Skip to main content
Log in

What generates flux of tubulin in kinetochore microtubules?

  • Viewpoint
  • Published:
Protoplasma Aims and scope Submit manuscript

Summary.

We discuss models for production of tubulin flux in kinetochore microtubules. Current models concentrate solely on microtubules and their associated motors and enzymes. For example, in some models the driving force for flux is enzymes at the poles and the kinetochores; in others the driving force is motor molecules that are associated with a stationary spindle matrix. We present a different viewpoint, that microtubules are propelled poleward by forces arising from the spindle matrix, that the forces on the microtubules “activate” polymerising and depolymerising enzymes at kinetochores and poles, that matrix forces utilise actin, myosin, and microtubule motors, and that the matrix itself may not necessarily be static.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • LA Cameron G Yang D Cimini JC Canman O Kisurina-Evgenieva A Khodjakov G Danuser ED Salmon (2006) ArticleTitleKinesin 5-independent poleward flux of kinetochore microtubules in PtK1 cells J Cell Biol 173 173–179 Occurrence Handle16636143 Occurrence Handle10.1083/jcb.200601075 Occurrence Handle1:CAS:528:DC%2BD28XktVCgu74%3D

    Article  PubMed  CAS  Google Scholar 

  • W Chen D Zhang (2004) ArticleTitleKinetochore fibre dynamics outside the context of the spindle during anaphase Nat Cell Biol 6 227–231 Occurrence Handle15039774

    PubMed  Google Scholar 

  • G Civelekoglu-Scholey DJ Sharp A Mogilner JM Scholey (2006) ArticleTitleModel of chromosome motility in Drosophila embryos: adaptation of a general mechanism for rapid mitosis Biophys J 90 3966–3982 Occurrence Handle16533843 Occurrence Handle10.1529/biophysj.105.078691 Occurrence Handle1:CAS:528:DC%2BD28XltF2mt78%3D

    Article  PubMed  CAS  Google Scholar 

  • L Fabian A Forer (2005) ArticleTitleRedundant mechanisms for anaphase chromosome movements: crane-fly spermatocyte spindles normally use actin filaments but also can function without them Protoplasma 225 169–184 Occurrence Handle16228898 Occurrence Handle10.1007/s00709-005-0094-6

    Article  PubMed  Google Scholar 

  • L Fabian A Forer (2007) ArticleTitlePossible roles of actin and myosin during anaphase chromosome movements in locust spermatocytes Protoplasma 231 201–213 Occurrence Handle17922265 Occurrence Handle10.1007/s00709-007-0262-y

    Article  PubMed  Google Scholar 

  • L Fabian J Troscianczuk A Forer (2007a) ArticleTitleCalyculin A, an enhancer of myosin, speeds up anaphase chromosome movement BMC Cell Chromosome 6 1 Occurrence Handle10.1186/1475-9268-6-1

    Article  Google Scholar 

  • L Fabian A Xia DV Venkitaramani KM Johansen J Johansen DJ Andrew A Forer (2007b) ArticleTitleTitin in insect spermatocyte spindle fibers associates with microtubules, actin, myosin and the matrix proteins skeletor, megator and chromator J Cell Sci 120 2190–2204 Occurrence Handle10.1242/jcs.03465 Occurrence Handle1:CAS:528:DC%2BD2sXosVOiuro%3D

    Article  CAS  Google Scholar 

  • A Forer JD Pickett-Heaps (1998) ArticleTitleCytochalasin D and latrunculin affect chromosome behaviour during meiosis in crane-fly spermatocytes Chromosome Res 6 533–549 Occurrence Handle9886773 Occurrence Handle10.1023/A:1009224322399 Occurrence Handle1:CAS:528:DyaK1MXisVygsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • A Forer PJ Wilson (1994) ArticleTitleA model for chromosome movement during mitosis Protoplasma 179 95–105 Occurrence Handle10.1007/BF01403947

    Article  Google Scholar 

  • A Forer PJ Wilson (2000) ArticleTitleEvidence that kinetochore fibre microtubules shorten predominantly at the pole in anaphase flea-beetle spermatocytes Chromosome Res 8 151–163 Occurrence Handle10780704 Occurrence Handle10.1023/A:1009298620707 Occurrence Handle1:CAS:528:DC%2BD3cXislSnt7k%3D

