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Biochemistry (Moscow)

, Volume 81, Issue 13, pp 1589–1601 | Cite as

Investigation of structure of the ribosomal L12/P stalk

  • I. V. Mitroshin
  • M. B. GarberEmail author
  • A. G. Gabdulkhakov
Review

Abstract

This review contains recent data on the structure of the functionally important ribosomal domain, L12/P stalk, of the large ribosomal subunit. It is the most mobile site of the ribosome; it has been found in ribosomes of all living cells, and it is involved in the interaction between ribosomes and translation factors. The difference between the structures of the ribosomal proteins forming this protuberance (despite their general resemblance) determines the specificity of interaction between eukaryotic and prokaryotic ribosomes and the respective protein factors of translation. In this review, works on the structures of ribosomal proteins forming the L12/P-stalk in bacteria, archaea, and eukaryotes and data on structural aspects of interactions between these proteins and rRNA are described in detail.

Keywords

ribosome stalk ribosomal proteins 

Abbreviations

IF2

translation initiation factor 2

mRNA

messenger RNA

rRNA

ribosomal RNA

tRNA

transport RNA

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References

  1. 1.
    Lake, J. A. (1976) Ribosome structure determined by electron microscopy of Escherichia coli small subunits, large subunits and monomeric ribosomes, J. Mol. Biol., 105, 131–159.CrossRefPubMedGoogle Scholar
  2. 2.
    Boublik, M., Hellmann, W., and Roth, H. E. (1976) Localization of ribosomal proteins L7L12 in the 50S subunit of Escherichia coli ribosomes by electron microscopy, J. Mol. Biol., 107, 479–490.CrossRefPubMedGoogle Scholar
  3. 3.
    Spirin, A. S. (2011) Molecular Biology: Ribosomes and Protein Biosynthesis [in Russian], Akademiya, Moscow.Google Scholar
  4. 4.
    Huang, C., Mandava, C. S., and Sanyal, S. (2010) The ribosomal stalk plays a key role in IF2-mediated association of the ribosomal subunits, J. Mol. Biol., 399, 145–153CrossRefPubMedGoogle Scholar
  5. 5.
    Kaltschmidt, E., and Wittmann, H. G. (1970) Ribosomal proteins. XII. Number of proteins in small and large ribosomal subunits of Escherichia coli as determined by twodimensional gel electrophoresis, Proc. Natl. Acad. Sci. USA, 67, 1276–1282.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Liao, D., and Dennis, P. P. (1994) Molecular phylogenies based on ribosomal protein L11, L1, L10, and L12 sequences, J. Mol. Evol., 38, 405–419.CrossRefPubMedGoogle Scholar
  7. 7.
    Ban, N., Beckmann, R., Cate, J. H. D., Dinman, J. D., Dragon, F., Ellis, S. R., Lafontaine, D. L. J., Lindahl, L., Liljas, A., Lipton, J. M., McAlear, M., Moore, P. B., Noller, H. F., Ortega, J., Panse, V. G., Ramakrishnan, V., Spahn, C. M. T., Steitz, T., 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.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Highland, J. H., and Howard, G. A. (1975) Assembly of ribosomal proteins L7, L10, L11, and L12 on the 50S subunit of Escherichia coli, J. Biol. Chem., 250, 831–834.Google Scholar
  9. 9.
    Hardy, S. J. S. (1975) The stoichiometry of the ribosomal proteins of Escherichia coli, Mol. Gen. Genet., 140, 253–274.CrossRefPubMedGoogle Scholar
  10. 10.
