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.
Similar content being viewed by others
References
Erickson, H. P., 1974. J. Cell Biol. 60: 153–167.
Amos, L. A. & Klug, A., 1974. J. Cell Sci. 14: 523–549.
Mandelkow, E., Thomas, J. & Cohen, C., 1977. Proc. Nat. Acad. Sci. U.S.A. 74: 3370–3374.
Oosawa, F. & Asakura, S., 1975. In: Thermodynamics of the Polymerization of Proteins. Acadamic Press, New York.
Voter, W. A. & Erickson, H. P., 1979. J. Supramol. Struct. 10: 419–431.
Weisenberg, R. C., Decry, W. J. & Dickinson, P. J., 1976. Biochemistry 15: 4248–4254.
Arai, T. & Kaziro, Y., 1976. Biochem. Biophys. Res. Comm. 69: 369–376.
Snyder, J. A. & McIntosh, J. R., 1976. Ann. Rev. Biochem. 45: 699–720.
Kirschner, M. W., 1978. Ann. Rev. Cytol. 1–68.
Scheele, R. B. & Borisy, G. G., 1979. In: Microtubules (Roberts & Hyams, eds.) pp. 175–254, Academic Press, New York.
Timasheff, S. N. & Grisham, L. M., 1980. Ann. Rev. Biochem. 49: 565–591.
Weisenberg, R. C., Borisy, G. G. & Taylor, E. W., 1968. Biochemistry 7: 4466–4479.
Weisenberg, R. C., 1972. Science 177: 1104–1105.
Shelanski, M. L., Gaskin, F. & Cantor, C. R., 1973. Proc. Nat. Acad. Sci. U.S.A. 70: 765–768.
Bryan, J., 1972. J. Mol. Biol. 66: 157–168.
Luduena, R. F. & Woodward, D. O., 1973. Proc. Nat. Acad. Sci. U.S.A. 70: 3594–3598.
Luduena, R. F. & Woodward, D. O., 1975. Ann. N.Y. Acad. Sci. 253: 272–283.
Geahlen, R. L. & Haley, B. E., 1977. Proc. Nat. Acad. Sci. U.S.A. 7: 4375–4377.
Geahlen, R. L. & Haley, B. E., 1979. J. Biol. Chem. 254: 11982–11987.
Valenzuela P., Quiroga, M., Zaldivar, J., Rutter, W. J., Kirschner, M. W. & Cleveland, D. W., 1981. Nature 289: 650–655.
Krauhs, E., Little, M., Kempf, T., Hofer-Warbinek, R., Ade, W. & Ponstingl, H., 1981. Proc. Nat. Acad. Sci. U.S.A. 78: 4156–4160.
Spiegelman, B. M., Penningroth, S. M. & Kirschner, M. W., 1977. Cell 12: 587–600.
Little, M., Luduena, R. F., Langford, G. M., Asnes, C. F. & Farrell, K., 1981. J. Mol. Biol. 149: 95–107.
Sheir-Neiss, G., Lai, M. H. & Morris, N. R., 1978. Cell 15: 639–647.
Cabral, F., Sobel, M. E. & Gottesman, M. M., 1980. Cell 20: 29–36.
Oakley, B. R. & Morris, N. R., 1981. Cell 24: 837–845.
Jacobs, M. & Caplow, M., 1976. Biochem. Biophys. Res. Comi. 68: 127–135.
Arai, T., Ihara, Y., Arai, K. & Kaziro, Y., 1975. J. Biochem. (Tokyo) 77: 647–658.
Zeeberg, B. & Caplow, M., 1979. Biochemistry 18: 3880–3886.
Jacobs, M., Smith, H. & Taylor, E. W., 1974. J. Mol. Biol. 89: 455–468.
30. Hammes, G. G. & Schimmel, P. R., 1970. In: The Enzymes (Boyer, ed.) Vol. II 3 en. pp. 67–114. Academic Press, N.Y.
Sherline, P., Leung, J. T. & Kipnis, D. M., 1975. J. Biol. Chem. 250: 5481–5486.
Waechter, F. & Engel, J., 1977. Eur. J. Biochem. 74: 227–232.
Gekko, K. & Timasheff, S. N., 1981. Biochemistry 20: 4667–4677.
Gekko, K. & Timasheff, S. N., 1981. Biochemistry 20: 4677–4687.