    Article  PubMed  CAS  Google Scholar 

  • A Forer T Spurck JD Pickett-Heaps (1997) ArticleTitleUltraviolet microbeam irradiations of spindle fibres in crane-fly spermatocytes and newt epithelial cells: resolution of previously conflicting observations Protoplasma 197 230–240 Occurrence Handle10.1007/BF01288032

    Article  Google Scholar 

  • A Forer T Spurck JD Pickett-Heaps PJ Wilson (2003) ArticleTitleStructure of kinetochore fibres in crane-fly spermatocytes after irradiation with an ultraviolet microbeam: neither microtubules nor actin filaments remain in the irradiated region Cell Motil Cytoskeleton 56 173–192 Occurrence Handle14569597 Occurrence Handle10.1002/cm.10144

    Article  PubMed  Google Scholar 

  • A Forer T Spurck JD Pickett-Heaps (2007) ArticleTitleActin and myosin inhibitors block elongation of kinetochore fibre stubs in metaphase crane-fly spermatocytes Protoplasma 232 79–85 Occurrence Handle18094930 Occurrence Handle10.1007/s00709-007-0265-8 Occurrence Handle1:STN:280:DC%2BD1c%2FhsVyksw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • NJ Ganem K Upton DA Compton (2005) ArticleTitleEfficient mitosis in human cells lacking poleward microtubule flux Curr Biol 15 1827–1832 Occurrence Handle16243029 Occurrence Handle10.1016/j.cub.2005.08.065 Occurrence Handle1:CAS:528:DC%2BD2MXhtFCjsL%2FM

    Article  PubMed  CAS  Google Scholar 

  • GJ Gorbsky PJ Sammak GG Borisy (1987) ArticleTitleChromosomes move poleward in anaphase along stationary microtubules that coordinately disassemble from their kinetochore ends J Cell Biol 104 9–18 Occurrence Handle3793763 Occurrence Handle10.1083/jcb.104.1.9 Occurrence Handle1:STN:280:BiiD1czlsFw%3D

    Article  PubMed  CAS  Google Scholar 

  • KM Johansen J Johansen (2002) ArticleTitleRecent glimpses of the elusive spindle matrix Cell Cycle 1 312–314 Occurrence Handle12461290 Occurrence Handle1:CAS:528:DC%2BD38XpvVWhu7Y%3D

    PubMed  CAS  Google Scholar 

  • KM Johansen J Johansen (2007) ArticleTitleCell and molecular biology of the spindle matrix Int Rev Cytol 263 155–206 Occurrence Handle17725967 Occurrence Handle10.1016/S0074-7696(07)63004-6 Occurrence Handle1:CAS:528:DC%2BD1cXhs1ajt7s%3D

    Article  PubMed  CAS  Google Scholar 

  • TM Kapoor MA Lampson P Hergert L Cameron D Cimini ED Salmon BF McEwen A Khodjakov (2006) ArticleTitleChromosomes can congress to the metaphase plate before biorientation Science 311 388–391 Occurrence Handle16424343 Occurrence Handle10.1126/science.1122142 Occurrence Handle1:CAS:528:DC%2BD28XlvFSguw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • JR LaFountain SuffixJr CS Cohan AJ Siegel DJ LaFountain (2004) ArticleTitleDirect visualization of microtubule flux during metaphase and anaphase in crane fly spermatocytes Mol Biol Cell 15 5724–5732 Occurrence Handle15469981 Occurrence Handle10.1091/mbc.E04-08-0750 Occurrence Handle1:CAS:528:DC%2BD2cXhtVGlsLfO

    Article  PubMed  CAS  Google Scholar 

  • P Lénárt CP Bacher N Daigle AR Hand R Eils M Terasaki J Ellenberg (2005) ArticleTitleA contractile nuclear actin network drives chromosome congression in oocytes Nature 436 812–818 Occurrence Handle16015286 Occurrence Handle10.1038/nature03810

    Article  PubMed  Google Scholar 

  • H Maiato CL Rieder A Khodjakov (2004) ArticleTitleKinetochore-driven formation of kinetochore fibers contributes to spindle assembly during animal mitosis J Cell Biol 167 831–840 Occurrence Handle15569709 Occurrence Handle10.1083/jcb.200407090 Occurrence Handle1:CAS:528:DC%2BD2cXhtVOlsbrJ

