Gemin5 promotes IRES interaction and translation control through its C-terminal region

Nucleic Acids Research

Volumn 41, Issue 2, 2013, Pages 1017-1028

  Piñeiro, David ^a   Fernández, Noemi ^a   Ramajo, Jorge ^a   Martínez Salas, Encarnación ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GEMIN5; MESSENGER RNA; POLYPYRIMIDINE BINDING PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ACYLATION; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA HAIRPIN; DOWN REGULATION; IN VITRO STUDY; INTERNAL RIBOSOME ENTRY SITE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN RNA BINDING; RNA BINDING; RNA CONFORMATION; RNA PROBE; RNA SEQUENCE; RNA STRUCTURE; RNA TRANSLATION; STRUCTURE ACTIVITY RELATION;

BASE SEQUENCE; BINDING SITES; DOWN-REGULATION; FOOT-AND-MOUTH DISEASE VIRUS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; POLYPYRIMIDINE TRACT-BINDING PROTEIN; PROTEIN BIOSYNTHESIS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA, VIRAL; SMN COMPLEX PROTEINS;

EID: 84875417552     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1212     Document Type: Article

References (50)

1. Cooper, T.A., Wan, L. and Dreyfuss, G. (2009) RNA and disease. Cell, 136, 777-793.
2. Isken, O. and Maquat, L.E. (2008) The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat. Rev. Genet., 9, 699-712.
3. Sweet, T., Kovalak, C. and Coller, J. (2012) The DEAD-Box protein Dhh1 promotes decapping by slowing ribosome movement. PLoS Biol., 10, e1001342.
4. Cooke, A., Prigge, A., Opperman, L. and Wickens, M. (2011) Targeted translational regulation using the PUF protein family scaffold. Proc. Natl Acad. Sci. USA, 108, 15870-15875.
5. Lee, E.K., Kim, W., Tominaga, K., Martindale, J.L., Yang, X., Subaran, S.S., Carlson, O.D., Mercken, E.M., Kulkarni, R.N., Akamatsu, W. et al. (2012) RNA-binding protein HuD controls insulin translation. Mol. Cell, 45, 826-835.
6. Sonenberg, N. and Hinnebusch, A.G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell, 136, 731-745.
7. Sonenberg, N. and Dever, T.E. (2003) Eukaryotic translation initiation factors and regulators. Curr. Opin. Struct. Biol., 13, 56-63. (Pubitemid 36170255)
8. Spriggs, K.A., Bushell, M. and Willis, A.E. (2010) Translational regulation of gene expression during conditions of cell stress. Mol. Cell, 40, 228-237.
9. Martinez-Salas, E., Pacheco, A., Serrano, P. and Fernandez, N. (2008) New insights into internal ribosome entry sites relevant for viral gene expression. J. Gen. Virol., 2008, 611-626.
10. Walsh, D. and Mohr, I. (2011) Viral subversion of the host protein synthesis machinery. Nat. Rev. Microbiol., 9, 860-875.
11. Martinez-Salas, E. (2008) The impact of RNA structure on picornavirus IRES activity. Trends Microbiol., 16, 230-237.
12. Andreev, D.E., Fernandez-Miragall, O., Ramajo, J., Dmitriev, S.E., Terenin, I.M., Martinez-Salas, E. and Shatsky, I.N. (2007) Differential factor requirement to assemble translation initiation complexes at the alternative start codons of foot-and-mouth disease virus RNA. RNA, 13, 1366-1374. (Pubitemid 47080480)
13. Bedard, K.M., Daijogo, S. and Semler, B.L. (2007) A nucleo-cytoplasmic SR protein functions in viral IRES-mediated translation initiation. EMBO J., 26, 459-467. (Pubitemid 46160946)
14. Cammas, A., Pileur, F., Bonnal, S., Lewis, S.M., Leveque, N., Holcik, M. and Vagner, S. (2007) Cytoplasmic relocalization of heterogeneous nuclear ribonucleoprotein A1 controls translation initiation of specific mRNAs. Mol. Biol. Cell, 18, 5048-5059. (Pubitemid 350246704)
