Dynamic properties of nucleated microtubules: GTP utilisation in the subcritical concentration regime

Journal of Cell Science

Volumn 109, Issue 11, 1996, Pages 2755-2766

  Symmons, Martyn F ^a   Martin, Stephen R ^a   Bayley, Peter M ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Biotinylated; Coupled GTP hydrolysis; EGS seed; GDP assay; Microtubule nucleation; Tubulin

Indexed keywords

GUANOSINE TRIPHOSPHATE; NOCODAZOLE; TUBULIN;

ARTICLE; FLUORESCENCE ANALYSIS; IMMUNOELECTRON MICROSCOPY; MICROSCOPY; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL;

ANIMALS; BIOTIN; COMPUTER SIMULATION; CROSS-LINKING REAGENTS; FLUOROMETRY; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; MICROTUBULES; MONTE CARLO METHOD; NUMERICAL ANALYSIS, COMPUTER-ASSISTED; RABBITS; SUCCINIMIDES; SWINE; TIME FACTORS; TUBULIN;

EID: 0029858894     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Archer, J. and Solomon, F. (1994). Deconstructing the microtubule organizing center. Cell 76, 589-591.
2. Baas, P. W. and Black, M. M. (1990). Individual microtubules in the axon consist of domains that differ in both composition and stability. J. Cell Biol. 111, 495-509.
3. Bailey, N. J. T. (1975). Mathematical Theory of Infectious Diseases. Macmillan, New York.
4. Bayley, P. M. and Martin, S. R. (1989). The Lateral Cap model for dynamic microtubules. Biophys. J. 55, 256a.
5. Bayley, P. M., Schilstra, M. J. and Martin, S. R. (1989). A simple formulation of microtubule dynamics: quantitative implications of the dynamic instability of microtubule populations in vivo and in vitro. J. Cell Sci. 93, 241-254.
6. Bayley, P. M. (1990). What makes microtubules dynamic? J. Cell Sci. 95, 329-334.
7. Bayley, P. M., Schilstra, M. J. and Martin, S. R. (1990). Microtubule dynamic instability: numerical simulation of microtubule transition properties using a Lateral Cap model. J. Cell Sci. 95, 33-48.
8. Bayley, P. M. and Martin, S. R. (1991). Microtubule dynamic instability - some possible physical mechanisms and their implications. Biochem. Soc. Trans. 4, 1023-1028
9. Bayley, P. M., Sharma, K. K. and Martin, S. R. (1993). Microtubule dynamics in vitro. In Microtubules (ed. J. S. Hyams and C. Lloyd), pp. 111-137. Wiley-Liss, New York.
10. Bergen, L. G. and Borisy, G. G. (1980). Head-to-tail polymerisation of microtubules in vitro. J. Cell Biol. 84, 141-150.
11. Bevington, P. (1969). Data Reduction in the Physical Sciences. 1st edn. McGraw Hill, New York.
12. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
13. Brylawski, B. P. and Caplow, M. (1983). Rate for nucleotide release from tubulin. J. Biol. Chem. 258, 760-763.
14. Burns, R. G. (1991). Kinetics of GTP hydrolysis during the assembly of chick brain MAP2-tubulin microtubule protein. Biochem. J. 277, 239-243.
15. Caplow, M. and Shanks, J. (1990). Mechanism of the microtubule GTPase reaction J. Biol. Chem. 265, 8935-8941.
16. Caplow, M. (1992). Microtubule dynamics. Curr. Opin. Cell Biol. 4, 58-65.
17. Carlier, M.-F., Hill, T. L. and Chen, Y. D. (1984). Interference of GTP hydrolysis in the mechanism of microtubule assembly: an experimental study. Proc. Nat. Acad. Sci. USA 81, 771-775.
18. Carlier, M.-F., Didry, D. and Pantaloni, D. (1987). Microtubule elongation and GTP hydrolysis. Role of guanine nucleotides in microtubule dynamics Biochemistry 26, 4428-4437.
19. Carlier, M.-F., Didry, D., Simon, C. and Pantaloni, D. (1989). Mechanism of GTP hydrolysis in tubulin polymerisation - characterization of the kinetic intermediate microtubule GDP-Pi using phosphate analogs. Biochemistry 28, 1783-1791.
