Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1998 Aug 17;17(16):4545–4558. doi: 10.1093/emboj/17.16.4545

The crystal structure of ribosomal protein S4 reveals a two-domain molecule with an extensive RNA-binding surface: one domain shows structural homology to the ETS DNA-binding motif.

C Davies 1, R B Gerstner 1, D E Draper 1, V Ramakrishnan 1, S W White 1
PMCID: PMC1170785  PMID: 9707415

Abstract

We report the 1.7 A crystal structure of ribosomal protein S4 from Bacillus stearothermophilus. To facilitate the crystallization, 41 apparently flexible residues at the N-terminus of the protein have been deleted (S4Delta41). S4Delta41 has two domains; domain 1 is completely alpha-helical and domain 2 comprises a five-stranded antiparallel beta-sheet with three alpha-helices packed on one side. Domain 2 is an insertion within domain 1, and it shows significant structural homology to the ETS domain of eukaryotic transcription factors. A phylogenetic analysis of the S4 primary structure shows that the likely RNA interaction surface is predominantly on one side of the protein. The surface is extensive and highly positively charged, and is centered on a distinctive canyon at the domain interface. The latter feature contains two arginines that are totally conserved in all known species of S4 including eukaryotes, and are probably crucial in binding RNA. As has been shown for other ribosomal proteins, mutations within S4 that affect ribosome function appear to disrupt the RNA-binding sites. The structure provides a framework with which to probe the RNA-binding properties of S4 by site-directed mutagenesis.

Full Text

The Full Text of this article is available as a PDF (954.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adamski F. M., Atkins J. F., Gesteland R. F. Ribosomal protein L9 interactions with 23 S rRNA: the use of a translational bypass assay to study the effect of amino acid substitutions. J Mol Biol. 1996 Aug 23;261(3):357–371. doi: 10.1006/jmbi.1996.0469. [DOI] [PubMed] [Google Scholar]
  2. Allen P. N., Noller H. F. Mutations in ribosomal proteins S4 and S12 influence the higher order structure of 16 S ribosomal RNA. J Mol Biol. 1989 Aug 5;208(3):457–468. doi: 10.1016/0022-2836(89)90509-3. [DOI] [PubMed] [Google Scholar]
  3. Arndt E., Scholzen T., Krömer W., Hatakeyama T., Kimura M. Primary structures of ribosomal proteins from the archaebacterium Halobacterium marismortui and the eubacterium Bacillus stearothermophilus. Biochimie. 1991 Jun;73(6):657–668. doi: 10.1016/0300-9084(91)90045-3. [DOI] [PubMed] [Google Scholar]
  4. Baker A. M., Draper D. E. Messenger RNA recognition by fragments of ribosomal protein S4. J Biol Chem. 1995 Sep 29;270(39):22939–22945. doi: 10.1074/jbc.270.39.22939. [DOI] [PubMed] [Google Scholar]
  5. Birge E. A., Kurland C. G. Reversion of a streptomycin-dependent strain of Escherichia coli. Mol Gen Genet. 1970;109(4):356–369. doi: 10.1007/BF00267704. [DOI] [PubMed] [Google Scholar]
  6. Blake C. C., Koenig D. F., Mair G. A., North A. C., Phillips D. C., Sarma V. R. Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2 Angstrom resolution. Nature. 1965 May 22;206(4986):757–761. doi: 10.1038/206757a0. [DOI] [PubMed] [Google Scholar]
  7. Brennan R. G. The winged-helix DNA-binding motif: another helix-turn-helix takeoff. Cell. 1993 Sep 10;74(5):773–776. doi: 10.1016/0092-8674(93)90456-z. [DOI] [PubMed] [Google Scholar]
  8. Brimacombe R. RNA-protein interactions in the Escherichia coli ribosome. Biochimie. 1991 Jul-Aug;73(7-8):927–936. doi: 10.1016/0300-9084(91)90134-m. [DOI] [PubMed] [Google Scholar]