    Article  PubMed  CAS  Google Scholar 

  • H Maiato A Khodjakov CL Rieder (2005) ArticleTitle Drosophila CLASP is required for the incorporation of microtubule subunits into fluxing kinetochore fibres Nat Cell Biol 7 42–47 Occurrence Handle15592460 Occurrence Handle10.1038/ncb1207 Occurrence Handle1:CAS:528:DC%2BD2MXlvFWi

    Article  PubMed  CAS  Google Scholar 

  • TJ Mitchison (1989) ArticleTitlePolewards microtubule flux in the mitotic spindle: evidence from photoactivation of fluorescence J Cell Biol 109 637–652 Occurrence Handle2760109 Occurrence Handle10.1083/jcb.109.2.637 Occurrence Handle1:CAS:528:DyaL1MXltlSjtbk%3D

    Article  PubMed  CAS  Google Scholar 

  • TJ Mitchison P Maddox J Gaetz A Groen M Shirasu A Desai ED Salmon TM Kapoor (2005) ArticleTitleRoles of polymerisation dynamics, opposed motors, and a tensile element in governing the length of Xenopus extract meiotic spindles Mol Biol Cell 16 3064–3076 Occurrence Handle15788560 Occurrence Handle10.1091/mbc.E05-02-0174 Occurrence Handle1:CAS:528:DC%2BD2MXkvFGgsr8%3D

    Article  PubMed  CAS  Google Scholar 

  • DT Miyamoto ZE Perlman KS Burbank AC Groen TJ Mitchison (2004) ArticleTitleThe kinesin Eg5 drives poleward microtubule flux in Xenopus laevis egg extract spindles J Cell Biol 167 813–818 Occurrence Handle15583027 Occurrence Handle10.1083/jcb.200407126 Occurrence Handle1:CAS:528:DC%2BD2cXhtVOlsbrP

    Article  PubMed  CAS  Google Scholar 

  • J Pickett-Heaps T Spurck D Tippit (1984) ArticleTitleChromosome motion and the spindle matrix J Cell Biol 99 137s–143s Occurrence Handle6746726 Occurrence Handle10.1083/jcb.99.1.137s Occurrence Handle1:STN:280:BiuB28vnsFQ%3D

    Article  PubMed  CAS  Google Scholar 

  • JD Pickett-Heaps A Forer T Spurck (1996) ArticleTitleRethinking anaphase: where “Pac-Man” fails and why a role for the spindle matrix is likely Protoplasma 192 1–10 Occurrence Handle10.1007/BF01273239

    Article  Google Scholar 

  • JD Pickett-Heaps A Forer T Spurck (1997) ArticleTitleTraction fibre: toward a “tensegral” model of the spindle Cell Motil Cytoskeleton 37 1–6 Occurrence Handle9142434 Occurrence Handle10.1002/(SICI)1097-0169(1997)37:1<1::AID-CM1>3.0.CO;2-D Occurrence Handle1:STN:280:ByiB1cjjsVY%3D

    Article  PubMed  CAS  Google Scholar 

  • H Qi U Rath D Wang Y-Z Xu Y Ding W Zhang M Blacketer M Paddy J Girton J Johansen KM Johansen (2004) ArticleTitleMegator, an essential coiled-coil protein, localizes to the putative spindle matrix during mitosis Mol Biol Cell 15 4854–4865 Occurrence Handle15356261 Occurrence Handle10.1091/mbc.E04-07-0579 Occurrence Handle1:CAS:528:DC%2BD2cXpslKgu7g%3D

    Article  PubMed  CAS  Google Scholar 

  • H Qi U Rath Y Ding Y Ji MJ Blacketer J Girton J Johansen KM Johansen (2005) ArticleTitleEAST interacts with Megator and localizes to the putative spindle matrix during mitosis in Drosophila J Cell Biochem 95 1284–1291 Occurrence Handle15962301 Occurrence Handle10.1002/jcb.20495 Occurrence Handle1:CAS:528:DC%2BD2MXnvVWlsb8%3D

    Article  PubMed  CAS  Google Scholar 

  • Qi H, Ding Y, Zhu L, Rath U, Johansen KM, Johansen J (2007) Mutational analysis of the role of spindle matrix proteins in tubulin spindle assemble and function. American Society for Cell Biology Meeting, December 2007, abstract 1481

