Re-localization of cellular protein SRp20 during poliovirus infection: Bridging a viral IRES to the host cell translation apparatus

PLoS Pathogens

Volumn 7, Issue 7, 2011, Pages

  Fitzgerald, Kerry D ^a   Semler, Bert L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SRP20; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA; PCBP2 PROTEIN, HUMAN; RNA BINDING PROTEIN; SRSF3 PROTEIN, HUMAN;

ARTICLE; CYTOPLASM; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; NEUROBLASTOMA CELL; NONHUMAN; POLIOMYELITIS; POLIOMYELITIS VIRUS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIRUS TRANSCRIPTION; WILD TYPE; ACTIVE TRANSPORT; BIOLOGICAL MODEL; CELL NUCLEUS; GENETICS; HELA CELL; METABOLISM; MUTATION; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN SYNTHESIS; VIROLOGY;

POLIOVIRUS;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; CELL NUCLEUS; CYTOPLASM; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; MUTATION; POLIOMYELITIS; POLIOVIRUS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RNA, VIRAL; RNA-BINDING PROTEINS;

EID: 79960948097     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002127     Document Type: Article

References (58)

1. Kozak M, (1984) Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res 12: 857-872.
2. Fitzgerald KD, Semler BL, (2009) Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim Biophys Acta 1789: 518-528.
3. Baird SD, Lewis SM, Turcotte M, Holcik M, (2007) A search for structurally similar cellular internal ribosome entry sites. Nucleic Acids Res 35: 4664-4677.
4. Baird SD, Turcotte M, Korneluk RG, Holcik M, (2006) Searching for IRES. RNA 12: 1755-1785.
5. Jang SK, Krausslich HG, Nicklin MJ, Duke GM, Palmenberg AC, et al. (1988) A segment of the 5′ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J Virol 62: 2636-2643.
6. Pelletier J, Kaplan G, Racaniello VR, Sonenberg N, (1988) Cap-independent translation of poliovirus mRNA is conferred by sequence elements within the 5′ noncoding region. Mol Cell Biol 8: 1103-1112.
7. Pelletier J, Sonenberg N, (1988) Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334: 320-325.
8. Etchison D, Milburn SC, Edery I, Sonenberg N, Hershey JW, (1982) Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J Biol Chem 257: 14806-14810.
9. Krausslich HG, Nicklin MJ, Toyoda H, Etchison D, Wimmer E, (1987) Poliovirus proteinase 2A induces cleavage of eucaryotic initiation factor 4F polypeptide p220. J Virol 61: 2711-2718.
10. Lloyd RE, Jense HG, Ehrenfeld E, (1987) Restriction of translation of capped mRNA in vitro as a model for poliovirus-induced inhibition of host cell protein synthesis: relationship to p220 cleavage. J Virol 61: 2480-2488.
11. Joachims M, Van Breugel PC, Lloyd RE, (1999) Cleavage of poly(A)-binding protein by enterovirus proteases concurrent with inhibition of translation in vitro. J Virol 73: 718-727.
12. Kerekatte V, Keiper BD, Badorff C, Cai A, Knowlton KU, et al. (1999) Cleavage of Poly(A)-binding protein by coxsackievirus 2A protease in vitro and in vivo: another mechanism for host protein synthesis shutoff? J Virol 73: 709-717.
13. Kuyumcu-Martinez NM, Joachims M, Lloyd RE, (2002) Efficient cleavage of ribosome-associated poly(A)-binding protein by enterovirus 3C protease. J Virol 76: 2062-2074.
14. Makeyev AV, Liebhaber SA, (2002) The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms. RNA 8: 265-278.
15. Walter BL, Nguyen JH, Ehrenfeld E, Semler BL, (1999) Differential utilization of poly(rC) binding protein 2 in translation directed by picornavirus IRES elements. RNA 5: 1570-1585.