  9. Brünger A. T. Crystallographic refinement by simulated annealing. Application to a 2.8 A resolution structure of aspartate aminotransferase. J Mol Biol. 1988 Oct 5;203(3):803–816. doi: 10.1016/0022-2836(88)90211-2. [DOI] [PubMed] [Google Scholar]
  10. Burley S. K., Petsko G. A. Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science. 1985 Jul 5;229(4708):23–28. doi: 10.1126/science.3892686. [DOI] [PubMed] [Google Scholar]
  11. Capel M. S., Engelman D. M., Freeborn B. R., Kjeldgaard M., Langer J. A., Ramakrishnan V., Schindler D. G., Schneider D. K., Schoenborn B. P., Sillers I. Y. A complete mapping of the proteins in the small ribosomal subunit of Escherichia coli. Science. 1987 Dec 4;238(4832):1403–1406. doi: 10.1126/science.3317832. [DOI] [PubMed] [Google Scholar]
  12. Changchien L. M., Craven G. R. Specific ribosomal RNA recognition by a fragment of E. coli ribosomal protein S4 missing the C-terminal 36 amino acid residues. Nucleic Acids Res. 1985 Sep 11;13(17):6343–6360. doi: 10.1093/nar/13.17.6343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Changchien L. M., Craven G. R. The function of the N-terminal region of ribosomal protein S4. J Mol Biol. 1976 Dec;108(2):381–401. doi: 10.1016/s0022-2836(76)80126-x. [DOI] [PubMed] [Google Scholar]
  14. Changchien L. M., Craven G. R. The use of hydroxylamine cleavage to produce a fragment of ribosomal protein S4 which retains the capacity to specifically bind 16S ribosomal RNA. Nucleic Acids Res. 1986 Mar 11;14(5):1957–1966. doi: 10.1093/nar/14.5.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Clemons W. M., Jr, Davies C., White S. W., Ramakrishnan V. Conformational variability of the N-terminal helix in the structure of ribosomal protein S15. Structure. 1998 Apr 15;6(4):429–438. doi: 10.1016/s0969-2126(98)00045-8. [DOI] [PubMed] [Google Scholar]
  16. Conrad R. C., Craven G. R. A cyanogen bromide fragment of S4 that specifically rebinds 16S RNA. Nucleic Acids Res. 1987 Dec 23;15(24):10331–10343. doi: 10.1093/nar/15.24.10331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dahlberg A. E. The functional role of ribosomal RNA in protein synthesis. Cell. 1989 May 19;57(4):525–529. doi: 10.1016/0092-8674(89)90122-0. [DOI] [PubMed] [Google Scholar]
  18. Davies C., Bussiere D. E., Golden B. L., Porter S. J., Ramakrishnan V., White S. W. Ribosomal proteins S5 and L6: high-resolution crystal structures and roles in protein synthesis and antibiotic resistance. J Mol Biol. 1998 Jun 19;279(4):873–888. doi: 10.1006/jmbi.1998.1780. [DOI] [PubMed] [Google Scholar]
  19. Davies C., Ramakrishnan V., White S. W. Structural evidence for specific S8-RNA and S8-protein interactions within the 30S ribosomal subunit: ribosomal protein S8 from Bacillus stearothermophilus at 1.9 A resolution. Structure. 1996 Sep 15;4(9):1093–1104. doi: 10.1016/s0969-2126(96)00115-3. [DOI] [PubMed] [Google Scholar]
  20. Davies C., White S. W., Ramakrishnan V. The crystal structure of ribosomal protein L14 reveals an important organizational component of the translational apparatus. Structure. 1996 Jan 15;4(1):55–66. doi: 10.1016/s0969-2126(96)00009-3. [DOI] [PubMed] [Google Scholar]
  21. Daya-Grosjean L., Garrett R. A., Pongs O., Stöffler G., Wittmann H. G. Properties of the interaction of ribosomal protein S4 and 16S RNA in Escherichia coli revertants from Streptomycin dependence to independence. Mol Gen Genet. 1972;119(3):277–286. doi: 10.1007/BF00333865. [DOI] [PubMed] [Google Scholar]
  22. Dean D., Nomura M. Feedback regulation of ribosomal protein gene expression in Escherichia coli. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3590–3594. doi: 10.1073/pnas.77.6.3590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Deckman I. C., Draper D. E. S4-alpha mRNA translation regulation complex. II. Secondary structures of the RNA regulatory site in the presence and absence of S4. J Mol Biol. 1987 Jul 20;196(2):323–332. doi: 10.1016/0022-2836(87)90693-0. [DOI] [PubMed] [Google Scholar]
