Summary.
Actin inhibitors block or slow anaphase chromosome movements in crane-fly spermatocytes, but stopping of movement is only temporary; we assumed that cells adapt to loss of actin by switching to mechanism(s) involving only microtubules. To test this, we produced actin-filament-free spindles: we added latrunculin B during prometaphase, 9–80 min before anaphase, after which chromosomes generally moved normally during anaphase. We confirmed the absence of actin filaments by staining with fluorescent phalloidin and by showing that cytochalasin D had no effect on chromosome movement. Thus, actin filaments are involved in normal anaphase movements, but in vivo, spindles nonetheless can function normally without them. We tested whether chromosome movements in actin-filament-free spindles arise via microtubules by challenging such spindles with anti-myosin drugs. Y-27632 and BDM (2,3-butanedione monoxime), inhibitors that affect myosin at different regulatory levels, blocked chromosome movement in normal spindles and in actin-filament-free spindles. We tested whether BDM has side effects on microtubule motors. BDM had no effect on ciliary and sperm motility or on ATPase activity of isolated ciliary axonemes, and thus it does not directly block dynein. Nor does it block kinesin, assayed by a microtubule sliding assay. BDM could conceivably indirectly affect these microtubule motors, though it is unlikely that it would have the same side effect on the motors as Y-27632. Since BDM and Y-27632 both affect chromosome movement in the same way, it would seem that both affect spindle myosin; this suggests that spindle myosin interacts with kinetochore microtubules, either directly or via an intermediate component.
Similar content being viewed by others
References
KA Adames A Forer (1996) ArticleTitleEvidence for polewards forces on chromosome arms during anaphase. Cell Motil Cytoskeleton 34 13–25 Occurrence Handle10.1002/(SICI)1097-0169(1996)34:1<13::AID-CM2>3.0.CO;2-J Occurrence Handle1:STN:280:DyaK2s%2FhtleqsA%3D%3D Occurrence Handle8860228
FJ Ahmad J Hughey T Wittmann A Hyman M Greaser PW Baas (2000) ArticleTitleMotor proteins regulate force interactions between microtubules and microfilaments in the axon. Nat Cell Biol 2 276–280 Occurrence Handle1:CAS:528:DC%2BD3cXktlygsLY%3D Occurrence Handle10806478
TJA Allen G Mikala X-P Wu AC Dolphin (1998) ArticleTitleEffects of 2,3-butanedione monoxime (BDM) on calcium channels expressed in Xenopus oocytes. J Physiol 508 1–14 Occurrence Handle1:CAS:528:DyaK1cXis1Cqs74%3D Occurrence Handle9490807
PB Antin S Forry-Schaudies TM Friedman SJ Tapscott H Holtzer (1981) ArticleTitleTaxol induces postmitotic myoblasts to assemble interdigitating microtubule-myosin arrays that exclude actin filaments. J Cell Biol 90 300–308 Occurrence Handle10.1083/jcb.90.2.300 Occurrence Handle1:CAS:528:DyaL3MXlsVClsrc%3D Occurrence Handle6116716
Ayscough K (1998) Use of Latrunculin-A, an actin monomer-binding drug. In: Vallee R (ed) Molecular motors and the cytoskeleton, part B. Academic Press, London, pp 18–25 (Methods in enzymology, vol 298)
JD Banks R Heald (2001) ArticleTitleChromosome movement: dynein-out at the kinetochore. Curr Biol 11 R128–R131 Occurrence Handle10.1016/S0960-9822(01)00059-8 Occurrence Handle1:CAS:528:DC%2BD3MXhsFWht7Y%3D Occurrence Handle11250166
AR Bresnick (1999) ArticleTitleMolecular mechanisms of nonmuscle myosin-II regulation. Curr Opin Cell Biol 11 26–33 Occurrence Handle10.1016/S0955-0674(99)80004-0 Occurrence Handle1:CAS:528:DyaK1MXhsFSntbk%3D Occurrence Handle10047526
TT Cao W Chang SE Masters MS Mooseker (2004) ArticleTitleMyosin-Va binds to and mechanochemically couples microtubules to actin filaments. Mol Biol Cell 15 151–161 Occurrence Handle1:CAS:528:DC%2BD2cXlsFSntA%3D%3D Occurrence Handle14565972
N Chaffey P Barlow (2002) ArticleTitleMyosin, microtubules and microfilaments: cooperation between cytoskeletal components during cambial cell division and secondary vascular differentiation in trees. Planta 214 526–536 Occurrence Handle10.1007/s004250100652 Occurrence Handle1:CAS:528:DC%2BD38XhtFWitL8%3D Occurrence Handle11925036