15. Kim, T.D., Woo, K.C., Cho, S., Ha, D.C., Jang, S.K. and Kim, K.T. (2007) Rhythmic control of AANAT translation by hnRNP Q in circadian melatonin production. Genes Dev., 21, 797-810. (Pubitemid 46572359)
16. Liwak, U., Thakor, N., Jordan, L.E., Roy, R., Lewis, S.M., Pardo, O.E., Seckl, M. and Holcik, M. (2012) Tumor suppressor PDCD4 represses internal ribosome entry site-mediated translation of antiapoptotic proteins and is regulated by S6 kinase Mol. Cell Biol., 32, 1818-1829.
17. Pacheco, A. and Martinez-Salas, E. (2010) Insights into the biology of IRES elements through riboproteomic approaches. J. Biomed. Biotechnol., 2010, 458927.
18. Komar, A.A. and Hatzoglou, M. (2011) Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle, 10, 229-240.
19. Pacheco, A., Reigadas, S. and Martinez-Salas, E. (2008) Riboproteomic analysis of polypeptides interacting with the internal ribosome-entry site element of foot-and-mouth disease viral RNA. Proteomics, 8, 4782-4790.
20. Pacheco, A., Lopez de Quinto, S., Ramajo, J., Fernandez, N. and Martinez-Salas, E. (2009) A novel role for Gemin5 in mRNA translation. Nucleic Acids Res., 37, 582-590.
21. Bradrick, S.S. and Gromeier, M. (2009) Identification of gemin5 as a novel 7-methylguanosine cap-binding protein. PLoS One, 4, e7030.
22. Castello, A., Fischer, B., Eichelbaum, K., Horos, R., Beckmann, B.M., Strein, C., Davey, N.E., Humphreys, D.T., Preiss, T., Steinmetz, L.M. et al. (2012) Insights into RNA Biology from an Atlas of Mammalian mRNA-Binding Proteins. Cell, 149, 1393-1406.
23. Battle, D.J., Lau, C.K., Wan, L., Deng, H., Lotti, F. and Dreyfuss, G. (2006) The Gemin5 protein of the SMN complex identifies snRNAs. Mol. Cell, 23, 273-279. (Pubitemid 44062371)
24. Cauchi, R.J. (2010) SMN and Gemins: 'we are family'. or are we?: insights into the partnership between Gemins and the spinal muscular atrophy disease protein SMN. Bioessays, 32, 1077-1089.
25. Battle, D.J., Kasim, M., Wang, J. and Dreyfuss, G. (2007) SMN-independent subunits of the SMN complex. Identification of a small nuclear ribonucleoprotein assembly intermediate. J. Biol. Chem., 282, 27953-27959. (Pubitemid 47529485)
26. Yong, J., Kasim, M., Bachorik, J.L., Wan, L. and Dreyfuss, G. (2010) Gemin5 delivers snRNA precursors to the SMN complex for snRNP biogenesis. Mol. Cell, 38, 551-562.
27. Piñ eiro, D., Ramajo, J., Bradrick, S.S. and Martinez-Salas, E. (2012) Gemin5 proteolysis reveals a novel motif to identify L protease targets. Nucleic Acids Res., 40, 4942-4953.
28. Almstead, L.L. and Sarnow, P. (2007) Inhibition of U snRNP assembly by a virus-encoded proteinase. Genes Dev., 21, 1086-1097. (Pubitemid 46686477)
29. Lopez de Quinto, S., Lafuente, E. and Martinez-Salas, E. (2001) IRES interaction with translation initiation factors: functional characterization of novel RNA contacts with eIF3, eIF4B, and eIF4GII. RNA, 7, 1213-1226. (Pubitemid 32831351)
30. Meyer, K., Petersen, A., Niepmann, M. and Beck, E. (1995) Interaction of eukaryotic initiation factor eIF-4B with a picornavirus internal translation initiation site. J. Virol., 69, 2819-2824.
31. Ramos, R. and Martinez-Salas, E. (1999) Long-range RNA interactions between structural domains of the aphthovirus internal ribosome entry site (IRES). RNA, 5, 1374-1383. (Pubitemid 29489819)
32. Fernandez, N., Fernandez-Miragall, O., Ramajo, J., Garcia-Sacristan, A., Bellora, N., Eyras, E., Briones, C. and Martinez-Salas, E. (2011) Structural basis for the biological relevance of the invariant apical stem in IRES-mediated translation. Nucleic Acids Res., 39, 8572-8585.