  24. Deckman I. C., Draper D. E. Specific interaction between ribosomal protein S4 and the alpha operon messenger RNA. Biochemistry. 1985 Dec 31;24(27):7860–7865. doi: 10.1021/bi00348a002. [DOI] [PubMed] [Google Scholar]
  25. Deckman I. C., Draper D. E., Thomas M. S. S4-alpha mRNA translation repression complex. I. Thermodynamics of formation. J Mol Biol. 1987 Jul 20;196(2):313–322. doi: 10.1016/0022-2836(87)90692-9. [DOI] [PubMed] [Google Scholar]
  26. Dickerson R. E., Takano T., Eisenberg D., Kallai O. B., Samson L., Cooper A., Margoliash E. Ferricytochrome c. I. General features of the horse and bonito proteins at 2.8 A resolution. J Biol Chem. 1971 Mar 10;246(5):1511–1535. [PubMed] [Google Scholar]
  27. Donaldson L. W., Petersen J. M., Graves B. J., McIntosh L. P. Solution structure of the ETS domain from murine Ets-1: a winged helix-turn-helix DNA binding motif. EMBO J. 1996 Jan 2;15(1):125–134. [PMC free article] [PubMed] [Google Scholar]
  28. Draper D. E. How do proteins recognize specific RNA sites? New clues from autogenously regulated ribosomal proteins. Trends Biochem Sci. 1989 Aug;14(8):335–338. doi: 10.1016/0968-0004(89)90167-9. [DOI] [PubMed] [Google Scholar]
  29. Ehresmann C., Stiegler P., Carbon P., Ungewickell E., Garrett R. A. A topographical study of the 5'-region of 16 S rna of Escherichia coli in the presence and absence of protein S4. FEBS Lett. 1977 Sep 1;81(1):188–192. doi: 10.1016/0014-5793(77)80956-3. [DOI] [PubMed] [Google Scholar]
  30. Fleischmann R. D., Adams M. D., White O., Clayton R. A., Kirkness E. F., Kerlavage A. R., Bult C. J., Tomb J. F., Dougherty B. A., Merrick J. M. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995 Jul 28;269(5223):496–512. doi: 10.1126/science.7542800. [DOI] [PubMed] [Google Scholar]
  31. Funatsu G., Puls W., Schiltz E., Reinbolt J., Wittmann H. G. Ribosomal proteins. XXXI. Comparative studies on altered proteins S4 of six Escherichia coli revertants from streptomycin dependence. Mol Gen Genet. 1972;115(2):131–139. doi: 10.1007/BF00277293. [DOI] [PubMed] [Google Scholar]
  32. Gluick T. C., Gerstner R. B., Draper D. E. Effects of Mg2+, K+, and H+ on an equilibrium between alternative conformations of an RNA pseudoknot. J Mol Biol. 1997 Jul 18;270(3):451–463. doi: 10.1006/jmbi.1997.1119. [DOI] [PubMed] [Google Scholar]
  33. Green M., Kurland C. G. Mutant ribosomal protein with defective RNA binding site. Nat New Biol. 1971 Dec 29;234(52):273–275. doi: 10.1038/newbio234273a0. [DOI] [PubMed] [Google Scholar]
  34. Greuer B., Osswald M., Brimacombe R., Stöffler G. RNA-protein cross-linking in Escherichia coli 30S ribosomal subunits; determination of sites on 16S RNA that are cross-linked to proteins S3, S4, S7, S9, S10, S11, S17, S18 and S21 by treatment with bis-(2-chloroethyl)-methylamine. Nucleic Acids Res. 1987 Apr 24;15(8):3241–3255. doi: 10.1093/nar/15.8.3241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Grundy F. J., Henkin T. M. Cloning and analysis of the Bacillus subtilis rpsD gene, encoding ribosomal protein S4. J Bacteriol. 1990 Nov;172(11):6372–6379. doi: 10.1128/jb.172.11.6372-6379.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Heilek G. M., Marusak R., Meares C. F., Noller H. F. Directed hydroxyl radical probing of 16S rRNA using Fe(II) tethered to ribosomal protein S4. Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):1113–1116. doi: 10.1073/pnas.92.4.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Heilek G. M., Noller H. F. Site-directed hydroxyl radical probing of the rRNA neighborhood of ribosomal protein S5. Science. 1996 Jun 14;272(5268):1659–1662. doi: 10.1126/science.272.5268.1659. [DOI] [PubMed] [Google Scholar]
