Microtubule dynamic instability: A new model with coupled GTP hydrolysis and multistep catastrophe

Abstract

A key question in understanding microtubule dynamics is how GTP hydrolysis leads to catastrophe, the switch from slow growth to rapid shrinkage. We first provide a review of the experimental and modeling literature, and then present a new model of microtubule dynamics. We demonstrate that vectorial, random, and coupled hydrolysis mechanisms are not consistent with the dependence of catastrophe on tubulin concentration and show that, although single‐protofilament models can explain many features of dynamics, they do not describe catastrophe as a multistep process. Finally, we present a new combined (coupled plus random hydrolysis) multiple‐protofilament model that is a simple, analytically solvable generalization of a single‐protofilament model. This model accounts for the observed lifetimes of growing microtubules, the delay to catastrophe following dilution and describes catastrophe as a multistep process.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 54

1. 1.

   Mitchison T, Kirschner M. Dynamic instability of microtubule growth. Nature. 1984;312:237-42.

   Not in our library10.1038/312237a0

2. 2.

   Walker R, O'Brien E, Pryer N, Soboero M, et al. Dynamic instability of individual microtubules analyzed by video light-microscopy – rate constants and transition frequencies. J Cell Biol. 1988;107:1437-48.

   Not in our library10.1083/jcb.107.4.1437

3. 3.

   Gardner MK, Zanic M, Gell C, Bormuth V, et al. Depolymerizing kinesins Kip3 and MCAK shape cellular microtubule architecture by differential control of catastrophe. Cell. 2011;147:1092-103.

   Not in our library10.1016/j.cell.2011.10.037

4. 4.

   Odde DJ, Cassimeris L, Buettner HM. Kinetics of microtubule catastrophe assessed by probabilistic analysis. Biophys J. 1995;69:796-802.

   Not in our library10.1016/s0006-3495(95)79953-2

5. 5.

   Verde F, Dogterom M, Stelzer E, Karsenti E, et al. Control of microtubule dynamics and length by cyclin A-and cyclin B-dependent kinases in Xenopus egg extracts. J Cell Biol. 1992;118:1097-108.

   Not in our library10.1083/jcb.118.5.1097

6. 6.

   Dogterom M, Leibler S. Physical aspects of the growth and regulation of microtubule structures. Phys Rev Lett. 1993;70:1347-50.

   Not in our library10.1103/physrevlett.70.1347

7. 7.

   Hyman AA, Salser S, Drechsel DN, Unwin N, et al. Role of GTP hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue, GMPCPP. Mol Biol Cell. 1992;3:1155-67.

   Not in our library10.1091/mbc.3.10.1155

8. 8.

   Walker RA, Inoué S, Salmon ED. Asymmetric behavior of severed microtubule ends after ultraviolet-microbeam irradiation of individual microtubules in vitro. J Cell Biol. 1989;108:931-7.

   Not in our library10.1083/jcb.108.3.931

9. 9.

   Walker RA, Pryer NK, Salmon ED. Dilution of individual microtubules observed in real time in vitro: evidence that cap size is small and independent of elongation rate. J Cell Biol. 1991;114:73-81.

   Not in our library10.1083/jcb.114.1.73

10. 10.

    Voter WA, O'Brien ET, Erickson HP. Dilution-induced disassembly of microtubules: relation to dynamic instability and the GTP cap. Cell Motil Cytoskeleton. 1990;18:55-62.

    Not in our library10.1002/cm.970180106

11. 11.

    Mickey B, Howard J. Rigidity of microtubules is increased by stabilizing agents. J Cell Biol. 1995;130:909-17.

    Not in our library10.1083/jcb.130.4.909

12. 12.

    Drechsel DN, Kirschner MW. The minimum GTP cap required to stabilize microtubules. Curr Biol. 1994;4:1053-61.

    Not in our library10.1016/s0960-9822(00)00243-8

13. 13.

    Caplow M, Shanks J. Evidence that a single monolayer tubulin-GTP cap is both necessary and sufficient to stabilize microtubules. Mol Biol Cell. 1996;7:663-75.

    Not in our library10.1091/mbc.7.4.663

14. 14.

    O'Brien ET, Voter WA, Erickson HP. GTP hydrolysis during microtubule assembly. Biochemistry. 1987;26:4148-56.

    Not in our library10.1021/bi00387a061

15. 15.

    Melki R, Fievez S, Carlier MF. Continuous monitoring of Pi release following nucleotide hydrolysis in actin or tubulin assembly using 2-amino-6-mercapto-7-methylpurine ribonucleoside and purine-nucleoside phosphorylase as an enzyme-linked assay. Biochemistry. 1996;35:12038-45.

    Not in our library10.1021/bi961325o

16. 16.

    Vandecandelaere A, Brune M, Webb MR, Martin SR, et al. Phosphate release during microtubule assembly: what stabilizes growing microtubules. Biochemistry. 1999;38:8179-88.

    Not in our library10.1021/bi9830765

17. 17.

    Nogales EE, Wolf SGS, Downing KHK. Structure of the alpha beta tubulin dimer by electron crystallography. Nature. 1998;391:199-203.

    Not in our library10.1038/34465

18. 18.

    Kerssemakers JW, Munteanu EL, Laan L, Noetzel TL, et al. Assembly dynamics of microtubules at molecular resolution. Nature. 2006;442:709-12.

    Not in our library10.1038/nature04928

19. 19.

    Schek HT, Gardner MK, Cheng J, Odde DJ, et al. Microtubule assembly dynamics at the nanoscale. Curr Biol. 2007;17:1445-55.

    Not in our library10.1016/j.cub.2007.07.011

20. 20.

    Howard J, Hyman AA. Microtubule polymerases and depolymerases. Curr Opin Cell Biol. 2007;19:31-5.

    Not in our library10.1016/j.ceb.2006.12.009

21. 21.

    Dimitrov A, Quesnoit M, Moutel S, Cantaloube I, et al. Detection of GTP-tubulin conformation in vivo reveals a role for GTP remnants in microtubule rescues. Science. 2008;322:1353-6.

    Not in our library10.1126/science.1165401

22. 22.

    Gardner MK, Charlebois BD, Jánosi IM, Howard J, et al. Rapid microtubule self-assembly kinetics. Cell. 2011;146:582-92.

    Not in our library10.1016/j.cell.2011.06.053

23. 23.

    Chrétien D, Fuller SD, Karsenti E. Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates. J Cell Biol. 1995;129:1311-28.

    Not in our library10.1083/jcb.129.5.1311

24. 24.

    Wade RHR, Hyman AAA. Microtubule structure and dynamics. Curr Opin Cell Biol. 1997;9:12-7.

    Not in our library10.1016/s0955-0674(97)80146-9

25. 25.

    Erickson HP, Voter WA. Nucleation of microtubule assembly. Experimental kinetics, computer fitting of models, and observations on tubulin rings. Ann N Y Acad Sci. 1986;466:552-65.

    Not in our library10.1111/j.1749-6632.1986.tb38432.x

26. 26.

    Howard J. Mechanics of Motor Proteins and the Cytoskeleton. 2001.

    Not in our library

27. 27.

    Hinow P, Rezania V, Tuszyński J. Continuous model for microtubule dynamics with catastrophe, rescue, and nucleation processes. Phys Rev E Stat Nonlin Soft Matter Phys. 2009;80:031904.

    Not in our library10.1103/physreve.80.031904

28. 28.

    Mazilu I, Zamora G, Gonzalez J. A stochastic model for microtubule length dynamics. Physica A. 2010;389:419-27.

    Not in our library

29. 29.

    Ranjith P, Lacoste D, Mallick K, Joanny J-F. Nonequilibrium self-assembly of a filament coupled to ATP/GTP hydrolysis. Biophys J. 2009;96:2146-59.

    Not in our library10.1016/j.bpj.2008.12.3920

30. 30.

    Ranjith P, Mallick K, Joanny J-F, Lacoste D. Role of ATP-hydrolysis in the dynamics of a single actin filament. Biophys J. 2010;98:1418-27.

    Not in our library10.1016/j.bpj.2009.12.4306

31. 31.

    Mirny LA, Needleman DJ. Quantitative Characterization of Filament Dynamics by Single-Molecule Lifetime Measurements in Microtubules, in vitro. 2010.

    Not in our library10.1016/s0091-679x(10)95029-2

32. 32.

    Ranjith P, Kolomeisky AB, Lacoste D. Random hydrolysis controls the dynamic instability of microtubules. Biophys J. 2012;102:1274-83.

    Not in our library10.1016/j.bpj.2011.12.059

33. 33.

    Brun L, Rupp B, Ward JJ, Nédélec F. A theory of microtubule catastrophes and their regulation. Proc Natl Acad Sci USA. 2009;106:21173-8.

    Not in our library10.1073/pnas.0910774106

34. 34.

    Flyvbjerg H, Holy T, Leibler S. Stochastic dynamics of microtubules – a model for caps and catastrophes. Phys Rev Lett. 1994;73:2372-5.

    Not in our library10.1103/physrevlett.73.2372

35. 35.

    Flyvbjerg H, Holy T, Leibler S. Microtubule dynamics: caps, catastrophes, and coupled hydrolysis. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1996;54:5538-60.

    Not in our library10.1103/physreve.54.5538

36. 36.

    Drechsel DN, Hyman AA, Cobb MH, Kirschner MW. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein Tau. Mol Biol Cell. 1992;3:1141-54.

    Not in our library10.1091/mbc.3.10.1141

37. 37.

    Margolin G, Gregoretti IV, Goodson HV, Alber MS. Analysis of a mesoscopic stochastic model of microtubule dynamic instability. Nat Methods. 2006;74:041920.

    Not in our library10.1103/physreve.74.041920

38. 38.

    Chen YD, Hill TL. Monte Carlo study of the GTP cap in a five-start helix model of a microtubule. Proc Natl Acad Sci USA. 1985;82:1131-5.

    Not in our library10.1073/pnas.82.4.1131

39. 39.

    Bayley PM, Schilstra MJ, Martin SR. Microtubule dynamic instability: numerical simulation of microtubule transition properties using a lateral cap model. J Cell Sci. 1990;95:33-48.

    Not in our library10.1242/jcs.95.1.33

40. 40.

    Martin SR, Schilstra MJ, Bayley PM. Dynamic instability of microtubules: Monte Carlo simulation and application to different types of microtubule lattice. Biophys J. 1993;65:578-96.

    Not in our library10.1016/s0006-3495(93)81091-9

Cited by papers we hold 1

• The size of the EB cap determines instantaneous microtubule stability · 2016
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.