    Terhorst, C., Moller, W., Laursen, R., and WittmannLiebold, B. (1972) Amino acid sequence of a 50S ribosomal protein involved in both EF-G and EF-T dependent GTPhydrolysis, FEBS Lett., 28, 325–328.CrossRefPubMedGoogle Scholar
  11. 11.
    Ramagopal, S., and Subramanian, A. R. (1974) Alteration in the acetylation level of ribosomal protein L12 during growth cycle of Escherichia coli, Proc. Natl. Acad. Sci. USA, 71, 2136–2140.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Gordiyenko, Y., Deroo, S., Zhou, M., Videler, H., and Robinson, C. V. (2008) Acetylation of L12 increases interactions in the Escherichia coli ribosomal stalk complex, J. Mol. Biol., 380, 404–414.CrossRefPubMedGoogle Scholar
  13. 13.
    Pettersson, I., and Kurland, C. G. (1980) Ribosomal protein L7/L12 is required for optimal translation, Biochemistry, 77, 4007–4010.Google Scholar
  14. 14.
    Kirsebom, L. A., and Isaksson, L. A. (1985) Involvement of ribosomal protein L7/L12 in control of translational accuracy, Proc. Natl. Acad. Sci. USA, 82, 717–721.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Sander, G., Marsh, R. C., Voigt, J., and Parmeggiani, A. (1975) A comparative study of the 50S ribosomal subunit and several 50S subparticles in EF-T- and EF-G-dependent activities, Biochemistry, 14, 1805–1814.CrossRefPubMedGoogle Scholar
  16. 16.
    Koteliansky, V. E., Domogatsky, S. P., and Gudkov, A. T. (1978) Dimer state of protein L7/L12 and EF-G-dependent reactions on ribosomes, FEBS J., 90, 319–323.CrossRefGoogle Scholar
  17. 17.
    Donner, D., Villems, R., Liljas, A., and Kurland, C. G. (1978) Guanosinetriphosphatase activity dependent on elongation factor Tu and ribosomal protein L7/L12, Proc. Natl. Acad. Sci. USA, 75, 3192–3195.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Brot, N., and Weissbach, H. (1981) Chemistry and biology of E. coli ribosomal protein L12, Mol. Cell. Biochem., 63, 47–63.CrossRefGoogle Scholar
  19. 19.
    Wong, K.-P., and Paradies, H. H. (1974) Shape properties of proteins L7 and L12 from E. coli ribosomes, Biochem. Biophys. Res. Commun., 61, 178–184.CrossRefPubMedGoogle Scholar
  20. 20.
    Kar, E. G., and Aune, K. C. (1981) Solution behavior of proteins L7/L12 from the 50S ribosomal subunit of Escherichia coli, Biochemistry, 20, 4638–4646.CrossRefPubMedGoogle Scholar
  21. 21.
    Gudkov, A. T., and Behlke, J. (1978) The N-terminal sequence protein of L7/L12 is responsible for its dimerization, FEBS J., 90, 309–312.CrossRefGoogle Scholar
  22. 22.
    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.CrossRefPubMedGoogle Scholar
  23. 23.
    Gudkov, A. T., Gongadze, G. M., Bushuev, V. N., and Okon, M. S. (1982) Proton nuclear magnetic resonance study of the ribosomal protein L7/L12 in situ, FEBS Lett., 138, 229–232.CrossRefPubMedGoogle Scholar
  24. 24.
    Olson, H. M., Tewari, D. S., Traut, R. R., and Glitz, D. G. (1986) Localization of two epitopes of protein L7/L12 to both the body and stalk of the large ribosomal subunit, J. Biol. Chem., 261, 6924–6932.PubMedGoogle Scholar
  25. 25.
    Oleinikov, A. V., Jokhadze, G. G., and Traut, R. R. (1998) A single-headed dimer of Escherichia coli ribosomal protein L7/L12 supports protein synthesis, Proc. Natl. Acad. Sci. USA, 95, 4215–4218.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Bocharov, E. V., Sobol, A. G., Pavlov, K. V., Korzhnev, D. M., Jaravine, V. A., Gudkov, A. T., and Arseniev, A. S. (2004) From structure and dynamics of protein L7/L12 to molecular switching in ribosome, J. Biol. Chem., 279, 17697–17706.CrossRefPubMedGoogle Scholar