20. Carlier, M.-F. and Pantaloni, D. (1981). Kinetic-analysis of the GTP hydrolysis associated with tubulin polymerisation. Biochemistry 20, 1918-1924.
21. Chen, Y. D. and Hill, T. L. (1983). Use of Monte-Carlo calculations in the study of microtubule subunit kinetics. Proc. Nat. Acad. Sci. USA 80, 7520-7523.
22. Chen, Y. D. and Hill, T. L. (1985a). A Monte Carlo study of the GTP cap in a five-start helix model of a microtubule. Proc. Nat. Acad. Sci. USA 82, 1131-1135.
23. Chen, Y. D. and Hill, T. L. (1985b). Theoretical study of microtubules disappearing in solution. Proc. Nat. Acad. Sci. USA 82, 4127-4131.
24. Clark, D. C., Martin, S. R. and Bayley, P. M. (1981). Conformation and assembly characteristics of tubulin and microtubule protein from bovine brain. Biochemistry 20, 1924-1932.
25. Cornish-Bowden, A. (1975). Principles of Enzyme Kinetics. Butterworth, London.
26. Dogterom, M. and Leibler, S. (1993). Physical aspects of the growth and regulation of microtubule structures. Physiol. Rev. Lett. 70, 1347-1350.
27. Drechsel, D. N. and Kirschner, M. W. (1994). The minimum cap required to stabilise microtubules. Curr. Biol. 4, 1053-1061.
28. Engelborghs, Y. (1994). Microtubules - dissipative structures formed by self-assembly. Biosensors and Bioelectronics 9, 685-689.
29. Fygenson, D. K., Braun, E. and Libchaber, A. (1994). Phase diagram of microtubules. Physiol. Rev. E 50, 1579-1588.
30. Gutfreund, H. (1995). Kinetics for the Life Sciences: Receptors, Transmitters and Catalysts. Cambridge University Press, Cambridge.
31. Harlow, E. and Lane, D. (1988). Antibodies: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
32. Hill, T. L. and Carlier, M.-F. (1983). Steady-state theory of the interference of GTP hydrolysis in the mechanism of microtubule assembly. Proc. Nat. Acad. Sci. USA 80, 7234-7238.
33. Hill, T. L. (1984). Introductory analysis of the GTP-cap phase-change kinetics at the end of a microtubule. Proc. Nat. Acad. Sci. USA 81, 6728-6732.
34. Hill, T. L. and Chen, Y. (1984). Phase changes at the end of a microtubule with a GTP Cap. Proc. Nat. Acad. Sci. USA 81, 5772-5776.
35. Hill, T. L. and Kirschner, M. W. (1984). Bioenergetics and kinetics of microtubule and actin filament assembly-disassembly. Int. Rev. Cytol. 78, 1-125.
36. Hill, T. L. (1987). Linear Aggregation Theory in Cell Biology. Springer Verlag, New York.
37. Holy, T. E. and Leibler, S. (1994). Dynamic instability as an efficient way to search space. Proc. Nat. Acad. Sci. USA 91, 5682-5685.
38. Horio, T. and Hotani, H. (1986). Visualization of the dynamic instability of individual microtubules by dark-field microscopy. Nature 321, 605-607.
39. Johnson, K. A. and Rosenbaum, J. L. (1992) Replication of basal bodies and centrioles. Curr. Opin. Cell Biol. 4, 80-85.
40. Jordan, M. A., Thrower, D. and Wilson, L. (1992). Effects of vinblastine, podophyllotoxin and nocodazole on mitotic spindles. Implications for the role of microtubule dynamics in mitosis. J. Cell Sci. 102, 401-416.
41. Koshland, D. E., Mitchison, T. J. and Kirschner, M. W. (1988). Polewards chromosome movement driven by microtubule depolymerization in vitro. Nature 331, 499-504.
42. Martin, S. R., Schilstra, M. J. and Bayley, P. M. (1991). Opposite-end behaviour of dynamic microtubules. Biochim. Biophys. Acta 1073, 555-561.
43. Martin, S. R., Schilstra, M. J. and Bayley, P. M. (1993). Dynamic instability of microtubules: Monte Carlo simulation and application to different types of microtubule lattice. Biophys. J. 65, 578-596.
