Functional role of the sarcin-ricin loop of the 23s rRNA in the elongation cycle of protein synthesis

Journal of Molecular Biology

Volumn 419, Issue 3-4, 2012, Pages 125-138

  Shi, Xinying ^a   Khade, Prashant K ^a   Sanbonmatsu, Karissa Y ^b   Joseph, Simpson ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

GTP hydrolysis; peptide bond; ribosome; translocation; tRNA selection

Indexed keywords

ELONGATION FACTOR G; ELONGATION FACTOR TU; GUANOSINE TRIPHOSPHATE; MESSENGER RNA; RICIN; RNA 23S; SARCIN RICIN LOOP; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; GENE MUTATION; GENE TRANSLOCATION; HYDROLYSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

EID: 84860767838     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.03.016     Document Type: Article

References (56)

1. Cannone J.J., Subramanian S., Schnare M.N., Collett J.R., D'Souza L.M., and Du Y. The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs BMC Bioinformat. 3 2002 2
2. Endo Y., Huber P.W., and Wool I.G. The ribonuclease activity of the cytotoxin alpha-sarcin. The characteristics of the enzymatic activity of alpha-sarcin with ribosomes and ribonucleic acids as substrates J. Biol. Chem. 258 1983 2662 2667
3. Fernandez-Puentes C., and Vazquez D. Effects of some proteins that inactivate the eukaryotic ribosome FEBS Lett. 78 1977 143 146 (Pubitemid 8138615)
4. Endo Y., and Tsurugi K. RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes J. Biol. Chem. 262 1987 8128 8130 (Pubitemid 17104265)
5. Endo Y., and Wool I.G. The site of action of alpha-sarcin on eukaryotic ribosomes. The sequence at the alpha-sarcin cleavage site in 28 S ribosomal ribonucleic acid J. Biol. Chem. 257 1982 9054 9060
6. Hausner T.P., Atmadja J., and Nierhaus K.H. Evidence that the G2661 region of 23S rRNA is located at the ribosomal binding sites of both elongation factors Biochimie 69 1987 911 923
7. Chan Y.L., and Wool I.G. The integrity of the sarcin/ricin domain of 23 S ribosomal RNA is not required for elongation factor-independent peptide synthesis J. Mol. Biol. 378 2008 12 19
8. Garcia-Ortega L., Alvarez-Garcia E., Gavilanes J.G., Martinez-del-Pozo A., and Joseph S. Cleavage of the sarcin-ricin loop of 23S rRNA differentially affects EF-G and EF-Tu binding Nucleic Acids Res. 38 2010 4108 4119
9. Blanchard S.C., Gonzalez R.L., Kim H.D., Chu S., and Puglisi J.D. tRNA selection and kinetic proofreading in translation Nat. Struct. Mol. Biol. 11 2004 1008 1014 (Pubitemid 39315306)
10. Moazed D., Robertson J.M., and Noller H.F. Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA Nature 334 1988 362 364
11. Munishkin A., and Wool I.G. The ribosome-in-pieces: binding of elongation factor EF-G to oligoribonucleotides that mimic the sarcin/ricin and thiostrepton domains of 23S ribosomal RNA Proc. Natl Acad. Sci. USA 94 1997 12280 12284
12. Schuette J.C., Murphy F.V. t., Kelley A.C., Weir J.R., Giesebrecht J., and Connell S.R. GTPase activation of elongation factor EF-Tu by the ribosome during decoding EMBO J. 28 2009 755 765
13. Villa E., Sengupta J., Trabuco L.G., LeBarron J., Baxter W.T., and Shaikh T.R. Ribosome-induced changes in elongation factor Tu conformation control GTP hydrolysis Proc. Natl Acad. Sci. USA 106 2009 1063 1068
14. Connell S.R., Takemoto C., Wilson D.N., Wang H., Murayama K., and Terada T. Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors Mol. Cell 25 2007 751 764 (Pubitemid 46341918)
15. Valle M., Zavialov A., Sengupta J., Rawat U., Ehrenberg M., and Frank J. Locking and unlocking of ribosomal motions Cell 114 2003 123 134 (Pubitemid 36859846)
