Requirements for eIF4A and eIF2 during translation of Sindbis virus subgenomic mRNA in vertebrate and invertebrate host cells

Cellular Microbiology

Volumn 15, Issue 5, 2013, Pages 823-840

  Garcia Moreno, Manuel ^a   Sanz, Miguel Angel ^a   Pelletier, Jerry ^b   Carrasco, Luis ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 2; INITIATION FACTOR 4A; MICRORNA;

ARTICLE; HOST CELL; MAMMAL CELL; MOSQUITO; NONHUMAN; PRIORITY JOURNAL; RNA TRANSLATION; SINDBIS VIRUS;

ARTHROPODA; INVERTEBRATA; MAMMALIA; SINDBIS VIRUS; VERTEBRATA;

ANIMALS; CRICETINAE; CULICIDAE; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-4A; HOST-PATHOGEN INTERACTIONS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA, VIRAL; SINDBIS VIRUS;

EID: 84876339347     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12079     Document Type: Article

References (54)

1. Abaeva, I.S., Marintchev, A., Pisareva, V.P., Hellen, C.U., and Pestova, T.V. (2011) Bypassing of stems versus linear base-by-base inspection of mammalian mRNAs during ribosomal scanning. EMBO J 30: 115-129.
2. Balvay, L., Soto Rifo, R., Ricci, E.P., Decimo, D., and Ohlmann, T. (2009) Structural and functional diversity of viral IRESes. Biochim Biophys Acta 1789: 542-557.
3. Belsham, G.J. (2009) Divergent picornavirus IRES elements. Virus Res 139: 183-192.
4. Bolte, S., and Cordelieres, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213-232.
5. Bordeleau, M.E., Mori, A., Oberer, M., Lindqvist, L., Chard, L.S., Higa, T., etal. (2006) Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat Chem Biol 2: 213-220.
6. Burgui, I., Yanguez, E., Sonenberg, N., and Nieto, A. (2007) Influenza virus mRNA translation revisited: is the eIF4E cap-binding factor required for viral mRNA translation? J Virol 81: 12427-12438.
7. Bushell, M., and Sarnow, P. (2002) Hijacking the translation apparatus by RNA viruses. J Cell Biol 158: 395-399.
8. Carrasco, L., and Smith, A.E. (1976) Sodium ions and the shut-off of host cell protein synthesis by picornaviruses. Nature 264: 807-809.
9. Castello, A., Sanz, M.A., Molina, S., and Carrasco, L. (2006) Translation of Sindbis virus 26S mRNA does not require intact eukariotic initiation factor 4G. J Mol Biol 355: 942-956.
10. Castello, A., Alvarez, E., and Carrasco, L. (2011) The multifaceted poliovirus 2A protease: regulation of gene expression by picornavirus proteases. J Biomed Biotechnol 2011: 369648.
11. Connor, J.H., and Lyles, D.S. (2002) Vesicular stomatitis virus infection alters the eIF4F translation initiation complex and causes dephosphorylation of the eIF4E binding protein 4E-BP1. J Virol 76: 10177-10187.
12. Fata-Hartley, C.L., and Palmenberg, A.C. (2005) Dipyridamole reversibly inhibits mengovirus RNA replication. J Virol 79: 11062-11070.
13. Fitzgerald, K.D., and Semler, B.L. (2009) Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim Biophys Acta 1789: 518-528.
14. Frolov, I., and Schlesinger, S. (1994) Translation of Sindbis virus mRNA: effects of sequences downstream of the initiating codon. J Virol 68: 8111-8117.
15. Frolov, I., and Schlesinger, S. (1996) Translation of Sindbis virus mRNA: analysis of sequences downstream of the initiating AUG codon that enhance translation. J Virol 70: 1182-1190.
