Eukaryotic initiation factor 5A dephosphorylation is required for translational arrest in stationary phase cells

Biochemical Journal

Volumn 451, Issue 2, 2013, Pages 257-267

  Chung, Janete ^a   Rocha, Antonio A ^a   Tonelli, Renata R ^a   Castilho, Beatriz A ^a   Schenkman, Sergio ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Eukaryotic initiation factor 5A (eIF5A); Protein phosphorylation; Translation initiation factor; Translation regulation; Trypanosoma cruzi

Indexed keywords

ASPARTIC ACID; INITIATION FACTOR 5A;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE PHASE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; STATIONARY PHASE; TRYPANOSOMA CRUZI;

ALANINE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ASPARTIC ACID; MOLECULAR SEQUENCE DATA; PEPTIDE INITIATION FACTORS; PHOSPHORYLATION; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RNA-BINDING PROTEINS; SERINE; TRYPANOSOMA CRUZI; TYROSINE;

EUKARYOTA; TRYPANOSOMA CRUZI;

EID: 84875635981     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121553     Document Type: Article

References (58)

1. Zanelli, C. F. and Valentini, S. R. (2007) Is there a role for eIF5A in translation Amino Acids 33, 351-358
2. Park, M. H., Lee, Y. B. and Joe, Y. A. (1997) Hypusine is essential for eukaryotic cell proliferation. Biol. Signals 6, 115-123
3. Saini, P., Eyler, D. E., Green, R. and Dever, T. E. (2009) Hypusine-containing protein eIF5A promotes translation elongation. Nature 459, 118-121
4. Gregio, A. P., Cano, V. P., Avaca, J. S., Valentini, S. R. and Zanelli, C. F. (2009) eIF5A has a function in the elongation step of translation in yeast. Biochem. Biophys. Res. Commun. 380, 785-790
5. Valentini, S. R., Casolari, J. M., Oliveira, C. C., Silver, P. A. and McBride, A. E. (2002) Genetic interactions of yeast eukaryotic translation initiation factor 5A (eIF5A) reveal connections to poly(A)-binding protein and protein kinase C signaling. Genetics 160, 393-405
6. Chatterjee, I., Gross, S. R., Kinzy, T. G. and Chen, K. Y. (2006) Rapid depletion of mutant eukaryotic initiation factor 5A at restrictive temperature reveals connections to actin cytoskeleton and cell cycle progression. Mol. Genet. Genomics 275, 264-276
7. Park, M. H., Nishimura, K., Zanelli, C. F. and Valentini, S. R. (2010) Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 38, 491-500
8. Cooper, H. L., Park, M. H., Folk, J. E., Safer, B. and Braverman, R. (1983) Identification of the hypusine-containing protein hy+ as translation initiation factor eIF-4D. Proc. Natl. Acad. Sci. U.S.A. 80, 1854-1857
9. Park, M. H. (2006) The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A). J. Biochem. 139, 161-169
10. Kang, H. A., Schwelberger, H. G. and Hershey, J. W. (1993) Translation initiation factor eIF-5A, the hypusine-containing protein, is phosphorylated on serine in Saccharomyces cerevisiae. J. Biol. Chem. 268, 14750-14756
11. Klier, H., Wohl, T., Eckerskorn, C., Magdolen, V. and Lottspeich, F. (1993) Determination and mutational analysis of the phosphorylation site in the hypusine-containing protein Hyp2p. FEBS Lett. 334, 360-364