16. Blyn LB, Towner JS, Semler BL, Ehrenfeld E, (1997) Requirement of poly(rC) binding protein 2 for translation of poliovirus RNA. J Virol 71: 6243-6246.
17. Walter BL, Parsley TB, Ehrenfeld E, Semler BL, (2002) Distinct poly(rC) binding protein KH domain determinants for poliovirus translation initiation and viral RNA replication. J Virol 76: 12008-12022.
18. Bedard KM, Daijogo S, Semler BL, (2007) A nucleo-cytoplasmic SR protein functions in viral IRES-mediated translation initiation. EMBO J 26: 459-467.
19. Zahler AM, Lane WS, Stolk JA, Roth MB, (1992) SR proteins: a conserved family of pre-mRNA splicing factors. Genes Dev 6: 837-847.
20. Caceres JF, Misteli T, Screaton GR, Spector DL, Krainer AR, (1997) Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J Cell Biol 138: 225-238.
21. 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.
22. Huang Y, Steitz JA, (2001) Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol Cell 7: 899-905.
23. Long JC, Caceres JF, (2009) The SR protein family of splicing factors: master regulators of gene expression. Biochem J 417: 15-27.
24. Bjork P, Jin S, Zhao J, Singh OP, Persson JO, et al. (2009) Specific combinations of SR proteins associate with single pre-messenger RNAs in vivo and contribute different functions. J Cell Biol 184: 555-568.
25. Sanford JR, Gray NK, Beckmann K, Caceres JF, (2004) A novel role for shuttling SR proteins in mRNA translation. Genes Dev 18: 755-768.
26. Swartz JE, Bor YC, Misawa Y, Rekosh D, Hammarskjold ML, (2007) The shuttling SR protein 9G8 plays a role in translation of unspliced mRNA containing a constitutive transport element. J Biol Chem 282: 19844-19853.
27. Swanson CM, Sherer NM, Malim MH, (2010) SRp40 and SRp55 promote the translation of unspliced human immunodeficiency virus type 1 RNA. J Virol 84: 6748-6759.
28. Baltimore D, Girard M, Darnell JE, (1966) Aspects of Synthesis of Poliovirus Rna and Formation of Virus Particles. Virology 29: 179-189.
29. Puck TT, Marcus PI, Cieciura SJ, (1956) Clonal growth of mammalian cells in vitro; growth characteristics of colonies from single HeLa cells with and without a feeder layer. J Exp Med 103: 273-283.
30. Hargous Y, Hautbergue GM, Tintaru AM, Skrisovska L, Golovanov AP, et al. (2006) Molecular basis of RNA recognition and TAP binding by the SR proteins SRp20 and 9G8. EMBO J 25: 5126-5137.
31. Kuhn RJ, Wimmer E, Semler BL, (1987) Expression of the poliovirus genome from infectious cDNA is dependent upon arrangements of eukaryotic and prokaryotic sequences in recombinant plasmids. Virology 157: 560-564.
32. Dildine SL, Semler BL, (1992) Conservation of RNA-protein interactions among picornaviruses. J Virol 66: 4364-4376.
33. Sean P, Nguyen JH, Semler BL, (2008) The linker domain of poly(rC) binding protein 2 is a major determinant in poliovirus cap-independent translation. Virology 378: 243-253.
34. Neugebauer KM, Roth MB, (1997) Distribution of pre-mRNA splicing factors at sites of RNA polymerase II transcription. Genes Dev 11: 1148-1159.
35. Gustin KE, Sarnow P, (2001) Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J 20: 240-249.
36. Escudero-Paunetto L, Li L, Hernandez FP, Sandri-Goldin RM, (2010) SR proteins SRp20 and 9G8 contribute to efficient export of herpes simplex virus 1 mRNAs. Virology 401: 155-164.
37. Gamarnik AV, Andino R, (1997) Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA 3: 882-892.
38. Fujimura K, Kano F, Murata M, (2008) Identification of PCBP2, a facilitator of IRES-mediated translation, as a novel constituent of stress granules and processing bodies. RNA 14: 425-431.
39. Svitkin YV, Costa-Mattioli M, Herdy B, Perreault S, Sonenberg N, (2007) Stimulation of picornavirus replication by the poly(A) tail in a cell-free extract is largely independent of the poly(A) binding protein (PABP). RNA 13: 2330-2340.
