RNA chaperone activity of protein components of human Ro RNPs

RNA

Volumn 11, Issue 7, 2005, Pages 1084-1094

  Belisova, Aurélia ^a   Semrad, Katharina ^a   Mayer, Oliver ^a   Kocian, Grazia ^a   Waigmann, Elisabeth ^a   Schroeder, Renée ^a   Steiner, Günter ^a,b  

^a Vienna Biocenter   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

hnRNPs; La; RNA chaperone; Ro60; trans splicing

Indexed keywords

BINDING PROTEIN; CHAPERONE; ISOPROTEIN; LA ANTIGEN; RIBONUCLEOPROTEIN; RIBONUCLEOPROTEIN RO 60; RNA; UNCLASSIFIED DRUG;

ARTICLE; CYTOTOXICITY; INTRON; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN TARGETING; RNA BINDING; RNA SPLICING;

AUTOANTIGENS; CYTOPLASM; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; INTRONS; MOLECULAR CHAPERONES; MUTATION; PROTEIN BINDING; RECOMBINANT PROTEINS; RIBONUCLEOPROTEINS; RNA; RNA, SMALL CYTOPLASMIC; SULFUR RADIOISOTOPES; TRANS-SPLICING; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 22244466113     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.7263905     Document Type: Article

References (61)

