The La protein functions redundantly with tRNA modification enzymes to ensure tRNA structural stability

RNA

Volumn 12, Issue 4, 2006, Pages 644-654

  Copela, Laura A ^a   Chakshusmathi, Ghadiyaram ^a   Sherrer, R Lynn ^a   Wolin, Sandra L ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aminoacyl tRNA synthetase; La protein; RNA stability; Subcellular localization; tRNA; tRNA modification

Indexed keywords

LA ANTIGEN; TRANSFER RNA;

ARTICLE; ENZYME MODIFICATION; IN SITU HYBRIDIZATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA STABILITY; SACCHAROMYCES CEREVISIAE; YEAST; YEAST CELL;

AMINO ACYL-TRNA SYNTHETASES; BASE SEQUENCE; BLOTTING, NORTHERN; DNA PRIMERS; IN SITU HYBRIDIZATION; MUTAGENESIS; NUCLEIC ACID CONFORMATION; PLASMIDS; RNA, TRANSFER, ARG; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRNA METHYLTRANSFERASES;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 33645473067     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2307206     Document Type: Article

References (55)

1. Alexandrov, A., Chernyakov, I., Gu, W., Hiley, S.L., Hughes, T.R., Grayhack, E.J., and Phizicky, E.M. 2006. Rapid tRNA decay can result from lack of nonessential modifications. Mol. Cell 21: 87-96.
2. Anderson, J., Phan, L., Cuesta, R., Carlson, B.A., Pak, M., Asano, K., Bjork, G.R., Tamame, M., and Hinnebusch, A.G. 1998. The essential Gcd10p-Gcd14p nuclear complex is required for 1-methyladenosine modification and maturation of initiator methionyl-tRNA. Genes & Dev. 12: 3650-3662.
3. Arhin, G.K., Shen, S., Perez, I.F., Tschudi, C., and Ullu, E. 2005. Downregulation of the essential Trypanosoma brucei La protein affects accumulation of elongator methionyl-tRNA. Mol. Biochem. Parasitol. 144: 104-108.
4. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. 1998. Current protocols in molecular biology. John Wiley & Sons, New York.
5. Bai, C. and Tolias, P.P. 2000. Genetic analysis of a La homolog in Drosophila melanogaster. Nucleic Acids Res. 28: 1078-1084.
6. Becker, H.F., Motorin, Y., Planta, R.J., and Grosjean, H. 1997. The yeast gene YNL292w encodes a pseudouridine synthase (Pus4) catalyzing the formation of psi55 in both mitochondrial and cytoplasmic tRNAs. Nucleic Acids Res. 25: 4493-4499.
7. Calvo, O., Cuesta, R., Anderson, J., Gutierrez, N., Garcia-Barrio, M.T., Hinnebusch, A.G., and Tamame, M. 1999. GCD14p, a repressor of GCN4 translation, cooperates with Gcd10p and Lhp1p in the maturation of initiator methionyl-tRNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 4167-4181.
8. Cavaille, J., Chetouani, F., and Bachellerie, J.P. 1999. The yeast Saccharomyces cerevisiae YDL112w ORF encodes the putative 2′-O-ribose methyltransferase catalyzing the formation of Gm18 in tRNAs. RNA 5: 66-81.
9. 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.
10. Delagoutte, B., Moras, D., and Cavarelli, J. 2000. tRNA aminoacylation by arginyl-tRNA synthetase: Induced conformations during substrates binding. EMBO J. 19: 5599-5610.
11. Edqvist, J., Blomqvist, K., and Straby, K.B. 1994. Structural elements in yeast tRNAs required for homologous modification of guanosine-26 into dimethylguanosine-26 by the yeast Trm1 tRNA-modifying enzyme. Biochemistry 33: 9546-9551.
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. Fender, A., Geslain, R., Eriani, G., Giege, R., Sissler, M., and Florentz, C. 2004. A yeast arginine specific tRNA is a remnant aspartate acceptor. Nucleic Acids Res. 32: 5076-5086.
