rRNA suppressor of a eukaryotic translation initiation factor 5B/initiation factor 2 mutant reveals a binding site for translational GTPases on the small ribosomal subunit∇

Molecular and Cellular Biology

Volumn 29, Issue 3, 2009, Pages 808-821

  Shin, Byung Sik ^a   Kim, Joo Ran ^a   Acker, Michael G ^b   Maher, Kathryn N ^a   Lorsch, Jon R ^b   Dever, Thomas E ^a,c  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR; GUANOSINE TRIPHOSPHATASE; HISTIDINE; HYDROXYL RADICAL; INITIATION FACTOR 2; INITIATION FACTOR 5A; INITIATION FACTOR 5B; RNA 18S; UNCLASSIFIED DRUG; ELONGATION FACTOR 1; FUN12 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL GROWTH; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; SMALL RIBOSOMAL SUBUNIT; SUPPRESSOR GENE; TRANSLATION INITIATION; YEAST CELL; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENE REPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF; PROTEIN SYNTHESIS; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

EUKARYOTA;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BASE SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; EUKARYOTIC INITIATION FACTOR-2; GENES, SUPPRESSOR; GTP PHOSPHOHYDROLASES; HISTIDINE; HYDROXYL RADICAL; MOLECULAR SEQUENCE DATA; PEPTIDE ELONGATION FACTOR 1; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; RIBOSOME SUBUNITS, SMALL; RNA, RIBOSOMAL, 18S; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPPRESSION, GENETIC;

EID: 59249086519     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00896-08     Document Type: Article

References (57)