1. Ali, N. and Siddiqui, A. 1995. Interaction of polypyrimidine tractbinding protein with the 50 noncoding region of the hepatitis C virus RNA genome and its functional requirement in internal initiation of translation. J. Virol. 69: 6367-6375.
2. Ali, N., Pruijn, G.J., Kenan, D.J., Keene, J.D., and Siddiqui, A. 2000. Human La antigen is required for the hepatitis C virus internal ribosome entry site-mediated translation. J. Biol.Chem. 275: 27531-27540.
3. Brown, E.C. and Jackson, R.J. 2004. All five cold-shock domains of unr (upstream of N-ras) are required for stimulation of human rhinovirus RNA translation. J. Gen. Virol. 85: 2279-2287.
4. Chakshusmathi, G., Kim, S.D., Rubinson, D.A., and Wolin, S.L. 2003. A La protein requirement for efficient pre-tRNA folding. EMBO J. 22: 6562-6572.
5. Chen, X., Quinn, A.M., and Wolin, S.L. 2000. Ro ribonucleoproteins contribute to the resistance of Deinococcus radiodurans to ultraviolet irradiation. Genes & Dev. 14: 777-782.
6. Chen, X., Smith, J.D., Shi, H., Yang, D.D., Flavell, R.A., and Wolin, S.L. 2003. The Ro autoantigen binds misfolded U2 small nuclear RNAs and assists mammalian cell survival after UV irradiation. Curr. Biol. 13: 2206-2211.
7. Clodi, E., Semrad, K., and Schroeder, R. 1999. Assaying RNA chaperone activity in vivo using a novel RNA folding trap. EMBO J. 18: 3776-3782.
8. Coetzee, T., Herschlag, D., and Belfort, M. 1994. Escherichia coli proteins, including ribosomal protein S12, facilitate in vitro splicing of phage T4 introns by acting as RNA chaperones. Genes & Dev. 8: 1575-1588.
9. Evans, J.R., Mitchell, S.A., Spriggs, K.A., Ostrowski, J., Bomsztyk, K., Ostarek, D., and Willis, A.E. 2003. 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 22: 8012-8020.
10. Expert-Bezancon, A., Le Caer, J.P., and Marie, J. 2002. Heterogeneous nuclear ribonucleoprotein (hnRNP) K is a component of an intronic splicing enhancer complex that activates the splicing of the alternative exon 6A from chicken β-tropomyosin pre-mRNA. J. Biol. Chem. 277: 16614-16623.
11. Fabini, G., Raijmakers, R., Hayer, S., Fouraux, M.A., Pruijn, G.J., and Steiner, G. 2001. The heterogeneous nuclear ribonucleoproteins I and K interact with a subset of the Ro ribonucleoprotein-associated Y RNAs in vitro and in vivo. J. Biol. Chem. 276: 20711-20718.
12. Fan, H., Goodier, J.L., Chamberlain, J.R., Engelke, D.R., and Maraia, R.J. 1998. 5′ processing of tRNA precursors can be modulated by the human La antigen phosphoprotein. Mol. Cell. Biol. 18: 3201-3211.
13. Farris, A.D., O'Brien, C.A., and Harley, J.B. 1995. Y3 is the most conserved small RNA component of Ro ribonucleoprotein complexes in vertebrate species. Gene 154: 193-198.
14. Fouraux, M.A., Bouvet, P., Verkaart, S., van Venrooij, W.J., and Pruijn, G.J. 2002. Nucleolin associates with a subset of the human Ro ribonucleoprotein complexes. J. Mol. Biol. 320: 475-488.
15. Geissmann, T.A. and Touati, D. 2004. Hfq, a new chaperoning role: Binding to messenger RNA determines access for small RNA regulator. EMBO J. 23: 396-405.
16. Ghetti, A., Pinol-Roma, S., Michael, W.M., Morandi, C., and Dreyfuss, G. 1992. hnRNP I, the polypyrimidine tract-binding protein: Distinct nuclear localization and association with hnRNAs. Nucleic Acids Res. 20: 3671-3678.
17. Grimm, C., Lund, E., and Dahlberg, J.E. 1997. In vivo selection of RNAs that localize in the nucleus. EMBO J. 16: 793-806.
18. Hellen, C.U., Witherell, G.W., Schmid, M., Shin, S.H., Pestova, T,V., Gil, A., and Wimmer, E. 1993. A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein. Proc. Natl. Acad. Sci. 90: 7642-7646.
19. Herschlag, D. 1995. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270: 20871-20874.
20. Intine, R.V., Sakulich, A.L., Koduru, S.B., Huang, Y., Pierstorff, E., Goodier, J.L., Phan, L., and Maraia, R.J. 2000. Control of transfer RNA maturation by phosphorylation of the human La antigen on serine 366. Mol. Cell 6: 339-348.
21. Izumi, R.E., Valdez, B., Banerjee, R., Srivastava, M., and Dasgupta, A. 2001. Nucleolin stimulates viral internal ribosome entry site-mediated translation. Virus Res. 76: 17-29.