14. Fernandez, C.F., Pannone, B.K., Chen, X., Fuchs, G., and Wolin, S.L. 2004. An Lsm2-Lsm7 complex in Saccharomyces cerevisiae associates with the small nucleolar RNA snR5. Mol. Biol. Cell 15: 2842-2852.
15. Foldynova-Trantirkova, S., Paris, Z., Sturm, N.R., Campbell, D.A., and Lukes, J. 2005. The Trypanosoma brucei La protein is a candidate poly(U) shield that impacts spliced leader RNA maturation and tRNA intron removal. Int. J. Parasitol. 35: 359-366.
16. Grosshans, H., Hurt, E., and Simos, G. 2000. An aminoacylation-dependent nuclear tRNA export pathway in yeast. Genes & Dev. 14: 830-840.
17. Grosshans, H., Lecointe, F., Grosjean, H., Hurt, E., and Simos, G. 2001. Pus1p-dependent tRNA pseudouridinylation becomes essential when tRNA biogenesis is compromised in yeast. J. Biol. Chem. 276: 46333-46339.
18. Hall, K.B., Sampson, J.R., Uhlenbeck, O.C., and Redfield, A.G. 1989. Structure of an unmodified tRNA molecule. Biochemistry 28: 5794-5801.
19. Hoang, C. and Ferre-D'Amare, A.R. 2001. Cocrystal structure of a tRNA Psi55 pseudouridine synthase: Nucleotide flipping by an RNA-modifying enzyme. Cell 107: 929-939.
20. Hopper, A.K. and Phizicky, E.M. 2003. tRNA transfers to the lime-light. Genes & Dev. 17: 162-180.
21. Hopper, A.K., Furukawa, A.H., Pham, H.D., and Martin, N.C. 1982. Defects in modification of cytoplasmic and mitochondrial transfer RNAs are caused by single nuclear mutations. Cell 28: 543-550.
22. Huang, L., Pookanjanatavip, M., Gu, X., and Santi, D.V. 1998. A conserved aspartate of tRNA pseudouridine synthase is essential for activity and a probable nucleophilic catalyst. Biochemistry 37: 344-351.
23. Huh, W.K., Falvo, J.V., Gerke, L.C., Carroll, A.S., Howson, R.W., Weissman, J.S., and O'Shea, E.K. 2003. Global analysis of protein localization in budding yeast. Nature 425: 686-691.
24. Inada, M. and Guthrie, C. 2004. Identification of Lhp1p-associated RNAs by microarray analysis in Saccharomyces cerevisiae reveals association with coding and noncoding RNAs. Proc. Nat. Acad. Sci. 101: 434-439.
25. Johansson, M.J. and Bystrom, A.S. 2002. Dual function of the tRNA(m(5)U54)methyltransferase in tRNA maturation. RNA 8: 324-335.
26. Kadaba, S., Krueger, A., Trice, T., Krecic, A.M., Hinnebusch, A.G., and Anderson, J. 2004. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes & Dev. 18: 1227-1240.
27. 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.
28. LaCava, J., Houseley, J., Saveanu, C., Petfalski, E., Thompson, E., Jacquier, A., and Tollervey, D. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121: 713-724.
29. Lecointe, F., Simos, G., Sauer, A., Hurt, E.C., Motorin, Y., and Grosjean, H. 1998. Characterization of yeast protein Deg1 as pseudouridine synthase (Pus3) catalyzing the formation of psi 38 and psi 39 in tRNA anticodon loop. J. Biol. Chem. 273: 1316-1323.
30. Lecointe, F., Namy, O., Hatin, I., Simos, G., Rousset, J.P., and Grosjean, H. 2002. Lack of pseudouridine 38/39 in the anticodon arm of yeast cytoplasmic tRNA decreases in vivo recoding efficiency. J. Biol. Chem. 277: 30445-30453.
31. Long, K.S., Cedervall, T., Walch-Solimena, C., Noe, D.A., Huddleston, M.J., Annan, R.S., and Wolin, S.L. 2001. Phosphorylation of the Saccharomyces cerevisiae La protein does not appear to be required for its functions in tRNA maturation and nascent RNA stabilization. RNA 7: 1589-1602.
32. Longtine, M.S., McKenzie III, A., Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J.R. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
33. Lund, E. and Dahlberg, J.E. 1998. Proofreading and aminoacylation of tRNAs before export from the nucleus. Science 282: 2082-2085.
