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Structural Aspects of Ribosomal RNA Recognition by Ribosomal Proteins

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Abstract

This review is focused on the structural aspects of interaction between ribosomal proteins and ribosomal RNA in bacterial ribosomes and complexes of ribosomal proteins with specific fragments of ribosomal RNA. Special attention is given to the recognition of specific spatial architecture of the double-stranded ribosomal RNA by ribosomal proteins and to the role of unstructured protein regions in stabilization of distant ribosomal RNA segments.

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Abbreviations

EM:

electron microscopy

LRS:

50S (large) ribosomal subunit

NMR:

nuclear magnetic resonance

r-protein:

ribosomal protein

rRNA:

ribosomal RNA

SRS:

30S (small) ribosomal subunit

References

  1. Spirin, A. S. (2011) Molecular Biology. Ribosomes and Protein Biosynthesis [in Russian], Akademiya, Moscow.

    Google Scholar 

  2. Klein, D. J., Moore, P. B., and Steitz, T. A. (2004) The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit, J. Mol. Biol., 340, 141–177.

    CAS  PubMed  Google Scholar 

  3. Lecompte, O., Ripp, R., Thierry, J.-C., Moras, D., and Poch, O. (2002) Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale, Nucleic Acids Res., 30, 5382–5390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Korobeinikova, A. V., Garber, M. B., and Gongadze, G. M. (2012) Ribosomal proteins: structure, function and evolution, Biochemistry (Moscow), 77, 562–574.

    Article  CAS  Google Scholar 

  5. Hartman, H., Favaretto, P., and Smith, T. F. (2006) The archaeal origins of the eukaryotic translational system, Archaea, 2, 1–9.

    Article  CAS  PubMed  Google Scholar 

  6. Ban, N., Beckmann, R., Cate, J. H., Dinman, J. D., Dragon, F., Ellis, S. R., Lafontaine, D. L., Lindahl, L., Liljas, A., Lipton, J. M., McAlear, M. A., Moore, P. B., Noller, H. F., Ortega, J., Panse, V. G., Ramakrishnan, V., Spahn, C. M., Steitz, T. A., Tchorzewski, M., Tollervey, D., Warren, A. J., Williamson, J. R., Wilson, D., Yonath, A., and Yusupov, M. (2014) A new system for naming ribosomal proteins, Curr. Opin. Struct. Biol., 24, 165–169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kaczanowska, M., and Ryden-Aulin, M. (2007) Ribosome biogenesis and the translation process in Escherichia coli, Microbiol. Mol. Biol. Rev., 71, 477–494.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hamacher, K., Trylska, J., and McCammon, J. A. (2006) Dependency map of proteins in the small ribosomal subunit, PLoS Comput. Biol., 2, e10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Rohl, R., and Nierhaus, K. H. (1982) Assembly map of the large subunit (50S) of Escherichia coli ribosomes, Proc. Natl. Acad. Sci. USA, 79, 729–733.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Herold, M., and Nierhaus, K. H. (1987) Incorporation of six additional proteins to complete the assembly map of the 50S subunit from Escherichia coli ribosomes, J. Biol. Chem., 262, 8826–8833.

    CAS  PubMed  Google Scholar 

  11. Spillmann, S., Dohme, F., and Nierhaus, K. H. (1977) Assembly in vitro of the 50S subunit from Escherichia coli ribosomes: proteins essential for the first heat-dependent conformational change, J. Mol. Biol., 115, 513–523.

    Article  CAS  PubMed  Google Scholar 

  12. Held, W. A., and Nomura, M. (1973) Rate determining step in the reconstitution of Escherichia coli 30S ribosomal subunits, Biochemistry, 12, 3273–3281.

    Article  CAS  PubMed  Google Scholar 

  13. Schuwirth, B. S. (2005) Structures of the bacterial ribosome at 3.5 Å resolution, Science, 310, 827–834.

    Article  CAS  PubMed  Google Scholar 

  14. Porse, B. T., and Garrett, R. A. (1999) Ribosomal mechanics, antibiotics, and GTP hydrolysis, Cell, 97, 423–426.

    CAS  PubMed  Google Scholar 

  15. Diaconu, M., Kothe, U., Schlunzen, F., Fischer, N., Harms, J. M., Tonevitsky, A. G., Stark, H., Rodnina, M. V., and Wahl, M. C. (2005) Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation, Cell, 121, 991–1004.

    Article  CAS  PubMed  Google Scholar 

  16. Leijonmarck, M., and Liljas, A. (1987) Structure of the C-terminal domain of the ribosomal protein L7/L12 from Escherichia coli at 1.7 Å, J. Mol. Biol., 195, 555–579.

