Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F

EMBO Journal

Volumn 17, Issue 19, 1998, Pages 5811-5821

  Piron, Maria ^a   Vende, Patrice ^a   Cohen, Jean ^a   Poncet, Didier ^a  

^a Lab Virologie Immunol M   (France)

Author keywords

eIF4G; Poly(A) binding protein; RNA binding; Rotavirus; Translation regulation

Indexed keywords

INITIATION FACTOR; MESSENGER RNA; POLYADENYLIC ACID; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA LIBRARY; ESCHERICHIA COLI; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA TRANSLATION; ROTAVIRUS;

AMINO ACID SEQUENCE; EUKARYOTIC INITIATION FACTOR-4F; EUKARYOTIC INITIATION FACTOR-4G; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PEPTIDE FRAGMENTS; PEPTIDE INITIATION FACTORS; POLY(A)-BINDING PROTEINS; PROTEIN BINDING; RNA-BINDING PROTEINS; ROTAVIRUS; VIRAL NONSTRUCTURAL PROTEINS;

ANIMALIA; ESCHERICHIA COLI; EUKARYOTA; ROTAVIRUS;

EID: 0032190508     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.19.5811     Document Type: Article

References (65)

1. Aponte, C., Mattion, N.M., Estes, M.K., Charpilienne, A. and Cohen, J. (1993) Expression of two bovine rotavirus non-structural proteins (NSP2, NSP3) in the baculovirus system and production of monoclonal antibodies directed against the expressed proteins. Arch. Virol., 133, 85-95.
2. Aponte, C., Poncet, D. and Cohen, J. (1996) Recovery and characterization of a replicase complex in rotavirus-infected cells using a monoclonal antibody against NSP2. J. Virol., 70, 985-991.
3. Bartel, P.L. and Fields, S. (1995) Analyzing protein-protein interactions using two-hybrid system. Methods Enzymol., 254, 241-263.
4. Bartel, P., Chien, C.T., Sternglanz, R. and Fields, S. (1993) Elimination of false positives that arise in using the two-hybrid system. Biotechniques, 14, 920-924.
5. Beelman, C.A. and Parker, R. (1995) Degradation of mRNA in eukaryotes. Cell, 81, 179-183.
6. Caponigro, G. and Parker, R. (1996) Mechanisms and control of mRNA turnover in Saccharomyces cerevisiae. Microbiol. Rev., 60, 233-249.
7. Craig, A.W., Haghighat, A., Yu, A.T. and Sonenberg, N. (1998) Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature, 392, 520-523.
8. Ehrenfeld, E. (1996) Initiation of translation by Picornavirus RNAs. In Hershey, J.W.B., Mathews, M.B. and Sonenberg, N. (eds), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 549-573.
9. Estes, M.K. (1990) Rotaviruses and their replication. In Fields, B. and Knipe, D.M. (eds), Virology. Raven Press, New York, NY, pp. 1324-1352.
10. Estojak, J., Brent, R. and Golemis, E.A. (1995) Correlation of two-hybrid affinity data with in vitro measurements. Mol. Cell. Biol., 15, 5820-5829.
11. Fields, S. and Song, O. (1989) A novel genetic system to detect protein-protein interactions. Nature, 340, 245-246.
12. Ford, L.P., Bagaa, P.S. and Wilusz, J. (1997) The poly(A) tail inhibits the assembly of a 3′-to-5′ exonuclease in an in vitro RNA stability system. Mol. Cell. Biol., 17, 398-406.
13. Fuentes, A., Blackball, J. and Magnusson, G. (1997) Mechanism of rotavirus inhibition of host cell protein synthesis. Sixth International Symposium on Double Stranded RNA viruses, Cocoyoc, Mexico.
14. Gallie, D.R. and Traugh, J.A. (1994) Serum and insulin regulate cap function in 3T3-L1 cells. J. Biol. Chem., 269, 7174-7179.
15. Gallie, D.R. Lewis, N.J. and Marzluff, W.F. (1996) The histone 3′-terminal stem-loop is necessary for translation in Chinese hamster ovary cells. Nucleic Acids Res., 24, 1954-1962.
16. Görlach, M., Burd, C.G. and Dreyfuss, G. (1994) The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp. Cell Res., 211, 400-407.
17. Goyer, C., Altmann, M., Lee, H.S., Blanc, A., Deshmukh, M., Woolford, J.L., Jr, Trachsel, H. and Sonenberg, N. (1993) TIF4631 and TIF4632: two yeast genes encoding the high-molecular-weight subunits of the cap-binding protein complex (eukaryotic initiation factor 4F) contain an RNA recognition motif-like sequence and carry out an essential function. Mol. Cell. Biol., 13, 4860-4874.
18. Gradi, A., Imataka, H., Svitkin, Y.V., Rom, E., Raught, B., Morino, S. and Sonenberg, N. (1998) A novel functional human eukaryotic translation initiation factor 4G. Mol. Cell. Biol., 18, 334-342.
