Translation initiation in Leishmania major: Characterisation of multiple eIF4F subunit homologues

Molecular and Biochemical Parasitology

Volumn 140, Issue 1, 2005, Pages 23-41

  Dhalia, Rafael ^a,e   Reis, Christian R S ^b,e   Freire, Eden R ^b,e   Rocha, Pollyanna O ^b,e   Katz, Rodolfo ^b,e   Muniz, João R C ^c   Standart, Nancy ^d   De Melo Neto, Osvaldo P ^e  

^a UNIVERSITY OF BRASILIA   (Brazil)

^b FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

eIF4F; Leishmania major; Protein protein interaction; Translation initiation

Indexed keywords

7 METHYLGUANINE; CAP BINDING PROTEIN; INITIATION FACTOR 4F; PROTEIN SUBUNIT; SEPHAROSE;

ANTIBODY SPECIFICITY; ARTICLE; LEISHMANIA MAJOR; LIFE CYCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; STRUCTURAL HOMOLOGY; TRANSLATION INITIATION; WESTERN BLOTTING;

EUKARYOTA; LEISHMANIA MAJOR; PROTOZOA; TRYPANOSOMATIDAE;

EID: 13444273016     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2004.12.001     Document Type: Article

References (79)

1. M.L. Muhich, and J.C. Boothroyd Polycistronic transcripts in trypanosomes and their accumulation during heat shock: evidence for a precursor role in mRNA synthesis Mol Cell Biol 8 1988 3837 3846
2. E. Ullu, and C. Tschudi Trans splicing in trypanosomes requires methylation of the 5′ end of the spliced leader RNA Proc Natl Acad Sci USA 88 1991 10074 10078
3. D.A. Campbell, S. Thomas, and N.R. Sturm Transcription in kinetoplastid protozoa: why be normal? Microbes Infect 5 2003 1231 1240
4. X.H. Liang, A. Haritan, S. Uliel, and S. Michaeli Trans and cis splicing in trypanosomatids: mechanism, factors, and regulation Eukaryot Cell 2 2003 830 840
5. C.E. Clayton Life without transcriptional control? From fly to man and back again EMBO J 21 2002 1881 1888
6. J.D. Bangs, P.F. Crain, T. Hashizume, J.A. McCloskey, and J.C. Boothroyd Mass spectrometry of mRNA cap 4 from trypanosomatids reveals two novel nucleosides J Biol Chem 267 1992 9805 9815
7. T.W. Nilsen Trans-splicing: an update Mol Biochem Parasitol 73 1995 1 6
8. E. Pascolo, C. Blonski, D. Shire, and J.J. Toulme Antisense effect of oligodeoxynucleotides complementary to the mini-exon sequence of the protozoan parasite Leishmania amazonensis Biochimie 75 1993 43 47
9. C. Ramazeilles, R.K. Mishra, S. Moreau, E. Pascolo, and J.J. Toulme Antisense phosphorothioate oligonucleotides: selective killing of the intracellular parasite Leishmania amazonensis Proc Natl Acad Sci USA 91 1994 7859 7863
10. P.A. Maroney, J.A. Denker, E. Darzynkiewicz, R. Laneve, and T.W. Nilsen Most mRNAs in the nematode Ascaris lumbricoides are trans-spliced: a role for spliced leader addition in translational efficiency RNA 1 1995 714 723
11. G.M. Zeiner, N.R. Sturm, and D.A. Campbell The Leishmania tarentolae spliced leader contains determinants for association with polysomes J Biol Chem 278 2003 38269 38275
12. A.C. Gingras, B. Raught, and N. Sonenberg eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation Annu Rev Biochem 68 1999 913 963
13. J.W.B. Hershey, and W.C. Merrick Pathway and mechanism of initiation of protein synthesis N. Sonenberg Translational control of gene expression 2000 Cold Spring Harbor Laboratory Press New York 33 88
14. T.V. Pestova, V.G. Kolupaeva, and I.B. Lomakin Molecular mechanisms of translation initiation in eukaryotes Proc Natl Acad Sci USA 98 2001 7029 7036
15. N. Sonenberg, and T.E. Dever Eukaryotic translation initiation factors and regulators Curr Opin Struct Biol 13 2003 56 63