16. Garry, R.F. (1994) Sindbis virus-induced inhibition of protein synthesis is partially reversed by medium containing an elevated potassium concentration. J Gen Virol 75 (Part 2): 411-415.
17. Garry, R.F., Bishop, J.M., Parker, S., Westbrook, K., Lewis, G., and Waite, M.R. (1979) Na+ and K+ concentrations and the regulation of protein synthesis in Sindbis virus-infected chick cells. Virology 96: 108-120.
18. Gingras, A.C., Raught, B., and Sonenberg, N. (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963.
19. Gorchakov, R., Frolova, E., Williams, B.R., Rice, C.M., and Frolov, I. (2004) PKR-dependent and -independent mechanisms are involved in translational shutoff during Sindbis virus infection. J Virol 78: 8455-8467.
20. Hertz, M.I., and Thompson, S.R. (2011) Mechanism of translation initiation by Dicistroviridae IGR IRESs. Virology 411: 355-361.
21. Hofacker, I.L. (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31: 3429-3431.
22. Jackson, R.J., Hellen, C.U., and Pestova, T.V. (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
23. Karpf, A.R., and Brown, D.T. (1998) Comparison of Sindbis virus-induced pathology in mosquito and vertebrate cell cultures. Virology 240: 193-201.
24. Kim, J.H., Park, S.M., Park, J.H., Keum, S.J., and Jang, S.K. (2011) eIF2A mediates translation of hepatitis C viral mRNA under stress conditions. EMBO J 30: 2454-2464.
25. Komar, A.A., Mazumder, B., and Merrick, W.C. (2012) A new framework for understanding IRES-mediated translation. Gene 502: 75-86.
26. Lindqvist, L., Oberer, M., Reibarkh, M., Cencic, R., Bordeleau, M.E., Vogt, E., etal. (2008) Selective pharmacological targeting of a DEAD box RNA helicase. PLoS ONE 3: e1583.
27. Lorsch, J.R., and Dever, T.E. (2010) Molecular view of 43 S complex formation and start site selection in eukaryotic translation initiation. J Biol Chem 285: 21203-21207.
28. McInerney, G.M., Kedersha, N.L., Kaufman, R.J., Anderson, P., and Liljestrom, P. (2005) Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol Biol Cell 16: 3753-3763.
29. Madan, V., Castello, A., and Carrasco, L. (2008) Viroporins from RNA viruses induce caspase-dependent apoptosis. Cell Microbiol 10: 437-451.
30. Mazroui, R., Sukarieh, R., Bordeleau, M.E., Kaufman, R.J., Northcote, P., Tanaka, J., etal. (2006) Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol Biol Cell 17: 4212-4219.
31. Miller, M.L., and Brown, D.T. (1992) Morphogenesis of Sindbis virus in three subclones of Aedes albopictus (mosquito) cells. J Virol 66: 4180-4190.
32. Mir, M.A., and Panganiban, A.T. (2008) A protein that replaces the entire cellular eIF4F complex. EMBO J 27: 3129-3139.
33. Niepmann, M. (2009) Internal translation initiation of picornaviruses and hepatitis C virus. Biochim Biophys Acta 1789: 529-541.
34. Nieva, J.L., Madan, V., and Carrasco, L. (2012) Viroporins: structure and biological functions. Nat Rev Microbiol 10: 563-574.
35. Parsyan, A., Svitkin, Y., Shahbazian, D., Gkogkas, C., Lasko, P., Merrick, W.C., and Sonenberg, N. (2011) mRNA helicases: the tacticians of translational control. Nat Rev Mol Cell Biol 12: 235-245.
36. Patel, R.K., and Hardy, R.W. (2012) Role for the phosphatidylinositol 3-kinase-Akt-TOR pathway during sindbis virus replication in arthropods. J Virol 86: 3595-3604.