33. Fernandez-Miragall, O. and Martinez-Salas, E. (2003) Structural organization of a viral IRES depends on the integrity of the GNRA motif. RNA, 9, 1333-1344. (Pubitemid 37310864)
34. Martinez-Salas, E., Saiz, J.C., Davila, M., Belsham, G.J. and Domingo, E. (1993) A single nucleotide substitution in the internal ribosome entry site of foot-and-mouth disease virus leads to enhanced cap-independent translation in vivo. J. Virol., 67, 3748-3755. (Pubitemid 23180695)
35. Lopez de Quinto, S. and Martinez-Salas, E. (1999) Involvement of the aphthovirus RNA region located between the two functional AUGs in start codon selection. Virology, 255, 324-336. (Pubitemid 29393344)
36. Studier, F.W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif., 41, 207-234.
37. Lopez de Quinto, S. and Martinez-Salas, E. (2000) Interaction of the eIF4G initiation factor with the aphthovirus IRES is essential for internal translation initiation in vivo. RNA, 6, 1380-1392.
38. Fernandez, N., Garcia-Sacristan, A., Ramajo, J., Briones, C. and Martinez-Salas, E. (2011) Structural analysis provides insights into the modular organization of picornavirus IRES. Virology, 409, 251-261.
39. Wilkinson, K.A., Merino, E.J. and Weeks, K.M. (2006) Selective 20-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat. Protoc., 1, 1610-1616.
40. Gubitz, A.K., Mourelatos, Z., Abel, L., Rappsilber, J., Mann, M. and Dreyfuss, G. (2002) Gemin5, a novel WD repeat protein component of the SMN complex that binds Sm proteins. J. Biol. Chem., 277, 5631-5636. (Pubitemid 34968617)
41. Watts, J.M., Dang, K.K., Gorelick, R.J., Leonard, C.W., Bess, J.W. Jr, Swanstrom, R., Burch, C.L. and Weeks, K.M. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature, 460, 711-716.
42. Duncan, C.D. and Weeks, K.M. (2010) Nonhierarchical ribonucleoprotein assembly suggests a strain-propagation model for protein-facilitated RNA folding. Biochemistry, 49, 5418-5425.
43. Luz, N. and Beck, E. (1991) Interaction of a cellular 57-kilodalton protein with the internal translation initiation site of foot-and-mouth disease virus. J. Virol., 65, 6486-6494.
44. Golembe, T.J., Yong, J., Battle, D.J., Feng, W., Wan, L. and Dreyfuss, G. (2005) Lymphotropic herpesvirus saimiri uses the SMN complex to assemble Sm cores on its small RNAs. Mol. Cell Biol., 25, 602-611. (Pubitemid 40096582)
45. Lau, C.K., Bachorik, J.L. and Dreyfuss, G. (2009) Gemin5-snRNA interaction reveals an RNA binding function for WD repeat domains. Nat. Struct. Mol. Biol., 16, 486-491.
46. Hao le, T., Fuller, H.R., Lam le, T., Le, T.T., Burghes, A.H. and Morris, G.E. (2007) Absence of gemin5 from SMN complexes in nuclear Cajal bodies. BMC Cell Biol., 8, 28.
47. Otter, S., Grimmler, M., Neuenkirchen, N., Chari, A., Sickmann, A. and Fischer, U. (2007) A comprehensive interaction map of the human survival of motor neuron (SMN) complex. J. Biol. Chem., 282, 5825-5833. (Pubitemid 47093793)
48. Fuller, H.R., Man, N.T., Lam le, T., Thanh le, T., Keough, R.A., Asperger, A., Gonda, T.J. and Morris, G.E. (2010) The SMN interactome includes Myb-binding protein 1a. J. Proteome. Res., 9, 556-563.
49. Fierro-Monti, I., Mohammed, S., Matthiesen, R., Santoro, R., Burns, J.S., Williams, D.J., Proud, C.G., Kassem, M., Jensen, O.N. and Roepstorff, P. (2006) Quantitative proteomics identifies Gemin5, a scaffolding protein involved in ribonucleoprotein assembly, as a novel partner for eukaryotic initiation factor 4E. J. Proteome. Res., 5, 1367-1378. (Pubitemid 43865807)
50. Liu, Q. and Dreyfuss, G. (1996) A novel nuclear structure containing the survival of motor neurons protein. EMBO J., 15, 3555-3565. (Pubitemid 26239768)