16. N. Sonenberg, and A.C. Gingras The mRNA 5′ cap-binding protein eIF4E and control of cell growth Curr Opin Cell Biol 10 1998 268 275
17. B. Raught, and A.C. Gingras eIF4E activity is regulated at multiple levels Int J Biochem Cell Biol 31 1999 43 57
18. G.C. Scheper, and C.G. Proud Does phosphorylation of the cap-binding protein eIF4E play a role in translation initiation? Eur J Biochem 269 2002 5350 5359
19. A. Luking, U. Stahl, and U. Schmidt The protein family of RNA helicases Crit Rev Biochem Mol Biol 33 1998 259 296
20. P. Linder Yeast RNA helicases of the DEAD-box family involved in translation initiation Biol Cell 95 2003 157 167
21. S. Rocak, and P. Linder DEAD-box proteins: the driving forces behind RNA metabolism Nat Rev Mol Cell Biol 5 2004 232 241
22. D. Prevot, J.L. Darlix, and T. Ohlmann Conducting the initiation of protein synthesis: the role of eIF4G Biol Cell 95 2003 141 156
23. S. Mader, H. Lee, A. Pause, and N. Sonenberg 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 1995 4990 4997
24. S.Z. Tarun Jr., and A.B. Sachs Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G EMBO J 15 1996 7168 7177
25. H. Imataka, A. Gradi, and N. Sonenberg A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation EMBO J 17 1998 7480 7489
26. J. Marcotrigiano, I.B. Lomakin, N. Sonenberg, T.V. Pestova, C.U. Hellen, and S.K. Burley A conserved HEAT domain within eIF4G directs assembly of the translation initiation machinery Mol Cell 7 2001 193 203
27. N.L. Korneeva, B.J. Lamphear, F.L. Hennigan, and R.E. Rhoads Mutually cooperative binding of eukaryotic translation initiation factor (eIF) 3 and eIF4A to human eIF4G-1 J Biol Chem 275 2000 41369 41376
28. I.B. Lomakin, C.U. Hellen, and T.V. Pestova Physical association of eukaryotic initiation factor 4G (eIF4G) with eIF4A strongly enhances binding of eIF4G to the internal ribosomal entry site of encephalomyocarditis virus and is required for internal initiation of translation Mol Cell Biol 20 2000 6019 6029
29. H. Imataka, and N. Sonenberg Human eukaryotic translation initiation factor 4G (eIF4G) possesses two separate and independent binding sites for eIF4A Mol Cell Biol 17 1997 6940 6947
30. S. Morino, H. Imataka, Y.V. Svitkin, T.V. Pestova, and N. Sonenberg Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region Mol Cell Biol 20 2000 468 477
31. S. Pyronnet, H. Imataka, A.C. Gingras, R. Fukunaga, T. Hunter, and N. Sonenberg Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E EMBO J 18 1999 270 279
32. Y. Nakamura, T. Hashimoto, and T. Kamaishi Phylogenetic position of kinetoplastid protozoa inferred from the protein phylogenies of elongation factors 1alpha and 2 J Biochem (Tokyo) 119 1996 70 79
33. J.A. Batista, S.M. Teixeira, J.E. Donelson, L.V. Kirchhoff, and C.M. de Sa Characterization of a Trypanosoma cruzi poly(A)-binding protein and its genes Mol Biochem Parasitol 67 1994 301 312
34. T.L. Hotchkiss, G.E. Nerantzakis, S.C. Dills, L. Shang, and L.K. Read Trypanosoma brucei poly(A) binding protein I cDNA cloning, expression, and binding to 5′ untranslated region sequence elements Mol Biochem Parasitol 98 1999 117 129
35. E.J. Bates, E. Knuepfer, and D.F. Smith Poly(A)-binding protein I of Leishmania: functional analysis and localisation in trypanosomatid parasites Nucl Acids Res 28 2000 1211 1220
36. Y.A. Skeiky, M. Kennedy, and D. Kaufman LeIF: a recombinant Leishmania protein that induces an IL-12-mediated Th1 cytokine profile J Immunol 161 1998 6171 6179
