Advertisement

Translational Regulation of Ribosomal Proteins in Escherichia coli

Molecular Mechanisms
  • David E. Draper

Abstract

In 1979–1980, a number of papers appeared that suggested that control of ribosomal (r)-protein synthesis in Escherichia coli takes place at the translational level. Gene-dosage experiments, for instance, showed that messenger RNA (mRNA) synthesis rates increase with extra copies of an r-protein operon, but the r-protein synthesis rate changes very little.1–3 Overproduction of specific r-proteins in vivo repressed the synthesis of other r-proteins in the same operon,4 and the same effect was observed when purified r-proteins were added to in vitro translation systems.5–7 These and other experiments demonstrated that some r-proteins act as autogenous, translational repressors in a negative feedback mechanism that adjusts the r-protein synthesis rate to match ribosomal RNA (rRNA) synthesis (see Fig. 1). In detail, the autoregulation hypothesis proposes that (1) each r- protein operon codes for one r-protein repressor; (2) the repressor is able to bind specifically to rRNA and to a single mRNA target site; (3) repressor binding at the mRNA target site affects translation of all downstream cistrons (i.e., ribosomes do not load at independent sites, but only at a single regulated entry site); and (4) significant free r-protein accumulates and binds the mRNA target only when all the available rRNA is assembled into ribosomes. There is evidence for translational autoregulation in most of the E. coli r-protein operons, though other mechanisms may contribute in some operons (e.g., transcription attenuation in the S10 operon).8 Excellent reviews summarizing the evidence for this regulatory scheme and evaluating its importance for the regulation of ribosome biosynthesis have appeared.9,10