19. Hardwick, J.M. and Griffin, D.E. (1997) Viral effects on cellular functions. In Neal Nathanson, E.A. (ed.), Viral Pathogenesis. Lippincott-Raven Publishers, Philadelphia, PA, pp. 55-82.
20. Hua, J., Chen, X. and Patton, J.T. (1994) Deletion mapping of the rotavirus metalloprotein NS53 (NSP1): the conserved cysteine-rich region is essential for virus-specific RNA binding. J. Virol., 68, 3990-4000.
21. Ikeshima-Kataoka, H., Skeath, J.B., Nabeshima, Y., Doe, C.Q. and Matsuzaki, F. (1997) Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature, 390, 625-629.
22. Imai, M., Akatani, K., Ikegami, N. and Furuichi, Y. (1983) Capped add conserved terminal structures in human rotavirus genome double-stranded RNA segments. J. Virol., 47, 125-136.
23. Imataka, H. and Sonenberg, N. (1997) Human eukaryotic translation initiation factor 4G (eIF4G) possesses two separate and independent binding sites for eIF4A. Mol. Cell. Biol., 17, 6940-6947.
24. Imataka, H., Olsen, H.S. and Sonenberg, N. (1997) A new translational reaulator with homology to eukaryotic translation initiation factor 4G. EMBO J., 16, 817-825.
25. Jacobson, A. (1996) Poly(A) metabolism and translation: the closed-loop model In Hershey, J.W.B., Mathews, M.B. and Sonenberg, N. (eds), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 451-180.
26. Jacobson, A. and Peltz, S.W. (1996) Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem., 65, 693-739.
27. Katze, M.G. (1996) Translational control in cells infected with influenza virus and reovirus. In Hershey, J.W.B., Mathews, M.B. and Sonenberg, N. (eds), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 607-630.
28. Kessler, S.H. and Sachs, A.B. (1998) RNA recognition motif 2 of yeast Pab1p is required for its functional interaction with eukaryotic translation initiation factor 4G. Mol. Cell. Biol., 18, 51-57.
29. Kunkel, T.A., Bebenek, K. and McClary, J. (1991) Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol., 204, 125-139.
30. Lamphear, B.J., Kirchweger, R., Skem, T. and Rhoads, R.E. (1995) Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. J. Biol. Chem., 270, 21975-21983.
31. Le, H., Tanguay, R.L., Balasta, M.L., Wei, C.C., Browning, K.S., Metz, A.M., Goss, D.J. and Gallie, D.R. (1997) Translation initiation factors eIF-iso4G and eIF-4B interact with the poly(A)-binding protein and increase its RNA binding activity. J. Biol. Chem., 272, 16247-16255.
32. Lemay, G. (1988) Transcriptional and translational events during reovirus infection. Biochem. Cell. Biol., 66, 803-812.
33. Lemieux, R., Zarbl, H. and Millward, S. (1984) mRNA discrimination in extracts from uninfected and reovirus-infected L-cells. J. Virol., 51, 215-222.
34. Lindenbaum, M. (1998) Clone It: finding cloning strategies, in-frame deletions and frameshifts. Bioinformatics, in press.
35. Mader, S., Lee, H., Pause, A. and Sonenberg, N. (1995) The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol. Cell. Biol., 15, 4990-4997.
36. Martin, F., Schaller, A., Eglite, S., Schumperli, D. and Muller, B. (1997) The gene for histone RNA hairpin binding protein is located on human chromosome 4 and encodes a novel type of RNA binding protein. EMBO J., 16, 769-778.
37. Mathews, M.B. (1996) Interactions between viruses and the cellular machinery for protein synthesis. In Hershey, J.W.B., Mathews, M.B. and Sonenberg, N. (eds), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 505-548.
38. Mattion, N.M., Cohen, J. and Estes, M.K. (1994) Rotavirus proteins. In Kapikian, A. (ed.), Viral Infections of the Gastrointestinal Tract. Marcel Dekker, Inc., New York, NY. pp. 169-249.
39. Munroe, D. and Jacobson, A. (1990) mRNA poly(A) tail, a 3′ enhancer of translational initiation. Mol. Cell. Biol., 10, 3441-3455.
40. Ohlmann, T., Pain, V.M., Wood, W., Rau, M. and Morley, S.J. (1997) The proteolytic cleavage of eukaryotic initiation factor (eIF) 4G is prevented by eIF4E binding protein (PHAS-I; 4E-BP1) in the reticulocyte lysate. EMBO J., 16, 844-855.
41. Pestova, T.V., Shatsky, I.N. and Hellen, C.U. (1996) Functional dissection of eukaryotic initiation factor 4F: the 4A subunit and the central domain of the 4G subunit are sufficient to mediate internal entry of 43S preinitiation complexes. Mol. Cell. Biol. 16, 6870-6878.