M Coue SL Brenner I Spector ED Korn (1987) ArticleTitleInhibition of actin polymerization by latrunculin A. FEB 213 316–318 Occurrence Handle1:CAS:528:DyaL2sXitV2isbo%3D
– Lombillo VA, McIntosh JR (1991) Microtubule depolymerization promotes particle and chromosome movement in vitro. J Cell Biol 112: 1165–1175
LP Cramer TJ Mitchison (1995) ArticleTitleMyosin is involved in postmitotic cell spreading. J Cell Biol 131 179–189 Occurrence Handle10.1083/jcb.131.1.179 Occurrence Handle1:CAS:528:DyaK2MXot1Oku7s%3D Occurrence Handle7559774
BB Czaban A Forer (1992) ArticleTitleRhodamine-labelled phalloidin stains components in the chromosomal spindle fibres of crane-fly spermatocytes and Haemanthus endosperm cells. Biochem Cell Biol 70 664–676 Occurrence Handle1:CAS:528:DyaK3sXls1GmtQ%3D%3D Occurrence Handle1282338 Occurrence Handle10.1139/o92-102
JG DeLuca CN Newton RH Himes MA Jordan L Wilson (2001) ArticleTitlePurification and characterization of native conventional kinesin, HSET, and CENP-E from mitotic HeLa cells. J Biol Chem 276 28014–28021 Occurrence Handle10.1074/jbc.M102801200 Occurrence Handle1:CAS:528:DC%2BD3MXls1Srsrk%3D Occurrence Handle11382767
AS DePina (2000) ArticleTitleIdentification and characterization of a vesicle-associated myosin II in extracts of clam oocytes. Dissertation, Darmouth College, Dissertation Abstracts International 61-08B 3945
A Desai P Maddox TJ Mitchison ED Salmon (1998) ArticleTitleAnaphase A chromosome movement and poleward microtubule flux occur at similar rates in Xenopus extract spindles. J Cell Biol 141 703–713 Occurrence Handle10.1083/jcb.141.3.703 Occurrence Handle1:CAS:528:DyaK1cXivVGjsb0%3D Occurrence Handle9566970
– Murray A, Mitchison TJ, Walczak CE (1999) The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro. In: Rieder C (ed) Mitosis and meiosis. Academic Press, London, pp 38–412 (Methods in cell biology, vol 61)
JM Durán F Valderrama S Castel J Magdalema M Tomás H Hosoya J Renau-Pigueras V Malhotra G Egea (2003) ArticleTitleMyosin motors and not actin comets are mediators of the actin-based golgi-to-endoplasmic reticulum protein transport. Mol Biol Cell 14 445–459 Occurrence Handle12589046
CH Fiske Y Subbarow (1925) ArticleTitleThe colorimetric determination of phosphorus. J Biol Chem 66 375–400 Occurrence Handle1:CAS:528:DyaB28XoslGn
Forer A (1969) Chromosome movements during cell division. In: Lima-de-Faria A (ed) Handbook of molecular cytology. North-Holland, Amsterdam, pp 553–601
– (1982) Crane fly spermatocytes and spermatids: a system for studying cytoskeletal components. In: Wilson L (ed) The cytoskeleton, part B. Academic Press, London, pp 228–252 (Methods in cell biology, vol 25)
– Fabian L (2005) Does 2,3-butanedione monoxime inhibit nonmuscle myosin? Protoplasma 225: 1–4
– Pickett-Heaps JD (1998) Cytochalasin D and latrunculin affect chromosome behaviour during meiosis in crane-fly spermatocytes. Chromosome Res 6: 533–549
– Wilson PJ (1994) A model for chromosome movement during mitosis. Protoplasma 179: 95–105
– 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 region. Cell Motil Cytoskeleton 56: 173–192
E Fuchs I Karakesisoglou (2001) ArticleTitleBridging cytoskeletal intersections. Genes Dev 15 1–14 Occurrence Handle10.1101/gad.861501 Occurrence Handle1:CAS:528:DC%2BD3MXhvVKhurs%3D Occurrence Handle11156599
T Fujii R Tanaka (1979) ArticleTitleInteraction of rat brain microtubule proteins and 6S tubulin with rabbit skeletal muscle actomyosin. Life Sci 24 1683–1690 Occurrence Handle10.1016/0024-3205(79)90253-4 Occurrence Handle1:CAS:528:DyaE1MXktlCgt7s%3D Occurrence Handle158115
– Suzuki T, Hachimori A, Fujii M, Kondo Y, Ohki K (1984) Effect of taxol on the interaction of tubulin with myosin filaments. Can J Biochem Cell Biol 62: 878–884
K Fumoto T Uchimara T Iwasaki K Ueda H Hosoya (2003) ArticleTitlePhosphorylation of myosin II regulatory light chain is necessary for migration of HeLa cells but not for localization of myosin II at the leading edge. Biochem J 370 551–556 Occurrence Handle10.1042/BJ20021559 Occurrence Handle1:CAS:528:DC%2BD3sXhsVWjur4%3D Occurrence Handle12429016
