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Biochemistry (Moscow)

, Volume 75, Issue 13, pp 1501–1516 | Cite as

Ribosomal tunnel and translation regulation

  • A. A. BogdanovEmail author
  • N. V. Sumbatyan
  • A. V. Shishkina
  • V. V. Karpenko
  • G. A. Korshunova
Review

Abstract

This review describes the results of recent studies of the ribosomal tunnel (RT), the major function of which is to allow the smooth passage of nascent polypeptides with different sequences from the peptidyl transferase center of the ribosome to the tunnel exit, where the folding of protein molecules begins. The features of structural organization of RT and their role in modulation and stabilization of the nascent chain conformation are discussed. Structural features of macrolide binding sites as well as application of macrolide antibiotics and their derivatives as tools to investigate ligand-tunnel wall interactions are also considered. Several examples of strong and specific interactions of regulatory polypeptides with nucleotide and amino acid residues of RT that lead to ribosome stalling and translational arrest are described in detail. The role of these events in regulation of expression of certain genes is discussed on the basis of recent high-resolution structural studies of nascent chains in the RT.

Key words

ribosome ribosomal tunnel growing polypeptide chain macrolides leader peptides translation regulation cation-π interactions 

Abbreviations

cryo-EM

cryoelectron microscopy

FRET

Förster (fluorescence) resonance energy transfer

PTC

ribosome peptidyl transferase center

RT

ribosomal tunnel

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References

  1. 1.
    Malkin, L. I., and Rich, A. (1967) J. Mol. Biol., 26, 329–346.PubMedCrossRefGoogle Scholar
  2. 2.
    Blobel, G., and Sabatini, D. D. (1970) J. Cell. Biol., 45, 130–145.PubMedCrossRefGoogle Scholar
  3. 3.
    Bernabeu, C., and Lake, J. A. (1982) Proc. Natl. Acad. Sci. USA, 79, 3111–3115.PubMedCrossRefGoogle Scholar
  4. 4.
    Bernabeu, C., Tobin, E., Fowier, A., Zabin, I., and Lake, J. A. (1983) J. Cell. Biol., 96, 1471–1474.PubMedCrossRefGoogle Scholar
  5. 5.
    Milligan, R. A., and Unwin, P. N. T. (1986) Nature, 319, 693–695.PubMedCrossRefGoogle Scholar
  6. 6.
    Yonath, A., Leonard, K. R., and Wittmann, H. G. (1987) Science, 236, 813–816.PubMedCrossRefGoogle Scholar
  7. 7.
    Ryabova, L. A., Selivanova, O. M., Baranov, V. I., Vasiliev, V. D., and Spirin, A. S. (1988) FEBS Lett., 226, 255–260.PubMedCrossRefGoogle Scholar
  8. 8.
    Wang, S., Sakai, H., and Wiedmann, M. (1995) J. Cell. Biol., 130, 519–528.PubMedCrossRefGoogle Scholar
  9. 9.
    Frank, J., Zhu, J., Penczek, P., Li, Y., Srivastava, S., Verschoor, A., Radermacher, M., Grassucci, R., Lata, R. K., and Agrawal, R. K. (1995) Nature, 376, 441–444.PubMedCrossRefGoogle Scholar
