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Novel Cytoplasmic Cap Binding Proteins in Yeast

  • Nahum Sonenberg
  • Antony Blanc
  • Charles Goyer
Conference paper
Part of the NATO ASI Series book series (volume 71)

Abstract

The 5′ terminal cap structure, m7GpppX (where X is any nucleotide), is a ubiquitous feature of eukaryotic mRNAs that plays an important role in the cytoplasm and the nucleus. In the cytoplasm the cap structure enhances translational efficiency (Shatkin, 1985). In the nucleus, in vitro studies have demonstrated that the efficiency of mRNA splicing (Konarska et al, 1984;Edery and Sonenberg,1985), and 3′ end processing (Georgiev et al, 1984;Hart et al, 1985) is enhanced by the presence of a cap structure. Furthermore, the cap protects the mRNA against 5′ exonucleolytic degradation in both the nucleus and the cytoplasm (Furuichi et al,1977;Green et al, 1983) and is implicated in nucleocytoplasmic transport (Hamm and Mataj, 1990). Consistent with the role of the cap in nuclear events, recent data demonstrate that a significant portion of the cap binding protein (eIF-4E) is localized to the nucleus (Lejbkowicz et al,1992).

Keywords

Coat Protein Gene Disruption Covalent Bond Formation HeLa Nuclear Extract Protein Synthesis Initiation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Altmann M, Edery I, Sonenberg N, Trachsel H (1985). Purification and characterization of protein initiation factor eIF-4E from the yeast Saccharomyces cerevislae. Biochemistry 24: 6085–6089.PubMedCrossRefGoogle Scholar
  2. Altmann M, Handschin C, Trachsel H (1987). mRNA cap-binding protein:cloning of the gene encoding protein synthesis initiation factor eIF-4E from Saccharomyces cerevislae. Mol Cell Biol 7: 998–1003.PubMedGoogle Scholar
  3. Bandziulis RJ, Swanson MS, Dreyfuss G (1989). RNA-binding proteinsas developmental regulators. Genes & Dev 3: 431–437.CrossRefGoogle Scholar
  4. Blanc A, Goyer C, Sonenberg N (1992). The coat protein of the yeast double-stranded RNA virus L-A attaches covalently to the cap structure of eukaryotic mRNA. Mol Cell Biol 12: 3390–3398.PubMedGoogle Scholar
  5. Bruenn J, Keitz B (1976). The 5′ ends of yeast killer factor RNAs are pppGp. Nuc Acids Res 3: 2427–2436.Google Scholar
  6. Bruenn JA (1980). Virus-like particles of yeast. Annu Rev Microbiol 34: 49–68.PubMedCrossRefGoogle Scholar
  7. Courey AJ, Tjian R (1988). Analysis of Spl in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell 55: 887–898.PubMedCrossRefGoogle Scholar
  8. Edery I, Hümbelin M, Darveau A, Lee KAW, Milburn S, Hershey JWB, Trachsel H, Sonenberg N (1983). Involvement of eukaryotic initiation factor 4A in the cap recognition process. J Biol Chem 258: 11398–11403.PubMedGoogle Scholar
  9. Edery I, Sonenberg N (1985). Cap-dependent RNA splicing in a HeLa nuclear extract. Proc Natl Acad Sci USA 82: 7590–7594.PubMedCrossRefGoogle Scholar
  10. Edery I, Altmann M, Sonenberg N (1988). High level synthesis in Escherichla coll of functional eukaryotic initiation factor eIP-4E and affinity purification using a simplified cap-analog resin. Gene (Amst) 74: 517–525.CrossRefGoogle Scholar
  11. El-Sheirbeini M, Tipper DJ, Mitchell DJ, Bostian KA (1984). Virus-like particle capsid proteins encoded by different L double-stranded RNAs of Saccharomyces cerevlslae: their roles in maintenance of M double-stranded killer plasmids. Mol Cell Biol 4: 2818–2827.Google Scholar
  12. Etchison D, Hansen J, Ehrenfeld E, Edery I, Sonenberg N, Milburn SC, Hershey JWB (1984). Demonstration in vitro that eucaryotic initiation factor 3 is active but that a cap-binding protein complex is inactive in poliovirus infected HeLa cells. J Virol 51: 832–837.PubMedGoogle Scholar
