The Flexible N-terminal Domain of Ribosomal Protein L11 from Escherichia coli Is Necessary for the Activation of Stringent Factor

Journal of Molecular Biology

Volumn 365, Issue 3, 2007, Pages 764-772

  Jenvert, Rose Marie ^a,b   Schiavone, Lovisa Holmberg ^a  

^a School of Life Sciences Södertörn University   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

pppGpp; relA; ribosome; stringent response; tRNA

Indexed keywords

DNA; GENOMIC DNA; GUANOSINE TRIPHOSPHATE; GUANOSINE TRIPHOSPHATE PYROPHOSPHOKINASE; MUTANT PROTEIN; RECOMBINANT PROTEIN; RIBOSOME PROTEIN; RIBOSOME PROTEIN L11; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL MODIFICATION; CONTROLLED STUDY; DNA SEQUENCE; ESCHERICHIA COLI; MOLECULAR CLONING; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RIBOSOME;

ESCHERICHIA COLI;

EID: 33845743940     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.10.065     Document Type: Article

References (53)

1. Cashel M., Gentry D.R., Hernandez V.J., and Vinella D. The stringent response. In: Neiderhardt F.C., Curtis R., Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., et al. (Eds). In Esherichia coli and Salmonella: Cellular and Molecular Biology (1996), ASM Press, Washington DC 1458-1496
2. Haseltine W.A., and Block R. Synthesis of guanosine tetra- and penta phosphate requires the presence of a codon-specific, uncharged transfer ribonucleic acid in the acceptor site of ribosomes. Proc. Natl Acad. Sci. USA 70 (1973) 1564-1568
3. Pedersen F.S., Lund E., and Kjeldgaard N.O. Codon specific tRNA dependent in vitro synthesis of ppGpp and pppGpp. Nature New Biol. 243 (1973) 13-15
4. Wendrich T.M., Blaha G., Wilson D.N., Marahiel M.A., and Nierhaus K.N. Dissection of the mechanism for the stringent factor RelA. Mol. Cell 10 (2002) 779-788
5. Knutsson Jenvert R.-M., and Holmberg Shiavone L. Characterization of the tRNA and ribosome-dependent pppGpp-synthesis by recombinant stringent factor from Escherichia coli. FEBS J. 272 (2005) 685-695
6. Toulokhonov I.I., Shulgina I., and Hernandez V.J. Binding of the transcription effector ppGpp to Escherichia coli RNA polymerase is allosteric, modular, and occurs near the N terminus of the beta′-subunit. J. Biol. Chem. 276 (2001) 1220-1225
7. Artsimovitch I., Patlan V., Sekine S., Vassylyeva M.N., Hosaka T., Ochi K., et al. Structural basis for transcription regulation by alarmone ppGpp. Cell 117 (2004) 299-310
8. Friesen J.D., Fiil N.P., Parker J.M., and Haseltine A.W. A new relaxed mutant of Escherichia coli with an altered 50S ribosomal subunit. Proc. Natl Acad. Sci. USA 71 (1974) 3465-3469
9. Yang X., and Ishiguro E.E. Involvement of the N terminus of ribosomal protein L11 in regulation of the RelA protein of Escherichia coli. J. Bacteriol. 183 (2001) 6532-6537
10. Parker J.M., Watson R.J., and Friesen J.D. A relaxed mutant with an altered ribosomal protein L11. Mol. Gen. Genet. 144 (1976) 111-114
11. Thompson J., Cundliffe E., and Stark M. Binding of thiostrepton to a complex of 23-S rRNA with ribosomal protein L11. Eur. J. Biochem. 98 (1979) 261-265
12. Stark M.J.R., and Cundliffe E. On the biological role of ribosomal protein BM-L11 of Bacillus megaterium, homologous with Escherichia coli ribosomal protein L11. J. Mol. Biol. 134 (1979) 767-779
13. Schmidt F.J., Thompson J., Lee K., Dijk J., and Cundliffe E. The binding site for ribosomal protein L11 within 23 S ribosomal RNA of Escherichia coli. J. Biol. Chem. 256 (1981) 12301-12305