G Gallo HF Yee SuffixJr PC Letourneau (2002) ArticleTitleActin turnover is required to prevent axon retraction driven by endogenous actomyosin contractility. J Cell Biol 158 1219–1228 Occurrence Handle1:CAS:528:DC%2BD38Xns1eqtbY%3D Occurrence Handle12356866
IR Gibbons (1965) ArticleTitleChemical dissection of cilia. Arch Biol (Liege) 76 317–352 Occurrence Handle1:STN:280:DyaF28%2FotVWqtg%3D%3D
Gibson TM, Asai DJ (1999) Isolation and characterization of 22S outer arm dynein from Tetrahymena cilia. In: Asai DJ (ed) Tetrahymena thermophila. Academic Press, London, pp 433–440 (Methods in cell biology, vol 62)
LSB Goldstein (1993) ArticleTitleFunctional redundancy in mitotic force generation. J Cell Biol 120 1–3 Occurrence Handle10.1083/jcb.120.1.1 Occurrence Handle1:CAS:528:DyaK3sXlsVChsQ%3D%3D Occurrence Handle8416980
BL Goode DG Drubin G Barnes (2000) ArticleTitleFunctional cooperation between the microtubule and actin cytoskeletons. Curr Opin Cell Biol 12 63–71 Occurrence Handle10.1016/S0955-0674(99)00058-7 Occurrence Handle1:CAS:528:DC%2BD3cXhsVOjtr8%3D Occurrence Handle10679357
G Goshima RD Vale (2003) ArticleTitleThe roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J Cell Biol 162 1003–1016 Occurrence Handle10.1083/jcb.200303022 Occurrence Handle1:CAS:528:DC%2BD3sXnsVWjsLw%3D Occurrence Handle12975346
M Hayashi K Ohnishi K Hayashi (1980) ArticleTitleDense precipitate of brain tubulin with skeletal muscle myosin. J Biochem 87 1347–1355 Occurrence Handle1:CAS:528:DyaL3cXkt1Wjsbc%3D Occurrence Handle6104659
TA Hely DJ Willshaw (1998) ArticleTitleShort-term interactions between microtubules and actin filaments underlie long-term behaviour in neural growth cones. Proc R Soc Lond B 265 1801–1807 Occurrence Handle1:STN:280:DyaK1M%2FgtlOguw%3D%3D Occurrence Handle10.1098/rspb.1998.0505
C Herrmann J Wray F Travers T Barman (1992) ArticleTitleEffect of 2,3-butanedione monoxime on myosin and myofibrillar ATPases: an example of an uncompetitive inhibitor. Biochemistry 31 12227–12232 Occurrence Handle1:CAS:528:DyaK38XmsV2is7k%3D Occurrence Handle1457420
H Higuchi S Takemori (1989) ArticleTitleButanedione monoxime suppresses contraction and ATPase activity of rabbit skeletal muscle. J Biochem 105 638–643 Occurrence Handle1:CAS:528:DyaL1MXitVGmsrY%3D Occurrence Handle2527229
G-J Huang JJ McArdle (1992) ArticleTitleNovel suppression of an L-type calcium channel in neurones of murine dorsal root ganglia by 2,3-butanedione monoxime. J Physiol 447 257–274 Occurrence Handle1:CAS:528:DyaK38XotFWisA%3D%3D Occurrence Handle1317430
JD Huang ST Brady BW Richards D Stenolen JH Resau NG Copeland NA Jenkins (1999) ArticleTitleDirect interactions of microtubule- and actin-based transport motors. Nature 397 267–270 Occurrence Handle1:CAS:528:DyaK1MXpvVGlug%3D%3D Occurrence Handle9930703
E Hwang J Kusch Y Barral TC Huffaker (2003) ArticleTitleSpindle orientation in Saccharomyces cerevisiae depends on the transport of microtubule ends along polarized actin cables. J Cell Biol 161 483–488 Occurrence Handle10.1083/jcb.200302030 Occurrence Handle1:CAS:528:DC%2BD3sXjvVeqs7k%3D Occurrence Handle12743102
AB Ilagan A Forer (1997) ArticleTitleEffects of ultraviolet-microbeam irradiation of kinetochores in crane-fly spermatocytes. Cell Motil Cytoskeleton 36 266–275 Occurrence Handle10.1002/(SICI)1097-0169(1997)36:3<266::AID-CM7>3.0.CO;2-5 Occurrence Handle1:STN:280:DyaK2s3itVClsg%3D%3D Occurrence Handle9067622
G Jedd NH Chua (2002) ArticleTitleVisualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding. Plant Cell Physiol 43 384–392 Occurrence Handle10.1093/pcp/pcf045 Occurrence Handle1:CAS:528:DC%2BD38XjtFKnsbY%3D Occurrence Handle11978866
JF Kelleher MA Titus (1998) ArticleTitleIntracellular motility: how can we all work together? Curr Biol 8 R394–R397 Occurrence Handle10.1016/S0960-9822(98)70246-5 Occurrence Handle1:CAS:528:DyaK1cXjt1Kks70%3D Occurrence Handle9635187