40. Svitkin YV, Imataka H, Khaleghpour K, Kahvejian A, Liebig HD, et al. (2001) Poly(A)-binding protein interaction with elF4G stimulates picornavirus IRES-dependent translation. RNA 7: 1743-1752.
41. Summers DF, Maizel JVJ, Darnell JEJ, (1967) The decrease in size and synthetic activity of poliovirus polysomes late in the infectious cycle. Virology 31: 427-435.
42. Johannes G, Sarnow P, (1998) Cap-independent polysomal association of natural mRNAs encoding c-myc, BiP, and eIF4G conferred by internal ribosome entry sites. RNA 4: 1500-1513.
43. Johannes G, Carter MS, Eisen MB, Brown PO, Sarnow P, (1999) Identification of eukaryotic mRNAs that are translated at reduced cap binding complex eIF4F concentrations using a cDNA microarray. Proc Natl Acad Sci U S A 96: 13118-13123.
44. Blyn LB, Swiderek KM, Richards O, Stahl DC, Semler BL, et al. (1996) Poly(rC) binding protein 2 binds to stem-loop IV of the poliovirus RNA 5′ noncoding region: identification by automated liquid chromatography-tandem mass spectrometry. Proc Natl Acad Sci USA 93: 11115-11120.
45. Bedard KM, Walter BL, Semler BL, (2004) Multimerization of poly(rC) binding protein 2 is required for translation initiation mediated by a viral IRES. RNA 10: 1266-1276.
46. Kataoka N, Bachorik JL, Dreyfuss G, (1999) Transportin-SR, a nuclear import receptor for SR proteins. J Cell Biol 145: 1145-1152.
47. Lai MC, Lin RI, Huang SY, Tsai CW, Tarn WY, (2000) A human importin-beta family protein, transportin-SR2, interacts with the phosphorylated RS domain of SR proteins. J Biol Chem 275: 7950-7957.
48. Allemand E, Dokudovskaya S, Bordonne R, Tazi J, (2002) A conserved Drosophila transportin-serine/arginine-rich (SR) protein permits nuclear import of Drosophila SR protein splicing factors and their antagonist repressor splicing factor 1. Mol Biol Cell 13: 2436-2447.
49. Meerovitch K, Svitkin YV, Lee HS, Lejbkowicz F, Kenan DJ, et al. (1993) La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J Virol 67: 3798-3807.
50. Brunner JE, Ertel KJ, Rozovics JM, Semler BL, (2010) Delayed kinetics of poliovirus RNA synthesis in a human cell line with reduced levels of hnRNP C proteins. Virology 400: 240-247.
51. McBride AE, Schlegel A, Kirkegaard K, (1996) Human protein Sam68 relocalization and interaction with poliovirus RNA polymerase in infected cells. Proc Natl Acad Sci USA 93: 2296-2301.
52. Shiroki K, Isoyama T, Kuge S, Ishii T, Ohmi S, et al. (1999) Intracellular redistribution of truncated La protein produced by poliovirus 3Cpro-mediated cleavage. J Virol 73: 2193-2200.
53. Waggoner S, Sarnow P, (1998) Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirus-infected cells. J Virol 72: 6699-6709.
54. Back SH, Kim YK, Kim WJ, Cho S, Oh HR, et al. (2002) Translation of polioviral mRNA is inhibited by cleavage of polypyrimidine tract-binding proteins executed by polioviral 3C(pro). J Virol 76: 2529-2542.
55. Park N, Skern T, Gustin KE, (2010) Specific cleavage of the nuclear pore complex protein Nup62 by a viral protease. J Biol Chem 285: 28796-28805.
56. Belov GA, Lidsky PV, Mikitas OV, Egger D, Lukyanov KA, et al. (2004) Bidirectional increase in permeability of nuclear envelope upon poliovirus infection and accompanying alterations of nuclear pores. J Virol 78: 10166-10177.
57. Sonenberg N, Hinnebusch AG, (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
58. Blyn LB, Chen R, Semler BL, Ehrenfeld E, (1995) Host cell proteins binding to domain IV of the 5′ noncoding region of poliovirus RNA. J Virol 69: 4381-4389.