Midzone microtubule bundles are continuously required for cytokinesis in cultured epithelial cells [published erratum appears in J Cell Biol 1996 Dec;135(6 Pt 1):1679]

doi:10.1083/jcb.135.4.981

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Midzone microtubule bundles are continuously required for cytokinesis in cultured epithelial cells [published erratum appears in J Cell Biol 1996 Dec;135(6 Pt 1):1679]

SP Wheatley and Y Wang
Cell Biology Group, Worcester Foundation for Biomedical Research, Shrewsbury, Massachusetts 01545, USA.

The current model of cytokinesis proposes that spindle poles and associated microtubules determine the cleavage plane, and, once the signal has been delivered to the cortex, the entire mitotic apparatus can be removed without affecting cell division. While supported by compelling data from Echinoderm embryos, recent observations suggest that the model may not be universally applicable. In this study, we have examined the relationship(s) among microtubules, chromosomes, and cleavage activity in living normal rat kidney (NRK) cells with multipolar mitotic figures. We found that cleavage activity correlated with the distribution of midzone microtubule bundles and Telophase Disc 60 protein (TD60) rather than the position of spindle poles. In addition, reduction of midzone microtubules near the cortex, by either nocodazole treatment or spontaneous reorganization in tripolar cells, caused inhibition or regression of furrowing. These results demonstrate that continuous interaction between midzone microtubule bundles and the cortex is required for successful cleavage in tissue culture cells.
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Verbrugghe, K. J. C., White, J. G. (2007). Cortical centralspindlin and G{alpha} have parallel roles in furrow initiation in early C. elegans embryos. J. Cell Sci. 120: 1772-1778 [Abstract] [Full Text]
Lucero, A., Stack, C., Bresnick, A. R., Shuster, C. B. (2006). A Global, Myosin Light Chain Kinase-dependent Increase in Myosin II Contractility Accompanies the Metaphase-Anaphase Transition in Sea Urchin Eggs. Mol. Biol. Cell 17: 4093-4104 [Abstract] [Full Text]
Janetopoulos, C., Devreotes, P. (2006). Phosphoinositide signaling plays a key role in cytokinesis. JCB 174: 485-490 [Abstract] [Full Text]
Kamijo, K., Ohara, N., Abe, M., Uchimura, T., Hosoya, H., Lee, J.-S., Miki, T. (2006). Dissecting the Role of Rho-mediated Signaling in Contractile Ring Formation. Mol. Biol. Cell 17: 43-55 [Abstract] [Full Text]
Rasmussen, C. G., Glass, N. L. (2005). A Rho-Type GTPase, rho-4, Is Required for Septation in Neurospora crassa. Eukaryot Cell 4: 1913-1925 [Abstract] [Full Text]
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Cho, H. P., Liu, Y., Gomez, M., Dunlap, J., Tyers, M., Wang, Y. (2005). The Dual-Specificity Phosphatase CDC14B Bundles and Stabilizes Microtubules. Mol. Cell. Biol. 25: 4541-4551 [Abstract] [Full Text]
D'Avino, P. P., Savoian, M. S., Glover, D. M. (2005). Cleavage furrow formation and ingression during animal cytokinesis: a microtubule legacy. J. Cell Sci. 118: 1549-1558 [Abstract] [Full Text]
Mollinari, C., Kleman, J.-P., Saoudi, Y., Jablonski, S. A., Perard, J., Yen, T. J., Margolis, R. L. (2005). Ablation of PRC1 by Small Interfering RNA Demonstrates that Cytokinetic Abscission Requires a Central Spindle Bundle in Mammalian Cells, whereas Completion of Furrowing Does Not. Mol. Biol. Cell 16: 1043-1055 [Abstract] [Full Text]
Yokoyama, T., Goto, H., Izawa, I., Mizutani, H., Inagaki, M. (2005). Aurora-B and Rho-kinase/ROCK, the two cleavage furrow kinases, independently regulate the progression of cytokinesis: possible existence of a novel cleavage furrow kinase phosphorylates ezrin/radixin/moesin (ERM). GENES CELLS 10: 127-137 [Abstract] [Full Text]
Alsop, G. B., Zhang, D. (2004). Microtubules continuously dictate distribution of actin filaments and positioning of cell cleavage in grasshopper spermatocytes. J. Cell Sci. 117: 1591-1602 [Abstract] [Full Text]
Fan, J., Beck, K. A. (2004). A role for the spectrin superfamily member Syne-1 and kinesin II in cytokinesis. J. Cell Sci. 117: 619-629 [Abstract] [Full Text]
Saint, R., Somers, W. G. (2003). Animal cell division: a fellowship of the double ring?. J. Cell Sci. 116: 4277-4281 [Abstract] [Full Text]