  • U Rath D Wang Y Ding Y-Z Xu MJ Blacketer J Girton J Johansen KM Johansen (2004) ArticleTitleChromator, a novel and essential chromodomain protein, interacts directly with the spindle matrix protein skeletor in Drosophila J Cell Biochem 93 1033–1047 Occurrence Handle15389869 Occurrence Handle10.1002/jcb.20243 Occurrence Handle1:CAS:528:DC%2BD2cXhtVaqur3J

    Article  PubMed  CAS  Google Scholar 

  • CL Rieder SP Alexander (1990) ArticleTitleKinetochores are transported poleward along a single astral microtubule during chromosome attachment to the spindle in newt lung cells J Cell Biol 110 81–95 Occurrence Handle2295685 Occurrence Handle10.1083/jcb.110.1.81 Occurrence Handle1:STN:280:By%2BC3M%2Fjtl0%3D

    Article  PubMed  CAS  Google Scholar 

  • OC Rodriguez AW Schaefer CA Mandato P Forscher WM Bement CM Waterman-Storer (2003) ArticleTitleConserved microtubule-actin interactions in cell movement and morphogenesis Nat Cell Biol 5 599–609 Occurrence Handle12833063 Occurrence Handle10.1038/ncb0703-599 Occurrence Handle1:CAS:528:DC%2BD3sXkvFerurY%3D

    Article  PubMed  CAS  Google Scholar 

  • GC Rogers SL Rogers TA Schwimmer SC Ems-McClung CE Walczak RD Vale JM Scholey DJ Sharp (2004) ArticleTitleTwo mitotic kinesins cooperate to drive sister chromatid separation during anaphase Nature 427 364–370 Occurrence Handle14681690 Occurrence Handle10.1038/nature02256 Occurrence Handle1:CAS:528:DC%2BD2cXltFCgtQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • GC Rogers SL Rogers DJ Sharp (2005) ArticleTitleSpindle microtubules in flux J Cell Sci 118 1105–1116 Occurrence Handle15764594 Occurrence Handle10.1242/jcs.02284 Occurrence Handle1:CAS:528:DC%2BD2MXjs1Chs7k%3D

    Article  PubMed  CAS  Google Scholar 

  • K Sampson JD Pickett-Heaps A Forer (1996) ArticleTitleCytochalasin D blocks chromosomal attachment to the spindle in the green alga Oedogonium Protoplasma 192 130–144 Occurrence Handle10.1007/BF01273885 Occurrence Handle1:CAS:528:DyaK28XmsFSrsr4%3D

    Article  CAS  Google Scholar 

  • JM Scholey GC Rogers DJ Sharp (2001) ArticleTitleMitosis, microtubules, and the matrix J Cell Biol 154 261–266 Occurrence Handle11470815 Occurrence Handle10.1083/jcb.200101097 Occurrence Handle1:CAS:528:DC%2BD3MXlsVOjs7g%3D

    Article  PubMed  CAS  Google Scholar 

  • RV Silverman-Gavrila A Forer (2000) ArticleTitleEvidence that actin and myosin are involved in the poleward flux of tubulin in metaphase kinetochore microtubules of crane-fly spermatocytes J Cell Sci 113 597–609 Occurrence Handle10652253 Occurrence Handle1:CAS:528:DC%2BD3cXhvFSgtr8%3D

    PubMed  CAS  Google Scholar 

  • RV Silverman-Gavrila A Forer (2001) ArticleTitleEffects of anti-myosin drugs on anaphase chromosome movement and cytokinesis in crane-fly primary spermatocytes Cell Motil Cytoskeleton 50 180–197 Occurrence Handle11807939 Occurrence Handle10.1002/cm.10006 Occurrence Handle1:CAS:528:DC%2BD38XlvVCgsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • JA Snyder L Armstrong OG Stonington TP Spurck JD Pickett-Heaps (1991) ArticleTitleUV-microbeam irradiations of the mitotic spindle: spindle forces and structural analysis of lesions Eur J Cell Biol 55 122–132 Occurrence Handle1915410 Occurrence Handle1:STN:280:By2D3cjptlc%3D

    PubMed  CAS  Google Scholar 

  • T Spurck A Forer JD Pickett-Heaps (1997) ArticleTitleUltraviolet microbeam irradiations of epithelial and spermatocyte spindles suggest that forces act on the kinetochore fibre and are not generated by its disassembly Cell Motil Cytoskeleton 36 136–148 Occurrence Handle9015202 Occurrence Handle10.1002/(SICI)1097-0169(1997)36:2<136::AID-CM4>3.0.CO;2-7 Occurrence Handle1:STN:280:ByiC28jlvVA%3D