  13. Furuichi Y, LaFiandra A, Shatkin AJ (1977). 5′ terminal structure and mRNA stability. Nature (London) 266: 235–239.CrossRefGoogle Scholar
  14. Georgiev O, Mous J, Birnsteil M (1984). Processing and nucleo-cytoplasmic transport of histone gene transcripts. Nucl Acids Res 12: 8539–8551.PubMedCrossRefGoogle Scholar
  15. Goyer C, Altmann M, Trachsel H, Sonenberg N (1989). Identification and characterization of cap-binding proteins from yeast. J Biol Chem 264: 7603–7610.PubMedGoogle Scholar
  16. Green MR, Maniatis T, Melton DA (1983). Human β-globin pre-mRNA synthesized in vitro is accurately spliced in Xenopus oocyte nuclei. Cell 32: 681–694.PubMedCrossRefGoogle Scholar
  17. Grifo JA, Tahara SM, Morgan MA, Shatkin AJ, Merrick WC (1983). New initiation factor activity required for globin mRNA translation. J Biol Chem 258: 5804–5810.PubMedGoogle Scholar
  18. Hamm J, Mattaj IW (1990). Monomethylated cap structures facilitate RNA export from the nucleus. Cell 63: 109–118.PubMedCrossRefGoogle Scholar
  19. Hart RP, McDevitt MA, Nevins JR (1985). Poly(A) site cleavage in HeLa nuclear extract is dependent on downstream sequences. Cell 43: 677–683.PubMedCrossRefGoogle Scholar
  20. Haynes SR (1992). The RNP motif protein family. New Biol 4: 421–429.PubMedGoogle Scholar
  21. Hershey JWB (1991) Translational control in mammalian cells. Ann Rev Biochem 60: 717–755.PubMedCrossRefGoogle Scholar
  22. Hoffman DW, Query CC, Golden BL, White SW, Keene JD (1991). RNA-binding domain of the A protein component of the Ul small nuclear ribonucleoprotein analyzed by NMR spectroscopy is structurally similar to ribosomal protein. Proc Natl Acad Sci 88: 2495–2499.PubMedCrossRefGoogle Scholar
  23. Jaramillo M, Pelletier J, Edery I, Nielsen PJ, Sonenberg N (1991). Multiple mRNAs encode the murine translation initiation factor elF-4E. J Biol Chem 266: 10446–10451.PubMedGoogle Scholar
  24. Keene JD, Query CC (1991). Nuclear RNA-binding proteins. Prog Nucl Acid Res Mol Biol 41: 179–201.CrossRefGoogle Scholar
  25. Kenan DJ, Query CC, Keene JD (1991). RNA recognition: towards identifying determinants of specificity. Trends Bioch Sci 16: 214–220.CrossRefGoogle Scholar
  26. Konarska MM, Padgett RA, Sharp PA (1984). Recognition of the cap structure in splicing in vitro of mRNA precursors. Cell 38: 731–736.PubMedCrossRefGoogle Scholar
  27. Lanker S, Mueller PP, Altmann M, Goyer C, Sonenberg N, Trachsel H (1992). Interaction of the eIF-4F subunits in the yeast Saccharomyces cerevlslae. J Biol Chem 267: 21167–21171.PubMedGoogle Scholar
  28. Lee KAW, Edery I, Sonenberg N (1985). Isolation and structural characterization of cap-binding proteins from poliovirus-infected HeLa cells. J Virol 54: 515–524.PubMedGoogle Scholar
  29. Lejbkowicz F, Goyer C, Darveau A, Neron S, Lemieux R, Sonenberg N (1992). A fraction of the mRNA 5′ cap binding protein, eIF-4E, localizes to the nucleus. Proc Natl Acad Sci 89: 9612–9616.PubMedCrossRefGoogle Scholar
  30. Mattaj IW (1989). A binding consensus: RNA-binding-protein interactions in splicing, snRNPs, and sex. Cell 57: 1–3.PubMedCrossRefGoogle Scholar
  31. Mermod M, O’Neill EA, Kelly TJ, Tjian R (1989). The proline-rich transcriptional activator of CTF/NF-I is distinct from the replication and DNA binding domain. Cell 58: 741–753.PubMedCrossRefGoogle Scholar
  32. Nemeroff M, Bruenn J (1987). Initiation by the yeast viral transcriptase in vitro. J Biol Chem 262: 6785–6787.PubMedGoogle Scholar
  33. Olmsted JB (1981). Affinity purification of antibodies from diazotized paper blots of heterogeneous protein samples. J Biol Chem 256: 11955–11957.PubMedGoogle Scholar
  34. Pelletier J, Sonenberg N (1985). Photochemical cross-linking of capbinding proteins to eukaryotic mRNAs: Effect of mRNA 5′ secondary structure. Mol Cell Biol 5: 3222–3230.PubMedGoogle Scholar