22. James, M.C., Jeffrey, I.W., Pruijn, G.J., Thijssen, J.P., and Clemens, M.J. 1999. Translational control by the La antigen. Structure requirements for rescue of the double-stranded RNA-mediated inhibition of protein synthesis. Eur. J. Biochem. 266: 151-162.
23. Kufel, J., Allmang, C., Chanfreau, G., Petfalski, E., Lafontaine, D.L., and Tollervey, D. 2000. Precursors to the U3 small nucleolar RNA lack small nucleolar RNP proteins but are stabilized by La binding. Mol. Cell. Biol. 20: 5415-5424.
24. Labbe, J.C., Hekimi, S., and Rokeach, L.A. 1999. The levels of the RoRNP-associated Y RNA are dependent upon the presence of ROP-1, the Caenorhabditis elegans Ro60 protein. Genetics 151: 143-150.
25. Labbe, J.C., Burgess, J., Rokeach, L.A., and Hekimi, S. 2000. ROP-1, an RNA quality-control pathway component, affects Caenorhabditis elegans dauer formation. Proc. Natl. Acad. Sci. 97: 13233- 13238.
26. Lin, C.H. and Patton, J.G. 1995. Regulation of alternative 3′ splice site selection by constitutive splicing factors. RNA 1: 234-245.
27. Martinez-Salas, E., Ramos, R., Lafuente, E., and Lopez de Quinto, S. 2001. Functional interactions in internal translation initiation directed by viral and cellular IRES elements. J. Gen. Virol. 82: 973-984.
28. Mayer, O., Waldsich, C., Grossberger, R., and Schroeder, R. 2002. Folding of the td pre-RNA with the help of the RNA chaperone StpA. Biochem. Soc. Trans. 30: 1175-1180.
29. Michelotti, E.F., Michelotti, G.A., Aronsohn, A.I., and Levens, D. 1996. Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol. Cell. Biol. 16: 2350-2360.
30. Mitchell, S.A., Spriggs, K.A., Coldwell, M.J., Jackson, R.J., and Willis, A.E. 2003. The Apaf-1 internal ribosome entry segment attains the correct structural conformation for function via interactions with PTB and unr. Mol. Cell 11: 757-771.
31. O'Brien, C.A. and Wolin, S.L. 1994. A possible role for the 60-kD Ro autoantigen in a discard pathway for defective 5S rRNA precursors. Genes & Dev. 8: 2891-2903.
32. O'Brien, C.A., Margelot, K., and Wolin, S.L. 1993. Xenopus Ro ribonucleoproteins: Members of an evolutionarily conserved class of cytoplasmic ribonucleoproteins. Proc. Natl. Acad. Sci. 90: 7250-7254.
33. Ostareck, D.H., Ostareck-Lederer, A., Wilm, M., Thiele, B.J., Mann, M., and Hentze, M.W. 1997. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89: 597-606.
34. Ostareck-Lederer,A., Ostareck,D.H.,Cans,C.,Neubauer,G.,Bomsztyk,K., Superti-Furga, G., and Hentze, M.W. 2002. c-Src-mediated phosphorylation of hnRNP K drives translational activation of specifically silenced mRNAs. Mol. Cell. Biol. 22: 4535-4543.
35. Pannone, B.K., Xue, D., and Wolin, S.L. 1998. A role for the yeast La protein in U6 snRNP assembly: Evidence that the La protein is a molecular chaperone for RNA polymerase III transcripts. EMBO J. 15: 7442-7453.
36. Peek, R., Pruijn, G.J., van der Kemp, A.J., and van Venrooij, W.J. 1993. Subcellular distribution of Ro ribonucleoprotein complexes and their constituents. J. Cell Sci. 106(Pt 3): 929-935.
37. Pellizzoni, L., Lotti, F., Rutjes, S.A., and Pierandrei-Amaldi, P. 1998. Involvement of the Xenopus laevis Ro60 autoantigen in the alternative interaction of La and CNBP proteins with the 5′UTR of L4 ribosomal protein mRNA. J. Mol. Biol. 281: 593-608.
38. Pichler, A. and Schroeder, R. 2002. Folding problems of the 5′ splice-site containing P1 stem of the group I td intron: Substrate binding inhibition in vitro and mis-splicing in vivo. J. Biol. Chem. 277: 17987-17993.
39. Pickering, B.M., Mitchell, S.A., Spriggs, K.A., Stoneley, M., and Willis, A.E. 2004. Bag-1 internal ribosome entry segment activity is promoted by structural changes mediated by poly(rC) binding protein 1 and recruitment of polypyrimidine tract binding protein 1. Mol. Cell. Biol. 24: 5595-5605.
40. Pruijn, G.J., Slobbe, R.L., van Venrooij, W.J. 1991. Analysis of protein-RNA interactions within Ro ribonucleoprotein complexes. Nucleic Acids Res. 19: 5173-5180.