  27. 27.
    Dey, D., Oleinikov, D., Dey, A. V., and Traut, R. R. (1995) The hinge region of Escherichia coli ribosomal protein L7/L12 is required for factor binding and GTP hydrolysis, Biochimie, 77, 925–930.CrossRefPubMedGoogle Scholar
  28. 28.
    Bubunenko, M. G., Chuikov, S. V., and Gudkov, A. T. (1992) The length of the interdomain region of the L7/L12 protein is important for its function, FEBS J., 313, 232–234.CrossRefGoogle Scholar
  29. 29.
    Leijonmarck, M., Eriksson, S., and Liljas, A. (1980) Crystal structure of a ribosomal component at 2.6 Å resolution, Nature, 286, 824–826.CrossRefPubMedGoogle Scholar
  30. 30.
    Wahl, M. C., Bourenkov, G. P., Bartunik, H. D., and Huber, R. (2000) Flexibility, conformational diversity and two dimerization modes in complexes of ribosomal protein L12, EMBO J., 19, 174–186.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Gudkov, A. T., Tumanova, L. G., Venyaminov, S. Y., and Khechinashvilli, N. N. (1978) Stoichiometry and properties of the complex between ribosomal proteins L7 and L10 in solution, FEBS Lett., 93, 215–218.CrossRefPubMedGoogle Scholar
  32. 32.
    Pettersson, I., Hardy, S. J. S., and Liljas, A. (1976) The ribosomal protein L8 is a complex of L7/L12 and L10, FEBS Lett., 64, 135–138.CrossRefPubMedGoogle Scholar
  33. 33.
    Pettersson, I., and Liljas, A. (1979) The stoichiometry and reconstruction of a stable protein complex from Escherichia coli ribosomes, FEBS Lett., 98, 139–144.CrossRefPubMedGoogle Scholar
  34. 34.
    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.CrossRefPubMedGoogle Scholar
  35. 35.
    Ilag, L. L., Videler, H., McKay, A. R., Sobott, F., Fucini, P., Nierhaus, K. H., and Robinson, C. V. (2005) Heptameric (L12)6/L10 rather than canonical pentameric complexes are found by tandem MS of intact ribosomes from thermophilic bacteria, Proc. Natl. Acad. Sci. USA, 102, 8192–8197.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Gordiyenko, Y., Videler, H., Zhou, M., McKay, A. R., Fucini, P., Biegel, E., Muller, V., and Robinson, C. V. (2010) Mass spectrometry defines the stoichiometry of ribosomal stalk complexes across the phylogenetic tree, Mol. Cell. Proteom., 9, 1774–1783.CrossRefGoogle Scholar
  37. 37.
    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 backbone in the ribosomal GTPase centre, J. Mol. Biol., 234, 1013–1020.CrossRefPubMedGoogle Scholar
  38. 38.
    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.CrossRefPubMedGoogle Scholar
  39. 39.
    Climie, S. C., and Friesen, J. D. (1987) Feedback regulation of the rplJL-rpoBC ribosomal protein operon of Escherichia coli requires a region of mRNA secondary structure, J. Mol. Biol., 198, 371–381.CrossRefPubMedGoogle Scholar
  40. 40.
    Johnsen, M., Christensen, T., Dennis, P. P., and Fiil, N. P. (1982) Autogenous control: ribosomal protein L10–L12 complex binds to the leader sequence of its mRNA, EMBO J., 1, 999–1004.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Harms, J., Schluenzen, F., Zarivach, R., Bashan, A., Gat, S., Agmon, I., Bartels, H., and Yonath, A. (2001) High resolution structure of the large ribosomal subunit from a mesophilic eubacterium, Cell, 107, 679–688.CrossRefPubMedGoogle Scholar
  42. 42.
