Identification in the ancient protist Giardia lamblia of two eukaryotic translation initiation factor 4E homologues with distinctive functions

Eukaryotic Cell

Volumn 4, Issue 5, 2005, Pages 948-959

  Li, Lei ^a   Wang, Ching C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPPED RNA; INITIATION FACTOR 4E; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; GENETIC COMPLEMENTATION; GENETICS; GIARDIA LAMBLIA; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYLOGENY; PHYSIOLOGY; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; EUKARYOTIC INITIATION FACTOR-4E; GENETIC COMPLEMENTATION TEST; GIARDIA LAMBLIA; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PROTEIN BIOSYNTHESIS; PROTOZOAN PROTEINS; RNA CAPS; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

EUKARYOTA; GIARDIA; GIARDIA INTESTINALIS; PROTISTA;

EID: 18944375265     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.4.5.948-959.2005     Document Type: Article

References (52)

1. Adam, R. D. 2001. Biology of Giardia lamblia. Clin. Microbiol. Rev. 14:447-475.
2. Adam. R. D. 2000. The Giardia lamblia genome. Int. J. Parasitol. 30:475-484.
3. Altmann, M., P. P. Muller, J. Pelletier, N. Sonenberg, and H. Trachsel. 1989. A mammalian translation initiation factor can substitute for its yeast homologue in vivo. J. Biol. Chem. 264:12145-12147.
4. Carberry, S. E., R. E. Rhoads, and D. J. Goss. 1989. A spectroscopic study of the binding of m7GTP and m7GpppG to human protein synthesis initiation factor 4E. Biochemistry 28:8078-8083.
5. Clauser, K. R., P. Baker, and A. L. Burlingame. 1999. Role of accurate mass measurement (±10 ppm) in protein identification strategies employing MS or MS/MS and database searching. Anal. Chem. 71:2871-2882.
6. Cougot, N., E. van Dijk, S. Babajko, and B. Seraphin. 2004. Cap-tabolism. Trends Biochem. Sci. 29:436-444.
7. Dan, M., A. L. Wang, and C. C. Wang. 2000. Inhibition of pyruvate-ferredoxin oxidoreductase gene expression in Giardia lamblia by a virus-mediated hammerhead ribozyme. Mol. Microbiol. 36:447-456.
8. Dan, M., and C. C. Wang. 2000. Role of alcohol dehydrogenase E (ADHE) in the energy metabolism of Giardia lamblia. Mol. Biochem. Parasitol. 109:25-36.
9. Dennis, P. P. 1997. Ancient ciphers: translation in Archaea. Cell 89:1007-1010.
10. Eliceiri, G. L. 1999. Small nucleolar RNAs. Cell. Mol. Life Sci. 56:22-31.
11. Furuichi, Y., and A. J. Shatkin. 2000. Viral and cellular mRNA capping: past and prospects. Adv. Virus Res. 55:135-184.
12. Ghosh, S., R. Ghosh, P. Das, and D. Chattopadhyay. 2001. Expression and purification of recombinant Giardia fibrillarin and its interaction with small nuclear RNAs. Protein Expr. Purif. 21:40-48.
13. Gingras, A. C., B. Raught, and N. Sonenberg. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68:913-963.
14. Hentze, M. W. 1997. eIF4G: a multipurpose ribosome adapter? Science 275:500-501.
15. Huber, J., U. Cronshagen, M. Kadokura, C. Marshallsay, T. Wada, M. Sekine, and R. Luhrmann. 1998. Snurportin1, an m3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J. 17:4114-4126.
16. Imataka, H., and N. Sonenberg. 1997. Human eukaryotic translation initiation factor 4G (eIF4G) possesses two separate and independent binding sites for eIF4A. Mol. Cell. Biol. 17:6940-6947.
17. Inagaki, Y., and W. F. Doolittle. 2000. Evolution of the eukaryotic translation termination system: origins of release factors. Mol. Biol. Evol. 17:882-889.
18. Jankowska-Anyszka, M., B. J. Lamphear, E. J. Aamodt, T. Harrington, E. Darzynkiewicz, R. Stolarski, and R. E. Rhoads. 1998. Multiple isoforms of eukaryotic protein synthesis initiation factor 4E in Caenorhabditis elegans can distinguish between mono- and trimethylated mRNA cap structures. J. Biol. Chem. 273:I0538-I0542.
19. Joshi, B., A. Cameron, and R. Jagus. 2004. Characterization of mammalian eIF4E-family members. Eur. J. Biochem. 271:2189-2203.
20. Keiper, B. D., W. Gan, and R. E. Rhoads. 1999. Protein synthesis initiation factor 4G. Int. J. Biochem. Cell Biol. 31:37-41.
21. Keiper, B. D., B. J. Lamphear, A. M. Deshpande, M. Jankowska-Anyszka, E. J. Aamodt, T. Blumenthal, and R. E. Rhoads. 2000. Functional characterization of five eIF4E isoforms in Caenorhabditis elegans. J. Biol. Chem. 275:10590-10596
22. Kozak, M. 1991. Effects of long 5′ leader sequences on initiation by eukaryotic ribosomes in vitro. Gene Expr. 1:117-125.
23. Kozak, M. 1991. A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes. Gene Expr. 1:111-115.
24. Lamphear, B. J., R. Kirchweger, T. Skern, and R. E. Rhoads. 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.
25. Lasko, P. 2000. The drosophila melanogaster genome: translation factors and RNA binding proteins. J. Cell Biol. 150:F51-F56.