  38. Held W. A., Ballou B., Mizushima S., Nomura M. Assembly mapping of 30 S ribosomal proteins from Escherichia coli. Further studies. J Biol Chem. 1974 May 25;249(10):3103–3111. [PubMed] [Google Scholar]
  39. Hinck A. P., Markus M. A., Huang S., Grzesiek S., Kustonovich I., Draper D. E., 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. 1997 Nov 21;274(1):101–113. doi: 10.1006/jmbi.1997.1379. [DOI] [PubMed] [Google Scholar]
  40. Hinrichs W., Kisker C., Düvel M., Müller A., Tovar K., Hillen W., Saenger W. Structure of the Tet repressor-tetracycline complex and regulation of antibiotic resistance. Science. 1994 Apr 15;264(5157):418–420. doi: 10.1126/science.8153629. [DOI] [PubMed] [Google Scholar]
  41. Holm L., Sander C. Dali: a network tool for protein structure comparison. Trends Biochem Sci. 1995 Nov;20(11):478–480. doi: 10.1016/s0968-0004(00)89105-7. [DOI] [PubMed] [Google Scholar]
  42. Hutchinson E. G., Thornton J. M. PROMOTIF--a program to identify and analyze structural motifs in proteins. Protein Sci. 1996 Feb;5(2):212–220. doi: 10.1002/pro.5560050204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Jones T. A., Zou J. Y., Cowan S. W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A. 1991 Mar 1;47(Pt 2):110–119. doi: 10.1107/s0108767390010224. [DOI] [PubMed] [Google Scholar]
  44. Kodandapani R., Pio F., Ni C. Z., Piccialli G., Klemsz M., McKercher S., Maki R. A., Ely K. R. A new pattern for helix-turn-helix recognition revealed by the PU.1 ETS-domain-DNA complex. Nature. 1996 Apr 4;380(6573):456–460. doi: 10.1038/380456a0. [DOI] [PubMed] [Google Scholar]
  45. Malhotra A., Severinova E., Darst S. A. Crystal structure of a sigma 70 subunit fragment from E. coli RNA polymerase. Cell. 1996 Oct 4;87(1):127–136. doi: 10.1016/s0092-8674(00)81329-x. [DOI] [PubMed] [Google Scholar]
  46. Markus M. A., Gerstner R. B., Draper D. E., Torchia D. A. The solution structure of ribosomal protein S4 delta41 reveals two subdomains and a positively charged surface that may interact with RNA. EMBO J. 1998 Aug 17;17(16):4559–4571. doi: 10.1093/emboj/17.16.4559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Marqusee S., Baldwin R. L. Helix stabilization by Glu-...Lys+ salt bridges in short peptides of de novo design. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8898–8902. doi: 10.1073/pnas.84.24.8898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Matthews B. W. Solvent content of protein crystals. J Mol Biol. 1968 Apr 28;33(2):491–497. doi: 10.1016/0022-2836(68)90205-2. [DOI] [PubMed] [Google Scholar]
  49. Mueller F., Brimacombe R. A new model for the three-dimensional folding of Escherichia coli 16 S ribosomal RNA. II. The RNA-protein interaction data. J Mol Biol. 1997 Aug 29;271(4):545–565. doi: 10.1006/jmbi.1997.1211. [DOI] [PubMed] [Google Scholar]
  50. Nicholls A., Sharp K. A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins. 1991;11(4):281–296. doi: 10.1002/prot.340110407. [DOI] [PubMed] [Google Scholar]
  51. Nikonov S., Nevskaya N., Eliseikina I., Fomenkova N., Nikulin A., Ossina N., Garber M., Jonsson B. H., Briand C., Al-Karadaghi S. Crystal structure of the RNA binding ribosomal protein L1 from Thermus thermophilus. EMBO J. 1996 Mar 15;15(6):1350–1359. [PMC free article] [PubMed] [Google Scholar]
  52. Noller H. F., Hoffarth V., Zimniak L. Unusual resistance of peptidyl transferase to protein extraction procedures. Science. 1992 Jun 5;256(5062):1416–1419. doi: 10.1126/science.1604315. [DOI] [PubMed] [Google Scholar]