37. Y.A. Skeiky, J.A. Guderian, and D.R. Benson A recombinant Leishmania antigen that stimulates human peripheral blood mononuclear cells to express a Th1-type cytokine profile and to produce interleukin 12 J Exp Med 181 1995 1527 1537
38. S. Kumar, K. Tamura, I.B. Jakobsen, and M. Nei MEGA2: molecular evolutionary genetics analysis software Bioinformatics 17 2001 1244 1245
39. N. Saitou, and M. Nei The neighbor-joining method: a new method for reconstructing phylogenetic trees Mol Biol Evol 4 1987 406 425
40. D.T. Jones GenTHREADER: an efficient and reliable protein fold recognition method for genomic sequences J Mol Biol 287 1999 797 815
41. J. Marcotrigiano, A.C. Gingras, N. Sonenberg, and S.K. Burley Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP Cell 89 1997 951 961
42. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J Mol Biol 234 1993 779 815
43. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton Procheck: a program to check the stereochemical quality of protein structures J Appl Crystallogr 26 1993 283 291
44. R. Luthy, J.U. Bowie, and D. Eisenberg Assessment of protein models with three-dimensional profiles Nature 356 1992 83 85
45. G. Vriend WHATIF: a molecular modelling and drug design program J Mol Graph 8 1990 52 56
46. O.P. de Melo Neto, N. Standart, and C.M. de Sa Autoregulation of poly(A)-binding protein synthesis in vitro Nucl Acids Res 23 1995 2198 2205
47. N. Minshall, G. Thom, and N. Standart A conserved role of a DEAD box helicase in mRNA masking RNA 7 2001 1728 1742
48. T.V. Pestova, C.U. Hellen, and I.N. Shatsky Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry Mol Cell Biol 16 1996 6859 6869
49. E.O. Melo, R. Dhalia, C.M. de Sa, N. Standart, and O.P. de Melo Neto Identification of a C-terminal PABP-PABP interaction domain: role in cooperative binding to poly(A) and efficient cap distal translational repression J Biol Chem 278 2003 46357 46368
50. C. Clayton, M. Adams, and R. Almeida Genetic nomenclature for Trypanosoma and Leishmania Mol Biochem Parasitol 97 1998 221 224
51. M. Jankowska-Anyszka, B.J. Lamphear, and E.J. Aamodt R.E. Rhoads 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 1998 10538 10542
52. H. Matsuo, H. Li, and A.M. McGuire Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein Nat Struct Biol 4 1997 717 724
53. J. Marcotrigiano, A.C. Gingras, N. Sonenberg, and S.K. Burley Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G Mol Cell 3 1999 707 716
54. A. Niedzwiecka, J. Marcotrigiano, and J. Stepinski Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 5′ cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins J Mol Biol 319 2002 615 635
55. M. Ptushkina, T. von der Haar, S. Vasilescu, R. Frank, R. Birkenhager, and J.E. McCarthy Cooperative modulation by eIF4G of eIF4E-binding to the mRNA 5′ cap in yeast involves a site partially shared by p20 EMBO J 17 1998 4798 4808
56. T. von der Haar, and J.E. McCarthy Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in cap-complex function Mol Microbiol 46 2002 531 544
57. A. Nicholls, K.A. Sharp, and B. Honig Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons Proteins 11 1991 281 296
58. Q. Li, H. Imataka, and S. Morino Eukaryotic translation initiation factor 4AIII (eIF4AIII) is functionally distinct from eIF4AI and eIF4AII Mol Cell Biol 19 1999 7336 7346
59. J. Lu, H. Aoki, and M.C. Ganoza Molecular characterization of a prokaryotic translation factor homologous to the eukaryotic initiation factor eIF4A Int J Biochem Cell Biol 31 1999 215 219