26. Li, L., and C. C. Wang. 2004. Capped mRNA with a single nucleotide leader is optimally translated in a primitive eukaryote, Giardia lamblia. J. Biol. Chem. 279:14656-14664.
27. Marcotrigiano, J., A. C. Gingras, N. Sonenberg, and S. K. Burley. 1999. Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol. Cell 3:707-716.
28. Marcotrigiano, J., A. C. Gingras, N. Sonenberg, and S. K. Burley. 1997. Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDH. Cell 89:951-961.
29. Matsuo, H., H. Li, A. M. McGuire, C. M. Fletcher, A. C. Gingras, N. Sonenberg, and G. Wagner. 1997. Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat. Struct. Biol. 4:717-724.
30. McKendrick, L., V. M. Pain, and S. J. Morley. 1999. Translation initiation factor 4E. Int. J. Biochem. Cell Biol. 31:31-35.
31. Miyoshi, H., D. S. Dwyer, B. D. Keiper, M. Jankowska-Anyszka, E. Darzynkiewiecz, and R. E. Rhoads. 2002. Discrimination between mono- and trimethylated cap structures by two isoforms of Caenorhabditis elegans eIF4E. EMBO J. 21:4680-4690.
32. Morino, S., H. Hazama, M. Ozaki, Y. Teraoka, S. Shibata, M. Doi, H. Ueda, T. Ishida, and S. Uesugi. 1996. Analysis of the mRNA cap-binding ability of human eukaryotic initiation factor-4E by use of recombinant wild-type and mutant forms. Eur. J. Biochem. 239:597-601.
33. Munagala, N., and C. C. Wang. 2002. The pivotal role of guanine phosphoribosyltransferase in purine salvage by Giardia lamblia. Mol. Microbiol. 44:1073-1079.
34. Narcisi, E. M., C. V. Glover, and M. Fechheimer. 1998. Fibrillarin, a conserved pre-ribosomal RNA processing protein of Giardia. J. Eukaryot. Microbiol. 45:105-111.
35. Niu, X. H., T. Hartshorne, X. Y. He, and N. Agabian. 1994. Characterization of putative small nuclear RNAs from Giardia lamblia. Mol. Biochem. Parasitol. 66:49-57.
36. Nixon, J. E., A. Wang, H. G. Morrison, A. G. McArthur, M. L. Sogin, H. J. Loftus, and J. Samuelson. 2002. A spliceosomal intron in Giardia lamblia. Proc. Natl. Acad. Sci. USA 99:3701-3705.
37. Ochs, R. L., M. A. Lischwe, W. H. Spohn, and H. Busch. 1985. Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol. Cell 54:123-133.
38. Ptushkina, M., K. Berthelot, T. von der Haar, L. Geffers, J. Warwicker, and J. E. McCarthy. 2001. A second eIF4E protein in Schizosaccharomyces pombe has distinct eIF4G-binding properties. Nucleic Acids Res. 29:4561-4569.
39. Ptushkina, M., T. von der Haar, M. M. Karim, J. M. Hughes, and J. E. McCarthy. 1999. Repressor binding to a dorsal regulatory site traps human eIF4E in a high cap-affinity state. EMBO J. 18:4068-4075.
40. Reed, R. 2000. Mechanisms of fidelity in pre-mRNA splicing. Curr. Opin. Cell Biol. 12:340-345.
41. Ro-Choi, T. S. 1999. Nuclear snRNA and nuclear function (discovery of 5′ cap structures in RNA). Crit. Rev. Eukaryot. Gene Expr. 9:107-158.
42. Roger, A. J., S. G. Svard, J. Tovar, C. G. Clark, M. W. Smith, F. D. Gillin, and M. L. Sogin. 1998. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc. Natl. Acad. Sci. USA 95:229-234.
43. Rom, E., H. C. Kim, A. C. Gingras, J. Marcotrigiano, D. Kavre, H. Olsen, S. K. Burley, and N. Sonenberg. 1998. Cloning and characterization of 4EHP, a novel mammalian eIF4E-related cap-binding protein. J. Biol. Chem. 273:13104-13109.
44. Ruud, K. A., C. Kuhlow, D. J. Goss, and K. S. Browning. 1998. Identification and characterization of a novel cap-binding protein from Arabidopsis thaliana. J. Biol. Chem. 273:10325-10330.
45. Shuman, S. 2001. Structure, mechanism, and evolution of the mRNA capping apparatus. Prog. Nucleic Acid Res. Mol. Biol. 66:1-40.
46. Sogin, M. L., J. H. Gunderson, H. J. Elwood, R. A. Alonso, and D. A. Peattie. 1989. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243:75-77.
47. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
48. 7GpppA)-bound human full-length eukaryotic initiation factor 4E: biological importance of the C-terminal flexible region. Biochem. J. 362:539-544.
49. Vasilescu, S., M. Ptushkina, B. Linz, P. P. Muller, and J. E. McCarthy. 1996. Mutants of eukaryotic initiation factor eIF-4E with altered mRNA cap binding specificity reprogram mRNA selection by ribosomes in Saccharomyces cerevisiae. J. Biol. Chem. 271:7030-7037.
50. Wang, A. L., and C. C. Wang. 1986. Discovery of a specific double-stranded RNA virus in Giardia lamblia. Mol. Biochem. Parasitol. 21:269-276.
51. Wieczorek, Z., K. Zdanowski, L. Chlebicka, J. Stepinski, M. Jankowska, U. Kierdaszuk, A. Temeriusz, E. Darzynkiewicz, and R. Stolarski. 1997. Fluorescence and NMR studies of intramolecular stacking of mRNA cap-analogues. Biochim. Biophys. Acta 1354:145-152.
52. Yu, D. C., A. L. Wang, C. H. Wu, and C. C. Wang. 1995. Virus-mediated expression of firefly luciferase in the parasitic protozoan Giardia lamblia. Mol. Cell. Biol. 15:4867-4872.