Radial compression of microtubules and the mechanism of action of taxol and associated proteins

Biophysical Journal

Volumn 89, Issue 5, 2005, Pages 3410-3423

  Needleman, Daniel J ^a,b   Ojeda Lopez, Miguel A ^a,b   Raviv, Uri ^a,b   Ewert, Kai ^a,b   Miller, Herbert P ^b   Wilson, Leslie ^b   Safinya, Cyrus R ^a,b  

^a University of California   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN; PACLITAXEL; POLYMER; TUBULIN;

ARTICLE; CANCER CHEMOTHERAPY; COMPRESSION; CONTROLLED STUDY; CYTOSKELETON; DEPOLYMERIZATION; DRUG MECHANISM; MICROSCOPY; MICROTUBULE; MICROTUBULE ASSEMBLY; NONHUMAN; OSMOTIC PRESSURE; OSMOTIC STRESS; PROTOFILAMENT; SYNCHROTRON; TRANSMISSION ELECTRON MICROSCOPY; X RAY DIFFRACTION;

EID: 27744552013     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.057679     Document Type: Article

References (84)

1. Lowe, J., H. Li, K. H. Downing, and E. Nogales. 2001. Refined structure of alpha beta-tubulin at 3.5 Å resolution. J. Mol. Biol. 313:1045-1057.
2. Li, H., D. J. DeRosier, W. V. Nicholson, E. Nogales, and K. H. Downing. 2002. Microtubule structure at 8 Å resolution. Structure. 10:1317-1328.
3. Chretien, D., S. D. Fuller, and E. Karsenti. 1995. Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates. J. Cell Biol. 129:1311-1328.
4. Mandelkow, E. M., E. Mandelkow, and R. A. Milligan. 1991. Microtubule dynamics and microtubule caps: a time-resolved cryoelectron microscopy study. J. Cell Biol. 114:977-991.
5. Desai, A., and T. J. Mitchison. 1997. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13:83-117.
6. Olmsted, J. B., and G. G. Borisy. 1975. Ionic and nucleotide requirements for microtubule polymerization in vitro. Biochemistry. 14:2996-3005.
7. Jordan, M. A., and L. Wilson. 2004. Microtubules as a target for anticancer drugs. Nat. Rev. Cancer. 4:253-265.
8. Derry, W. B., L. Wilson, and M. A. Jordan. 1995. Substoichiometric binding of taxol suppresses microtubule dynamics. Biochemistry. 34:2203-2211.
9. Amos, L. A., and J. Lowe. 1999. How taxol stabilises microtubule structure. Chem. Biol. 6:R65-R69.
10. Arnal, I., and R. H. Wade. 1995. How does taxol stabilize microtubules? Curr. Biol. 5:900-908.
11. Panda, D., B. L. Goode, S. C. Feinstein, and L. Wilson. 1995. Kinetic stabilization of microtubule dynamics at steady state by tau and microtubule-binding domains of tau. Biochemistry. 34:11117-11127.
12. Bunker, J. M., L. Wilson, M. A. Jordan, and S. C. Feinstein. 2004. Modulation of microtubule dynamics by tau in living cells: implications for development and neurodegeneration. Mol. Biol. Cell. 15:2720-2728.
13. Lee, V. M. Y., M. Goedert, and J. Q. Trojanowski. 2001. Neurodegenerative taupathies. Annu. Rev. Neurosci. 24:1121-1159.
14. Cassimeris, L., and C. Spittle. 2001. Regulation of microtubule- associated proteins. Int. Rev. Cytol. 210:163-226.
15. Hirokawa, N. 1991. Molecular architecture and dynamics of the neuronal cytoskeleton. In The Neuronal Cytoskeleton. R. D. Burgoyne, editor. Wiley-Liss, New York. 5-74.
16. MacRae, T. H. 1992. Microtubule organization by cross-linking and bundling proteins. Biochim. Biophys. Acta. 1160:145-155.
17. Lida, J., T. J. Itoh, H. Hotani, K. Nishiyama, H. Murofushi, J. C. Bulinski, and S. Hisanaga. 2002. The projection domain of MAP4 suppresses the microtubule-bundling activity of the microtubule-binding domain. J. Mol. Biol. 320:97-106.
