Advertisement

Molecular and Cellular Biochemistry

, Volume 47, Issue 2, pp 97–113 | Cite as

Guanosine-5′-triphosphate hydrolysis and tubulin polymerization

Review article
  • Marie-France Carlier
Article

Summary

GTP hydrolysis associated with polymerization is a distinctive feature of microtubule assembly. This reaction may be fundamentally linked to the dynamic properties of microtubules in vivo. Kinetic analysis of the connection between microtubule assembly and associated GTP hydrolysis indicates that these two events are kinetically uncoupled, GTP hydrolysis occurring after tubulin incorporation in the microtubule. As a consequence, the combination of the diffusionnal incorporation of GTP in microtubules at steady-state and of subsequent GTP hydrolysis results in the formation of a steady-state GTP cap at microtubule ends. The interplay between GTP and GDP at microtubule ends is examined. Inhibition by GDP of steady-state GTP hydrolysis at microtubule ends and of microtubule elongation is understood within a tight reversible binding of GDP at microtubule ends generating ‘inactive’ elongation sites. Nucleotides are freely exchangeable at microtubule ends. This result indicates that the nature of the nucleotide present at microtubule ends must be considered in a model for microtubule assembly.

These data are pooled in order to define the general features of a model describing microtubule assembly and treadmilling in terms somewhat different from previously proposed models.

