The 3′ untranslated region of the rabies virus glycoprotein mRNA specifically interacts with cellular PCBP2 protein and promotes transcript stability

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Palusa, Saiprasad ^a   Ndaluka, Christina ^a   Bowen, Richard A ^a   Wilusz, Carol J ^a   Wilusz, Jeffrey ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; POLY(RC) BINDING PROTEIN 2; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; GLYCOPROTEIN; GLYCOPROTEIN G, RABIES VIRUS; PCBP2 PROTEIN, HUMAN; RNA BINDING PROTEIN; VIRUS ANTIGEN; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN RNA BINDING; RABIES; RABIES VIRUS; REPORTER GENE; RNA SEQUENCE; RNA STABILITY; TRANSCRIPTION REGULATION; ANIMAL; CELL LINE; CELL STRAIN HEK293; GENETICS; HAMSTER; HELA CELL; HOST PATHOGEN INTERACTION; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RNA PROCESSING; VIROLOGY;

RABIES VIRUS; RHABDOVIRIDAE;

3' UNTRANSLATED REGIONS; ANIMALS; ANTIGENS, VIRAL; BASE SEQUENCE; CELL LINE; CRICETINAE; GLYCOPROTEINS; HEK293 CELLS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; RABIES; RABIES VIRUS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; RNA, VIRAL; RNA-BINDING PROTEINS; VIRAL ENVELOPE PROTEINS;

EID: 84858383397     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033561     Document Type: Article

References (41)