SM King (2000) ArticleTitleThe dynein microtubule motor. Biochim Biophys Acta 1496 60–75 Occurrence Handle1:CAS:528:DC%2BD3cXhslamu7s%3D Occurrence Handle10722877
MW Klymkowsky (1999) ArticleTitleWeaving a tangled web: the interconnected cytoskeleton. Nat Cell Biol 1 E121–E123 Occurrence Handle10.1038/12950 Occurrence Handle1:CAS:528:DyaK1MXlvFChurs%3D Occurrence Handle10559951
G Komis P Apostolakos B Galatis (2003) ArticleTitleActomyosin is involved in the plasmolytic cycle: gliding movement of the deplasmolyzing protoplast. Protoplasma 221 245–256 Occurrence Handle1:STN:280:DC%2BD3s3nsFyiuw%3D%3D Occurrence Handle12802632
M Krendel G Sgourdas EM Bonder (1998) ArticleTitleDisassembly of actin filaments leads to increased rate and frequency of mitochondrial movement along microtubules. Cell Motil Cytoskeleton 40 368–378 Occurrence Handle10.1002/(SICI)1097-0169(1998)40:4<368::AID-CM5>3.0.CO;2-7 Occurrence Handle1:CAS:528:DyaK1cXlsVCntr8%3D Occurrence Handle9712266
J Kusch A Meyer MP Snyder Y Barral (2002) ArticleTitleMicrotubule capture by the cleavage apparatus is required for proper spindle positioning in yeast. Genes Dev 16 1627–1639 Occurrence Handle1:CAS:528:DC%2BD38XlsVSmtL4%3D Occurrence Handle12101122
SA Kuznetsov GM Langford DG Weiss (1992) ArticleTitleActin-dependent organelle movement in squid axoplasm. Nature 356 722–725 Occurrence Handle10.1038/356722a0 Occurrence Handle1:CAS:528:DyaK38XisFaltr0%3D Occurrence Handle1570018
JR LaFountain SuffixJr R Oldenbourg RW Cole CL Rieder (2001) ArticleTitleMicrotubule flux mediates poleward motion of acentric chromosome fragments during meiosis in insect spermatocytes. Mol Biol Cell 12 4054–4065 Occurrence Handle1:CAS:528:DC%2BD3MXpt1Giu7g%3D Occurrence Handle11739800
– Cohan CS, Siegel AJ, LaFountain DJ (2004) Direct visualization of microtubule flux during metaphase and anaphase in crane-fly spermatocytes. Mol Biol Cell 15: 5724–5732
GM Langford (1995) ArticleTitleActin- and microtubule-dependent organelle motors: interrelationships between the two motile systems. Curr Opin Cell Biol 7 82–88 Occurrence Handle10.1016/0955-0674(95)80048-4 Occurrence Handle1:CAS:528:DyaK2MXjsVyktrY%3D Occurrence Handle7755993
VA Lantz GK Miller (1998) ArticleTitleA class VI unconventional myosin is associated with a homologue of a microtubule-binding protein, cytoplasmic linker protein-170, in neurons and at the posterior pole of Drosophila embryos. J Cell Biol 140 897–910 Occurrence Handle10.1083/jcb.140.4.897 Occurrence Handle1:CAS:528:DyaK1cXhtlegtb8%3D Occurrence Handle9472041
LA Ligon O Steward (2000) ArticleTitleRole of microtubules and actin filaments in the movement of mitochondria in the axons and dendrites of cultured hippocampal neurons. J Comp Neurol 427 351–361 Occurrence Handle1:STN:280:DC%2BD3M%2FmvV2ltw%3D%3D Occurrence Handle11054698
CH Lin EM Espreafico MS Mooseker P Forscher (1996) ArticleTitleMyosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16 769–782 Occurrence Handle10.1016/S0896-6273(00)80097-5 Occurrence Handle1:CAS:528:DyaK28XislCms7g%3D Occurrence Handle8607995
OH Lowry NJ Rosebrough AL Farr LJ Randall (1951) ArticleTitleProtein measurement with the Folin phenol reagent. J Biol Chem 193 265–275 Occurrence Handle1:CAS:528:DyaG38XhsVyrsw%3D%3D Occurrence Handle14907713
CA Mandato WM Bement (2003) ArticleTitleActomyosin transports microtubules and microtubules control actomyosin recruitment during Xenopus oocyte wound healing. Curr Biol 13 1096–1105 Occurrence Handle10.1016/S0960-9822(03)00420-2 Occurrence Handle1:CAS:528:DC%2BD3sXlt1entrg%3D Occurrence Handle12842008
JB Manneville S Etienne-Manneville P Skehel T Carter D Ogden M Ferenczi (2003) ArticleTitleInteraction of the actin cytoskeleton with microtubules regulates secretory organelle movement near the plasma membrane in human endothelial cells. J Cell Sci 116 3927–3938 Occurrence Handle10.1242/jcs.00672 Occurrence Handle1:CAS:528:DC%2BD3sXosFCrs7k%3D Occurrence Handle12928328