37. Pestova, T.V., Kolupaeva, V.G., Lomakin, I.B., Pilipenko, E.V., Shatsky, I.N., Agol, V.I., and Hellen, C.U. (2001) Molecular mechanisms of translation initiation in eukaryotes. Proc Natl Acad Sci USA 98: 7029-7036.
38. Pisareva, V.P., Pisarev, A.V., Komar, A.A., Hellen, C.U., and Pestova, T.V. (2008) Translation initiation on mammalian mRNAs with structured 5′UTRs requires DExH-box protein DHX29. Cell 135: 1237-1250.
39. Redondo, N., Sanz, M.A., Welnowska, E., and Carrasco, L. (2011) Translation without eIF2 promoted by poliovirus 2A protease. PLoS ONE 6: e25699.
40. Sanz, M.A., Castello, A., Ventoso, I., Berlanga, J.J., and Carrasco, L. (2009) Dual mechanism for the translation of subgenomic mRNA from Sindbis virus in infected and uninfected cells. PLoS ONE 4: e4772.
41. Sanz, M.A., Welnowska, E., Redondo, N., and Carrasco, L. (2010) Translation driven by picornavirus IRES is hampered from Sindbis virus replicons: rescue by poliovirus 2A protease. J Mol Biol 402: 101-117.
42. Skabkin, M.A., Skabkina, O.V., Dhote, V., Komar, A.A., Hellen, C.U., and Pestova, T.V. (2010) Activities of Ligatin and MCT-1/DENR in eukaryotic translation initiation and ribosomal recycling. Genes Dev 24: 1787-1801.
43. Soderlund, H., and Ulmanen, I. (1977) Transient association of Semliki Forest virus capsid protein with ribosomes. J Virol 24: 907-909.
44. Sonenberg, N., and Hinnebusch, A.G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
45. van Steeg, H., Thomas, A., Verbeek, S., Kasperaitis, M., Voorma, H.O., and Benne, R. (1981) Shutoff of neuroblastoma cell protein synthesis by Semliki Forest virus: loss of ability of crude initiation factors to recognize early Semliki Forest virus and host mRNA's. J Virol 38: 728-736.
46. Strauss, J.H., and Strauss, E.G. (1994) The alphaviruses: gene expression, replication, and evolution. Microbiol Rev 58: 491-562.
47. Terenin, I.M., Dmitriev, S.E., Andreev, D.E., and Shatsky, I.N. (2008) Eukaryotic translation initiation machinery can operate in a bacterial-like mode without eIF2. Nat Struct Mol Biol 15: 836-841.
48. Ulmanen, I., Soderlund, H., and Kaariainen, L. (1976) Semliki Forest virus capsid protein associates with the 60S ribosomal subunit in infected cells. J Virol 20: 203-210.
49. Ventoso, I. (2012) Adaptive changes in Alphavirus mRNA translation allowed the colonization of vertebrate hosts. J Virol 86: 9484-9494.
50. Ventoso, I., Sanz, M.A., Molina, S., Berlanga, J.J., Carrasco, L., and Esteban, M. (2006) Translational resistance of late alphavirus mRNA to eIF2alpha phosphorylation: a strategy to overcome the antiviral effect of protein kinase PKR. Genes Dev 20: 87-100.
51. Walsh, D. (2010) Manipulation of the host translation initiation complex eIF4F by DNA viruses. Biochem Soc Trans 38: 1511-1516.
52. Welnowska, E., Castello, A., Moral, P., and Carrasco, L. (2009) Translation of mRNAs from vesicular stomatitis virus and vaccinia virus is differentially blocked in cells with depletion of eIF4GI and/or eIF4GII. J Mol Biol 394: 506-521.
53. Welnowska, E., Sanz, M.A., Redondo, N., and Carrasco, L. (2011) Translation of viral mRNA without active eIF2: the case of picornaviruses. PLoS ONE 6: e22230.
54. Yang, Y.L., Reis, L.F., Pavlovic, J., Aguzzi, A., Schafer, R., Kumar, A., etal. (1995) Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J 14: 6095-6106.