34. Maglott, E.J., Deo, S.S., Przykorska, A., and Glick, G.D. 1998. Conformational transitions of an unmodified tRNA: Implications for RNA folding. Biochemistry 37: 16349-16359.
35. Motorin, Y., Keith, G., Simon, C., Foiret, D., Simos, G., Hurt, E., and Grosjean, H. 1998. The yeast tRNA:pseudouridine synthase Pus1p displays a multisite substrate specificity. RNA 4: 856-869.
36. Nishikura, K. and De Robertis, E.M. 1981. RNA processing in microinjected Xenopus oocytes. Sequential addition of base modifications in a spliced transfer RNA. J. Mol. Biol. 145: 405-420.
37. 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. 17: 7442-7453.
38. Pannone, B.K., Kim, S.D., Noe, D.A., and Wolin, S.L. 2001. Multiple functional interactions between components of the Lsm2-Lsm8 complex, U6 snRNA, and the yeast La protein. Genetics 158: 187-196.
39. Purushothaman, S.K., Bujnicki, J.M., Grosjean, H., and Lapeyre, B. 2005. Trm11p and Trm112p are both required for the formation of 2-methylguanosine at position 10 in yeast tRNA. Mol. Cell. Biol. 25: 4359-4370.
40. Rose, A.M., Belford, H.G., Shen, W.C., Greer, C.L., Hopper, A.K., and Martin, N.C. 1995. Location of N2,N2-dimethylguanosine-specific tRNA methyltransferase. Biochimie 77: 45-53.
41. Sarkar, S., Azad, A.K., and Hopper, A.K. 1999. Nuclear tRNA aminoacylation and its role in nuclear export of endogenous tRNAs in Saccharomyces cerevisiae. Proc. Nat. Acad. Sci. 96: 14366-14371.
42. Phe. Nucleic Acids Res. 26: 2723-2728.
43. Shaheen, H.H. and Hopper, A.K. 2005. Retrograde movement of tRNAs from the cytoplasm to the nucleus in Saccharomyces cerevisiae. Proc. Nat. Acad. Sci. 102: 11290-11295.
44. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194: 3-21.
45. Sikorski, R.S. and Hieter, P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccaromyces cerevisiae. Genetics 122: 19-27.
46. Steinberg, S. and Cedergren, R. 1995. A correlation between N2-dimethylguanosine presence and alternate tRNA conformers. RNA 1: 886-891.
47. Takano, A., Endo, T., and Yoshihisa, T. 2005. tRNA actively shuttles between the nucleus and cytosol in yeast. Science 309: 140-142.
48. Van Horn, D.J., Yoo, C.J., Xue, D., Shi, H., and Wolin, S.L. 1997. The La protein in Schizosaccharomyces pombe: A conserved yet dispensable phosphoprotein that functions in tRNA maturation. RNA 3: 1434-1443.
49. Varshney, U., Lee, C.P., and RajBhandary, U.L. 1991. Direct analsysis of aminoacylation levels of tRNAs in vivo. Application to studying recognition of Escherichia coli initiator tRNA mutants by glutaminyl-tRNA synthetase. J. Biol. Chem. 266: 24712-24718.
50. Vermeulen, A., McCallum, S.A., and Pardi, A. 2005. Comparison of the global structure and dynamics of native and unmodified tRNA-val. Biochemistry 44: 6024-6033.
51. Wolin, S.L. and Cedervall, T. 2002. The La protein. Annu. Rev. Biochem. 71: 375-402.
52. Wyers, F., Rougemaille, M., Badis, G., Rousselle, J.-C., Dufour, M.-E., Boulay, J., Regnault, B., Devaux, F., Namane, A., Seraphin, B., et al. 2005. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737.
53. 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.
54. Yoo, C.J. and Wolin, S.L. 1994. La proteins from Drosophila melanogaster and Saccharomyces cerevisiae: A yeast homolog of the La autoantigen is dispensable for growth. Mol. Cell. Biol. 14: 5412-5424.
55. _. 1997. The yeast La protein is required for the 3′ endonucleolytic cleavage that matures tRNA precursors. Cell 89: 393-402.