  10. 10.
    Choi, K. M., and Brimacombe, R. (1998) Nucleic Acid Res., 15, 887–895.CrossRefGoogle Scholar
  11. 11.
    Mueller, F., Sommer, I., Baranov, P., Matadeen, R., Stoldt, M., Woehnert, J., Goerlach, M., van Heel, M., and Brimacombe, R. (2000) J. Mol. Biol., 298, 35–59.PubMedCrossRefGoogle Scholar
  12. 12.
    Ban, N., Nissen, P., Hansen, J., Moore, P. B., and Steitz, T. A. (2000) Science, 289, 905–920.PubMedCrossRefGoogle Scholar
  13. 13.
    Nissen, P., Hansen, J., Ban, N., Moore, P. B., and Steitz, T. A. (2000) Science, 289, 920–930.PubMedCrossRefGoogle Scholar
  14. 14.
    Harms, J., Schluenzen, F., Zarivach, R., Bashan, A., Gat, S., Agmon, I., Bartels, H., Franceschi, F., and Yonath, A. (2001) Cell, 107, 679–688.PubMedCrossRefGoogle Scholar
  15. 15.
    Brimacombe, R. (2000) Structure, 8, R195–R200.PubMedCrossRefGoogle Scholar
  16. 16.
    Sergiev, P., Leonov, A., Dokudovskaya, S., Shpanchenko, O., Dontsova, O., Bogdanov, A., Rinke-Appel, J., Mueller, F., Osswald, M., von Knoblauch, K., and Brimacombe, R. (2001) Cold Spring Harb. Symp. Quant. Biol., 66, 87–100.PubMedCrossRefGoogle Scholar
  17. 17.
    Sergiev, P. V., Dontsova, O. V., and Bogdanov, A. A. (2001) Mol. Biol. (Moscow), 35, 559–583.CrossRefGoogle Scholar
  18. 18.
    Schmeing, T. M., and Ramakrishnan, V. (2009) Nature, 461, 1234–1242.PubMedCrossRefGoogle Scholar
  19. 19.
    Hardesty, B., and Kramer, G. (2001) Progr. Nucleic Acid Res. Mol. Biol., 66, 41–66.CrossRefGoogle Scholar
  20. 20.
    Ramu, H., Mankin, A., and Vazquez-Laslop, N. (2008) Mol. Microbiol., 71, 811–824.PubMedCrossRefGoogle Scholar
  21. 21.
    Reusch, R. N., and Sadoff, H. L. (1988) Proc. Natl. Acad. Sci. USA, 85, 4176–4180.PubMedCrossRefGoogle Scholar
  22. 22.
    Reusch, R. N. (2000) Biochemistry (Moscow), 65, 280–295.Google Scholar
  23. 23.
    Rospert, S. (2004) Curr. Biol., 14, R386–R388.PubMedCrossRefGoogle Scholar
  24. 24.
    Mears, J. A., Cannone, J. J., Stegg, S. M., Guttell, R. R., Agrawal, R. K., and Harvey, S. C. (2002) J. Mol. Biol., 321, 215–234.PubMedCrossRefGoogle Scholar
  25. 25.
    Sharma, M. R., Booth, T. M., Simpson, L., Maslov, D. A., and Agrawal, R. K. (2009) Proc. Natl. Acad. Sci. USA, 106, 9637–9642.PubMedCrossRefGoogle Scholar
  26. 26.
    Kovalskaya, O. M., Sergiev, P. V., Bogdanov, A. A., and Dontsova, O. A. (2007) Uspekhi Biol. Khim., 47, 129–188.Google Scholar
  27. 27.
    Kramer, G., Boehringer, D., Ban, N., and Bukau, B. (2009) Nat. Struct. Mol. Biol., 16, 589–597.PubMedCrossRefGoogle Scholar
  28. 28.
    Giglione, C., Filulaine, S., and Meinnel, T. (2009) Trends Biochem. Sci., 34, 417–426.PubMedCrossRefGoogle Scholar
  29. 29.
    Lu, J., Kobertz, W. R., and Deutsch, C. (2007) J. Mol. Biol., 371, 1378–1391.PubMedCrossRefGoogle Scholar