Alsop, G. B., Zhang, D. (2003). Microtubules are the only structural constituent of the spindle apparatus required for induction of cell cleavage. JCB 162: 383-390 [Abstract] [Full Text]
Abaza, A., Soleilhac, J.-M., Westendorf, J., Piel, M., Crevel, I., Roux, A., Pirollet, F. (2003). M Phase Phosphoprotein 1 Is a Human Plus-end-directed Kinesin-related Protein Required for Cytokinesis. J. Biol. Chem. 278: 27844-27852 [Abstract] [Full Text]
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Aumais, J. P., Williams, S. N., Luo, W., Nishino, M., Caldwell, K. A., Caldwell, G. A., Lin, S.-H., Yu-Lee, L.-y. (2003). Role for NudC, a dynein-associated nuclear movement protein, in mitosis and cytokinesis. J. Cell Sci. 116: 1991-2003 [Abstract] [Full Text]
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Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R., Mitchison, T. J. (2003). Dissecting Temporal and Spatial Control of Cytokinesis with a Myosin II Inhibitor. Science 299: 1743-1747 [Abstract] [Full Text]
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Murata-Hori, M., Wang, Y.-l. (2002). Both midzone and astral microtubules are involved in the delivery of cytokinesis signals: insights from the mobility of aurora B. JCB 159: 45-53 [Abstract] [Full Text]
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Matuliene, J., Kuriyama, R. (2002). Kinesin-like Protein CHO1 Is Required for the Formation of Midbody Matrix and the Completion of Cytokinesis in Mammalian Cells. Mol. Biol. Cell 13: 1832-1845 [Abstract] [Full Text]
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Piel, M., Nordberg, J., Euteneuer, U., Bornens, M. (2001). Centrosome-Dependent Exit of Cytokinesis in Animal Cells. Science 291: 1550-1553 [Abstract] [Full Text]
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Noguchi, T, Mabuchi, I (2001). Reorganization of actin cytoskeleton at the growing end of the cleavage furrow of Xenopus egg during cytokinesis. J. Cell Sci. 114: 401-412 [Abstract]
Benink, H. A., Mandato, C. A., Bement, W. M. (2000). Analysis of Cortical Flow Models In Vivo. Mol. Biol. Cell 11: 2553-2563 [Abstract] [Full Text]
Jantsch-Plunger, V., Gonczy, P., Romano, A., Schnabel, H., Hamill, D., Schnabel, R., Hyman, A. A., Glotzer, M. (2000). Cyk-4: A Rho Family Gtpase Activating Protein (Gap) Required for Central Spindle Formation and Cytokinesis. JCB 149: 1391-1404 [Abstract] [Full Text]
Emoto, K., Umeda, M. (2000). An Essential Role for a Membrane Lipid in Cytokinesis: Regulation of Contractile Ring Disassembly by Redistribution of Phosphatidylethanolamine. JCB 149: 1215-1224 [Abstract] [Full Text]
O'Connell, C. B., Wang, Y.-l. (2000). Mammalian Spindle Orientation and Position Respond to Changes in Cell Shape in a Dynein-dependent Fashion. Mol. Biol. Cell 11: 1765-1774 [Abstract] [Full Text]
Manandhar, G, Moreno, R., Simerly, C, Toshimori, K, Schatten, G (2000). Contractile apparatus of the normal and abortive cytokinetic cells during mouse male meiosis. J. Cell Sci. 113: 4275-4286 [Abstract]
Nguyen, T., Sawa, H, Okano, H, White, J. (2000). The C. elegans septin genes, unc-59 and unc-61, are required for normal postembryonic cytokineses and morphogenesis but have no essential function in embryogenesis. J. Cell Sci. 113: 3825-3837 [Abstract]
Foe, V., Field, C., Odell, G. (2000). Microtubules and mitotic cycle phase modulate spatiotemporal distributions of F-actin and myosin II in Drosophila syncytial blastoderm embryos. Development 127: 1767-1787 [Abstract]
Shuster, C. B., Burgess, D. R. (1999). Parameters That Specify the Timing of Cytokinesis. JCB 146: 981-992 [Abstract] [Full Text]
Sparks, C. A., Morphew, M., McCollum, D. (1999). Sid2p, a Spindle Pole Body Kinase That Regulates the Onset of Cytokinesis. JCB 146: 777-790 [Abstract] [Full Text]
, J., , B. E., , R., , B., , A. (1999). The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell. Am. J. Bot. 86: 153-172 [Abstract] [Full Text]
Savoian, M. S., Earnshaw, W. C., Khodjakov, A., Rieder, C. L. (1999). Cleavage Furrows Formed between Centrosomes Lacking an Intervening Spindle and Chromosomes Contain Microtubule Bundles, INCENP, and CHO1 but Not CENP-E. Mol. Biol. Cell 10: 297-311 [Abstract] [Full Text]
O'Connell, C. B., Wheatley, S. P., Ahmed, S., Wang, Y.-l. (1999). The Small GTP-binding Protein Rho Regulates Cortical Activities in Cultured Cells during Division. JCB 144: 305-313 [Abstract] [Full Text]
