Intrinsic bending of microtubule protofilaments

Structure

Volumn 19, Issue 3, 2011, Pages 409-417

  Grafmüller, Andrea ^a   Voth, Gregory A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HETERODIMER; NUCLEOTIDE; TUBULIN;

ARTICLE; CYTOSKELETON; MICROTUBULE; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTOFILAMENT; SIMULATION;

DIMERIZATION; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HUMANS; HYDROLYSIS; MICROTUBULES; MOLECULAR DYNAMICS SIMULATION; POLYMERIZATION; PROTEIN CONFORMATION; THERMODYNAMICS; TUBULIN;

EID: 79952476602     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2010.12.020     Document Type: Article

References (68)

1. Aldaz, H., Rice, L.M., Stearns, T., and Agard, D.A. (2005). Insights into microtubule nucleation from the crystal structure of human gamma-tubulin. Nature 435, 523-527. (Pubitemid 40734251)
2. Arnal, I., Karsenti, E., and Hyman, A.A. (2000). Structural transitions at microtubule ends correlate with their dynamic properties in Xenopus egg extracts. J. Cell Biol. 149, 767-774. (Pubitemid 30327229)
3. Baker, N.A., Sept, D., Joseph, S., Holst, M.J., and McCammon, J.A. (2001). Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98, 10037-10041.
4. Bennett, M.J., Chik, J.K., Slysz, G.W., Luchko, T., Tuszyńnski, J., Sackett, D.L., and Schriemer, D.C. (2009). Structural mass spectrometry of the alpha beta-tubulin dimer supports a revised model of microtubule assembly. Biochemistry 48, 4858-4870.
5. Buey, R.M., Diaz, J.F., and Andreu, J.M. (2006). The nucleotide switch of tubulin and microtubule assembly: A polymerization-driven structural change. Biochemistry 45, 5933-5938. (Pubitemid 43727084)
6. Caplow, M., and Shanks, J. (1996). Evidence that a single monolayer tubulin-GTP cap is both necessary and sufficient to stabilize microtubules. Mol. Biol. Cell 7, 663-675.
7. Chrétien, D., Fuller, S.D., and Karsenti, E. (1995). Structure of growing microtubule ends: 2-dimensional sheets close into tubes at variable rates. J. Cell Biol. 129, 1311-1328.
8. Chu, J.W., and Voth, G.A. (2005). Allostery of actin filaments: molecular dynamics simulations and coarse-grained analysis. Proc. Natl. Acad. Sci. USA 102, 13111-13116.
9. Darden, T., York, D., and Pedersen, L. (1993). Particle mesh Ewald: an N.log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092.
10. de Pablo, P.J., Schaap, I.A.T., MacKintosh, F.C., and Schmidt, C.F. (2003). Deformation and collapse of microtubules on the nanometer scale. Phys. Rev. Lett. 91.
11. Deriu, M.A., Soncini, M., Orsi, M., Patel, M., Essex, J.W., Montevecchi, F.M., and Redaelli, A. (2010). Anisotropic elastic network modeling of entire microtubules. Biophys. J. 99, 2190-2199.
12. Desai, A., and Mitchison, T.J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117.
13. Dima, R.I., and Joshi, H. (2008). Probing the origin of tubulin rigidity with molecular simulations. Proc. Natl. Acad. Sci. USA 105, 15743-15748.
14. Dimitrov, A., Quesnoit, M., Moutel, S., Cantaloube, I., Pous, C., and Perez, F. (2008). Detection of GTP-tubulin conformation in vivo reveals a role for GTP remnants in microtubule rescues. Science 322, 1353-1356. (Pubitemid 352775242)
15. Drabik, P., Gusarov, S., and Kovalenko, A. (2007). Microtubule stability studied by three-dimensional molecular theory of solvation. Biophys. J. 92, 394-403. (Pubitemid 46145773)
16. Drechsel, D.N., and Kirschner, M.W. (1994). The minimum GTP cap required to stabilize microtubules. Curr. Biol. 4, 1053-1061.
17. Elie-Caille, C., Severin, F., Helenius, J., Howard, J., Muller, D.J., and Hyman, A.A. (2007). Straight GDP-tubulin protofilaments form in the presence of taxol. Curr. Biol. 17, 1765-1770.
18. Felgner, H., Frank, R., and Schliwa, M. (1996). Flexural rigidity of microtubules measured with the use of optical tweezers. J. Cell Sci. 109, 509-516. (Pubitemid 26057131)
19. Feller, S.E., Zhang, Y.H., Pastor, R.W., and Brooks, B.R. (1995). Constant-pressure molecular-dynamics simulation: the Langevin piston method. J. Chem. Phys. 103, 4613-4621.
20. Gebremichael, Y., Chu, J.W., and Voth, G.A. (2008). Intrinsic bending and structural rearrangement of tubulin dimer: molecular dynamics simulations and coarse-grained analysis. Biophys. J. 95, 2487-2499.
