Riboproteomic analysis of polypeptides interacting with the internal ribosome-entry site element of foot-and-mouth disease viral RNA

Proteomics

Volumn 8, Issue 22, 2008, Pages 4782-4790

  Pacheco, Almudena ^a   Reigadas, Sandrine ^a,b   Martínez Salas, Encarnación ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Hepatitis C; Internal initiation of translation; Mass spectrometry; Picornavirus; RNA binding proteins

Indexed keywords

PROTEIN DAZ1; PROTEIN PA2G4; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FOOT AND MOUTH DISEASE VIRUS; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INTERNAL RIBOSOME ENTRY SITE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION;

5' UNTRANSLATED REGIONS; BINDING SITES; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; EUKARYOTIC INITIATION FACTORS; FOOT-AND-MOUTH DISEASE VIRUS; HEPACIVIRUS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; PROTEOMICS; RIBOSOMES; RNA, VIRAL; RNA-BINDING PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

FOOT-AND-MOUTH DISEASE VIRUS; HEPATITIS C VIRUS; PICORNAVIRIDAE;

EID: 55849150550     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200800338     Document Type: Article

References (62)

1. Merrick, W. C., Cap-dependent and cap-independent translation in eukaryotic systems. Gene 2004, 332, 1-11.
2. Martinez-Salas, E., Pacheco, A., Serrano, P., Fernandez, N., New insights into internal ribosome entry site elements relevant for viral gene expression. J. Gen. Virol. 2008, 89, 611-626.
3. Pelletier, J., Sonenberg, N., Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 1988, 334, 320-325.
4. Fraser, C. S., Doudna, J. A., Structural and mechanistic insights into hepatitis C viral translation initiation. Nat. Rev. Microbiol. 2007, 5, 29-38.
5. Martinez-Salas, E., Fernandez-Miragall, O., Picornavirus IRES: structure function relationship. Curr. Pharm. Des. 2004, 10, 3757-3767.
6. Fernandez-Miragall, O., Martinez-Salas, E., Structural organization of a viral IRES depends on the integrity of the GNRA motif. RNA 2003, 9, 1333-1344.
7. Martinez-Salas, E., The impact of RNA structure on picornavirus IRES activity. Trends Microbiol. 2008. 16, 230-237.
8. Hellen, C. U., Sarnow, P., Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 2001, 15, 1593-1612.
9. Belsham, G. J., Sonenberg, N., Picornavirus RNA translation: roles for cellular proteins. Trends Microbiol. 2000, 8, 330-335.
10. Tsukiyama-Kohara, K., Lizuka, N., Kohara, M., Nomoto, A., Internal ribosome entry site within hepatitis C virus RNA. J. Virol. 1992, 66, 1476-1483.
11. Honda, M., Ping, L. H., Rijnbrand, R. C., Amphlett, E. et al., Structural requirements for initiation of translation by internal ribosome entry within genome-length hepatitis C virus RNA. Virology 1996, 222, 31-42.
12. Pestova, T. V., Shatsky, I. N., Fletcher, S. P., Jackson, R. J., Hellen, C. U., A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNA. Genes Dev. 1998, 12, 67-83.
13. Otto, G. A., Puglisi, J. D., The pathway of HCV IRES-mediated translation initiation. Cell 2004, 119, 369-380.
14. Kieft, J. S., Zhou, K., Jubin, R., Doudna, J. A., Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA 2001, 7, 194-206.
15. Lu, H., Li, W., Noble, W. S., Payan, D., Anderson, D. C., Ribo-proteomics of the hepatitis C virus internal ribosomal entry site. J. Proteome Res. 2004, 3, 949-957.
16. Lopez de Quinto, S., Lafuente, E., Martinez-Salas, E., IRES interaction with translation initiation factors: functional characterization of novel RNA contacts with eIF3, eIF4B, and eIF4GII. RNA 2001, 7, 1213-1226.
17. Link, A. J., Fleischer, T. C., Weaver, C. M., Gerbasi, V. R., Jennings, J. L., Purifying protein complexes for mass spectrometry: applications to protein translation. Methods 2005, 35, 274-290.
18. Lafuente, E., Ramos, R., Martinez-Salas, E., Long-range RNA-RNA interactions between distant regions of the hepatitis C virus internal ribosome entry site element. J. Gen. Virol. 2002, 83, 1113-1121.
19. Lopez de Quinto, S., Martinez-Salas, E., Interaction of the eIF4G initiation factor with the aphthovirus IRES is essential for internal translation initiation in vivo. RNA 2000, 6, 1380-1392.