14. Tate W.P., Dognin M.J., Noah M., Stoffler-Meilicke M., and Stoffler G. The NH2-terminal domain of Escherichia coli ribosomal protein L11. Its three-dimensional location and its role in the binding of release factors 1 and 2. J. Biol. Chem. 259 (1984) 7317-7324
15. Bouakaz L., Bouakaz E., Murgola E.J., Ehrenberg M., and Sanyal S. The role of ribosomal protein L11 in class I release factor-mediated translation termination and translational accuracy. J. Biol. Chem. 281 (2006) 4548-4556
16. Sato H., Ito K., and Nakamura Y. Ribosomal protein L11 mutations in two functional domains equally affect release factors 1 and 2 activity. Mol. Microbiol. 60 (2006) 108-120
17. Cundliffe E. Involvement of specific portions of ribosomal RNA in defined ribosomal functions: A study utilizing antibiotics. In: Hardesty B., and Kramer G. (Eds). Structure, Function and Genetics of Ribosomes (1986), Springer-Verlag, New York 586-604
18. Lentzen G., Klinck R., Matassova N., Aboul-ela F., and Murchie A.I. Structural basis for contrasting activities of ribosome binding thiazole antibiotics. Chem. Biol. 10 (2003) 769-778
19. Agrawal R.K., Penczek P., Grassucci R.A., and Frank J. Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc. Natl Acad. Sci. USA 95 (1998) 6134-6138
20. Agrawal R.K., Linde J., Sengupta J., Nierhaus K.H., and Frank J. Localization of L11 protein on the ribosome and elucidation of its involvement in EF-G-dependent translocation. J. Mol. Biol. 311 (2001) 777-787
21. Valle M., Zavialov A., Li W., Stagg S.M., Sengupta J., Nielsen R.C., et al. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy. Nature Struct. Biol. 10 (2003) 899-906
22. Datta P.P., Sharma M.R., Qi L., Frank J., and Agrawal R.K. Interaction of the G′ domain of elongation factor G and the C-terminal domain of ribosomal protein L7/L12 during translocation as revealed by cryo-EM. Mol. Cell 20 (2005) 723-731
23. 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 A resolution. Science 289 (2000) 905-920
24. Yusupov M.M., Yusupova G.Z., Baucom A., Lieberman K., Earnest T.N., Cate J.H., and Noller H.F. Crystal structure of the ribosome at 5.5 A resolution. Science 292 (2001) 883-896
25. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., and Cate J.H. Structures of the bacterial ribosome at 3.5 A resolution. Science 310 (2005) 827-834
26. Egebjerg J., Douthwaite S., and Garrett R.A. Antibiotic interactions at the GTPase-associated centre within Escherichia coli 23 S rRNA. EMBO J. 8 (1989) 607-611
27. Rosendahl G., and Douthwaite S. Ribosomal proteins L11 and L10.(L12)4 and the antibiotic thiostrepton interact with overlapping regions of the 23 S rRNA backbone in the ribosomal GTPase centre. J. Mol. Biol. 234 (1993) 1013-1020
28. Rosendahl G., and Douthwaite S. The antibiotics micrococcin and thiostrepton interact directly with 23 S rRNA nucleotides 1067 A and 1095 A. Nucl. Acids Res. 22 (1994) 357-363
29. Porse B.T., Leviev I., Mankin A.S., and Garrett R.A. The antibiotic thiostrepton inhibits a functional transition within protein L11 at the ribosomal GTPase centre. J. Mol. Biol. 276 (1998) 391-404
30. Porse B.T., Cundliffe E., and Garrett R.A. The antibiotic micrococcin acts on protein L11 at the ribosomal GTPase centre. J. Mol. Biol. 287 (1999) 33-45
31. Stöffler G., Cundliffe E., Stöffler-Meilicke M., and Dabbs E.R. Mutants of Escherichia coli lacking ribosomal protein L11. J. Biol. Chem. 255 (1980) 10517-10522
32. Van Dyke N., Xu W., and Murgola E.J. Limitation of ribosomal protein L11 availability in vivo affects translation termination. J. Mol. Biol. 319 (2002) 329-339
33. Stark M.J.R., Cundliffe E., Dijk J., and Stöffler G. Functional homology between E. coli ribosomal protein L11 and B. megaterium protein BM-L11. Mol. Gen. Genet. 180 (1980) 11-15