12. Lebska, M., Ciesielski, A., Szymona, L., Godecka, L., Lewandowska-Gnatowska, E., Szczegielniak, J. and Muszynska, G. (2010) Phosphorylation of maize eukaryotic translation initiation factor 5A (eIF5A) by casein kinase 2: identification of phosphorylated residue and influence on intracellular localization of eIF5A. J. Biol. Chem. 285, 6217-6226
13. Chou, W. C., Huang, Y. W., Tsay, W. S., Chiang, T. Y., Huang, D. D. and Huang, H. J. (2004) Expression of genes encoding the rice translation initiation factor, eIF5A, is involved in developmental and environmental responses. Physiol. Plant. 121, 50-57
14. Lan, P. and Schmidt, W. (2011) The enigma of eIF5A in the iron deficiency response of Arabidopsis. Plant Signaling Behav. 6, 528-530
15. Schrader, R., Young, C., Kozian, D., Hoffmann, R. and Lottspeich, F. (2006) Temperature-sensitive eIF5A mutant accumulates transcripts targeted to the nonsense-mediated decay pathway. J. Biol. Chem. 281, 35336-35346
16. Szoor, B., Ruberto, I., Burchmore, R. and Matthews, K. R. (2010) A novel phosphatase cascade regulates differentiation in Trypanosoma brucei via a glycosomal signaling pathway. Genes Dev. 24, 1306-1316
17. Haile, S. and Papadopoulou, B. (2007) Developmental regulation of gene expression in trypanosomatid parasitic protozoa. Curr. Opin. Microbiol. 10, 569-577
18. Clayton, C. and Shapira, M. (2007) Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol. Biochem. Parasitol. 156, 93-101
19. Avila, A. R., Dallagiovanna, B., Yamada-Ogatta, S. F., Monteiro-Goes, V., Fragoso, S. P., Krieger, M. A. and Goldenberg, S. (2003) Stage-specific gene expression during Trypanosoma cruzi metacyclogenesis. GMR, Genet. Mol. Res. 2, 159-168
20. Goldenberg, S. and Avila, A. R. (2011) Aspects of Trypanosoma cruzi stage differentiation. Adv. Parasitol. 75, 285-305
21. Contreras, V. T., Araujo-Jorge, T. C., Bonaldo, M. C., Thomaz, N., Barbosa, H. S., Meirelles, M. N. and Goldenberg, S. (1988) Biological aspects of the Dm 28c clone of Trypanosoma cruzi after metacyclogenesis in chemically defined media. Mem. Inst. Oswaldo Cruz 83, 123-133
22. Cano, M. I., Gruber, A., Vazquez, M., Cort, S. A., Levin, M. J., Gonzalez, A., Degrave, W., Rondinelli, E., Zingales, B. and Ramirez, J. L. (1995) Molecular karyotype of clone CL Brener chosen for the Trypanosoma cruzi genome project. Mol. Biochem. Parasitol. 71, 273-278
23. Contreras, V. T., Salles, J. M., Thomas, N., Morel, C. M. and Goldenberg, S. (1985) In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Mol. Biochem. Parasitol. 16, 315-327
24. Abuin, G., Freitas-Junior, L. H. G., Colli, W., Alves, M. J. and Schenkman, S. (1999) Expression of trans-sialidase and 85 kDa glycoprotein genes in Trypanosoma cruzi is differentially regulated at the post-transcriptional level by labile protein factors. J. Biol. Chem. 274, 13041-13047
25. McDowell, M. A., Ransom, D. M. and Bangs, J. D. (1998) Glycosylphosphatidylinositol-dependent secretory transport in Trypanosoma brucei. Biochem. J. 335, 681-689
26. de Oliveira, J. F., Castilho, B. A., Sforca, M. L., Krieger, M. A., Zeri, A. C., Guimaraes, B. G. and Zanchin, N. I. (2009) Characterization of the Trypanosoma cruzi ortholog of the SBDS protein reveals an intrinsically disordered extended C-terminal region showing RNA-interacting activity. Biochimie 91, 475-483