21. Gigant, B., Curmi, P.A., Martin-Barbey, C., Charbaut, E., Lachkar, S., Lebeau, L., Siavoshian, S., Sobel, A., and Knossow, M. (2000). The 4 A X-ray structure of a tubulin: stathmin-like domain complex. Cell 102, 809-816.
22. Gigant, B., Wang, C.G., Ravelli, R.B.G., Roussi, F., Steinmetz, M.O., Curmi, P.A., Sobel, A., and Knossow, M. (2005). Structural basis for the regulation of tubulin by vinblastine. Nature 435, 519-522. (Pubitemid 40734250)
23. Grant, B.J., Gorfe, A.A., and McCammon, J.A. (2010). Large conformational changes in proteins: signaling and other functions. Curr. Opin. Struct. Biol. 20, 142-147.
24. Howard, J., and Hyman, A.A. (2003). Dynamics and mechanics of the microtubule plus end. Nature 422, 753-758. (Pubitemid 36514118)
25. Humphrey, W., Dalke, A., and Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38.
26. Hyams, J.S., and Lloyd, C.W. (1993). Microtubules (New York: J. B. Harfort, Wiley-Liss).
27. Jiang, H.Q., Jiang, L.Y., Posner, J.D., and Vogt, B.D. (2008). Atomistic-based continuum constitutive relation for microtubules: elastic modulus prediction. Comput. Mech. 42, 607-618.
28. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., and Klein, M.L. (1983). Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935.
29. Kawaguchi, K., Ishiwata, S., and Yamashita, T. (2008). Temperature dependence of the flexural rigidity of single microtubules. Biochem. Biophys. Res. Commun. 366, 637-642.
30. Keskin, O., Durell, S.R., Bahar, I., Jernigan, R.L., and Covell, D.G. (2002). Relating molecular flexibility to function: a case study of tubulin. Biophys. J. 83, 663-680. (Pubitemid 34803607)
31. Kikumoto, M., Kurachi, M., Tosa, V., and Tashiro, H. (2006). Flexural rigidity of individual microtubules measured by a buckling force with optical traps. Biophys. J. 90, 1687-1696.
32. Li, H., DeRosier, D.J., Nicholson, W.V., Nogales, E., and Downing, K.H. (2002). Microtubule structure at 8 angstrom Resolution. Structure 10, 1317-1328.
33. Löwe, J., Li, H., Downing, K.H., and Nogales, E. (2001). Refined structure of alpha beta-tubulin at 3.5 A resolution. J. Mol. Biol. 313, 1045-1057.
34. Luchko, T., Huzil, J.T., Stepanova, M., and Tuszyński, J. (2008). Conformational analysis of the carboxy-terminal tails of human beta-tubulin isotypes. Biophys. J. 94, 1971-1982.
35. MacKerell, A.D., Jr., Bellot, M., Dunbrack, R.L., Evanseck, J.D., Field, M.J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., et al. (1998). All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616.
36. Mackerell, A.D., Feig, M., and Brooks, C.L. (2004). Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25, 1400-1415.
37. Manuel Andreu, J., Garcia de Ancos, J., Starling, D., Hodgkinson, J.L., and Bordas, J. (1989). A synchrotron X-ray scattering characterization of purified tubulin and of its expansion induced by mild detergent binding. Biochemistry 28, 4036-4040. (Pubitemid 19125458)
38. Martyna, G.J., Tobias, D.J., and Klein, M.L. (1994). Constant pressure molecular dynamics algorithms. J. Chem. Phys. 101, 4177-4189.
39. Mickey, B., and Howard, J. (1995). Rigidity of microtubules is increased by stabilizing agents. J. Cell Biol. 130, 909-917.
40. Mitchison, T., and Kirschner, M. (1984). Dynamic instability of microtubule growth. Nature 312, 237-242.
41. Mitra, A., and Sept, D. (2004). Localization of the antimitotic peptide and depsipeptide binding site on beta-tubulin. Biochemistry 43, 13955-13962. (Pubitemid 39482745)
42. Mitra, A., and Sept, D. (2006). Binding and interaction of dinitroanilines with apicomplexan and kinetoplastid alpha-tubulin. J. Med. Chem. 49, 5226-5231.
43. Mitra, A., and Sept, D. (2008). Taxol allosterically alters the dynamics of the tubulin dimer and increases the flexibility of microtubules. Biophys. J. 95, 3252-3258.
44. Morrissette, N.S., Mitra, A., Sept, D., and Sibley, L.D. (2004). Dinitroanilines bind alpha-tubulin to disrupt microtubules. Mol. Biol. Cell 15, 1960-1968.
45. Mozziconacci, J., Sandblad, L., Wachsmuth, M., Brunner, D., and Karsenti, E. (2008). Tubulin dimers oligomerize before their incorporation into microtubules. PLoS ONE 3.