AI Marcus W Li H Ma RJ Cyr (2003) ArticleTitleA kinesin mutant with an atypical bipolar spindle undergoes normal mitosis. Mol Biol Cell 14 1717–1726 Occurrence Handle10.1091/mbc.E02-09-0586 Occurrence Handle1:CAS:528:DC%2BD3sXjtValsbo%3D Occurrence Handle12686621
ME Martin SJ Iyadurai A Gassman JG Gindhart SuffixJr TS Hays WM Saxton (1999) ArticleTitleCytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol Biol Cell 10 3717–3728 Occurrence Handle1:CAS:528:DyaK1MXntlyrsL8%3D Occurrence Handle10564267
M McGrail TS Hays (1997) ArticleTitleThe microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124 2409–2419 Occurrence Handle1:CAS:528:DyaK2sXktlWksb4%3D Occurrence Handle9199367
AL Miller Y Wang MS Mooseker AJ Koleske (2004) ArticleTitleThe Abl-related gene (Arg) requires its F-actin-microtubule cross-linking activity to regulate lamellipodial dynamics during fibroblast adhesion. J Cell Biol 165 407–419 Occurrence Handle10.1083/jcb.200308055 Occurrence Handle1:CAS:528:DC%2BD2cXjvFKjs7g%3D Occurrence Handle15138293
TM Molchan AH Valster PK Hepler (2002) ArticleTitleActomyosin promotes cell plate alignment and late lateral expansion in Tradescantia11 stamen hair cells. Planta 214 683–693 Occurrence Handle10.1007/s004250100672 Occurrence Handle1:CAS:528:DC%2BD38Xhs1yqs7g%3D Occurrence Handle11882936
WM Morton KR Ayscough PJ McLaughlin (2000) ArticleTitleLatrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat Cell Biol 2 376–378 Occurrence Handle1:CAS:528:DC%2BD3cXlt1SlsLw%3D Occurrence Handle10854330
Narumiya S, Ishizaki T, Uehata M (2000) Use and properties of ROCK-specific inhibitor Y-27632. In: Balch W, Der C, Hall A (eds) Regulators and effectors of small GTPases, part D: Rho family. Academic Press, London, pp 273–284 (Methods in enzymology, vol 325)
A Nebenführ LA Gallagher TG Dunahay JA Frohlick AM Mazurkiewicz JB Meehl LA Staehelin (1999) ArticleTitleStop-and-go movements of plant Golgi stacks are mediated by the actomyosin system. Plant Physiol 121 1127–1141 Occurrence Handle10594100
P Neco A Gil M Del Mar Frances S Viniegra LM Gutierrez (2002) ArticleTitleThe role of myosin in vesicle transport during bovine chromaffin cell secretion. Biochem J 368 405–413 Occurrence Handle1:CAS:528:DC%2BD38XovF2jt70%3D Occurrence Handle12225290
Orias E, Hamilton EP, Orias JD (2000) Tetrahymena as a laboratory organism: useful strains, cell culture, and cell maintenance. In: Asai DJ (ed) Tetrahymena thermophila. Academic Press, London, pp 189–211 (Methods in cell biology, vol 62)
Osborn M, Weber K (1982) Immunofluorescence and immunocytochemical procedures with affinity purified antibodies: tubulin containing structures. In: Wilson L (ed) The cytoskeleton, part A. Academic Press, London, pp 97–132 (Methods in cell biology, vol 24)
EM Ostap (2002) ArticleTitle2,3-Butanedione monoxime (BDM) as a myosin inhibitor. J Muscle Res Cell Motil 23 305–308 Occurrence Handle10.1023/A:1022047102064 Occurrence Handle1:CAS:528:DC%2BD3sXkvFejuw%3D%3D Occurrence Handle12630704
RJ Pelham Y Wang (1999) ArticleTitleHigh resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate. Mol Biol Cell 10 935–945 Occurrence Handle1:CAS:528:DyaK1MXisVGks7w%3D Occurrence Handle10198048
JD Pickett-Heaps A Forer (2001) ArticleTitlePac-Man does not resolve the enduring problem of anaphase chromosome movement. Protoplasma 215 16–20 Occurrence Handle10.1007/BF01280300 Occurrence Handle1:STN:280:DC%2BD3Mnos1OgsQ%3D%3D Occurrence Handle11732055
– – Spurck T (1996) Rethinking anaphase: where Pac-Man fails and why a role for the spindle matrix is likely. Protoplasma 192: 1–10
G Piperno B Huang DJL Luck (1977) ArticleTitleTwo-dimensional analysis of flagellar proteins from wild-type and paralyzed mutants of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 74 1600–1604 Occurrence Handle1:CAS:528:DyaE2sXhvVGls74%3D Occurrence Handle266200
V Pizon A Iakovenko PFM van der Ven R Kelly C Fatu DO Furst E Karsenti M Gautel (2002) ArticleTitleTransient association of titin and myosin with microtubules in nascent myofibrils directed by the MURF2 RING-finger protein. J Cell Sci 115 4469–4482 Occurrence Handle10.1242/jcs.00131 Occurrence Handle1:CAS:528:DC%2BD38XpvVSqtL0%3D Occurrence Handle12414993