  30. 30.
    Lu, J., and Deutsch, C. (2005) Nat. Struct. Biol., 12, 1123–1129.CrossRefGoogle Scholar
  31. 31.
    Lu, J., and Deutsch, C. (2008) J. Mol. Biol., 384, 73–86.PubMedCrossRefGoogle Scholar
  32. 32.
    Voss, N. R., Gerstein, M., Steitz, T. M., and Moore, P. B. (2006) J. Mol. Biol., 360, 893–906.PubMedCrossRefGoogle Scholar
  33. 33.
    Steitz, T. A. (2008) Nat. Rev. Mol. Cell Biol., 9, 242–253.PubMedCrossRefGoogle Scholar
  34. 34.
    Spirin, A. S. (2009) J. Biol. Chem., 284, 21103–21119.PubMedCrossRefGoogle Scholar
  35. 35.
    Valle, M., Zavialov, A., Sengupta, J., Rawat, U., Ehrenberg, M., and Frank, J. (2003) Cell, 114, 123–134.PubMedCrossRefGoogle Scholar
  36. 36.
    Schmeing, T. M., Voorhees, R. M., Kelly, A. C., Gao, Y. G., Murphy, F. V., 4th, Weir, J. R., and Ramakrishnan, V. (2009) Science, 326, 688–694.PubMedCrossRefGoogle Scholar
  37. 37.
    Gao, Y. G., Selmer, M., Dunham, C. M., Weixbaumer, A., Kelly, A. C., and Ramakrishnan, V. (2009) Science, 326, 694–699.PubMedCrossRefGoogle Scholar
  38. 38.
    Gabashvili, I. S., Grgory, S. T., Valle, M., Grassucci, R., Worbs, M., Wahl, M. C., Dahlberg, A. T., and Frank, J. (2001) Mol. Cell, 8, 181–188.PubMedCrossRefGoogle Scholar
  39. 39.
    Gilbert, R. J., Fucini, P., Connel, S., Fuller, S. D., Nierhaus, K. H., Robinson, C. V., Dobson, C. M., and Stuart, D. I. (2004) Mol. Cell, 14, 57–66.PubMedCrossRefGoogle Scholar
  40. 40.
    Fulle, S., and Gohlke, H. (2009) J. Mol. Biol., 387, 502–517.PubMedCrossRefGoogle Scholar
  41. 41.
    Sergiev, P. V., Bogdanov, A. A., and Dontsova, O. A. (2005) FEBS Lett., 579, 5439–5442.PubMedGoogle Scholar
  42. 42.
    Kiparisov, S. V., Sergiev, P. V., Bogdanov, A. A., and Dontsova, O. A. (2006) Mol. Biol. (Moscow), 40, 755–768.Google Scholar
  43. 43.
    Halic, M., Becker, T., Pool, M. R., Spahn, C. M., Grassucci, R. A., Frank, J., and Beckmann, R. (2004) Nature, 427, 808–814.PubMedCrossRefGoogle Scholar
  44. 44.
    Halic, M., Becker, T., Mielke, T., Pool, M. R., Wild, K., Sinning, I., and Beckmann, R. (2006) Nature, 444, 507–511.PubMedCrossRefGoogle Scholar
  45. 45.
    Schaffitzel, C., and Ban, N. (2007) J. Struct. Biol., 158, 463–471.PubMedCrossRefGoogle Scholar
  46. 46.
    Seidelt, B., Innis, C. F., Wilson, D. N., Gartmann, M., Armache, J.-P., Villa, E., Trabuco, L. G., Becker, T., Mielke, T., Schulten, K., Steitz, T. A., and Beckmann, R. (2009) Science, 326, 1412–1415.PubMedCrossRefGoogle Scholar
  47. 47.
    Becker, T., Bhushan, S., Jarasch, A., Armache, J.-P., Funes, S., Jossinet, F., Gumbart, J., Mielke, T., Berninghausen, O., Schulten, K., Westhof, E., Gilmore, R., Mandon, E. C., and Beckmann, R. (2009) Science, 326, 1369–1373.PubMedCrossRefGoogle Scholar
  48. 48.
    Woolhead, C. A., McCormick, P. J., and Johnson, A. E. (2004) Cell, 116, 725–736.PubMedCrossRefGoogle Scholar
