Biochemistry (Moscow)

, Volume 73, Issue 13, pp 1405–1417 | Cite as

Bacterial 5S rRNA-binding proteins of the CTC family

  • G. M. GongadzeEmail author
  • A. P. Korepanov
  • A. V. Korobeinikova
  • M. B. Garber


The presence of CTC family proteins is a unique feature of bacterial cells. In the CTC family, there are true ribosomal proteins (found in ribosomes of exponentially growing cells), and at the same time there are also proteins temporarily associated with the ribosome (they are produced by the cells under stress only and incorporate into the ribosome). One feature is common for these proteins — they specifically bind to 5S rRNA. In this review, the history of investigations of the best known representatives of this family is described briefly. Structural organization of the CTC family proteins and their occurrence among known taxonomic bacterial groups are discussed. Structural features of 5S rRNA and CTC protein are described that predetermine their specific interaction. Taking into account the position of a CTC protein and its intermolecular contacts in the ribosome, a possible role of its complex with 5S rRNA in ribosome functioning is discussed.

Key words

5S rRNA-binding proteins CTC proteins ribosome translation Bacteria 



catabolite controlled, a protein whose gene (ctc) is controlled by catabolism products. Names of the individual ribosomal proteins are given according to their belonging to the ribosome subparticle (“L”, Large) and serial number on the two-dimensional electrophoregram (e.g. L25). The first letter of the organism name (“T”, Thermus) has been added to the name of ribosomal protein TL5


