewart V, Pelchat M, (2010) Interaction of host cellular proteins with components of the hepatitis delta virus. Viruses 2: 189-212.
22. Sikora D, Greco-Stewart VS, Miron P, Pelchat M, (2009) The hepatitis delta virus RNA genome interacts with eEF1A1, p54(nrb), hnRNP-L, GAPDH and ASF/SF2. Virology 390: 71-78.
23. Zahler AM, Lane WS, Stolk JA, Roth MB, (1992) SR proteins: a conserved family of pre-mRNA splicing factors. Genes Dev 6: 837-847.
24. Zahler AM, Neugebauer KM, Lane WS, Roth MB, (1993) Distinct functions of SR proteins in alternative pre-mRNA splicing. Science 260: 219-222.
25. Birney E, Kumar S, Krainer AR, (1993) Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res 21: 5803-5816.
26. Cramer P, Caceres JF, Cazalla D, Kadener S, Muro AF, et al. (1999) Coupling of transcription with alternative splicing: RNA pol II promoters modulate SF2/ASF and 9G8 effects on an exonic splicing enhancer. Mol Cell 4: 251-258.
27. McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G, et al. (1997) The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385: 357-361.
28. Millhouse S, Manley JL, (2005) The C-terminal domain of RNA polymerase II functions as a phosphorylation-dependent splicing activator in a heterologous protein. Mol Cell Biol 25: 533-544.
29. Huang Y, Steitz JA, (2005) SRprises along a messenger's journey. Mol Cell 17: 613-615.
30. Caceres JF, Screaton GR, Krainer AR, (1998) A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev 12: 55-66.
31. Lemaire R, Prasad J, Kashima T, Gustafson J, Manley JL, et al. (2002) Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: a novel function for SR proteins. Genes Dev 16: 594-607.
32. Sanford JR, Gray NK, Beckmann K, Caceres JF, (2004) A novel role for shuttling SR proteins in mRNA translation. Genes Dev 18: 755-768.
33. Li X, Manley JL, (2005) Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 122: 365-378.
34. Rocheleau L, Pelchat M, (2006) The Subviral RNA Database: a toolbox for viroids, the hepatitis delta virus and satellite RNAs research. BMC Microbiol 6: 24.
35. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
36. Crooks GE, Hon G, Chandonia JM, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
37. Chang J, Gudima SO, Tarn C, Nie X, Taylor JM, (2005) Development of a novel system to study hepatitis delta virus genome replication. J Virol 79: 8182-8188.
38. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
39. Ge H, Zuo P, Manley JL, (1991) Primary structure of the human splicing factor ASF reveals similarities with Drosophila regulators. Cell 66: 373-382.
40. Krainer AR, Mayeda A, Kozak D, Binns G, (1991) Functional expression of cloned human splicing factor SF2: homology to RNA-binding proteins, U1 70K, and Drosophila splicing regulators. Cell 66: 383-394.
41. Eftink MR, Ghiron CA, (1976) Exposure of tryptophanyl residues in proteins. Quantitative determination by fluorescence quenching studies. Biochemistry 15: 672-680.
42. Benzaghou I, Bougie I, Picard-Jean F, Bisaillon M, (2006) Energetics of RNA binding by the West Nile virus RNA triphosphatase. FEBS Lett 580: 867-877.
43. Souliere MF, Perreault JP, Bisaillon M, (2008) Magnesium-binding studies reveal fundamental differences between closely related RNA triphosphatases. Nucleic Acids Res 36: 451-461.
44. Greco-Stewart VS, Schissel E, Pelchat M, (2009) The hepatitis delta virus RNA genome interacts with the human RNA polymerases I and III. Virology 386: 12-15.
45. Graveley BR, (2000) Sorting out the complexity of SR protein functions. RNA 6: 1197-1211.
46. Wang X, Juan L, Lv J, Wang K, Sanford JR, et al. (2011) Predicting sequence and structural specificities of RNA binding regions recognized by splicing factor SRSF1. BMC Genomics 12Suppl 5: S8.
47. Sanford JR, Wang X, Mort M, Vanduyn N, Cooper DN, et al. (2009) Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res 19: 381-394.