Schumacher, J. M., Golden, A., Donovan, P. J. (1998). AIR-2: An Aurora/Ipl1-related Protein Kinase Associated with Chromosomes and Midbody Microtubules Is Required for Polar Body Extrusion and Cytokinesis in Caenorhabditis elegans Embryos. JCB 143: 1635-1646 [Abstract] [Full Text]
Carmena, M., Riparbelli, M. G., Minestrini, G., Tavares, A. M., Adams, R., Callaini, G., Glover, D. M. (1998). Drosophila Polo Kinase Is Required for Cytokinesis. JCB 143: 659-671 [Abstract] [Full Text]
Raich, W. B., Moran, A. N., Rothman, J. H., Hardin, J. (1998). Cytokinesis and Midzone Microtubule Organization in Caenorhabditis elegans Require the Kinesin-like Protein ZEN-4. Mol. Biol. Cell 9: 2037-2049 [Abstract] [Full Text]
Wheatley, S. P., O'Connell, C. B., Wang, Y.-l. (1998). Inhibition of Chromosomal Separation Provides Insights into Cleavage Furrow Stimulation in Cultured Epithelial Cells. Mol. Biol. Cell 9: 2173-2184 [Abstract] [Full Text]
Sawin, K. E., Nurse, P. (1998). Regulation of Cell Polarity by Microtubules in Fission Yeast. JCB 142: 457-471 [Abstract] [Full Text]
O'Connell, K. F., Leys, C. M., White, J. G. (1998). A Genetic Screen for Temperature-Sensitive Cell-Division Mutants of Caenorhabditis elegans. Genetics 149: 1303-1321 [Abstract] [Full Text]
Swan, K., Severson, A., Carter, J., Martin, P., Schnabel, H, Schnabel, R, Bowerman, B (1998). cyk-1: a C. elegans FH gene required for a late step in embryonic cytokinesis. J. Cell Sci. 111: 2017-2027 [Abstract]
Adams, R. R., Tavares, A. A.M., Salzberg, A., Bellen, H. J., Glover, D. M. (1998). pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for�cytokinesis. Genes Dev. 12: 1483-1494 [Abstract] [Full Text]
Mackay, A. M., Ainsztein, A. M., Eckley, D. M., Earnshaw, W. C. (1998). A Dominant Mutant of Inner Centromere Protein (INCENP), a Chromosomal Protein, Disrupts Prometaphase Congression and Cytokinesis. JCB 140: 991-1002 [Abstract] [Full Text]
Harris, S. D., Kraus, P. R. (1998). Regulation of Septum Formation in Aspergillus nidulans by a DNA Damage Checkpoint Pathway. Genetics 148: 1055-1067 [Abstract] [Full Text]
Giansanti, M. G., Bonaccorsi, S., Williams, B., Williams, E. V., Santolamazza, C., Goldberg, M. L., Gatti, M. (1998). Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis. Genes Dev. 12: 396-410 [Abstract] [Full Text]
Weinstein, J. (1997). Cell Cycle-regulated Expression, Phosphorylation, and Degradation of p55Cdc. A MAMMALIAN HOMOLOG OF CDC20/Fizzy/slp1. J. Biol. Chem. 272: 28501-28511 [Abstract] [Full Text]
Wheatley, S. P., Hinchcliffe, E. H., Glotzer, M., Hyman, A. A., Sluder, G., Wang, Y.-l. (1997). CDK1 Inactivation Regulates Anaphase Spindle Dynamics and Cytokinesis In Vivo. JCB 138: 385-393 [Abstract] [Full Text]
Oegema, K., Mitchison, T. J. (1997). Rappaport rules: Cleavage furrow induction in�animal�cells. Proc. Natl. Acad. Sci. USA 94: 4817-4820 [Full Text]
Rieder, C. L., Khodjakov, A., Paliulis, L. V., Fortier, T. M., Cole, R. W., Sluder, G. (1997). Mitosis in vertebrate somatic cells with two spindles: Implications for the metaphase/anaphase transition checkpoint�and�cleavage. Proc. Natl. Acad. Sci. USA 94: 5107-5112 [Abstract] [Full Text]
Eckley, D. M., Ainsztein, A. M., Mackay, A. M., Goldberg, I. G., Earnshaw, W. C. (1997). Chromosomal Proteins and Cytokinesis: Patterns of Cleavage Furrow Formation and Inner Centromere Protein Positioning in Mitotic Heterokaryons and Mid-anaphase Cells. JCB 136: 1169-1183 [Abstract] [Full Text]
Walker, G., Shuster, C., Burgess, D. (1997). Microtubule-entrained kinase activities associated with the cortical cytoskeleton during cytokinesis. J. Cell Sci. 110: 1373-1386 [Abstract]
Ohkura, H, Torok, T, Tick, G, Hoheisel, J, Kiss, I, Glover, D. (1997). Mutation of a gene for a Drosophila kinesin-like protein, Klp38B, leads to failure of cytokinesis. J. Cell Sci. 110: 945-954 [Abstract]
Murata-Hori, M., Tatsuka, M., Wang, Y.-L. (2002). Probing the Dynamics and Functions of Aurora B Kinase in Living Cells during Mitosis and Cytokinesis. Mol. Biol. Cell 13: 1099-1108 [Abstract] [Full Text]
Chen, M.-C., Zhou, Y., Detrich, H. W. III (2002). Zebrafish mitotic kinesin-like protein 1 (Mklp1) functions in embryonic cytokinesis. Physiol. Genomics 8: 51-66 [Abstract] [Full Text]