20. Lopez de Quinto, S., Saiz, M., de la Morena, D., Sobrino, F., Martinez-Salas, E., IRES-driven translation is stimulated separately by the FMDV 30-NCR and poly(A) sequences. Nucleic Acids Res. 2002, 30, 4398-4405.
21. Reigadas, S., Pacheco, A., Ramajo, J., de Quinto, S. L., Martinez-Salas, E., Specific interference between two unrelated internal ribosome entry site elements impairs translation efficiency. FEBS Lett. 2005, 579, 6803-6808.
22. Shevchenko, A., Wilm, M., Vorm, O., Mann, M., Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68, 850-858.
23. Alonso, J., Santaren, J. F., Characterization of the Drosophila melanogaster ribosomal proteome. J. Proteome Res. 2006, 5, 2025-2032.
24. Mackay, D. T., Botting, C. H., Taylor, G. L., White, M. F., An acetylase with relaxed specificity catalyses protein N-terminal acetylation in Sulfolobus solfataricus. Mol. Microbiol. 2007, 64, 1540-1548.
25. Lopez de Quinto, S., Martinez-Salas, E., Conserved structural motifs located in distal loops of aphthovirus internal ribosome entry site domain 3 are required for internal initiation of translation. J. Virol. 1997, 71, 4171-4175.
26. Fernandez-Miragall, O., Ramos, R., Ramajo, J., Martinez-Salas, E., Evidence of reciprocal tertiary interactions between conserved motifs involved in organizing RNA structure essential for internal initiation of translation. RNA 2006, 12, 223-234.
27. Serrano, P., Gomez, J., Martinez-Salas, E., Characterization of a cyanobacterial RNase P ribozyme recognition motif in the IRES of foot-and-mouth disease virus reveals a unique structural element. RNA 2007, 13, 849-859.
28. Saiz, J. C., Lopez de Quinto, S., Ibarrola, N., Lopez-Labrador, F. X. et al., Internal initiation of translation efficiency in different hepatitis C genotypes isolated from interferon treated patients. Arch. Virol. 1999, 144, 215-229.
29. Walter, B. L., Nguyen, J. H., Ehrenfeld, E., Semler, B. L., Differential utilization of poly(rC) binding protein 2 in translation directed by picornavirus IRES elements. RNA 1999, 5, 1570-1585.
30. Monie, T. P., Perrin, A. J., Birtley, J. R., Sweeney, T. R. et al., Structural insights into the transcriptional and translational roles of Ebp1. EMBO J. 2007, 26, 3936-3944.
31. Collier, B., Gorgoni, B., Loveridge, C., Cooke, H. J., Gray, N. K., The DAZL family proteins are PABP-binding proteins that regulate translation in germ cells. EMBO J. 2005, 24, 2656-2666.
32. Doi, N., Zenno, S., Ueda, R., Ohki-Hamazaki, H. et al., Short-interfering-RNA-mediated gene silencing in mammalian cells requires Dicer and eIF2C translation initiation factors. Curr. Biol. 2003, 13, 41-46.
33. Battle, D. J., Kasim, M., Yong, J., Lotti, F. et al., The SMN complex: an assembly machine for RNPs. Cold Spring Harb. Symp. Quant. Biol. 2006, 71, 313-320.
34. Ginisty, H., Sicard, H., Roger, B., Bouvet, P., Structure and functions of nucleolin. J. Cell Sci.1999, 112, 761-772.
35. Parker, F., Maurier, F., Delumeau, I., Duchesne, M. et al., A Ras-GTPase-activating protein SH3-domain-binding protein. Mol. Cell. Biol. 1996, 16, 2561-2569.
36. Svitkin, Y. V., Costa-Mattioli, M., Herdy, B., Perreault, S., Sonenberg, N., Stimulation of picornavirus replication by the poly(A) tail in a cell-free extract is largely independent of the poly(A) binding protein (PABP). RNA 2007, 13, 2330-2340.
37. Stoneley, M., Willis, A. E., Cellular internal ribosome entry segments: structures, trans-acting factors and regulation of gene expression. Oncogene 2004, 23, 3200-3207.
38. Semler, B. L., Waterman, M. L., IRES-mediated pathways to polysomes: nuclear versus cytoplasmic routes. Trends Microbiol. 2008, 16, 1-5.
39. Bedard, K. M., Daijogo, S., Semler, B. L., A nucleo-cytoplasmic SR protein functions in viral IRES-mediated translation initiation. EMBO J. 2007, 26, 459-467.
40. Vazquez-Pianzola, P., Urlaub, H., Rivera-Pomar, R., Proteomic analysis of reaper 50 untranslated region-interacting factors isolated by tobramycin affinity-selection reveals a role for La antigen in reaper mRNA translation. Proteomics 2005, 5, 1645-1655.