16. Taylor D.J., Nilsson J., Merrill A.R., Andersen G.R., Nissen P., and Frank J. Structures of modified eEF2 80S ribosome complexes reveal the role of GTP hydrolysis in translocation EMBO J. 26 2007 2421 2431 (Pubitemid 46685859)
17. Stark H., Rodnina M.V., Wieden H.J., van Heel M., and Wintermeyer W. Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation Cell 100 2000 301 309 (Pubitemid 30353086)
18. Stark H., Rodnina M.V., Wieden H.J., Zemlin F., Wintermeyer W., and van Heel M. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex Nat. Struct. Biol. 9 2002 849 854 (Pubitemid 35257786)
19. Schmeing T.M., Voorhees R.M., Kelley A.C., Gao Y.G., Murphy F.V. t., Weir J.R., and Ramakrishnan V. The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA Science 326 2009 688 694
20. Gao Y.G., Selmer M., Dunham C.M., Weixlbaumer A., Kelley A.C., and Ramakrishnan V. The structure of the ribosome with elongation factor G trapped in the posttranslocational state Science 326 2009 694 699
21. Voorhees R.M., Schmeing T.M., Kelley A.C., and Ramakrishnan V. The mechanism for activation of GTP hydrolysis on the ribosome Science 330 2010 835 838
22. Yu H., Chan Y.L., and Wool I.G. The identification of the determinants of the cyclic, sequential binding of elongation factors Tu and G to the ribosome J. Mol. Biol. 386 2009 802 813
23. Clementi N., Chirkova A., Puffer B., Micura R., and Polacek N. Atomic mutagenesis reveals A2660 of 23S ribosomal RNA as key to EF-G GTPase activation Nat. Chem. Biol. 6 2010 344 351
24. Macbeth M.R., and Wool I.G. The phenotype of mutations of G2655 in the sarcin/ricin domain of 23 S ribosomal RNA J. Mol. Biol. 285 1999 965 975 (Pubitemid 29054310)
25. Macbeth M.R., and Wool I.G. Characterization of in vitro and in vivo mutations in non-conserved nucleotides in the ribosomal RNA recognition domain for the ribotoxins ricin and sarcin and the translation elongation factors J. Mol. Biol. 285 1999 567 580 (Pubitemid 29041793)
26. Leonov A.A., Sergiev P.V., Bogdanov A.A., Brimacombe R., and Dontsova O.A. Affinity purification of ribosomes with a lethal G2655C mutation in 23 S rRNA that affects the translocation J. Biol. Chem. 278 2003 25664 25670 (Pubitemid 36835321)
27. Marchant A., and Hartley M.R. Mutational studies on the alpha-sarcin loop of Escherichia coli 23S ribosomal RNA Eur. J. Biochem. 226 1994 141 147
28. Ali I.K., Lancaster L., Feinberg J., Joseph S., and Noller H.F. Deletion of a conserved, central ribosomal intersubunit RNA bridge Mol. Cell 23 2006 865 874 (Pubitemid 44363047)
29. Youngman E.M., and Green R. Affinity purification of in vivo-assembled ribosomes for in vitro biochemical analysis Methods 36 2005 305 312 (Pubitemid 41074962)
30. Belitsina N.V., and Spirin A.S. Studies on the structure of ribosomes. IV. Participation of aminoacyl-transfer RNA and peptidyl-transfer RNA in the association of ribosomal subparticles J. Mol. Biol. 52 1970 45 55
31. Garcia-Ortega L., Stephen J., and Joseph S. Precise alignment of peptidyl tRNA by the decoding center is essential for EF-G-dependent translocation Mol. Cell 32 2008 292 299
32. Daviter T., Wieden H.J., and Rodnina M.V. Essential role of histidine 84 in elongation factor Tu for the chemical step of GTP hydrolysis on the ribosome J. Mol. Biol. 332 2003 689 699 (Pubitemid 37075990)
33. Pape T., Wintermeyer W., and Rodnina M.V. Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E. coli ribosome EMBO J. 17 1998 7490 7497 (Pubitemid 29002715)
34. Ledoux S., and Uhlenbeck O.C. Different aa-tRNAs are selected uniformly on the ribosome Mol. Cell 31 2008 114 123 (Pubitemid 351905919)
35. Cochella L., and Green R. An active role for tRNA in decoding beyond codon:anticodon pairing Science 308 2005 1178 1180 (Pubitemid 40696436)