    Klein, D. J., Schmeing, T. M., Moore, P. B., and Steitz, T. A. (2001) The kink-turn: a new RNA secondary structure motif, EMBO J., 20, 4214–4221.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Iben, J. R., and Draper, D. E. (2008) Specific interactions of the L10–(L12)4 ribosomal protein complex with mRNA, rRNA, and L11, Biochemistry, 10, 2721–2731.CrossRefGoogle Scholar
  44. 44.
    Dijk, J., Garrett, R. A., and Muller, R. (1979) Studues on the binding of the ribosomal protein complex L7/12–L10 and protein L11 to the 5′-one third of 23S RNA: a functional centre of the 50S subunit, Nucleic Acids Res., 6, 2717–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Stark, M. J. R., Cundliffe, E., Dijk, J., and Stoeffler, G. (1980) Functional homology between E. coli ribosomal protein L11 and B. megaterium protein BM-L11, Mol. Gen. Genet., 15, 11–15.CrossRefGoogle Scholar
  46. 46.
    Tate, W. P., Dognin, M. J., Noah, M., Stoffler-Meilicke, M., and Stoffler, G. (1984) The NH2-terminal domain of Escherichia coli ribosomal protein L11, J. Biol. Chem., 259, 7317–7324.PubMedGoogle Scholar
  47. 47.
    Schrier, P. I., and Moller, W. (1975) The involvement of 50S ribosomal protein L11 in the EF-G dependent GTP hydrolysis of E. coli ribosomes, FEBS Lett., 54, 130–134.CrossRefPubMedGoogle Scholar
  48. 48.
    Kazemie, M. (1976) Binding of aminoacyl-tRNA to reconstituted subparticles of Escherichia coli large ribosomal subunits, Eur. J. Biochem., 67, 373–378.CrossRefPubMedGoogle Scholar
  49. 49.
    Ilin, S., Hoskins, A., Ohlenschläger, O., Jonker, H. R. A., Schwalbe, H., and Wohnert, J. (2005) Domain reorientation and induced fit upon RNA binding: solution structure and dynamics of ribosomal protein L11 from Thermotoga maritima, ChemBioChem, 6, 1611–1618.CrossRefPubMedGoogle Scholar
  50. 50.
    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.CrossRefPubMedGoogle Scholar
  51. 51.
    Harms, J. M., Wilson, D. N., Schluenzen, F., Connell, S. R., Stachelhaus, T., Zaborowska, Z., Spahn, C. M. T., and Fucini, P. (2008) Translational regulation via L11: molecular switches on the ribosome turned on and off by thiostrepton and micrococcin, Mol. Cell, 30, 26–38.CrossRefPubMedGoogle Scholar
  52. 52.
    Bausch, S. L., Poliakova, E., and Draper, D. E. (2005) Interactions of the N-terminal domain of ribosomal protein L11 with thiostrepton and rRNA, J. Biol. Chem., 280, 29956–29963.CrossRefPubMedGoogle Scholar
  53. 53.
    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.CrossRefPubMedGoogle Scholar
  54. 54.
    Thompson, J., Cundliffe, E., and Stark, M. (1979) Binding of thiostrepton to a complex of 23S rRNA with ribosomal protein L11, FEBS J., 98, 261–265.CrossRefGoogle Scholar
  55. 55.
    Cundliffe, E., Dixon, P., Stark, M., Stoffler, G., Ehrlich, R., Stoffler-Meilicke, M., and Cannon, M. (1979) Ribosomes in thiostrepton-resistant mutants of Bacillus megaterium lacking a single 50S subunit protein, J. Mol. Biol., 132, 235–252.CrossRefPubMedGoogle Scholar
  56. 56.
    Uchiumi, T., Albert, J. W., and Traut, R. R. (1987) Topography and stoichiometry of acidic proteins in large ribosomal subunits from Artemia salina as determined by crosslinking, Proc. Natl. Acad. Sci. USA, 84, 5580–5584.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Van Agthoven, A., Kriek, J., Amons, R., and Moller, W. (1978) Isolation and characterization of the acidic phosphoproteins of 60S ribosomes from Artemia salina and rat liver, Eur. J. Biochem., 91, 553–565.CrossRefPubMedGoogle Scholar