Keywords

Translational Repression Ribosome Binding Site Translational Regulation Initiation Complex Displacement Model 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Fallon, A. M., Jinks, C. S., Yamamoto, M., Nomura, M., 1979, J. Bacteriol. 138: 383.PubMedGoogle Scholar
  2. 2.
    Fallon, A. M., Jinks, C. S., Strycharz, G. D., Nomura, M., 1979, Proc. Natl. Acad. Sci. U.S.A. 76: 3411.PubMedCrossRefGoogle Scholar
  3. 3.
    Dennis, P. P., Fiil, N. P., 1979, J. Biol. Chem. 254: 7540.PubMedGoogle Scholar
  4. 4.
    Lindahl, L., Zengel, J. M., 1979, Proc. Natl. Acad. Sci. U.S.A. 76: 6542.PubMedCrossRefGoogle Scholar
  5. 5.
    Yates, J. L., Arfsten, A. E., Nomura, M., 1980, Proc. Natl. Acad. Sci. U.S.A. 77: 1837.PubMedCrossRefGoogle Scholar
  6. 6.
    Brot, N., Caldwell, P., Weissbach, H., 1980, Proc. Natl. Acad. Sci. U.S.A. 77: 2592.PubMedCrossRefGoogle Scholar
  7. 7.
    Fukada, R., 1980, Mol. Gen. Genet. 178: 483.CrossRefGoogle Scholar
  8. 8.
    Lindahl, L., Archer, R., Zengel, J. M., 1983, Cell 33: 241.PubMedCrossRefGoogle Scholar
  9. 9.
    Nomura, N., Gourse, R., Baughman, G., 1984, Annu. Rev. Biochem. 53: 75.PubMedCrossRefGoogle Scholar
  10. 10.
    Lindahl, L., Zengel, J. M., 1986, Annu. Rev. Genet. 20: 297–326.PubMedCrossRefGoogle Scholar
  11. 11.
    Bedwell, D., Davis, G., Gosink, M., Post, L., Nomura, M., Kestler, H., Zengel, J. M., Lindahl, L., 1985, Nucleic Acids Res. 13: 3891.PubMedCrossRefGoogle Scholar
  12. 12.
    Dean, D., Nomura, M., 1980, Proc. Natl. Acad. Sci. U.S.A. 77: 3590.PubMedCrossRefGoogle Scholar
  13. 13.
    Jinks-Robertson, S., Nomura, M., 1982, J. Bacteriol. 515: 193.Google Scholar
  14. 14.
    Nomura, M., Yates, J. L., Dean, D., Post, L. E., 1980, Proc. Natl. Acad. Sci. U.S.A. 77: 7084.PubMedCrossRefGoogle Scholar
  15. 15.
    Deckman, I. C., Draper, D. E., 1985, Biochemistry 24: 7860.PubMedCrossRefGoogle Scholar
  16. 16.
    Meek, D. V., Hayward, R. S., 1984, Nucleic Acids Res. 12: 5813.PubMedCrossRefGoogle Scholar
  17. 17.
    Deckman, I. C., Draper, D. E., Thomas, M. E., 1987, J. Mol. Biol, (in press).Google Scholar
  18. 18.
    Schwarzbauer, J., Craven, G. R., 1981, Nucleic Acids Res. 9: 2223.PubMedCrossRefGoogle Scholar
  19. 19.
    Gausing, K., 1974, Mol. Gen. Genet. 129: 61.PubMedCrossRefGoogle Scholar
  20. 20.
    Kjeldgaard, N. O., Gausing, K., 1974, in: Ribosomes (M. Nomura, A. Tissieres, P. Lengyel, eds.), p. 369, Cold Spring Harbor Laboratory, New York.Google Scholar
  21. 21.
    Christensen, T., Johnsen, M., Fiil, N. P., Friesen, J. P., 1984, Eur. Mol. Biol. Org. J. 3: 1609.Google Scholar
  22. 22.
    Draper, D. E., 1977, Ph.D. thesis, University of Oregon.Google Scholar
  23. 23.
    Deckman, I. C., Draper, D. E., 1987, J. Mol. Biol, (in press).Google Scholar
  24. 24.
    Stern, S., Wilson, R. C., Noller, H. D., 1986, J. Mol. Biol. 192: 101 - 110.PubMedCrossRefGoogle Scholar
  25. 25.
    Noller, H. F., 1984, Annu. Rev. Biochem. 53: 119.PubMedCrossRefGoogle Scholar
  26. 26.
    Atmadja, J., Brimacombe, R., Blocker, Frand R., 1985, Nucleic Acids Res. 13: 6919.PubMedCrossRefGoogle Scholar
  27. 27.
    Brot, N., Caldwell, P., Weissbach, H., 1980, Arch. Biochem. Biophys. 206: 51.CrossRefGoogle Scholar
  28. 28.
    Yates, J. L., Nomura, M., 1981, Cell 24: 243.PubMedCrossRefGoogle Scholar
  29. 29.
    Baughman, G., Nomura, M., 1983, Cell 34: 979.PubMedCrossRefGoogle Scholar
  30. 30.
    Baughman, G., Nomura, M., 1984, Proc. Natl. Acad. Sci. U.S.A. 81: 5389.PubMedCrossRefGoogle Scholar
  31. 31.