36. Kothe U., and Rodnina M.V. Codon reading by tRNAAla with modified uridine in the wobble position Mol. Cell 25 2007 167 174 (Pubitemid 46049055)
37. Hetrick B., Khade P.K., Lee K., Stephen J., Thomas A., and Joseph S. Polyamines accelerate codon recognition by transfer RNAs on the ribosome Biochemistry 49 2010 7179 7189
38. Dix D.B., Wittenberg W.L., Uhlenbeck O.C., and Thompson R.C. Effect of replacing uridine 33 in yeast tRNAPhe on the reaction with ribosomes J. Biol. Chem. 261 1986 10112 10118 (Pubitemid 17221944)
39. Lancaster L., Lambert N.J., Maklan E.J., Horan L.H., and Noller H.F. The sarcin-ricin loop of 23S rRNA is essential for assembly of the functional core of the 50S ribosomal subunit RNA 14 2008 1999 2012
40. Joseph S., and Noller H.F. EF-G-catalyzed translocation of anticodon stem-loop analogs of transfer RNA in the ribosome EMBO J. 17 1998 3478 3483 (Pubitemid 28279520)
41. Studer S.M., Feinberg J.S., and Joseph S. Rapid kinetic analysis of EF-G-dependent mRNA translocation in the ribosome J. Mol. Biol. 327 2003 369 381 (Pubitemid 36298708)
42. Walker S.E., Shoji S., Pan D., Cooperman B.S., and Fredrick K. Role of hybrid tRNA-binding states in ribosomal translocation Proc. Natl Acad. Sci. USA 105 2008 9192 9197
43. Ermolenko D.N., and Noller H.F. mRNA translocation occurs during the second step of ribosomal intersubunit rotation Nat. Struct. Mol. Biol. 18 2011 457 462
44. Khade P.K., and Joseph S. Messenger RNA interactions in the decoding center control the rate of translocation Nat. Struct. Mol. Biol. 18 2011 1300 1302
45. Ban N., Nissen P., Hansen J., Moore P.B., and Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution Science 289 2000 905 920 (Pubitemid 30659939)
46. Correll C.C., Munishkin A., Chan Y.L., Ren Z., Wool I.G., and Steitz T.A. Crystal structure of the ribosomal RNA domain essential for binding elongation factors Proc. Natl Acad. Sci. USA 95 1998 13436 13441 (Pubitemid 28522990)
47. Szewczak A.A., Moore P.B., Chang Y.L., and Wool I.G. The conformation of the sarcin/ricin loop from 28S ribosomal RNA Proc. Natl Acad. Sci. USA 90 1993 9581 9585 (Pubitemid 23315829)
48. Voorhees R.M., Schmeing T.M., Kelley A.C., and Ramakrishnan V. Response to comment on "the mechanism for activation of GTP hydrolysis on the ribosome" Science 333 2011 37
49. Liljas A., Ehrenberg M., and Aqvist J. Comment on "the mechanism for activation of GTP hydrolysis on the ribosome" Science 333 2011 37
50. Agrawal R.K., Heagle A.B., Penczek P., Grassucci R.A., and Frank J. EF-G-dependent GTP hydrolysis induces translocation accompanied by large conformational changes in the 70S ribosome Nat. Struct. Biol. 6 1999 643 647 (Pubitemid 29318953)
51. Frank J., and Agrawal R.K. A ratchet-like inter-subunit reorganization of the ribosome during translocation Nature 406 2000 318 322 (Pubitemid 30604411)
52. Ratje A.H., Loerke J., Mikolajka A., Brunner M., Hildebrand P.W., and Starosta A.L. Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites Nature 468 2010 713 716
53. Shi X., Chiu K., Ghosh S., and Joseph S. Bases in 16S rRNA important for subunit association, tRNA binding, and translocation Biochemistry 48 2009 6772 6782
54. 32P]-labeling tRNA with nucleotidyltransferase for assaying aminoacylation and peptide bond formation Methods 44 2008 74 80 (Pubitemid 351172805)
55. Fahlman R.P., and Uhlenbeck O.C. Contribution of the esterified amino acid to the binding of aminoacylated tRNAs to the ribosomal P- and A-sites Biochemistry 43 2004 7575 7583 (Pubitemid 38745773)
56. Ticu C., Nechifor R., Nguyen B., Desrosiers M., and Wilson K.S. Conformational changes in switch I of EF-G drive its directional cycling on and off the ribosome EMBO J. 28 2009 2053 2065