    Article  CAS  PubMed  Google Scholar 

  17. Mitroshin, I. V., Garber, M. B., and Gabdulkhakov, A. G. (2016) Investigation of structure of the ribosomal L12/P stalk, Biochemistry (Moscow), 81, 1589–1601.

    Article  CAS  Google Scholar 

  18. Xing, Y., and Draper, D. E. (1996) Cooperative interactions of RNA and thiostrepton antibiotic with two domains of ribosomal protein L11, Biochemistry, 35, 1581–1588.

    Article  CAS  PubMed  Google Scholar 

  19. Jonker, H. R. A., Ilin, S., Grimm, S. K., Wohnert, J., and Schwalbe, H. (2006) L11 domain rearrangement upon binding to RNA and thiostrepton studied by NMR spectroscopy, Nucleic Acids Res., 35, 441–454.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Wimberly, B. T., Guymon, R., McCutcheon, J. P., White, S. W., and Ramakrishnan, V. (1999) A detailed view of a ribosomal active site: the structure of the L11–RNA complex, Cell, 97, 491–502.

    Article  CAS  PubMed  Google Scholar 

  21. Conn, G. L., Draper, D. E., Lattman, E. E., and Gittis, A. G. (1999) Crystal structure of a conserved ribosomal protein–RNA complex, Science, 284, 1171–1174.

    Article  CAS  PubMed  Google Scholar 

  22. Murzin, A. G., Brenner, S. E., Hubbard, T., and Chothia, C. (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures, J. Mol. Biol., 247, 536–540.

    CAS  PubMed  Google Scholar 

  23. Brennan, R. G., and Matthews, B. W. (1989) The helix-turn-helix DNA binding motif, J. Biol. Chem., 264, 1903–1906.

    CAS  PubMed  Google Scholar 

  24. Matthews, B. W., Ohlendorf, D. H., Anderson, W. F., and Takeda, Y. (1982) Structure of the DNA-binding region of lac repressor inferred from its homology with cro repressor, Proc. Natl. Acad. Sci. USA, 79, 1428–1432.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Muller, C. W. (2001) Transcription factors: global and detailed views, Curr. Opin. Struct. Biol., 11, 26–32.

    Article  CAS  PubMed  Google Scholar 

  26. Gudkov, A. T., Tumanova, L. G., Gongadze, G. M., and Bushuev, V. N. (1980) Role of different regions of ribosomal proteins L7 and L10 in their complex formation and in the interaction with the ribosomal 50S subunit, FEBS Lett., 109, 34–38.

    Article  CAS  PubMed  Google Scholar 

  27. Rosendahl, G., and Douthwaite, S. (1993) Ribosomal proteins L11 and L10-(L12)4 and the antibiotic thiostrepton interact with overlapping regions of the 23S rRNA back-bone in the ribosomal GTPase center, J. Mol. Biol., 234, 1013–1020.

    Article  CAS  PubMed  Google Scholar 

  28. Noeske, J., Wasserman, M. R., Terry, D. S., Altman, R. B., Blanchard, S. C., and Cate, J. H. D. (2015) High-resolution structure of the Escherichia coli ribosome, Nat. Struct. Mol. Biol., 22, 336–341.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Cocozaki, A. I., Altman, R. B., Huang, J., Buurman, E. T., Kazmirski, S. L., Doig, P., Prince, D. B., Blanchard, S. C., Cate, J. H. D., and Ferguson, A. D. (2016) Resistance mutations generate divergent antibiotic susceptibility profiles against translation inhibitors, Proc. Natl. Acad. Sci. USA, 113, 8188–8193.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lin, J., Gagnon, M. G., Bulkley, D., and Steitz, T. A. (2015) Conformational changes of elongation factor G on the ribosome during tRNA translocation, Cell, 160, 219–227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gagnon, M. G., Lin, J., and Steitz, T. A. (2016) Elongation factor 4 remodels the A-site tRNA on the ribosome, Proc. Natl. Acad. Sci. USA, 113, 4994–4999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Fischer, N., Konevega, A. L., Wintermeyer, W., Rodnina, M. V., and Stark, H. (2010) Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy, Nature, 466, 329–333.

    Article  CAS  PubMed  Google Scholar 

  33. Trabuco, L. G., Schreiner, E., Eargle, J., Cornish, P., Ha, T., Luthey-Schulten, Z., and Schulten, K. (2010) The role of L1 stalk–tRNA interaction in the ribosome elongation cycle, J. Mol. Biol., 402, 741–760.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ban, N., Nissen, P., Hansen, J., Moore, P. B., and Steitz, T. A. (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution, Science, 289, 905–920.