18. Chen, J., Y. Kanai, N. J. Cowan, and N. Hirokawa. 1992. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature. 360:674-677.
19. Chapin, S. J., J. C. Bulinski, and G. G. Gundersen. 1991. Microtubule bundling in cells. Nature. 349:24.
20. Marx, A., J. Pless, E. M. Mandelkow, and E. Mandelkow. 2000. On the rigidity of the cytoskeleton: are MAPs crosslinkers or spacers of microtubules? Cell. Mol. Biol. 46:949-965.
21. Lee, G., and R. Brandt. 1992. Microtubule-bundling studies revisited: is there a role for MAPs. Trends Cell Biol. 2:286-289.
22. Asakura, S., and F. Oosawa. 1958. Interaction between particles suspended in solutions of macromolecules. J. Polym. Sci. [B]. 33:183-192.
23. Dogic, Z., and S. Fraden. 2001. Development of model colloidal liquid crystals and the kinetics of the isotropic-smectic transition. Philisophical Transactions of the Royal Society of London. 359:997-1014.
24. Adams, M., and S. Fraden. 1998. Phase behavior of mixtures of rods (tobacco mosaic virus) and spheres (polyethylene oxide, bovine serum albumin). Biophys. J. 74:669-677.
25. Bloomfield, V. 1996. DNA condensation. Curr. Opin. Struct. Biol. 6:334-341.
26. Hosek, M., and J. X. Tang. 2004. Polymer-induced bundling of F-actin and the depletion force. Phys. Rev. E. 69:051907.
27. Needleman, D. J., et al. 2004. Synchrotron x-ray diffraction study of microtubules buckling and bundling under osmotic stress: a probe of interprotofilament interactions. Phys. Rev. Lett. 93:198104.
28. Walter, H., and D. E. Brooks. 1995. Phase separation in cytoplasm, due to macromolecular crowding, is the basis for microcompartmentation. FEBS Lett. 361:135-139.
29. Parsegian, V. A., R. P. Rand, and D. C. Rau. 1995. Macromolecules and water: probing with osmotic stress. Methods Enzymol. 259:43-94.
30. Millman, B. M., T. C. Irving, B. G. Nickel, and M. E. Loosley-Millman. 1984. Interred forces in aqueous gels of tobacco mosaic virus. Biophys. J. 45:551-556.
31. Rau, R. C., B. Lee, and V. A. Parsegian. 1984. Measurement of the repulsive force between polyelectrolyte molecules in ionic solution: hydration forces between parallel DNA double helices. Proc. Natl. Acad. Sci. USA. 81:2621-2625.
32. Dogic, Z., et al. 2004. Isotropic-nematic phase transition in suspensions of filamentous virus and the neutral polymer dextran. Phys. Rev. E. 69:051702.
33. Mason, T. G. 2002. Osmotically driven shape-dependent colloidal separations. Phys. Rev. E. 66:060402.
34. Kurz, J. C., and R. C. Williams. 1995. Microtubule-associated proteins and the flexibility of microtubules. Biochemistry. 34:13374-13380.
35. Gittes, F., B. Mickey, J. Nettleton, and J. Howard. 1993. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120:923-934.
36. Mickey, B., and J. Howard. 1995. Rigidity of microtubules is increased by stabilizing agents. J. Cell Biol. 130:909-917.
37. Venier, P., A. C. Maggs, M. F. Carlier, and D. Pantaloni. 1994. Analysis of microtubule rigidity using hydrodynamic flow and thermal fluctuations. J. Biol. Chem. 269:13353-13360.
38. Felgner, H., R. Frank, J. Biernat, E. M. Mandelkow, E. Mandelkow, B. Ludin, A. Matus, and M. Schliwa. 1997. Domains of neuronal microtubule- associated proteins and flexural rigidity of microtubules. J. Cell Biol. 138:1067-1075.
39. Felgner, H., R. Frank, and M. Schliwa. 1996. Flexural rigidity of microtubules measured with the use of optical tweezers. J. Cell Sci. 109:509-516.
