A structured RNA in hepatitis B virus post-transcriptional regulatory element represses alternative splicing in a sequence-independent and position-dependent manner

FEBS Journal

Volumn 278, Issue 9, 2011, Pages 1533-1546

  Huang, Chen ^a,b   Xie, Mao Hua ^a   Liu, Wei ^a   Yang, Bo ^a   Yang, Fan ^a   Huang, Jingang ^a   Huang, Jie ^a   Wu, Qijia ^a   Fu, Xiang Dong ^a,c   Zhang, Yi ^a,b  

^a WUHAN UNIVERSITY   (China)

^b ABLife Inc   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

alternative splicing; HBV PRE; hepatitis B virus (HBV); intronic splicing silencer (ISS); RNA structure

Indexed keywords

NUCLEOTIDE; POLYPYRIMIDINE TRACT BINDING PROTEIN; RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING SITE; CELL LINE; CONTROLLED STUDY; GENE MUTATION; GENE SILENCING; HEPATITIS B VIRUS; HOST; HUMAN; HUMAN CELL; INTRON; INTRONIC SPLICING SILENCER; NUCLEIC ACID STRUCTURE; POSTTRANSCRIPTIONAL REGULATORY ELEMENT; PRIORITY JOURNAL; REPORTER GENE; RNA STRUCTURE; VIRUS GENOME; VIRUS REPLICATION;

ALTERNATIVE SPLICING; BASE SEQUENCE; EXONS; GENE SILENCING; GENOME, VIRAL; HEPATITIS B VIRUS; INTRONS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; REGULATORY SEQUENCES, NUCLEIC ACID; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, VIRAL;

HEPATITIS B VIRUS;

EID: 79955069036     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08077.x     Document Type: Article

References (47)