27. Ramirez, M. I., Yamauchi, L. M., de Freitas, L. H., Uemura, H. and Schenkman, S. (2000) The use of the green fluorescent protein to monitor and improve transfection in Trypanosoma cruzi. Mol. Biochem. Parasitol. 111, 235-240
28. Brecht, M. and Parsons, M. (1998) Changes in polysome profiles accompany trypanosome development. Mol. Biochem. Parasitol. 97, 189-198
29. Tonelli, R. R., Augusto, L. d. S., Castilho, B. A. and Schenkman, S. (2011) Protein synthesis attenuation by phosphorylation of eIF2α is required for the differentiation of Trypanosoma cruzi into infective forms. PLoS ONE 6, e27094
30. Werner, W. E. (2003) Run parameters affecting protein patterns from second dimension electrophoresis gels. Anal. Biochem. 317, 280-283
31. Candiano, G., Bruschi, M., Musante, L., Santucci, L., Ghiggeri, G. M., Carnemolla, B., Orecchia, P., Zardi, L. and Righetti, P. G. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25, 1327-1333
32. Steinberg, T. H., Agnew, B. J., Gee, K. R., Leung, W. Y., Goodman, T., Schulenberg, B., Hendrickson, J., Beechem, J. M., Haugland, R. P. and Patton, W. F. (2003) Global quantitative phosphoprotein analysis using Multiplexed Proteomics technology. Proteomics 3, 1128-1144
33. Mann, M. and Pandey, A. (2001) Use of mass spectrometry-derived data to annotate nucleotide and protein sequence databases. Trends Biochem. Sci. 26, 54-61
34. Chen, E. I., Cociorva, D., Norris, J. L. and Yates, 3rd, J. R. (2007) Optimization of mass spectrometry-compatible surfactants for shotgun proteomics. J. Proteome Res. 6, 2529-2538
35. Lee, S. B., Park, J. H., Kaevel, J., Sramkova, M., Weigert, R. and Park, M. H. (2009) The effect of hypusine modification on the intracellular localization of eIF5A. Biochem. Biophys. Res. Commun. 383, 497-502
36. Jao, D. L. and Yu Chen, K. (2002) Subcellular localization of the hypusine-containing eukaryotic initiation factor 5A by immunofluorescent staining and green fluorescent protein tagging. J. Cell. Biochem. 86, 590-600
37. Jakus, J., Wolff, E. C., Park, M. H. and Folk, J. E. (1993) Features of the spermidine-binding site of deoxyhypusine synthase as derived from inhibition studies. Effective inhibition by bis- and mono-guanylated diamines and polyamines. J. Biol. Chem. 268, 13151-13159
38. Chawla, B., Jhingran, A., Singh, S., Tyagi, N., Park, M. H., Srinivasan, N., Roberts, S. C. and Madhubala, R. (2010) Identification and characterization of a novel deoxyhypusine synthase in Leishmania donovani. J. Biol. Chem. 285, 453-463
39. Nett, I. R. E., Martin, D. M. A., Miranda-Saavedra, D., Lamont, D., Barber, J. D., Mehlert, A. and Ferguson, M. A. J. (2009) The phosphoproteome of bloodstream form Trypanosoma brucei, causative agent of African sleeping sickness. Mol. Cell. Proteomics 8, 1527-1538
40. Pinna, L. A. (2002) Protein kinase CK2: a challenge to canons. J. Cell Sci. 115, 3873-3878
41. Jensen, B. C., Kifer, C. T., Brekken, D. L., Randall, A. C., Wang, Q., Drees, B. L. and Parsons, M. (2007) Characterization of protein kinase CK2 from Trypanosoma brucei. Mol. Biochem. Parasitol. 151, 28-40
42. De Lima, A. R., Medina, R., Uzcanga, G. L., Noris Suarez, K., Contreras, V. T., Navarro, M. C., Arteaga, R. and Bubis, J. (2006) Tight binding between a pool of the heterodimeric α/β tubulin and a protein kinase CK2 in Trypanosoma cruzi epimastigotes. Parasitology 132, 511-523