34. Wimberly B.T., Guymon R., McCutcheon J.P., White S.W., and Ramakrishnan V. A detailed view of a ribosomal active site: the structure of the L11-RNA complex. Cell 97 (1999) 491-502
35. Thompson J., Musters W., Cundliffe E., and Dahlberg A.E. Replacement of the L11 binding region within E.coli 23 S ribosomal RNA with its homologue from yeast: in vivo and in vitro analysis of hybrid ribosomes altered in the GTPase centre. EMBO J. 12 (1993) 1499-1504
36. Van Dyke N., and Murgola E.J. Site of functional interaction of release factor 1 with the ribosome. J. Mol. Biol. 330 (2003) 9-13
37. Xing Y., and Draper D.E. Cooperative interactions of RNA and thiostrepton antibiotic with two domains of ribosomal protein L11. Biochemistry 35 (1996) 1581-1588
38. Bausch S.L., Poliakova E., and Draper D.E. Interactions of the N-terminal domain of ribosomal protein L11 with thiostrepton and rRNA. J. Biol. Chem. 280 (2005) 29956-29963
39. Li W., Sengupta J., Rath B.K., and Frank J. Functional conformations of the L11-ribosomal RNA complex revealed by correlative analysis of cryo-EM and molecular dynamics simulations. Rna 12 (2006) 1240-1253
40. Egebjerg J., Douthwaite S.R., Liljas A., and Garrett R.A. Characterization of the binding sites of protein L11 and the L10.(L12)4 pentameric complex in the GTPase domain of 23 S ribosomal RNA from Escherichia coli. J. Mol. Biol. 213 (1990) 275-288
41. Holmberg L., and Noller H.F. Mapping the ribosomal RNA neighborhood of protein L11 by directed hydroxyl radical probing. J. Mol. Biol. 289 (1999) 223-233
42. Bowen W.S., Van Dyke N., Murgola E.J., Lodmell J.S., and Hill W.E. Interaction of thiostrepton and elongation factor-G with the ribosomal protein L11-binding domain. J. Biol. Chem. 280 (2005) 2934-2943
43. Valle M., Sengupta J., Swami N.K., Grassucci R.A., Burkhardt N., Nierhaus K.H., et al. Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process. EMBO J. 21 (2002) 3557-3567
44. Pedersen F.S., and Kjeldgaard N.O. Analysis of the relA gene product of Escherichia coli. Eur. J. Biochem. 76 (1977) 91-97
45. Traub P., Mizushima S., Lowry C.V., and Nomura M. Reconstitution of ribosomes from subribosomal components. In: Moldave K. (Ed). RNA and Protein Synthesis (1981), Academic Press, New York 521-544
46. Hinck A.P., Markus M.A., Huang S., Grzesiek S., Kustonovich I., Draper D.E., and Torchia D.A. The RNA binding domain of ribosomal protein L11: three-dimensional structure of the RNA-bound form of the protein and its interaction with 23 S rRNA. J. Mol. Biol. 274 (1997) 101-113
47. Kini R.M., and Evans H.J. A hypothetical structural role for proline residues in the flanking segments of protein-protein interaction sites. Biochem. Biophys. Res. Commun. 212 (1995) 1115-1124
48. Gerstein M., Lesk A.M., and Chothia C. Structural mechanisms for domain movements in proteins. Biochemistry 33 (1994) 6739-6749
49. Gerstein M., and Krebs W. A database of macromolecular motions. Nucl. Acids Res. 26 (1998) 4280-4290
50. Moazed D., Robertson J.M., and Noller H.F. Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23 S RNA. Nature 334 (1988) 362-364
51. 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. Nature Struct. Biol. 9 (2002) 849-854
52. Yang X., and Ishiguro E.E. Dimerization of the relA protein of Escherichia coli. Biochem. Cell Biol. 79 (2001) 729-736
53. Larsson S.L., and Nygård O. Proposed secondary structure of eukaryote specific expansion segment 15 in 28 S rRNA from mice, rats, and rabbits. Biochemistry 40 (2001) 3222-3231