    Article  CAS  PubMed  Google Scholar 

  35. Selmer, M. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA, Science, 313, 1935–1942.

    Article  CAS  PubMed  Google Scholar 

  36. Nikonov, S., Nevskaya, N., Eliseikina, I., Fomenkova, N., Nikulin, A., Ossina, N., Garber, M., Jonsson, B. H., Briand, C., Al-Karadaghi, S., Svensson, A., Aevarsson, A., and Liljas, A. (1996) Crystal structure of the RNA binding ribosomal protein L1 from Thermus thermophiles, EMBO J., 15, 1350–1359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tishchenko, S., Nikonova, E., Kostareva, O., Gabdulkhakov, A., Piendl, W., Nevskaya, N., Garber, M., and Nikonov, S. (2011) Structural analysis of interdomain mobility in ribosomal L1 proteins, Acta Crystallogr. D, 67, 1023–1027.

    Article  CAS  PubMed  Google Scholar 

  38. Nikulin, A., Eliseikina, I., Tishchenko, S., Nevskaya, N., Davydova, N., Platonova, O., Piendl, W., Selmer, M., Liljas, A., Drygin, D., Zimmermann, R., Garber, M., and Nikonov, S. (2003) Structure of the L1 protuberance in the ribosome, Nat. Struct. Biol., 10, 104–108.

    Article  CAS  PubMed  Google Scholar 

  39. Willumeit, R., Forthmann, S., Beckmann, J., Diedrich, G., Ratering, R., Stuhrmann, H. B., and Nierhaus, K. H. (2001) Localization of the protein L2 in the 50S subunit and the 70S E. coli ribosome, J. Mol. Biol., 305, 167–177.

    Article  CAS  PubMed  Google Scholar 

  40. Diedrich, G., Spahn, C. M. T., Stelzl, U., Schafer, M. A., Wooten, T., Bochkariov, D. E., Cooperman, B. S., Traut, R. R., and Nierhaus, K. H. (2000) Ribosomal protein L2 is involved in the association of the ribosomal subunits, tRNA binding to A and P sites and peptidyl transfer, EMBO J., 19, 5241–5250.

    CAS  PubMed  Google Scholar 

  41. Cooperman, B. S., Wooten, T., Romero, D. P., and Traut, R. R. (1995) Histidine 229 in protein L2 is apparently essential for 50S peptidyl transferase activity, Biochem. Cell Biol., 73, 1087–1094.

    Article  CAS  PubMed  Google Scholar 

  42. Gao, H., Sengupta, J., Valle, M., Korostelev, A., Eswar, N., Stagg, S. M., Van Roey, P., Agrawal, R. K., Harvey, S. C., Sali, A., Chapman, M. S., and Frank, J. (2003) Study of the structural dynamics of the E. coli 70S ribosome using real-space refinement, Cell, 113, 789–801.

    Article  CAS  PubMed  Google Scholar 

  43. Uhlein, M., Weglohner, W., Urlaub, H., and Wittmann-Liebold, B. (1998) Functional implications of ribosomal protein L2 in protein biosynthesis as shown by in vivo replacement studies, Biochem. J., 331, 423–430.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Nowotny, V., and Nierhaus, K. H. (1982) Initiator proteins for the assembly of the 50S subunit from Escherichia coli ribosomes, Proc. Natl. Acad. Sci. USA, 79, 7238–7242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Petrov, A., Meskauskas, A., and Dinman, J. D. (2004) Ribosomal protein L3: influence on ribosome structure and function, RNA Biol., 1, 59–65.

    Article  CAS  PubMed  Google Scholar 

  46. Pringle, M., Poehlsgaard, J., Vester, B., and Long, K. S. (2004) Mutations in ribosomal protein L3 and 23S ribosomal RNA at the peptidyl transferase center are associated with reduced susceptibility to tiamulin in Brachyspira spp. isolates, Mol. Microbiol., 54, 1295–1306.

    Article  CAS  PubMed  Google Scholar 

  47. Klitgaard, R. N., Ntokou, E., Norgaard, K., Biltoft, D., Hansen, L. H., Trædholm, N. M., Kongsted, J., and Vester, B. (2015) Mutations in the bacterial ribosomal protein L3 and their association with antibiotic resistance, Antimicrob. Agents Chemother., 59, 3518–3528.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Urlaub, H., Kruft, V., Bischof, O., Muller, E. C., and Wittmann-Liebold, B. (1995) Protein–rRNA binding features and their structural and functional implications in ribosomes as determined by cross-linking studies, EMBO J., 14, 4578–4588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Wower, I., Wower, J., Meinke, M., and Brimacombe, R. (1981) The use of 2-iminothiolane as an RNA–protein cross-linking agent in Escherichia coli ribosomes, and the localization on 23S RNA of sites cross-linked to proteins L4, L6, L21, L23, L27 and L29, Nucleic Acids Res., 9, 4285–4302.