  58. 58.
    Santos, C., and Ballesta, J. P. (1994) Ribosomal protein P0, contrary to phosphoproteins P1 and P2, is required for ribosome activity and Saccharomyces cerevisiae viability, J. Biol. Chem., 269, 15689–15696.PubMedGoogle Scholar
  59. 59.
    Maki, Y., Hashimoto, T., Zhou, M., Naganuma, T., Ohta, J., Nomura, T., Robinson, C. V., and Uchiumi, T. (2007) Three binding sites for stalk protein dimers are generally present in ribosomes from archaeal organism, J. Biol. Chem., 282, 32827–32833.CrossRefPubMedGoogle Scholar
  60. 60.
    Casiano, C., Matheson, A. T., and Traut, R. R. (1990) Occurrence in the archaebacterium Sulfolobus solfutaricus ribosomal protein complex corresponding to Escherichia coli (L7/L12)4–L10 and eukaryotic (P1)2/(P2)2–P0, J. Biol. Chem., 265, 18757–18761.PubMedGoogle Scholar
  61. 61.
    Szick, K., Springer, M., and Bailey-Serres, J. (1998) Evolutionary analyses of the 12-kDa acidic ribosomal Pproteins reveal a distinct protein of higher plant ribosomes, Proc. Natl. Acad. Sci. USA, 95, 2378–2383.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Bailey-Serres, J., Vangala, S., Szick, K., and Lee, C.-H. K. (1997) Acidic phosphoprotein complex of the 60S ribosomal subunit of maize seedling roots, Plant Physiol., 114, 1293–1305.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Tchorzewski, M., Boldyreff, B., Issinger, O. G., and Grankowski, N. (2000) Analysis of the protein–protein interactions between the human acidic ribosomal P-proteins: evaluation by the two hybrid system, Int. J. Biochem. Cell Biol., 32, 737–746.CrossRefPubMedGoogle Scholar
  64. 64.
    Nusspaumer, G., Remacha, M., and Ballesta, J. P. (2000) Phosphorylation and N-terminal region of yeast ribosomal protein P1 mediate its degradation, which is prevented by protein P2, EMBO J., 19, 6075–6084.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Casiano, C., and Traut, R. R. (1991) Protein topography of Sulfolobus solfataricus ribosomes by cross-linking with 2iminothiolane, J. Biol. Chem., 266, 21578–21583.PubMedGoogle Scholar
  66. 66.
    Lee, K.-M., Yu, C. W.-H., Chiu, T. Y.-H., Sze, K.-H., Shaw, P.-C., and Wong, K.-B. (2012) Solution structure of the dimerization domain of the eukaryotic stalk P1/P2 complex reveals the structural organization of eukaryotic stalk complex, Nucleic Acids Res., 40, 3172–3182.CrossRefPubMedGoogle Scholar
  67. 67.
    Naganuma, T., Nomura, N., Yao, M., Mochizuki, M., Uchiumi, T., and Tanaka, I. (2010) Structural basis for translation factor recruitment to the eukaryotic/archaeal ribosomes, J. Biol. Chem., 285, 4747–4756.CrossRefPubMedGoogle Scholar
  68. 68.
    Nomura, T., Nakano, K., Maki, Y., Naganuma, T., Nakashima, T., Tanaka, I., Kimura, M., Hachimori, A., and Uchiumi, T. (2006) In vitro reconstitution of the GTPase-associated centre of the archaebacterial ribosome: the functional features observed in a hybrid form with Escherichia coli 50S subunits, Biochem. J., 396, 565–571.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Nomura, N., Honda, T., Baba, K., Naganuma, T., Tanzawa, T., Arisaka, F., Noda, M., Uchiyama, S., Tanaka, I., Yao, M., and Uchiumi, T. (2012) Archaeal ribosomal stalk protein interacts with translation factors in a nucleotide-independent manner via its conserved C-terminus, Proc. Natl. Acad. Sci. USA, 109, 3748–3753.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Naganuma, T., Shiogama, K., and Uchiumi, T. (2007) The N-terminal regions of eukaryotic acidic phosphoproteins P1 and P2 are crucial for heterodimerization and assembly into the ribosomal GTPase-associated center, Genes Cells, 12, 501–510.CrossRefPubMedGoogle Scholar