  49. 49.
    Kosolapov, A., and Deutsch, C. (2009) Nat. Struct. Biol., 16, 405–411.CrossRefGoogle Scholar
  50. 50.
    Tu, L., and Deutsch, C. (2010) J. Mol. Biol., 396, 1346–1350.PubMedCrossRefGoogle Scholar
  51. 51.
    Lim, V. I., and Spirin, A. S. (1986) J. Mol. Biol., 188, 565–577.PubMedCrossRefGoogle Scholar
  52. 52.
    Bhushan, S., Gartmann, M., Halic, M., Armache, J.-P., Jarasch, A., Mielke, T., Berninghausen, O., Wilson, D. N., and Beckmann, R. (2010) Nat. Struct. Biol., 17, 313–317.CrossRefGoogle Scholar
  53. 53.
    Marqusee, S., and Baldwin, R. L. (1987) Proc. Natl. Acad. Sci. USA, 84, 8898–8902.PubMedCrossRefGoogle Scholar
  54. 54.
    Sicheri, F., and Yang, D. S. (1995) Nature, 375, 427–431.PubMedCrossRefGoogle Scholar
  55. 55.
    Barron, L. D., Hecht, L., and Wilson, G. (1997) Biochemistry, 36, 13143–13147.PubMedCrossRefGoogle Scholar
  56. 56.
    Mankin, A. (2001) Mol. Biol. (Moscow), 35, 597–609.Google Scholar
  57. 57.
    Wilson, D. N., Harms, J. M., Nierhaus, K. H., Schluenzen, F., and Fucini, P. (2005) Biol. Chem., 386, 1239–1252.PubMedCrossRefGoogle Scholar
  58. 58.
    Wimberly, B. T. (2009) Curr. Opin. Investig. Drugs, 10, 750–765.PubMedGoogle Scholar
  59. 59.
    Schlunzen, F., Zarivach, R., Harms, J., Bashan, A., Tocilj, A., Albrecht, R., Yonath, A., and Franceschi, F. (2001) Nature, 413, 814–821.PubMedCrossRefGoogle Scholar
  60. 60.
    Hansen, J., Ippolito, J. A., Ban, N., Nissen, P., Moore, P. B., and Steitz, T. A. (2002) Mol. Cell, 10, 117–128.PubMedCrossRefGoogle Scholar
  61. 61.
    Omura, S. (2002) Macrolide Antibiotics: Chemistry, Biology and Practice, 2nd Edn., Academic Press.Google Scholar
  62. 62.
    Hansen, L. H., Mauvais, P., and Douthwaite, S. (1999) Mol. Microbiol., 31, 623–631.PubMedCrossRefGoogle Scholar
  63. 63.
    Moazed, D., and Noller, H. F. (1987) Biochemie, 69, 879–884.CrossRefGoogle Scholar
  64. 64.
    Poulsen, S. M., Kofoed, C., and Vester, B. (2000) J. Mol. Biol., 304, 471–481.PubMedCrossRefGoogle Scholar
  65. 65.
    Liu, M., and Douthwaite, S. (2002) Proc. Natl. Acad. Sci. USA, 99, 14658–14663.PubMedCrossRefGoogle Scholar
  66. 66.
    Lai, C. J., and Weisblum, B. (1971) Proc. Natl. Acad. Sci. USA, 68, 856–860.PubMedCrossRefGoogle Scholar
  67. 67.
    Skinner, R., Cundliffe, E., and Schmidt, F. J. (1983) J. Biol. Chem., 258, 12702–12706.PubMedGoogle Scholar
  68. 68.
    Douthwaite, S. (1992) J. Bacteriol., 174, 1333–1338.PubMedGoogle Scholar
  69. 69.
    Sigmund, C. D., and Morgan, E. A. (1982) Proc. Natl. Acad. Sci. USA, 79, 5602–5606.PubMedCrossRefGoogle Scholar
  70. 70.
    Weisblum, B. (1995) Antimicrob. Agents Chemother., 39, 577–585.PubMedGoogle Scholar
  71. 71.
    Vester, B., and Douthwaite, S. (2001) Antimicrob. Agents Chemother., 45, 1–12.PubMedCrossRefGoogle Scholar
