SRP RNA provides the physiologically essential GTPase activation function in cotranslational protein targeting

RNA

Volumn 13, Issue 2, 2007, Pages 240-250

  Siu, Fai Y ^a   Spanggord, Richard J ^a   Doudna, Jennifer A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

4.5S RNA; GNRA tetraloop; GTPase activating protein; Signal recognition particle; SRP receptor

Indexed keywords

DOCKING PROTEIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; SIGNAL RECOGNITION PARTICLE;

ARTICLE; BINDING AFFINITY; CELL GROWTH; CELL VIABILITY; COMPLEX FORMATION; ENZYME ACTIVATION; ENZYME ACTIVITY; HYDROLYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TARGETING; RNA BINDING; RNA TRANSLATION;

BACTERIAL PROTEINS; CARRIER PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; GTP PHOSPHOHYDROLASES; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, BACTERIAL; RNA, RIBOSOMAL; SIGNAL RECOGNITION PARTICLE;

EID: 33846456974     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.135407     Document Type: Article

References (38)

1. Allain, F.H. and Varani, G. 1995. Structure of the P1 helix from group I self-splicing introns. J. Mol. Biol. 250: 333-353.
2. Antao, V.P., Lai, S.Y., and Tinoco Jr., I. 1991. A thermodynamic study of unusually stable RNA and DNA hairpins. Nucleic Acids Res. 19: 5901-5905.
3. Batey, R.T. and Doudna, J.A. 2002. Structural and energetic analysis of metal ions essential to SRP signal recognition domain assembly. Biochemistry 41: 11703-11710.
4. Batey, R.T., Rambo, R.P., Lucast, L., Rha, B., and Doudna, J.A. 2000. Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science 287: 1232-1239.
5. Batey, R.T., Sagar, M.B., and Doudna, J.A. 2001. Structural and energetic analysis of RNA recognition by a universally conserved protein from the signal recognition particle. J. Mol. Biol. 307: 229-246.
6. Brown, S. and Fournier, M.J. 1984. The 4.5 S RNA gene of Escherichia coli is essential for cell growth. J. Mol. Biol. 178: 533-550.
7. Brown, S., Thon, G., and Tolentino, E. 1989. Genetic selection and DNA sequences of 4.5S RNA homologs. J. Bacteriol. 171: 6517-6520.
8. Buskiewicz, I., Peske, F., Wieden, H.J., Gryczynski, I., Rodnina, M.V., and Wintermeyer, W. 2005. Conformations of the signal recognition particle protein Ffh from Escherichia coli as determined by FRET. J. Mol. Biol. 351: 417-430.
9. Butcher, S.E., Dieckmann, T., and Feigon, J. 1997. Solution structure of the conserved 16 S-like ribosomal RNA UGAA tetraloop. J. Mol. Biol. 268: 348-358.
10. Cheong, C., Varani, G., and Tinoco Jr., I. 1990. Solution structure of an unusually stable RNA hairpin, 5′GGAC(UUCG)GUCC. Nature 346: 680-682.
11. Doudna, J.A. and Batey, R.T. 2004. Structural insights into the signal recognition particle. Annu. Rev. Biochem. 73: 539-557.
12. Egea, P.F., Shan, S.O., Napetschnig, J., Savage, D.F., Walter, P., and Stroud, R.M. 2004. Substrate twinning activates the signal recognition particle and its receptor. Nature 427: 215-221.
13. Ennifar, E., Nikulin, A., Tishchenko, S., Serganov, A., Nevskaya, N., Garber, M., Ehresmann, B., Ehresmann, C., Nikonov, S., and Dumas, P. 2000. The crystal structure of UUCG tetraloop. J. Mol. Biol. 304: 35-42.
14. Focia, P.J., Shepotinovskaya, I.V., Seidler, J.A., and Freymann, D.M. 2004. Heterodimeric GTPase core of the SRP targeting complex. Science 303: 373-377.
15. Focia, P.J., Gawronski-Salerno, J., Coon, J.S.T., and Freymann, D.M. 2006. Structure of a GDP:AlF4 complex of the SRP GTPases Ffh and FtsY, and identification of a peripheral nucleotide interaction site. J. Mol. Biol. 360: 631-643.
16. Gu, S.Q., Jockel, J., Beinker, P., Warnecke, J., Semenkov, Y.P., Rodnina, M.V., and Wintermeyer, W. 2005. Conformation of 4.5S RNA in the signal recognition particle and on the 30S ribosomal subunit. RNA 11: 1374-1384.