  71. 71.
    Uchiumi, T., Traut, R. R., and Kominami, R. (1990) Monoclonal antibodies against acidic phosphoproteins P0, P1, and P2 of eukaryotic ribosomes as functional probes, J. Biol. Chem., 265, 89–95.PubMedGoogle Scholar
  72. 72.
    Lee, K.-M., Yusa, K., Chu, L.-O., Yu, C. W.-H., Oono, M., Miyoshi, T., Ito, K., Shaw, P.-C., Wong, K.-B., and Uchiumi, T. (2013) Solution structure of human P1•P2 heterodimer provides insights into the role of eukaryotic stalk in recruiting the ribosome-inactivating protein trichosanthin to the ribosome, Nucleic Acids Res., 41, 8776–8787.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Ito, K., Honda, T., Suzuki, T., Miyoshi, T., Murakami, R., Yao, M., and Uchiumi, T. (2014) Molecular insights into the interaction of the ribosomal stalk protein with elongation factor 1α, Nucleic Acids Res., 42, 14042–14052.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Grela, P., Bernado, P., Svergun, D., Kwiatowski, J., Abramczyk, D., Grankowski, N., and Tchorzewski, M. (2008) Structural relationships among the ribosomal stalk proteins from the three domains of life, J. Mol. Evol., 67, 154–167.CrossRefPubMedGoogle Scholar
  75. 75.
    Baba, K., Tumuraya, K., Tanaka, I., Yao, M., and Uchiumi, T. (2013) Molecular dissection of the silkworm ribosomal stalk complex: the role of multiple copies of the stalk proteins, Nucleic Acids Res., 41, 3635–3643.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Hagiya, A., Naganuma, T., Maki, Y., Ohta, J., Tohkairin, Y., Shimizu, T., Nomura, T., Hachimori, A., and Uchiumi, T. (2005) A mode of assembly of P0, P1, and P2 proteins at the GTPase-associated center in animal ribosome: in vitro analyses with P0 truncation mutants, J. Biol. Chem., 280, 39193–39199.CrossRefPubMedGoogle Scholar
  77. 77.
    Kravchenko, O., Mitroshin, I., Nikonov, S., Piendl, W., and Garber, M. (2010) Structure of a two-domain N-terminal fragment of ribosomal protein L10 from Methanococcus jannaschii reveals a specific piece of the archaeal ribosomal stalk, J. Mol. Biol., 399, 214–220.CrossRefPubMedGoogle Scholar
  78. 78.
    Santos, C., Remacha, M., and Ballesta, J. P. G. (2004) Ribosomal P0 protein domain involved in selectivity of antifungal sordarin derivatives, Antimicrob. Agents Chemother., 48, 2930–2936.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Choi, A., Wong, E., Lee, K.-M., and Wong, K.-B. (2015) Structures of eukaryotic ribosomal stalk proteins and its complex with trichosanthin, and their implications in recruiting ribosome-inactivating proteins to the ribosomes, Toxins, 7, 638–647.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Shimizu, T., Nakagaki, M., Nishi, Y., Kobayashi, Y., Hachimori, A., and Uchiumi, T. (2002) Interaction among silkworm ribosomal proteins P1, P2 and P0 required for functional protein binding to the GTPase-associated domain of 28S rRNA, Nucleic Acids Res., 30, 2620–2627.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Uchiumi, T., and Kominami, R. (1997) Binding of mammalian ribosomal protein complex P0•P1•P2 and protein L12 to the GTPase-associated domain of 28S ribosomal RNA and effect on the accessibility to anti-28S RNA autoantibody, J. Biol. Chem., 272, 3302–3308.CrossRefPubMedGoogle Scholar