  72. 72.
    Gregory, S. T., and Dahlberg, A. E. (1999) J. Mol. Biol., 289, 827–834.PubMedCrossRefGoogle Scholar
  73. 73.
    Garza-Ramos, G., Xiong, L., Zhong, P., and Mankin, A. (2001) J. Bacteriol., 183, 6898–6907.PubMedCrossRefGoogle Scholar
  74. 74.
    Petropoulos, A. D., Kouvela, E. C., Dinos, G. P., and Kalpaxis, D. L. (2008) J. Biol. Chem., 283, 4756–4765.PubMedCrossRefGoogle Scholar
  75. 75.
    Rodriguez-Fonseca, C., Amils, R., and Garrett, R. A. (1995) J. Mol. Biol., 247, 224–235.PubMedCrossRefGoogle Scholar
  76. 76.
    Auerbach, T., Bashan, A., and Yonath, A. (2004) Trends Biotechnol., 22, 570–576.PubMedCrossRefGoogle Scholar
  77. 77.
    Steitz, T. A. (2005) FEBS Lett., 579, 955–958.PubMedCrossRefGoogle Scholar
  78. 78.
    Tu, D., Blaha, G., Moore, P. B., and Steitz, T. A. (2005) Cell, 121, 257–270.PubMedCrossRefGoogle Scholar
  79. 79.
    Vazquez-Laslop, N., Thum, C., and Mankin, A. S. (2008) Mol. Cell, 30, 190–202.PubMedCrossRefGoogle Scholar
  80. 80.
    Tenson, T., Lovmar, M., and Ehrenberg, M. (2003) J. Mol. Biol., 330, 1005–1014.PubMedCrossRefGoogle Scholar
  81. 81.
    Matsuoka, M., Inoue, M., Endo, Y., and Nakajima, Y. (2003) FEMS Microbiol. Lett., 220, 287–293.PubMedCrossRefGoogle Scholar
  82. 82.
    Furneri, P. M., Rapazzo, G., Musumarra, M., Pietro, P., Catania, L. S., and Roccasalva, L. S. (2001) Antibiot. Chemother., 45, 2958–2960.CrossRefGoogle Scholar
  83. 83.
    Sutcliffe, J. A. (2004) Features, 70, 513–519.Google Scholar
  84. 84.
    Douthwaite, S., Crain, P. F., Liu, M., and Poehlsgaard, J. (2004) J. Mol. Biol., 337, 1073–1077.PubMedCrossRefGoogle Scholar
  85. 85.
    Pfister, P., Corti, N., Hobbie, S., Bruell, C., Zarivach, R., Yonath, A., and Bottger, E. C. (2005) Proc. Natl. Acad. Sci. USA, 102, 5180–5185.PubMedCrossRefGoogle Scholar
  86. 86.
    Mankin, A. S. (2008) Curr. Opin. Microbiol., 11, 414–421.PubMedCrossRefGoogle Scholar
  87. 87.
    Schroeder, S. J., Blaha, G., and Moore, P. B. (2007) Antimicrob. Agents Chemother., 51, 4462–4465.PubMedCrossRefGoogle Scholar
  88. 88.
    Sumbatyan, N. V., Korshunova, G. A., and Bogdanov, A. A. (2003) Biochemistry (Moscow), 68, 1156–1158.CrossRefGoogle Scholar
  89. 89.
    Korshunova, G. A., Sumbatyan, N. V., Fedorova, N. V., Kuznetsova, I. V., Shishkina, A. V., and Bogdanov, A. A. (2007) Bioorg. Khim., 33, 235–244.PubMedGoogle Scholar
  90. 90.
    Sumbatyan, N. V., Kuznetsova, I. V., Karpenko, V. V., Fedorova, N. V., Chertkov, V. A., Korshunova, G. A., and Bogdanov, A. A. (2010) Bioorg. Khim., 36, 265–276.Google Scholar
  91. 91.
    Starosta, A. L., Karpenko, V. V., Shishkina, A. V., Mikolajka, A., Sumbatyan, N. V., Schluenzen, F., Korshunova, G. A., Bogdanov, A. A., and Wilson, D. N. (2010) Chem. Biol., 17, 504–514.PubMedCrossRefGoogle Scholar
  92. 92.