JL Platt AF Michael (1983) ArticleTitleRetardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J Histochem Cytochem 31 840–842 Occurrence Handle1:CAS:528:DyaL3sXktlGnsL0%3D Occurrence Handle6341464
R Pogge-von Strandmann RR Kay JP Dufour (1984) ArticleTitleAn electrogenic proton pump in plasma membranes from the cellular slime mould Dictyostelium discoideum. FEBS Lett 175 422–428 Occurrence Handle1:CAS:528:DyaL2cXmt1KmsbY%3D
OC Rodriguez AW Schaefer CA Mandato P Forsher WM Bement CM Waterman-Storer (2003) ArticleTitleConserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5 599–609 Occurrence Handle10.1038/ncb0703-599 Occurrence Handle1:CAS:528:DC%2BD3sXkvFerurY%3D Occurrence Handle12833063
GC Rogers SL Rogers DJ Sharp (2005) ArticleTitleSpindle microtubules in flux. J Cell Sci 118 1105–1116 Occurrence Handle10.1242/jcs.02284 Occurrence Handle1:CAS:528:DC%2BD2MXjs1Chs7k%3D Occurrence Handle15764594
SL Rogers VI Gelfand (1998) ArticleTitleMyosin cooperates with microtubules motors during organelle transport in melanophores. Curr Biol 8 161–164 Occurrence Handle10.1016/S0960-9822(98)70063-6 Occurrence Handle1:CAS:528:DyaK1cXhtVWjur8%3D Occurrence Handle9443916
J Rosenblatt LP Cramer B Baum KM McGee (2004) ArticleTitleMyosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 117 361–372 Occurrence Handle10.1016/S0092-8674(04)00341-1 Occurrence Handle1:CAS:528:DC%2BD2cXjvFemtrw%3D Occurrence Handle15109496
A Royou C Field JC Sisson W Sullivan R Karess (2004) ArticleTitleReassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos. Mol Biol Cell 15 838–850 Occurrence Handle1:CAS:528:DC%2BD2cXhtlGlsr4%3D Occurrence Handle14657248
ML Ruchhoeft WA Harris (1997) ArticleTitleMyosin functions in Xenopus retinal ganglion cell growth cone motility in vivo. J Neurobiol 32 567–578 Occurrence Handle10.1002/(SICI)1097-4695(19970605)32:6<567::AID-NEU3>3.0.CO;2-Y Occurrence Handle1:CAS:528:DyaK2sXktVCnt7Y%3D Occurrence Handle9183738
J Samaj M Peters D Volkmann F Baluska (2000) ArticleTitleEffects of myosin ATPase inhibitor 2,3-butanedione 2-monoxime on distribution of myosins, F-actin, microtubules, and cortical endoplasmic reticulum in maize root apices. Plant Cell Physiol 41 571–582 Occurrence Handle1:CAS:528:DC%2BD3cXjs1yqurs%3D Occurrence Handle10929940
D Saul L Fabian A Forer JA Brill (2004) ArticleTitleContinuous phosphatidylinositol metabolism is required for cleavage of crane fly spermatocytes. J Cell Sci 117 3887–3896 Occurrence Handle10.1242/jcs.01236 Occurrence Handle1:CAS:528:DC%2BD2cXns1aqtLk%3D Occurrence Handle15265984
MS Savoian ML Goldberg CL Rieder (2000) ArticleTitleThe rate of poleward chromosome motion is attenuated in Drosophila zw10 and rod mutants. Nat Cell Biol 2 948–952 Occurrence Handle1:CAS:528:DC%2BD3cXptFSnu7c%3D Occurrence Handle11146661
CJ Schaap A Forer (1979) ArticleTitleTemperature effects on anaphase chromosome movement in the spermatocytes of two species of crane flies (Nephrotoma suturalis Loew and Nephrotoma ferruginea Fabricius). J Cell Sci 39 29–52 Occurrence Handle1:STN:280:DyaL3c7hsFyktw%3D%3D Occurrence Handle528584
DJ Sharp HM Brown M Kwon GC Rogers G Holland JM Scholey (2000a) ArticleTitleFunctional coordination of three mitotic motors in Drosophila embryos. Mol Biol Cell 11 241–253 Occurrence Handle1:CAS:528:DC%2BD3cXosFyisg%3D%3D
– Rogers GC, Scholey JM (2000b) Cytoplasmic dynein is required for poleward chromosome movement during mitosis in Drosophila embryos. Nat Cell Biol 2: 922–930
T Shimo-Oka M Hayashi Y Watanabe (1980) ArticleTitleTubulin-myosin interaction. Some properties of binding between tubulin and myosin. Biochemistry 19 4921–4926 Occurrence Handle10.1021/bi00562a034 Occurrence Handle1:CAS:528:DyaL3cXlvF2ntLs%3D Occurrence Handle6448636
LC Sellin JJ McArdle (1994) ArticleTitleMultiple effects of 2,3-butanedione monoxime. Pharmacol Toxicol 74 305–313 Occurrence Handle1:CAS:528:DyaK2cXkslGgtbc%3D Occurrence Handle7937562 Occurrence Handle10.1111/j.1600-0773.1994.tb01365.x