  53. Nowotny V., Nierhaus K. H. Assembly of the 30S subunit from Escherichia coli ribosomes occurs via two assembly domains which are initiated by S4 and S7. Biochemistry. 1988 Sep 6;27(18):7051–7055. doi: 10.1021/bi00418a057. [DOI] [PubMed] [Google Scholar]
  54. Ogata K., Hojo H., Aimoto S., Nakai T., Nakamura H., Sarai A., Ishii S., Nishimura Y. Solution structure of a DNA-binding unit of Myb: a helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6428–6432. doi: 10.1073/pnas.89.14.6428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Ollis D. L., Brick P., Hamlin R., Xuong N. G., Steitz T. A. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. 1985 Feb 28-Mar 6Nature. 313(6005):762–766. doi: 10.1038/313762a0. [DOI] [PubMed] [Google Scholar]
  56. Pennisi E. Taking a structured approach to understanding proteins. Science. 1998 Feb 13;279(5353):978–979. doi: 10.1126/science.279.5353.978. [DOI] [PubMed] [Google Scholar]
  57. Powers T., Noller H. F. A functional pseudoknot in 16S ribosomal RNA. EMBO J. 1991 Aug;10(8):2203–2214. doi: 10.1002/j.1460-2075.1991.tb07756.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Powers T., Noller H. F. A temperature-dependent conformational rearrangement in the ribosomal protein S4.16 S rRNA complex. J Biol Chem. 1995 Jan 20;270(3):1238–1242. doi: 10.1074/jbc.270.3.1238. [DOI] [PubMed] [Google Scholar]
  59. Powers T., Noller H. F. Hydroxyl radical footprinting of ribosomal proteins on 16S rRNA. RNA. 1995 Apr;1(2):194–209. [PMC free article] [PubMed] [Google Scholar]
  60. Ramakrishnan V., White S. W. Ribosomal protein structures: insights into the architecture, machinery and evolution of the ribosome. Trends Biochem Sci. 1998 Jun;23(6):208–212. doi: 10.1016/s0968-0004(98)01214-6. [DOI] [PubMed] [Google Scholar]
  61. Randolph-Anderson B. L., Boynton J. E., Gillham N. W., Huang C., Liu X. Q. The chloroplast gene encoding ribosomal protein S4 in Chlamydomonas reinhardtii spans an inverted repeat--unique sequence junction and can be mutated to suppress a streptomycin dependence mutation in ribosomal protein S12. Mol Gen Genet. 1995 May 10;247(3):295–305. doi: 10.1007/BF00293197. [DOI] [PubMed] [Google Scholar]
  62. Rayment I., Rypniewski W. R., Schmidt-Bäse K., Smith R., Tomchick D. R., Benning M. M., Winkelmann D. A., Wesenberg G., Holden H. M. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 1993 Jul 2;261(5117):50–58. doi: 10.1126/science.8316857. [DOI] [PubMed] [Google Scholar]
  63. Sapag A., Vartikar J. V., Draper D. E. Dissection of the 16S rRNA binding site for ribosomal protein S4. Biochim Biophys Acta. 1990 Aug 27;1050(1-3):34–37. doi: 10.1016/0167-4781(90)90137-q. [DOI] [PubMed] [Google Scholar]
  64. Shinozaki K., Ohme M., Tanaka M., Wakasugi T., Hayashida N., Matsubayashi T., Zaita N., Chunwongse J., Obokata J., Yamaguchi-Shinozaki K. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 1986 Sep;5(9):2043–2049. doi: 10.1002/j.1460-2075.1986.tb04464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Spedding G., Draper D. E. Allosteric mechanism for translational repression in the Escherichia coli alpha operon. Proc Natl Acad Sci U S A. 1993 May 15;90(10):4399–4403. doi: 10.1073/pnas.90.10.4399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Stern S., Wilson R. C., Noller H. F. Localization of the binding site for protein S4 on 16 S ribosomal RNA by chemical and enzymatic probing and primer extension. J Mol Biol. 1986 Nov 5;192(1):101–110. doi: 10.1016/0022-2836(86)90467-5. [DOI] [PubMed] [Google Scholar]