    Nomura, M., 1986, in: Symposia of the Society for General Microbiology, Vol. 39, Regulation of Gene Expression (I. R. Booth, C. F. Higgins, eds.), p. 199, Cambridge University Press, Cambridge.Google Scholar
  32. 32.
    Gourse, R. L., Thurlow, D. L., Gerbi, S.A., Zimmerman, R. A., Proc. Natl. Acad. Sci. U.S.A. 78: 2722.Google Scholar
  33. 33.
    Post, L. E., Strycharz, G. D., Nomura, M., Lewis, H., Dennis, P. P., 1979, Proc. Natl. Acad. Sci. U.S.A. 76: 1697.PubMedCrossRefGoogle Scholar
  34. 34.
    Petterson, I., Liljas, A., 1979, FEBS Lett. 98: 139.CrossRefGoogle Scholar
  35. 35.
    Barry, G., Squires, C. L., Squires, C., 1979, Proc. Natl. Acad. Sci. U.S.A. 77: 3331.CrossRefGoogle Scholar
  36. 36.
    Yates, J. L., Dean, D., Strycharz, W. A., Nomura, M., 1981, Nature (London) 294: 190.CrossRefGoogle Scholar
  37. 37.
    Fiil, N. P., Friesen, J. D., Downing, W. L., Dennis, P. P., 1980, Cell 19: 837.PubMedCrossRefGoogle Scholar
  38. 38.
    Friesen, J. D., Tropak, M., An, G., 1983, Cell 32: 361.PubMedCrossRefGoogle Scholar
  39. 39.
    Johnsen, M., Christensen, T., Dennis, P. P., Fiil, N. P., 1982, Eur. Mol. Biol. Org. J. 1: 999.Google Scholar
  40. 40.
    Beauclerk, A. A. D., Cundliffe, E., Dijk, J., 1984, J. Biol. Chem. 259: 6559.PubMedGoogle Scholar
  41. 41.
    Jarsch, M., Bock, A., 1985, Mol. Gen. Genet. 200: 305.CrossRefGoogle Scholar
  42. 42.
    Veldmun, G. M., Klootwijk, J., de Regt, V., Planta, R. J., Branlant, С., Krol, A., Ebel, J.-P., 1981, Nucleic Acids Res. 9: 6935.CrossRefGoogle Scholar
  43. 43.
    Ware, V. C., Tague, B. W., Clark, C. G., Gourse, R. L., Brand, R. C., Gerbi, S. A., 1983, Nucleic Acids Res. 11: 7795.PubMedCrossRefGoogle Scholar
  44. 44.
    Schmidt, F. J., Thompson, J., Lee, K., Dijk, J., Cundliffe, E., 1981, J. Biol. Chem. 256: 1 2301.Google Scholar
  45. 45.
    Lodish, H. F., 1975, in: RNA Phages (N. Zinder, ed.), p. 301, Cold Spring Harbor Laboratory, New York.Google Scholar
  46. 46.
    Lecanidou, R., Richards, E. G., 1975, Eur. J. Biochem. 57: 127.PubMedCrossRefGoogle Scholar
  47. 47.
    Richards, E. G., Lecanidou, R., Geroch, M. E., 1973, Eur. J. Biochem. 34: 262.PubMedCrossRefGoogle Scholar
  48. 48.
    Johnston, H. M., Barnes, W. M., Chumley, F. G., Bossi, L., Roth, J. D., 1980, Proc. Natl. Acad. Sci. U.S.A. 77: 508.PubMedCrossRefGoogle Scholar
  49. 49.
    Parsons, G. D., Mackie, G. A., 1983, J. Bacteriol. 154: 152.PubMedGoogle Scholar
  50. 50.
    Olins, P. O., Nomura, M., 1981, Nucleic Acids Res. 9: 1757.PubMedCrossRefGoogle Scholar
  51. 51.
    Carey, J., Cameron, V., de Haseth, P. L., Uhlenbeck, О. C., 1983, Biochemistry 22: 2601.PubMedCrossRefGoogle Scholar
  52. 52.
    Karam, J., Gold, L., Singer, B. S., Dawson, M., 1981, Proc. Natl. Acad. Sci. U.S.A. 78: 4669.PubMedCrossRefGoogle Scholar
  53. 53.
    Krisch, H. M., Allet, B., 1982, Proc. Natl. Acad. Sci. U.S.A. 79: 4937.PubMedCrossRefGoogle Scholar
  54. 54.
    Pabo, C. O., Sauer, R. T., 1984, Annu. Rev. Biochem. 53: 293.PubMedCrossRefGoogle Scholar
  55. 55.
    Carey, J., Lowary, P. T., Uhlenbeck, O. C., 1983, Biochemistry 22: 4723.PubMedCrossRefGoogle Scholar
  56. 56.
    Walter, G., Zillig, W., Palen, P., Fuchs, E., 1967, Eur. J. Biochem. 3: 194.PubMedCrossRefGoogle Scholar
  57. 57.
    McClure, W. R., 1985, Annu. Rev. Biochem. 54: 171.PubMedCrossRefGoogle Scholar
  58. 58.
    Gold, L., Pribnow, D., Schneider, T., Schinedling, S., Singer, S., Stormo, G., 1981, Annu. Rev. Microbiol. 35: 365.PubMedCrossRefGoogle Scholar
  59. 59.