  35. Ray BK, Brendler TG, Adhya A, Daniel-McQueen S, Kelvin-Miller J, Hershey JWB, Grifo JA, Merrick WC, Thach RE (1983). Role of mRNA competition in regulating translation:further characterization of mRNA discriminatory initiation factors. Proc Natl Acad Sci USA. 80: 663–667.PubMedCrossRefGoogle Scholar
  36. Rhee SK, Icho T, Wickner RB (1989). Structure and nuclear localization signal of the SK13 antiviral protein of Saccharomyces cerevlslae. Yeast 5: 149–158.PubMedCrossRefGoogle Scholar
  37. Rhoads RE (1988). Cap recognition and entry of mRNA into the protein synthesis initiation cycle. Trends Biochem Sci 13: 52–56.PubMedCrossRefGoogle Scholar
  38. Ridley SP, Sommer SS, Wickner RB (1984). Superkiller mutations in Saccharomyces cerevlslae suppress exclusion of M2 double-stranded RNA by L-A-NH and confer cold sensitivity in the presence of M and L-A-NH. Mol Cell Biol 4: 761–770.PubMedGoogle Scholar
  39. Rychlik W, Domier LL, Gardner PR, Hellmann GM, Rhoads RE (1987). Amino acid sequence of the mRNA cap-binding protein from human tissues. Proc Natl Acid Sci USA 84: 945–949.CrossRefGoogle Scholar
  40. Safer B (1989). Nomenclature of initiation, elongation and termination factors for translation in eucaryotes. Recommendations 1988. Eur J Biochem 186: 3384–3386.Google Scholar
  41. Sarkar G, Edery I, Gallo R, Sonenberg N (1984). Preferential stimulation of rabbit α globin mRNA translation by a cap binding protein complex. Biochem Biophys Acta 783: 122–129.PubMedGoogle Scholar
  42. Shatkin AJ (1985). mRNA cap binding proteins:essential factors for initiating translation. Cell 40: 223–224.PubMedCrossRefGoogle Scholar
  43. Sommer S, Wickner RB (1982). Yeast L dsRNA consists of at least three distinct RNAs;evidence that the non-mendelian genes [HOK], [NEX], and [EXL] are on one of these RNAs. Cell 31: 429–441.PubMedCrossRefGoogle Scholar
  44. Sommer S, Wickner RB (1987). Gene disruption indicates that the only essential function of the SK18 chromosomal gene is to protect Saccharomyces cerevlslae from viral cytopathology. Virology 157: 252–256.PubMedCrossRefGoogle Scholar
  45. Sonenberg N, Morgan MA, Merrick WC, Shatkin AJ (1978). A polypeptide in eukaryotic initiation factors that cross-links specifically to the 5′-terminal cap in mRNA. Proc Natl Acad Sci USA 74: 4288–4292.CrossRefGoogle Scholar
  46. Sonenberg N (1987). Translation control by poliovirus. In “Advances in virus research”. Academic Press (ed:K. Maramorosch). 33: 175–204.Google Scholar
  47. Sonenberg N (1988). Cap-binding proteins of eukaryotic messenger RNA: Functions in initiation of translation. Prog Nucl Acid Res Mol Biol 35: 173–207.CrossRefGoogle Scholar
  48. Tahara SM, Morgan MA, Shatkin AJ (1981). Two forms of m7G-cap binding protein with different effects on capped mRNA translation in extracts of uninfected and poliovirus-infected HeLa cells. J Biol Chem 256: 7691–7694.PubMedGoogle Scholar
  49. Tobin GJ, Young DC, Flanegan JB (1989). Self-catalyzed linkage of poliovirus terminal protein VPg to poliovirus RNA. Cell 59: 511–519.PubMedCrossRefGoogle Scholar
  50. Wickner RB (1992). Double-stranded and single-stranded RNA viruses of Saccharomyces cerevlslae. Annu Rev Microbiol 46: 347–375.PubMedCrossRefGoogle Scholar
  51. Zamore PD, Patton JG, Green MR (1990). Cloning and domain structure of the mammalian splicing factor U2AF. Nature 355: 609–614.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1993

Authors and Affiliations

  • Nahum Sonenberg
    • 1
  • Antony Blanc
    • 1
  • Charles Goyer
    • 1
  1. 1.Department of BiochemistryMcGill UniversityMontrealCanada

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