46. Needleman, D.J., Ojeda-Lopez, M.A., Raviv, U., Ewert, K., Miller, H.P., Wilson, L., and Safinya, C.R. (2005). Radial compression of microtubules and the mechanism of action of taxol and associated proteins. Biophys. J. 89, 3410-3423. (Pubitemid 41636096)
47. Neek-Amal, M., Radja, N.H., and Ejtehadi, M.R. (2008). Effective potential of longitudinal interactions between microtubule protofilaments. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 78.
48. Newstead, S., Fowler, P.W., Bilton, P., Carpenter, E.P., Sadler, P.J., Campopiano, D.J., Sansom, M.S.P., and Iwata, S. (2009). Insights into how nucleotide-binding domains power ABC transport. Structure 17, 1213-1222.
49. Nogales, E., and Wang, H.W. (2006). Structural mechanisms underlying nucleotide-dependent self-assembly of tubulin and its relatives. Curr. Opin. Struct. Biol. 16, 221-229.
50. Nogales, E., Wolf, S.G., and Downing, K.H. (1998). Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391, 199-203. (Pubitemid 28092482)
51. Nogales, E., Wang, H.W., and Niederstrasser, H. (2003). Tubulin rings: which way do they curve? Curr. Opin. Struct. Biol. 13, 256-261.
52. Oliva, M.A., Trambaiolo, D., and Löwe, J. (2007). Structural insights into the conformational variability of FtsZ. J. Mol. Biol. 373, 1229-1242.
53. Phillips, J.C., et al. (2005). Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802.
54. Ravelli, R.B.G., Gigant, B., Curmi, P.A., Jourdain, I., Lachkar, S., Sobel, A., and Knossow, M. (2004). Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain. Nature 428, 198-202. (Pubitemid 38374318)
55. Rice, L.M., Montabana, E.A., and Agard, D.A. (2008). The lattice as allosteric effector: Structural studies of alpha beta- and gamma-tubulin clarify the role of GTP in microtubule assembly. Proc. Natl. Acad. Sci. USA 105, 5378-5383.
56. Ryckaert, J., Ciccotti, G., and Berendsen, H. (1977). Numerical-integration of Cartesian equations of motion of a system with constraints: molecular dynamics of N-alkanes. J. Comput. Phys. 23, 327-341.
57. Schek, H.T., Gardner, M.K., Cheng, J., Odde, D.J., and Hunt, A.J. (2007). Microtubule assembly dynamics at the nanoscale. Curr. Biol. 17, 1445-1455.
58. Schlieper, D., Oliva, M.A., Andreu, J.M., and Löwe, J. (2005). Structure of bacterial tubulin BtubA/B: Evidence for horizontal gene transfer. Proc. Natl. Acad. Sci. USA 102, 9170-9175.
59. Sept, D., and MacKintosh, F.C. (2010). Microtubule elasticity: connecting all-atom simulations with continuum mechanics. Phys. Rev. Lett. 104, 018101.
60. Sept, D., Baker, N.A., and McCammon, J.A. (2003). The physical basis of microtubule structure and stability. Protein Sci. 12, 2257-2261.
61. Shearwin, K.E., and Timasheff, S.N. (1994). Effect of colchicine analogs on the dissociation of alpha-beta-tubulin into subunits: the locus of colchicine binding. Biochemistry 33, 894-901. (Pubitemid 24058427)
62. Tuszyński, J.A., Brown, J.A., Crawford, E., Carpenter, E.J., Nip, M.L.A., Dixon, J.M., and Satarić, M.V. (2005). Molecular dynamics simulations of tubulin structure and calculations of electrostatic properties of microtubules. Math. Comput. Model. 41, 1055-1070.
63. VanBuren, V., Odde, D.J., and Cassimeris, L. (2002). Estimates of lateral and longitudinal bond energies within the microtubule lattice. Proc. Natl. Acad. Sci. USA 99, 6035-6040.
64. VanBuren, V., Cassimeris, L., and Odde, D.J. (2005). Mechanochemical model of microtubule structure and self-assembly kinetics. Biophys. J. 89, 2911-2926. (Pubitemid 41636049)
65. Venier, P., Maggs, A.C., Carlier, M.F., and Pantaloni, D. (1994). Analysis of microtubule rigidity using hydrodynamic flow and thermal fluctuations. J. Biol. Chem. 269, 13353-13360.
66. Wang, H.W., and Nogales, E. (2005). Nucleotide-dependent bending flexibility of tubulin regulates microtubule assembly. Nature 435, 911-915.
67. Wassenaar, T.A., and Mark, A.E. (2006). The effect of box shape on the dynamic properties of proteins simulated under periodic boundary conditions. J. Comput. Chem. 27, 316-325.
68. Wells, D.B., and Aksimentiev, A. (2010). Mechanical properties of a complete microtubule revealed through molecular dynamics simulation. Biophys. J. 99, 629-737.