    Lovett, P. S., and Rogers, E. J. (1996) Microbiol. Rev., 60, 366–385.PubMedGoogle Scholar
  93. 93.
    Morris, D. R., and Geballe, A. P. (2000) Mol. Cell Biol., 20, 8635–8642.PubMedCrossRefGoogle Scholar
  94. 94.
    Tenson, T., and Ehrenberg, M. (2002) Cell, 108, 591–594.PubMedCrossRefGoogle Scholar
  95. 95.
    Nakatogawa, H., and Ito, K. (2002) Cell, 108, 629–636.PubMedCrossRefGoogle Scholar
  96. 96.
    Gong, F., and Yanofsky, C. (2002) Science, 297, 1864–1867.PubMedCrossRefGoogle Scholar
  97. 97.
    Vazquez-Laslop, N., Thum, C., and Mankin, A. S. (2008) Mol. Cell, 30, 190–202.PubMedCrossRefGoogle Scholar
  98. 98.
    Wang, Z., Fang, P., and Sachs, M. (1997) Mol. Cell Biol., 18, 7528–7536.Google Scholar
  99. 99.
    Raney, A., Law, G. L., Mize, G. J., and Morris, D. R. (2002) J. Biol. Chem., 277, 5988–5994.PubMedCrossRefGoogle Scholar
  100. 100.
    Lovett, P. S. (1994) J. Bacteriol., 176, 6415–6417.PubMedGoogle Scholar
  101. 101.
    Gu, Z., Harrod, R., Rogers, E. J., and Lovett, P. S. (1994) Proc. Natl. Acad. Sci. USA, 91, 5612–5616.PubMedCrossRefGoogle Scholar
  102. 102.
    Rogers, E. J., and Lovett, P. S. (1994) Mol. Microbiol., 12, 181–186.PubMedCrossRefGoogle Scholar
  103. 103.
    Weisblum, B. (1995) Antimicrob. Agents Chemother., 39, 797–805.PubMedGoogle Scholar
  104. 104.
    Ramu, H., Mankin, A., and Vasquez-Laslop, N. (2008) Mol. Microbiol., 71, 811–824.PubMedCrossRefGoogle Scholar
  105. 105.
    Bayfield, M. A., Thompson, J., and Dahlberg, A. E. (2004) Nucleic Acids Res., 32, 5512–5518.PubMedCrossRefGoogle Scholar
  106. 106.
    Nakatogawa, H., and Ito, K. (2004) ChemBioChem, 5, 48–51.PubMedCrossRefGoogle Scholar
  107. 107.
    Muto, H., Nakatogawa, H., and Ito, K. (2006) Mol. Cell, 22, 545–552.PubMedCrossRefGoogle Scholar
  108. 108.
    Pavlov, M. Y., Watts, R. E., Tan, Z., Cornish, V. W., Ehrenberg, M., and Forster, A. C. (2009) Proc. Natl. Acad. Sci. USA, 106, 50–54.PubMedCrossRefGoogle Scholar
  109. 109.
    Muto, H., and Ito, K. (2008) Biochem. Biophys. Res. Commun., 366, 1043–1047.PubMedCrossRefGoogle Scholar
  110. 110.
    Wohlgemuth, I., Brenner, S., Beringer, M., and Rodnina, M. V. (2008) J. Biol. Chem., 283, 32229–32235.PubMedCrossRefGoogle Scholar
  111. 111.
    Suhonara, T., Abo, T., Inada, T., and Aiba, H. (2002) RNA, 8, 1416–1427.CrossRefGoogle Scholar
  112. 112.
    Roche, E. D., and Sauer, R. T. (2001) J. Biol. Chem., 276, 28509–28515.PubMedCrossRefGoogle Scholar
  113. 113.
    Tanner, D. R., Carillo, D. A., Woolstenhulme, C. J., Broadbent, M. A., and Buskirk, A. R. (2009) J. Biol. Chem., 284, 34809–34818.PubMedCrossRefGoogle Scholar
  114. 114.
    Shpanchenko, O. V., Ivanov, P. V., Zvereva, M. E., Bogdanov, A. A., and Dontsova, O. A. (2004) Mol. Biol. (Moscow), 38, 914–925.CrossRefGoogle Scholar
  115. 115.