1. Wang ET, &, Sandberg R, (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470-476. (Pubitemid 352759009)
2. Pan Q, Shai O, Lee FJ, Frey BJ, &, Blencowe BJ, (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40, 1413-1415.
3. Cooper TA, (2005) Alternative splicing regulation impacts heart development. Cell 120, 1-2. (Pubitemid 40094593)
4. Li Q, Lee JA, &, Black DL, (2007) Neuronal regulation of alternative pre-mRNA splicing. Nat Rev Neurosci 8, 819-831. (Pubitemid 350006218)
5. Wang Z, &, Burge CB, (2008) Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 14, 802-813. (Pubitemid 351574901)
6. Black DL, (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72, 291-336. (Pubitemid 36930448)
7. Hertel KJ, (2008) Combinatorial control of exon recognition. J Biol Chem 283, 1211-1215.
8. Shepard PJ, &, Hertel KJ, (2008) Conserved RNA secondary structures promote alternative splicing. RNA 14, 1463-1469.
9. Warf MB, &, Berglund JA, (2010) Role of RNA structure in regulating pre-mRNA splicing. Trends Biochem Sci 35, 169-178.
10. Buratti E, &, Baralle FE, (2004) Influence of RNA secondary structure on the pre-mRNA splicing process. Mol Cell Biol 24, 10505-10514. (Pubitemid 39603113)
11. Buratti E, Muro AF, Giombi M, Gherbassi D, Laconcig A, &, Baralle FE, (2004) RNA folding affects the recruitment of SR proteins by mouse and human polypurinic enhancer elements in the fibronectin EDA exon. Mol Cell Biol 24, 1387-1400. (Pubitemid 38112198)
12. Giedroc DP, &, Cornish PV, (2009) Frameshifting RNA pseudoknots: structure and mechanism. Virus Res 139, 193-208.
13. Balvay L, Soto RR, Ricci EP, Decimo D, &, Ohlmann T, (2009) Structural and functional diversity of viral IRESes. Biochim Biophys Acta 1789, 542-557.
14. Saliou JM, Bourgeois CF, Ayadi-Ben ML, Ropers D, Jacquenet S, Marchand V, Stevenin J, &, Branlant C, (2009) Role of RNA structure and protein factors in the control of HIV-1 splicing. Front Biosci 14, 2714-2729.
15. Sommer G, &, Heise T, (2008) Posttranscriptional control of HBV gene expression. Front Biosci 13, 5533-5547.
16. Park GS, Kim HY, Shin HS, Park S, Shin HJ, &, Kim K, (2008) Modulation of hepatitis B virus replication by expression of polymerase-surface fusion protein through splicing: implications for viral persistence. Virus Res 136, 166-174.
17. Ma ZM, Lin X, Wang YX, Tian XC, Xie YH, &, Wen YM, (2009) A double-spliced defective hepatitis B virus genome derived from hepatocellular carcinoma tissue enhanced replication of full-length virus. J Med Virol 81, 230-237.
18. Soussan P, Tuveri R, Nalpas B, Garreau F, Zavala F, Masson A, Pol S, Brechot C, &, Kremsdorf D, (2003) The expression of hepatitis B spliced protein (HBSP) encoded by a spliced hepatitis B virus RNA is associated with viral replication and liver fibrosis. J Hepatol 38, 343-348. (Pubitemid 36286548)
19. Huang J, &, Liang TJ, (1993) A novel hepatitis B virus (HBV) genetic element with Rev response element-like properties that is essential for expression of HBV gene products. Mol Cell Biol 13, 7476-7486. (Pubitemid 23354272)
20. Donello JE, Beeche AA, Smith GJ III, Lucero GR, &, Hope TJ, (1996) The hepatitis B virus posttranscriptional regulatory element is composed of two subelements. J Virol 70, 4345-4351. (Pubitemid 26187436)
21. Patzel V, &, Sczakiel G, (1997) The hepatitis B virus posttranscriptional regulatory element contains a highly stable RNA secondary structure. Biochem Biophys Res Commun 231, 864-867. (Pubitemid 27218312)
22. Heise T, Sommer G, Reumann K, Meyer I, Will H, &, Schaal H, (2006) The hepatitis B virus PRE contains a splicing regulatory element. Nucleic Acids Res 34, 353-363. (Pubitemid 43160058)
23. Miyaso H, Okumura M, Kondo S, Higashide S, Miyajima H, &, Imaizumi K, (2003) An intronic splicing enhancer element in survival motor neuron (SMN) pre-mRNA. J Biol Chem 278, 15825-15831. (Pubitemid 36799697)
24. Muh SJ, Hovhannisyan RH, &, Carstens RP, (2002) A non-sequence-specific double-stranded RNA structural element regulates splicing of two mutually exclusive exons of fibroblast growth factor receptor 2 (FGFR2). J Biol Chem 277, 50143-50154. (Pubitemid 36014468)