1. Abel, K., and F. Jurnak. 1996. A complex profile of protein elongation: translating chemical energy into molecular movement. Structure 4:229-238.
2. Agrawal, R. K., P. Penczek, R. A. Grassucci, and J. Frank. 1998. Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc. Natl. Acad. Sci. USA 95:6134-6138.
3. Allen, G. S., A. Zavialov, R. Gursky, M. Ehrenberg, and J. Frank. 2005. The cryo-EM structure of a translation initiation complex from Escherichia coli. Cell 121:703-712.
4. Andersen, G. R., and J. Nyborg. 2001. Structural studies of eukaryotic elongation factors. Cold Spring Harbor Symp. Quant. Biol. 66:425-437.
5. Antoun, A., M. Y. Pavlov, K. Andersson, T. Tenson, and M. Ehrenberg. 2003. The roles of initiation factor 2 and guanosine triphosphate in initiation of protein synthesis. EMBO J. 22:5593-5601.
6. Asano, K., J. Clayton, A. Shalev, and A. G. Hinnebusch. 2000. A multifactor complex of eukaryotic initiation factors, eIF1, eIF2, eIF3, eIF5, and initiator tRNA(Met) is an important translation initiation intermediate in vivo. Genes Dev. 14:2534-2546.
7. Ban, N., P. Nissen, J. Hansen, P. B. Moore, and T. A. Steitz. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289:905-920.
8. Beckmann, R., C. M. Spahn, N. Eswar, J. Helmers, P. A. Penczek, A. Sali, J. Frank, and G. Blobel. 2001. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107:361-372.
9. Berchtold, H., L. Reshetnikova, C. O. Reiser, N. K. Schirmer, M. Sprinzl, and R. Hilgenfeld. 1993. Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature 365:126-132.
10. Bourne, H. R., D. A. Sanders, and F. McCormick. 1991. The GTPase super-family: conserved structure and molecular mechanism. Nature 349:117-127.
11. Cate, J. H., M. M. Yusupov, G. Z. Yusupova, T. N. Earnest, and H. F. Noller. 1999. X-ray crystal structures of 70S ribosome functional complexes. Science 285:2095-2104.
12. Choi, S. K., D. S. Olsen, A. Roll-Mecak, A. Martung, K. L. Remo, S. K. Burley, A. G. Hinnebusch, and T. E. Dever. 2000. Physical and functional interaction between the eukaryotic orthologs of prokaryotic translation initiation factors IF1 and IF2. Mol. Cell. Biol. 20:7183-7191.
13. Connell, S. R., C. Takemoto, D. N. Wilson, H. Wang, K. Murayama, T. Terada, M. Shirouzu, M. Rost, M. Schuler, J. Giesebrecht, M. Dabrowski, T. Mielke, P. Fucini, S. Yokoyama, and C. M. Spahn. 2007. Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors. Mol. Cell 25:751-764.
14. DeLano, W. 2004. The PyMol user's manual. DeLano Scientific, San Carlos, CA.
15. Diaconu, M., U. Kothe, F. Schlunzen, N. Fischer, J. M. Harms, A. G. Tonevitsky, H. Stark, M. V. Rodnina, and M. C. Wahl. 2005. Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell 121:991-1004.
16. Dinman, J. D., and T. G. Kinzy. 1997. Translational misreading: mutations in translation elongation factor 1alpha differentially affect programmed ribosomal frameshifting and drug sensitivity. RNA 3:870-881.
17. Ditzelmuller, G., W. Wohrer, C. P. Kubicek, and M. Rohr. 1983. Nucleotide pools of growing, synchronized and stressed cultures of Saccharomyces cerevisiae. Arch. Microbiol. 135:63-67.
18. Duisterwinkel, F. J., B. Kraal, J. M. De Graaf, A. Talens, L. Bosch, G. W. Swart, A. Parmeggiani, T. F. La Cour, J. Nyborg, and B. F. Clark. 1984. Specific alterations of the EF-Tu polypeptide chain considered in the light of its three-dimensional structure. EMBO J. 3:113-120.
19. Fringer, J. M., M. G. Acker, C. A. Fekete, J. R. Lorsch, and T. E. Dever. 2007. Coupled release of eukaryotic translation initiation factors 5B and 1A from 80S ribosomes following subunit joining. Mol. Cell. Biol. 27:2384-2397.
20. Gao, H., Z. Zhou, U. Rawat, C. Huang, L. Bouakaz, C. Wang, Z. Cheng, Y. Liu, A. Zavialov, R. Gursky, S. Sanyal, M. Ehrenberg, J. Frank, and H. Song. 2007. RF3 induces ribosomal conformational changes responsible for dissociation of class I release factors. Cell 129:929-941.
21. Harger, J. W., and J. D. Dinman. 2003. An in vivo dual-luciferase assay system for studying translational recoding in the yeast Saccharomyces cerevisiae. RNA 9:1019-1024.
22. Heilek, G. M., R. Marusak, C. F. Meares, and H. F. Noller. 1995. Directed hydroxyl radical probing of 16S rRNA using Fe(II) tethered to ribosomal protein S4. Proc. Natl. Acad. Sci. USA 92:1113-1116.
23. Jorgensen, R., P. A. Ortiz, A. Carr-Schmid, P. Nissen, T. G. Kinzy, and G. R. Andersen. 2003. Two crystal structures demonstrate large conformational changes in the eukaryotic ribosomal translocase. Nat. Struct. Biol. 10:379-385.
24. Katunin, V. I., A. Savelsbergh, M. V. Rodnina, and W. Wintermeyer. 2002. Coupling of GTP hydrolysis by elongation factor G to translocation and factor recycling on the ribosome. Biochemistry 41:12806-12812.
25. Kisselev, L., M. Ehrenberg, and L. Frolova. 2003. Termination of translation: interplay of mRNA, rRNAs and release factors? EMBO J. 22:175-182.
26. Kjeldgaard, M., P. Nissen, S. Thirup, and J. Nyborg. 1993. The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure 1:35-50.
27. Klaholz, B. P., A. G. Myasnikov, and M. Van Heel. 2004. Visualization of release factor 3 on the ribosome during termination of protein synthesis. Nature 427:862-865.
28. Kong, C., K. Ito, M. A. Walsh, M. Wada, Y. Liu, S. Kumar, D. Barford, Y. Nakamura, and H. Song. 2004. Crystal structure and functional analysis of the eukaryotic class II release factor eRF3 from S. pombe. Mol. Cell 14: 233-245.
29. La Teana, A., C. Gualerzi, and A. Dahlberg. 2001. Initiationfactor IF2 binds the α-sarcin loop and helix 89 of Escherichia coli 23S ribosomal RNA. RNA 7:1173-1179.
