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Movement of chromosomes with severed kinetochore microtubules

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Abstract

Experiments dating from 1966 and thereafter showed that anaphase chromosomes continued to move poleward after their kinetochore microtubules were severed by ultraviolet microbeam irradiation. These observations were initially met with scepticism as they contradicted the prevailing view that kinetochore fibre microtubules pulled chromosomes to the pole. However, recent experiments using visible light laser microbeam irradiations have corroborated these earlier experiments as anaphase chromosomes again were shown to move poleward after their kinetochore microtubules were severed. Thus, multiple independent studies using different techniques have shown that chromosomes can indeed move poleward without direct microtubule connections to the pole, with only a kinetochore ‘stub’ of microtubules. An issue not yet settled is: what propels the disconnected chromosome? There are two not necessarily mutually exclusive proposals in the literature: (1) chromosome movement is propelled by the kinetochore stub interacting with non-kinetochore microtubules and (2) chromosome movement is propelled by a spindle matrix acting on the stub. In this review, we summarise the data indicating that chromosomes can move with severed kinetochore microtubules and we discuss proposed mechanisms for chromosome movement with severed kinetochore microtubules.

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Notes

  1. However, in Videos S1 and S4 of Sikirzhytski et al. (2014), illustrating severing of kinetochore microtubules in metaphase and anaphase, the associated chromosomes moved as described by Elting et al. (2014).

  2. Crane-fly spermatocyte chromosomes do not change speed when kinetochore microtubules are severed; possible reasons [discussed in Forer et al. (2003)] may relate to the physical connections (‘tethers’) between separating half-bivalents and to signalling between half-bivalents.

References

  • Bajer A, Molè-Bajer J (1970) Effects of UV microbeam irradiation on fine structure of the mitotic spindle. 7th Congrès International de microscopie électronique Grenoble 267

  • Bajer A (1972) Influence of UV microbeam on spindle fine structure and anaphase chromosome movements. Chromosom Today 3:63–69

    Google Scholar 

  • Botvinick EL, Venugopalan V, Shah JV, Liaw LH, Berns MW (2004) Controlled ablation of microtubules using a picosecond laser. Biophys J 87:4203–4212

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen W, Zhang D (2004) Kinetochore fibre dynamics outside the context of the spindle during anaphase. Nat Cell Biol 6:227–231

    PubMed  Google Scholar 

  • Dick AE, Gerlich DW (2013) Kinetic framework of spindle assembly checkpoint signalling. Nat Cell Biol 15:1370–1377

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ding Y, Yao C, Lince-Faria M, Rath U, Cai W, Maiato H, Girton J, Johansen KM, Johansen J (2009) Chromator is required for proper microtubule spindle formation and mitosis in Drosophila. Devtal Biol 334:253–263

    Article  CAS  Google Scholar 

  • Dionne MA, Howard L, Compton DA (1999) NuMA is a component of an insoluble matrix at spindle poles. Cell Motil Cytoskel 42:189–203

    Article  CAS  Google Scholar 

  • Dumont S, Mitchison TJ (2009) Compression regulates mitotic spindle length by a mechanochemical switch at the poles. Curr Biol 19:1086–1095

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Elting MW, Hueschen CL, Udy DB, Dumont S (2014) Force on spindle microtubule minus ends moves chromosomes. J Cell Biol 206:245–256

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Forer A (1965) Local reduction of spindle fiber birefringence in living Nephrotoma suturalis (Loew) spermatocytes induced by ultraviolet microbeam irradiation. J Cell Biol 25 (No.1 pt.2): 95–118

  • Forer A (1966) Characterization of the mitotic traction system and evidence that birefringent spindle fibers neither produce nor transmit force for chromosome movement. Chromosoma 19:44–98

    Article  CAS  PubMed  Google Scholar 

  • Forer A, Wilson PJ (1994) A model for chromosome movement during mitosis. Protoplasma 179:95–105

    Article  Google Scholar 

  • Forer A, Ferraro-Gideon J, Berns M (2013) Distance segregation of sex chromosomes in crane-fly spermatocytes studied using laser microbeam irradiations. Protoplasma 250:1045–1055

    Article  CAS  PubMed  Google Scholar 

  • Forer A, Spurck T, Pickett-Heaps JD (2007) Actin and myosin inhibitors block elongation of kinetochore fibre stubs in metaphase crane-fly spermatocytes. Protoplasma 232:79–85

    Article  CAS  PubMed  Google Scholar 

  • Forer A, Spurck T, Pickett-Heaps JD, Wilson PJ (2003) Structure of kinetochore fibres in crane-fly spermatocytes after irradiation with an ultraviolet microbeam: neither microtubules nor actin filaments remain in the irradiated area. Cell Motil Cytoskel 56:173–192