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  1. 1.
    Lecompte, O., Ripp, R., Thierry, J. C., Moras, D., and Poch, O. (2002) Nucleic Acids Res., 30, 5382–5390.PubMedCrossRefGoogle Scholar
  2. 2.
    Gryaznova, O. I., Davydova, N. L., Gongadze, G. M., Jonsson, B. H., Garber, M. B., and Liljas, A. (1996) Biochimie, 78, 915–919.PubMedCrossRefGoogle Scholar
  3. 3.
    Benson, D. A., Karsch-Mizrashi, I., Lipman, D. J., Ostell, J., and Wheeler, D. L. (2006) Nucleic Acids Res., 34, 16–20.CrossRefGoogle Scholar
  4. 4.
    Frishman, D., Mokrejs, M., Kosykh, D., Kostenmuller, G., Kolesov, G., Zubrzycki, I., Gruber, C., Geier, B., Kaps, A., Albermann, K., Volz, A., Wagner, C., Fellenberg, M., Heumann, K., and Mewes, H. W. (2003) Nucleic Acids Res., 31, 207–211.PubMedCrossRefGoogle Scholar
  5. 5.
    Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D., and Bairoch, A. (2003) Nucleic Acids Res., 31, 3784–3788.PubMedCrossRefGoogle Scholar
  6. 6.
    Haldenwang, W. G., and Losick, R. (1979) Nature, 282, 256–260.PubMedCrossRefGoogle Scholar
  7. 7.
    Haldenwang, W. G., and Losick, R. (1980) Proc. Natl. Acad. Sci. USA, 77, 7000–7004.PubMedCrossRefGoogle Scholar
  8. 8.
    Moran, C. P. Jh., Lang, N., Banner, C. D., Haldenwang, W. G., and Losick, R. (1981) Cell, 25, 783–791.PubMedCrossRefGoogle Scholar
  9. 9.
    Moran, C. P. Jh., Lang, N., and Losick, R. (1981) Nucleic Acids Res., 9, 5979–5990.PubMedCrossRefGoogle Scholar
  10. 10.
    Haldenwang, W. G. (1995) Microbiol. Rev., 59, 1–30.PubMedGoogle Scholar
  11. 11.
    Volker, U., Engelmann, S., Maul, B., Riethdorf, S., Volker, A., Schmid, R., Mach, H., and Hecker, M. (1994) Microbiology, 140, 741–752.PubMedCrossRefGoogle Scholar
  12. 12.
    Hecker, M., and Volker, U. (1990) FEMS Microbiol. Ecol., 74, 197–214.CrossRefGoogle Scholar
  13. 13.
    Korepanov, A. P., Gongadze, G. M., and Garber, M. B. (2004) Biochemistry (Moscow), 69, 607–611.CrossRefGoogle Scholar
  14. 14.
    Schmalisch, M., Langbein, I., and Stulke, J. (2002) J. Mol. Microbiol. Biotechnol., 4, 495–501.PubMedGoogle Scholar
  15. 15.
    Duche, O., Tremoulet, F., Glaser, P., and Labadie, J. (2002) Appl. Environ. Microbiol., 68, 1491–1498.PubMedCrossRefGoogle Scholar
  16. 16.
    Kazmierczak, M. G., Mithoe, S. C., Boor, K. J., and Wiedmann, M. (2003) J. Bacteriol., 185, 5722–5734.PubMedCrossRefGoogle Scholar
  17. 17.
    Truitt, C. L., Weaver, E. A., and Haldenwang, W. G. (1988) Mol. Gen. Genet., 212, 166–171.PubMedCrossRefGoogle Scholar
  18. 18.
    Horne, J. R., and Erdmann, V. A. (1972) Mol. Gen. Genet., 119, 337–344.PubMedGoogle Scholar
  19. 19.
    Gongadze, G. M., Tishchenko, S. V., Sedelnikova, S. E., and Garber, M. B. (1993) FEBS Lett., 330, 46–48.PubMedCrossRefGoogle Scholar
  20. 20.
    Dovgas, N. V., Markova, L. F., Mednikova, T. A., Vinokurov, L. M., Alakhov, Y. B., and Ovchinnikov, Y. A. (1975) FEBS Lett., 53, 351–354.PubMedCrossRefGoogle Scholar
  21. 21.
    Igo, M., Lampe, M., and Losick, R. (1988) Genetics and Biotechnology of Bacilli (Ganesan, A. T., and Hoch, J. A., eds.) Vol. 2, Academic Press, San Diego, CA, pp. 151–156.Google Scholar
  22. 22.
    Gongadze, G. M., Meshcheryakov, V. A., Serganov, A. A., Fomenkova, N. P., Mudrik, E. S., Jonsson, B.-H., Liljas, A., Nikonov, S. V., and Garber, M. B. (1999) FEBS Lett., 451, 51–55.PubMedCrossRefGoogle Scholar
  23. 23.
    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
  24. 24.
    Korobeinikova, A. V., Gongadze, G. M., Korepanov, A. P., Eliseev, B. D., Bazhenova, M. V., and Garber, M. B. (2008) Biochemistry (Moscow), 73, 156–163.Google Scholar