    Gualerzi, C., Risuelo, G., Pon, C. L., 1977, Biochemistry 16: 1684.PubMedCrossRefGoogle Scholar
  60. 60.
    Wintermeyer, W., Gualerzi, C., 1983, Biochemistry 22: 690.PubMedCrossRefGoogle Scholar
  61. 61.
    Gualerzi, C., Risuelo, G., Pon, C. L., 1979, J. Biol. Chem. 254: 44.PubMedGoogle Scholar
  62. 62.
    Pon, C. L., Gualerzi, C. O., 1984, FEBS Lett. 175: 203.PubMedCrossRefGoogle Scholar
  63. 63.
    Steitz, J. A., Jakes, K., 1975, Proc. Natl. Acad. U.S.A. 72: 4734.CrossRefGoogle Scholar
  64. 64.
    Grunberg-Manago, M., 1979, in: Ribosomes: Structure, Function, and Genetics (G. Chambliss, G. R. Craven, J. Da vies, K. Davis, L. Kahan, M. Nomura, eds.), p. 445, University Park Press, Baltimore.Google Scholar
  65. 65.
    Draper, D. E., Gold, L., 1980, Biochemistry 19: 1774.PubMedCrossRefGoogle Scholar
  66. 66.
    Forchhammer, J., Lindahl, L., 1971, J. Mol. Biol. 55: 563.PubMedCrossRefGoogle Scholar
  67. 67.
    Kennell, D., Reizman, H., 1977, J. Mol. Biol. 114: 1.PubMedCrossRefGoogle Scholar
  68. 68.
    Von Hippel, P. H., Fairfield, F. R., 1983, in: Mobility and Recognition in Cell Biology (H. Sund, C. Veeger, eds.), p. 213, W. de Gruyter, Berlin.Google Scholar
  69. 69.
    Cole, J. R., Nomura, M., 1986, Proc. Natl. Acad. Sci. U.S.A. 83: 4129–4133.PubMedCrossRefGoogle Scholar
  70. 70.
    Green, M., Kurland, C. G., 1971, Nature (London) New Biol. 234: 273.CrossRefGoogle Scholar
  71. 71.
    Olsson, M. O., Isaksson, L. A., 1979, Mol. Gen. Genet. 169: 271.PubMedCrossRefGoogle Scholar
  72. 72.
    Olsson, M. O., Gausing, K., 1980, Nature (London) 283: 599.CrossRefGoogle Scholar
  73. 73.
    Wirth, R., Bock, A., 1980, Mol. Gen. Genet. 178: 479.PubMedCrossRefGoogle Scholar
  74. 74.
    Singer, P., Nomura, M., 1985, Mol. Gen. Genet. 199: 543.PubMedCrossRefGoogle Scholar
  75. 75.
    Cole, J. R., Nomura, M., 1986, J. Mol. Biol. 188: 383–391.PubMedCrossRefGoogle Scholar
  76. 76.
    Schneider, E., Blundell, M., Kennell, D., 1978, Mol. Gen. Genet. 160: 121.PubMedCrossRefGoogle Scholar
  77. 77.
    Roe, J.-H., Record, M. T., 1985, Biochemistry 24: 4721.PubMedCrossRefGoogle Scholar
  78. 78.
    Coleman, J., Inouye, M., Nakamura, K., 1985, J. Mol. Biol. 181: 139.PubMedCrossRefGoogle Scholar
  79. 79.
    Hall, M. N., Gabbay, J., Débarbouillé, M., Schwartz, M., 1982, Nature (London) 295: 616.CrossRefGoogle Scholar
  80. 80.
    Nomura, M., Ohsuye, K., Sakuragawa, Y., Tanaka, S., 1984, Nucleic Acids Symp. Ser. 15: 173.PubMedGoogle Scholar
  81. 81.
    Tinoco, I., Borer, P. N., Dengler, B. V., Levine, M. D., Uhlenbeck, O. C., Crothers, D., Gralla, J., 1973, Nature (London) New Biol. 246: 40.Google Scholar
  82. 82.
    Van Dieijen, G., van Knippenberg, P. H., van Duin, J., 1976, Eur. J. Biochem. 64: 511.PubMedCrossRefGoogle Scholar
  83. 83.
    Vermeer, C., van Alphen, W. J., van Knippenberg, P. H., Bosch, L., 1973, Eur. J. Biochem. 40: 295.PubMedCrossRefGoogle Scholar
  84. 84.
    Abrahamson, J. K., Laue, T. M., Miller, D.L., Johnson, A. E., 1985, Biochemistry 24: 692.PubMedCrossRefGoogle Scholar
  85. 85.
    Wirth, R., Kohles, V., Bock, A., 1981, Eur. J. Biochem. 114: 429.PubMedCrossRefGoogle Scholar
  86. 86.
    Blumberg, B. M., Nakamoto, T., Kézdy, F. J., 1979, Proc. Natl. Acad. Sci. U.S.A. 76: 251.PubMedCrossRefGoogle Scholar
  87. 87.
    Jay, G., Kaempfer, R., 1974, Proc. Natl. Acad. Sci. U.S.A. 71: 3199.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1987

Authors and Affiliations

  • David E. Draper
    • 1
  1. 1.Department of ChemistryJohns Hopkins UniversityBaltimoreUSA

Personalised recommendations