    CAS  Google Scholar 

  50. Gabashvili, I. S., Gregory, S. T., Valle, M., Grassucci, R., Worbs, M., Wahl, M. C., Dahlberg, A. E., and Frank, J. (2001) The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22, Mol. Cell, 8, 181–188.

    Article  CAS  PubMed  Google Scholar 

  51. Zaman, S., Fitzpatrick, M., Lindahl, L., and Zengel, J. (2007) Novel mutations in ribosomal proteins L4 and L22 that confer erythromycin resistance in Escherichia coli, Mol. Microbiol., 66, 1039–1050.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Chittum, H. S., and Champney, W. S. (1994) Ribosomal protein gene sequence changes in erythromycin-resistant mutants of Escherichia coli, J. Bacteriol., 176, 6192–6198.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zengel, J. M. (2003) The extended loops of ribosomal proteins L4 and L22 are not required for ribosome assembly or L4-mediated autogenous control, RNA, 9, 1188–1197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Worbs, M., Huber, R., and Wahl, M. C. (2000) Crystal structure of ribosomal protein L4 shows RNA-binding sites for ribosome incorporation and feedback control of the S10 operon, EMBO J., 19, 807–818.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Hoffman, D. W., Davies, C., Gerchman, S. E., Kycia, J. H., Porter, S. J., White, S. W., and Ramakrishnan, V. (1994) Crystal structure of prokaryotic ribosomal protein L9: a bilobed RNA-binding protein, EMBO J., 13, 205–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hoffman, D. W., Cameron, C. S., Davies, C., White, S. W., and Ramakrishnan, V. (1996) Ribosomal protein L9: a structure determination by the combined use of X-ray crystallography and NMR spectroscopy, J. Mol. Biol., 264, 1058–1071.

    Article  CAS  PubMed  Google Scholar 

  57. Selmer, M., Gao, Y.-G., Weixlbaumer, A., and Ramakrishnan, V. (2012) Ribosome engineering to promote new crystal forms, Acta Crystallogr. Sect. D, 68, 578–583.

    Article  CAS  Google Scholar 

  58. Fischer, N., Neumann, P., Konevega, A. L., Bock, L. V., Ficner, R., Rodnina, M. V., and Stark, H. (2015) Structure of the E. coli ribosome–EF-Tu complex at <3 Å resolution by Cs-corrected cryo-EM, Nature, 520, 567–570.

    Article  PubMed  CAS  Google Scholar 

  59. Naganathan, A., Wood, M. P., and Moore, S. D. (2015) The large ribosomal subunit protein L9 enables the growth of EF-P deficient cells and enhances small subunit maturation, PLoS One, 10, e0120060.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Raibaud, S., Vachette, P., Guillier, M., Allemand, F., Chiaruttini, C., and Dardel, F. (2003) How bacterial ribosomal protein L20 assembles with 23S ribosomal RNA and its own messenger RNA, J. Biol. Chem., 278, 36522–36530.

    Article  CAS  PubMed  Google Scholar 

  61. Guillier, M., Allemand, F., Graffe, M., Raibaud, S., Dardel, F., Springer, M., and Chiaruttini, C. (2005) The N-terminal extension of Escherichia coli ribosomal protein L20 is important for ribosome assembly, but dispensable for translational feedback control, RNA, 11, 728–738.

    CAS  Google Scholar 

  62. Franceschi, F. J., and Nierhaus, K. H. (1988) Ribosomal protein L20 can replace the assembly-initiator protein L24 at low temperature, Biochemistry, 27, 7056–7059.

    Article  CAS  PubMed  Google Scholar 

  63. Raibaud, S., Lebars, I., Guillier, M., Chiaruttini, C., Bontems, F., Rak, A., Garber, M., Allemand, F., Springer, M., and Dardel, F. (2002) NMR structure of bacterial ribosomal protein L20: implications for ribosome assembly and translational control, J. Mol. Biol., 323, 143–151.

    Article  CAS  PubMed  Google Scholar 

  64. Timsit, Y., Allemand, F., Chiaruttini, C., and Springer, M. (2006) Coexistence of two protein folding states in the crystal structure of ribosomal protein L20, EMBO Rep., 7, 1013–1018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Timsit, Y., Acosta, Z., Allemand, F., Chiaruttini, C., and Springer, M. (2009) The role of disordered ribosomal protein extensions in the early steps of eubacterial 50S ribosomal subunit assembly, Int. J. Mol. Sci., 10, 817–834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Kramer, G., Rauch, T., Rist, W., Vorderwulbecke, S., Patzelt, H., Schulze-Specking, A., Ban, N., Deuerling, E., and Bukau, B. (2002) L23 protein functions as a chaperone docking site on the ribosome, Nature, 419, 171–174.