Weingarten, M. D., Lockwood, A. H., Hwo, S. Y. & Kirschner, M. W., 1975. Proc. Nat. Acad. Sci. U.S.A. 72: 1858–1862.
Borisy, G. G., Marcum, J. M., Olmsted, J. B., Murphy, D. B. & Johnson, K. A., 1975. Ann. N.Y. Acad. Sci. 253: 107–132.
Vallee, R. B. & Borisy, G. G., 1978. J. Biol. Chem. 253: 2834–2845.
Jacobs, M. & Huitorel, P., 1979. Eur. J. Biochem. 99: 613–622.
Zeeberg, B., Cheek, J. & Caplow, M., 1980. Biochemistry 19: 5078–5086.
Pantaloni, D., Carlier, M. F., Simon, C. & Batelier, G., 1981. Biochemistry 20: 4709–4716.
Lee, J. C., Corfman, D., Frigon, R. P. & Timasheff, S. N., 1978. Arch. Biochem. Biophys. 185: 4–14.
Karr, T. L. & Purich, D. L., 1978. Biochem. Biophys. Res. Comm. 84: 957–961.
Margolis, R. L. & Rauch, C. T., 1981. Biochemistry 20: 4451–4458.
Burns, R. G. & Pollard, T. D., 1974. FEBS Letters 40: 274–280.
Gaskin, F., Cramer, S. B., Cantor, C.R., Adelstein, R. & Shelanski, M. L., 1974. FEBS Letters 40: 281–286.
White, H. D., Coughlin, B. A. & Purich, D. L., 1980. J. Biol. Chem. 255: 486–491.
Kobayashi, T. & Simizu, T., 1976. J. Biol. Chem. (Tokyo) 79: 1357–1364.
Penningroth, S. M. & Kirschner, M. W., 1976. J. Cell. Biol. 70: 407a.
Lee, J. C. & Timasheff, S. N., 1975. Biochemistry 14: 5183–5187.
Hamel, E. & Lin, C. M., 1981. Arch. Biochem. Biophys. 209: 29–40.
Carlier, M. F. & Pantaloni, D., 1978. Biochemistry 17: 1908–1915.
Berne, B. J., 1974. J. Mol. Biol. 89: 755–758.
Erickson, H. P. & Pantaloni, D., 1981. Biophys. J. 34: 293–309.
David-Pfeuty, T., Erickson, H. P. & Pantaloni, D., 1977. Proc. Nat. Acad. Sci. U.S.A. 74: 5372–5376.
David-Pfeuty, T., Laporte, J. & Pantaloni, D., 1978. Nature 272: 282–284.
Asakura, S., 1961. Biochem. Biophys. Acta 52: 65–75.
Nakaoka, Y. & Kasai, M., 1969. J. Mol. Biol. 44: 319.
Carlier, M. F. & Pantaloni, D., 1981. Biochemistry 20: 1918–1924.
Chien, J. Y., 1948. J. Am. Chem. Soc. 70: 2256–2261.
Bonne, D. & Pantaloni, D., 1982. Biochemistry 21: 1075–1081.
Weisenberg, R. C. & Decry, W. J., 1976. Nature 263: 792.
Penningroth, S. M. & Kirschner, M. W., 1978. Biochemistry 17: 734–740.
Karr, T. L., Podrasky, A. E. & Purich, D. L., 1979. Proc. Nat. Acad. Sci. U.S.A. 76: 5475–5479.
Cooke, R., 1975. Biochemistry 14: 3250–3256.
Carlier, M. F. & Pantaloni, D. Biochemistry 21: 1215–1224 (1982).
Crepeau, R., McEwen, B., Dykes, G. & Edelstein, S., 1977. J. Mol. Biol. 116: 301–315.
Heidemann, S. R. & McIntosh, J. R., 1980. Nature (London) 286: 517–519.
Dentler, W., Granett, S., Witamn, G. B. & Rosenbaum, J. L., 1974. Proc. Nat. Acad. Sci. U.S.A. 71: 1710–1714.
Allen, C. & Borisy, G. G., 1974. J. Mol. Biol. 90: 381–402.
Summers, K. & Kirschner, M. W., 1979. J. Cell Biol. 83: 205–217.
Wegner, A., 1976. J. Mol. Biol. 108: 139–150.
Hill, T. L., 1980. Proc. Nat. Acad. Sci. U.S.A. 77: 4803–4807.
Hill, T. L., 1981. Biophys. J. 33: 353–371.