40. Vinckier, A., C. Dumortier, Y. Engelborghs, and L. Hellemans. 1996. Dynamical and mechanical study of immobilized microtubules with atomic force microscopy. Journal of Vacuum Science and Technology B. 14:1427-1431.
41. de Pablo, P. J., I. A. Schaap, F. C. MacKintosh, and C. F. Schmidt. 2003. Deformation and collapse of microtubules on the nanometer scale. Phys. Rev. Lett. 91:098101.
42. Chretien, D., and S. D. Fuller. 2000. Microtubules switch occasionally into unfavorable configurations during elongation. J. Mol. Biol. 298:663-676.
43. Chretien, D., H. Flyvbjerg, and S. D. Fuller. 1998. Limited flexibility of the interprotofilament bonds in microtubules assembled from pure tubulin. Eur. Biophys. J. 27:490-500.
44. Janosi, I. M., D. Chretien, and H. Flyvbjerg. 2002. Structural microtubule cap: stability, catastrophe, rescue, and third state. Biophys. J. 83:1317-1330.
45. Janosi, I. M., D. Chretien, and H. Flyvbjerg. 1998. Modeling elastic properties of microtubule tips and walls. Eur. Biophys. J. 27:501-513.
46. Arakawa, T., and S. N. Timasheff. 1982. Stabilization of protein structure by sugars. Biochemistry. 21:6536-6544.
47. Arakawa, T., and S. N. Timasheff. 1985. Mechanism of poly(ethylene glycol) interaction with proteins. Biochemistry. 24:6756-6762.
48. Lee, J. C., and L. L. Y. Lee. 1979. Interaction of calf brain tubulin with poly(ethylene glycols). Biochemistry. 18:5518-5526.
49. Herzog, W., and K. Weber. 1978. Microtubule formation by pure brain tubulin in vitro. The influence of dextran and poly(ethylene glycol). Eur. J. Biochem. 91:249-254
50. Fuller, N., and R. P. Rand. 1999. Water in actin polymerization. Biophys. J. 76:3261-3266.
51. Hitt, A. L., A. R. Cross, and R. C. Williams. 1990. Microtubule solutions display nematic liquid crystal structure. J. Biol. Chem. 265:1639-1647.
52. Doi, M., and S. F. Edwards. 1986. The Theory of Polymer Dynamics. International Series of Monographs on Physics, Vol. 73. Clarendon Press, Oxford.
53. Andreu, J. M., J. Bordas, J. F. Diaz, J. Garcia de Ancos, R. Gil, F. J. Medrano, E. Nogales, E. Pantos, and E. Towns-Andrews. 1992. Low resolution structure of microtubules in solution. J. Mol. Biol. 226:169-184.
54. Bordas, J., E. M. Mandelkow, and E. Mandelkow. 1983. Stages of tubulin assembly and disassembly studied by time-resolved synchrotron x-ray scattering. J. Mol. Biol. 164:89-135.
55. Needleman, D. J., M. A. Ojeda-Lopez, U. Raviv, H. P. Miller, L. Wilson, and C. R. Safinya. 2004. Higher order assembly of microtubules by counter-ions: from hexagonal bundles to living necklaces. Proc. Natl. Acad. Sci. USA. 101:16099-16103.
56. Als-Nielsen, J., and D. McMorrow. 2001. Elements of Modem X-Ray Physics. John Wiley & Sons, New York.
57. Kittel, C. 1995. Introduction to Solid State Physics. Wiley, Hoboken, NJ.
58. Curry, S., H. Mandelkow, P. Brick, and N. Franks. 1998. Crystal structure of human serum albumin complexed with fatty acid reveals an asymmetric distribution of binding sites. Nat. Struct. Biol. 5:827-835.
59. Santos, S. F., et al. 2003. A systematic study of bovine serum albumin (BSA) and sodium dodecyl sulfate (SDS) interactions by surface tension and small angle x-ray scattering. J. Colloid Interface Sci. 262:400-408.
60. Giddings, J. C., et al. 1968. Statistical theory for the equilibrium distribution of rigid molecules in inert porous networks. Exclusion chromatography. J. Phys. Chem. 72:4397-4408.