1. Cheadle C, Fan J, Cho-Chung YS, Werner T, Ray J, et al. (2005) Control of gene expression during T cell activation: alternate regulation of mRNA transcription and mRNA stability. BMC Genomics 6: 75.
2. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, et al. (2011) Global quantification of mammalian gene expression control. Nature 473: 337-342.
3. Morris AR, Mukherjee N, Keene J, (2010) Systematic analysis of posttranscriptional gene expression. Wiley Interdiscip Rev Syst Biol Med 2: 162-180.
4. Keene JD, (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8: 533-543.
5. Djuranovic S, Nahvi A, Green R, (2011) A parsimonious model for gene regulation by miRNAs. Science 331: 550-553.
6. Albertini AA, Ruigrok RW, Blondel D, (2011) Rabies virus transcription and replication. Adv Virus Res 79: 1-22.
7. Dickson AM, Wilusz J, (2011) Strategies for viral RNA stability: live long and prosper. Trends Genet 27: 286-293.
8. Whelan SP, Barr JN, Wertz GW, (2004) Transcription and replication of nonsegmented negative-strand RNA viruses. Curr Top Microbiol Immunol 283: 61-119.
9. Schnell MJ, McGettigan JP, Wirblich C, Papaneri A, (2010) The cell biology of rabies virus: using stealth to reach the brain. Nat Rev Microbiol 8: 51-61.
10. Morimoto K, Hooper DC, Spitsin S, Koprowski H, Dietzschold B, (1999) Pathogenicity of different rabies virus variants inversely correlates with apoptosis and rabies virus glycoprotein expression in infected primary neuron cultures. J Virol 73: 510-518.
11. Sarmento L, Li XQ, Howerth E, Jackson AC, Fu ZF, (2005) Glycoprotein-mediated induction of apoptosis limits the spread of attenuated rabies viruses in the central nervous system of mice. J Neurovirol 11: 571-581.
12. Ravkov EV, Smith JS, Nichol ST, (1995) Rabies virus glycoprotein gene contains a long 3′ noncoding region which lacks pseudogene properties. Virology 206: 718-723.
13. Wu X, Franka R, Velasco-Villa A, Rupprecht CE, (2007) Are all lyssavirus genes equal for phylogenetic analyses? Virus Res 129: 91-103.
14. Kong J, Ji X, Liebhaber SA, (2003) The KH-domain protein alpha CP has a direct role in mRNA stabilization independent of its cognate binding site. Mol Cell Biol 23: 1125-1134.
15. Waggoner SA, Liebhaber SA, (2003) Identification of mRNAs associated with alphaCP2-containing RNP complexes. Mol Cell 23: 7055-7067.
16. Xu L, Sterling CR, Tank AW, (2009) cAMP-mediated stimulation of tyrosine hydroxylase mRNA translation is mediated by polypyrimidine-rich sequences within its 3′-untranslated region and poly(C)-binding protein 2. Mol Pharmacol 76: 872-883.
17. Ghosh D, Srivastava GP, Xu D, Schulz LC, Roberts RM, (2008) A link between SIN1 (MAPKAP1) and poly(rC) binding protein 2 (PCBP2) in counteracting environmental stress. Proc Natl Acad Sci U S A 105: 11673-11678.
18. Du Z, Fenn S, Tjhen R, James TL, (2008) Structure of a construct of a human poly(C)-binding protein containing the first and second KH domains reveals insights into its regulatory mechanisms. J Biol Chem 283: 28757-28766.
19. Finke S, Cox JH, Conzelmann KK, (2000) Differential transcription attenuation of rabies virus genes by intergenic regions: generation of recombinant viruses overexpressing the polymerase gene. J Virol 74: 7261-7269.
20. Dölken L, Ruzsics Z, Rädle B, Friedel CC, Zimmer R, et al. (2008) High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA 14: 1959-1972.
21. Friedel CC, Dölken L, Ruzsics Z, Koszinowski UH, Zimmer R, (2009) Conserved principles of mammalian transcriptional regulation revealed by RNA half-life. Nucleic Acids Res 37: e115.
22. Bergman N, Moraes KC, Anderson JR, Zaric B, Kambach C, et al. (2007) Lsm proteins bind and stabilize RNAs containing 5′ poly(A) tracts. Nat Struct Mol Biol 14: 824-831.
23. Ford LP, Watson J, Keene JD, Wilusz J, (1999) ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system. Genes Dev 13: 188-201.
24. Gao M, Fritz DT, Ford LP, Wilusz J, (2000) Interaction between a poly(A)-specific ribonuclease and the 5′ cap influences mRNA deadenylation rates in vitro. Mol Cell 5: 479-488.
25. Gao M, Wilusz CJ, Peltz SW, Wilusz J, (2001) A novel mRNA-decapping activity in HeLa cytoplasmic extracts is regulated by AU-rich elements. EMBO J 20: 1134-1143.
26. Mukherjee D, Gao M, O'Connor JP, Raijmakers R, Pruijn G, et al. (2002) The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J 21: 165-174.
27. Waggoner SA, Johannes GJ, Liebhaber SA, (2009) Depletion of the poly(C)-binding proteins alphaCP1 and alphaCP2 from K562 cells leads to p53-independent induction of cyclin-dependent kinase inhibitor (CDKN1A) and G1 arrest. J Biol Chem 284: 9039-9049.
28. Fenn S, Du Z, Lee JK, Tjhen R, Stroud RM, et al. (2007) Crystal structure of the third KH domain of human poly(C)-binding protein-2 in complex with a C-rich strand of human telomeric DNA at 1.6 A resolution. Nucleic Acids Res 35: 2651-2660.
29. Fujimura K, Katahira J, Kano F, Yoneda Y, Murata M, (2009) Selective localization of PCBP2 to cytoplasmic processing bodies. Biochim Biophys Acta 1793: 878-887.
30. Ogram SA, Spear A, Sharma N, Flanegan JB, (2010) The 5′CL-PCBP RNP complex, 3′ poly(A) tail and 2A(pro) are required for optimal translation of poliovirus RNA. Virology 397: 14-22.
31. Sean P, Nguyen JH, Semler BL, (2009) Altered interactions between stem-loop IV within the 5′ noncoding region of coxsackievirus RNA and poly(rC) binding protein 2: effects on IRES-mediated translation and viral infectivity. Virology 389: 45-58.
32. Toyoda H, Franco D, Fujita K, Paul AV, Wimmer E, (2007) Replication of poliovirus requires binding of the poly(rC) binding protein to the cloverleaf as well as to the adjacent C-rich spacer sequence between the cloverleaf and the internal ribosomal entry site. J 81: 10017-10028.
33. Perera R, Daijogo S, Walter BL, Nguyen JH, Semler BL, (2007) Cellular protein modification by poliovirus: the two faces of poly(rC)-binding protein. J Virol 81: 8919-8932.
34. Fontanes V, Raychaudhuri S, Dasgupta A, (2009) A cell-permeable peptide inhibits hepatitis C virus replication by sequestering IRES transacting factors. Virology 394: 82-90.
35. Wang L, Jeng KS, Lai MM, (2011) Poly(C)-binding protein 2 interacts with sequences required for viral replication in the hepatitis C virus (HCV) 5′ untranslated region and directs HCV RNA replication through circularizing the viral genome. J Virol 85: 7954-7964.
36. You F, Sun H, Zhou X, Sun W, Liang S, et al. (2009) PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat Immunol 10: 1300-1308.
37. Silvera D, Gamarnik AV, Andino R, (1999) The N-terminal K homology domain of the poly(rC)-binding protein is a major determinant for binding to the poliovirus 5′-untranslated region and acts as an inhibitor of viral translation. J Biol Chem 274: 38163-38170.
38. Dinh PX, Beura LK, Panda D, Das A, Pattnaik AK, (2011) Antagonistic effects of cellular poly(C) binding proteins on vesicular stomatitis virus gene expression. J Virol 85: 9459-9471.
39. Fitzgerald KD, Semler B, (2011) Re-localization of cellular protein SRp20 during poliovirus infection: bridging a viral IRES to the host cell translation apparatus. PLoS Pathog 7: e1002127.
40. Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, et al. (2011) Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell 43: 327-339.
41. Wilusz J, Shenk T, (1988) A 64 kd nuclear protein binds to RNA segments that include the AAUAAA polyadenylation motif. Cell 52: 221-228.