MJ Siegman SU Mooers TB Warren DM Warshaw M Ikebe TM Butler (1994) ArticleTitleComparison of the effects of 2,3-butanedione monoxime on force production, myosin light chain phosphorylation and chemical energy usage in intact and permeabilized smooth and skeletal muscles. J Muscle Res Cell Motil 15 457–472 Occurrence Handle10.1007/BF00122119 Occurrence Handle1:CAS:528:DyaK2cXmslKis7o%3D Occurrence Handle7806639
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 Handle1:CAS:528:DC%2BD3cXhvFSgtr8%3D Occurrence Handle10652253
– – (2001) Effects of anti-myosin drugs on anaphase chromosome movement and cytokinesis in crane-fly primary spermatocytes. Cell Motil Cytoskeleton 50: 180–197
– – (2003) Myosin localization during meiosis I of crane-fly spermatocytes gives indications about its role in division. Cell Motil Cytoskeleton 55: 97–113
VJ Small I Kaverina (2003) ArticleTitleMicrotubules meet substrate adhesions to arrange cell polarity. Curr Opin Cell Biol 15 40–47 Occurrence Handle10.1016/S0955-0674(02)00008-X Occurrence Handle1:CAS:528:DC%2BD3sXotVKn Occurrence Handle12517702
I Spector F Braet NR Shochet MR Bubb (1999) ArticleTitleNew anti-actin drugs in the study of the organization and function of the actin cytoskeleton. Microsc Res Tech 47 18–37 Occurrence Handle10.1002/(SICI)1097-0029(19991001)47:1<18::AID-JEMT3>3.0.CO;2-E Occurrence Handle1:CAS:528:DyaK1MXmvFaksLo%3D Occurrence Handle10506759
AF Straight A Cheung J Limouze I Chen NJ Westwood JR Sellers TJ Mitchison (2003) ArticleTitleDissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299 1743–1747 Occurrence Handle10.1126/science.1081412 Occurrence Handle1:CAS:528:DC%2BD3sXitVSjt7c%3D Occurrence Handle12637748
Theriot JA (2000) The polymerization motor. Traffic 1: 19–28
MA Titus (2003) ArticleTitleCaveat experimentor – is your myosin really inhibited? Nat Cell Biol 5 95 Occurrence Handle10.1038/ncb0203-95 Occurrence Handle1:CAS:528:DC%2BD3sXot12rug%3D%3D Occurrence Handle12563270
M Tominaga E Yokota S Sonobe T Shimmen (2000) ArticleTitleMechanism of inhibition of cytoplasmic streaming by a myosin inhibitor, 2,3-butanedione monoxime. Protoplasma 213 46–54 Occurrence Handle10.1007/BF01280504 Occurrence Handle1:CAS:528:DC%2BD3cXotVOhsr0%3D
S Uemura H Higuchi AO Olivares EM De La Cruz S Ishiwata (2004) ArticleTitleMechanochemical coupling of two substeps in a single myosin V motor. Nat Struct Mol Biol 11 877–883 Occurrence Handle10.1038/nsmb806 Occurrence Handle1:CAS:528:DC%2BD2cXmvFyqt7o%3D Occurrence Handle15286720
RD Vale RA Milligan (2000) ArticleTitleThe way things move: looking under the hood of molecular motor proteins. Science 288 88–95 Occurrence Handle10.1126/science.288.5463.88 Occurrence Handle1:CAS:528:DC%2BD3cXisVGjsrw%3D Occurrence Handle10753125
CM Waterman-Storer ED Salmon (1997) ArticleTitleActomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J Cell Biol 139 417–434 Occurrence Handle10.1083/jcb.139.2.417 Occurrence Handle1:CAS:528:DyaK2sXmvV2gurk%3D Occurrence Handle9334345
– – (1999) Positive feedback interactions between microtubules and actin dynamics during cell motility. Curr Opin Cell Biol 11: 61–67
– Duey DY, Weber KL, Keech J, Cheney RE, Salmon ED, Bement WM (2000) Microtubules remodel actomyosin networks in Xenopus egg extracts via two mechanisms of F-actin transport. J Cell Biol 150: 361–376
KL Weber AM Sokac RE Cheney WB Bement (2002) ArticleTitleXenopus myosin-10 may facilitate microtubule-F-actin interactions. Mol Biol Cell 13 181a
– – Berg JS, Cheney RE, Bement WB (2004) A microtubule-binding myosin required for nuclear anchoring and spindle assembly. Nature 431: 325–329
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 Handle10.1002/(SICI)1097-0169(1997)37:1<20::AID-CM3>3.0.CO;2-L Occurrence Handle1:CAS:528:DyaK2sXjtleqtLw%3D Occurrence Handle9142436
– – Leggiadro C (1994) Evidence that kinetochore microtubules in crane-fly spermatocytes disassemble during anaphase primarily at the poleward end. J Cell Sci 107: 3015–3027