25. Singh RN, (2007) Evolving concepts on human SMN pre-mRNA splicing. RNA Biol 4, 7-10. (Pubitemid 47328287)
26. Liu W, Zhou Y, Hu Z, Sun T, Denise A, Fu XD, &, Zhang Y, (2010) Regulation of splicing enhancer activities by RNA secondary structures. FEBS Lett 584, 4401-4407.
27. Singh NK, Singh NN, Androphy EJ, &, Singh RN, (2006) Splicing of a critical exon of human survival motor neuron is regulated by a unique silencer element located in the last intron. Mol Cell Biol 26, 1333-1346. (Pubitemid 43202560)
28. Miyajima H, Miyaso H, Okumura M, Kurisu J, &, Imaizumi K, (2002) Identification of a cis-acting element for the regulation of SMN exon 7 splicing. J Biol Chem 277, 23271-23277. (Pubitemid 34952155)
29. Singh NN, Singh RN, &, Androphy EJ, (2007) Modulating role of RNA structure in alternative splicing of a critical exon in the spinal muscular atrophy genes. Nucleic Acids Res 35, 371-389. (Pubitemid 46232056)
30. Kashima T, Rao N, &, Manley JL, (2007) An intronic element contributes to splicing repression in spinal muscular atrophy. Proc Natl Acad Sci USA 104, 3426-3431. (Pubitemid 46364175)
31. Gladman JT, &, Chandler DS, (2009) Intron 7 conserved sequence elements regulate the splicing of the SMN genes. Hum Genet 126, 833-841.
32. Smith GJ III, Donello JE, Luck R, Steger R, &, Hope TJ, (1998) The hepatitis B virus post-transcriptional regulatory element contains two conserved RNA stem-loops which are required for function. Nucleic Acids Res 26, 4818-4827. (Pubitemid 28491157)
33. Carstens RP, Wagner EJ, &, Garcia-Blanco MA, (2000) An intronic splicing silencer causes skipping of the IIIb exon of fibroblast growth factor receptor 2 through involvement of polypyrimidine tract binding protein. Mol Cell Biol 20, 7388-7400.
34. Xue Y, Zhou Y, Wu T, Zhu T, Ji X, Kwon YS, Zhang C, Yeo G, Black DL, Sun H, et al. (2009) Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol Cell 36, 996-1006.
35. Sen S, Talukdar I, &, Webster NJ, (2009) SRp20 and CUG-BP1 modulate insulin receptor exon 11 alternative splicing. Mol Cell Biol 29, 871-880.
36. Zang WQ, Li B, Huang PY, Lai MM, &, Yen SS, (2001) Role of polypyrimidine tract binding protein in the function of the hepatitis B virus posttranscriptional regulatory element. J Virol 75, 10779-10786. (Pubitemid 33031547)
37. Sawicka K, Bushell M, Spriggs KA, &, Willis AE, (2008) Polypyrimidine-tract-binding protein: A multifunctional RNA-binding protein. Biochem Soc Trans 36, 641-647.
38. Corrionero A, &, Valcarcel J, (2009) RNA processing: redrawing the map of charted territory. Mol Cell 36, 918-919.
39. Horne C, &, Young PJ, (2009) Is RNA manipulation a viable therapy for spinal muscular atrophy? J Neurol Sci 287, 27-31.
40. Lorson CL, Hahnen E, Androphy EJ, &, Wirth B, (1999) A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc Natl Acad Sci USA 96, 6307-6311. (Pubitemid 29256661)
41. Burghes AH, &, Beattie CE, (2009) Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick? Nat Rev Neurosci 10, 597-609.
42. Shukla S, Del Gatto-Konczak F, Breathnach R, &, Fisher SA, (2005) Competition of PTB with TIA proteins for binding to a U-rich cis-element determines tissue-specific splicing of the myosin phosphatase targeting subunit 1. RNA 11, 1725-1736. (Pubitemid 41505547)
43. Sharma S, Kohlstaedt LA, Damianov A, Rio DC, &, Black DL, (2008) Polypyrimidine tract binding protein controls the transition from exon definition to an intron defined spliceosome. Nat Struct Mol Biol 15, 183-191. (Pubitemid 351207512)
44. Wang J, Smith PJ, Krainer AR, &, Zhang MQ, (2005) Distribution of SR protein exonic splicing enhancer motifs in human protein-coding genes. Nucleic Acids Res 33, 5053-5062. (Pubitemid 41487813)
45. Ibrahim EC, Schaal TD, Hertel KJ, Reed R, &, Maniatis T, (2005) Serine/arginine-rich protein-dependent suppression of exon skipping by exonic splicing enhancers. Proc Natl Acad Sci USA 102, 5002-5007.
46. Stoltzfus CM, &, Madsen JM, (2006) Role of viral splicing elements and cellular RNA binding proteins in regulation of HIV-1 alternative RNA splicing. Curr HIV Res 4, 43-55.
47. Crooks GE, Hon G, Chandonia JM, &, Brenner SE, (2004) WebLogo: A sequence logo generator. Genome Res 14, 1188-1190. (Pubitemid 38811555)