    Article  CAS  PubMed  Google Scholar 

  67. Gu, S.-Q., Peske, F., Wieden, H.-J., Rodnina, M. V., and Wintermeyer, W. (2003) The signal recognition particle binds to protein L23 at the peptide exit of the Escherichia coli ribosome, RNA, 9, 566–573.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Ullers, R. S., Houben, E. N. G., Raine, A., ten Hagen-Jongman, C. M., Ehrenberg, M., Brunner, J., Oudega, B., Harms, N., and Luirink, J. (2003) Interplay of signal recognition particle and trigger factor at L23 near the nascent chain exit site on the Escherichia coli ribosome, J. Cell Biol., 161, 679–684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Ohman, A., Rak, A., Dontsova, M., Garber, M. B., and Hard, T. (2003) NMR structure of the ribosomal protein L23 from Thermus thermophiles, J. Biomol. NMR, 26, 131–137.

    Article  PubMed  Google Scholar 

  70. Spillmann, S., and Nierhaus, K. H. (1978) The ribosomal protein L24 of Escherichia coli is an assembly protein, J. Biol. Chem., 253, 7047–7050.

    CAS  PubMed  Google Scholar 

  71. Mitra, K., Schaffitzel, C., Shaikh, T., Tama, F., Jenni, S., Brooks, C. L., Ban, N., and Frank, J. (2005) Structure of the E. coli protein-conducting channel bound to a translating ribosome, Nature, 438, 318–324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Szymanski, M., Barciszewska, M. Z., Erdmann, V. A., and Barciszewski, J. (2002) 5S ribosomal RNA database, Nucleic Acids Res., 30, 176–178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Gongadze, G. M., Korepanov, A. P., Korobeinikova, A. V., and Garber, M. B. (2008) Bacterial 5S rRNA-binding proteins of the CTC family, Biochemistry (Moscow), 73, 1405–1417.

    Article  CAS  Google Scholar 

  74. Gongadze, G. M. (2011) 5S rRNA and ribosome, Biochemistry (Moscow), 76, 1450–1464.

    Article  CAS  Google Scholar 

  75. Selivanova, O. M., Gongadze, G. M., Gudkov, A. T., and Vasiliev, V. D. (1986) Structure of protein-deficient 50S ribosomal subunits. Particles without 5S RNA–protein complex retain the L7/L12 stalk and associate with 30S subunits, FEBS Lett., 197, 79–83.

    Article  CAS  PubMed  Google Scholar 

  76. Gongadze, G. M., Perederina, A. A., Meshcheriakov, V. A., Fedorov, R. V., Moskalenko, S. E., Rak, A. V., Serganov, A. A., Shcherbakov, D. V., Nikonov, S. V., and Garber, M. B. (2001) The Thermus thermophilus 5S rRNA–protein complex: identifications of specific binding sites for proteins L5 and L18 in 5S rRNA, Mol. Biol. (Moscow), 35, 610–616.

    Article  CAS  Google Scholar 

  77. Shpanchenko, O. V., Zvereva, M. I., Dontsova, O. A., Nierhaus, K. H., and Bogdanov, A. A. (1996) 5S rRNA sugar-phosphate backbone protection in complexes with specific ribosomal proteins, FEBS Lett., 394, 71–75.

    Article  CAS  PubMed  Google Scholar 

  78. Spierer, P., and Zimmermann, R. A. (1978) Stoichiometry, cooperativity, and stability of interactions between 5S RNA and proteins L5, L18, and L25 from the 50S ribosomal subunit of Escherichia coli, Biochemistry, 17, 2474–2479.

    CAS  PubMed  Google Scholar 

  79. Korepanov, A. P., Gongadze, G. M., Garber, M. B., Court, D. L., and Bubunenko, M. G. (2007) Importance of the 5S rRNA-binding ribosomal proteins for cell viability and translation in Escherichia coli, J. Mol. Biol., 366, 1199–1208.

    Article  CAS  PubMed  Google Scholar 

  80. Osswald, M., Doring, T., and Brimacombe, R. (1995) The ribosomal neighborhood of the central fold of tRNA: cross-links from position 47 of tRNA located at the A, P or E site, Nucleic Acids Res., 23, 4635–4641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Korepanov, A. P., Korobeinikova, A. V., Shestakov, S. A., Garber, M. B., and Gongadze, G. M. (2012) Protein L5 is crucial for in vivo assembly of the bacterial 50S ribosomal subunit central protuberance, Nucleic Acids Res., 40, 9153–9159.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Nakashima, T., Yao, M., Kawamura, S., Iwasaki, K., Kimura, M., and Tanaka, I. (2001) Ribosomal protein L5 has a highly twisted concave surface and flexible arms responsible for rRNA binding, RNA, 7, 692–701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Perederina, A., Nevskaya, N., Nikonov, O., Nikulin, A., Dumas, P., Yao, M., Tanaka, I., Garber, M., Gongadze, G., and Nikonov, S. (2002) Detailed analysis of RNA–protein interactions within the bacterial ribosomal protein L5/5S rRNA complex, RNA, 8, 1548–1557.