60. R.M. Story, H. Li, and J.N. Abelson Crystal structure of a DEAD box protein from the hyperthermophile Methanococcus jannaschii Proc Natl Acad Sci USA 98 2001 1465 1470
61. N.K. Tanner, O. Cordin, J. Banroques, M. Doere, and P. Linder The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis Mol Cell 11 2003 127 138
62. J.M. Caruthers, E.R. Johnson, and D.B. McKay Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase Proc Natl Acad Sci USA 97 2000 13080 13085
63. N. Minshall, G. Thom, and N. Standart A conserved role of a DEAD box helicase in mRNA masking RNA 7 2001 1728 1742
64. J.M. Coller, M. Tucker, U. Sheth, M.A. Valencia-Sanchez, and R. Parker The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes RNA 7 2001 1717 1727
65. R. Duncan, S.C. Milburn, and J.W. Hershey Regulated phosphorylation and low abundance of HeLa cell initiation factor eIF-4F suggest a role in translational control. Heat shock effects on eIF-4F J Biol Chem 262 1987 380 388
66. M. Rau, T. Ohlmann, S.J. Morley, and V.M. Pain A reevaluation of the cap-binding protein, eIF4E, as a rate-limiting factor for initiation of translation in reticulocyte lysate J Biol Chem 271 1996 8983 8990
67. K. Asano, A. Shalev, and L. Phan Multiple roles for the C-terminal domain of eIF5 in translation initiation complex assembly and GTPase activation EMBO J 20 2001 2326 2337
68. H. He, T. von der Haar, and C.R. Singh The yeast eukaryotic initiation factor 4G (eIF4G) HEAT domain interacts with eIF1 and eIF5 and is involved in stringent AUG selection Mol Cell Biol 23 2003 5431 5445
69. S.Z. Tarun Jr., S.E. Wells, J.A. Deardorff, and A.B. Sachs Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation Proc Natl Acad Sci USA 94 1997 9046 9051
70. B. Joshi, R. Yan, and R.E. Rhoads In vitro synthesis of human protein synthesis initiation factor 4 gamma and its localization on 43 and 48 S initiation complexes J Biol Chem 269 1994 2048 2055
71. J.D. Gross, N.J. Moerke, and T. von der Haar Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E Cell 115 2003 739 750
72. M. Lewdorowicz, Y. Yoffe, and J. Zuberek Chemical synthesis and binding activity of the trypanosomatid cap-4 structure RNA 10 2004 1 10
73. Y. Yoffe, J. Zuberek, and M. Lewdorowicz Cap-binding activity of an eIF4E homolog from Leishmania RNA 10 2004 1764 1775
74. B.D. Keiper, B.J. Lamphear, and A.M. Deshpande Functional characterization of five eIF4E isoforms in Caenorhabditis elegans J Biol Chem 275 2000 10590 10596
75. A. Amiri, B.D. Keiper, and I. Kawasaki An isoform of eIF4E is a component of germ granules and is required for spermatogenesis in C. elegans Development 128 2001 3899 3912
76. D.R. Gallie, and K.S. Browning eIF4G functionally differs from eIFiso4G in promoting internal initiation, cap-independent translation, and translation of structured mRNAs J Biol Chem 276 2001 36951 36960
77. Y. Wu, Y. El Fakhry, D. Sereno, S. Tamar, and B. Papadopoulou A new developmentally regulated gene family in Leishmania amastigotes encoding a homolog of amastin surface proteins Mol Biochem Parasitol 110 2000 345 357
78. N. Boucher, Y. Wu, and C. Dumas A common mechanism of stage-regulated gene expression in Leishmania mediated by a conserved 3'-untranslated region element J Biol Chem 277 2002 19511 19520
79. R. Almeida, B.J. Gilmartin, and S.H. McCann Expression profiling of the Leishmania life cycle: cDNA arrays identify developmentally regulated genes present but not annotated in the genome Mol Biochem Parasitol 136 2004 87 100