U Wolfrum X Liu A Schmitt IP Udovichenko DS Williams (1998) ArticleTitleMyosin VIIa as a component of cilia and microvilli. Cell Motil Cytoskeleton 40 261–271 Occurrence Handle10.1002/(SICI)1097-0169(1998)40:3<261::AID-CM5>3.0.CO;2-G Occurrence Handle1:CAS:528:DyaK1cXks1aqtL0%3D Occurrence Handle9678669
R Wong A Forer (2003) ArticleTitleSignalling between chromosomes in crane-fly spermatocytes studied using ultraviolet microbeam irradiation. Chromosome Res 11 771–786 Occurrence Handle10.1023/B:CHRO.0000005753.97458.20 Occurrence Handle1:CAS:528:DC%2BD3sXptlGltL8%3D Occurrence Handle14712863
X Wu B Kocher Q Wei JA Hammer Suffix3rd (1998) ArticleTitleMyosin Va associates with microtubule-rich domains in both interphase and dividing cells. Cell Motil Cytoskeleton 40 286–303 Occurrence Handle10.1002/(SICI)1097-0169(1998)40:3<286::AID-CM7>3.0.CO;2-B Occurrence Handle1:CAS:528:DyaK1cXks1aqtLs%3D Occurrence Handle9678671
CJ Yarrow T Lechler R Li TJ Mitchison (2003) ArticleTitleRapid de-localization of actin leading edge components with BDM treatment. BMC Cell Biol 4 5 Occurrence Handle10.1186/1471-2121-4-5 Occurrence Handle12783627
B Yin A Forer (1996) ArticleTitleCoordinated movements between autosomal half-bivalents in crane-fly spermatocytes: evidence that stop signals are sent between partner half-bivalents. J Cell Sci 109 155–163 Occurrence Handle1:CAS:528:DyaK28XosVagtg%3D%3D Occurrence Handle8834800
H Yin D Pruyne TC Huffaker A Bretscher (2000) ArticleTitleMyosin V orients the mitotic spindle in yeast. Nature 406 1013–1015 Occurrence Handle1:CAS:528:DC%2BD3cXmtlOjt7Y%3D Occurrence Handle10984058
E Yokota N Imamichi M Tominaga T Shimmen (2000) ArticleTitleActin cytoskeleton is responsible for the change of cytoplasmic organization in root hair cells induced by a protein phosphatase inhibitor, calyculin A. Protoplasma 213 184–193 Occurrence Handle10.1007/BF01282156 Occurrence Handle1:CAS:528:DC%2BD3cXotlymurg%3D
AC Yvon P Wadsworth (2000) ArticleTitleRegion-specific microtubule transport in motile cells. J Cell Biol 151 1003–1012 Occurrence Handle10.1083/jcb.151.5.1003 Occurrence Handle1:CAS:528:DC%2BD3cXovVyks78%3D Occurrence Handle11086002
– Gross DJ, Wadsworth P (2001) Antagonistic forces generated by myosin II and cytoplasmic dynein regulate microtubule turnover, movement, and organization in interphase cells. Proc Natl Acad Sci USA 98: 8656–8661
Author information
Authors and Affiliations
Corresponding author
Additional information
Correspondence and reprints: Biology Department, York University, 4700 Keele Street, Toronto, ON M3J 1P3, Canada.
Electronic supplementary material
Movie 1.
Control crane-fly spermatocyte undergoing meiosis I and starting cleavage. Three pairs of bivalents are visible (two pairs in one focal plane and one pair in another focal plane). The smaller sex chromosomes remain at the equator until the half-bivalents reach the poles. Time is in hours, minutes, seconds
Movie 2.
A double-treated crane-fly spermatocyte. The spermatocyte was treated with Latrunculin B during prometaphase (at 16:59:00). The cell entered anaphase at about 17:38:00 and it was treated with Cytochalasin D and Latrunculin B at 17:38:50. Chromosome movements were not affected by the Cytochalasin D. Note that only two bivalents aligned at the equator in metaphase, which is not uncommon in cells treated with Latrunculin B during prometaphase. Time is in hours, minutes, seconds
Movie 3. Rhodamine-labelled microtubules sliding along kinesin-coated coverslips. The first sequence is from a control preparation. The second sequence is from a different preparation to which 5 mM BDM was added. The third sequence is from the same preparation as the control experiment but was recorded after 20 mM BDM was added. The speed of microtubule sliding is similar in all three experiments
Rights and permissions
About this article
Cite this article
Fabian, L., Forer, A. Redundant mechanisms for anaphase chromosome movements: crane-fly spermatocyte spindles normally use actin filaments but also can function without them. Protoplasma 225, 169–184 (2005). https://doi.org/10.1007/s00709-005-0094-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-005-0094-6