42. Petrie, B.L., Greenberg, H.B., Graham, D.Y. and Estes, M.K. (1984) Ultrastructural localization of rotavirus antigens using colloidal gold. Virus Res., 1, 133-152.
43. Piron, M. and Poncet, D. (1997) RNA binding and dimenzation domain of rotavirus NSP3. Sixth International Symposium on Double Stranded RNA Viruses, Cocoyoc, Mexico.
44. Poncet, D., Aponte, C. and Cohen, J. (1993) Rotavirus protein NSP3 (NS34) is bound to the 3′ end consensus sequence of viral mRNAs in infected cells. J. Virol., 67, 3159-3165.
45. Poncet, D., Laurent, S. and Cohen, J. (1994) Four nucleotides are the minimal requirement for RNA recognition by rotavirus non-structural protein NSP3. EMBO J., 13, 4165-4173.
46. Poncet, D., Lindenbaum, P., L'Haridon, R. and Cohen, J. (1997) In vivo and in vitro phosphorylation of rotavirus NSP5 correlates with its localization in viroplasms. J. Virol., 71, 34-41.
47. Preiss, T. and Hentze, M.W. (1998) Dual function of the messenger RNA cap structure in poly(A)-tail-promoted translation in yeast. Nature, 392, 516-520.
48. Qian, Y., Jiang, B., Saif, J.L., Kang, S., Ojeh, C. and Green, K. (1991) Molecular analysis of the gene 6 from a porcine group C rotavirus that encodes the NS34 equivalent of group A rotavirus. Virology, 184, 752-757.
49. Richter, J.D. (1996) Dynamics of poly(A) addition and removal during development. In Hershey, J.W.B., Mathews, M.B. and Sonenberg, N. (eds), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 481-503.
50. Ross, A.F., Oleynikov, Y., Kislauskis, E.H., Taneja, K.L. and Singer, R.H. (1997) Characterization of a beta-actin mRNA zipcode-binding protein. Mol. Cell. Biol., 17, 2158-2165.
51. Schneider, R.J. (1996) Adenovirus and vaccinia virus translational control. In Hershey, J.W.B., Mathews, M.B. and Sonenberg, N. (eds), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 575-605.
52. Sen Gupta, D.J., Zhang, B.L., Kraemer, B., Pochart, P., Fields, S. and Wickens, M. (1996) A three-hybrid system to detect RNA-protein interactions in vivo. Proc. Natl Acad. Sci. USA, 93, 8496-8501.
53. Shama, S., Avni, D., Frederickson, R.M., Sonenberg, N. and Meyuhas, O. (1995) Overexpression of initiation factor eIF-4E does not relieve the translational repression of ribosomal protein mRNAs in quiescent cells. Gene Expression 4, 241-252.
54. Singer, R.H. (1996) RNA: traffic report. Trends Cell. Biol., 6, 486-489.
55. Skup, D. and Millward, S. (1980) Reovirus-induced modification of cap-dependent translation in infected L cells. Proc. Natl Acad. Sci. USA, 77, 152-156.
56. Studier, F.W. (1991) Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J. Mol. Biol., 219, 37-44.
57. Tanguay, R.L. and Gallie, D.R. (1996) Translational efficiency is regulated by the length of the 3′ untranslated region. Mol. Cell. Biol., 16, 146-156.
58. Tarun, S.Z. and Sachs, A.B. (1995) A common function for mRNA 5′ and 3′ ends in translation initiation in yeast. Genes Dev., 9, 2997-3007.
59. Tarun, S.Z., Jr and Sachs, A.B. (1996) Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J., 15, 7168-7177.
60. Tarun, S.Z., Jr, Wells, S.E., Deardorff, J.A. and Sachs, A.B. (1997) Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc. Natl Acad. Sci. USA, 94, 9046-9051.
61. Wang, Z.F., Whitfield, M.L., Ingledue, T.C.R., Dominski, Z. and Marzluff, W.F. (1996) The protein that binds the 3′ end of histone mRNA: a novel RNA-binding protein required for histone pre-mRNA processing. Genes Dev., 10, 3028-3040.
62. Wei, C.C., Balasta, M.L., Ren, J. and Goss, D.J. (1998) Wheat germ poly(A) binding protein enhances the binding affinity of eukaryotic initiation factor 4F and (iso)4F for cap analogues. Biochemistry, 37, 1910-1916.
63. Wickner, R.B. (1996) Double-stranded RNA viruses of Saccharomyces cerevisiae. Microbiol. Rev., 60, 250-265.
64. Yan, R., Rychlik, W., Etchison, D. and Rhoads, R.E. (1992) Amino acid sequence of the human protein synthesis initiation factor eIF-4 gamma. J. Biol. Chem., 267, 23226-23231.
65. Zelus, B.D., Stewart, R.S. and Ross, J. (1996) The virion host shutoff protein of herpes simplex virus type 1: messenger ribonucleolytic activity in vitro. J. Virol. 70, 2411-2419.