Margolis, R. L. & Wilson, L., 1978. Cell 13: 1–8.
Bergen, L. G. & Borisy, G. G., 1980. J. Cell. Biol. 84: 141–150.
Zeeberg, B., Reid, R. & Caplow, M., 1980. J. Biol. Chem. 255: 9891–9899.
Terry, B. J. & Purich, D. L., 1980. J. Biol. Chem. 255: 10532–10536.
Margolis, R. L., 1981. Proc. Nat. Acad. Sci. U.S.A. 78: 1586–1590.
Decry, W. J. & Weisenberg, R. C., 1981 Biochemistry 20: 2316–2324.
Margolis, R. L., Wilson, L. & Kiefer, B. I., 1978. Nature (London) 272: 450–452.
Cote, R. H. & Borisy, G. G., 1981. J. Mol. Biol. 150: 577–602.
Jameson, L. & Caplow, M., 1981. Proc. Nat. Acad. Sci. U.S.A. 78: 3413–3417.
Margolis, R. L. & Wilson, L., 1981. Nature 293: 705–711.
Bershadsky, A. D. & Gelfand, V. I. Proc. Nat. Acad. Sci. U.S.A. 78: 3610–3613.
Kirschner, M. W., 1980. J. Cell Biol. 86: 330–334.
Black, M. M. & Lasek, R. J., 1980. J. Cell Biol. 86: 615–623.
Hill, T. L., 1981. Proc. Nat. Acad. Sci. U.S.A. 78: 5613–5617.
Hill, T. L. & Kirschner, M. W., 1982. Proc. Nat. Acad. Sci. U.S.A. 79: 490–494.
Zackroff, R. V., Decry, W. J. & Weisenberg, R. C., 1980. J. Mol. Biol. 139: 641–659.
Deery, W. J., Zackaroff, R. V. & Weisenberg, R. C., 1978. J. Cell Biol. 79: 302a.
Engelborghs, Y. & Van Houtte, A., 1981. Biophys. Chem., 14: 195–202.
Na, G. C. & Timasheff, G. N., 1981. J. Mol. Biol. 151: 165–178.
Weisenberg, R. C., 1980. J. Mol. Biol. 139: 660–677.
Sandoval, I. V. & Weber, K., 1980. J. Biol. Chem. 225: 6966–6974.
Feller, W. In: Introduction to probability and its Applications, Vol. 1 3 edn., John Wiley, New York.
David-Pfeuty, T., Simon, C. & Pantaloni, D., 1979. J. Biol. Chem. 254: 11696–11702.
Saltarelli, D. & Pantaloni, D., 1981. Biochemistry. (in press.)
Lin, O. M. & Hamel, E., 1981. J. Biol. Chem. 256: 9242–9246.
Brenner, S. L. & Korn, E. D., 1980. J. Biol. Chem. 255: 841–844.
Brenner, S. L. & Korn, E. D., 1981. J. Biol. Chem. 256: 8663–8670.
Heusèle, C. & Carlier, M. F., 1981. Biochem. Biophys. Res. Comm., 1981. 103: 332–338
Larsson, H., Wallin, M. & Edstrom, A., 1976. Exp. Cell Res. 100: 104–110.
Gaskin, F., 1981. Biochemistry 20: 1318–1322.
Baker, T. S. & Amos, L. A., 1978. J. Mol. Biol. 123: 89–106.
Crepeau, R. H., McEwen, B. & Edelstein, S. J., 1978. Proc. Nat. Acad. Sci. U.S.A. 75: 5006–5010.
Pierson, G. B., Burton, P. R. & Himes, R. H., 1978. J. Cell. Biol. 76: 223–228.
Mandelkow, E. and Mandelkow, E-M. (1981) J. Ultrastruct. Res. 74: 11–33.
McEwen, B. & Edelstein, S. J., 1980. J. Mol. Biol. 139: 123–145.
Langford, G. M., 1980. J. Cell. Biol. 87: 521–526.
Mockrin, S. C. & Korn, E. D., 1980. Biochemistry 19: 5359–5362.
Vallee, R. B. & Borisy, G. G., 1978. J. Biol. Chem. 253: 2834–2845.
Weisenberg, R. C., 1981. Cell motility. (in press.)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Carlier, MF. Guanosine-5′-triphosphate hydrolysis and tubulin polymerization. Mol Cell Biochem 47, 97–113 (1982). https://doi.org/10.1007/BF00234410
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00234410