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Spierer, P., Wang, C. C., Marsh, T. L., and Zimmermann, R. A. (1979) Cooperative interactions among protein and RNA components of the 50S ribosomal subunit of Escherichia coli, Nucleic Acids Res., 6, 1669–1682.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Woestenenk, E. A., Gongadze, G. M., Shcherbakov, D. V., Rak, A. V., Garber, M. B., Hard, T., and Berglund, H. (2002) The solution structure of ribosomal protein L18 from Thermus thermophilus reveals a conserved RNA-binding fold, Biochem. J., 363, 553–561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Turner, C. F., and Moore, P. B. (2004) The solution structure of ribosomal protein L18 from Bacillus stearother-mophilus, J. Mol. Biol., 335, 679–684.

    Article  CAS  PubMed  Google Scholar 

  87. Ciesiolka, J., Lorenz, S., and Erdmann, V. A. (1992) Structural analysis of three prokaryotic 5S rRNA species and selected 5S rRNA-ribosomal–protein complexes by means of Pb(II)-induced hydrolysis, Eur. J. Biochem., 204, 575–581.

    Article  CAS  PubMed  Google Scholar 

  88. Newberry, V., and Garrett, R. A. (1980) The role of the basic N-terminal region of protein L18 in 5S RNA–23S RNA complex formation, Nucleic Acids Res., 8, 4131–4142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Szymanski, M., Barciszewska, M. Z., Erdmann, V., and Barciszewski, J. (2003) 5S rRNA: structure and interactions, Biochem. J., 371, 641–651.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Douthwaite, S., Garrett, R. A., Wagner, R., and Feunteun, J. (1979) A ribonuclease-resistant region of 5S RNA and its relation to the RNA binding sites of proteins L18 and L25, Nucleic Acids Res., 6, 2453–2470.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Harms, J., Schluenzen, F., Zarivach, R., Bashan, A., Gat, S., Agmon, I., Bartels, H., Franceschi, F., and Yonath, A. (2001) High resolution structure of the large ribosomal subunit from a mesophilic eubacterium, Cell, 107, 679–688.

    Article  CAS  PubMed  Google Scholar 

  92. Stoldt, M., Wohnert, J., Gorlach, M., and Brown, L. R. (1998) The NMR structure of Escherichia coli ribosomal protein L25 shows homology to general stress proteins and glutaminyl-tRNA synthetases, EMBO J., 17, 6377–6384.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Lu, M., and Steitz, T. A. (2000) Structure of Escherichia coli ribosomal protein L25 complexed with a 5S rRNA fragment at 1.8 Å resolution, Proc. Natl. Acad. Sci. USA, 97, 2023–2028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Fedorov, R., Meshcheryakov, V., Gongadze, G., Fomenkova, N., Nevskaya, N., Selmer, M., Laurberg, M., Kristensen, O., Al-Karadaghi, S., Liljas, A., Garber, M., and Nikonov, S. (2001) Structure of ribosomal protein TL5 complexed with RNA provides new insights into the CTC family of stress proteins, Acta Crystallogr. D, 57, 968–976.

    Article  CAS  PubMed  Google Scholar 

  95. Gongadze, G. M., Korepanov, A. P., Korobeinikova, A. V., and Garber, M. B. (2008) Bacterial 5S rRNA-binding proteins of the CTC family, Biochemistry (Moscow), 73, 1405–1417.

    Article  CAS  Google Scholar 

  96. Petrov, A. S., Bernier, C. R., Gulen, B., Waterbury, C. C., Hershkovits, E., Hsiao, C., Harvey, S. C., Hud, N. V., Fox, G. E., Wartell, R. M., and Williams, L. D. (2014) Secondary structures of rRNAs from all three domains of life, PLoS One, 9, e88222.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Nowotny, V., and Nierhaus, K. H. (1988) Assembly of the 30S subunit from Escherichia coli ribosomes occurs via two assembly domains which are initiated by S4 and S7, Biochemistry, 27, 7051–7055.

    Article  CAS  PubMed  Google Scholar 

  98. Stern, S., Powers, T., Changchien, L. M., and Noller, H. F. (1989) RNA–protein interactions in 30S ribosomal subunits: folding and function of 16S rRNA, Science, 244, 783–790.