  25. 25.
    Gongadze, G. M., Korepanov, A. P., Stolboushkina, E. A., Zelinskaya, N. V., Korobeinikova, A. V., Ruzanov, M. V., Eliseev, B. D., Nikonov, O. S., Nikonov, S. V., Garber, M. B., and Lim, V. I. (2005) J. Biol. Chem., 280, 16151–16156.PubMedCrossRefGoogle Scholar
  26. 26.
    Deckert, G., Warren, P. V., Gaasterland, T., Young, W. G., Lenox, A. L., Graham, D. E., Overbeek, R., Snead, M. A., Keller, M., Aujay, M., Huber, R., Feldman, R. A., Short, J. M., Olsen, G. J., and Swanson, R. V. (1998) Nature, 392, 353–358.PubMedCrossRefGoogle Scholar
  27. 27.
    Newberry, V., and Garrett, R. A. (1980) Nucleic Acids Res., 8, 4131–4142.PubMedCrossRefGoogle Scholar
  28. 28.
    Stoldt, M., Wohnert, J., Gorlach, M., and Brown, L. R. (1998) EMBO J., 17, 6377–6384.PubMedCrossRefGoogle Scholar
  29. 29.
    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) Acta Crystallogr. D, 57, 968–976.PubMedCrossRefGoogle Scholar
  30. 30.
    Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) Nucleic Acids Res., 22, 4673–4680.PubMedCrossRefGoogle Scholar
  31. 31.
    Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G., and Thompson, J. D. (2003) Nucleic Acids Res., 31, 3497–3500.PubMedCrossRefGoogle Scholar
  32. 32.
    Barciszewska, M. Z., Erdmann, V. A., and Barciszewski, J. (1996) Biol. Rev. Camb. Phylos. Soc., 71, 1–25.CrossRefGoogle Scholar
  33. 33.
    Chen-Schmeisser, U., and Garrett, R. A. (1977) FEBS Lett., 74, 287–291.PubMedCrossRefGoogle Scholar
  34. 34.
    Stoffler, G., and Stoffler-Meilicke, M. (1984) Ann. Rev. Biophys. Bioeng., 13, 303–330.CrossRefGoogle Scholar
  35. 35.
    Bogdanov, A. A., Dontsova, O. A., Dokudovskaya, S. S., and Lavrik, I. N. (1995) Biochem. Cell Biol., 73, 869–876.PubMedCrossRefGoogle Scholar
  36. 36.
    Moore, P. B. (1996) Ribosomal RNA: Structure, Evolution, Processing, and Function in Protein Biosynthesis (Zimmermann, R., and Dahlberg, A., eds.) CRC Press, Boca Raton-New York-London-Tokyo, pp. 199–236.Google Scholar
  37. 37.
    Douthwaite, S., Garrett, R. A., Wagner, R., and Feunteun, J. (1979) Nucleic Acids Res., 6, 2453–2470.PubMedCrossRefGoogle Scholar
  38. 38.
    Szymanski, M., Barciszewska, M. Z., Erdmann, V. A., and Barciszewska, J. (2002) Nucleic Acids Res., 30, 176–178.PubMedCrossRefGoogle Scholar
  39. 39.
    Kjems, J., Olesen, S. O., and Garrett, R. A. (1985) Biochemistry, 24, 241–250.PubMedCrossRefGoogle Scholar
  40. 40.
    Wrede, P., and Erdmann, V. A. (1977) Proc. Natl. Acad. Sci. USA, 74, 2706–2709.PubMedCrossRefGoogle Scholar
  41. 41.
    Dallas, A., and Moore, P. B. (1997) Structure, 5, 1639–1653.PubMedCrossRefGoogle Scholar
  42. 42.
    Correll, C. C., Freeborn, B., Moore, P. B., and Steitz, T. A. (1997) Cell, 91, 705–712.PubMedCrossRefGoogle Scholar
  43. 43.
    MacKey, R. M., Spencer, D. F., Schnare, M. N., Doolittle, W. F., and Gray, M. W. (1982) Can. J. Biochem., 60, 480–489.CrossRefGoogle Scholar
  44. 44.
    Lu, M., and Steitz, T. A. (2000) Proc. Natl. Acad. Sci. USA, 97, 2023–2028.PubMedCrossRefGoogle Scholar
  45. 45.
    Stoldt, M., Wohnert, J., Ohlenschlager, O., Gorlach, M., and Brown, L. R. (1999) EMBO J., 18, 6508–6521.PubMedCrossRefGoogle Scholar
  46. 46.
    Nevskaya, N. A., Nikonov, O. S., Revtovich, S. V., Garber, M. B., and Nikonov, S. V. (2004) Mol. Biol. (Moscow), 38, 789–798.Google Scholar
  47. 47.
    Shatsky, I. N., Evstafieva, A. G., Bystrova, T. F., Bogdanov, A. A., and Vasiliev, V. D. (1980) FEBS Lett., 121, 97–100.PubMedCrossRefGoogle Scholar
  48. 48.