    Article  Google Scholar 

  • Gordon GW (1980) The control of mitotic motility as influenced by ultraviolet microbeam irradiation of kinetochore fibers: a dissertation in biology. Ph D Thesis University of Pennsylvania

  • Gordon GW, Inoué S (1979) Unexpected increase in poleward velocities of mitotic chromosomes after UV irradiation of their kinetochore fibers. J Cell Biol 83 (number 2 part 2) 376a

  • Grill SW, Gönczy P, Stelzer EHK, Hyman AA (2001) Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409:630–633

    Article  CAS  PubMed  Google Scholar 

  • Heisterkamp A, Maxwell IZ, Mazur E, Underwood JM, Nickerson JA, Kumar S, Ingber DE (2005) Pulse energy dependence of subcellular dissection by femtosecond laser pulses. Opt Express 13:3690–3696

    Article  CAS  PubMed  Google Scholar 

  • Hughes K, Forer A, Wilson P, Leggiadro C (1988) Ultraviolet microbeam irradiation of microtubules in vitro. The action spectrum for local depolymerization of marginal band microtubules in vitro matches that for reducing birefringence of chromosomal spindle fibres in vivo. J Cell Sci 91:469–478

    CAS  PubMed  Google Scholar 

  • Johansen KM, Johansen J (2007) Cell and molecular biology of the spindle matrix. Int Rev Cytol 263:155–210

    Article  CAS  PubMed  Google Scholar 

  • Johansen KM, Forer A, Yao C, Girton J, Johansen J (2011) Do nuclear envelope and intranuclear proteins reorganize during mitosis to form an elastic hydrogel-like spindle matrix? Chromosom Res 19:345–365

    Article  CAS  Google Scholar 

  • Johansen KM, Johansen J, Baek K-H, Jin Y (1996) Remodeling of nuclear architecture during the cell cycle in Drosophila embryos. J Cell Biochem 63:268–279

    Article  CAS  PubMed  Google Scholar 

  • Khodjakov A, La Terra S, Chang F (2004) Laser microsurgery in fission yeast: role of the mitotic spindle midzone in anaphase B. Curr Biol 14:1330–1340

    Article  CAS  PubMed  Google Scholar 

  • Kurachi M, Kikumoto M, Tashiro H, Komiya Y, Tashiro T (1999) Real-time observation of the disassembly of stable neuritic microtubules induced by laser transection: possible mechanisms of microtubule stabilization in neurites. Cell Motil Cytoskel 42:87–100

    Article  CAS  Google Scholar 

  • Labbé J-C, McCarthy E, Goldstein B (2004) The forces that position a mitotic spindle asymmetrically are tethered until after the time of spindle assembly. J Cell Biol 167:245–256

    Article  PubMed Central  PubMed  Google Scholar 

  • Mitchison TJ, Maddox P, Gaetz J, Groen A, Shirasu M, Desai A, Salmon ED, Kapoor TM (2005) Role of polymerisation dynamics opposed motors and a tensile element in governing the length of Xenopus extract meiotic spindles. Mol Biol Cell 16:3064–3076

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nicklas RB (1975) Chromosome movements: current models and experiments on living cells. In: Inoué S, Stephens RE (eds) Molecules and cell movement. Raven, New York, pp 97–107

    Google Scholar 

  • Nicklas RB (1983) Measurements of the force produced by the mitotic spindle in anaphase. J Cell Biol 97:542–548

    Article  CAS  PubMed  Google Scholar 

  • Pickett-Heaps J, Forer A (2009) Mitosis: spindle evolution and the matrix model. Protoplasma 235:91–99

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Pickett-Heaps JD, Tippit DH, Porter KR (1982) Rethinking mitosis. Cell 29:729–744

    Article  CAS  PubMed  Google Scholar 

  • Rath U, Wang D, Ding Y, Xu Y-Z, Qi H, Zhang W, Blacketer ML, Girton J, Johansen J, Johansen KM (2004) Chromator, a novel and essential chromodomain protein interacts directly with the putative spindle matrix protein skeletor. J Cell Biochem 93:1033–1047

    Article  CAS  PubMed  Google Scholar 

  • Sandquist JC, Kita AM, Bement WM (2011) And the dead shall rise: actin and myosin return to the spindle. Dev Cell 21:410–419

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sheykhani R, Shirodkar PV, Forer A (2013a) The role of myosin phosphorylation in anaphase chromosome movement. Eur J Cell Biol 92:175–186

    Article  CAS  PubMed  Google Scholar 

  • Sheykhani R, Baker N, Gomez-Godinez V, Liaw L-H, Shah J, Berns MW, Forer A (2013b) The role of actin and myosin in PtK2 spindle length changes induced by laser microbeam irradiations across the spindle. Cytoskeleton 70:241–259