  67. Stevenson J. K., Drager R. G., Copertino D. W., Christopher D. A., Jenkins K. P., Yepiz-Plascencia G., Hallick R. B. Intercistronic group III introns in polycistronic ribosomal protein operons of chloroplasts. Mol Gen Genet. 1991 Aug;228(1-2):183–192. doi: 10.1007/BF00282464. [DOI] [PubMed] [Google Scholar]
  68. Stöffler G., Stöffler-Meilicke M. Immunoelectron microscopy of ribosomes. Annu Rev Biophys Bioeng. 1984;13:303–330. doi: 10.1146/annurev.bb.13.060184.001511. [DOI] [PubMed] [Google Scholar]
  69. Tanaka I., Nakagawa A., Hosaka H., Wakatsuki S., Mueller F., Brimacombe R. Matching the crystallographic structure of ribosomal protein S7 to a three-dimensional model of the 16S ribosomal RNA. RNA. 1998 May;4(5):542–550. doi: 10.1017/s1355838298972004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Tang C. K., Draper D. E. Evidence for allosteric coupling between the ribosome and repressor binding sites of a translationally regulated mRNA. Biochemistry. 1990 May 8;29(18):4434–4439. doi: 10.1021/bi00470a025. [DOI] [PubMed] [Google Scholar]
  71. Tang C. K., Draper D. E. Unusual mRNA pseudoknot structure is recognized by a protein translational repressor. Cell. 1989 May 19;57(4):531–536. doi: 10.1016/0092-8674(89)90123-2. [DOI] [PubMed] [Google Scholar]
  72. Thomas M. S., Bedwell D. M., Nomura M. Regulation of alpha operon gene expression in Escherichia coli. A novel form of translational coupling. J Mol Biol. 1987 Jul 20;196(2):333–345. doi: 10.1016/0022-2836(87)90694-2. [DOI] [PubMed] [Google Scholar]
  73. Urlaub H., Kruft V., Bischof O., Müller E. C., Wittmann-Liebold B. Protein-rRNA binding features and their structural and functional implications in ribosomes as determined by cross-linking studies. EMBO J. 1995 Sep 15;14(18):4578–4588. doi: 10.1002/j.1460-2075.1995.tb00137.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Urlaub H., Thiede B., Müller E. C., Brimacombe R., Wittmann-Liebold B. Identification and sequence analysis of contact sites between ribosomal proteins and rRNA in Escherichia coli 30 S subunits by a new approach using matrix-assisted laser desorption/ionization-mass spectrometry combined with N-terminal microsequencing. J Biol Chem. 1997 Jun 6;272(23):14547–14555. doi: 10.1074/jbc.272.23.14547. [DOI] [PubMed] [Google Scholar]
  75. Vartikar J. V., Draper D. E. S4-16 S ribosomal RNA complex. Binding constant measurements and specific recognition of a 460-nucleotide region. J Mol Biol. 1989 Sep 20;209(2):221–234. doi: 10.1016/0022-2836(89)90274-x. [DOI] [PubMed] [Google Scholar]
  76. Wittmann-Liebold B., Uhlein M., Urlaub H., Müller E. C., Otto A., Bischof O. Structural and functional implications in the eubacterial ribosome as revealed by protein-rRNA and antibiotic contact sites. Biochem Cell Biol. 1995 Nov-Dec;73(11-12):1187–1197. doi: 10.1139/o95-128. [DOI] [PubMed] [Google Scholar]
  77. Yates J. L., Arfsten A. E., Nomura M. In vitro expression of Escherichia coli ribosomal protein genes: autogenous inhibition of translation. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1837–1841. doi: 10.1073/pnas.77.4.1837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Zimmermann R. A., Mackie G. A., Muto A., Garrett R. A., Ungewickell E., Ehresmann C., Stiegler P., Ebel J. P., Fellner P. Location and characteristics of ribosomal protein binding sites in the 16S RNA of Escherichia coli. Nucleic Acids Res. 1975 Feb;2(2):279–302. doi: 10.1093/nar/2.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. van Acken U. Proteinchemical studies on ribosomal proteins S4 and S12 from ram (ribosomal ambiguity) mutants of Escherichia coli. Mol Gen Genet. 1975 Sep 15;140(1):61–68. doi: 10.1007/BF00268989. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES