• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of biophysjLink to Publisher's site
Biophys J. Sep 1995; 69(3): 796–802.
PMCID: PMC1236309

Kinetics of microtubule catastrophe assessed by probabilistic analysis.

Abstract

Microtubules are cytoskeletal filaments whose self-assembly occurs by abrupt switching between states of roughly constant growth and shrinkage, a process known as dynamic instability. Understanding the mechanism of dynamic instability offers potential for controlling microtubule-dependent cellular processes such as nerve growth and mitosis. The growth to shrinkage transitions (catastrophes) and the reverse transitions (rescues) that characterize microtubule dynamic instability have been assumed to be random events with first-order kinetics. By direct observation of individual microtubules in vitro and probabilistic analysis of their distribution of growth times, we found that while the slower growing and biologically inactive (minus) ends obeyed first-order catastrophe kinetics, the faster growing and biologically active (plus) ends did not. The non-first-order kinetics at plus ends imply that growing microtubule plus ends have an effective frequency of catastrophe that depends on how long the microtubules have been growing. This frequency is low initially but then rises asymptotically to a limiting value. Our results also suggest that an additional parameter, beyond the four parameters typically used to describe dynamic instability, is needed to account for the observed behavior and that changing this parameter can significantly affect the distribution of microtubule lengths at steady state.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.3M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bamburg JR, Bray D, Chapman K. Assembly of microtubules at the tip of growing axons. Nature. 1986 Jun 19;321(6072):788–790. [PubMed]
  • Bayley PM, Schilstra MJ, Martin SR. A simple formulation of microtubule dynamics: quantitative implications of the dynamic instability of microtubule populations in vivo and in vitro. J Cell Sci. 1989 Jun;93(Pt 2):241–254. [PubMed]
  • Bayley PM, Schilstra MJ, Martin SR. Microtubule dynamic instability: numerical simulation of microtubule transition properties using a Lateral Cap model. J Cell Sci. 1990 Jan;95(Pt 1):33–48. [PubMed]
  • Belmont LD, Hyman AA, Sawin KE, Mitchison TJ. Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell. 1990 Aug 10;62(3):579–589. [PubMed]
  • Bentley D, Toroian-Raymond A. Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment. Nature. 1986 Oct 23;323(6090):712–715. [PubMed]
  • Buettner HM, Pittman RN, Ivins JK. A model of neurite extension across regions of nonpermissive substrate: simulations based on experimental measurement of growth cone motility and filopodial dynamics. Dev Biol. 1994 Jun;163(2):407–422. [PubMed]
  • Carlier MF, Pantaloni D. Kinetic analysis of guanosine 5'-triphosphate hydrolysis associated with tubulin polymerization. Biochemistry. 1981 Mar 31;20(7):1918–1924. [PubMed]
  • Cassimeris L, Pryer NK, Salmon ED. Real-time observations of microtubule dynamic instability in living cells. J Cell Biol. 1988 Dec;107(6 Pt 1):2223–2231. [PMC free article] [PubMed]
  • Cassimeris LU, Wadsworth P, Salmon ED. Dynamics of microtubule depolymerization in monocytes. J Cell Biol. 1986 Jun;102(6):2023–2032. [PMC free article] [PubMed]
  • Chen YD, Hill TL. Monte Carlo study of the GTP cap in a five-start helix model of a microtubule. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1131–1135. [PMC free article] [PubMed]
  • Daniels MP. Colchicine inhibition of nerve fiber formation in vitro. J Cell Biol. 1972 Apr;53(1):164–176. [PMC free article] [PubMed]
  • Dogterom M, Leibler S. Physical aspects of the growth and regulation of microtubule structures. Phys Rev Lett. 1993 Mar 1;70(9):1347–1350. [PubMed]
  • 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 Oct;3(10):1141–1154. [PMC free article] [PubMed]
  • Erickson HP, O'Brien ET. Microtubule dynamic instability and GTP hydrolysis. Annu Rev Biophys Biomol Struct. 1992;21:145–166. [PubMed]
  • Flyvbjerg H, Holy TE, Leibler S. Stochastic dynamics of microtubules: A model for caps and catastrophes. Phys Rev Lett. 1994 Oct 24;73(17):2372–2375. [PubMed]
  • Gliksman NR, Parsons SF, Salmon ED. Okadaic acid induces interphase to mitotic-like microtubule dynamic instability by inactivating rescue. J Cell Biol. 1992 Dec;119(5):1271–1276. [PMC free article] [PubMed]
  • Gliksman NR, Skibbens RV, Salmon ED. How the transition frequencies of microtubule dynamic instability (nucleation, catastrophe, and rescue) regulate microtubule dynamics in interphase and mitosis: analysis using a Monte Carlo computer simulation. Mol Biol Cell. 1993 Oct;4(10):1035–1050. [PMC free article] [PubMed]
  • Hill TL. Introductory analysis of the GTP-cap phase-change kinetics at the end of a microtubule. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6728–6732. [PMC free article] [PubMed]
  • Horio T, Hotani H. Visualization of the dynamic instability of individual microtubules by dark-field microscopy. Nature. 1986 Jun 5;321(6070):605–607. [PubMed]
  • Kirschner M, Mitchison T. Beyond self-assembly: from microtubules to morphogenesis. Cell. 1986 May 9;45(3):329–342. [PubMed]
  • Kowalski RJ, Williams RC., Jr Microtubule-associated protein 2 alters the dynamic properties of microtubule assembly and disassembly. J Biol Chem. 1993 May 5;268(13):9847–9855. [PubMed]
  • Mandelkow EM, Mandelkow E, Milligan RA. Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopy study. J Cell Biol. 1991 Sep;114(5):977–991. [PMC free article] [PubMed]
  • Martin SR, Schilstra MJ, Bayley PM. Dynamic instability of microtubules: Monte Carlo simulation and application to different types of microtubule lattice. Biophys J. 1993 Aug;65(2):578–596. [PMC free article] [PubMed]
  • Mitchison T, Kirschner M. Dynamic instability of microtubule growth. Nature. 1984 Nov 15;312(5991):237–242. [PubMed]
  • Mitchison TJ, Kirschner MW. Some thoughts on the partitioning of tubulin between monomer and polymer under conditions of dynamic instability. Cell Biophys. 1987 Dec;11:35–55. [PubMed]
  • O'Brien ET, Voter WA, Erickson HP. GTP hydrolysis during microtubule assembly. Biochemistry. 1987 Jun 30;26(13):4148–4156. [PubMed]
  • Odde DJ, Buettner HM. Time series characterization of simulated microtubule dynamics in the nerve growth cone. Ann Biomed Eng. 1995 May-Jun;23(3):268–286. [PubMed]
  • Pryer NK, Walker RA, Skeen VP, Bourns BD, Soboeiro MF, Salmon ED. Brain microtubule-associated proteins modulate microtubule dynamic instability in vitro. Real-time observations using video microscopy. J Cell Sci. 1992 Dec;103(Pt 4):965–976. [PubMed]
  • Salmon T, Walker RA, Pryer NK. Video-enhanced differential interference contrast light microscopy. Biotechniques. 1989 Jun;7(6):624–633. [PubMed]
  • Sammak PJ, Borisy GG. Direct observation of microtubule dynamics in living cells. Nature. 1988 Apr 21;332(6166):724–726. [PubMed]
  • Schnapp BJ. Viewing single microtubules by video light microscopy. Methods Enzymol. 1986;134:561–573. [PubMed]
  • Shelden E, Wadsworth P. Observation and quantification of individual microtubule behavior in vivo: microtubule dynamics are cell-type specific. J Cell Biol. 1993 Feb;120(4):935–945. [PMC free article] [PubMed]
  • Tanaka EM, Kirschner MW. Microtubule behavior in the growth cones of living neurons during axon elongation. J Cell Biol. 1991 Oct;115(2):345–363. [PMC free article] [PubMed]
  • Verde F, Dogterom M, Stelzer E, Karsenti E, Leibler S. Control of microtubule dynamics and length by cyclin A- and cyclin B-dependent kinases in Xenopus egg extracts. J Cell Biol. 1992 Sep;118(5):1097–1108. [PMC free article] [PubMed]
  • 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 Mar;108(3):931–937. [PMC free article] [PubMed]
  • Walker RA, O'Brien ET, Pryer NK, Soboeiro MF, Voter WA, Erickson HP, Salmon ED. Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J Cell Biol. 1988 Oct;107(4):1437–1448. [PMC free article] [PubMed]
  • Yamada KM, Spooner BS, Wessells NK. Axon growth: roles of microfilaments and microtubules. Proc Natl Acad Sci U S A. 1970 Aug;66(4):1206–1212. [PMC free article] [PubMed]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...