    Stoffler-Meilicke, M., Stoffler, G., Odom, O. W., Zinn, A., Kramer, G., and Hardesty, B. (1981) Proc. Natl. Acad. Sci. USA, 78, 5538–5542.PubMedCrossRefGoogle Scholar
  49. 49.
    Evstafieva, A. G., Shatsky, I. N., Bogdanov, A. A., and Vasiliev, V. D. (1982) FEBS Lett., 185, 57–62.CrossRefGoogle Scholar
  50. 50.
    Stoffler-Meilicke, M., Noah, M., and Stoffler, G. (1983) Proc. Natl. Acad. Sci. USA, 80, 6780–6784.PubMedCrossRefGoogle Scholar
  51. 51.
    Lotti, M., Noah, M., Stoffler-Meilicke, M., and Stoffler, G. (1989) Mol. Gen. Genet., 216, 245–253.PubMedCrossRefGoogle Scholar
  52. 52.
    Ban, N., Nissen, P., Hansen, J., Moore, P. B., and Steitz, T. A. (2000) Science, 289, 905–920.PubMedCrossRefGoogle Scholar
  53. 53.
    Schuwirth, B. S., Borovinskaya, M. A., Hau, C. W., Zhang, W., Vila-Sunjurjo, A., Holton, J. M., and Cate, J. H. (2005) Science, 310, 827–834.PubMedCrossRefGoogle Scholar
  54. 54.
    Selmer, M., Dunham, C. M., Murphy, F. V. IV, Weixlbaumer, A., Petry, S., Kelley, A. C., Weir, J. R., and Ramakrishnan, V. (2006) Science, 313, 1935–1942.PubMedCrossRefGoogle Scholar
  55. 55.
    Christiansen, J., Douthwaite, S. R., Christiansen, A., and Garrett, R. A. (1985) EMBO J., 4, 1019–1024.PubMedGoogle Scholar
  56. 56.
    Dontsova, O., Tishkov, V., Dokudovskaya, S., Bogdanov, A., Doring, T., Rinke-Appel, J., Thamm, S., Greuer, B., and Brimacombe, R. (1994) Proc. Natl. Acad. Sci. USA, 91, 4125–4129.PubMedCrossRefGoogle Scholar
  57. 57.
    Dokudovskaya, S., Dontsova, O., Shpanchenko, O., Bogdanov, A., and Brimacombe, R. (1996) RNA, 2, 146–152.PubMedGoogle Scholar
  58. 58.
    Sergiev, P., Dokudovskaya, S., Romanova, E., Topin, A., Bogdanov, A., Brimacombe, R., and Dontsova, O. (1998) Nucleic Acids Res., 26, 2519–2525.PubMedCrossRefGoogle Scholar
  59. 59.
    Osswald, M., and Brimacombe, R. (1999) Nucleic Acids Res., 27, 2283–2290.PubMedCrossRefGoogle Scholar
  60. 60.
    Osswald, M., Greuer, B., and Brimacombe, R. (1990) Nucleic Acids Res., 18, 6755–6760.PubMedCrossRefGoogle Scholar
  61. 61.
    Gongadze, G. M., Perederina, A. A., Meshcheryakov, 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) Mol. Biol. (Moscow), 35, 521–526.CrossRefGoogle Scholar
  62. 62.
    Szymkowiak, C., and Wagner, R. (1985) Nucleic Acids Res., 13, 3953–3968.PubMedCrossRefGoogle Scholar
  63. 63.
    Spierer, P., and Zimmermann, R. A. (1978) Biochemistry, 17, 2474–2479.PubMedCrossRefGoogle Scholar
  64. 64.
    Nierhaus, K. H., and Dohme, F. (1974) Proc. Natl. Acad. Sci. USA, 71, 4713–4717.PubMedCrossRefGoogle Scholar
  65. 65.
    Dohme, F., and Nierhaus, K. H. (1976) Proc. Natl. Acad. Sci. USA, 73, 2221–2225.PubMedCrossRefGoogle Scholar
  66. 66.
    Nissen, P., Ippolito, J. A., Ban, N., Moore, P. B., and Steitz, T. A. (2001) Proc. Natl. Acad. Sci. USA, 98, 4899–4903.PubMedCrossRefGoogle Scholar
  67. 67.
    Klein, D. J., Moore, P. B., and Steitz, T. A. (2004) J. Mol. Biol., 340, 141–177.PubMedCrossRefGoogle Scholar
  68. 68.
    Moore, V. G., Atchison, R. E., Thomas, G., Moran, M., and Noller, H. F. (1975) Proc. Natl. Acad. Sci. USA, 72, 844–848.PubMedCrossRefGoogle Scholar
  69. 69.
    Hampl, H., Schulze, H., and Nierhaus, K. H. (1981) J. Biol. Chem., 256, 2284–2288.PubMedGoogle Scholar
  70. 70.
    Kazemie, M. (1976) Eur. J. Biochem., 67, 373–378.PubMedCrossRefGoogle Scholar
  71. 71.
    Yusupov, M. M., Yusupova, G. Z., Baucom, A., Lieberman, K., Earnest, T. N., Cate, J. H., and Noller, H. F. (2001) Science, 292, 883–896.PubMedCrossRefGoogle Scholar
  72. 72.