Keywords

Nucleotide General Feature Triphosphate Distinctive Feature Dynamic Property 
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.
    Erickson, H. P., 1974. J. Cell Biol. 60: 153–167.Google Scholar
  2. 2a.
    Amos, L. A. & Klug, A., 1974. J. Cell Sci. 14: 523–549.Google Scholar
  3. 2b.
    Mandelkow, E., Thomas, J. & Cohen, C., 1977. Proc. Nat. Acad. Sci. U.S.A. 74: 3370–3374.Google Scholar
  4. 3.
    Oosawa, F. & Asakura, S., 1975. In: Thermodynamics of the Polymerization of Proteins. Acadamic Press, New York.Google Scholar
  5. 4.
    Voter, W. A. & Erickson, H. P., 1979. J. Supramol. Struct. 10: 419–431.Google Scholar
  6. 5.
    Weisenberg, R. C., Decry, W. J. & Dickinson, P. J., 1976. Biochemistry 15: 4248–4254.Google Scholar
  7. 6.
    Arai, T. & Kaziro, Y., 1976. Biochem. Biophys. Res. Comm. 69: 369–376.Google Scholar
  8. 7.
    Snyder, J. A. & McIntosh, J. R., 1976. Ann. Rev. Biochem. 45: 699–720.Google Scholar
  9. 8.
    Kirschner, M. W., 1978. Ann. Rev. Cytol. 1–68.Google Scholar
  10. 9.
    Scheele, R. B. & Borisy, G. G., 1979. In: Microtubules (Roberts & Hyams, eds.) pp. 175–254, Academic Press, New York.Google Scholar
  11. 10.
    Timasheff, S. N. & Grisham, L. M., 1980. Ann. Rev. Biochem. 49: 565–591.Google Scholar
  12. 11.
    Weisenberg, R. C., Borisy, G. G. & Taylor, E. W., 1968. Biochemistry 7: 4466–4479.Google Scholar
  13. 12.
    Weisenberg, R. C., 1972. Science 177: 1104–1105.Google Scholar
  14. 13.
    Shelanski, M. L., Gaskin, F. & Cantor, C. R., 1973. Proc. Nat. Acad. Sci. U.S.A. 70: 765–768.Google Scholar
  15. 14.
    Bryan, J., 1972. J. Mol. Biol. 66: 157–168.Google Scholar
  16. 15.
    Luduena, R. F. & Woodward, D. O., 1973. Proc. Nat. Acad. Sci. U.S.A. 70: 3594–3598.Google Scholar
  17. 16.
    Luduena, R. F. & Woodward, D. O., 1975. Ann. N.Y. Acad. Sci. 253: 272–283.Google Scholar
  18. 17.
    Geahlen, R. L. & Haley, B. E., 1977. Proc. Nat. Acad. Sci. U.S.A. 7: 4375–4377.Google Scholar
  19. 18.
    Geahlen, R. L. & Haley, B. E., 1979. J. Biol. Chem. 254: 11982–11987.Google Scholar
  20. 19.
    Valenzuela P., Quiroga, M., Zaldivar, J., Rutter, W. J., Kirschner, M. W. & Cleveland, D. W., 1981. Nature 289: 650–655.Google Scholar
  21. 20.
    Krauhs, E., Little, M., Kempf, T., Hofer-Warbinek, R., Ade, W. & Ponstingl, H., 1981. Proc. Nat. Acad. Sci. U.S.A. 78: 4156–4160.Google Scholar
  22. 21.
    Spiegelman, B. M., Penningroth, S. M. & Kirschner, M. W., 1977. Cell 12: 587–600.Google Scholar
  23. 22.
    Little, M., Luduena, R. F., Langford, G. M., Asnes, C. F. & Farrell, K., 1981. J. Mol. Biol. 149: 95–107.Google Scholar
  24. 23.
    Sheir-Neiss, G., Lai, M. H. & Morris, N. R., 1978. Cell 15: 639–647.Google Scholar
  25. 24.
    Cabral, F., Sobel, M. E. & Gottesman, M. M., 1980. Cell 20: 29–36.Google Scholar
  26. 25.
    Oakley, B. R. & Morris, N. R., 1981. Cell 24: 837–845.Google Scholar
  27. 26.
    Jacobs, M. & Caplow, M., 1976. Biochem. Biophys. Res. Comi. 68: 127–135.Google Scholar
  28. 27.
    Arai, T., Ihara, Y., Arai, K. & Kaziro, Y., 1975. J. Biochem. (Tokyo) 77: 647–658.Google Scholar
  29. 28.
    Zeeberg, B. & Caplow, M., 1979. Biochemistry 18: 3880–3886.Google Scholar
  30. 29.
    Jacobs, M., Smith, H. & Taylor, E. W., 1974. J. Mol. Biol. 89: 455–468.Google Scholar
  31. 30.
    30. Hammes, G. G. & Schimmel, P. R., 1970. In: The Enzymes (Boyer, ed.) Vol. II 3 en. pp. 67–114. Academic Press, N.Y.Google Scholar
  32. 31.
    Sherline, P., Leung, J. T. & Kipnis, D. M., 1975. J. Biol. Chem. 250: 5481–5486.Google Scholar
  33. 32.
    Waechter, F. & Engel, J., 1977. Eur. J. Biochem. 74: 227–232.Google Scholar
  34. 33.
    Gekko, K. & Timasheff, S. N., 1981. Biochemistry 20: 4667–4677.Google Scholar
  35. 34.
    Gekko, K. & Timasheff, S. N., 1981. Biochemistry 20: 4677–4687.Google Scholar
  36. 35.
    Weingarten, M. D., Lockwood, A. H., Hwo, S. Y. & Kirschner, M. W., 1975. Proc. Nat. Acad. Sci. U.S.A. 72: 1858–1862.Google Scholar