    Article  CAS  PubMed  Google Scholar 

  99. Mayerle, M., and Woodson, S. A. (2013) Specific contacts between protein S4 and ribosomal RNA are required at multiple stages of ribosome assembly, RNA, 19, 574–585.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Ramaswamy, P., and Woodson, S. A. (2009) Global stabilization of rRNA structure by ribosomal proteins S4, S17, and S20, J. Mol. Biol., 392, 666–677.

    Article  CAS  PubMed  Google Scholar 

  101. Powers, T., and Noller, H. F. (1995) Hydroxyl radical foot-printing of ribosomal proteins on 16S rRNA, RNA, 1, 194–209.

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Davies, C., Gerstner, R. B., Draper, D. E., Ramakrishnan, V., and White, S. W. (1998) 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, EMBO J., 17, 4545–4558.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Markus, M. A., Gerstner, R. B., Draper, D. E., and Torchia, D. A. (1998) The solution structure of ribosomal protein S4 delta41 reveals two subdomains and a positively charged surface that may interact with RNA, EMBO J., 17, 4559–4571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Greuer, B., Thiede, B., and Brimacombe, R. (1999) The cross-link from the upstream region of mRNA to ribosomal protein S7 is located in the C-terminal peptide: experimental verification of a prediction from modeling studies, RNA, 5, 1521–1525.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Osswald, M., Doring, T., and Brimacombe, R. (1995) The ribosomal neighborhood of the central fold of tRNA: cross-links from position 47 of tRNA located at the A, P or E site, Nucleic Acids Res., 23, 4635–4641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Hosaka, H., Nakagawa, A., Tanaka, I., Harada, N., Sano, K., Kimura, M., Yao, M., and Wakatsuki, S. (1997) Ribosomal protein S7: a new RNA-binding motif with structural similarities to a DNA architectural factor, Structure, 5, 1199–1208.

    Article  CAS  PubMed  Google Scholar 

  107. Wimberly, B. T., White, S. W., and Ramakrishnan, V. (1997) The structure of ribosomal protein S7 at 1.9 Å resolution reveals a beta-hairpin motif that binds double-stranded nucleic acids, Structure, 5, 1187–1198.

    Article  CAS  PubMed  Google Scholar 

  108. Held, W. A., Ballou, B., Mizushima, S., and Nomura, M. (1974) Assembly mapping of 30S ribosomal proteins from Escherichia coli, further studies, J. Biol. Chem., 249, 3103–3111.

    CAS  PubMed  Google Scholar 

  109. Ramakrishnan, V., Wimberly, B. T., Brodersen, D. E., Clemons, W. M., Morgan-Warren, R. J., Carter, A. P., Vonrhein, C., and Hartsch, T. (2000) Structure of the 30S ribosomal subunit, Nature, 407, 327–339.

    Article  PubMed  Google Scholar 

  110. Svensson, P., Changchien, L. M., Craven, G. R., and Noller, H. F. (1988) Interaction of ribosomal proteins, S6, S8, S15 and S18 with the central domain of 16S ribosomal RNA, J. Mol. Biol., 200, 301–308.

    CAS  PubMed  Google Scholar 

  111. Allmang, C., Mougel, M., Westhof, E., Ehresmann, B., and Ehresmann, C. (1994) Role of conserved nucleotides in building the 16S rRNA binding site of E. coli ribosomal protein S8, Nucleic Acids Res., 22, 3708–3714.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Mougel, M., Allmang, C., Eyermann, F., Cachia, C., Ehresmann, B., and Ehresmann, C. (1993) Minimal 16S rRNA binding site and role of conserved nucleotides in Escherichia coli ribosomal protein S8 recognition, Eur. J. Biochem., 215, 787–792.

    Article  CAS  PubMed  Google Scholar 

  113. Tishchenko, S., Nikulin, A., Fomenkova, N., Nevskaya, N., Nikonov, O., Dumas, P., Moine, H., Ehresmann, B., Ehresmann, C., Piendl, W., Lamzin, V., Garber, M., and Nikonov, S. (2001) Detailed analysis of RNA–protein interactions within the ribosomal protein S8–rRNA complex from the archaeon Methanococcus jannaschii, J. Mol. Biol., 311, 311–324.

    Article  CAS  PubMed  Google Scholar 

  114. Davlieva, M., Donarski, J., Wang, J., Shamoo, Y., and Nikonowicz, E. P. (2014) Structure analysis of free and bound states of an RNA aptamer against ribosomal protein S8 from Bacillus anthracis, Nucleic Acids Res., 42, 10795–10808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Davies, C., Ramakrishnan, V., and White, S. W. (1996) Structural evidence for specific S8–RNA and S8–protein interactions within the 30S ribosomal subunit: ribosomal protein S8 from Bacillus stearothermophilus at 1.9 Å resolution, Structure, 4, 1093–1104.