    Woolhead, C. A., Johnson, A. E., and Bernstein, H. D. (2006) Mol. Cell, 22, 587–598.PubMedCrossRefGoogle Scholar
  116. 116.
    Yap, M.-N., and Bernstein, H. D. (2009) Mol. Cell, 34, 201–211.PubMedCrossRefGoogle Scholar
  117. 117.
    Schmeing, T. M., Seila, A. C., Hansen, J. L., Freeborn, B., Soukup, J. K., Scaringe, S. A., Strobel, S. A., Moore, P. B., and Steitz, T. A. (2002) Nat. Struct. Biol., 9, 225–230.PubMedGoogle Scholar
  118. 118.
    Hansen, J. L., Schmeing, T. M., Moore, P. B., and Steitz, T. A. (2002) Proc. Natl. Acad. Sci. USA, 99, 11670–11675.PubMedCrossRefGoogle Scholar
  119. 119.
    Bogdanov, A. A. (2003) Mol. Biol. (Moscow), 37, 436–439.CrossRefGoogle Scholar
  120. 120.
    Wang, D., Ding, X., and Rather, P. N. (2001) J. Bacteriol., 183, 4210–4216.PubMedCrossRefGoogle Scholar
  121. 121.
    Ren, D., Bedzyk, L. A., Ye, R. W., Thomas, S. M., and Wood, T. K. (2004) Appl. Environ. Microbiol., 70, 2038–2043.PubMedCrossRefGoogle Scholar
  122. 122.
    Hirakawa, H., Inazumi, Y., Masaki, T., Hirata, T., and Yamaguchi, A. (2005) Mol. Microbiol., 55, 1113–1126.PubMedCrossRefGoogle Scholar
  123. 123.
    Kazarinoff, M. N., and Snell, E. E. (1977) J. Biol. Chem., 252, 7598–7602.PubMedGoogle Scholar
  124. 124.
    Gollnicky, P., and Yanofsky, C. J. (1990) J. Bacteriol., 172, 3100–3107.Google Scholar
  125. 125.
    Gong, F., and Yanofsky, C. (2001) J. Biol. Chem., 276, 1974–1983.PubMedGoogle Scholar
  126. 126.
    Yanofsky, C. (2007) RNA, 13, 1141–1154.PubMedCrossRefGoogle Scholar
  127. 127.
    Gong, F., Ito, K., Nakamura, Y., and Yanofsky, C. (2001) Proc. Natl. Acad. Sci. USA, 98, 8997–9001.PubMedCrossRefGoogle Scholar
  128. 128.
    Gong, M., Cruz-Vera, L. R., and Yanofsky, C. (2007) J. Bacteriol., 189, 3147–3155.PubMedCrossRefGoogle Scholar
  129. 129.
    Cruz-Vera, L. R., Rajagopal, S., Squires, C., and Yanofsky, C. (2005) Mol. Cell, 19, 333–343.PubMedCrossRefGoogle Scholar
  130. 130.
    Cruz-Vera, L. R., New, A., Squires, C., and Yanofsky, C. (2007) J. Bacteriol., 189, 3140–3146.PubMedCrossRefGoogle Scholar
  131. 131.
    Mankin, A. S. (2006) Trends Biochem. Sci., 31, 11–13.PubMedCrossRefGoogle Scholar
  132. 132.
    Torrice, M. M., Bower, K. S., Lester, H. A., and Dougherty, D. A. (2009) Proc. Natl. Acad. Sci. USA, 106, 11919–11924.PubMedCrossRefGoogle Scholar
  133. 133.
    Trabuco, L. G., Harrison, C. B., Schreiner, E., and Schulten, K. (2010) Structure, 18, 627–637.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  • A. A. Bogdanov
    • 1
    Email author
  • N. V. Sumbatyan
    • 1
  • A. V. Shishkina
    • 1
  • V. V. Karpenko
    • 1
  • G. A. Korshunova
    • 1
  1. 1.Belozersky Institute of Physico-Chemical Biology and Chemical FacultyLomonosov Moscow State UniversityMoscowRussia

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