43. Szoor, B., Wilson, J., McElhinney, H., Tabernero, L. and Matthews, K. R. (2006) Protein tyrosine phosphatase TbPTP1: a molecular switch controlling life cycle differentiation in trypanosomes. J. Cell Biol. 175, 293-303
44. Gauci, S., Helbig, A. O., Slijper, M., Krijgsveld, J., Heck, A. J. R. and Mohammed, S. (2009) Lys-N and trypsin cover complementary parts of the phosphoproteome in a refined SCX-based approach. Anal. Chem. 81, 4493-4501
45. Albuquerque, C. P., Smolka, M. B., Payne, S. H., Bafna, V., Eng, J. and Zhou, H. (2008) A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol. Cell. Proteomics 7, 1389-1396
46. Li, X., Gerber, S. A., Rudner, A. D., Beausoleil, S. A., Haas, W., Vilĺen, J., Elias, J. E. and Gygi, S. P. (2007) Large-scale phosphorylation analysis of α-factor-arrested Saccharomyces cerevisiae. J. Proteome Res. 6, 1190-1197
47. Zuk, D. and Jacobson, A. (1998) A single amino acid substitution in yeast eIF-5A results in mRNA stabilization. EMBO J. 17, 2914-2925
48. Dias, C. A., Cano, V. S., Rangel, S. M., Apponi, L. H., Frigieri, M. C., Muniz, J. R., Garcia, W., Park, M. H., Garratt, R. C., Zanelli, C. F. and Valentini, S. R. (2008) Structural modeling and mutational analysis of yeast eukaryotic translation initiation factor 5A reveal new critical residues and reinforce its involvement in protein synthesis. FEBS J. 275, 1874-1888
49. Jao, D. L. and Chen, K. Y. (2006) Tandem affinity purification revealed the hypusine-dependent binding of eukaryotic initiation factor 5A to the translating 80S ribosomal complex. J. Cell. Biochem. 97, 583-598
50. Anderson, P. and Kedersha, N. (2006) RNA granules. J. Cell Biol. 172, 803-808
51. Cassola, A., De Gaudenzi, J. G. and Frasch, A. C. (2007) Recruitment of mRNAs to cytoplasmic ribonucleoprotein granules in trypanosomes. Mol. Microbiol. 65, 655-670
52. Holetz, F. B., Correa, A., Avila, A. R., Nakamura, C. V., Krieger, M. A. and Goldenberg, S. (2007) Evidence of P-body-like structures in Trypanosoma cruzi. Biochem. Biophys. Res. Commun. 356, 1062-1067
53. Alves, L. R., Avila, A. R., Correa, A., Holetz, F. B., Mansur, F. C., Manque, P. A., de Menezes, J. P., Buck, G. A., Krieger, M. A. and Goldenberg, S. (2010) Proteomic analysis reveals the dynamic association of proteins with translated mRNAs in Trypanosoma cruzi. Gene 452, 72-78
54. Zanelli, C. F., Maragno, A. L., Gregio, A. P., Komili, S., Pandolfi, J. R., Mestriner, C. A., Lustri, W. R. and Valentini, S. R. (2006) eIF5A binds to translational machinery components and affects translation in yeast. Biochem. Biophys. Res. Commun. 348, 1358-1366
55. Blaha, G., Stanley, R. E. and Steitz, T. A. (2009) Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science 325, 966-970
56. Doerfel, L., Wohlgemuth, I., Kothe, C., Peske, F., Urlaub, H. and Rodnina, M. (2012) EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339, 85-88
57. Li, C. H., Ohn, T., Ivanov, P., Tisdale, S. and Anderson, P. (2010) eIF5A promotes translation elongation, polysome disassembly and stress granule assembly. PLoS ONE 5, e9942
58. Ma, F., Liu, Z., Wang, T. W., Hopkins, M. T., Peterson, C. A. and Thompson, J. E. (2010) Arabidopsis eIF5A3 influences growth and the response to osmotic and nutrient stress. Plant Cell Environ. 33, 1682-1696