44. McClure, W. R. (1969). A kinetic analysis of coupled enzyme assays. Biochemistry 8, 2782-2786.
45. i intermediates in microtubule assembly. Biochemistry 29, 8921-8932.
46. Mitchison, T. and Kirschner, M. (1984a). Microtubule assembly nucleated by isolated centrosomes. Nature 312, 232-237.
47. Mitchison, T. and Kirschner, M. (1984b). Dynamic instability of microtubule growth. Nature 312, 237-242.
48. Oakley, B. R. (1995). Cell biology - a nice ring to the centrosome. Nature 378, 555-556.
49. Odde, D. J., Cassimeris, L. and Buettner, H. M. (1995). Kinetics of microtubule catastrophe assessed by probabilistic analysis. Biophys. J. 69, 796-802.
50. O'Brien, E. T., Voter, W. A. and Erickson, H. P. (1987). GTP hydrolysis during microtubule assembly. Biochemistry 26, 4148-4156.
51. Prescott, A. R., Dowrick, P. G. and Warn, R. M. (1992). Stable and slow-turning over microtubules characterise the processes of motile epithelial cells treated with scatter factor. J. Cell Sci. 92, 103-112.
52. Purich, D. L. and Kristofferson, D. (1984). Microtubule assembly: a review of progress, principles and perspectives. Advan. Protein Chem. 36, 133-212.
53. Rothwell, S. W., Grasser, W. A. and Murphy, D. B. (1986). End-to-end annealing of microtubules in vitro. J. Biol. Chem. 102, 619-627.
54. Sage, C. R., Dougherty, C. A., Davis, A. S., Burns, R. G., Wilson, L. and Farrell, K. W. (1995). Site-directed mutagenesis of putatative GTP-binding sites of yeast β-tubulin, evidence that α, β and γ-tubulin are atypical GTPases. Biochemistry 34, 7409-7419.
55. Schilstra, M. J., Martin, S. R. and Bayley, P. M. (1987). On the relationship between nucleotide hydrolysis and microtubule assembly: studies with a GTP-regenerating system. Biochem. Biophys. Res. Commun. 147, 588-595.
56. Schilstra, M. J., Bayley, P. M. and Martin, S. R. (1991). The effect of solution composition on microtubule dynamic instability. Biochem. J. 277, 839-847.
57. Stewart, R. J., Farrell, K. W. and Wilson, L. (1990). Role of GTP hydrolysis in microtubule polymerisation: evidence for a coupled hydrolysis mechanism. Biochemistry 29, 6489-6498.
58. Symmons, M. F. and Burns, R. G. (1991). Assembly of chick brain MAP2-tubulin microtubule protein. Analysis of tubulin subunit flux rates by immunofluorescence. Biochem. J. 277, 245-253.
59. Terry, B. J. and Purich, D. L. (1979). Nucleotide release from tubulin and nucleoside-5′-diphosphate kinase action in microtubule assembly. J. Biol. Chem. 254, 9469-9476.
60. Vandecandelaere, A., Martin, S. R., Schilstra, M. J. and Bayley, P. M. (1994). Effects of tubulin-colchicine complex on microtubule dynamic instability. Biochemistry 33, 2792-2801
61. Vandecandelaere, A., Martin, S. R. and Bayley, P. M. (1995). Regulation of microtubule dynamic instability by tubulin-GDP. Biochemistry 34, 1332-1343.
62. Voter, W. A., O'Brien, E. T. and Erickson, H. P. (1991). Dilution-induced disassembly of microtubules: relation to dynamic instability and the GTP cap. Cell Motil. Cytoskel. 18, 55-62.
63. Walker, R. A., O'Brien, E. T., Pryer, N. K., Soboeiro, M. F., Voter, W. A., Erickson, H. P. and Salmon, E. D. (1988). Dynamic instability of individual, MAP-free microtubules analysed by video light microscopy: rate constants and transition frequencies. J. Cell Biol. 107, 1437-1448.
64. Walker, R. A., Pryer, N. K. and Salmon, E. D. (1991). Dilution of individual microtubule observed in real time in vitro: evidence that cap size is small and independent of elongation rate. J. Cell Biol. 114, 73-81.