    Article  CAS  PubMed  Google Scholar 

  • Sikirzhytski V, Magidson V, Steinman JB, He J, Le Berre M, Tikhonenko I, Ault JG, McEwen BF, Chen JK, Sui H, Piel M, Kapoor TM, Khodjakov A (2014) Direct kinetochore-spindle pole connections are not required for chromosome segregation. J Cell Biol 206:231–243

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sillers PJ, Forer A (1981a) Analysis of chromosome movement in crane fly spermatocytes by ultraviolet microbeam irradiation of individual chromosomal spindle fibres. I. General results. Can J Biochem 59:770–776

    Article  CAS  PubMed  Google Scholar 

  • Sillers PJ, Forer A (1981b) Analysis of chromosome movement in crane fly spermatocytes by ultraviolet microbeam irradiation of individual chromosomal spindle fibres. II. Action spectra for stopping chromosome movement and for blocking ciliary beating and myofibril contractions. Can J Biochem 59:777–792

    Article  CAS  PubMed  Google Scholar 

  • Sillers PJ, Forer A (1983) Action spectrum for changes in spindle fibre birefringence after ultraviolet microbeam irradiations of single chromosomal spindle fibres in crane-fly spermatocytes. J Cell Sci 62:1–25

    CAS  PubMed  Google Scholar 

  • Silverman-Gavrila RV, Forer A (2000) Evidence 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

    CAS  PubMed  Google Scholar 

  • Snyder JA, Armstrong L, Stonington OG, Spurck TP, Pickett-Heaps JD (1991) UV-microbeam irradiations of the mitotic spindle: spindle forces and structural analysis of lesions. Eur J Cell Biol 55:122–132

    CAS  PubMed  Google Scholar 

  • Spurck TP, Stonington OG, Snyder JA, Pickett-Heaps JD, Bajer A, Molè-Bajer J (1990) UV microbeam irradiations of the mitotic spindle. II Spindle fiber dynamics and force production. J Cell Biol 111:1505–1518

    Article  CAS  PubMed  Google Scholar 

  • Spurck T, Forer A, Pickett-Heaps JD (1997) Ultraviolet microbeam irradiations of epithelial and spermatocyte spindles suggest that forces act on the kinetochore fibre and are not generated by its disassembly. Cell Motil Cytoskel 36:136–148

    Article  CAS  Google Scholar 

  • Walker DL, Wang D, Jin Y, Rath U, Wang Y, Johansen J, Johansen KM (2000) Skeletor, a novel chromosomal protein that redistributes during mitosis provides evidence for the formation of a spindle matrix. J Cell Biol 151:1401–1411

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilson PJ, Forer A (1988) Ultraviolet microbeam irradiation of chromosomal spindle fibres shears microtubules and permits study of the new free ends in vivo. J Cell Sci 91:455–468

    PubMed  Google Scholar 

  • Yao C, Rath U, Maiato H, Sharp D, Girton J, Johansen KM, Johansen J (2012) A nuclear-derived proteinaceous matrix embeds the microtubule spindle apparatus during mitosis. Mol Biol Cell 23:3532–3541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yao C, Wang C, Li Y, Ding Y, Rath U, Sengupta S, Girton J, Johansen KM, Johansen J (2014) The spindle matrix protein Chromator is a novel tubulin binding protein that can interact with both microtubules and free tubulin. PLoS ONE 9(7):e103855. doi:10.1371/journal. pone.0103855

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This study was supported by grants (to AF) from the Natural Sciences and Engineering Research Council of Canada and grant MCB0817107 (to KMJ) from the National Science Foundation.

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Authors and Affiliations

  1. Biology Department, York University, North York, Ontario, M3J 1P3, Canada

    Arthur Forer

  2. Department of Biophysics Biochemistry and Molecular Biology, Iowa State University, Ames, IA, 50011, USA

    Kristen M. Johansen & Jørgen Johansen

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  1. Arthur Forer
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  2. Kristen M. Johansen
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  3. Jørgen Johansen
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Correspondence to Arthur Forer.

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Handling Editor: David Robinson

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Single images for the montage in Fig. 1 were taken from this sequence. The sequence begins in late metaphase. The upper left autosomal fibre was irradiated in early anaphase, from frame 19463 (time: 16:24:01) until frame 19477 (16:24:12), for a total of about 11 seconds. (MP4 13643 kb)

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Forer, A., Johansen, K.M. & Johansen, J. Movement of chromosomes with severed kinetochore microtubules. Protoplasma 252, 775–781 (2015). https://doi.org/10.1007/s00709-014-0752-7

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