    Article  PubMed  CAS  Google Scholar 

  • TP Spurck OG Stonington JA Snyder JD Pickett-Heaps A Bajer J Mole-Bajer (1990) ArticleTitleUV microbeam irradiations of the mitotic spindle. II Spindle fiber dynamics and force production J Cell Biol 111 1505–1518 Occurrence Handle2211823 Occurrence Handle10.1083/jcb.111.4.1505 Occurrence Handle1:STN:280:By6D3cbkvVE%3D

    Article  PubMed  CAS  Google Scholar 

  • JR Stout RS Rizk SL Kline CE Walczak (2006) ArticleTitleDeciphering protein function during mitosis in PtK cells using RNAi BMC Cell Biol 7 26 Occurrence Handle16796742 Occurrence Handle10.1186/1471-2121-7-26

    Article  PubMed  Google Scholar 

  • DH Tippit JD Pickett-Heaps R Leslie (1980) ArticleTitleCell division in two large pennate diatoms Hantzschia and Nitzschia III. A new proposal for kinetochore function during prometaphase J Cell Biol 86 402–416 Occurrence Handle7400213 Occurrence Handle10.1083/jcb.86.2.402 Occurrence Handle1:STN:280:Bi%2BB2cbmsFY%3D

    Article  PubMed  CAS  Google Scholar 

  • AS Tsvetkov A Samsonov A Akhmanova N Galjart SV Popov (2007) ArticleTitleMicrotubule-binding proteins CLASP1 and CLASP2 interact with actin filaments Cell Motil Cytoskeleton 64 519–530 Occurrence Handle17342765 Occurrence Handle10.1002/cm.20201 Occurrence Handle1:CAS:528:DC%2BD2sXot1SqtLs%3D

    Article  PubMed  CAS  Google Scholar 

  • DL Walker D Wang Y Jin U Rath Y Wang J Johansen KM Johansen (2000) ArticleTitleSkeletor, a novel chromosomal protein that redistributes during mitosis provides evidence for the formation of a spindle matrix J Cell Biol 151 1401–1411 Occurrence Handle11134070 Occurrence Handle10.1083/jcb.151.7.1401 Occurrence Handle1:CAS:528:DC%2BD3MXoslaq

    Article  PubMed  CAS  Google Scholar 

  • PJ Wilson A Forer (1989) ArticleTitleIdentifying the site of microtubule polymerization during regrowth of UV-sheared kinetochore fibres using antibodies against acetylated alpha-tubulin Cell Biol Int Rep 13 823–832 Occurrence Handle2680109 Occurrence Handle10.1016/0309-1651(89)90123-9 Occurrence Handle1:STN:280:By%2BD3s%2FksVI%3D

    Article  PubMed  CAS  Google Scholar 

  • PJ Wilson A Forer (1997) ArticleTitleEffects of nanomolar taxol on crane-fly spermatocyte spindles indicate that acetylation of kinetochore microtubules can be used as a marker of poleward tubulin flux Cell Motil Cytoskeleton 37 20–32 Occurrence Handle9142436 Occurrence Handle10.1002/(SICI)1097-0169(1997)37:1<20::AID-CM3>3.0.CO;2-L Occurrence Handle1:CAS:528:DyaK2sXjtleqtLw%3D

    Article  PubMed  CAS  Google Scholar 

  • PJ Wilson A Forer C Leggiadro (1994) ArticleTitleEvidence that kinetochore microtubules in crane-fly spermatocytes disassemble during anaphase primarily at the poleward end J Cell Sci 107 3015–3027 Occurrence Handle7699001 Occurrence Handle1:CAS:528:DyaK2MXisFSksbc%3D

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arthur Forer.

Additional information

Correspondence: A. Forer, Biology Department, York University, 4700 Keele Street, Toronto, ON M3J 1P3, Canada.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Forer, A., Pickett-Heaps, J. & Spurck, T. What generates flux of tubulin in kinetochore microtubules?. Protoplasma 232, 137–141 (2008). https://doi.org/10.1007/s00709-008-0286-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-008-0286-y

Navigation