48. Li X, Wang J, Manley JL, (2005) Loss of splicing factor ASF/SF2 induces G2 cell cycle arrest and apoptosis, but inhibits internucleosomal DNA fragmentation. Genes Dev 19: 2705-2714.
49. Bougie I, Bisaillon M, (2007) Characterization of the RNA binding energetics of the Candida albicans poly(A) polymerase. Yeast 24: 431-446.
50. Bougie I, Parent A, Bisaillon M, (2004) Thermodynamics of ligand binding by the yeast mRNA-capping enzyme reveals different modes of binding. Biochem J 384: 411-420.
51. Elton D, Medcalf L, Bishop K, Harrison D, Digard P, (1999) Identification of amino acid residues of influenza virus nucleoprotein essential for RNA binding. J Virol 73: 7357-7367.
52. Flowers S, Biswas EE, Biswas SB, (2003) Conformational dynamics of DnaB helicase upon DNA and nucleotide binding: analysis by intrinsic tryptophan fluorescence quenching. Biochemistry 42: 1910-1921.
53. Teale FW, Weber G, (1957) Ultraviolet fluorescence of the aromatic amino acids. Biochem J 65: 476-482.
54. Tintaru AM, Hautbergue GM, Hounslow AM, Hung ML, Lian LY, et al. (2007) Structural and functional analysis of RNA and TAP binding to SF2/ASF. EMBO Rep 8: 756-762.
55. Brun F, Toulme JJ, Helene C, (1975) Interactions of aromatic residues of proteins with nucleic acids. Fluorescence studies of the binding of oligopeptides containing tryptophan and tyrosine residues to polynucleotides. Biochemistry 14: 558-563.
56. Gorlach M, Wittekind M, Beckman RA, Mueller L, Dreyfuss G, (1992) Interaction of the RNA-binding domain of the hnRNP C proteins with RNA. EMBO J 11: 3289-3295.
57. Jessen TH, Oubridge C, Teo CH, Pritchard C, Nagai K, (1991) Identification of molecular contacts between the U1 A small nuclear ribonucleoprotein and U1 RNA. EMBO J 10: 3447-3456.
58. Petrik J, Parker H, Alexander GJ, (1999) Human hepatic glyceraldehyde-3-phosphate dehydrogenase binds to the poly(U) tract of the 3′ non-coding region of hepatitis C virus genomic RNA. J Gen Virol 80 (Pt 12): 3109-3113.
59. Oubridge C, Ito N, Evans PR, Teo CH, Nagai K, (1994) Crystal structure at 1.92 A resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature 372: 432-438.
60. Ueda H, Iyo H, Doi M, Inoue M, Ishida T, (1991) Cooperative stacking and hydrogen bond pairing interactions of fragment peptide in cap binding protein with mRNA cap structure. Biochim Biophys Acta 1075: 181-186.
61. Manley JL, Tacke R, (1996) SR proteins and splicing control. Genes Dev 10: 1569-1579.
62. Smith PJ, Zhang C, Wang J, Chew SL, Zhang MQ, et al. (2006) An increased specificity score matrix for the prediction of SF2/ASF-specific exonic splicing enhancers. Hum Mol Genet 15: 2490-2508.
63. Sanford JR, Coutinho P, Hackett JA, Wang X, Ranahan W, et al. (2008) Identification of nuclear and cytoplasmic mRNA targets for the shuttling protein SF2/ASF. PLoS ONE 3: e3369.
64. Maris C, Dominguez C, Allain FH, (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272: 2118-2131.
65. Allain FH, Gubser CC, Howe PW, Nagai K, Neuhaus D, et al. (1996) Specificity of ribonucleoprotein interaction determined by RNA folding during complex formulation. Nature 380: 646-650.
66. Showalter SA, Hall KB, (2004) Altering the RNA-binding mode of the U1A RBD1 protein. J Mol Biol 335: 465-480.
67. Sinha R, Allemand E, Zhang Z, Karni R, Myers MP, et al. (2010) Arginine methylation controls the subcellular localization and functions of the oncoprotein splicing factor SF2/ASF. Mol Cell Biol 30: 2762-2774.
68. Misteli T, (1999) RNA splicing: What has phosphorylation got to do with it? Curr Biol 9: R198-200.
69. Ong SE, Mittler G, Mann M, (2004) Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat Methods 1: 119-126.