41. Pruijn, G.J., Wingens, P.A., Peters, S.L., Thijssen, J.P., and van Venrooij, W.J. 1993. Ro RNP associated Y RNAs are highly conserved among mammals. Biochim. Biophys. Acta 1216: 395-401.
42. Pruijn, G.J., Simons, F.H., and van Venrooij, W.J. 1997. Intracellular localization and nucleocytoplasmic transport of Ro RNP components. Eur. J. Cell. Biol. 74: 123-132.
43. Ritchie, S.A., Pasha, M.K., Batten, D.J., Sharma, R.K., Olson, D.J., Ross, A.R., and Bonham, K. 2003. Identification of the SRC pyrimidine-binding protein (SPy) as hnRNP K: Implications in the regulation of SRC1A transcription. Nucleic Acids Res. 31: 1502-1513.
44. Rutjes, S.A., Lund, E., van der Heijden, A., Grimm, C., van Venrooij, W.J., and Pruijn, G.J. 2001. Identification of a novel cis-acting RNA element involved in nuclear export of hY RNAs. RNA 7: 741-752.
45. Salvo, J.L., Coetzee, T., and Belfort, M. 1990. Deletion-tolerance and trans-splicing of the bacteriophage T4 td intron. Analysis of the P6-L6a region. J. Mol. Biol. 211: 537-549.
46. Semrad, K., Green, R., and Schroeder, R. 2004. RNA chaperone activity of large ribosomal subunit proteins from Escherichia coli. RNA 10: 1855-1860.
47. Shi, H., O'Brien, C.A., Van Horn, D.J., and Wolin, S.L. 1996. A misfolded form of 5S rRNA is complexed with the Ro and La autoantigens. RNA 2: 769-784.
48. Simons, F.H., Rutjes, S.A., van Venrooij, W.J., and Pruijn, G.J. 1996. The interactions with Ro60 and La differentially affect nuclear export of hY1 RNA. RNA 2: 264-273.
49. Stoneley, M. and Willis, A.E. 2004. Cellular internal ribosome entry segments: Structures, trans-acting factors and regulation of gene expression. Oncogene 23: 3200-3207.
50. Svitkin, Y.V., Meerovitch, K., Lee, H.S., Dholakia, J.N., Kenan, D.J., Agol, V.I., and Sonenberg, N. 1994. Internal translation initiation on poliovirus RNA: Further characterization of La function in poliovirus translation in vitro. J. Virol. 68: 1544-1550.
51. Takimoto, M., Tomonaga, T., Matunis, M., Avigan, M., Krutzsch, H., Dreyfuss, G., and Levens, D. 1993. Specific binding of heterogeneous ribonucleoprotein particle protein K to the human c-myc promoter, in vitro. J. Biol. Chem. 268: 18249-18258.
52. Wagner, E.J. and Garcia-Blanco, M.A. 2001. Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell. Biol. 21: 3281-3288.
53. Waldsich, C., Grossberger, R., and Schroeder, R. 2002. RNA chaperone StpA loosens interactions of the tertiary structure in the td group I intron in vivo. Genes & Dev. 16: 2300-2312.
54. Weng, Z., Thomas, S.M., Rickles, R.J., Taylor, J.A., Brauer, A.W., Seidel-Dugan, C., Michael, W.M., Dreyfuss, G., and Brugge, J.S. 1994. Identification of Src, Fyn, and Lyn SH3-binding proteins: Implications for a function of SH3 domains. Mol. Cell. Biol. 14: 4509-4521.
55. Wolin, S.L. and Cedervall, T. 2002. The La protein. Annu. Rev. Biochem. 71: 375-403.
56. Wolin, S.L. and Steitz, J.A. 1984. The Ro small cytoplasmic ribonucleoproteins: Identification of the antigenic protein and its binding site on the Ro RNAs. Proc. Natl. Acad. Sci. 81: 1996-2000.
57. Xue, D., Rubinson, D.A., Pannone, B.K., Yoo, C.J., and Wolin, S.L. 2000. U snRNP assembly in yeast involves the La protein. EMBO J. 19: 1650-1660.
58. Xue, D., Shi, H., Smith, J.D., Chen, X., Noe, D.A., Cedervall, T., Yang, D.D., Eynon, E., Brash, D.E., Kashgarian, M., et al. 2003. A lupus-like syndrome develops in mice lacking the Ro 60-kDa protein, a major lupus autoantigen. Proc. Natl. Acad. Sci. 100: 7503-7508.
59. Yoo, C.J. and Wolin, S.L. 1997. The yeast La protein is required for the 3′ endonucleolytic cleavage that matures tRNA precursors. Cell 89: 393-402.
60. Youinou, P., Adler, Y., Muller, S., Lamour, A., Baron, D., and Humbel, R.L. 1994. Anti-Ro(SSA) and anti-La(SSB) antibodies in autoimmune rheumatic diseases. Clin. Rev. Allergy 12: 253-274.
61. Zhang, A., Derbyshire, V., Salvo, J.L., and Belfort, M. 1995. Escherichia coli protein StpA stimulates self-splicing by promoting RNA assembly in vitro. RNA 1: 783-793.