  82. 82.
    Uchiumi, T., Kikuchi, M., Terao, K., Iwasaki, K., and Ogata, K. (1986) Cross-linking of elongation factor 2 to rat-liver ribosomal proteins by 2-iminothiolane, Eur. J. Biochem., 156, 37–48.CrossRefPubMedGoogle Scholar
  83. 83.
    Ben-Shem, A., De Loubresse, S., Melnikov, N. G., Jenner, L., Yusupova, G., and Yusupov, M. (2011) The structure of the eukaryotic ribosome at 3.0 Å resolution, Science, 334, 1524–1529.CrossRefPubMedGoogle Scholar
  84. 84.
    Gabdulkhakov, A., Nikonov, S., and Garber, M. (2013) Revisiting the Haloarcula marismortui 50S ribosomal subunit model, Acta Crystallogr. Sect. D Biol. Crystallogr., 69, 997–1004.CrossRefGoogle Scholar
  85. 85.
    Shcherbakov, D., Dontsova, M., Tribus, M., Garber, M., and Piendl, W. (2006) Stability of the “L12 stalk” in ribosomes from mesophilic and (hyper)thermophilic Archaea and Bacteria, Nucleic Acids Res., 34, 5800–5814.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Beauclerk, A. A. D., Hummel, H., Holmes, D. J., Bock, A., and Cundliffe, E. (1985) Studies of the GTPase domain of archaebacterial ribosomes, FEBS J., 151, 245–255.CrossRefGoogle Scholar
  87. 87.
    Sanchez-Madrid, F., Vidales, F. J., and Ballesta, J. P. G. (1981) Functional role of acidic ribosomal poteins. Interchangeability of proteins from bacterial and eukaryotic cells, Biochemistry, 20, 3263–3266.CrossRefPubMedGoogle Scholar
  88. 88.
    Stoffler-Meilicke, M., and Stoffler, G. (1991) The binding site of ribosomal protein L10 in Eubacteria and Archaebacteria is conserved: reconstitution of chimeric 50S subunits, Biochimie, 73, 797–804.CrossRefPubMedGoogle Scholar
  89. 89.
    Uchiumi, T., Hori, K., Nomura, T., and Hachimori, A. (1999) Replacement of L7/L12–L10 protein complex in Escherichia coli ribosomes with the eukaryotic counterpart changes the specificity of elongation factor binding, J. Biol. Chem., 274, 27578–27582.CrossRefPubMedGoogle Scholar
  90. 90.
    Han, M.-J., Cimen, H., Miller-Lee, J. L., Koc, H., and Koc, E. C. (2011) Purification of human mitochondrial ribosomal L7/L12 stalk proteins and reconstitution of functional hybrid ribosomes in Escherichia coli, Protein Expr. Purif., 78, 48–54.CrossRefPubMedGoogle Scholar
  91. 91.
    Uchiumi, T., Honma, S., Endo, Y., and Hachimori, A. (2002) Ribosomal proteins at the stalk region modulate functional rRNA structures in the GTPase center, J. Biol. Chem., 277, 41401–41409.CrossRefPubMedGoogle Scholar
  92. 92.
    Ban, N., Nissen, P., Hansen, J., Capel, M., Moore, P. B., and Steitz, T. A. (1999) Placement of protein and RNA structures into a 5 Å-resolution map of the 50S ribosomal subunit, Nature, 400, 841–847.CrossRefPubMedGoogle Scholar
  93. 93.
    Gao, Y.-G., Selmer, M., Dunham, C. M., Weixlbaumer, A., Kelley, A. C., and Ramakrishnan, V. (2009) The structure of the ribosome with elongation factor G trapped in the posttranslocational state, Science, 326, 694–699.CrossRefPubMedPubMedCentralGoogle Scholar

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© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • I. V. Mitroshin
    • 1
  • M. B. Garber
    • 1
    Email author
  • A. G. Gabdulkhakov
    • 1
  1. 1.Institute of Protein ResearchRussian Academy of SciencesPushchino, Moscow RegionRussia

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