17. Heus, H.A. and Pardi, A. 1991. Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops. Science 253: 191-194.
18. Jagath, J.R., Matassova, N.B., de Leeuw, E., Warnecke, J.M., Lentzen, G., Rodnina, M.V., Luirink, J., and Wintermeyer, W. 2001. Important role of the tetraloop region of 4.5S RNA in SRP binding to its receptor FtsY. RNA 7: 293-301.
19. Jensen, C.G. and Pedersen, S. 1994. Concentrations of 4.5S RNA and Ffh protein in Escherichia coli: The stability of Ffh protein is dependent on the concentration of 4.5S RNA. J. Bacteriol. 176: 7148-7154.
20. Joseph, S. and Noller, H.F. 2000. Directed hydroxyl radical probing using iron(II) tethered to RNA. Methods Enzymol. 318: 175-190.
21. Jucker, F.M., Heus, H.A., Yip, P.F., Moors, E.H., and Pardi, A. 1996. A network of heterogeneous hydrogen bonds in GNRA tetraloops. J. Mol. Biol. 264: 968-980.
22. Karbstein, K., Jonas, S., and Doudna, J.A. 2005. An essential GTPase promotes assembly of preribosomal RNA processing complexes. Mol. Cell 20: 633-643.
23. Lentzen, G., Moine, H., Ehresmann, C., Ehresmann, B., and Wintermeyer, W. 1996. Structure of 4.5S RNA in the signal recognition particle of Escherichia coli as studied by enzymatic and chemical probing. RNA 2: 244-253.
24. Peluso, P., Herschlag, D., Nock, S., Freymann, D.M., Johnson, A.E., and Walter, P. 2000. Role of 4.5S RNA in assembly of the bacterial signal recognition particle with its receptor. Science 288: 1640-1643.
25. Peluso, P., Shan, S.O., Nock, S., Herschlag, D., and Walter, P. 2001. Role of SRP RNA in the GTPase cycles of Ffh and FtsY. Biochemistry 40: 15224-15233.
26. Powers, T. and Walter, P. 1995. Reciprocal stimulation of GTP hydrolysis by two directly interacting GTPases. Science 269: 1422-1424.
27. Rosenblad, M.A., Gorodkin, J., Knudsen, B., Zwieb, C., and Samuelsson, T. 2003. SRPDB: Signal recognition particle database. Nucleic Acids Res. 31: 363-364.
28. Rosendal, K.R., Wild, K., Montoya, G., and Sinning, I. 2003. Crystal structure of the complete core of archaeal signal recognition particle and implications for interdomain communication. Proc. Natl. Acad. Sci. 100: 14701-14706.
29. Sagar, M.B., Lucast, L., and Doudna, J.A. 2004. Conserved but nonessential interaction of SRP RNA with translation factor EF-G. RNA 10: 772-778.
30. Shan, S.O. and Walter, P. 2003. Induced nucleotide specificity in a GTPase. Proc. Natl. Acad. Sci. 100: 4480-4485.
31. Shan, S.O. and Walter, P. 2005a. Co-translational protein targeting by the signal recognition particle. FEBS Lett. 579: 921-926.
32. Shan, S.O. and Walter, P. 2005b. Molecular crosstalk between the nucleotide specificity determinant of the SRP GTPase and the SRP receptor. Biochemistry 44: 6214-6222.
33. Shan, S.O., Stroud, R.M., and Walter, P. 2004. Mechanism of association and reciprocal activation of two GTPases. PLoS Biol. 2: e320.
34. Shepotinovskaya, I.V., Focia, P.J., and Freymann, D.M. 2003. Crystallization of the GMPPCP complex of the NG domains of Thermus aquaticus Ffh and FtsY. Acta Crystallogr. 59: 1834-1837.
35. Spanggord, R.J., Siu, F., Ke, A., and Doudna, J.A. 2005. RNA-mediated interaction between the peptide-binding and GTPase domains of the signal recognition particle. Nat. Struct. Mol. Biol. 12: 1116-1122.
36. Tian, H. and Beckwith, J. 2002. Genetic screen yields mutations in genes encoding all known components of the Escherichia coli signal recognition particle pathway. J. Bacteriol. 184: 111-118.
37. Williams, D.J. and Hall, K.B. 2000. Experimental and computational studies of the G[UUCG]C RNA tetraloop. J. Mol. Biol. 297: 1045-1061.
38. Wu, S., Ke, A., and Doudna, J.A. 2006. A fast and efficient procedure to produce scFvs specific for large macromolecular complexes. J. Immunol. Methods ePub # 17126854.