  37. 36.
    Borisy, G. G., Marcum, J. M., Olmsted, J. B., Murphy, D. B. & Johnson, K. A., 1975. Ann. N.Y. Acad. Sci. 253: 107–132.Google Scholar
  38. 37.
    Vallee, R. B. & Borisy, G. G., 1978. J. Biol. Chem. 253: 2834–2845.Google Scholar
  39. 38.
    Jacobs, M. & Huitorel, P., 1979. Eur. J. Biochem. 99: 613–622.Google Scholar
  40. 39.
    Zeeberg, B., Cheek, J. & Caplow, M., 1980. Biochemistry 19: 5078–5086.Google Scholar
  41. 40.
    Pantaloni, D., Carlier, M. F., Simon, C. & Batelier, G., 1981. Biochemistry 20: 4709–4716.Google Scholar
  42. 41.
    Lee, J. C., Corfman, D., Frigon, R. P. & Timasheff, S. N., 1978. Arch. Biochem. Biophys. 185: 4–14.Google Scholar
  43. 42.
    Karr, T. L. & Purich, D. L., 1978. Biochem. Biophys. Res. Comm. 84: 957–961.Google Scholar
  44. 43.
    Margolis, R. L. & Rauch, C. T., 1981. Biochemistry 20: 4451–4458.Google Scholar
  45. 44.
    Burns, R. G. & Pollard, T. D., 1974. FEBS Letters 40: 274–280.Google Scholar
  46. 45.
    Gaskin, F., Cramer, S. B., Cantor, C.R., Adelstein, R. & Shelanski, M. L., 1974. FEBS Letters 40: 281–286.Google Scholar
  47. 46.
    White, H. D., Coughlin, B. A. & Purich, D. L., 1980. J. Biol. Chem. 255: 486–491.Google Scholar
  48. 47.
    Kobayashi, T. & Simizu, T., 1976. J. Biol. Chem. (Tokyo) 79: 1357–1364.Google Scholar
  49. 48.
    Penningroth, S. M. & Kirschner, M. W., 1976. J. Cell. Biol. 70: 407a.Google Scholar
  50. 49.
    Lee, J. C. & Timasheff, S. N., 1975. Biochemistry 14: 5183–5187.Google Scholar
  51. 50.
    Hamel, E. & Lin, C. M., 1981. Arch. Biochem. Biophys. 209: 29–40.Google Scholar
  52. 51.
    Carlier, M. F. & Pantaloni, D., 1978. Biochemistry 17: 1908–1915.Google Scholar
  53. 52.
    Berne, B. J., 1974. J. Mol. Biol. 89: 755–758.Google Scholar
  54. 53.
    Erickson, H. P. & Pantaloni, D., 1981. Biophys. J. 34: 293–309.Google Scholar
  55. 54.
    David-Pfeuty, T., Erickson, H. P. & Pantaloni, D., 1977. Proc. Nat. Acad. Sci. U.S.A. 74: 5372–5376.Google Scholar
  56. 55.
    David-Pfeuty, T., Laporte, J. & Pantaloni, D., 1978. Nature 272: 282–284.Google Scholar
  57. 56.
    Asakura, S., 1961. Biochem. Biophys. Acta 52: 65–75.Google Scholar
  58. 57.
    Nakaoka, Y. & Kasai, M., 1969. J. Mol. Biol. 44: 319.Google Scholar
  59. 58.
    Carlier, M. F. & Pantaloni, D., 1981. Biochemistry 20: 1918–1924.Google Scholar
  60. 59.
    Chien, J. Y., 1948. J. Am. Chem. Soc. 70: 2256–2261.Google Scholar
  61. 60.
    Bonne, D. & Pantaloni, D., 1982. Biochemistry 21: 1075–1081.Google Scholar
  62. 61.
    Weisenberg, R. C. & Decry, W. J., 1976. Nature 263: 792.Google Scholar
  63. 62.
    Penningroth, S. M. & Kirschner, M. W., 1978. Biochemistry 17: 734–740.Google Scholar
  64. 63.
    Karr, T. L., Podrasky, A. E. & Purich, D. L., 1979. Proc. Nat. Acad. Sci. U.S.A. 76: 5475–5479.Google Scholar
  65. 64.
    Cooke, R., 1975. Biochemistry 14: 3250–3256.Google Scholar
  66. 65.
    Carlier, M. F. & Pantaloni, D. Biochemistry 21: 1215–1224 (1982).Google Scholar
  67. 66.
    Crepeau, R., McEwen, B., Dykes, G. & Edelstein, S., 1977. J. Mol. Biol. 116: 301–315.Google Scholar
  68. 67.
    Heidemann, S. R. & McIntosh, J. R., 1980. Nature (London) 286: 517–519.Google Scholar
  69. 68.
    Dentler, W., Granett, S., Witamn, G. B. & Rosenbaum, J. L., 1974. Proc. Nat. Acad. Sci. U.S.A. 71: 1710–1714.Google Scholar
  70. 69.
    Allen, C. & Borisy, G. G., 1974. J. Mol. Biol. 90: 381–402.Google Scholar
  71. 70.
    Summers, K. & Kirschner, M. W., 1979. J. Cell Biol. 83: 205–217.Google Scholar
  72. 71.
    Wegner, A., 1976. J. Mol. Biol. 108: 139–150.Google Scholar
  73. 72.
    Hill, T. L., 1980. Proc. Nat. Acad. Sci. U.S.A. 77: 4803–4807.Google Scholar
  74. 73.
    Hill, T. L., 1981. Biophys. J. 33: 353–371.Google Scholar
  75. 74.
    Margolis, R. L. & Wilson, L., 1978. Cell 13: 1–8.Google Scholar
  76. 75.