    Article  CAS  PubMed  Google Scholar 

  116. Nevskaya, N., Tishchenko, S., Nikulin, A., Al-Karadaghi, S., Liljas, A., Ehresmann, B., Ehresmann, C., Garber, M., and Nikonov, S. (1998) Crystal structure of ribosomal protein S8 from Thermus thermophilus reveals a high degree of structural conservation of a specific RNA binding site, J. Mol. Biol., 279, 233–244.

    Article  CAS  PubMed  Google Scholar 

  117. Menichelli, E., Edgcomb, S. P., Recht, M. I., and Williamson, J. R. (2012) The structure of Aquifex aeolicus ribosomal protein S8 reveals a unique subdomain that contributes to an extremely tight association with 16S rRNA, J. Mol. Biol., 415, 489–502.

    Article  CAS  PubMed  Google Scholar 

  118. Nikulin, A., Serganov, A., Ennifar, E., Tishchenko, S., Nevskaya, N., Shepard, W., Portier, C., Garber, M., Ehresmann, B., Ehresmann, C., Nikonov, S., and Dumas, P. (2000) Crystal structure of the S15–rRNA complex, Nat. Struct. Mol. Biol., 7, 273–277.

    Article  CAS  Google Scholar 

  119. Agalarov, S. C. (2000) Structure of the S15, S6, S18–rRNA complex: assembly of the 30S ribosome central domain, Science, 288, 107–112.

    Article  CAS  PubMed  Google Scholar 

  120. Berglund, H., Rak, A., Serganov, A., Garber, M., and Hard, T. (1997) Solution structure of the ribosomal RNA binding protein S15 from Thermus thermophiles, Nat. Struct. Biol., 4, 20–23.

    Article  CAS  PubMed  Google Scholar 

  121. Clemons, W. M., Davies, C., White, S. W., and Ramakrishnan, V. (1998) Conformational variability of the N-terminal helix in the structure of ribosomal protein S15, Structure, 6, 429–438.

    Article  CAS  PubMed  Google Scholar 

  122. Yaguchi, M., Wittmann, H. G., Cabezon, T., DeWilde, M., Villarroel, R., Herzog, A., and Bollen, A. (1976) Alteration of ribosomal protein S17 by mutation linked to neamine resistance in Escherichia coli. II. Localization of the amino acid replacement in protein S17 from a meaA mutant, J. Mol. Biol., 104, 617–620.

    Article  CAS  PubMed  Google Scholar 

  123. Bollen, A., Cabezon, T., De Wilde, M., Villarroel, R., and Herzog, A. (1975) Alteration of ribosomal protein S17 by mutation linked to neamine resistance in Escherichia coli. I. General properties of neaA mutants, J. Mol. Biol., 99, 795–806.

    Article  CAS  PubMed  Google Scholar 

  124. Golden, B. L., Hoffman, D. W., Ramakrishnan, V., and White, S. W. (1993) Ribosomal protein S17: characterization of the three-dimensional structure by proton and nitrogen-15 NMR, Biochemistry, 32, 12812–12820.

    Article  CAS  PubMed  Google Scholar 

  125. Hedrick, E. G., and Hill, W. E. (2010) Protein S20 binds two 16S rRNA sites as assembly is initiated, J. Mol. Biol., 401, 493–502.

    Article  CAS  PubMed  Google Scholar 

  126. Tobin, C., Mandava, C. S., Ehrenberg, M., Andersson, D. I., and Sanyal, S. (2010) Ribosomes lacking protein S20 are defective in mRNA binding and subunit association, J. Mol. Biol., 397, 767–776.

    Article  CAS  PubMed  Google Scholar 

  127. Ryden-Aulin, M., Shaoping, Z., Kylsten, P., and Isaksson, L. A. (1993) Ribosome activity and modification of 16S RNA are influenced by deletion of ribosomal protein S20, Mol. Microbiol., 7, 983–992.

    Article  CAS  PubMed  Google Scholar 

  128. Gotz, F., Dabbs, E. R., and Gualerzi, C. O. (1990) Escherichia coli 30S mutants lacking protein S20 are defective in translation initiation, Biochim. Biophys. Acta, 1050, 93–97.

    Article  CAS  PubMed  Google Scholar 

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  1. Institute of Protein Research, Russian Academy of Sciences, 142290, Pushchino, Moscow Region, Russia

    A. D. Nikulin

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Original Russian Text © A. D. Nikulin, 2018, published in Uspekhi Biologicheskoi Khimii, 2018, Vol. 58, pp. 241–284.

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Nikulin, A.D. Structural Aspects of Ribosomal RNA Recognition by Ribosomal Proteins. Biochemistry Moscow 83 (Suppl 1), S111–S133 (2018). https://doi.org/10.1134/S0006297918140109

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