30. Lee, J. H., T. V. Pestova, B. S. Shin, C. Cao, S. K. Choi, and T. E. Dever. 2002. Initiation factor eIF5B catalyzes second GTP-dependent step in eukaryotic translation initiation. Proc. Natl. Acad. Sci. USA 99:16689-16694.
31. Marzi, S., W. Knight, L. Brandi, E. Caserta, N. Soboleva, W. E. Hill, C. O. Gualerzi, and J. S. Lodmell. 2003. Ribosomal localization of translation initiation factor IF2. RNA 9:958-969.
32. Muldoon-Jacobs, K. L., and J. D. Dinman. 2006. Specific effects of ribosome - tethered molecular chaperones on programmed-1 ribosomal frameshifting. Eukaryot. Cell 5:762-770.
33. Myasnikov, A. G., S. Marzi, A. Simonetti, A. M. Giuliodori, C. O. Gualerzi, G. Yusupova, M. Yusupov, and B. P. Klaholz. 2005. Conformational transition of initiation factor 2 from the GTP- to GDP-bound state visualized on the ribosome. Nat. Struct. Mol. Biol. 12:1145-1149.
34. Nielsen, P. J., and E. H. McConkey. 1980. Evidence for control of protein synthesis in HeLa cells via the elongation rate. J. Cell Physiol. 104:269-281.
35. Ortiz, P. A., R. Ulloque, G. K. Kihara, H. Zheng, and T. G. Kinzy. 2006. Translation elongation factor 2 anticodon mimicry domain mutants affect fidelity and diphtheria toxin resistance. J. Biol. Chem. 281:32639-32648.
36. Pestova, T. V., I. B. Lomakin, J. H. Lee, S. K. Choi, T. E. Dever, and C. U. Hellen. 2000. The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403:332-335.
37. Ramakrishnan, V. 2002. Ribosome structure and the mechanism of translation. Cell 108:557-572.
38. Rodnina, M. V., and W. Wintermeyer. 2001. Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms. Annu. Rev. Biochem. 70:415-435.
39. Roll-Mecak, A., C. Cao, T. E. Dever, and S. K. Burley. 2000. X-ray structures of the universal translation initiation factor IF2/eIF5B: conformational changes on GDP and GTP binding. Cell 103:781-792.
40. Roll-Mecak, A., B. S. Shin, T. E. Dever, and S. K. Burley. 2001. Engaging the ribosome: universal IFs of translation. Trends Biochem. Sci. 26:705-709.
41. Shenton, D., J. B. Smirnova, J. N. Selley, K. Carroll, S. J. Hubbard, G. D. Pavitt, M. P. Ashe, and C. M. Grant. 2006. Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. J. Biol. Chem. 281:29011-29021.
42. Shin, B. S., M. G. Acker, D. Maag, J. R. Kim, J. R. Lorsch, and T. E. Dever. 2007. Intragenic suppressor mutations restore GTPase and translation functions of a eukaryotic initiation factor 5B switch II mutant. Mol. Cell. Biol. 27:1677-1685.
43. Shin, B. S., and T. E. Dever. 2007. Molecular genetic structure-function analysis of translation initiation factor eIF5B. Methods Enzymol. 429:185-201.
44. Shin, B. S., D. Maag, A. Roll-Mecak, M. S. Arefin, S. K. Burley, J. R. Lorsch, and T. E. Dever. 2002. Uncoupling of initiation factor eIF5B/IF2 GTPase and translational activities by mutations that lower ribosome affinity. Cell 111:1015-1025.
45. Simonetti, A., S. Marzi, A. G. Myasnikov, A. Fabbretti, M. Yusupov, C. O. Gualerzi, and B. P. Klaholz. 2008. Structure of the 30S translation initiation complex. Nature 455:416-420.
46. Spahn, C. M., R. Beckmann, N. Eswar, P. A. Penczek, A. Sali, G. Blobel, and J. Frank. 2001. Structure of the 80S ribosome from Saccharomyces cerevisiae-tRNA-ribosome and subunit-subunit interactions. Cell 107: 373-386.
47. Spahn, C. M., M. G. Gomez-Lorenzo, R. A. Grassucci, R. Jorgensen, G. R. Andersen, R. Beckmann, P. A. Penczek, J. P. Ballesta, and J. Frank. 2004. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J. 23:1008-1019.
48. Sprang, S. R. 1997. G protein mechanisms: insights from structural analysis. Annu. Rev. Biochem. 66:639-678.
49. Stark, H., M. V. Rodnina, J. Rinke-Appel, R. Brimacombe, W. Wintermeyer, and M. van Heel. 1997. Visualization of elongation factor Tu on the Esch- erichia coli ribosome. Nature 389:403-406.
50. Stern, S., D. Moazed, and H. F. Noller. 1988. Structural analysis of RNA using chemical and enzymatic probing monitored by primer extension. Methods Enzymol. 164:481-489.
51. Swart, G. W., A. Parmeggiani, B. Kraal, and L. Bosch. 1987. Effects of the mutation gycine-222→aspartic acid on the functions of elongation factor Tu. Biochemistry 26:2047-2054.
52. Taylor, D., J. Frank, and T. Kinzy. 2007. Structure and function of eukaryotic ribosome and elongation factors, p. 59-85. In M. Mathews, N. Sonen- berg, and J. Hershey (ed.), Translational control in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
53. Taylor, D., J. Nilsson, A. Merrill, G. Andersen, P. Nissen, and J. Frank. 2007. Structures of modified eEF2 · 80S ribosome complexes reveal the role of GTP hydrolysis in translocation. EMBO J. 26:2421-2431.
54. Unbehaun, A., A. Marintchev, I. B. Lomakin, T. Didenko, G. Wagner, C. U. Hellen, and T. V. Pestova. 2007. Position of eukaryotic initiation factor eIF5B on the 80S ribosome mapped by directed hydroxyl radical probing. EMBO J. 26:3109-3123.
55. Valle, M., A. Zavialov, W. Li, S. M. Stagg, J. Sengupta, R. C. Nielsen, P. Nissen, S. C. Harvey, M. Ehrenberg, and J. Frank. 2003. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryoelectron microscopy. Nat. Struct. Biol. 10:899-906.
56. Vorstenbosch, E., T. Pape, M. V. Rodnina, B. Kraal, and W. Wintermeyer. 1996. The G222D mutation in elongation factor Tu inhibits the codon-induced conformational changes leading to GTPase activation on the ribosome. EMBO J. 15:6766-6774.
57. Wai, H. H., L. Vu, M. Oakes, and M. Nomura. 2000. Complete deletion of yeast chromosomal rDNA repeats and integration of a new rDNA repeat: use of rDNA deletion strains for functional analysis of rDNA promoter elements in vivo. Nucleic Acids Res. 28:3524-3534.