    Bergen, L. G. & Borisy, G. G., 1980. J. Cell. Biol. 84: 141–150.Google Scholar
  77. 76.
    Zeeberg, B., Reid, R. & Caplow, M., 1980. J. Biol. Chem. 255: 9891–9899.Google Scholar
  78. 77.
    Terry, B. J. & Purich, D. L., 1980. J. Biol. Chem. 255: 10532–10536.Google Scholar
  79. 78.
    Margolis, R. L., 1981. Proc. Nat. Acad. Sci. U.S.A. 78: 1586–1590.Google Scholar
  80. 79.
    Decry, W. J. & Weisenberg, R. C., 1981 Biochemistry 20: 2316–2324.Google Scholar
  81. 80.
    Margolis, R. L., Wilson, L. & Kiefer, B. I., 1978. Nature (London) 272: 450–452.Google Scholar
  82. 81.
    Cote, R. H. & Borisy, G. G., 1981. J. Mol. Biol. 150: 577–602.Google Scholar
  83. 82.
    Jameson, L. & Caplow, M., 1981. Proc. Nat. Acad. Sci. U.S.A. 78: 3413–3417.Google Scholar
  84. 83.
    Margolis, R. L. & Wilson, L., 1981. Nature 293: 705–711.Google Scholar
  85. 84.
    Bershadsky, A. D. & Gelfand, V. I. Proc. Nat. Acad. Sci. U.S.A. 78: 3610–3613.Google Scholar
  86. 85.
    Kirschner, M. W., 1980. J. Cell Biol. 86: 330–334.Google Scholar
  87. 86.
    Black, M. M. & Lasek, R. J., 1980. J. Cell Biol. 86: 615–623.Google Scholar
  88. 87.
    Hill, T. L., 1981. Proc. Nat. Acad. Sci. U.S.A. 78: 5613–5617.Google Scholar
  89. 88.
    Hill, T. L. & Kirschner, M. W., 1982. Proc. Nat. Acad. Sci. U.S.A. 79: 490–494.Google Scholar
  90. 89.
    Zackroff, R. V., Decry, W. J. & Weisenberg, R. C., 1980. J. Mol. Biol. 139: 641–659.Google Scholar
  91. 90.
    Deery, W. J., Zackaroff, R. V. & Weisenberg, R. C., 1978. J. Cell Biol. 79: 302a.Google Scholar
  92. 91.
    Engelborghs, Y. & Van Houtte, A., 1981. Biophys. Chem., 14: 195–202.Google Scholar
  93. 92.
    Na, G. C. & Timasheff, G. N., 1981. J. Mol. Biol. 151: 165–178.Google Scholar
  94. 93.
    Weisenberg, R. C., 1980. J. Mol. Biol. 139: 660–677.Google Scholar
  95. 94.
    Sandoval, I. V. & Weber, K., 1980. J. Biol. Chem. 225: 6966–6974.Google Scholar
  96. 95.
    Feller, W. In: Introduction to probability and its Applications, Vol. 1 3 edn., John Wiley, New York.Google Scholar
  97. 96.
    David-Pfeuty, T., Simon, C. & Pantaloni, D., 1979. J. Biol. Chem. 254: 11696–11702.Google Scholar
  98. 97.
    Saltarelli, D. & Pantaloni, D., 1981. Biochemistry. (in press.)Google Scholar
  99. 98.
    Lin, O. M. & Hamel, E., 1981. J. Biol. Chem. 256: 9242–9246.Google Scholar
  100. 99.
    Brenner, S. L. & Korn, E. D., 1980. J. Biol. Chem. 255: 841–844.Google Scholar
  101. 100.
    Brenner, S. L. & Korn, E. D., 1981. J. Biol. Chem. 256: 8663–8670.Google Scholar
  102. 101.
    Heusèle, C. & Carlier, M. F., 1981. Biochem. Biophys. Res. Comm., 1981. 103: 332–338Google Scholar
  103. 102.
    Larsson, H., Wallin, M. & Edstrom, A., 1976. Exp. Cell Res. 100: 104–110.Google Scholar
  104. 103.
    Gaskin, F., 1981. Biochemistry 20: 1318–1322.Google Scholar
  105. 104.
    Baker, T. S. & Amos, L. A., 1978. J. Mol. Biol. 123: 89–106.Google Scholar
  106. 105.
    Crepeau, R. H., McEwen, B. & Edelstein, S. J., 1978. Proc. Nat. Acad. Sci. U.S.A. 75: 5006–5010.Google Scholar
  107. 106a.
    Pierson, G. B., Burton, P. R. & Himes, R. H., 1978. J. Cell. Biol. 76: 223–228.Google Scholar
  108. 106b.
    Mandelkow, E. and Mandelkow, E-M. (1981) J. Ultrastruct. Res. 74: 11–33.Google Scholar
  109. 107.
    McEwen, B. & Edelstein, S. J., 1980. J. Mol. Biol. 139: 123–145.Google Scholar
  110. 108.
    Langford, G. M., 1980. J. Cell. Biol. 87: 521–526.Google Scholar
  111. 109.
    Mockrin, S. C. & Korn, E. D., 1980. Biochemistry 19: 5359–5362.Google Scholar
  112. 110.
    Vallee, R. B. & Borisy, G. G., 1978. J. Biol. Chem. 253: 2834–2845.Google Scholar
  113. 111.
    Weisenberg, R. C., 1981. Cell motility. (in press.)Google Scholar

Copyright information

© Martinus Nijhoff/Dr W. Junk Publishers 1982

Authors and Affiliations

  • Marie-France Carlier
    • 1
  1. 1.Laboratoire d'EnzymologieC.N.R.S.Gif-sur-YvetteFrance

Personalised recommendations