    Nissen, P., Hansen, J., Ban, N., Moore, P. B., and Steitz, T. A. (2000) Science, 289, 920–930.PubMedCrossRefGoogle Scholar
  73. 73.
    Nishimura, M., Yoshida, T., Shirouzu, M., Terada, T., Kuramitsu, S., Yokoyama, S., Ohkudo, T., and Kobayashi, Y. (2004) J. Mol. Biol., 344, 1369–1383.PubMedCrossRefGoogle Scholar
  74. 74.
    Stark, H., Rodnina, M. V., Rinke-Appel, J., Brimacombe, R., Wintermeyer, W., and van Heel, M. (1997) Nature, 389, 403–406.PubMedCrossRefGoogle Scholar
  75. 75.
    Wilson, K. S., and Noller, H. F. (1998) Cell, 92, 131–139.PubMedCrossRefGoogle Scholar
  76. 76.
    Wilson, K. S., Ito, K., Noller, H. F., and Nakamura, Y. (2000) Nat. Struct. Biol., 7, 866–870.PubMedCrossRefGoogle Scholar
  77. 77.
    Stark, H., Rodnina, M. V., Wieden, H. J., Zemlin, F., Wintermeyer, W., and van Heel, M. (2002) Nat. Struct. Mol. Biol., 9, 849–854.Google Scholar
  78. 78.
    Lancaster, L., Kiel, M. C., Kaji, A., and Noller, H. F. (2002) Cell, 111, 129–140.PubMedCrossRefGoogle Scholar
  79. 79.
    Marzi, S., Knight, W., Brandi, L., Caserta, E., Soboleva, N., Hill, W. E., Gualerzi, C. O., and Lodmell, J. S. (2003) RNA, 9, 958–969.PubMedCrossRefGoogle Scholar
  80. 80.
    Klaholz, B. P., Myasnikov, A. G., and van Heel, M. (2004) Nature, 427, 862–865.PubMedCrossRefGoogle Scholar
  81. 81.
    Wilson, K. S., and Nechifor, R. (2004) J. Mol. Biol., 337, 15–30.PubMedCrossRefGoogle Scholar
  82. 82.
    Scarlett, D.-J. G., McCaughan, K. K., Wilson, D. N., and Tate, W. P. (2005) J. Biol. Chem., 278, 15095–15104.CrossRefGoogle Scholar
  83. 83.
    Wilson, D. N., Schluenzen, F., Harms, J. M., Yoshida, T., Ohkubo, T., Albrecht, R., Buerger, J., Kobayashi, Y., and Fucini, P. (2005) EMBO J., 24, 251–260.PubMedCrossRefGoogle Scholar
  84. 84.
    Petry, S., Brodersen, D. E., Murphy, F. V. IV, Dunham, C. M., Selmer, M., Tarry, M. J., Kelley, A. C., and Ramakrishnan, V. (2005) Cell, 123, 1255–1266.PubMedCrossRefGoogle Scholar
  85. 85.
    Weixlbaumer, A., Petry, S., Dunham, C. M., Selmer, M., Kelley, A. C., and Ramakrishnan, V. (2007) Nat. Struct. Mol. Biol., 14, 733–737.PubMedCrossRefGoogle Scholar
  86. 86.
    Erdmann, V. A., Fahnestock, S., Higo, K., and Nomura, M. (1971) Proc. Natl. Acad. Sci. USA, 68, 2932–2936.PubMedCrossRefGoogle Scholar
  87. 87.
    Selivanova, O. M., Gongadze, G. M., Gudkov, A. T., and Vasiliev, V. D. (1986) FEBS Lett., 197, 79–83.PubMedCrossRefGoogle Scholar
  88. 88.
    Ammons, D., Rampersad, J., and Fox, G. E. (1999) Nucleic Acids Res., 27, 637–642.PubMedCrossRefGoogle Scholar
  89. 89.
    Ammons, D., and Rampersad, J. (2001) Curr. Microbiol., 43, 89–92.PubMedCrossRefGoogle Scholar
  90. 90.
    Dabbs, E. R. (1991) Biochimie, 73, 639–645.PubMedCrossRefGoogle Scholar
  91. 91.
    Korepanov, A. P., Gongadze, G. M., Garber, M. B., Court, D. L., and Bubunenko, M. G. (2007) J. Mol. Biol., 366, 1199–1208.PubMedCrossRefGoogle Scholar
  92. 92.
    Rohl, R., and Nierhaus, K. H. (1982) Proc. Natl. Acad. Sci. USA, 79, 729–733.PubMedCrossRefGoogle Scholar
  93. 93.
    Bashan, A., Agmon, I., Zarivach, R., Schluenzen, F., Harms, J., Berisio, R., Bartels, H., Franceschi, F., Auerbach, T., Hansen, H. A. S., Kossoy, E., Kessler, M., and Yonath, A. (2003) Mol. Cell, 11, 91–102.PubMedCrossRefGoogle Scholar

Copyright information

© MAIK Nauka 2008

Authors and Affiliations

  • G. M. Gongadze
    • 1
    Email author
  • A. P. Korepanov
    • 1
  • A. V. Korobeinikova
    • 1
  • M. B. Garber
    • 1
  1. 1.Institute of Protein ResearchRussian Academy of SciencesPushchino, Moscow RegionRussia

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