41. Ji, H., Fraser, C. S., Yu, Y., Leary, J., Doudna, J. A., Coordinated assembly of human translation initiation complexes by the hepatitis C virus internal ribosome entry site RNA. Proc. Natl. Acad. Sci. USA 2004, 101, 16990-16995.
42. Cobbold, L. C., Spriggs, K. A., Haines, S. J., Dobbyn, H. C. et al., Identification of internal ribosome entry segment (IRES)-trans-acting factors for the Myc family of IRES. Mol. Cell. Biol. 2008, 28, 40-49.
43. Gerbasi, V. R., Link, A. J., The myotonic dystrophy type 2 protein ZNF9 is part of an ITAF complex that promotes cap-independent translation. Mol. Cell. Proteomics 2007, 6, 1049-1058.
44. Waggoner, S., Sarnow, P., Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirus-infected cells. J. Virol. 1998, 72, 6699-6709.
45. Harris, D., Zhang, Z., Chaubey, B., Pandey, V. N., Identification of cellular factors associated with the 30-nontranslated region of the hepatitis C virus genome. Mol. Cell. Proteomics 2006, 5, 1006-1018.
46. Isken, O., Baroth, M., Grassmann, C. W., Weinlich, S. et al., Nuclear factors are involved in hepatitis C virus RNA replication. RNA 2007, 13, 1675-1692.
47. Fernandez-Miragall, O., Martinez-Salas, E., In vivo footprint of a picornavirus internal ribosome entry site reveals differences in accessibility to specific RNA structural elements. J. Gen. Virol. 2007, 88, 3053-3062.
48. Kim, J. H., Hahm, B., Kim, Y. K., Choi,M., Jang, S. K., Protein-protein interaction among hnRNP shuttling between nucleus and cytoplasm. J. Mol. Biol. 2000, 298, 395-405.
49. Kiledjian, M., Dreyfuss, G., Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J. 1992, 11, 2655-2664.
50. Evans, J. R., Mitchell, S. A., Spriggs, K. A., Ostrowski, J. et al., Members of the poly (rC) binding protein family stimulate the activity of the c-myc internal ribosome entry segment in vitro and in vivo. Oncogene 2003, 22, 8012-8020.
51. Gamarnik, A. V., Boddeker, N., Andino, R., Translation and replication of human rhinovirus type 14 and mengovirus in Xenopus oocytes. J. Virol. 2000, 74, 11983-11987.
52. Matunis, E. L., Matunis, M. J., Dreyfuss, G., Characterization of the major hnRNP proteins from Drosophila melanogaster. J. Cell. Biol. 1992, 116, 257-269.
53. Pilipenko, E. V., Pestova, T. V., Kolupaeva, V. G., Khitrina, E. V. et al., A cell cycle-dependent protein serves as a template-specific translation initiation factor. Genes Dev. 2000, 14, 2028-2045.
54. Squatrito, M., Mancino, M., Donzelli, M., Areces, L. B., Draetta, G. F., EBP1 is a nucleolar growth-regulating protein that is part of pre-ribosomal ribonucleoprotein complexes. Oncogene 2004, 23, 4454-4465.
55. Andreev, D. E., Fernandez-Miragall, O., Ramajo, J., Dmitriev, S. E. et al., Differential factor requirement to assemble translation initiation complexes at the alternative start codons of foot-and-mouth disease virus RNA. RNA 2007, 13, 1366-1374.
56. Hartman, T. R., Qian, S., Bolinger, C., Fernandez, S. et al., RNA helicase A is necessary for translation of selected messenger RNA. Nat. Struct. Mol. Biol. 2006, 13, 509-516.
57. Mikula, M., Dzwonek, A., Karczmarski, J., Rubel, T. et al., Landscape of the hnRNP K protein-protein interactome. Proteomics 2006, 6, 2395-2406.
58. Godbout, R., Packer, M., Bie, W., Overexpression of a DEAD box protein (DDX1) in neuroblastoma and retinoblastoma cell lines. J. Biol. Chem. 1998, 273, 21161-21168.
59. Chen, H. C., Lin,W. C., Tsay, Y. G., Lee, S. C., Chang, C. J., An RNA helicase, DDX1, interacting with poly(A) RNA and heterogeneous nuclear ribonucleoprotein K. J. Biol. Chem. 2002, 277, 40403-40409.
60. Kukalev, A., Nord, Y., Palmberg, C., Bergman, T., Percipalle, P., Actin and hnRNP U cooperate for productive transcription by RNA polymerase II. Nat. Struct. Mol. Biol. 2005, 12, 238-244.
61. Villace, P., Marion, R. M., Ortin, J., The composition of Staufen-containing RNA granules from human cells indicates their role in the regulated transport and translation of messenger RNA. Nucleic Acids Res. 2004, 32, 2411-2420.
62. Spriggs, K. A., Stoneley, M., Bushell, M., Willis, A. E., Reprogramming of translation following cell stress allows IRES-mediated translation to predominate. Biol. Cell 2008, 100, 27-38.