61. Devanand, K., and J. C. Selser. 1991. Asymptotic-behavior and long-range interactions in aqueous-solutions of poly(ethylene oxide). Macromolecules. 24:5943-5947.
62. Nodmeier, E. 1993. Static and dynamic light-scattering solution behavior of pullulan and dextran in comparison. J. Phys. Chem. 97:5770-5785.
63. Casassa, E. F. 1967. Equilibrium distribution of flexible polymer chains between a macroscopic solution phase and small voids. J. Polym. Sci. 5:773-778.
64. Daoud, M., and P. G. D. Gennes. 1977. Statistic of macromolecular solutions trapped in small pores. J. Phys. [E]. 38:85-93.
65. Farrell, K. W., and L. Wilson. 1984. Tubulin-colchicine complexes differentially poison opposite microtubule ends. Biochemistry. 23:3741-3748.
66. Li, Y. K., R. Edsall Jr., P. G. Jagtap, D. G. Kingston, and S. Bane. 2000. Equilibrium studies of a fluorescent paclitaxel derivative binding to microtubules. Biochemistry. 39:616-623.
67. Leckband, D., and J. Israelachvili. 2001. Intermolecular forces in biology. Q. Rev. Biophys. 34:105-267.
68. Baker, N. A., D. Sept, S. Joseph, M. J. Holst, and J. A. McCammon. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA. 98:10037-10041.
69. Strey, H. H., R. Podgornik, D. C. Rau, and V.A. Parsegian. 1998. DNA-DNA interactions. Curr. Opin. Struct. Biol. 8:309-313.
70. Howard, J. 2001. Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates, Sunderland, MA.
71. Ventsel, E., and T. Krauthammer. 2001. Thin Plates and Shells. Marcel Dekker, Inc., New York.
72. Sept, D., N. A. Bakr, and J. A. Mccammon. 2003. The physical basis of microtubule structure and stability. Protein Sci. 12:2257-2261.
73. Keskin, O., S. R. Durell, I. Bahar, R. L. Jernigan, and D. G. Cove. 2002. Relating molecular flexibility to function: a case study of tubulin. Biophys. J. 83:663-680.
74. Stukalin, E. B., and A. B. Kolomeisky. 2004. Simple growth models of rigid multifilament biopolymers. J. Chem. Phys. 121:1097-1104.
75. Landau, L. D., and E. M. Lifshitz. 2000. Theory of Elasticity. Butterworth-Heinemann, Oxford.
76. Schaap, I. A. T., P. J. de Pablo, and C. F. Schmidt. 2004. Resolving the molecular structure of microtubules under physiological conditions with scanning force microscopy. Eur. Biophys. J. 33:462-467.
77. Chan, S. P., et al. 2003. Carbon nanotube bundles under high pressure: transformation to low-symmetry structures. Phys. Rev. B. 68:075404.
78. Elliot, J. A., et al. 2004. Collapse of single-wall carbon nanotubes is diameter dependent. Phys. Rev. Lett. 92:095501.
79. Lorman, V., R. Podgornik, and B. Zeks. 2001. Positional, reorientational, and bond orientational order in DNA mesophases. Phys. Rev. Lett. 87:218101.
80. Zhang, X. H., Z. F. Liu, and X. G. Gong. 2004. Comment on "Collapse of single-wall carbon nanotubes is diameter dependent". Phys. Rev. Lett. 93:149601.
81. Dogterom, M., and B. Yurke. 1997. Measurement of the force-velocity relation of growing microtubules. Science. 278:856-860.
82. Krasilnikov, O. V., and S. M. Bezrukov. 2004. Polymer partitioning from nonideal solutions into protein voids. Macromolecules. 37:2650-2657.
83. Bray, D. 2001. Cell Movements. Garland, New York.
84. Rieder, C., and A. S. Bajer. 1977. Heat-induced reversible hexagonal packing of spindle microtubules. J. Cell Biol. 74:717-725.